Sports Med 2010; 40 (1): 1-25 0112-1642/10/0001-0001/$49.95/0
REVIEW ARTICLE
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Combining Hypoxic Methods for Peak Performance Gregoire P. Millet,1 B. Roels,2 L. Schmitt,3 X. Woorons4 and J.P. Richalet4 1 2 3 4
ISSUL, Institute of Sport Science, University of Lausanne, Lausanne, Switzerland ORION, Clinical Services Ltd, London, UK National Nordic Ski Centre, Pre´manon, France Universite´ Paris 13, Laboratoire `Re´ponses cellulaires et fonctionnelles a` l’hypoxie’, EA2363 ARPE, Bobigny, France
Contents Abstract. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 1. Traditional ‘Live High-Train High’ Altitude Training . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 1.1 Different Phases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 1.1.1 Acclimatization Phase . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 1.1.2 Primary Training Phase . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 1.1.3 Recovery and Preparation for Return to Sea Level. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 1.1.4 Return to Sea Level . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 1.2 Altitude Training Sites . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 2. Live High-Train Low (LHTL) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 2.1 Haematological Adaptations. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 2.2 Non-Haematological Adaptations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8 2.2.1 Economy. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8 2.2.2 pH Regulation and Muscle Buffer Capacity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8 2.3 Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8 2.3.1 Aerobic Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9 2.3.2 Anaerobic Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10 2.4 LHTL: Summary and Proposals to Athletes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10 2.5 Advances in the LHTL Method: LHTLi, LHTL Interspersed. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11 3. Intermittent Hypoxic Exposure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11 3.1 Definition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11 3.2 Haematological Adaptations. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11 3.3 Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12 4. Intermittent Hypoxic Training (IHT) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13 4.1 Haematological Adaptations. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13 4.2 Muscular Adaptations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14 4.3 Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15 4.3.1 Aerobic Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15 4.3.2 Anaerobic Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16 4.4 An Original IHT Method: Training with Voluntary Hypoventilation . . . . . . . . . . . . . . . . . . . . . . . . . . . 16 4.5 IHT: Summary and Proposals to Athletes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17 4.6 A Promising Combination: Living High-Training Low and High, Interspersed . . . . . . . . . . . . . . . . . . 17 5. Proposals for Optimal Combination of Hypoxic Methods in the Yearly Training Plan . . . . . . . . . . . . . . . 17 5.1 Combining High-High Hypoxic and Sea-Level Training . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19 5.2 Combining All Hypoxic Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20 5.2.1 Endurance Sports. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20
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5.2.2 ‘Glycolytic’ Sports . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20 5.2.3 Intermittent Sports . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20 6. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21
Abstract
New methods and devices for pursuing performance enhancement through altitude training were developed in Scandinavia and the USA in the early 1990s. At present, several forms of hypoxic training and/or altitude exposure exist: traditional ‘live high-train high’ (LHTH), contemporary ‘live high-train low’ (LHTL), intermittent hypoxic exposure during rest (IHE) and intermittent hypoxic exposure during continuous session (IHT). Although substantial differences exist between these methods of hypoxic training and/ or exposure, all have the same goal: to induce an improvement in athletic performance at sea level. They are also used for preparation for competition at altitude and/or for the acclimatization of mountaineers. The underlying mechanisms behind the effects of hypoxic training are widely debated. Although the popular view is that altitude training may lead to an increase in haematological capacity, this may not be the main, or the only, factor involved in the improvement of performance. Other central (such as ventilatory, haemodynamic or neural adaptation) or peripheral (such as muscle buffering capacity or economy) factors play an important role. LHTL was shown to be an efficient method. The optimal altitude for living high has been defined as being 2200–2500 m to provide an optimal erythropoietic effect and up to 3100 m for non-haematological parameters. The optimal duration at altitude appears to be 4 weeks for inducing accelerated erythropoiesis whereas <3 weeks (i.e. 18 days) are long enough for beneficial changes in economy, muscle buffering capacity, the hypoxic ventilatory response or Na+/K+-ATPase activity. One critical point is the daily dose of altitude. A natural altitude of 2500 m for 20–22 h/day (in fact, travelling down to the valley only for training) appears sufficient to increase erythropoiesis and improve sea-level performance. ‘Longer is better’ as regards haematological changes since additional benefits have been shown as hypoxic exposure increases beyond 16 h/day. The minimum daily dose for stimulating erythropoiesis seems to be 12 h/day. For non-haematological changes, the implementation of a much shorter duration of exposure seems possible. Athletes could take advantage of IHT, which seems more beneficial than IHE in performance enhancement. The intensity of hypoxic exercise might play a role on adaptations at the molecular level in skeletal muscle tissue. There is clear evidence that intense exercise at high altitude stimulates to a greater extent muscle adaptations for both aerobic and anaerobic exercises . and limits the decrease in power. So although IHT induces no increase in VO2max due to the low ‘altitude dose’, improvement in athletic performance is likely to happen with high-intensity exercise (i.e. above the ventilatory threshold) due to an increase in mitochondrial efficiency and pH/lactate regulation. We propose a new combination of hypoxic method (which we suggest naming Living High-Training Low and High, interspersed; LHTLHi) combining LHTL (five nights at 3000 m and two nights at sea level) with training at sea level except for a few (2.3 per week) IHT sessions of supra-threshold training. This review also
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provides a rationale on how to combine the different hypoxic methods and suggests advances in both their implementation and their periodization during the yearly training programme of athletes competing in endurance, glycolytic or intermittent sports.
To date, several forms of hypoxic training and/or altitude exposure exist: traditional ‘live high-train high’ (LHTH), contemporary ‘live high-train low’ (LHTL or LH + TLO2) or ‘live lowtrain high’ (LLTH) approaches. More recently, interest has focused on the potential of intermittent hypoxic methods (figure 1) using intermittent hypoxic exposure during rest (IHE), during continuous sessions (IHT), during interval-training (IHIT) or ‘live high-train low and high’ (LHTLH). Although substantial differences exist between these types of hypoxic training and/or exposure, all have the same primary goal: to induce an improvement in athletic performance at sea level. These methods are also used for preparation for competition at altitude or for the acclimatization of mountaineers.
1. Traditional ‘Live High-Train High’ Altitude Training Traditional altitude camps consist of living and training at moderate altitude (1800–2500 m) for several weeks, usually between 2 and 4 weeks. These LHTH camps are mostly carried out two to three times a year.
Altitude/hypoxic training LH + TH Natural/ terrestrial
LH + TL
LHTLH
Nitrogen dilution
Supplemental oxygen
Oxygen filtration
LL + TH IHE
IHT
IHIT
Fig. 1. Different hypoxic methods (modified from Wilber[1]). IHE = intermittent hypoxic exposure during rest; IHT = intermittent hypoxic training; IHIT = intermittent hypoxic exposure during interval training; LH = live high; LHTLH = live high-train low and high; LL = live low; TH = train high; TL = train low.
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1.1 Different Phases
These LHTH camps consist of several progressive phases: the acclimatization phase, the primary training phase, the recovery and preparation for return to sea-level phase, and the return to sea level. 1.1.1 Acclimatization Phase
The first phase starts immediately on arrival to altitude and is called the acclimatization phase. As the name indicates, the purpose of this phase is to acclimatize the athletes to the reduced PIO2 (partial pressure of inspired oxygen) at altitude. To facilitate the athletes’ acclimatization to altitude, they are exposed to as much open air activity as possible. This phase is the most critical one. Therefore, high-intensity exercise is not recommended. The athletes have to be advised to increase their recovery and their fluid intake. The acclimatization phase usually lasts 7–10 days, depending on the total duration of the LHTH camp and the athlete’s frequency of hypoxic exposure, with the duration of exposure usually being decreased in athletes who have experienced regular exposure to altitude.[2] 1.1.2 Primary Training Phase
The primary training phase follows after the acclimatization phase. This phase lasts between 2 and 3 weeks, but may be prolonged according to the age, experience and goals for functional adaptation of the athletes. The purpose of this phase is to progressively increase training volume up to levels similar to those that are achieved at sea level, but also to progressively increase the intensity of training. Large workloads are necessary to induce the cumulative and residual effects of altitude training.[2] However, many athletes use shorter repetitions to maximize the speed aspect of training, or use the same work intervals that they carry out in training in normoxia whilst Sports Med 2010; 40 (1)
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increasing their recovery by a factor of 2–3. This area requires further scientific studies. 1.1.3 Recovery and Preparation for Return to Sea Level
This recovery phase lasts 2–5 days. The aim of this phase is to recover completely from the complementary altitude-induced fatigue. During this phase, training volume and intensity are gradually reduced. 1.1.4 Return to Sea Level
Low intensity
Good individual level of aerobic capacity
Low intensity
On return to sea level after an altitude training camp, three phases have been observed by coaches (figure 2). So far, however, these are not fully supported by the scientific evidence and are therefore under debate: (i) A positive phase observed during the first 2–4 days, but not in all athletes. (ii) A phase of progressive reestablishment of sealevel training volume and intensity. The probability of good performance is reduced. (iii) 15–21 days after return to sea level, a third phase is characterized by a plateau in fitness. The optimal delay for competition is during this third phase, although some athletes reach their peak performance during the first phase.[3]
The time course of the different physiological factors that explain these post-altitude phases has not been studied and therefore remains unclear. However, one may postulate that the immediate positive effects (phase 1) are primarily due to the haemodilution resulting from the return to sea level and persistence of the ventilatory adaptations to altitude training. The decrease in performance fitness (phase 2) might be related to the altered energy cost and loss of the neuromuscular adaptations induced by training at altitude. Improvement in the latter factors after several days at sea level, in conjunction with the further increase in O2 transport and delayed hypoxic ventilatory responses (HVRs) benefits, may explain the third positive phase. In addition, some benefits coming from the increased training capability that is directly induced by altitude training may lead to a delayed period (up to 6–7 weeks after finishing the altitude camp) of increased fitness.[2] In any case, the post-training period requires further scientific investigation. 1.2 Altitude Training Sites
Several altitude training sites exist around the world. The most famous within the sporting
Possible competition Secure distance for a good competition result
Large individual variation
2 4 6 8 10 12 14 16 18 20
Unstable phase
Re-acclim.
Acclim.
Re-acclimatization
2 4 6 8 10 12 14 16 18 20 22 24 26 28 Time (days)
Fig. 2. Schematic view of the development of the aerobic capacity during and after ‘live-high train-high’ (LHTH) training (adapted from Fuchs and Reiss[3]). Acclim. = acclimatization.
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community are (by ascending altitude; see Wilber[4] for a comprehensive review): Pre´manon (1200 m, France); Thredbo (1350 m, Australia); Crans-Montana (1500 m, Switzerland); Albuquerque (1500 m, USA); Potchefstroom (1550 m, South-Africa); Snowfarm (1560 m, New Zealand); Pretoria (1750 m, South Africa); Boulder (1780 m, USA); Ifrane (1820 m, Morocco); St. Moritz (1820 m, Switzerland); Font-Romeu (1850 m, France); Colorado Springs (1860 m, USA); Kunming (1860 m, China); Belmeken (2000 m, Bulgaria); Eldoret (2100 m, Kenya); Flagstaff (2130 m, USA); Sierra Nevada (2320 m, Spain); Iten (2350 m, Kenya); Addis Ababa (2400 m, Ethiopia); Bogota (2640 m, Colombia); Quito (2740 m, Ecuador); La Paz (3600 m, Bolivia). These sites can offer relatively comfortable living and training conditions to athletes and coaches of all performance levels. The first investigations into LHTH appeared during the mid-1960s. Since the 1990s, the LHTH method has largely been complemented by the other hypoxic methods. 2. Live High-Train Low (LHTL) The traditional LHTH altitude training strategy has been replaced or complemented by the LHTL method.[1,5,6] The LHTL method was developed to invoke the beneficial effects of altitude (as regards cardiovascular, respiratory and metabolic adaptations) whilst avoiding, firstly, the need for a decrease in training intensity and, secondly, the detrimental effects of chronic hypoxia (such as muscular mass loss, fatigue or deteriorated aerobic performance, that are observed to a greater extent in endurance elite athletes subject to a more pronounced hypoxaemia[7]). Levine’s research team first investigated the LHTL methods by transporting the athletes from sea level or low altitude (<1300 m) to train whilst spending the rest of their time, i.e. living and sleeping at moderate altitude (1800–2500 m).[8] This method involved living at moderate altitude and performing low-intensity training at moderate altitude, and high-intensity training at sea level or lower altitude.[9] However, this method placed a large amount of stress and fatigue on the ª 2010 Adis Data Information BV. All rights reserved.
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athletes as a result of descending from and ascending to altitude, travelling to and from training sites, adapting to weather differences between altitude and sea level, financial costs, etc. The technical development of new devices made it possible to use artificial altitude (i.e. normobaric hypoxia via nitrogen dilution or oxygen extraction, altitude tents and/or hypoxic sleeping units, decompression chambers, or supplemental oxygen[4]) as an additional training stimulus without travelling to the mountains. 2.1 Haematological Adaptations
Levine et al.[8] found that levels of erythropoietin (EPO) were almost doubled, and haemoglobin concentration (Hb) was increased, in elite athletes after 27 days of living at 2500 m and training at 1250 m. In addition, Stray-Gundersen et al.[10] investigated the effects of 27 days of living at moderate altitude of 2500 m, training intensively at 1250 m, and undergoing base training at both 1250 and 3000 m. They observed a 92% increase in EPO within the first 20 hours of exposure. This was followed by a progressive decline in EPO, up to the 19th day, to the (initial) sea-level values. Moreover, after the 27 days of LHTL, Hb, haematocrit (Hct) and arterial O2 saturation (SaO2) were increased. Dehnert et al.[11] investigated the haematological acclimatization to intensive training at low altitude (800 m) and spending13 h/day at moderate altitude (1960 m) in 15 male and six female triathletes over a period of 2 weeks. EPO increased significantly (30%) but temporarily in LHTL. Total Hb was unchanged in the LHTL group but showed a small significant decrease in the control sea-level group. Reticulocyte (Ret) count also showed a tendency to increase in the LHTL group, but was unchanged in the control group. The authors suggested that the observed EPO stimulation at altitude served to compensate for the exercise-induced destruction of red blood cells (RBCs). Moreover, Stray-Gundersen et al.[12] reported that, for elite athletes living at 2500 m and performing high-intensity training at 1250 m, EPO was almost doubled and both soluble transferrin receptor level and Hb were Sports Med 2010; 40 (1)
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increased. In contrast, Hahn et al.[13] evaluated the effects of LHTL (i.e. 8–11 h a night over 11–23 nights at 2650–3000 m) in six different studies with several athletic populations (runners, triathletes, kayakers, cyclists and cross-country skiers). They concluded that the increase in serum EPO (sEPO) did not always induce an increase in Ret production and that the other haematological parameters were not significantly different between the LHTL and control groups. The Finnish research group, led by Rusko, reported important increases in EPO, Ret or RBCs with LHTL methods in elite athletes. Unfortunately, the training characteristics of their studies, which often lacked control groups, were sometimes poorly controlled. In six female elite cross-country skiers, living 14 h/day at a simulated altitude of 2500 m, and living and training at sea level for 10 h/day, a significant increase over the initial sea-level values was observed in both sEPO (31%) and Ret count (5%) after 11 days.[14] However, no sea-level control group was included in the study. Laitinen et al.[15] observed in seven male trained runners who lived 16–18 h/day at a simulated altitude of 2500 m and lived and trained the other 6–8 h/day at sea level, sEPO (84%) and RBC mass (7%) to be significantly increased (by 84% and 7% ,respectively) after 15 days of LHTL, and remain unchanged in the sea-level control group. Rusko et al.[16] demonstrated a 60% increase in sEPO when measured on the second day of LHTL in 12 female and male cross-country skiers and triathletes who lived 12–16 h/day for 25 days at a simulated altitude of 2500 m, and trained at sea level. They also noted a 5% increase in RBC mass following the 25 days of LHTL. However, the increase in sEPO was not correlated to the increase in RBC mass. The same research team[17] also recorded significant increases in sEPO, RBC, 2,3-diphosphoglycerate. Ret count and soluble transferrin receptors in ten healthy subjects who lived 12 h/day in a 15.4% O2 (~2500 m) nitrogen room over a period of 7 days. Thus, 12 h/day of moderate normobaric hypoxia, for 1 week, was sufficient to stimulate erythropoiesis. Moreover, Phiel-Aulin et al.[18] evaluated six endurance athletes who completed 10 days of living 12 h/day ª 2010 Adis Data Information BV. All rights reserved.
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at a simulated altitude of 2000 m whilst living and training for the rest of the day at sea level. After 2 days of LHTL, an increase was observed in sEPO (80%) and Ret count (60%). In addition, 1 week after the end of the LHTL period, measurements indicated that Hb (-2%) and Hct (-3%) were slightly decreased from the initial sealevel values. These post-LHTL decreases in Hb and Hct were attributed to haemodilution. Thus, a 10-day period of LHTL training induced a significant increase in sEPO but did not significantly change post-LHTL Hb or Hct in trained endurance athletes. The same authors[18] investigated the same 10-day LHTL period (i.e. 12 h/day living at 2700 m, and 12 h/day living and training at sea level) but at a higher simulated altitude of 2700 m in nine endurance athletes. Within the initial five days of LHTL a significant increase in sEPO (85%) and Ret count (38%) was observed. One week after the end of the LHTL period, higher Hb (3%) and lower Hct (-4%) values, compared with initial sea-level values, were observed. In contrast, the Australian Institute of Sport scientists observed very little haematological change with the LHTL method: i.e. no changes in any of the following measured haematological variables, % Ret, mean corpuscular Hb, reticulocyte Hb and total Hb mass, in six female road cyclists who slept for 12 nights at a simulated altitude of 2650 m and trained at 600 m above sea level.[19] They also studied, in six male middle distance runners, the effects of three 8-day LHTL periods (involving five 8- to 11-hour nights at a simulated altitude of 2650 m and training at 600 m, followed by 3 days of living and training at 600 m).[20] sEPO was increased in the LHTL group after the first (57%) and the fifth night (42%) of the first period but this increase was not as great in the second (13% and -4%) and third (26% and 14%) periods. Moreover, there were no changes in the other haematological variables. It appears, therefore, that 5 nights at 2650 m increased sEPO, but was insufficient to induce any other haematological changes. This hypoxic-induced sEPO response was downregulated during a hypoxic stimulus. The same Australian team[21] investigated the effects of an increased LHTL hypoxic stimulus, Sports Med 2010; 40 (1)
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i.e. a higher altitude (3000 m) over a longer period of time (23 days of 8–10 hours per night) in six male endurance athletes. No significant changes were observed in any of the measured variables. Recently, the same team reported that a much longer LHTL period (i.e. 46 nights of 9 hours per night at a simulated altitude of 2860 m, coupled with training at 600 m) induced a significant (~5.0%) increase in total Hb mass.[22] These results support the principle that the hypoxic dose is the primary factor leading to the observed haematological benefits resulting from LHTL. Recently, a project funded by the IOC in Pre´manon (in the Jura region of France) investigated the effects of various hypoxic training methods and more specifically the LHTL method.[23-34] These studies evaluated the responses to LHTL (i.e. 13–18 days of sleeping high at 2500–3500 m and training low at 1200 m) in cross-country skiers,[23,25,27,33] swimmers[24-26,28,29,31-33] and distance runners.[25,29,30,33,34] Overall, LHTL was well tolerated[23,29,33] for altitude up to 3000 m. These studies highlighted the benefits of monitoring sleeping SaO2 since oxygen desaturation and progressive re-saturation can be a good index of the degree of acclimatization. In line with the Scandinavian findings mentioned above[14-18] and summarized by Rusko et al.[35] in 2003, this set of studies support the principle of a minimum dose of hypoxia (of at least 14 hours, ideally 18 h/day) – at an altitude of at least 2500 m – and, ideally, 3000 m – for 3 weeks, being required to induce increased erythropoiesis. In fact, the runners who stayed for the longest time (18 days, 14 h/day) at 3000 m evidenced greater increases in Hb.[34] All the parameters except indirect markers of submaximal performance (see later) had returned to the baseline values 2 weeks after the LHTL session. In summary, whereas some studies demonstrated significantly increased EPO and Ret count,[13-15,35-37] other studies did not observe either any or too low an erythropoietic effect to induce haematological changes after LHTL normobaric hypoxic exposure.[18-21] Probably the differences in duration and level of the hypoxic exposure, in training content or in the methods of measurement of blood volume parameters that were used (e.g. Evans blue dye vs CO reª 2010 Adis Data Information BV. All rights reserved.
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breathing) play a role in the observed discrepancies. Only an absolute increase in RBC mass or Hb mass can be seen as an effective haematological benefit induced by altitude training. Unfortunately, many studies still report relative value(s) in terms of RBCs, Hb and Hct – all of which are influenced by change in volaemia. It was reported that the mean error of measurement for Hb mass with the CO-rebreathing method is 2.2% (90% CI 1.4, 3.5) since the error of measurement of the volume of RBCs is 2.8% (90% CI 2.4, 3.2) for the 51 chromium-labelled RBC technique, 6.7% (90% CI 4.9, 9.4) for the Evans blue dye technique and 6.7% (90% CI 3.4, 14) with the CO-rebreathing method.[38] These errors include analytical error, day-to-day biological variation and the interindividual variability in response to altitude training, and have direct implications for the monitoring of the athletes. Therefore, comparisons of values for RBC mass, plasma or RBC volume that have been obtained via different methods is unsatisfactory. Moreover, a large variation in RBC volume reported in previous LHTL studies[9,39] might arise from measurement errors obtained with the Evans blue dye method.[38] Another confounding factor is the level of the subjects, i.e. trained versus elite athletes. It is known that endurance training induces an increase in blood volume. Heinicke et al.,[40] for example, reported that in elite endurance athletes, Hb mass and blood volume were ~35% higher, but Hb was no different, from the values observed in sedentary subjects. In contrast, acute altitude exposure has long been known to decrease (plasma) blood volume.[41] However, by comparing untrained subjects or elite cyclists native to either sea level or altitude (~2600 m), Schmidt et al.[42] showed that chronic altitude has a synergistic effect on blood volume parameters. Both Hb mass (for which the observed values were [mean – SD] 17.1 – 1.4 for cyclists native to altitude; 15.4 – 0.9 for cyclists native to sea level; 13.4 – 0.9 for sedentary individuals from altitude and 11.1 – 1.1 g/kg for sedentary individuals native to sea level) and blood volume (for which the corresponding values were 116 – 11; 107 – 6; 88 – 5 and 78 – 8 mL/kg, respectively) were Sports Med 2010; 40 (1)
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affected both by altitude and, to a greater extent, by training. To conclude, differences in the level of ability and or training of the study subjects, as well as differences in their responses to both altitude and to training, make it very difficult to compare the haematological benefits of different hypoxic protocols across studies. 2.2 Non-Haematological Adaptations
Whether increased RBC volume is the primary factor that is responsible for the altitude-induced improvement in performance has recently been the subject of great debate.[43,44] It was noted that the change in performance . is not necessarily associated in elite athwith an increase in VO2max, especially . letes, and that the 86% variance in VO2max could be attributed to factors other than change in RBC volume.[45] Two main peripheral factors have been proposed, as outlined below. 2.2.1 Economy
Several research groups have demonstrated 3–10% improvements in exercise economy[25,45-48] with altitude training. This might come from a decreased cost of ventilation, greater carbohydrate (CHO) use for phosphorylation, or, more likely, from improved mitochondrial efficiency (as denoted by P/O ratio or an increase in ATP production per mole of oxygen used). 2.2.2 pH Regulation and Muscle Buffer Capacity
The altitude-induced increase in the co-transport of lactate is related to the increase in the content of the relevant transporters (i.e. monocarboxylate MCT1 and MCT4). This allows for better lactate exchange and removal and, consequently, a slower pH decrease within ‘glycolyic’ exercise.[49] In addition, it is known that altitude acclimatization induces an increase in isoforms of carbonic anhydrase (CA) that influence both H+ and HCO-3 regulation.[50] These adaptive responses to altitude are likely to improve muscle buffering capacity, as reported previously,[45,48,51] and have been postulated to be, therefore, important in the explanation of post-altitude improvement in performance.[45,48] Whether this is actually the case is debatable. It was shown recently that acidosis (reduced pH) of muscles, is ª 2010 Adis Data Information BV. All rights reserved.
not a primary factor in the development of muscular fatigue. At physiological temperatures, acidification has a small effect on force production, shortening speed, the rate of glycolyic enzyme reactions or on the contractile process.[52] Moreover, acidification seems to preserve the muscle excitability.[53] It is beyond the scope of this review to discuss the main factors (i.e. inorganic phosphate) of muscle fatigue, but since the relationship between acidosis and fatigue is questioned, so is the direct influence of muscle buffering on performance. This is supported by the results of Gore et al.[48] that demonstrated no change in the total work performed during a 2-minute ‘all-out’ cycling trial despite an 18% increase in muscle buffer capacity. However, it is likely that the increased muscle buffer capacity observed after altitude training[51] is of high interest in high-intensity intermittent exercises. 2.3 Performance
Overall the improvement in performance that is obtained with LHTL has been evaluated as 1.0–1.5% for events lasting between 45 seconds and 17 minutes.[6,45] Presenting altitude-induced change in performance or biological variables does not always provide information that is relevant for the practitioner (athlete, coach). As stated in Batterham and Hopkins,[54] ‘‘a non significant result (p > 0.05) effect does not necessary imply that there is no worthwhile effect.’’ The smallest worthwhile effect on performance across a range of sports known for using altitude training (track and field, swimming, cycling) has been shown to be –1%.[55-57] Since the biological variables presented in this review have a direct influence on performance (e.g. haemoglobin mass, RBC mass, . economy or VO2max), one may also assume that –1% is a correct approximation for their smallest worthwhile effect. It is also important to note that the effectiveness of an altitude training regimen is customarily expressed by the ‘additional benefits’ that are obtained over compared periods when similar training is conducted at sea level. Therefore, a given percentage increase has little practical significance per se. Sports Med 2010; 40 (1)
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2.3.1 Aerobic Performance
Levine et al.[8] reported, for 14 elite men and 8 elite women, that sea-level endurance performance was significantly increased after 27 days of living at 2500 m and training at 1250 m. This performance increment amounted to a 1.1% enhancement in 3000. m run-time trial time, and a 3% increase in VO2max. Thus, even elite athletes improved their sea-level performance after 27 days of LHTL strategy. Indeed, 6 years later, Levine and Stray-Gundersen[9] showed that 4 weeks of living at moderate altitude (2500 m) and training at low altitude (1250 m) improved sea-level performance more than equivalent sea-level or LHTH training in 13 well-trained runners. 5000 m runtime trial time was only significantly improved over the initial sea-level value (by an average of 13 – 10 seconds 3 days after return to sea level) in . the LHTL group. Velocity at VO2max and the ventilatory threshold (VT) were also only improved in the LHTL condition. In addition, performance in the 5000 m run-time trial was similar 7, 14 and 21 days post-altitude, suggesting that the beneficial effects of LHTL may last for up to 3 weeks postaltitude. In contrast, the sea-level control group did not improve their 5000 m run performance at any time after completion of the 28-day training period. The effectiveness of the LHTL method was confirmed later by the same research group who noted a 1.1–1.2% increase in sea-level 3000 m run time.[39] This improvement . was accompanied by a 3% improvement in VO2max. The same group concluded that 4 weeks of acclimatization to moderate altitude, accompanied by high-intensity training at low altitude, improved sea-level endurance performance even in elite runners. In contrast, Hahn et al.[13] analysed six different LHTL studies and reported no significant increase in performance . and even a tendency towards a decrease in VO2max. This tendency can be explained partly by the fact that Hb did not increase (see haematological adaptations) and that athletes with . a high VO2max at sea level probably regress to a large extent during altitude training[58] due to the loss of skeletal muscle mitochondria, and reduced oxidative enzyme activity[59,60] caused by the hypoxic stimulus. Therefore, apparently, mitochondrial alteration can occur at moderate altitudes ª 2010 Adis Data Information BV. All rights reserved.
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(2650–3000 m) during a LHTL protocol. It is well known that for trained athletes, .endurance performance may be independent of VO2max and that other submaximal and/or non-haematological variables may have a great influence on their performance.[45,61] In the study of Rusko et al.,[16] 1% and 3% in. creases in sea-level VO2max at day 1 and 7 after the end of the LHTL period were observed. The latter authors concluded that living at a simulated altitude of 2500 . m for 25 days significantly increased sea-level VO2max approximately 1 week after the LHTL period. The same group[37] observed a 4% improvement in 40 km time trial performance on the fifth day following an 11-day LHTL period of living 14 hours a day at a simulated altitude of 2500 m. Since they did not include a control group in their study, it is difficult to know whether this performance enhancement was not primarily training induced. In six male endurance athletes, after sleeping for 23 nights at a simulated altitude of 3000 . m and training at 600 m, both a 4% decrease in VO2 at different submaximal intensities and a 1% increase in mechanical efficiency were reported.[48] In five elite female cyclists who performed LHTL (12 hours at 2650 m, 12 hours at 600 m) over 12 days, the mean power output during a 4-minute cycling time trial was increased to a greater extent (2.3%) in the LHTL group than in the control group (0.1%). In contrast, the mean power output during a 30-minute time trial was decreased in the LHTL group (-1.1%) but increased by 2.4% in the control group.[62] More[46] over, . Saunders et al. observed a 3.3% decrease in VO2 averaged across three submaximal running speeds (14, 16 and 18 km/h) after 20 days of LHTL at 2000–3100 m and 600 m in elite distance runners. In addition, 5, 10 and 15 days of LHTL (8–10 hours at 2650 m and training at 600 m) in 19 well-trained cyclists did not induce any change in performance-related variables.[63] Saunders et al.[46] consequently suggested that 10 or 15 days of LHTL are not more effective than 5 days. In contrast, when combining all the data, i.e. 5, 10 and 15 days of LHTL, a 4% increase in mean power output during a 4-minute time trial over initial values was noticed after LHTL, Sports Med 2010; 40 (1)
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whereas no changes were shown in the sea-level control group. Nor was any change in sea-level . VO2max observed after 10 days of LHTL (12 h/day at 2700 m and training at sea level) in nine endurance athletes.[18] Four groups had 4 weeks of ‘high-high-low’ training camp where they lived at 1780 m, 2085 m, 2454 m or 2805 m and trained together at low to moderate altitude (high-intensity workouts . 1250–1780 m; base training 1700–3000 m). VO2max increased after 4 weeks only at the three highest altitude exposures by 8 – 85 mL, 206 – 60 mL, 308 – 60 mL, and 301 – 73 mL respectively, with 2085 m and 2454 m statistically greater than 1780 m. Both of the groups living at 2085 m and 2454 m improved their 3000 m time by 2.8 – 0.7% and 2.7 – 0.6%, respectively; or 15.7 – 4.0 and 16.6 – 4.2 seconds, respectively (p = 0.003 and 0.002). The groups living at 1780 m and 2805 m did not improve these times (1.1 – 0.05% and 1.4 – 1.1%; 6.3 – 3.1 and 9.0 – 7.1 seconds, respectively).[64] In the French multicentric project,[23-34] an increase in aerobic performance has been observed in some conditions, i.e. in swimmers[28] and runners,[34] but not in others, i.e. Nordic skiers.[27] The change in aerobic fitness. and performance is determined by enhanced VO2max[34] or submaximal parameters.[25,28,34] Overall, these findings show a greater increase in endurance performance with LHTL than with sea-level training, together with an improvement in mechanical efficiency and running economy in elite endurance athletes. LHTL seems to enhance performance to a greater extent in middle-distance aerobic exercise (i.e. lasting 4–10 min, such as the 4000 m team pursuit cycling event or 1500 m running) than in longer events (>30 min). However, few studies report no difference between LHTL and sea-level training.[13,27] Thus, the stress stimuli induced by the combination of training loads, recovery, hypoxic level and duration appear more important in terms of their influence on the ensuing physiological adaptations than those that are induced by hypoxia on its own. 2.3.2 Anaerobic Performance
Only a few investigations into the effects of LHTL on anaerobic performance have been conª 2010 Adis Data Information BV. All rights reserved.
ducted. Nummela and Rusko[65] observed a 1% improvement in 400 m race time in eight 400 m runners after a 10-day LHTL period (16–17 h/day at 2200 m and training at sea level), whereas no difference was observed in the control sea-level group. Moreover, the LHTL group ran significantly faster than the control group at 5.0 mmol/L blood La. The authors suggested that the improved 400 m sprint time after the LHTL period might have been due to an improvement in muscle buffer capacity. This was confirmed by Gore et al.’s[48] finding of a significant (18%) increase in skeletal muscle buffer capacity in six endurance athletes after 23 days of LHTL (sleeping at 3000 m and training at 600 m). Hahn et al.[13] summarized several LHTL normobaric hypoxia studies and stated that sleeping in moderate normobaric hypoxia (2650–3000 m) for longer than 3 weeks could induce practical advantages for elite athletes, but that most of these potential benefits were not likely to result from haematologi. cal (i.e. increased Hb mass or increased VO2max) but, rather, from peripheral adaptations (i.e. muscle buffer capacity or mechanical efficiency). The physiological adaptations are supposed to be identical when training in nitrogen-enriched or with oxygen-extracted hypoxia. However, the uncontrolled use of personal oxygenextracted hypoxic devices (i.e. hypoxic tents) may lead to potential health problems that are not encountered in nitrogen-enriched equipment that is used under medical supervision. The preliminary studies[66,67] conducted on the Hypoxic Altitude Tent System (HAT) reported a large (16 ·) increase in CO2 inside the HAT within the first hour of exposure at the simulated altitude of 2500 m. However, CO2 did not reach unhealthy levels (>3.0%) and the athletes reported only small levels of discomfort or (adverse) side effects. These authors suggested that altitude tents provide a relatively safe and comfortable normobaric hypoxic environment. 2.4 LHTL: Summary and Proposals to Athletes
The optimal altitude for living high has been defined as 2200–2500 m to provide an optimal erythropoietic effect and up to 3100 m for Sports Med 2010; 40 (1)
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non-haematological parameters.[35,64,68,69] Owing to the flat shape of the oxy-haemoglobin dissociation curve above 60 mmHg, changes in PaO2 may not have much effect on SaO2. Indeed, PaO2 values below 60 mmHg are reached from altitudes of about 2500 m,[70] the optimal altitude for LHTH is therefore between 2200 and 2500 m.[71] It is well documented that 1800–1900 m is too low an altitude for inducing consistent and large increase in EPO. The optimal duration at altitude appears to be 4 weeks for inducing accelerated erythropoiesis[9,68,69] whereas less than 3 weeks (i.e. 18 days) is long enough for beneficial changes in economy,[25,32,42,46] muscle buffering capacity,[45,48] the hypoxic ventilatory response[72] or Na+/K+ ATPase activity.[73,74] One critical point is the daily dose of altitude. A natural altitude of 2500 m for 20–22 h/day (in fact, travelling down to the valley only for training) appears sufficient to increase erythropoiesis and improve sea-level performance.[9,46,69] ‘Longer is better’ as regards haematological changes, since additional benefits have been shown as hypoxic exposure increases beyond 16 h/day.[68] The minimum daily dose for stimulating erythropoiesis seems to be 12 h/day,[35] but larger benefits have been reported for exposure of 14–18 h/day.[28,34] For non-haematological changes, the implementation of a much shorter duration of exposure seems possible.
2.5 Advances in the LHTL Method: LHTLi, LHTL Interspersed
It is known that chronic hypoxia reduces muscle Na+/K+ ATPase content, whereas fatiguing contractions reduce Na+/K+ ATPase activity, both of which factors may impair performance.[74] One observed potential side effect of LHTL is the decrease in Na+/K+ ATPase activity that is detrimental to excitation-contraction coupling properties and, therefore, particularly relevant to high-intensity intermittent sports.[75] One way to reverse this detrimental effect is to alternate nights in hypoxia and nights in normoxia, for example, 5 nights in LHTL interspersed with 2 nights in normoxia.[73] ª 2010 Adis Data Information BV. All rights reserved.
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This leads to an improved LHTL method that we call LHTLi (LHTL interspersed). 3. Intermittent Hypoxic Exposure 3.1 Definition
Intermittent hypoxic exposure (IHE) or periodic exposure to hypoxia is defined as an exposure to hypoxia lasting from seconds to hours that is repeated over several days to weeks. These intermittent hypoxic bouts are separated by a return to normoxia or lower levels of hypoxia.[76] IHE in combination with training sessions in hypoxia is referred to as intermittent hypoxic training (IHT).[4,6] Intermittent hypoxic interval training (IHIT) is defined as a method where during a single training session, there is alternation of hypoxia and normoxia. Several experimental designs with a great variability in the length of exposure (seconds to hours), the number of hypoxic exposures a day, the number of consecutive days of exposure, and the level of the hypoxic stimulus are used in endurance sport and have been studied. IHE or IHT raise the question of the minimum duration of exposure for inducing erythropoiesis. Since only relative short periods of hypoxic stimulus are needed to stimulate EPO production,[77-81] it is assumed that IHE and IHT would be sufficient to induce significant increases in sEPO and RBCs and to consequently improve . the endurance performance and VO2max, without all the negative effects of prolonged hypoxic exposure, such as fatigue, decrease in muscle mass or immunodepression. 3.2 Haematological Adaptations
After IHE in progressively increased hypobaric hypoxia (4000–5500 m) for 90 minutes three times a week for 3 weeks, Rodriguez et al.[78] reported a significant increase in Ret count (180%), RBCs (7%), Hb (13%) and Hct (6%). These authors showed that 90 minutes of passive hypoxic exposure was sufficient to obtain significant changes in haematological parameters. An interesting finding from their study was that blood viscosity was not increased. The SaO2 during hypoxia was Sports Med 2010; 40 (1)
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improved (from 60% to 78%). Unfortunately, no control group was included in the investigation. In 16 male triathletes who were exposed 3 hours a day for 5 days a week over 4 weeks to a progressively increased simulated altitude (4000–5000 m), the same research group[82] observed significant 100% and 440% increases in sEPO 3 hours after the first and last IHE sessions, respectively. However, no significant changes were observed in the other haematological parameters (Ret, RBC, total plasma and serum transferrin receptors) that were monitored. The authors suggested that 180 minutes daily of IHE was sufficient to increase endogenous EPO secretion even in highly trained athletes but without producing the subsequent erythropoietic response. Therefore, it was unlikely that the performance would have been increased. Their findings were confirmed by Ricart et al.,[83] who investigated the effects of IHE, i.e. 2 hours a day at a simulated altitude of 5000 m over 14 days, on resting and exercise responses in normoxia and hypoxia. After the IHE period, no changes were observed in any of the measured variables at rest or during a normoxic submaximal exercise. However, during a submaximal hypoxic exercise, ventilatory responses (VE from 55.5 to 67.7 L/min; tidal volume: from 2.0 to 2.6 L) and SaO2 (from 65% to 71%) significantly increased, showing the beginning of an acclimatization to altitude without any potential benefits for sea-level endurance performance. In addition, Frey et al.[84] observed no changes in haematological variables after a 21-day IHE period, 75 minutes a day at 6400 m (FIO2 » 9%), in moderately trained athletes. Meanwhile, a significant increase in sEPO (38%) was measured 2 hours after the first IHE session. Nevertheless, Hellemans[80] showed evidence that contradicted the results of previous IHE studies reporting an increase in EPO without any erythropoietic responses. He investigated the effects of a different IHE method that consisted of alternating 5 minutes of inhaling low O2 gas mixture with 5 minutes of ambient air during 60 minutes. The protocol was two IHE sessions a day during 20 days in ten elite endurance athletes. The FIO2 was ~10% (5800 m) for the first 10 days and then ~9% (6400 m) for the last 10 days. ª 2010 Adis Data Information BV. All rights reserved.
Significant increases in Ret count (29%), Hb (4%) and Hct (5%) were reported. 3.3 Performance
The findings as regards the effect of IHE on endurance performance are equivocal: Hellemans[80] reported a significant improvement (3%) in endurance performance. Rodriguez et al.[78] reported a significantly increased power output at the anaerobic. threshold, but no significant changes in either VO2max or cycling exercise time. Frey et al.[84] observed, after an IHE of 75 minutes a day at 6400 m (FIO2 » 9%) over 21 days, no changes in submaximal or maximal exercise responses in moderately trained female and male athletes. Unfortunately, neither of these two studies included a non-IHE control group. In addition, Rodriguez et al.[85] divided 23 well-trained swimmers and runners to either a hypobaric hypoxic (IHE; simulated altitude of 4000–5500 m) or normoxic (control; 0–500 m) group. Both groups rested in a hypobaric chamber for 3 hours a day, 5 days a week over 4 weeks. No significant changes in time trial performance, i.e. 3000 m run or 100 m and 400 m swim, were observed, within or between . groups. A significant increase in VO2max (3.3% and 0.9%) and in ventilation at peak exercise (VEmax) [8.1% and 1.2%] in the IHE and control groups, respectively, was observed 3 weeks after the IHE period. However, no significant differences between groups were detected. Thus, IHE did not improve swimming or running performance in welltrained athletes to a greater extent than was observed in athletes who followed the same training programme without any hypoxic exposure. In addition, Julian et al.[86] evaluated the effect of 4 weeks of IHE in seven elite distance runners. The IHE protocol was close to the one shown in Hellemans[80] and consisted of altering 5 minutes of hypoxic breathing with 5 minutes of normoxic ambient air over 70 minutes, five times a week. The FIO2 decreased progressively, from 12% in the first week to 11% in the second week and 10% in the third and fourth weeks. A sea-level control group, who followed the same protocol in normoxic conditions, was included. At days 1, 5, 10, and 19 of the IHE protocol and 10 and 25 days Sports Med 2010; 40 (1)
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after the IHE .period, there were no significant differences in VO2max, 3000 m time trial performance, EPO, soluble transferrin receptor or reticulocyte parameters between groups. Thus, 4 weeks of IHE of 5:5 minutes hypoxic:normoxic exposure over 70 minutes five times a week did not induce any improvements in sea-level performance. Recently the inefficiency of IHE has been demonstrated again in a double-blind study:[87] after 15 days of IHE (1 h/day of 6 minutes of breathing 10–11% O2 gas mixture alternated with 4 minutes of breathing . room air), neither the aerobic performance (VO2max) nor the anaerobic variables (peak or mean power during a Wingate test) differed from those of the control group. Overall, in studies with control groups, IHE does not induce any substantial change in either haematological parameters or in endurance performance. 4. Intermittent Hypoxic Training (IHT) Another way to benefit from hypoxic stimulus without undergoing the detrimental effects of a prolonged exposure to hypoxia is to train under hypoxic conditions and to remain at sea level for the rest of the time. Yet the living low training high (LLTH) approach, also called intermittent hypoxic training (IHT), may appear surprising since the time spent in hypoxia may not be sufficient to elicit a raise in RBCs like LHTL, and therefore improve O2 carrying capacity. Furthermore, as during a long sojourn at altitude, the training velocity cannot be as . high as at sea level because of the decrease in VO2max with hypoxia.[88,89] However, LLTH could be advantageous anyway since it can induce an additional stimulus as compared with sea-level training. Specific molecular adaptations at muscular level have been reported after IHT unlike training in normoxia.[90] Over the last 20 years, many studies have reported interesting information about the effects of IHT at haematological and muscular levels and its consequences on performance. Roels et al.[61] also investigated the effects of a new simulated altitude strategy, i.e. IHIT, which is defined as a method whereby during a single training session, there is alternation of hypoxia and normoxia. ª 2010 Adis Data Information BV. All rights reserved.
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4.1 Haematological Adaptations
As expected, in view of the time required for erythropoiesis, no haematological change was reported by most of the studies after IHT. Three training sessions a week, each lasting 45 minutes to 1 hour, at simulated altitudes varying from 2500 to 4000 m over a period of 3–5 weeks did not induce a change in Hct or Hb.[91-93] According to several studies, an exposure of 1 h/day would be insufficient to elicit haematological changes.[93-96] Terrados et al.[97] have reported that even training sessions of 2 hours at 2300 m, repeated 4–5 times a week for 4 weeks, did not modify haematological parameters. These results are in agreement with the fact that several hours of continuous exposure to hypoxia are needed to obtain an increase in the levels of EPO.[79,98] These results were confirmed by Vallier et al.[91] in elite triathletes performing IHT 3 days a week over 3 weeks at a hypobaric-simulated altitude of 4000 m. The training sessions consisted of ~60 minutes of steady workouts at 66% of maximum power and interval workouts at 85% of maximum power. Seven days after the end of the IHT protocol, no significant differences were observed in the haematological variables. However, IHT may be more efficient at improving haematological parameters if combined with IHE. Rodriguez et al.[77] examined the combined effects of IHE and IHT in 17 subjects who conducted a high-altitude expedition. IHE consisted in an exposure of 3–5 h/day for 9 days at altitudes that progressively increased (from 4000 m to 5500 m). In addition, the subjects had to perform three to five training sessions a week (30–75 minutes each) at low intensity. The authors observed a significantly increased RBC (+12%), Ret (+54%), Hb (+18%) and Hct (+11%) when the data of both groups were combined. These authors concluded that IHE in hypobaric hypoxia could stimulate the erythropoietic response. Casas et al.,[99] using the same protocol as Rodriguez et al.[77] but for 17 days, found significant increases in packed cell volume from 41% to 44.6%, in RBC from 4.61 to 4.97 106 cells/mL and in Hb from 14.8 to 16.4 g/dL. The authors suggested that short-term hypobaric hypoxia with Sports Med 2010; 40 (1)
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low-intensity training induced an improvement in the blood oxygen transport capacity. To our knowledge, Meeuwsen et al.[100] are the only authors who reported an increase in Hct and Hb following a non-combined IHT. In their study, eight triathletes had to cycle for 2 h/day at 2500 m (60–70% of heart rate [HR] reserve) for 10 consecutive days. Two days after the IHT period, there was an increase in both Hct (48 – 2% vs 43 – 2%) and Hb (9.6 – 0.19 vs 9.17 – 0.27). Nevertheless, 9 days after the end of the training period these parameters had returned to their baseline values. According to the authors, this unexpected increase in both Hct and Hb cannot be explained by dehydration since there was no change in the plasma volume. On the other hand, it is possible that the concentration of training sessions over a 10-day period as well as their duration played a role in these haematological changes. In view of all the results of the studies mentioned above, IHT alone does not seem to have any significant effect on haematological parameters. Combining this kind of training with IHE may, however, be efficient as a method of improving O2 carrying capacity. 4.2 Muscular Adaptations
Training per se in hypoxia increases mitochondrial and capillary density, capillary-to-fibre ratio, fibre cross-section area, myoglobin content and oxidative enzyme activity such as citrate Moreover, LLTH protocols synthase.[101-104] . improved VO2max and endurance performance not only in hypoxic conditions but also at sea level.[97,101] Therefore, training under hypoxic conditions (~3850 m) seems to induce specific muscular and peripheral adaptations, due to activation of hypoxia-inducible factor 1a (HIF-1a), which is not activated to the same extent by training in normoxia or by passive hypoxic exposure.[90] The study of Terrados et al.[102] is one of the first to have investigated the effects of IHT on muscle tissue in man. The protocol consisted of training one leg in normoxia and the other one in hypoxia (corresponding to 2300 m) for 30 minutes 3–4 times a week. Analysis of the muscular biopsies revealed ª 2010 Adis Data Information BV. All rights reserved.
that both citrate synthase activity and myoglobin content were higher after IHT as compared with sea-level training. Another study using a similar protocol confirmed that citrate synthase increased more after IHT (~3500 m; FIO2 = 13.5%) than after training in normoxia.[101] On the other hand, Terrados et al.[102] did not report any change in citrate synthase after a 1-month IHT at ~2300 m in elite cyclists. More recent studies have tested the effects of a 6-week IHT (five sessions/week) on muscular adaptations in untrained men.[90,105,106] The subjects were divided into normoxic and IHT (3850 m; FIO2 = 13%) groups. Within each group, a high (at the anaerobic threshold) and a low (at ~25% below the anaerobic threshold) training intensity subgroup was formed. Muscle biopsies of the vastus lateralis showed an enhancement of capillary length density after IHT only, as well as a greater increase in mitochondrial volume density after IHT than after training at sea level. Interestingly, the greatest increases in both these parameters occurred in the IHT group who trained at high intensity. Thus, when IHT was performed at high intensity, it induced greater muscle adaptations to compensate for the decreased O2 availability. Together, these results demonstrate that IHT leads to muscular adaptations that either do not occur in normoxic conditions or, if they do so, do so to a lesser degree. These muscular changes may have an origin at the molecular level, via the activation of a transcription factor, namely HIF-1, expressed in skeletal muscle of all mammalians. Vogt et al.[90] have reported an increase in HIF-1a messenger RNA (mRNA) after both high (+ 82.4%) and low (+78.4%) training intensity in hypoxia (3850 m), demonstrating that IHT could modify the gene expression. The higher concentration of HIF-1a mRNA was accompanied by an increase in both mRNA of vascular endothelial growth factor (VEGF) and myoglobin but only after the high-intensity training in hypoxia. These findings made the authors conclude that training in hypoxia at high intensity is the most likely way to favour oxygen transport and utilization under hypoxic conditions. Very recently, another study emphasized the role of exercising at high intensity on the extent Sports Med 2010; 40 (1)
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of muscular adaptations during IHT.[49,107] In this study, endurance-trained subjects performed 6 weeks of training at the second VT (VT2). Contrary to the previous studies, training in hypoxia was not carried out at each session but included twice a week within the normal training of the athletes. Furthermore, the simulated altitude was lower (~2500 m). After the training period, most results of the muscular biopsies were significant. The authors especially found an increase in mRNA concentrations of HIF-1a (+104%), glucose transporter-4 (+32%), phosphofructokinase (+32%), citrate synthase (+28%), carbonic anhydrase-3 (+74%) or monocarboxylate transporter-1 (+44%). No change occurred in the control group. However, unlike what was previously reported,[78] there was no significant difference in mRNA concentrations of VEGF and myoglobin after IHT. The practical implications of the responses of the genes to training are still questionable.[108] Firstly, the observed increase in mRNA of these encoding proteins (enzymes, transcription factor) does not automatically induce an increase in the synthesis of the specific proteins regulating the response to altitude training. The continuity between specific signalling pathways and subsequent protein synthesis in response to altitude training has not been detailed. Secondly, there is a discrepancy between the local molecular changes and the global physiological changes, as shown for example in IHT by Vogt et al.[90] However, these results, by showing that the expression of many genes in muscles is specific to training in hypoxia and different to training in normoxia, highlight the complexity of the adaptive multifactorial response to altitude training. 4.3 Performance
The main objective of altitude training is to improve sea-level performance. Therefore, one could wonder whether the molecular and structural adaptations following IHT are advantageous after the return at sea level. Since the LLTH method has been reported to improve some factors involved in O2 utilization within the muscle[49,90,101,102,104,106,107] but also to positively modify pH regulation and lactate ª 2010 Adis Data Information BV. All rights reserved.
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transport,[49] an improvement in aerobic and/or anaerobic performance might be expected after IHT. 4.3.1 Aerobic Performance
While several studies have reported that IHT induced a better aerobic performance in hypoxic conditions,[97,106,109] what about performance in a normoxic environment? Like the other hypoxic methods, the results are controversial. Some studies did not find any change[91,97] or reported no greater improvement in normoxic . VO2max after LLTH than after sea-level training.[93,106] This result was confirmed by the studies of Roels et al.[61,110,111] IHIT and IHT of up to ~115 min/week were not sufficient to elicit a greater increase in aerobic performance or significant changes in haematological variables compared with a similar normoxic interval training.[61] However, these different training methods induced different responses during the 3-week post-training period: only the IHT group maintained their performance. An IHT of ~380 min/week was not sufficient to elicit a greater increase in aerobic or anaerobic performances or significant changes in haematological variables and MCT1 and MCT4 protein content, when compared with a similar normoxic interval training. However, IHT improved the aerobic power at altitude.[110] An IHT of ~380 min/week altered the intrinsic properties of mitochondrial function, i.e. the substrate preference such that lower fat oxidation and increased glutamate utilization were observed.[111] . On the other hand, VO2max increased 9 days after training in hypoxia in the study of Meeuwsen et al.,[100] whereas it was unchanged after 2 days. This may be explained by the higher concentration and duration of the training sessions. Nevertheless, . a 5% increase in VO2max has also been found by Dufour et al.[109] after 6 weeks of IHT in endurance trained runners. Furthermore, a dramatic improvement of the. time to exhaustion (+35%) as well as a higher VO2 at VT2 (+7%) was also reported in this study. According to the authors, these results were due to the combination of the hypoxic stimulus and the high training intensity that was established at VT2. Another study using Sports Med 2010; 40 (1)
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high-intensity interval training (45–60 minutes within a 2-hour session in hypoxia) 4–5 times a week in elite cyclists reported an increase both in work capacity and in maximal power output during a laboratory test in normoxia.[97] It was concluded that performance at sea level was at least as much improved by hypoxic as by normoxic training. Previously however, a 5-week high-intensity IHT did not lead to a greater improvement in . VO2max measured in normoxia in a 400 m freestyle than that obtained by sea-level training in . swimmers.[92] Similar results concerning VO2max as well as lactate threshold were reported in team sports players after a 4-week period of IHT that consisted of cycling 30 minutes at high intensity three times a week. In both these studies, the duration of the high-intensity exercises in hypoxia was shorter than in the study of Dufour et al.[109] (30 seconds to 1 minute vs 12–20 minutes) or Terrados et al.,[97] which could partly explain the lack of significant results. Recently, Roels et al.[110] have found that 3 weeks of IHT combining continuous training at low intensity (60% . VO2max three times a week) and interval training (100% of peak power output twice a week) had no . effect on VO2max and did not increase maximal power output more than training at sea level. Another way to perform IHT is to use interval exercises alternating hypoxia and normoxia periods (IHIT). This original approach does, however, not seem efficient in eliciting a greater increase in aerobic performance or significant changes in haematological variables compared with similar normoxic interval training.[61] Another strategy could be to combine IHE and IHT within the same training period. Using this approach, Rodriguez et al.[77] found a significant increase in exercise time (+3.9%) and . VEmax (+5.5%) but without any change in VO2max. These authors suggested that short-term IHE stimulates EPO secretion (see haematological adaptations), which in turn enhances endurance performance. The same research group[99] also reported that the combination of IHT and IHE induced a decrease in submaximal HR, a shift to the right of the lactate versus exercise load curve, and an increase in the anaerobic threshold, which indicates an enhanced endurance performance. ª 2010 Adis Data Information BV. All rights reserved.
When taking into account the results of all the studies presented above, one could conclude that IHT might have a positive impact on aerobic performance but whether it does so or not probably depends on the combination of exercise duration and intensity as well as on the degree of hypoxia during training. 4.3.2 Anaerobic Performance
Very few studies have, to date, focused on the effects of IHT on anaerobic performance. Among these studies only one has found positive effects.[100] In this study, 9 days after training in hypoxia, performance in the Wingate test (i.e. an anaerobic specific test) significantly increased, in contrast to what was observed in the control group. Both peak and mean power reached during this test were improved, by about 5% on average. Furthermore, the time to peak was decreased by 37%. Another study also found an improvement in peak and mean power during the Wingate test but the difference was not significant compared with the group who trained at sea level.[112] Truijens et al.,[92] who assessed anaerobic performance in swimmers using a 100 m freestyle time trial, did not find a greater improvement in the hypoxic than in the control group. They also reported no change in anaerobic capacity, as assessed by the accumulated oxygen deficit. The current data are probably insufficient to conclude whether IHT has a positive impact on anaerobic performance or not. Even though some factors involved in pH regulation or lactate transportation could change after IHT[49] and could therefore be advantageous for anaerobic glycolysis, further studies will have to be carried out to provide more information. 4.4 An Original Intermittent Hypoxic Training (IHT) Method: Training with Voluntary Hypoventilation
Very recently, two studies have demonstrated that it could be possible to get a significant arterial desaturation during exercise without being placed in an hypoxic environment.[113,114] This is actually possible by voluntarily reducing the breathing frequency and by holding one’s breath at low Sports Med 2010; 40 (1)
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pulmonary volumes. Thus, repeatedly using this respiratory technique during training would represent an intermittent hypoxic exposure and could therefore be likened to IHT, although hypoventilation also induces hypercapnia. Woorons et al.[113] have shown that training that way did not modify haematological parameters or aerobic performance. On the other hand, the authors reported both a higher pH and HCO-3 at a high submaximal intensity reflecting a delayed acidosis possibly due to an improvement in the buffer capacity. Furthermore, the velocity at maximal exercise was improved by 0.5 km/h in 85% of the subjects and correlated to the change in HCO-3 at submaximal exercise. Even though no other study has ever investigated the effects of voluntary hypoventilation training, these first results suggest that this training method could be advantageous for anaerobic performance. Further studies should in any case bring more knowledge to bear on this specific topic. 4.5 IHT: Summary and Proposals to Athletes
Athletes engaged in endurance sports could take advantage of IHT especially during the precompetitive phase. Twice a week, they should include in their training programme a training session including 30–45 minutes of high-intensity exercises at a simulated altitude of 2500–3000 m. The high-intensity exercises should be around the anaerobic threshold and organized in series of 10–20 minutes. To obtain a greater improvement in aerobic capacity, in addition to IHT, athletes could spend 3 hours in hypoxia at rest, 4–5 times a week. IHT seems more beneficial than IHE in performance enhancement, but without clear explanation. The results of Hoppeler and Vogt[115] are promising in that they show that hypoxic exercise intensity per se might play a role on adaptations at the molecular level in skeletal muscle tissue. While research on intermittent hypoxia has accelerated in the recent years, many basic and applied questions still remain to be answered. Overall as pointed out by Wilber,[1] it is unlikely that IHT induces any improvement in . VO2max as a result of the altitude dose (no IHT ª 2010 Adis Data Information BV. All rights reserved.
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studies have reported this increase). However, improvement in athletic performance is likely to happen with high intensity (above ventilatory threshold) due to an increase in mitochondrial efficiency and pH/lactate regulation.[49,107,116] 4.6 A Promising Combination: Living High-Training Low and High, Interspersed
There is an agreement that LHTL induces some slight increase in aerobic performance (1.0–1.5%)[1,117] and we propose using a modified pattern by alternating nights high and nights low (LHTLi; e.g. 5–2 or 6–1). In addition, there is clear evidence that intense exercise at high altitude stimulates to a greater extent the muscle adaptations for both aerobic and anaerobic exercise and limits the decrease in power. It is currently unknown if coupling LHTL and ITH would be the optimal combination and further scientific investigations are required. However, we suggest that a training pattern associating LHTLi (five nights at 3000 m and two nights at sea level) with training at sea level except for a few (2.3 per week) sessions of suprathreshold training might be very efficient, especially in intermittent sports (football, tennis, squash). Of interest is that this combination of hypoxic methods (that we suggest naming LHTLHi) is currently used with success by squash and football players in a sports academy, and was used by a national football team during the qualification games for the 2010 World Cup. 5. Proposals for Optimal Combination of Hypoxic Methods in the Yearly Training Plan One of the most difficult tasks of the coach is to lead his athletes at their peak fitness at the appropriate time, i.e. for the main competition. Periodization is critical in every sport and periodization of hypoxic training is very challenging. As described in this review, the underlying mechanisms behind the effects of hypoxic training are widely debated. Although the popular view is that altitude training may lead to an increase in haematological capacity, this may not be the main, or the Sports Med 2010; 40 (1)
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a Base model: combination between hypoxic training and normoxic training in the preparatory training period Hypoxia Normoxia
Training load
Very high High Medium Low Very low
Training Int
Days
Int ≤ VT1 strength training
Int ≤ VT1 Int ≤ VT2 strength training
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Int ≤ VT1 Int ≤ VT2 Int ≤ MAP strength training 7
Int ≤ VT1
Int ≤ VT1 Int ≤ VT2 strength training
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Int ≤ VT1 Int ≤ VT2 Int ≤ MAP strength training 7
Int ≤ VT1 Int ≤ VT2 Int ≤ MAP strength training 7
Recovery int ≤ VT1
Short recovery Int ≤ VT1
Competition period at altitude
2 to 3
1 to 15
Short recovery Int ≤ VT1
Competition period at sea level
2 to 3
1 to 15
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b Hypoxic training model: to prepare a period of competitions at altitude Hypoxia Normoxia
Training load
Very high High Medium Low Very low
Training intensity
Days
Int ≤ VT1 strength training
Int ≤ VT1 Int ≤ VT2 strength training
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Int ≤ VT1 Int ≤ VT2 Int ≤ MAP strength training 7
Int ≤ VT1
Int ≤ VT1 Int ≤ VT2 strength training
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Int ≤ VT1 Int ≤ VT2 Int ≤ MAP strength training 5
c Hypoxic training model: to prepare a period of competitions at sea level Hypoxia Normoxia
Training load
Training intensity
Days
Very high High Medium Low Very low Int ≤ VT1 strength training
Int ≤ VT1 Int ≤ VT2 strength training
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7
Int ≤ VT1 Int ≤ VT2 Int ≤ MAP strength training 7
Int ≤ VT1
Int ≤ VT1 Int ≤ VT2 strength training
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Int ≤ VT1 Int ≤ VT2 Int ≤ MAP strength training 5
Fig. 3. Schematic view of combinations between periods of training in hypoxic and normoxic conditions: one to three base models can be proposed during the preparatory training period depending on the duration of this period: (a) base training; (b) preparation for competitions at altitude; and (c) preparation for competitions at sea level. A base training model can be followed by an hypoxic training model to prepare competitions at sea level or at altitude. Int = intensity of the training; MAP = maximal aerobic power; VT1 = first ventilatory threshold; VT2 = second ventilatory threshold.
only, factor involved in the improvement of performance. Other central (such as ventilatory, haemodynamics or neural adaptations) or peripheral (such ª 2010 Adis Data Information BV. All rights reserved.
as muscle-buffering capacity or economy) factors play an important role. Therefore, it is logical that the extent to which an athlete may benefit from Sports Med 2010; 40 (1)
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19
these different methods of hypoxic training will differ according to both his/her general and specific training focus (i.e. between endurance, intermittent such as team sports and racket sports, or sprint/ power sports; and between different periods of the training year). To date, there is no study that has investigated how to incorporate hypoxic training into the athlete’s general training programme. So the following proposal requires further investigation. We propose two different patterns of combination of hypoxic and normoxic methods. The first proposal is a ‘traditional’ approach using only terrestrial LHTH hypoxic exposure and combines high-high and sea-level training phases during the base training (figure 3a), to prepare for a competition in altitude (figure 3b) and at sea level (figure 3c), respectively. The second proposal combines all the hypoxic methods described in this review (LHTH, LHTL,
LHTLHi and IHT) and therefore requires some specific technological equipment. 5.1 Combining High-High Hypoxic and Sea-Level Training
The choice of the duration, altitude level; i.e. altitude dose and training content; volume; intensity; i.e. training load is paramount in order to optimize the hypoxic benefits and to peak in elite athletes. The intensity of training lower or equal to the first VT (VT1) can be considered as the base of the training for the high-level athletes in endurance.[118-123] This intensity of training is particularly important in association with hypoxic stress, especially during the acute hypoxic period as shown by Schmitt et al.[24] Indeed, the acute hypoxic situation modifies autonomic nervous system (ANS) activity by decreasing the total LHTH IHT LHTLHi Preparatory competition Main competition/tournment
Endurance sports Preparation phase Altitude (m) 1 3000 2500 2000 1500
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‘Lactic’ sports Preparation phase Altitude (m) 1 3000 2500 2000 1500
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9
Precompetition phase
Competition phase
10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44
Intermittent sports Preparation phase Altitude (m) 1 3000 2500 2000 1500
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Precompetition phase
Competition phase
10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44
Fig. 4. Schematic view of periodization of hypoxic methods in endurance, glycolitic and intermittent sports. IHT = intermittent hypoxic training; LHTH = living high-training high; LHTLHi = living high-training low and high interspersed.
ª 2010 Adis Data Information BV. All rights reserved.
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Table I. Overall efficiency of various hypoxic methods (calculated from Wilber[1]) Hypoxic method
Number of studies
Increased performance/positive mechanisms
No additional effect
Negative mechanisms
Nitrogen dilution
19
12
2
5
Oxygen filtration
10
5
2
3
58%
14%
28%
8
8
0
50%
50%
0%
56%
18%
18%
LHTL IHT All
16 45
IHT = intermittent hypoxic training; LHTL = live high-train low.
heart rate variability (HRV) and especially high frequency activity (HF),[118] whereas training at or lower than VT1 intensity increases HRV and HF.[124] Furthermore, Seiler et al.[121] showed that VT1 may define ‘binary’ thresholds for ANS/ HRV recovery in highly trained athletes. The association of training at an intensity lower or equal to VT1 and hypoxic stress is thus well supported by athletes and is an optimal combination to improve aerobic capacities during the critical period of the acute hypoxia. Progressively after the acclimatization period, usually from the ~8th day, HRV and HF start to increase.[125] It is therefore possible to prescribe higher training intensities, for example, between VT1 and the second ventilatory threshold (VT2), and progressively intensities higher than VT2. 5.2 Combining All Hypoxic Methods
The second proposal aims to use advanced technological methods in order to combine haematological and peripheral benefits of each of these methods in order to improve peak performance in elite athletes. Periodization in three types of sports are proposed and summarized in figure 4. 5.2.1 Endurance Sports
Since extensive ‘base training’ is paramount in this type of sport, LHTH training during winter appears appropriate. The decline in exercise intensity will not be detrimental at this time of the year. Repeating several LHTH sojourns at high altitude will also help to speed up the acclimatization from one camp to another. It is known that the threshold altitude for a sustained increase in blood EPO concentration is about 2200 m. We ª 2010 Adis Data Information BV. All rights reserved.
therefore recommend two to three sojourns of 3–4 weeks each between 2200 and 2500 m. During the pre-competition phase, a shorter sojourn (18–21 days) at a lower altitude (1800–2000 m) will allow more intense intervaltraining sessions. During the competition period, athletes can benefit from intense IHT sessions or – if there is a break from a LHTLHi block (sleeping high at 3000 m for 5 days – sleeping at sea level for 2 days and training in normoxia except for two hypoxic ‘threshold’ sessions per week). 5.2.2 ‘Glycolytic’ Sports
During the winter preparation, the programme would benefit from a sojourn at altitude (2200–2500 m) aiming to increase the RBC volume. Later, inclusion of 3-week blocks (1–2 IHT sessions per week: supramaximal interval training and/or lactate tolerance session at high altitude 3000 m) alternated with normoxic-only training would boost the muscle ‘anaerobic’ adaptations. Prior to the main competition, LHTLHi (2–3 weeks of sleeping high 3000 m for 5 days – sleeping at sea level for 2 days and training in normoxia except for two hypoxic interval-training sessions per week) would allow peaking without reducing the intensity of the specific sessions. 5.2.3 Intermittent Sports
During phase 1 of the winter preparation, a sojourn at a low altitude (1500–1700 m) would be of benefit, aiming to develop aerobic fitness. Later, a few blocks of 3 consecutive weeks (1–2 IHT sessions per week: supramaximal interval training) would help to increase muscle adaptations for pH and buffer capacity. Sports Med 2010; 40 (1)
Combining Hypoxic Methods
LHTLHi (2–3 weeks of sleeping high at 2500 m for 5 days, sleeping at sea level for 2 days and training in normoxia except for one hypoxic interval-training session per week) would be appropriate to boost both central and peripheral adaptations prior to the main tournament/performance.
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6. Conclusions The aims and benefits of the various hypoxic methods are numerous and extend beyond an increase in O2 transport capacity. It is known that IHE is inefficient for performance enhancement. The efficiency of the other methods was evaluated in a recent review[1] and is summarized in table I. LHTL has been well investigated; the other methods (IHT and LHTLHi) still require further investigation to better understand their outcomes and mechanisms. However, the further development of practical expertise in hypoxic training will predominantly involve decisions about how to combine these methods in order to induce optimal performance in various types of sports and to reach peak performance in the athlete’s main competitions. Acknowledgements No sources of funding were used to assist in the preparation of this article. The authors have no conflicts of interest that are directly relevant to the content of this article. The authors acknowledge the anonymous reviewers for their valuable comments and Dr V.E. Vleck who thoroughly reviewed the English manuscript.
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72. Townsend NE, Gore CJ, Hahn AG, et al. Living hightraining low increases hypoxic ventilatory response of well-trained endurance athletes. J Appl Physiol 2002 Oct; 93 (4): 1498-505 73. Aughey RJ, Clark SA, Gore CJ, et al. Interspersed normoxia during live high, train low interventions reverses an early reduction in muscle Na+, K+ ATPase activity in well-trained athletes. Eur J Appl Physiol 2006 Oct; 98 (3): 299-309 74. Aughey RJ, Gore CJ, Hahn AG, et al. Chronic intermittent hypoxia and incremental cycling exercise independently depress muscle in vitro maximal Na+-K+-ATPase activity in well-trained athletes. J Appl Physiol 2005 Jan; 98 (1): 186-92 75. Girard O, Millet GP. Neuromuscular fatigue in racquet sports. Neurologic Clin 2008; 26 (1): 181-94 76. Powell FL, Garcia N. Physiological effects of intermittent hypoxia. High Alt Med Biol 2000 Summer; 1 (2): 125-36 77. Rodriguez FA, Casas H, Casas M, et al. Intermittent hypobaric hypoxia stimulates erythropoiesis and improves aerobic capacity. Med Sci Sports Exerc 1999 Feb; 31 (2): 264-8 78. Rodriguez FA, Ventura JL, Casas M, et al. Erythropoietin acute reaction and haematological adaptations to short, intermittent hypobaric hypoxia. Eur J Appl Physiol 2000 Jun; 82 (3): 170-7 79. Eckardt KU, Boutellier U, Kurtz A, et al. Rate of erythropoietin formation in humans in response to acute hypobaric hypoxia. J Appl Physiol 1989 Apr; 66 (4): 1785-8 80. Hellemans J. Intermittent hypoxic training: a pilot study. Proceedings of the Second Annual International Altitude Training Symposium; 1999 Feb 18-20; Flagstaff (AZ); 145-54 81. Knaupp W, Khilnani S, Sherwood J, et al. Erythropoietin response to acute normobaric hypoxia in humans. J Appl Physiol 1992 Sep; 73 (3): 837-40 82. Abellan R, Remacha AF, Ventura R, et al. Hematologic response to four weeks of intermittent hypobaric hypoxia in highly trained athletes. Haematologica 2005 Jan; 90 (1): 126-7 83. Ricart A, Casas H, Casas M, et al. Acclimatization near home? Early respiratory changes after short-term intermittent exposure to simulated altitude. Wilderness Environ Med 2000 Summer; 11 (2): 84-8 84. Frey WO, Zenhausern R, Colombani PC. Influence of intermittent exposure to normobaric hypoxia on hematological indexes and exercise performance [abstract]. Med Sci Sports 2000; 32 Suppl. 5: S65 85. Rodriguez FA, Murio J, Ventura JL. Effects of intermittent hypobaric hypoxia and altitude training on physiological and performance parameters in swimmers [abstract]. Med Sci Sports Exerc 2003; 35: S115 86. Julian CG, Gore CJ, Wilber RL, et al. Intermittent normobaric hypoxia does not alter performance or erythropoietic markers in highly trained distance runners. J Appl Physiol 2004 May; 96 (5): 1800-7 87. Tadibi V, Dehnert C, Menold E, et al. Unchanged anaerobic and aerobic performance after short-term intermittent hypoxia. Med Sci Sports Exerc 2007 May; 39 (5): 858-64
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88. Woorons X, Mollard P, Lamberto C, et al. Effect of acute hypoxia on maximal exercise in trained and sedentary women. Med Sci Sports Exerc 2005 Jan; 37 (1): 147-54 89. Mollard P, Woorons X, Letournel M, et al. Role of maximal.heart rate and arterial O2 saturation on the decrement of VO2max in moderate acute hypoxia in trained and untrained men. Int J Sports Med 2007 Mar; 28 (3): 186-92 90. Vogt M, Puntschart A, Geiser J, et al. Molecular adaptations in human skeletal muscle to endurance training under simulated hypoxic conditions. J Appl Physiol 2001 Jul; 91 (1): 173-82 91. Vallier JM, Chateau P, Guezennec CY. Effects of physical training in a hypobaric chamber on the physical performance of competitive triathletes. Eur J Appl Physiol Occup Physiol 1996; 73 (5): 471-8 92. Truijens MJ, Toussaint HM, Dow J, et al. Effect of highintensity hypoxic training on sea-level swimming performances. J Appl Physiol 2003 Feb; 94 (2): 733-43 93. Emonson DL, Aminuddin AH,. Wight RL, et al. Traininginduced increases in sea level VO2max and endurance are not enhanced by acute hypobaric exposure. Eur J Appl Physiol Occup Physiol 1997; 76 (1): 8-12 94. Siri WE, Van Dyke DC, Winchell HS, et al. Early erythropoietin, blood, and physiological responses to severe hypoxia in man. J Appl Physiol 1966 Jan; 21 (1): 73-80 95. Levine BD, Stray-Gundersen J. A practical approach to altitude training: where to live and train for optimal performance enhancement. Int J Sports Med 1992 Oct; 13 Suppl 1: S209-12 96. Engfred K, Kjaer M, Secher NH, et al. Hypoxia and training-induced adaptation of hormonal responses to exercise in humans. Eur J Appl Physiol Occup Physiol 1994; 68 (4): 303-9 97. Terrados N, Melichna J, Sylven C, et al. Effects of training at simulated altitude on performance and muscle metabolic capacity in competitive road cyclists. Eur J Appl Physiol Occup Physiol 1988; 57 (2): 203-9 98. Schmidt W, Eckardt KU, Hilgendorf A, et al. Effects of maximal and submaximal exercise under normoxic and hypoxic conditions on serum erythropoietin level. Int J Sports Med 1991 Oct; 12 (5): 457-61 99. Casas M, Casas H, Pages T, et al. Intermittent hypobaric hypoxia induces altitude acclimation and improves the lactate threshold. Aviat Space Environ Med 2000 Feb; 71 (2): 125-30 100. Meeuwsen T, Hendriksen IJ, Holewijn M. Traininginduced increases in sea-level performance are enhanced by acute intermittent hypobaric hypoxia. Eur J Appl Physiol 2001 Apr; 84 (4): 283-90 101. Melissa L, MacDougall JD, Tarnopolsky MA, et al. Skeletal muscle adaptations to training under normobaric hypoxic versus normoxic conditions. Med Sci Sports Exerc 1997 Feb; 29 (2): 238-43 102. Terrados N, Jansson E, Sylven C, et al. Is hypoxia a stimulus for synthesis of oxidative enzymes and myoglobin? J Appl Physiol 1990 Jun; 68 (6): 2369-72 103. Green H, MacDougall J, Tarnopolsky M, et al. Downregulation of Na+-K+-ATPase pumps in skeletal muscle with training in normobaric hypoxia. J Appl Physiol 1999 May; 86 (5): 1745-8
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Millet et al.
104. Desplanches D, Hoppeler H, Linossier MT, et al. Effects of training in normoxia and normobaric hypoxia on human muscle ultrastructure. Pflugers Arch 1993 Nov; 425 (3-4): 263-7 105. Hoppeler H, Vogt M, Weibel ER, et al. Response of skeletal muscle mitochondria to hypoxia. Exp Physiol 2003 Jan; 88 (1): 109-19 106. Geiser J, Vogt M, Billeter R, et al. Training high-living low: changes of aerobic performance and muscle structure with training at simulated altitude. Int J Sports Med 2001 Nov; 22 (8): 579-85 107. Ponsot E, Dufour SP, Zoll J, et al. Exercise training in normobaric hypoxia in endurance runners. II: Improvement of mitochondrial properties in skeletal muscle. J Appl Physiol 2006 Apr; 100 (4): 1249-57 108. Coffey VG, Hawley JA. The molecular bases of training adaptation. Sports Med 2007; 37 (9): 737-63 109. Dufour SP, Ponsot E, Zoll J, et al. Exercise training in normobaric hypoxia in endurance runners. I: Improvement in aerobic performance capacity. J Appl Physiol 2006 Apr; 100 (4): 1238-48 110. Roels B, Bentley DJ, Coste O, et al. Effects of intermittent hypoxic training on cycling performance in well-trained athletes. Eur J Appl Physiol 2007 Oct; 101 (3): 359-68 111. Roels B, Thomas C, Bentley DJ, et al. Effects of intermittent hypoxic training on amino and fatty acid oxidative combustion in human permeabilized muscle fibers. J Appl Physiol 2007 Jan; 102 (1): 79-86 112. Morton JP, Cable NT. Effects of intermittent hypoxic training on aerobic and anaerobic performance. Ergonomics 2005 Sep 15-Nov 15; 48 (11-14): 1535-46 113. Woorons X, Mollard P, Pichon A, et al. Effects of a 4-week training with voluntary hypoventilation carried out at low pulmonary volumes. Respir Physiol Neurobiol 2008 Feb 1; 160 (2): 123-30 114. Woorons X, Mollard P, Pichon A, et al. Prolonged expiration down to residual volume leads to severe arterial hypoxemia in athletes during submaximal exercise. Respir Physiol Neurobiol 2007 Aug 15; 158 (1): 75-82 115. Hoppeler H, Vogt M. Muscle tissue adaptations to hypoxia. J Exp Biol 2001 Sep; 204 (Pt 18): 3133-9 116. Katayama K, Matsuo H, Ishida K, et al. Intermittent hypoxia improves endurance performance and submaximal exercise efficiency. High Alt Med Biol 2003 Fall; 4 (3): 291-304 117. Wilber RL, Stray-Gundersen J, Levine BD. Effect of hypoxic ‘‘dose’’ on physiological responses and sea-level performance. Med Sci Sports Exerc 2007 Sep; 39 (9): 1590-9 118. Sevre K, Bendz B, Hanko E, et al. Reduced autonomic activity during stepwise exposure to high altitude. Acta Physiol Scand 2001 Dec; 173 (4): 409-17 119. Fiskerstrand A, Seiler KS. Training and performance characteristics among Norwegian international rowers 19702001. Scand J Med Sci Sports 2004 Oct; 14 (5): 303-10 120. Seiler KS, Kjerland GO. Quantifying training intensity distribution in elite endurance athletes: is there evidence for an ‘‘optimal’’ distribution? Scand J Med Sci Sports 2006 Feb; 16 (1): 49-56 121. Seiler S, Haugen O, Kuffel E. Autonomic recovery after exercise in trained athletes: intensity and duration effects. Med Sci Sports Exerc 2007 Aug; 39 (8): 1366-73
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Combining Hypoxic Methods
122. Esteve-Lanao J, Foster C, Seiler S, et al. Impact of training intensity distribution on performance in endurance athletes. J Strength Cond Res 2007 Aug; 21 (3): 943-9 123. Esteve-Lanao J, San Juan AF, Earnest CP, et al. How do endurance runners actually train? Relationship with competition performance. Med Sci Sports Exerc 2005 Mar; 37 (3): 496-504 124. Yamamoto K, Miyachi M, Saitoh T, et al. Effects of endurance training on resting and post-exercise cardiac autonomic control. Med Sci Sports Exerc 2001 Sep; 33 (9): 1496-502
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125. Bernardi L, Passino C, Serebrovskaya Z, et al. Respiratory and cardiovascular adaptations to progressive hypoxia: effect of interval hypoxic training. Eur Heart J 2001 May; 22 (10): 879-86
Correspondence: Dr Gregoire P. Millet, ISSUL, Institute of Sport Science, University of Lausanne, CH-1015, Lausanne, Switzerland. E-mail:
[email protected]
Sports Med 2010; 40 (1)
Sports Med 2010; 40 (1): 27-39 0112-1642/10/0001-0027/$49.95/0
REVIEW ARTICLE
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Glycaemic Index, Glycaemic Load and Exercise Performance John O’Reilly, Stephen H.S. Wong and Yajun Chen Department of Sports Science and Physical Education, The Chinese University of Hong Kong, Shatin, NT, Hong Kong, China
Contents Abstract. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. The Glycaemic Index (GI) of Pre-Exercise Carbohydrate Ingestion: Performance and Metabolic Responses. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.1 Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Glycaemic Effects of a Pre-Exercise Meal Combined with Sports Beverage Ingestion during Exercise 3. Effect of the GI of Recovery Meals on Subsequent Substrate Metabolism and Performance . . . . . . . 4. GI and Intermittent, Variable-Intensity Exercise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1 Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5. Glycaemic Load and Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6. Conclusions and Recommendations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Abstract
27 28 32 32 33 34 35 35 36
The concept of the glycaemic index (GI) was first introduced in the early 1980s as a method of functionally ranking carbohydrate foods based on their actual postprandial blood glucose response compared with a reference food (either glucose or white bread). Although the GI is a debatable topic among many exercise and health professionals, nutritional recommendations to improve exercise performance and enhance exercise capacity are regularly based on information related to the GI. Studies focusing on the consumption of a pre-exercise GI meal have provided evidence that a benefit exists in relation to endurance performance and substrate utilization when a low GI meal is compared with a high GI meal. However, other investigations have shown that when nutritional strategies incorporating GI are applied to multiple meals, there is no clear advantage to the athlete in terms of exercise performance and capacity. It has been suggested that carbohydrate ingestion during endurance exercise negates the effect of the consumption of pre-exercise GI meals. The glycaemic load (GL) is a relatively novel concept in the area of sports nutrition, and has not been widely investigated. Its premise is that the effect, if any, on exercise performance is determined by the overall glycaemic effect of a diet and not by the amount of carbohydrate alone. The claims for GL have been disputed by a number of sports nutrition specialists, and have gone largely unrecognized by professional and scientific bodies. Research on the effect of the GL on exercise performance and capacity is still at an early stage,
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but recent studies have shown that the concept may have some merit as far as sports nutrition is concerned. It has been suggested that the GL may be a better predictor of glycaemic responses than the GI alone.
The concept of the glycaemic index (GI) was first introduced in the early 1980s[1] as a method of functionally ranking carbohydrate foods based on their actual postprandial blood glucose response compared with a reference food (either glucose or white bread). The GI score is calculated by dividing the incremental area under the blood glucose concentration-time curve (AUC) following ingestion of a test food with 50 g of carbohydrate by an equal amount of glucose or white bread after an overnight fast.[1,2] The GI is an indication of the rate of carbohydrate digestion and is influenced by factors such as the macronutrient content of the food,[2] food particle size, cooking techniques,[3] food processing,[4] presence of fructose or lactose, form of starch, presence of antinutrients such as phytates and lectins,[5] and the training status of the individual concerned.[6] Various claims made in support of the supposed positive effects of the GI on exercise performance have not been accepted by many exercise and health professionals. Ludwig et al.,[7,8] for example, have reported that the practical relevance of the GI to energy regulation is unclear and that the clinical significance of the GI remains debatable. Similar reservations were also expressed by Febbraio et al.,[9] who noted that the effects on glycogen use and/or carbohydrate oxidation during exercise following pre-exercise high GI (HGI) carbohydrate ingestion were equivocal. Nevertheless, nutritional strategies to improve exercise performance and increase exercise capacity are regularly based on the information provided by studies on GI.[5,10-12] Until recently, the most common method of classifying carbohydrate food used the ‘simple’ or ‘complex’ categorization. This classification grouped carbohydrates according to their chemical structure. ‘Simple’ carbohydrate foods, which are deemed to be unhealthy and generally not nutrient-rich,[13] contain mono-, di- or oligosaccharides and cause rapid changes in blood glucose levels, while ‘complex’ carbohydrate foods, ª 2010 Adis Data Information BV. All rights reserved.
which are considered to be healthier and more nutritious, contain polysaccharides or starches and produce a more sustained and flatter glucose response.[14] This crude binary categorization obscures a number of important factors. Judging the effectiveness of a food in a nutritional strategy based purely on its predominant carbohydrate type is an imprecise science due to the unpredictable nature of the blood glucose response.[5] For example, many ‘complex’ carbohydrate foods (e.g. French fries) are often quite high in fat, while many ‘simple’ carbohydrate foods (e.g. fruit and yogurt) are low in fat and are good sources of protein and other vitamins. The information that the GI provides reflects the tendency of food ingested to affect postprandial glucose and insulin concentrations.[1] This can be influenced by factors such as food particle size, cooking techniques,[3] food processing,[4] presence of fructose or lactose, form of starch and presence of antinutrients such as phytates and lectins.[5] Given the deficiencies of the traditional carbohydrate food classification system and the possible merits of the GI approach, the purpose of this review is to examine recent findings in GIrelated research and to analyse their impact on nutritional strategies for exercise performance. The concept of the glycaemic load (GL) is also introduced and the relevant studies are discussed. 1. The Glycaemic Index (GI) of Pre-Exercise Carbohydrate Ingestion: Performance and Metabolic Responses The use of the GI as a method to potentially improve exercise performance has generated much scientific research over the past two decades. The majority of this research has been concerned principally with incorporating the GI as part of a preexercise nutritional strategy.[6,15-26] Despite the mixed results of these studies, which may be due to Sports Med 2010; 40 (1)
Glycaemic Index and Glycaemic Load in Exercise
contrasting methods, prescribed foods, timing of ingestion and modes of exercise, a broad consensus has emerged that certain benefits may be gained from the pre-exercise ingestion of low GI (LGI) carbohydrate food (see table I).[19-23,25-27] It is evident from the literature that an increase in fat oxidation has been shown to be the dominant result in many studies comparing the effect of LGI, HGI and moderate GI (MGI) carbohydrate ingestion.[21,23,27,29] It has also been demonstrated that fat oxidation can be maximized when an individual exercises in a fasted state.[27] Fasting, however, is not a practical option for most recreational or elite athletes, and because of its perceived advantages, the LGI diet has grown in popularity in recent years. In order to optimize the benefits of an LGI meal, subsequent exercise should occur at an intensity that is conducive to fat oxidation. Further insights on this issue were provided in a study[21] that used an exercise intensity (70%) that was not at the optimum for fat oxidation (50–64%[31]), and results showed that no difference in substrate oxidation was observed during LGI and HGI exercise trials. A study by Stevenson et al.[22] highlighted how differences in the glycaemic response to LGI and HGI trials during the postprandial period did not necessarily lead to differences in substrate oxidation during subsequent submaximal exercise. Previous studies had reported that a single LGI meal could improve glucose tolerance and therefore reduce hyperinsulinaemia at the second meal.[32-34] However, no study on this topic had investigated the response to exercise following a pre-exercise evening meal and HGI breakfast. Two previous studies[32,33] were conducted by using a single LGI carbohydrate food (lentils), while another[34] used a mixed meal comprising foods not suitable for an athlete’s diet. Stevenson et al.,[22] on the other hand, used a normal combination of foods that athletes may choose to eat, such as cereals, pasta and bread. Nonetheless, differences were observed in postprandial metabolic responses to such breakfasts, although these were still insufficient to alter substrate oxidation in subsequent exercise. It can therefore be concluded that a single LGI evening meal can improve glucose tolerance at breakfast, but not to ª 2010 Adis Data Information BV. All rights reserved.
29
the extent where metabolic responses to subsequent exercise are affected. Initially, studies on GI and exercise performance used only single foods that were ingested within 90 minutes of the exercise trials;[35-38] another used a mixed meal comprising foods not suitable for an athlete’s diet.[34] In tune with a more lifelike situation, however, Wee et al.[23] were the first to examine the effect of the GI of carbohydrate-rich meals consumed 3 hours before exercise on muscle glycogen metabolism. The HGI trial showed a 15% rise in muscle glycogen concentration during the postprandial period and a greater muscle glycogen use during exercise. No change in muscle glycogen concentration was evident postprandially in the LGI trial, but there was an increase in the rate of fat oxidation during exercise. The author suggested that such metabolic responses led to a sparing of muscle glycogen utilization, which allowed for more sustained carbohydrate availability over the course of the endurance exercise. A recent study[26] set out to investigate the effect on endurance running capacity of ingesting an LGI or HGI carbohydrate meal 3 hours prior to exercise. It was found that the subjects demonstrated a greater endurance capacity when running to exhaustion during the LGI trial than during the isocaloric, isomacronutrient HGI carbohydrate trial. In this study, mixed meals were consumed 3 hours prior to exercise, which more accurately reflects a real-life situation. The authors speculated that increased rate of fat oxidation and lower rate of glucogenolysis allowed a quicker ‘upregulation’ of fat metabolism, which supported energy expenditure for longer in the LGI trial than during the HGI trial. In a subsequent study measuring running performance over 16 km, it was found that all subjects achieved a faster performance time following the consumption of an LGI meal 2 hours prior to exercise when compared with a HGI meal.[25] Fat oxidation was also significantly higher in the LGI trial. This study also established that the GI of pre-exercise meals has no effect on hydration during exercise. Glycogen sparing, although it was not measured, was again suggested as a key reason for the performance enhancement. Sports Med 2010; 40 (1)
Study, year
Methods
30
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Table I. Summary of the main findings of pre-exercise glycaemic index (GI) studies Main findings metabolic responses
exercise performance
Wu and Williams,[26] 2006
n = 8; 2 trials (LGI, HGI). Overnight fast. . Run at 70% VO2max until exhaustion
› Fat oxidation rates during exercise after the LGI meal compared with after the HGI meal
Greater endurance capacity after LGI meal than after the ingestion of a HGI meal
Wong et al.,[25] 2008
n = 8; 2 trials (LGI, HGI). Overnight fast. Run . at 70% VO2max for 5 km followed by a 16 km performance run . n = 7; 60 min run at 65% VO2max , 3 h after ingesting a HGI breakfast and either a HGI or LGI evening meal the previous day
› Fat oxidation rates during exercise after the LGI meal compared with after the HGI meal
Faster performance time after LGI meal than after the ingestion of a HGI meal
› Plasma glucose and serum insulin concentrations following breakfast. Metabolic responses to subsequent exercise were not affected
Was not measured
› Plasma glucose and serum insulin response after HGI meal. Sparing of muscle glycogen utilization and › fat oxidation observed in the LGI trial
Was not measured
Stevenson et al.,[22] 2005
Wee et al.,[23] 2005
. n = 7; 30 min run at 71% VO2max , 3 h after consuming either HGI or LGI CHO breakfasts n = 9; 2 trials (HGI, LGI). Participants consumed breakfast and lunch, each followed by a 3 h resting and 60 min run . at 70% VO2max
› Plasma glucose and serum insulin response after HGI trial. › Fat oxidation during rest after lunch in the LGI trial. Plasma glucose was better maintained during LGI trial
NS
Wu et al.,[27] 2003
n = 9; 3 trials (HGI, LGI and FAST) each . separated by 7 d. 60 min run at 65% VO2max , 3 h after ingestion
› Fat oxidation during FAST compared with LGI and HGI. › Fat oxidation during LGI compared with HGI
Was not measured
Wong et al.,[24] 2009
n = 9; 3 trials (HGI, LGI and 0 GI) each separated by 7 d. Food consumed 2 h prior to 21 km time trial run. 6.6% CHO-electrolyte solution ingested over 2.5 km
› Fat oxidation in LGI trial compared with HGI pre-exercise, but no difference during exercise. All variables were all similar among trials
NS
Garcin et al.,[28] 2001
3 trials (HGI, LGI and water). Food ingested throughout the 3 h before a 1 h cycle . (80% VO2max )
Level of blood glucose mediates the intensity of peripheral exertion perceptions. No difference in RPE and hunger ratings for the three test foods
Was not measured
Bennard and Doucet,[16] 2006
n = 8; 4 trials (LGI before and after, HGI before and after). After an overnight fast, subjects were required to perform 400 kcal of treadmill exercise
› Fat oxidation when exercise was performed in a fasted state. No significant effect of meal GI on the amount of fat oxidized was noted
Was not measured
Backhouse et al.,[15] 2007
n = 6; 3 trials (HGI, MGI, water) at 50% . VO2max . Food ingested 3 h before exercise
No differences in substrate utilization between the two CHO trials. In the HGI and MGI trials, plasma glucose and serum insulin concentrations peaked 15 min into the postprandial period
Was not measured
Continued next page
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Stevenson et al.,[21] 2005
n = 8; 2 trials (HGI, LGI). Women ate breakfast 3 h before walking for 60 min Stevenson et al.,[30] 2009
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CHO = carbohydrate; FAST = fasting state; HGI = high GI; LGI = low GI; MGI = moderate GI; NS = no significant difference between trials; RPE = rating of perceived exertion; . VO2max = maximal oxygen uptake; › indicates increase.
Was not measured › Plasma glucose and serum insulin responses following the HGI breakfast. › Fat oxidation during exercise in LGI trial. › Satiety in the LGI trial
Was not measured n = 8; 2 trials (HGI, LGI). Women ate breakfast 3 h before performing a 60 min run . at 65% VO2max Stevenson et al.,[29] 2006
› Plasma glucose and serum insulin concentrations after HGI meal. No significant differences in substrate oxidation during postprandial period. › Fat oxidation during exercise in LGI trial
Both CHO trials were faster than placebo. More watts of power produced in final stages of CHO trials No significant difference between trials n = 9; 3 trials (LGI [honey], HGI [dextrose] and placebo). Ingested 15 g every 16 km Earnest et al.,[17] 2004
Main findings Methods Study, year
Table I. Contd
metabolic responses
exercise performance
Glycaemic Index and Glycaemic Load in Exercise
Further study is recommended to confirm this contention. Very few studies provide an indication of the effectiveness of pre-exercise MGI carbohydrate ingestion in relation to exercise performance and metabolism. As a result, the purpose of a recent study by Backhouse et al.[15] was to examine the metabolic responses of females during 1 hour of brisk walking, 3 hours after ingesting either a HGI or an MGI breakfast (consisting of a mixture of a HGI breakfast cereal and low GI carbohydrate foods). They found that the use of pre-exercise MGI food was an ineffective method of increasing fat oxidation during exercise. The results suggested that although the addition of LGI carbohydrate foods to a HGI breakfast cereal slightly reduced the overall GI of the meal, the metabolic response to exercise was similar to that following a breakfast consisting entirely of HGI foods. A slight difference in metabolic responses was noticed more recently in a study comparing the effect of MGI raisins and a HGI sports gel prior to a 45-minute cycle at 70% . VO2max (maximal oxygen uptake) followed by a 15-minute performance trial.[39] Although free fatty acid (FFA) concentrations were found to be higher in the MGI trial, no time differences in the performance trials were detected. While the exercise bout may have been slightly short to highlight an effect on performance, this study failed to promote MGI carbohydrate ingestion as a central element to performance enhancement. It seems from the literature that in order to observe an exercise response that is significantly different from that seen with some HGI foods, the GI of the comparison food needs to be sufficiently low. To date, no MGI food has satisfied this criterion. It is therefore unsurprising that pre-exercise MGI ingestion has not featured prominently in any GI-related nutritional recommendations. Mixed results have been reported regarding the difference between males and females in relative contribution from carbohydrate and fat to oxidative metabolism during exercise. Some studies have stated that gender differences exist,[40-42] while other studies have claimed that no significant differences can be found in the total amount of fat and carbohydrate oxidized, stating only that Sports Med 2010; 40 (1)
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different sources of lipids are used.[43,44] Stevenson and colleagues[29,30] added to the body of knowledge on this topic when they examined the effects of pre-exercise mixed meals providing HGI or LGI carbohydrate on substrate utilization during rest and exercise in women. Fat oxidation was shown to be greater in the LGI trial during subsequent exercise. The findings of this female-only study are consistent with those of similar studies on male subjects, which observed a higher fat oxidation rate during exercise after an LGI pre-exercise meal.[23,26,27,45,46] 1.1 Summary
Recent studies focusing on the consumption of a pre-exercise GI meal have highlighted the fact that a potential benefit exists in relation to endurance performance and substrate utilization when an LGI meal is compared with a HGI meal.[21-23,25-27] The primary benefit of preexercise LGI carbohydrate ingestion is that the resultant decrease in postprandial hyperglycaemia and hyperinsulinaemia causes an increase in FFA oxidation and possibly better maintenance of plasma glucose concentrations, leading to a more sustained carbohydrate availability during exercise. By contrast, some recent studies have shown that when nutritional strategies incorporating GI are applied to multiple meals, there is no clear advantage to the athlete in terms of exercise performance and capacity.[15,21,22] However, as previously mentioned, a number of limiting factors were involved in these particular studies and further research is required to investigate this topic in greater depth. Research also supports the claim that pre-exercise GI ingestion has a similar effect on females to that on males.[15,29] 2. Glycaemic Effects of a Pre-Exercise Meal Combined with Sports Beverage Ingestion during Exercise Various position papers by professional organizations[47,48] have recommended that in order to maximize performance in endurance events lasting ‡1 hours, carbohydrate solution should be ª 2010 Adis Data Information BV. All rights reserved.
ingested during exercise. Burke et al.[49] indicated that the GI of a pre-exercise meal has little impact on cycling performance once a carbohydrate drink is ingested during exercise. Until recently, however, little was known about the GI effect of ingesting a carbohydrate-electrolyte solution during running following the pre-exercise consumption of a meal with either a high or a low GI. In 2009, Wong et al.[24] conducted a study in which participants completed three 21 km performance runs, each separated by at least 7 days, following the ingestion of pre-exercise meals of HGI, LGI and a fat-free, sugar-free, low-calorie, zero GI jelly, respectively. During each trial, 2 mL/kg body mass of 6.6% carbohydrate-electrolyte solution was consumed immediately prior to and every 2.5 km during exercise. Despite differences between the groups in pre-exercise blood glucose, serum insulin and serum FFA concentrations, no significant difference was observed among the groups in the time taken to complete the 21 km run. Running speed, blood lactate, serum cortisol, heart rate, respiratory exchange ratio and other perceptual variables were similar across all three trials. These results suggested that when large amounts of carbohydrate-electrolyte solution were consumed during the endurance run, the typical metabolic responses seen with LGI pre-exercise ingestion were overridden during exercise to the extent that performance and substrate utilization were comparable, even to those in a control trial. A similar conclusion was drawn more recently, when comparing the effect of high and low GI ingestion pre-exercise on cytokine response and run performance.[50] It was again found that when a carbohydrate solution is consumed during exercise, the GI of the pre-exercise meal is irrelevant in relation to exercise performance. Other studies have also shown that an improvement in performance can occur when pre-exercise feeding is followed by continued carbohydrate feeding during exercise.[21,51] These findings therefore call into question the value of incorporating the GI into pre-exercise nutritional strategies, as its effect seems to be negated once carbohydrate is ingested during exercise. Since several previous studies concerning the GI effect of pre-exercise Sports Med 2010; 40 (1)
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carbohydrate ingestion focused particularly on endurance events,[9,17,21-24,26-28,35,52] it may be necessary to investigate further whether a compromise of pre-exercise and during-exercise carbohydrate ingestion can be reached that will positively influence glycaemic responses and enhance exercise performance. Carbohydrate ingestion during exercise was further investigated in a study examining the effect of LGI and HGI carbohydrate feedings during a simulated 64 km cycling time trial.[17] The time trial was performed by three groups of cyclists who were given pre-trial LGI, HGI and placebo meals, respectively. The cyclists also ingested carbohydrate 15 g every 16 km during the trial. Improvements in time and power output over the last 16 km of the 64 km simulated time trial were recorded, but there was no difference in the time taken by the different groups of cyclists to complete the time trial. These results indicate that the type of GI consumed during exercise has no bearing on performance outcome, and that the presence of exogenous carbohydrate was the primary reason for an improvement in performance time. Further study is needed to clarify this issue.
3. Effect of the GI of Recovery Meals on Subsequent Substrate Metabolism and Performance A number of studies have reported that the GI can play a significant role in exercise recovery.[53-56] Carbohydrate ingestion has repeatedly been shown to increase post-exercise glycogen repletion.[57,58] The amount and timing of postexercise carbohydrate ingestion have been widely examined, and standard guidelines have been produced.[59,60] The recommended type of carbohydrate to be ingested, however, is still a matter of debate. In relation to resistance exercise, standard nutritional guidelines recommend ingesting a combination of carbohydrate and protein to maximize recovery.[61] In a recent investigation, however, it was found that when combined with protein, the GI of carbohydrate consumed following resistance exercise had no ª 2010 Adis Data Information BV. All rights reserved.
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bearing on the repletion of insulin levels in the first 2 hours of recovery.[62] It has been reported in one study that in the first 6 hours following endurance exercise, muscle glycogen concentration was increased following the ingestion of HGI carbohydrate.[63] After 20 hours of post-exercise recovery, however, no differences existed in muscle glycogen storage between LGI and HGI diets. This suggests that a HGI diet may be more beneficial for increasing muscle glycogen stores if recovery time between exercise sessions is 6 hours or less. However, little information was provided regarding the description of the foods consumed, with the terms ‘HGI’ and ‘simple carbohydrate’ being used interchangeably. The results infer that the type of carbohydrate ingested seems to have less importance when there is a longer recovery time. Another study contradicted these claims by reporting that increased post-exercise muscle glycogen synthesis was still evident 24 hours following the consumption of a HGI carbohydrate meal in comparison with an isocaloric LGI meal.[64] The authors of this study, however, suggested that the decreased glycogen concentration in the LGI trial may be due to other factors such as the malabsorption of carbohydrate. There is also a possibility that the differences in muscle glycogen concentrations observed could have been due to the meal consumed 3 hours before the muscle biopsy samples were collected and not due to the effect of the meals in the preceding 20 hours. There is more recent evidence to suggest that the high insulin concentrations following a HGI meal later in the recovery period could facilitate increased muscle glycogen resynthesis compared with an LGI meal.[55] Therefore, the GI of the carbohydrate consumed during the immediate postexercise period might not be as important so long as a sufficient amount of carbohydrate is ingested by the athlete. In this particular study, eight trained male athletes.undertook two trials, i.e. a 90-minute run at 70% VO2max , where meals (either HGI or LGI isocaloric recovery meals) were provided 30 minutes (breakfast) and 2 hours (lunch) following cessation of exercise. The results showed that plasma glucose responses to both meals were similar immediately post-exercise, but serum Sports Med 2010; 40 (1)
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insulin concentrations were greater in the HGI trial following the second meal later in the recovery period. To shed further light on this issue, an investigation measuring muscle glycogen levels at regular time-points post-exercise following the ingestion of a high and low GI meal is recommended. This topic was further developed when a study was carried out examining the effects of the GI of post-exercise carbohydrate intake on endurance capacity the following day.[54] High and low GI trials were conducted, and the results showed that time to exhaustion was longer in the LGI trial, and that fat oxidation rates and FFA concentrations were also higher in the LGI trial. These findings are consistent with the results of some previous studies on this topic.[65,66] They indicate that although HGI carbohydrate ingestion postexercise will favour glycogen resynthesis, athletes should also be aware that LGI carbohydrate consumption can lead to enhanced endurance performance and should be considered when subsequent exercise occurs within 24 hours. These claims were substantiated by a recent investigation comparing HGI and LGI carbohydrate consumed following a 90-minute endurance cycle exercise and the effect on lipid oxidation during a similar exercise the following day.[67,68] The study reported an increase in the availability of non-esterified fatty acids and a decreased dependence on intramuscular lipid as a fuel source in the LGI (GI = 35) trial compared with the HGI (GI = 73) trial. It was speculated that this could lead to a positive effect on endurance performance. Further study is needed to confirm if glycogen sparing occurred in the LGI trial during subsequent exercise, as is suggested by the increase in fatty acid oxidation. In contrast to most other GI studies, where comparisons were drawn between the performance or metabolic effect of HGI and LGI ingestion, Siu et al.[56] analysed the effect of different feeding patterns of a HGI meal during short-term recovery on subsequent endurance capacity to determine whether more sustained elevations of blood glucose and insulin could influence the exercise performance that may have been caused by a greater stimulus for glycogen resynthesis in a short post-exercise recovery period.[69-71] The study ª 2010 Adis Data Information BV. All rights reserved.
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conditions had the advantage of being quite realistic, as athletes generally do not wish to consume a large meal shortly after performing prolonged strenuous exercise. In this particular study, eight men exercised on a treadmill before and after consuming a HGI meal by either ‘gorging’ in a single bolus post-exercise or ‘nibbling’ small portions during the 3 hours post-exercise. The results demonstrated that a greater utilization of fat oxidation occurs when food is ingested in a single bolus during short-term recovery. They also suggest that when smaller amounts of food are ingested over a longer period of time post-exercise (‘nibbling’), there is a greater reliance on carbohydrate oxidation during subsequent exercise bouts. Exercise performance was similar between the two trials even though the ‘nibbling’ intake pattern has been shown to result in greater muscle glycogen resynthesis during the first hour of post-exercise recovery in another study.[58] Overall, very little is known about the role played by the GI in post-exercise recovery. Further studies are required to investigate the purported benefits provided by a diet based on the GI in relation to muscle glycogen concentration and subsequent exercise performance. Until such studies provide clear evidence in support of these claims, athletes should more carefully consider the amount rather than the type of carbohydrate ingested post-exercise. 4. GI and Intermittent, Variable-Intensity Exercise While many of the studies mentioned previously concentrated on the pre- and post-exercise effect of the GI of carbohydrate ingestion on endurance exercise and time trials to exhaustion, very few focused solely on the possible influences of the GI on intermittent, variable-intensity exercise, such as that experienced in many field sports. Erith et al.[53] therefore examined the effects of HGI and LGI recovery diets on subsequent exercise capacity during intermittent high-intensity running. Seven male semiprofessional soccer players participated in two high-intensity exercise trials using the Loughborough Intermittent Shuttle Test (LIST),[72] each of which involved two runs separated by a recovery period of 22 hours. A mixed high carbohydrate Sports Med 2010; 40 (1)
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meal was ingested during recovery, which was either HGI or LGI. A previous study by Burke et al.[64] suggested that 24 hours following glycogendepleting exercise, there was an increase of 48% in muscle glycogen concentration following a HGI recovery diet as opposed to an LGI diet. Erith et al.,[53] however, found no differences between trials in time to fatigue or for sprint performance and distance covered. They therefore suggested that the GI of the diet during the 22 hours of recovery did not affect sprint and endurance performance the following day. It was suggested that the fatigue in the second run of each trial may have occurred due to the inability to resynthesize phosphocreatine rapidly enough to maintain adenosine triphosphate turnover at the required level,[73,74] as well as the accumulation of metabolites such as hydrogen ions, which contributed to the inability of the working muscles to sustain energy production.[75] 4.1 Summary
Recent studies on the GI effect of post-exercise carbohydrate consumption have considerably improved our limited knowledge of this subject. They have shown that the GI of a post-exercise meal may not be a factor as long as sufficient carbohydrate is consumed.[55] There is also evidence to suggest that the high insulin concentrations resulting from a HGI recovery meal may increase glycogen repletion.[55,64] However, some studies have suggested that an LGI post-exercise meal is most beneficial if endurance exercise occurs in the next 24 hours.[54,55] Frequency of post-exercise HGI feeding has not been found to affect subsequent performance, although a large single bolus of carbohydrate ingestion post-exercise will increase FFA oxidation in subsequent exercise more markedly than many smaller feedings spread over a larger period of time.[56] The GI of a post-exercise meal does not appear to have any impact on subsequent highintensity exercise, but this is an under-researched area that requires future investigation.[53] 5. Glycaemic Load and Performance The GL is a relatively new concept that has not been widely investigated in sports nutrition. It ª 2010 Adis Data Information BV. All rights reserved.
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was first proposed as a measure that incorporates both the quantity and quality of the dietary carbohydrate consumed,[76] and is derived by multiplying the amount of available carbohydrate consumed in the diet by its GI value. GL was initially applied in a more clinical setting where it was identified as a key variable in determining in which risk category for diabetes mellitus patients would be placed.[77] The GL concept has since been incorporated into exercise science and its premise is that the effect, if any, on exercise performance is determined by the overall glycaemic effect of a diet and not by the amount of carbohydrate alone. Research has shown that the amount of carbohydrate ingested displays a similar amount of variability in glycaemic response to the GI, and that together they account for ~90% of total variability.[78] It has recently been suggested that GL would be a much better predictor of glycaemic responses than carbohydrate amount/percentage or GI alone.[79] This contention has been strengthened by a recent study by Brand-Miller et al.,[80] which examined the validity of the GL as an indicator of the glucose response and insulin demand induced by a serving of food. In this study, ten lean subjects consumed ten different foods, each with the same GL as a slice of white bread. Each food except one (lentils) produced the same incremental AUC as that of white bread, and stepwise increases in GL produced predictable stepwise increases in glucose AUC. The authors therefore concluded a more accurate result would be obtained if GI and carbohydrate content were both taken into account in estimating postprandial glycaemia and insulin demand. The claims for GL have been disputed by a number of researchers, and have gone largely unrecognized by professional and scientific bodies. It is therefore unsurprising that the effect of altering the GI and GL of a pre-exercise meal on metabolism and physiological responses during exercise remains largely unclear. The first study to directly determine the role of the GL on preexercise metabolism and subsequent endurance exercise performance was conducted only recently.[81] The study by Chen et al.[82] was undertaken to reinforce previous claims that use of the GL can improve the reliability of predicting Sports Med 2010; 40 (1)
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the response of a given diet,[76] and to test the contention of Lambert et al.[83] that endurance capacity increased in trained athletes on a highfat diet. Three trials took place, with athletes ingesting three isocaloric meals, each with a different combination of GI and GL. These meals consisted of high GI-high GL (HH), low GI-low GL (LL) and high GI-low GL (HL). Both the HH and LL meals were high in carbohydrate, while the HL meal was low in carbohydrate. GI/GL was altered by changing either the GI or the amount of carbohydrate by replacing carbohydrate with fat. Meals were consumed 2 hours before a preloaded 1-hour run and 10 km time trial measuring metabolic responses and endurance running performance. The low GL diets were found to induce smaller metabolic changes during the postprandial period and during exercise, which were characterized by lower carbohydrate oxidation and a concomitant, higher glycerol and FFA concentration. These findings are in line with those of previous GI studies.[27,84] However, there was no difference in the time taken to complete the performance run between trials. As the isocaloric meals with equal GL produced similar glycaemic, insulin and other metabolic responses during the postprandial period and during exercise, the authors suggested that its results laid an encouraging foundation for further research on the topic incorporating preexercise carbohydrate loading. The same dataset provided information on the immune responses to the exercise performance in a separate study,[82] highlighting that the HH and LL meals resulted in less perturbation of the circulating numbers of leukocytes, neutrophils and T-lymphocyte subsets, and in decreased elevation of the plasma interleukin-6 concentrations immediately after exercise and during the 2-hour recovery period compared with the HL trial. The authors suggested that these results laid an encouraging foundation for further research on the topic incorporating pre-exercise carbohydrate loading. Athletes in a following study were therefore randomly assigned to one of the three GI/GL groups similar to the previous study so that the influence of 3-day carbohydrate loading on running performance and subsequent metaª 2010 Adis Data Information BV. All rights reserved.
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bolic responses could be investigated.[85] There was no difference in exercise performance between the two high-carbohydrate trials. However, enhanced performance was more evident in the high-carbohydrate LL trial than in the lowcarbohydrate HL trial. Differences in glycaemic, insulinaemic and other metabolic responses were only apparent between the high- and low-carbohydrate trials. These findings suggest that it is the amount, rather than the nature, of the carbohydrate consumed that is the most important factor influencing subsequent metabolism and endurance run performance. 6. Conclusions and Recommendations There is a potential benefit in relation to exercise performance and substrate utilization when an LGI meal is compared with a HGI meal.[21-23,25-27] When nutritional strategies incorporating GI are applied to multiple meals, there is no clear advantage to the athletes in terms of exercise performance and capacity.[15,21,22] It has recently been shown that if a large amount of carbohydrate is ingested during exercise, as is the case in the majority of endurance events, the GI of the pre-exercise meal is irrelevant, thus leading to no significant impact on exercise performance.[24] It has also been suggested that an LGI post-exercise meal is most beneficial if endurance exercise occurs in the next 24 hours,[54,55] while there is also evidence that the GI of the postexercise meal may not be a factor as long as sufficient carbohydrate is consumed.[55] The GL has been validated as a credible concept in nutrition,[80] and may be a better predictor of glycaemic responses than the GI alone.[79] Further findings have also suggested that the amount, rather than the type, of carbohydrate is the most crucial factor influencing subsequent metabolism and endurance run performance.[85] Further research is recommended on the link between GI and intermittent, variable-intensity exercise. There is also a dearth of information in the current literature in relation to glycogen levels at regular time-points post-exercise following the ingestion of a high- and low-GI meal. Also, the GI of a post-exercise meal does not appear to Sports Med 2010; 40 (1)
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have any impact on subsequent high-intensity exercise,[53] although further research is needed in this particular area. Research on the GI and its effect on exercise performance has been contributing to exercise science literature for over a quarter of a century. Through the use of ever-evolving techniques such as magnetic resonance studies and muscle biopsies, the investigations surrounding glycaemic responses and their impact on exercise performance will create further depth to the current body of literature on the topic. Similarly, it is envisaged that greater clarity will be brought to the issue of potential health benefits related to the combination of LGI meals and physical activity. While research on the GL is still at an early stage, initial indications are that it may prove to be an important consideration in sport nutrition. Both have their practical origins in a more clinical setting and far more is known about their specific role in that field. The effect of the GI and GL on exercise performance is an issue that warrants further investigation so that more comprehensive guidelines on the topic can be developed in the future. Acknowledgements The authors would like to acknowledge the valuable contributions made by Dr Donal O’Gorman and Dr Wendy Huang during the writing of this review. They would also like to thank Dr Chris Lonsdale and Dr David Wilmshurst for a number of editorial suggestions. No sources of funding were used to assist in the preparation of this review, and the authors have no conflicts of interest that are directly relevant to the content of this review.
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plementation and the application of amino acid or protein hydrolysate mixtures. Am J Clin Nutr 2000; 72 (1): 106-11 Nicholas CW, Nuttall FE, Williams C. The Loughborough Intermittent Shuttle Test: a field test that simulates the activity pattern of soccer. J Sports Sci 2000; 18 (2): 97-104 Bogdanis GC, Nevill ME, Boobis LH, et al. Contribution of phosphocreatine and aerobic metabolism to energy supply during repeated sprint exercise. J Appl Physiol 1996; 80 (3): 876-84 Gaitanos GC, Williams C, Boobis LH, et al. Human muscle metabolism during intermittent maximal exercise. J Appl Physiol 1993; 75 (2): 712-9 Sahlin K, Tonkonogi M, Soderlund K. Energy supply and muscle fatigue in humans. Acta Physiol Scand 1998; 162 (3): 261-6 Salmeron J, Manson JE, Stampfer MJ, et al. Dietary fiber, glycemic load, and risk of non-insulin-dependent diabetes mellitus in women. JAMA 1997; 277 (6): 472-7 Hu FB, Manson JE, Stampfer MJ, et al. Diet, lifestyle, and the risk of type 2 diabetes mellitus in women. N Engl J Med 2001; 345 (11): 790-7 Wolever TM, Bolognesi C. Source and amount of carbohydrate affect postprandial glucose and insulin in normal subjects. J Nutr 1996; 126 (11): 2798-806 Scaglioni S, Stival G, Giovannini M. Dietary glycemic load, overall glycemic index, and serum insulin concentrations in healthy schoolchildren. Am J Clin Nutr 2004; 79 (2): 339-40 Brand-Miller JC, Thomas M, Swan V, et al. Physiological validation of the concept of glycemic load in lean young adults. J Nutr 2003; 133 (9): 2728-32 Chen YJ, Wong SH, Wong CK, et al. Effect of pre-exercise meals with different glycemic indices and glycemic loads on metabolic responses and endurance running performance. Int J Sport Exerc Metab 2008; 18 (3): 281-300 Chen YJ, Wong SH, Wong CK, et al. The effect of a pre-exercise carbohydrate meal on immune responses to an endurance performance run. Br J Nutr 2008; 100 (6): 1260-8 Lambert EV, Speechly DP, Dennis SC, et al. Enhanced endurance in trained cyclists during moderate intensity exercise following 2 weeks adaptation to a high fat diet. Eur J Appl Physiol Occup Physiol 1994; 69 (4): 287-93 Wee SL, Williams C, Gray S, et al. Influence of high and low glycemic index meals on endurance running capacity. Med Sci Sports Exerc 1999; 31 (3): 393-9 Chen YJ, Wong SH, Xu X, et al. Effect of CHO loading patterns on running performance. Int J Sports Med 2008; 29 (7): 598-606 Jeukendrup A, Brouns F, Wagenmakers AJ, et al. Carbohydrate-electrolyte feedings improve 1 h time trial cycling performance. Int J Sports Med 1997; 18 (2): 125-9
Correspondence: Prof. Stephen H.S. Wong, Department of Sports Science and Physical Education, The Chinese University of Hong Kong, Shatin, NT, Hong Kong. E-mail:
[email protected]
Sports Med 2010; 40 (1)
Sports Med 2010; 40 (1): 41-58 0112-1642/10/0001-0041/$49.95/0
REVIEW ARTICLE
ª 2010 Adis Data Information BV. All rights reserved.
The Influence of Estrogen on Skeletal Muscle Sex Matters Deborah L. Enns and Peter M. Tiidus Department of Kinesiology and Physical Education, Faculty of Science, Wilfrid Laurier University, Waterloo, Ontario, Canada
Contents Abstract. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. The Action of Estrogens: An Overview. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Estrogen Influence on Muscle Structure and Function . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Estrogen and Muscle Damage, Inflammation and Repair . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1 Indices of Muscle Damage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2 Inflammation and Leukocyte Infiltration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3 Muscle Repair and Regeneration: The Role of Satellite Cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5. Implications for Humans and Future Research. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Abstract
41 42 44 45 45 48 50 53 53
As women enter menopause, the concentration of estrogen and other female hormones declines. This hormonal decrease has been associated with a number of negative outcomes, including a greater incidence of injury as well as a delay in recovery from these injuries. Over the past two decades, our understanding of the protective effects of estrogen against various types of injury and disease states has grown immensely. In skeletal muscle, studies with animals have demonstrated that sex and estrogen may potentially influence muscle contractile properties and attenuate indices of post-exercise muscle damage, including the release of creatine kinase into the bloodstream and activity of the intramuscular lysosomal acid hydrolase, b-glucuronidase. Furthermore, numerous studies have revealed an estrogen-mediated attenuation of infiltration of inflammatory cells such as neutrophils and macrophages into the skeletal muscles of rats following exercise or injury. Estrogen has also been shown to play a significant role in stimulating muscle repair and regenerative processes, including the activation and proliferation of satellite cells. Although the mechanisms by which estrogen exerts its influence upon indices of skeletal muscle damage, inflammation and repair have not been fully elucidated, it is thought that estrogen may potentially exert its protective effects by: (i) acting as an antioxidant, thus limiting oxidative damage; (ii) acting as a membrane stabilizer by intercalating within membrane phospholipids; and (iii) binding to estrogen receptors, thus governing the regulation of a number of downstream genes and molecular targets. In contrast to animal studies, studies with humans have not
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as clearly delineated an effect of estrogen on muscle contractile function or on indices of post-exercise muscle damage and inflammation. These inconsistencies have been attributed to a number of factors, including age and fitness level of subjects, the type and intensity of exercise protocols, and a focus on sex differences that typically involve factors and hormones in addition to estrogen. In recent years, hormone replacement therapy (HRT) or estrogen combined with exercise have been proposed as potentially therapeutic agents for postmenopausal women, as these agents may potentially limit muscle damage and inflammation and stimulate repair in this population. While the benefits and potential health risks of long-term HRT use have been widely debated, controlled studies using short-term HRT or other estrogen agonists may provide future new and valuable insights into understanding the effects of estrogen on skeletal muscle, and greatly benefit the aging female population. Recent studies with older females have begun to demonstrate their benefits.
Over the past 15 years, several reviews have documented the potential for estrogen to mitigate post-injury disruption and inflammatory responses.[1-3] This review, while providing new insights into this discussion, further incorporates recent developments in our understanding of the potential for estrogen to positively affect muscle repair mechanisms and muscle contractility as well as its application to the aging female population. This review incorporates most of the studies related to estrogen and muscle contraction/ damage/repair mechanisms that have appeared in the literature since the last major reviews by the authors and others in 2001–3,[2-4] as well as numerous relevant earlier works. An initial PubMed search using the keywords ‘estrogen’, ‘muscle’, ‘force’, ‘strength’, ‘injury’ and ‘repair’ yielded a significant number of papers from 2000 onward, which were selected for relevance for this focused updated overview. While not intended to be exhaustive, this review does highlight the major areas of advances and controversies within this area of research. For example, while many studies with animals have tended to support the potential of estrogen to mitigate indices of muscle damage and inflammation, until recently the literature has been much less clear with regard to humans. These discrepancies, while widely debated,[5] have generally been attributed to a number of factors, including differences in age, fitness levels and exercise protocols, as well as a focus on sex-based differences rather than estroª 2010 Adis Data Information BV. All rights reserved.
gen-specific effects. As sex differences are likely complicated by factors other than estrogen alone, the most effective experimental models for teasing out estrogenic effects are also included in this review. A summary of some of the suggested effects of estrogen on muscle function, as well as markers of post-injury damage, inflammation and repair, are included in table I. In addition, emerging insights into potential mechanisms of estrogenic influence on muscle repair, particularly relating to the activation and proliferation of satellite cells, are highlighted. Finally, a discussion of the potential application of hormone replacement therapy (HRT) and/or estrogen as therapeutic agents to the aging female population round out this updated review. 1. The Action of Estrogens: An Overview The term ‘estrogens’ describes a group of 18-carbon corticosteroid molecules secreted primarily by the ovaries in females and, to a lesser extent, by the testes in males.[3] Estrogens are primarily involved in the development and maintenance of normal sexual and reproductive function,[79] although they have also been shown to exert a wide range of biological effects in many physiological systems, including the cardiovascular, musculoskeletal, immune and central nervous systems.[80] The most potent and abundant form of estrogen produced in the body is 17b-estradiol, although two other metabolites of estrogen, Sports Med 2010; 40 (1)
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43
Table I. Summary of some potential estrogen effects on skeletal muscle Indicator
Effect measured
References sex/estrogen/ HRT effects
mixed effects
no sex/estrogen/ HRT effects
Muscle growth, size and mass
Rodents[6] Humans[7-12] Myoblasts[13]
Twitch characteristics
Rodents[20-22]
Tetanic force development, strength, endurance, fatigability or performance
Rodents[23-26] Humans[10,14,27-38]
Strength loss
Rodents[26]
Rodents[25,41] Humans[5,44-46,55-57]
Blood creatine kinase activity
Rodents[58-63] Humans[55,64-66]
Rodents [67] Humans[5,55-57]
Histology
Rodents[68,69]
Rodents[26] Humans[55]
Lysosomal enzyme activity
Rodents[69-72]
Post-damage muscle inflammation
Muscle leukocyte infiltration (neutrophils and macrophages)
Rodents[63,67,68,71-75] Humans[55]
Post-damage muscle repair
Satellite cells, muscle regeneration
Rodents[70,71,73,76-77] Humans[78]
Muscle structure and function
Muscle damage indicators
Humans[14-19]
Rodents[39] Humans[7,11,40]
Rodents[20,41-43] Humans[15-19,30,34,44-54]
Humans[45]
HRT = hormone replacement therapy.
estriol and estrone, are also present at lower levels, and exhibit tissue-specific effects.[81] Over the past two decades, our understanding of the protective roles of estrogen in a number of physiological systems has grown immensely. For example, estrogen has been reported to attenuate inflammation and damage, and enhance repair in skin, neural and hepatic tissues.[82-84] With respect to muscle, estrogen has been shown to exert protective effects on cardiac, smooth and skeletal muscle. For example, the incidence of cardiac disease in pre-menopausal women is lower than age-matched men, and this observation has been largely attributed to the presence of estrogen.[85] As well, several studies have reported an estrogenmediated reduction in the degree of myocardial injury following ischaemia-reperfusion injury.[86-90] With respect to skeletal muscle, most animal studies have demonstrated that female and estrogensupplemented rodents exhibit less myofibre injury and inflammation following exerciseinduced muscle injury,[2,4] while in humans these effects have not been as clearly delineated.[5] In addition, our laboratory has recently demonstrated that estrogen may also influence postª 2010 Adis Data Information BV. All rights reserved.
damage repair processes through activation and proliferation of satellite cells.[70,71,73] While the protective effects of estrogen on muscle have been well documented, the potential mechanism(s) underlying estrogenic action remain elusive. Three schools of thought are often used to explain the influence of estrogen: 1. Estrogen, due to its 18-carbon phenolic backbone and structural similarity to other potent antioxidants such as vitamin E, is thought to have a high antioxidant capacity and as such may have the ability to scavenge free radicals and stimulate the expression and activities of certain antioxidant enzymes, thus limiting oxidative damage.[91-93] 2. Due to its structural similarity to cholesterol, estrogen may have the ability to intercalate within membrane phospholipids in a similar fashion and exert a membrane-stabilizing effect.[1,94] 3. The discovery of three types of estrogen receptors (ERs) [ERa, ERb and plasma membrane ER] has led to the discovery that estrogen may govern the regulation of a number of downstream genes and molecular targets.[3,71,95] While each of these topics is addressed in individual subsections, it should be noted that Sports Med 2010; 40 (1)
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one, two or all of these processes is likely active during conditions of muscle injury. 2. Estrogen Influence on Muscle Structure and Function With respect to muscle size, estrogen has been shown to influence growth of myoblast cells in vitro,[6] and is also associated with in vivo development of muscle size in female mice.[13] In humans, however, the effects of estrogen on muscle size are not as well understood. For example, while some studies have demonstrated that estrogen or hormone replacement may attenuate or even reverse the age-related decline in lean muscle mass and size observed in postmenopausal women,[7-12] other studies have shown no effects of estradiol on muscle mass, size or cross-sectional area.[14-19] A number of studies have examined the influence of estrogen on muscle contractile properties. While some reports have clearly demonstrated a positive influence of estrogen or HRT on parameters such as twitch characteristics, tetanic force development and strength, other studies, particularly those involving humans, have been unable to demonstrate any estrogen-specific effects (table I). In animals, estrogen has been shown to affect muscle fatigue as well as twitch characteristics such as peak tension and half-relaxation time.[20-22] Reductions in skeletal muscle contractility and isometric tetanic force production have also been observed in mature, ovariectomized rodents,[23-25] although not all rodent studies have shown a positive estrogenic influence on tetanic force development.[20,41-43] While the underlying mechanisms for these potential force reductions by estrogen are still not known, some evidence is available. For example, Moran et al.[23,26] reported that the decrements in maximal tetanic force observed in ovariectomized rats were reversed with estrogen replacement. Interestingly, these authors also observed that the fraction of strong-binding myosin was greater in estrogensupplemented animals, and suggested that estrogen may influence muscle contractile properties through direct binding to myosin.[26] Estrogen may also potentially modulate force development ª 2010 Adis Data Information BV. All rights reserved.
through its effects on specific contractile proteins. For example, Kadi et al.[96] found that estrogen administration altered the expression patterns of myosin heavy chain (MHC) proteins in both fast- and slow-twitch muscles of rodents. In addition, Suzuki and Yamamuro[39] reported that the isometric twitch tension of the extensor digitorum longus muscle in rats (which primarily contains fast-twitch fibres) was lower in estrogensupplemented and ovary-intact rats compared with ovariectomized rats; however, estrogen had no effect on isometric twitch tension in the soleus, which primarily contains slow-twitch fibres. In contrast, McCormick et al.[20] observed no changes in MHC composition with estrogen replacement. While a number of human studies have examined sex differences in muscle strength and fatigability during exercise, the findings are inconsistent and therefore few conclusions can be drawn. For example, some studies have demonstrated that the skeletal muscles of women have greater muscular endurance (i.e. a longer time to fatigue) compared with men, particularly following intermittent or isometric contraction protocols of low to moderate intensity,[27-31] whereas studies using more intense protocols or dynamic exercise (i.e. mixed concentric and eccentric contractions) have reported no such differences.[30] Studies using eccentric exercise protocols, which induce a greater degree of muscle disruption, also tend to show no differences between the sexes with respect to relative strength loss and skeletal muscle fatigability,[44-46] although differences are often observed with other indices of muscle injury, as seen in section 3. As studies based on sex differences may be confounded by variables beyond the presence of estrogen, a more valid model may be to examine differences in muscle properties in pre- versus postmenopausal females or between age-matched older females with or without estrogen or hormone replacement. At the time of writing, approximately 25–30 studies and reviews were available in the literature that specifically examined differences in maximal isometric tension development, strength and/or muscle performance between males and females as well as between pre- and Sports Med 2010; 40 (1)
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postmenopausal women with or without HRT. While some studies have reported that HRT may have the potential to at least partly overcome the age-related declines in strength and increased levels of post-exercise muscle damage experienced by many women during and following menopause,[10,14,32-36] there is also a large body of evidence suggesting that HRT has little to no influence on muscle strength, performance or force development in humans.[15-19,34,47-53] Other studies have shown mixed results and demonstrated either increases in power or enhanced muscle performance with HRT, with no corresponding changes in maximal isometric tension.[7,11,40] In addition, a few studies have examined changes in muscle strength and force generation during the menstrual cycle. While some reports have noted significant increases in strength and force generation during the follicular and mid-cycle phases of the menstrual cycle (when estrogen levels are at their highest or rising),[37,38] others have reported no changes.[17,54] A very recent study compared 15 postmenopausal monozygotic twin pairs in which one twin had been using HRT for an average of approximately 7 years while the other had no history of HRT use.[11] They concluded that ‘‘long term HRT use was associated with better mobility, greater muscle power and favourable body and muscle composition among 54–62 year old women.’’[11] While another recent study which also compared postmenopausal females with or without HRT use reported that those women using HRT had significantly greater upregulation of proanabolic gene expression both at rest and following eccentric exercise.[97] Collectively, evidence concerning the effects of estrogen on muscle structure and contractile function has tended to be conflicting and depends upon a number of factors, including the species examined, study type (i.e. cross-sectional vs longitudinal), age of the subjects, types of comparisons made (e.g. pre- vs postmenopausal females, males vs females, or postmenopausal females with or without HRT), size and fibre type composition of the muscles examined, the type, duration and intensity of exercise, and the contractile properties chosen for testing. Thus, cauª 2010 Adis Data Information BV. All rights reserved.
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tion should be exercised before any definite conclusions regarding the efficacy of estrogen or HRT on muscle function can be drawn. However, some recent well-controlled studies have supported positive effects of HRT on skeletal muscle function and composition in postmenopausal females[11,97] and may now have shifted the balance of evidence toward a positive influence of estrogen and HRT on skeletal muscle.[98] 3. Estrogen and Muscle Damage, Inflammation and Repair 3.1 Indices of Muscle Damage
Unaccustomed exercise, exercise involving lengthening or eccentric contractions or myotrauma often result in muscle membrane disruption and injury to myofibres. This has been documented directly through ultrastructural analysis of muscle tissue and biopsy samples[99-101] and indirectly through indicators such as losses in muscle strength, appearance of myofibre proteins in the blood, and muscle soreness.[102] Following this type of exercise, a well-characterized series of events involving oedema, an infiltration of inflammatory cells (i.e. neutrophils and macrophages), and activation and proliferation of satellite cells takes place to repair and replenish the damaged tissue. Each of these steps is regulated by a myriad of factors released both systemically as well as from the damaged tissue.[103,104] Although many animal studies have demonstrated that estrogen and sex may significantly attenuate some indices of muscle membrane disruption and injury, including strength losses,[58-61,68-70,72] not all animal studies have found protective effects.[25,26,41,67] One of the most common markers of muscle membrane disruption is the appearance of the muscle protein creatine kinase (CK) in the bloodstream, and levels of this marker are significantly higher in male rats compared with female rats following conditions of muscle injury.[59-61] These differences have been specifically attributed to the presence of estrogen, as both male and ovariectomized Sports Med 2010; 40 (1)
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female rats supplemented with estrogen demonstrate reductions in CK activity similar to ovaryintact female rats.[58,60-63] While some human studies have shown similar trends with respect to post-injury indices of damage, strength loss and CK release,[55,64,65] many others have shown no differences between the sexes.[5,44-46,55-57] Use of blood CK levels as an indicator of postexercise muscle membrane disruption in human and intact animal studies has been shown to be problematical due to its high variability and to factors related to CK clearance rates from the blood.[105,106] For example, it has been reported that female mice and humans may clear CK from blood faster than male mice, and this could at least in part account for some of the reported sex differences in post-exercise blood CK activities.[105] However, this observation does not negate the possibility that post-exercise CK release from muscle is also attenuated by estrogen through its role as a membrane stabilizer. Indeed, an early study by Amelink et al.[61] used an isolated in vitro preparation to electrically stimulate muscles from normal male, female and ovariectomized female rats with or without prior estrogen treatment. They reported a direct inverse relationship between estrogen supplementation and in vitro CK release from the isolated muscles in all groups of animals. This and other studies by this group suggest that the membrane-stabilizing effects of estrogen may attenuate post-exercise CK release from skeletal muscle and that changes in circulating CK levels can at least indirectly and qualitatively reflect changes in exercise-induced muscle membrane disruption.[59,60] Less is known about whether estrogen and sex can specifically influence muscle structural damage. One of the first studies to explore this question was performed by Komulainen et al.,[69] who found that the hindlimb muscles of female rats exhibited significantly less myofibre structural damage and swelling compared with male rats up to 96 hours after downhill treadmill running. In addition, the muscles of male rats had significantly greater losses of sub-membrane proteins such as desmin and dystrophin compared with females. Activity of the intramuscular lysosomal enzyme, b-glucuronidase, which is ª 2010 Adis Data Information BV. All rights reserved.
Enns & Tiidus
commonly used as an indirect indicator of muscle damage, was higher post-exercise in male versus female hindlimb muscles. Our laboratory has confirmed that this protective effect is due to the presence of estrogen, as we have observed similarly attenuated post-exercise b-glucuronidase activities in red and white hindlimb muscles of ovariectomized female rats supplemented with estrogen.[70,71] Collectively, the above data suggest that early losses in sub-membrane proteins in the muscles of male and estrogen-deficient female rats following exercise-induced muscle damage may originate at the plasma membrane, and estrogen may prevent this disruption through potential membrane-stabilizing properties.[71,94] In this regard, a very recent study that examined a number of muscle and blood markers of exercise-induced muscle damage and inflammation in postmenopausal females concluded that postmenopausal women lacking estrogen replacement via HRT experienced significantly greater muscle damage following eccentric exercise and that there appeared to be a protective effect of HRT against exercise-induced muscle damage.[66] It is also possible that at least some of the reported estrogen-related differences in indicators of post-exercise muscle damage and inflammation can be attributed to differences in animal size. Ovariectomized female rats without estrogen supplementation are often larger than ovariectomized female rats that are estrogen supplemented,[70,71] possibly contributing to the differences in muscle damage reported in these groups following downhill running. For example, one study reported that large (100–200%) differences in weights of male rats may have been a factor contributing to higher indices of a specific marker of muscle damage following downhill running.[107] However, this study lacked statistical rigor and conceded that the differences between weight groups could also have been due to the large differences in rat ages, with heavier groups representing significantly older animals. Whether these much smaller weight differences in ovariectomized female animals of the same age are a factor in the repeatedly observed differences in indices of post-exercise muscle damage is not Sports Med 2010; 40 (1)
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known. However, we have previously reported that both ovary-intact female and heavier estrogen-supplemented male rats exhibited attenuated post-exercise muscle inflammation markers to a greater degree than heavier male rats who lacked estrogen supplementation.[74] As well, one study involving ischaemia reperfusion-induced injury (where rat bodyweight was not a factor) also demonstrated a post-damage attenuation effect of estrogen on muscle leukocyte infiltration.[68] As estrogen may also increase voluntary physical activity in rats,[108] it is possible that estrogen-supplemented animals may be more ‘trained’ and hence less susceptible to exercise-induced muscle damage than unsupplemented ovariectomized females. However, most of the studies demonstrating stimulatory effects of estrogen on rodent activity have used voluntary wheel running or open field observation to assess physical activity patterns.[108] It is uncertain whether relatively brief exposures to estrogen for animals confined to small cages with no access to running wheels may result in different levels of ‘training effect’ between groups. These questions should be further investigated. It is also possible that estrogen, due to its structural similarity to known antioxidants such as vitamin E, may protect muscle from damage and inflammation through a similar mechanism.[91,92] When cells are exposed to conditions of stress or injury, free radical-induced peroxidation reactions can occur, leading to membrane disruption. While in vitro studies have demonstrated that estrogen is able to substantially inhibit membrane lipid peroxidation,[62,92] there is some question as to whether the picomolar concentration of estrogen normally observed in physiological systems is high enough to exert significant antioxidant effects. Some studies have demonstrated in vivo antioxidant effects of estrogen following running exercise[109] and muscle injury,[58,68] while others have failed to find estrogen-related changes in post-exercise indices of oxidative stress.[110] Intriguingly, estrogen appears to reduce levels of antioxidants such as vitamin C and glutathione in some muscles and tissues,[110,111] thereby potentially undermining some of its antioxidant effects. ª 2010 Adis Data Information BV. All rights reserved.
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Studies examining the antioxidant effects of estrogen in humans are limited and the findings are equivocal, likely because human studies tend to examine chemical indicators of post-exercise oxidative stress in the blood (rather than muscle biopsies) and focus on sex-based differences rather than estrogen effects per se. Nevertheless, Dernbach et al.[112] found that female rowers had lower levels of an oxidative stress marker in the blood compared with males after a strenuous 4-week training programme, while Ayres et al.[113] reported that amenorrhoeic female athletes demonstrated a significantly greater potential for lipid peroxidation after an acute bout of exercise compared with eumenorrhoeic females. More recently, Kerksick et al.[57] found that females at the mid-luteal phase of their cycle had higher serum concentrations of the antioxidant enzyme superoxide dismutase (SOD) compared with males after eccentric exercise. However, Chung et al.[114] failed to observe any differences in postexercise oxidative stress markers between females who exercised at different phases of the menstrual cycle. As mentioned previously, many factors complicate the interpretation of data generated from human studies, including prior state of fitness, use of indirect rather than direct markers, and the presence of other sex hormones such as progesterone and testosterone. Future studies aimed at comparing these indices between preand postmenopausal women will hopefully yield further insights in this area. In addition to its potential role as an antioxidant, estrogen may also protect muscle from secondary damage through its influence on various regulators of muscle catabolism and apoptosis. Although relatively few studies are available in this area, Willoughby and Wilborn[115] reported that women in the midluteal phase of their cycle had decreased levels of myostatin mRNA, a regulator of skeletal muscle catabolism, 24 hours after a session of eccentric exercise, while men had increased levels. Stupka et al.[55] found that men had a greater number of skeletal muscle cells positive for the apoptotic indicator bcl-2 compared with women 48 hours after eccentric exercise, while Kerksick et al.[57] noted a significant decrease in the bax/bcl-2 ratio (an Sports Med 2010; 40 (1)
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indicator of the apoptotic state of the cell) in women versus men after a similar eccentric exercise protocol. Although more research needs to be done in this area, the current findings do support evidence of sex differences in apoptotic mechanisms following damaging exercise. Estrogen may also protect muscle from structural damage by interacting with heat shock proteins (HSPs), often referred to as molecular chaperones, which play an important role in protein assembly and maintenance of structural integrity following conditions of stress, trauma or injury. While there are many types of HSPs, each with their own expression patterns and regulatory properties, the most widely studied HSP in muscle is HSP70. Although HSP70 is constitutively expressed in skeletal muscle, its induction can be rapidly triggered by various stressors, including exercise-induced muscle damage.[109] As post-exercise expression of HSP70 in rodent skeletal muscle has been shown to differ between the sexes,[116] it has been suggested that estrogen, through its role as a potential antioxidant and/or membrane stabilizer, may protect muscle from injury and hence diminish HSP70 induction.[109] For example, Paroo et al.[109] reported that both female and estrogen-supplemented ovariectomized rats exhibited a diminished post-exercise HSP70 response. However, very recent collaborative work involving our laboratory further clarified these findings by suggesting that estrogen may in fact protect skeletal muscle from injury by augmenting basal HSP70 concentrations, as only minor further increases in muscle HSP70 expression are observed with exercise.[117] This suggestion is consistent with previous reports, which demonstrated that constitutive myocardial HSP70 expression was enhanced in the presence of estrogen, and that unlike male and ovariectomized female animals lacking estrogen replacement, exercise or training did not greatly increase myocardial HSP70 expression.[85,118] Taken together, the data suggest that some of the protective potential of estrogen on skeletal muscle may be due to its ability to upregulate basal levels of HSP70 expression. Our laboratory has also provided evidence that estrogen may protect skeletal muscle from ª 2010 Adis Data Information BV. All rights reserved.
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post-exercise damage and inflammation-related events through inhibition of calcium-activated proteases (calpains).[4,63] Calpains are a family of intracellular non-lysosomal proteases that, once activated, may further exacerbate muscle damage through their degradation of various muscle structural proteins. During exercise-induced muscle membrane disruption, calcium floods into the cell down its concentration gradient. If intracellular calcium levels are elevated for prolonged periods, activation of calpains may occur.[119,120] Since estrogen can act as a membrane stabilizer,[121] it may act to limit membrane disruption during injury and hence prevent the influx of calcium down its concentration gradient, which would in turn limit calpain activation and hence further structural damage. As well, because muscle proteins degraded by calpains may act as chemoattractants for inflammatory cells such as neutrophils,[122] estrogen may also protect muscle from further damage by inhibiting the recruitment of inflammatory leukocytes such as neutrophils into muscle.[63] 3.2 Inflammation and Leukocyte Infiltration
Leukocytes such as neutrophils and macrophages play an important role in the inflammatory response following muscle injury, and may also play a role in initiating downstream repair processes. Neutrophils are usually the first leukocytes to arrive at the site of injury, typically between 1 and 12 hours post-damage.[63,68,123] Their main function is to remove and degrade damaged tissue by generating hypochlorous acid and superoxide radicals through a series of oxidation reactions mediated by the enzymes myeloperoxidase and nicotinamide adenine dinucleotide oxidase, respectively. They also release a number of chemoattractants that serve to recruit more neutrophils to the site of injury or infection and amplify the response. While neutrophils play a beneficial role in eliminating damaged tissue, they are unable to distinguish between healthy and damaged structures, and as such may exacerbate tissue damage.[3,124] Macrophages are the other major type of leukocyte to infiltrate muscle tissue following injury. Sports Med 2010; 40 (1)
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Two major subpopulations, ED1+ and ED2+, have been shown to play important roles in the inflammatory response and may also be responsible for initiating downstream repair mechanisms. ED1+ macrophages invade tissue first, usually within 12 hours of injury, and are mainly responsible for phagocytic removal of damaged tissue and cytokine release, while ED2+ macrophages invade muscle later (24–48 hours post-injury) and are essential for activating downstream regeneration processes, including activation of satellite cells.[125-127] Over the past decade, a number of research studies aimed at exploring sex differences and, more specifically, the potential of corticosteroid hormones (particularly estrogen) to influence post-injury damage and repair processes have been performed. The protective effects of estrogen on brain, neural tissues and cardiac muscle have been well characterized,[95,128] and demonstrate the attenuating influence of estrogen on tissue damage and inflammation as well as its accentuating effect on regenerative processes. Animal studies from our laboratory[63,68,71,74,75] and others[72] have demonstrated that post-injury infiltration of leukocytes into skeletal muscle is influenced by sex and estrogen status. In an initial study, Tiidus and Bombardier[74] reported that compared with male rats, female rats had significantly attenuated neutrophil infiltration into skeletal muscles 24 hours after running exercise. When the male rats were supplemented with estrogen, they exhibited the same blunted response of post-exercise neutrophil infiltration as female rats.[74] While these earlier studies relied mainly on indirect quantification of neutrophils through myeloperoxidase activity, later studies using histochemical identification of neutrophils confirmed these findings.[68,71,73,75] Later studies from our laboratory using ovariectomized female rats, with or without estrogen replacement, confirmed that the attenuation of neutrophil infiltration into skeletal muscle was estrogen dependent.[63,68,71,75] For example, Tiidus et al.[63] found that estrogensupplemented ovariectomized female rats demonstrated significantly attenuated neutrophil infiltration into red and white skeletal muscles 1 hour post-exercise compared with unsuppleª 2010 Adis Data Information BV. All rights reserved.
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mented rats, while Stupka and Tiidus[68] noted similar findings 2 hours following hindlimb ischaemia-reperfusion injury. Relatively few studies have examined the influence of sex and estrogen on infiltration of macrophages following exercise or injury. St Pierre Schneider et al.[72] reported that macrophage infiltration was delayed in female versus male mice (peaking at 7 and 5 days, respectively) following lengthening exercise. More recently, our laboratory demonstrated that infiltration of ED1+ macrophages into rat skeletal muscles 24 hours after lengthening exercise (i.e. downhill running) was attenuated with estrogen supplementation.[71,75] Interestingly, a recent study examining damage to endothelial tissues reported that while estrogen also diminished post-damage leukocyte infiltration into endothelial cells, the presence of progesterone negated these effects.[129] This suggests that in vivo, when both progesterone and estrogen are present, estrogen may not have as great an anti-inflammatory effect on muscle as previously reported in studies using ovariectomized animals with estrogen supplementation alone. However, very recent work from our laboratory has suggested that progesterone does not alter the attenuating ability of estrogen on post-exercise leukocyte infiltration into skeletal muscle and that progesterone independently may have a small but significant ability to diminish post-exercise muscle leukocyte invasion.[75] Human studies examining the influence of estrogen on post-injury leukocyte infiltration tend to be less consistent and focus primarily on sex differences rather than estrogen replacement. While some studies have reported that females exhibit lower levels of muscle leukocyte infiltration after eccentric (i.e. lengthening) exercise compared with men,[55] others have reported no such differences.[45] These differences may be attributed in part to differences in exercise protocols and/or experimental methods; however, it is also possible that other sex hormones may exert independent effects on post-exercise leukocyte infiltration into skeletal muscle. The mechanisms by which estrogen may influence post-damage leukocyte infiltration into muscle are not yet known. Systemically, estrogen may prevent leukocyte entry from the bloodstream Sports Med 2010; 40 (1)
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into the damaged tissue by limiting the availability of endothelial adhesion molecules.[72] Estrogen has been shown to regulate leukocyte rolling and adhesion into damaged tissue by increasing the activity of endothelial nitric oxide synthase (NOS).[130,131] Nitric oxide (NO) may also play an important role in initiating muscle repair mechanisms, which is addressed in section 3.3. Similar to muscle damage, estrogen may also exert its protective influence on post-injury inflammatory processes through various estrogen hormone receptor-mediated and non-receptormediated mechanisms. While estrogen has been shown to inhibit inflammation and accelerate healing in a number of other tissues, including liver and nervous tissue through both hormone receptor- and non-receptor-mediated processes,[128,132] relatively little information is available on the mechanisms of post-injury estrogenic protection in skeletal muscle. Recent studies from our laboratory have provided compelling evidence that estrogen protects muscle from muscle injury and leukocyte infiltration primarily through non-receptor-mediated events.[68,70,71] As mentioned previously, estrogen, by intercalating within plasma membranes, can act as both an antioxidant or as a membrane stabilizer,[3,4] which may in turn limit membrane disruption and subsequent inflammation following an injury. Furthermore, we have proposed that the attenuation of neutrophil infiltration post-injury may be mediated through estrogenmediated stabilization of muscle membranes and inhibition of Ca2+-activated proteases (calpains).[63] This theory was originally based on findings from the laboratory of Belcastro,[119,122] who established a connection between calpain activity and neutrophil invasion of skeletal muscle 1–2 hours after running exercise. As protein fragments generated through the proteolytic actions of calpains may act as chemoattractants for neutrophils following exercise or injury, stabilization of membranes by estrogen may limit post-exercise membrane disruption and influx of Ca2+ into the cell, which would in turn inhibit the upregulation of calpain activity post-exercise. In a 2001 study from our laboratory,[63] we provided support for this theory by demonstrating that estrogen suppleª 2010 Adis Data Information BV. All rights reserved.
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mentation in ovariectomized female rats limited post-exercise neutrophil infiltration into muscle and simultaneously attenuated calpain activity. As mammalian skeletal muscle contains both a and b ERs,[133-135] it has been hypothesized that estrogen may exert its protective influence through one or more receptor-mediated events. Through estrogen binding, ERs regulate a number of diverse intracellular signalling pathways, including the phosphatidylinositol-3 kinase (PI3K)/protein kinase B (Akt) pathway, which stimulates protein synthesis and growth of skeletal muscle.[95,136] To date, the only study examining the receptormediated influence of estrogen on inflammatory cell infiltration into skeletal muscle is from our laboratory. In this recent work,[71] ovariectomized female rats were either exposed to estrogen supplementation, estrogen supplementation plus the ER antagonist ICI 182,780, or a sham procedure. ICI 182,780 is known as a ‘pure’ antiestrogen because it inhibits ERs with extremely high affinity and specificity and does not possess the partial agonistic properties commonly seen in nonsteroidal antiestrogens such as tamoxifen.[137] After prolonged exposure to the hormone treatments, a subset of animals ran downhill for 90 minutes on a treadmill. Hindlimb skeletal muscles were examined 1 and 3 days post-exercise for markers of damage (b-glucuronidase activity), inflammation (neutrophil and macrophage invasion) and repair (activation and proliferation of satellite cells). While estrogen treatment significantly attenuated post-exercise skeletal muscle b-glucuronidase activity and leukocyte infiltration, the ER antagonist had no influence on either of these indices. Collectively, the findings provide strong evidence that estrogenic influence on muscle injury and leukocyte invasion is primarily regulated through non-receptor-mediated mechanisms, while ERs may play a more vital role in downstream repair processes, as seen below. 3.3 Muscle Repair and Regeneration: The Role of Satellite Cells
Strenuous, unaccustomed exercise or exercise involving eccentric contractions can result in trauma or injury to myofibres. Following this Sports Med 2010; 40 (1)
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type of injury, skeletal muscle fibres undergo a period of regeneration to repair and replenish the damaged tissue. Chemotactic signals, including cytokines and growth factors, are generated by the injured tissue, which activates the inflammatory response, and attract leukocytes to the site of injury. This cascade of events also leads to the activation and proliferation of satellite cells, which is a pivotal event in muscle repair and regeneration.[138] Satellite cells are small, mononucleated cells that reside between the basal lamina and sarcolemma of muscle fibres.[139] While normally quiescent in adult skeletal muscle, in response to myofibre injury[140,141] or overload[142] they re-enter the cell cycle, where they proliferate and differentiate to provide muscle-specific proteins needed for skeletal muscle growth and regeneration.[143] Satellite activation and proliferation are regulated by a myriad of factors released from both the damaged tissue as well as from the leukocytes that are recruited to the site of injury.[104,144] As many of these factors are in turn influenced by circulating levels of estrogen,[68,89,145] we have hypothesized that estrogen may play an important role in satellite cell activation, and hence muscle repair. While the influence of estrogen on muscle damage and inflammatory processes has been relatively well characterized, much less is known about the potential for estrogen to stimulate muscle regenerative processes such as satellite cell activation and proliferation. McClung et al.[76] reported that regeneration and regrowth of rat skeletal muscle following a period of muscle atrophy induced by hindlimb suspension is dependent upon estrogen status. In addition, sex differences in satellite cell activation and proliferation have been observed in both human and animal studies.[77,78] For example, Roth et al.[78] reported that women exhibited a greater increase in the number of satellite cells in the vastus lateralis muscle than men after 9 weeks of resistance training. In animals, a study by Salimena et al.[77] involving mdx mice (which have a dysfunctional sarcolemma and undergo repeated cycles of damage and repair) noted that the skeletal muscles of female mice had less damage and ª 2010 Adis Data Information BV. All rights reserved.
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a greater number of myofibres staining positively for satellite cells compared with male mice. Our laboratory recently performed several studies aimed at examining the influence of estrogen on satellite cell populations following exercise-induced muscle injury.[70,71,73,146] In a preliminary study,[73] we observed that the skeletal muscles of estrogen-supplemented male rats had increased numbers of satellite cells 72 hours after a session of downhill running. We next attempted to determine which stages of the satellite cell cycle were influenced by estrogen by examining histochemical changes in numbers of total (Pax7-positive), activated (MyoD-positive) and proliferating (BrdU-incorporated) satellite cells following a similar exercise protocol. In this follow-up study,[70] ovariectomized female rats were either supplemented with estrogen or given a sham procedure. We observed post-exercise increases in the number of skeletal muscle fibres staining positively for all three satellite cell markers; moreover, the increases in all three of these markers were significantly augmented with estrogen. Taken together, the results suggest that (i) sex-mediated differences in muscle fibre regeneration and satellite cell numbers may be directly attributed to estrogenic influence, and (ii) estrogen may exert its influence on postexercise muscle satellite cell populations through events upstream of satellite cell activation. Although the mechanisms by which estrogen may augment post-exercise satellite cell numbers and potentially influence other muscle repair processes are as yet unknown, it is likely that, as with muscle injury, various receptor- and nonreceptor-mediated roles for estrogen also exist with muscle repair. Our recent study employing the ER antagonist ICI 182,870 provides compelling evidence that ERs play an important role in influencing muscle repair processes through augmentation of satellite cell activation and proliferation.[71] As shown in figure 1, blocking ERs completely abolished both exercise- and estrogen-mediated increases in all three satellite cell populations.[71] While the finding that the ER antagonist decreased post-exercise satellite cell populations to levels below the sham condition was unexpected, it was not surprising given that Sports Med 2010; 40 (1)
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Sham Estrogen Estrogen + ICI 182,780 a 6
Pax7 expression (% positive fibres)
5 *
4
*,** *,**
3
* ***
***
2 1 0 Control
24 h
72 h
b 6
MyoD expression (% positive fibres)
5 4 * 3
*,**
*
* 2
***
***
1 0 Control
24 h
72 h
c 6
BrdU incorporation (% positive fibres)
5 4 3
*,**
*
*
*,** 2
***
***
1 0 Control
24 h
72 h
Fig. 1. Effects of estrogen supplementation and ICI 182,780 administration on numbers of fibres positive for (a) Pax7 (paired box homeotic gene 7), (b) MyoD (myogenic differentiation factor D), and (c) BrdU (5-bromo-20 -deoxyuridine) satellite cell markers in rat soleus muscle 24 and 72 h following downhill running. Values are means – SEM. (reproduced from Enns et al.,[71] with permission of the authors). * p < 0.05 compared with control group, ** p < 0.05 compared with treatment-matched estrogen group, *** p < 0.05 compared with treatment-matched sham and estrogen groups.
ERs are expressed in many different organs of the body[80] and were also likely inhibited by the antagonist. This systemic inhibition of ERs may ª 2010 Adis Data Information BV. All rights reserved.
have also led to additional protection of skeletal muscle from injury by estrogen via other receptorand non-receptor-mediated mechanisms, as discussed below. We recently repeated this study, this time using an ER-a-specific agonist, which lacked other estrogenic properties and demonstrated that it is specifically through the ER-a that estrogen effect on satellite cells is manifested.[146] A number of downstream signalling pathways and targets of ER binding exist that could potentially be responsible for the upregulation of post-exercise satellite cell populations observed in the presence of estrogen. For example, the PI3K/Akt pathway has been shown to stimulate growth and protein synthesis through binding of estrogen to ERs.[95,136] In addition, 17b-estradiol is involved in the ER-mediated induction of the immediate early genes c-fos and egr-1 in myoblasts, which promotes cell growth.[6] As these pathways are essential for the growth and repair of myofibres, there appears to be support for a role of estrogen in this process. NO may also be a potential downstream effector of estrogenic influence during conditions of muscle injury.[130,131] NOS activity and NO levels are enhanced with estrogen in a number of tissues, and through a combination of receptor- and/ or non-receptor-mediated events may influence muscle damage and repair.[89,147] In skeletal muscle, inhibition of NOS with the antagonist N-nitro, L-arginine methyl ester prior to muscle injury prevents satellite cell activation.[148] In addition, the release and localization of hepatocyte growth factor, which regulates satellite cell activation,[149] is an NO-dependent process during conditions of muscle injury.[150] The question of whether estrogen influences post-exercise skeletal muscle damage and repair mechanisms through NO-mediated signalling is an intriguing one and merits further study. It is also possible that estrogen may influence muscle repair through its effects on specific leukocyte populations. A number of studies have postulated that leukocytes, and in particular ED2+ macrophages, may be important promoters of satellite cell activation and proliferation.[72,127,151,152] In vitro studies have demonstrated that macrophages added to myoblast Sports Med 2010; 40 (1)
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cultures increase satellite cell proliferation and enhance myotube formation.[127,152] In addition, Tidball and Wehling-Henricks[151] reported that depletion of macrophages in vivo following a modified loading protocol (hindlimb suspensioninduced muscle atrophy followed by reloading) impaired myofibre regeneration and satellite cell activation. New evidence has revealed that estrogen may also influence macrophage-mediated muscle repair through receptor-mediated mechanisms. ERs have been identified on murine and rat macrophages[153,154] and appear to have potent regulatory effects on macrophage function.[155] For example, a recent study by Calippe et al.[156] demonstrated that chronic administration of estrogen to ovariectomized mice markedly increased the expression of interleukin-6 and NOS, which are known satellite cell activators,[104,148] through ERa-mediated events. These data provide new and compelling evidence that estrogen may accentuate post-exercise muscle satellite cell activation and proliferation even while it attenuates muscle macrophage infiltration.[71] 4. Conclusion Studies with animals have provided some evidence that estrogen and sex may influence muscle membrane stability and limit exercise-induced muscle damage. Furthermore, estrogen appears to exert significant influence on post-damage leukocyte infiltration into skeletal muscle and may promote downstream repair processes through activation and proliferation of satellite cells as well as through leukocyte-mediated events. Although the mechanisms of estrogenic influence on skeletal muscle during conditions of muscle injury and repair have not been fully characterized, membrane stabilization, antioxidant activities and receptor-mediated processes likely play an important role. In partial contrast to animal studies, the influence of sex and estrogen on indices of muscle damage and repair has not been as clearly delineated in humans.[56] These inconsistencies have been attributed to a number of factors, including age of subjects, pre-study level of fitness, type and ª 2010 Adis Data Information BV. All rights reserved.
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intensity of exercise protocol, and a focus on sexbased differences rather than estrogen-specific effects. However, despite these inconsistencies, a limited body of evidence exists to support the contention that estrogen may influence skeletal muscle contractile properties as well as mitigate post-injury leukocyte infiltration and repair in humans.
5. Implications for Humans and Future Research The study of estrogenic influence on muscle function, damage, inflammation and repair is particularly relevant to the postmenopausal female population, as females tend to experience greater strength declines, decreased functional capacity, impairments in muscle repair and increased rates of sarcopenia with age than their male counterparts.[7,8] As studies with animals have demonstrated that estrogen reduces muscle atrophy[157,158] and accelerates recovery from experimentally induced atrophic conditions,[76,136] it is reasonable to speculate that estrogen or HRT may have similar beneficial effects on preserving muscle size, strength and injury protection in humans. Indeed, while some studies utilizing different therapeutic strategies such as strength training and/or HRT to limit postmenopausal losses in strength and muscle mass and accelerate post-damage muscle repair with this population have proven encouraging, other studies have shown no effects of estrogen or HRT on muscle size or function in postmenopausal women (table I). Interestingly, strength training has been shown to significantly increase satellite cell numbers in both younger and older individuals, with the biggest increases seen in older women;[78] thus, it is possible that HRT, combined with exercise, may be the most beneficial method for preserving muscle mass and strength in older women.[33,159] Several recent studies that found positive effects of HRT use in postmenopausal women on muscle mass, function, protection from exercise-induced damage and induction of proanabolic environment have further strengthened the case for positive estrogenic effects on skeletal muscle of older Sports Med 2010; 40 (1)
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women.[11,97,98] Future studies using postmenopausal women exposed to estrogen replacement, either with or without specific exercise regimens, may help us better determine the potential effects of estrogen and HRT, if any, in this population. Unfortunately, a significant drawback to HRT in older females, despite its potential to diminish muscle damage and speed repair, is the increased risk of cancer and other diseases associated with prolonged postmenopausal exposure to estrogen replacement.[160,161] Further research involving other pharmacological agents that mimic estrogenic effects and/or activate ERs[162] without inducing carcinogenic or other undesirable effects may be an important new avenue to influence the health and musculoskeletal functional abilities of aging females. Thus, increasing our understanding of the mechanisms by which estrogen may exert its protective effects and designing effective counter-measures to preserve the strength and functional abilities of older adults will greatly benefit this population.
8.
9.
10.
11.
12.
13.
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15.
Acknowledgements No sources of funding were used to assist in the preparation of this review. The authors have no conflicts of interest that are directly relevant to the content of this review.
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41. Sotiriadou S, Kyparos A, Albani M, et al. Soleus muscle force following downhill running in ovariectomized rats treated with estrogen. Appl Physiol Nutr Metab 2006; 31: 449-59 42. Tiidus PM, Bestic NM, Tupling R. Estrogen and gender do not affect fatigue resistance of extensor digitorum longus muscle in rats. Physiol Res 1999; 48: 209-13 43. Hubal MJ, Ingalls CP, Allen MR, et al. Effects of eccentric exercise training on cortical bone and muscle strength in the estrogen-deficient mouse. J Appl Physiol 2005; 98: 1674-81 44. Hubal MJ, Rubinstein SR, Clarkson PM. Muscle function in men and women during maximal eccentric exercise. J Strength Cond Res 2008; 22: 1332-8 45. MacIntyre DL, Reid WD, Lyster DM, et al. Different effects of strenuous eccentric exercise on the accumulation of neutrophils in muscle in women and men. Eur J Appl Physiol 2000; 81: 47-53 46. Rinard J, Clarkson PM, Smith LL, et al. Response of males and females to high-force eccentric exercise. J Sports Sci 2000; 18: 229-36 47. Seeley DG, Cauley JA, Grady D, et al. Is postmenopausal estrogen therapy associated with neuromuscular function or falling in elderly women? Study of the Osteoporotic Fractures Research Group. Arch Intern Med 1995; 155: 293-9 48. Uusi-Rasi K, Beck TJ, Sievanen H, et al. Associations of hormone replacement therapy with bone structure and physical performance among postmenopausal women. Bone 2003; 32: 704-10 49. Ribom EL, Piehl-Aulin K, Ljunghall S, et al. Six months of hormone replacement therapy does not influence muscle strength in postmenopausal women. Maturitas 2002; 42: 225-31 50. Kent-Braun JA, Ng AV. Specific strength and voluntary muscle activation in young and elderly women and men. J Appl Physiol 1999; 87: 22-9 51. Armstrong AL, Oborne J, Coupland CA, et al. Effects of hormone replacement therapy on muscle performance and balance in post-menopausal women. Clin Sci (Lond) 1996; 91: 685-90 52. Preisinger E, Alacamlioglu Y, Saradeth T, et al. Forearm bone density and grip strength in women after menopause, with and without estrogen replacement therapy. Maturitas 1995; 21: 57-63 53. Harman SM, Blackman MR. The effects of growth hormone and sex steroid on lean body mass, fat mass, muscle strength, cardiovascular endurance and adverse events in healthy elderly women and men. Horm Res 2003; 60: 121-4 54. Elliott KJ, Cable NT, Reilly T, et al. Effect of menstrual cycle phase on the concentration of bioavailable 17-beta oestradiol and testosterone and muscle strength. Clin Sci (Lond) 2003; 105: 663-9 55. Stupka N, Lowther S, Chorneyko K, et al. Gender differences in muscle inflammation after eccentric exercise. J Appl Physiol 2000; 89: 2325-32 56. Clarkson PM, Hubal MJ. Are women less susceptible to exercise-induced muscle damage? Curr Opin Clin Nutr Metab Care 2001; 4: 527-31
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75. Iqbal S, Thomas A, Bunyan K, et al. Progesterone and estrogen influence post-exercise leukocyte infiltration in ovariectomized female rats. Appl Physiol Nutr Met 2008; 33: 1207-12 76. McClung JM, Davis JM, Wilson MA, et al. Estrogen status and skeletal muscle recovery from disuse atrophy. J Appl Physiol 2006; 100: 2012-23 77. Salimena MC, Lagrota-Candido J, Quirico-Santos T. Gender dimorphism influences extracellular matrix expression and regeneration of muscular tissue in mdx dystrophic mice. Histochem Cell Biol 2004; 122: 435-44 78. Roth SM, Martel GF, Ivey FM, et al. Skeletal muscle satellite cell characteristics in young and older men and women after heavy resistance strength training. J Gerontol A Biol Sci Med Sci 2001; 56: B240-7 79. Heldring N, Pike A, Andersson S, et al. Estrogen receptors: how do they signal and what are their targets. Physiol Rev 2007; 87: 905-31 80. Katzenellenbogen BS, Montano MM, Le Goff P, et al. Antiestrogens: mechanisms and actions in target cells. J Steroid Biochem Mol Biol 1995; 53: 387-93 81. Gruber DM, Huber JC. Conjugated estrogens: the natural SERMs. Gynecol Endocrinol 1999; 13 Suppl. 6: 9-12 82. Harada H, Pavlick KP, Hines IN, et al. Selected contribution: effects of gender on reduced-size liver ischemia and reperfusion injury. J Appl Physiol 2001; 91: 2816-22 83. Sribnick EA, Ray SK, Banik NL. Estrogen as a multiactive neuroprotective agent in traumatic injuries. Neurochem Res 2004; 29: 2007-14 84. Ashcroft GS, Greenwell-Wild T, Horan MA, et al. Topical estrogen accelerates cutaneous wound healing in aged humans associated with an altered inflammatory response. Am J Pathol 1999; 155: 1137-46 85. Milne KJ, Noble EG. Response of the myocardium to exercise: sex-specific regulation of hsp70. Med Sci Sports Exerc 2008; 40: 655-63 86. Booth EA, Flint RR, Lucas KL, et al. Estrogen protects the heart from ischemia-reperfusion injury via COX-2derived PGI2. J Cardiovasc Pharmacol 2008; 52: 228-35 87. Versi E. Oestrogen and protection against myocardial ischaemia [letter]. Lancet 1993; 342: 871 88. Kolodgie FD, Farb A, Litovsky SH, et al. Myocardial protection of contractile function after global ischemia by physiologic estrogen replacement in the ovariectomized rat. J Mol Cell Cardiol 1997; 29: 2403-14 89. Node K, Kitakaze M, Kosaka H, et al. Amelioration of ischemia-and reperfusion-induced myocardial injury by 17beta-estradiol. Circulation 1997; 96: 1953-63 90. Delyani JA, Murohara T, Nossuli TO, et al. Protection from myocardial reperfusion injury by acute administration of 17 beta-estradiol. J Mol Cell Cardiol 1996; 28: 1001-8 91. Subbiah MT, Kessel B, Agrawal M, et al. Antioxidant potential of specific estrogens on lipid peroxidation. J Clin Endocrinol Metab 1993; 77: 1095-7 92. Sugioka K, Shimosegawa Y, Nakano M. Estrogens as natural antioxidants of membrane phospholipid peroxidation. FEBS Lett 1987; 210: 37-9 93. Strehlow K, Rotter S, Wassmann S, et al. Modulation of antioxidant enzyme expression and function by estrogen. Circ Res 2003; 93: 170-7
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94. Whiting KP, Restall CJ, Brain PF. Steroid hormoneinduced effects on membrane fluidity and their potential roles in non-genomic mechanisms. Life Sci 2000; 67: 743-57 95. Patten RD, Pourati I, Aronovitz MJ, et al. 17beta-estradiol reduces cardiomyocyte apoptosis in vivo and in vitro via activation of phospho-inositide-3 kinase/Akt signaling. Circ Res 2004; 95: 692-9 96. Kadi F, Karlsson C, Larsson B, et al. The effects of physical activity and estrogen treatment on rat fast and slow skeletal muscles following ovariectomy. J Muscle Res Cell Motil 2002; 23: 335-9 97. Dieli-Conwright CM, Spektor TM, Rice JC, et al. Influence of hormone replacement therapy on eccentric exercise induced myogenic gene expression in postmenopausal women. J Appl Physiol 2009; 107: 1381-8 98. Onambele-Pearson, GL. HRT affects skeletal muscle contractile characteristics: a definitive answer? J Appl Physiol 2009; 107: 4-5 99. Friden J, Sjostrom M, Ekblom B. A morphological study of delayed muscle soreness. Experientia 1981; 37: 506-7 100. Jones DA, Newham DJ, Round JM, et al. Experimental human muscle damage: morphological changes in relation to other indices of damage. J Physiol 1986; 375: 435-48 101. Newham DJ, McPhail G, Mills KR, et al. Ultrastructural changes after concentric and eccentric contractions of human muscle. J Neurol Sci 1983; 61: 109-22 102. Clarkson PM, Nosaka K, Braun B. Muscle function after exercise-induced muscle damage and rapid adaptation. Med Sci Sports Exerc 1992; 24: 512-20 103. Armstrong RB, Warren GL, Warren JA. Mechanisms of exercise-induced muscle fibre injury. Sports Med 1991; 12: 184-207 104. Vierck J, O’Reilly B, Hossner K, et al. Satellite cell regulation following myotrauma caused by resistance exercise. Cell Biol Int 2000; 24: 263-72 105. Warren GL, O’farrell L, Rogers KR, et al. CK-MM autoantibodies: prevalence, immune complexes, and effect on CK clearance. Muscle Nerve 2006; 34: 335-46 106. Hyatt JP, Clarkson PM. Creatine kinase release and clearance using MM variants following repeated bouts of eccentric exercise. Med Sci Sports Exerc 1998; 30: 1059-65 107. Kasperek GJ, Snider RD. The susceptibility to exerciseinduced muscle damage increases as rats grow larger. Experientia 1985; 41: 616-7 108. Lightfoot JT. Sex hormones’ regulation of rodent physical activity: a review. Int J Biol Sci 2008; 4: 126-32 109. Paroo Z, Dipchand ES, Noble EG. Estrogen attenuates postexercise HSP70 expression in skeletal muscle. Am J Physiol Cell Physiol 2002; 282: C245-51 110. Tiidus PM, Bombardier E, Hidiroglou N, et al. Estrogen administration, postexercise tissue oxidative stress and vitamin C status in male rats. Can J Physiol Pharmacol 1998; 76: 952-60 111. Tiidus PM, Bombardier E, Seaman C, et al. Vitamin C and vitamin E status in guinea pig tissues following estrogen administration. Nutr Res 1999; 19: 773-82 112. Dernbach AR, Sherman WM, Simonsen JC, et al. No evidence of oxidant stress during high-intensity rowing training. J Appl Physiol 1993; 74: 2140-5
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113. Ayres S, Baer J, Subbiah MT. Exercised-induced increase in lipid peroxidation parameters in amenorrheic female athletes. Fertil Steril 1998; 69: 73-7 114. Chung SC, Goldfarb AH, Jamurtas AZ, et al. Effect of exercise during the follicular and luteal phases on indices of oxidative stress in healthy women. Med Sci Sports Exerc 1999; 31: 409-13 115. Willoughby DS, Wilborn CD. Estradiol in females may negate skeletal muscle myostatin mRNA expression and serum myostatin mRNA propeptide levels after eccentric muscle contractions. J Sports Sci Med 2006; 5: 672-81 116. Paroo Z, Tiidus PM, Noble EG. Estrogen attenuates HSP 72 expression in acutely exercised male rodents. Eur J Appl Physiol Occup Physiol 1999; 80: 180-4 117. Bombardier E, Vigna C, Iqbal S, et al. Effects of ovarian sex hormones and downhill running on fibre-type-specific HSP70 expression in rat soleus. J Appl Physiol 2009; 106: 2009-15 118. Melling CW, Thorp DB, Noble EG. Regulation of myocardial heat shock protein 70 gene expression following exercise. J Mol Cell Cardiol 2004; 37: 847-55 119. Belcastro AN, Shewchuk LD, Raj DA. Exercise-induced muscle injury: a calpain hypothesis. Mol Cell Biochem 1998; 179: 135-45 120. Belcastro AN. Skeletal muscle calcium-activated neutral protease (calpain) with exercise. J Appl Physiol 1993; 74: 1381-6 121. McNulty PH, Jagasia D, Whiting JM, et al. Effect of 6-wk estrogen withdrawal or replacement on myocardial ischemic tolerance in rats. Am J Physiol Heart Circ Physiol 2000; 278: H1030-4 122. Raj DA, Booker TS, Belcastro AN. Striated muscle calcium-stimulated cysteine protease (calpain-like) activity promotes myeloperoxidase activity with exercise. Pflugers Arch 1998; 435: 804-9 123. Belcastro AN, Arthur GD, Albisser TA, et al. Heart, liver, and skeletal muscle myeloperoxidase activity during exercise. J Appl Physiol 1996; 80: 1331-5 124. McCord JM. Superoxide radical: controversies, contradictions, and paradoxes. Proc Soc Exp Biol Med 1995; 209: 112-7 125. Clarkson PM, Sayers SP. Etiology of exercise-induced muscle damage. Can J Appl Physiol 1999; 24: 234-48 126. Tidball JG. Inflammatory cell response to acute muscle injury. Med Sci Sports Exerc 1995; 27: 1022-32 127. Merly F, Lescaudron L, Rouaud T, et al. Macrophages enhance muscle satellite cell proliferation and delay their differentiation. Muscle Nerve 1999; 22: 724-32 128. Wise PM, Dubal DB, Wilson ME, et al. Neuroprotective effects of estrogen-new insights into mechanisms of action. Endocrinology 2001; 142: 969-73 129. Xing D, Miller A, Novak L, et al. Estradiol and progestins differentially modulate leukocyte infiltration after vascular injury. Circulation 2004; 109: 234-41 130. Prorock AJ, Hafezi-Moghadam A, Laubach VE, et al. Vascular protection by estrogen in ischemia-reperfusion injury requires endothelial nitric oxide synthase. Am J Physiol Heart Circ Physiol 2003; 284: H133-40 131. Simoncini T, Fornari L, Mannella P, et al. Novel nontranscriptional mechanisms for estrogen receptor signaling
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in the cardiovascular system: interaction of estrogen receptor alpha with phosphatidylinositol 3-OH kinase. Steroids 2002; 67: 935-9 Reid MB. Role of nitric oxide in skeletal muscle: synthesis, distribution and functional importance. Acta Physiol Scand 1998; 162: 401-9 Kalbe C, Mau M, Wollenhaupt K, et al. Evidence for estrogen receptor alpha and beta expression in skeletal muscle of pigs. Histochem Cell Biol 2007; 127: 95-107 Lemoine S, Granier P, Tiffoche C, et al. Effect of endurance training on oestrogen receptor alpha transcripts in rat skeletal muscle. Acta Physiol Scand 2002; 174: 283-9 Wiik A, Glenmark B, Ekman M, et al. Oestrogen receptor beta is expressed in adult human skeletal muscle both at the mRNA and protein level. Acta Physiol Scand 2003; 179: 381-7 Sitnick M, Foley AM, Brown M, et al. Ovariectomy prevents the recovery of atrophied gastrocnemius skeletal muscle mass. J Appl Physiol 2006; 100: 286-93 Wakeling AE, Dukes M, Bowler J. A potent specific pure antiestrogen with clinical potential. Cancer Res 1991; 51: 3867-73 Hawke TJ, Garry DJ. Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 2001; 91: 534-51 Mauro A. Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 1961; 9: 493-5 Hurme T, Kalimo H. Activation of myogenic precursor cells after muscle injury. Med Sci Sports Exerc 1992; 24: 197-205 Smith HK, Maxwell L, Rodgers CD, et al. Exerciseenhanced satellite cell proliferation and new myonuclear accretion in rat skeletal muscle. J Appl Physiol 2001; 90: 1407-14 Kadi F, Charifi N, Denis C, et al. The behaviour of satellite cells in response to exercise: what have we learned from human studies? Pflugers Arch 2005; 451: 319-27 Seale P, Asakura A, Rudnicki MA. The potential of muscle stem cells. Dev Cell 2001; 1: 333-42 Machida S, Booth FW. Insulin-like growth factor 1 and muscle growth: implication for satellite cell proliferation. Proc Nutr Soc 2004; 63: 337-40 Kamanga-Sollo E, Pampusch MS, Xi G, et al. IGF-I mRNA levels in bovine satellite cell cultures: effects of fusion and anabolic steroid treatment. J Cell Physiol 2004; 201: 181-9 Thomas A, Bunyan K, Tiidus PM. Oestrogen receptoralpha activation augments post-exercise myoblast proliferation. Acta Physiol 2010; 198: 81-9 Caulin-Glaser T, Garcia-Cardena G, Sarrel P, et al. 17-Beta-estradiol regulation of human endothelial cell basal nitric oxide release, independent of cytosolic Ca2+ mobilization. Circ Res 1997; 81: 885-92 Anderson JE. A role for nitric oxide in muscle repair: nitric oxide-mediated activation of muscle satellite cells. Mol Biol Cell 2000; 11: 1859-74
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149. Tatsumi R, Anderson JE, Nevoret CJ, et al. HGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells. Dev Biol 1998; 194: 114-28 150. Tatsumi R, Hattori A, Ikeuchi Y, et al. Release of hepatocyte growth factor from mechanically stretched skeletal muscle satellite cells and role of pH and nitric oxide. Mol Biol Cell 2002; 13: 2909-18 151. Tidball JG, Wehling-Henricks M. Macrophages promote muscle membrane repair and muscle fibre growth and regeneration during modified muscle loading in mice in vivo. J Physiol 2007; 578: 327-36 152. Massimino ML, Rapizzi E, Cantini M, et al. ED2+ macrophages increase selectively myoblast proliferation in muscle cultures. Biochem Biophys Res Commun 1997; 235: 754-9 153. Frazier-Jessen MR, Kovacs EJ. Estrogen modulation of JE/monocyte chemoattractant protein-1 mRNA expression in murine macrophages. J Immunol 1995; 154: 1838-45 154. Gulshan S, McCruden AB, Stimson WH. Oestrogen receptors in macrophages. Scand J Immunol 1990; 31: 691-7 155. Miller L, Hunt JS. Sex steroid hormones and macrophage function. Life Sci 1996; 59: 1-14 156. Calippe B, Douin-Echinard V, Laffargue M, et al. Chronic estradiol administration in vivo promotes the proinflammatory response of macrophages to TLR4 activation: involvement of the phosphatidylinositol 3-kinase pathway. J Immunol 2008; 180: 7980-8 157. Sugiura T, Ito N, Goto K, et al. Estrogen administration attenuates immobilization-induced skeletal muscle atrophy in male rats. J Physiol Sci 2006; 56: 393-9 158. Fisher JS, Hasser EM, Brown M. Effects of ovariectomy and hindlimb unloading on skeletal muscle. J Appl Physiol 1998; 85: 1316-21 159. Meeuwsen IB, Samson MM, Verhaar HJ. Evaluation of the applicability of HRT as a preservative of muscle strength in women. Maturitas 2000; 36: 49-61 160. Yager JD, Davidson NE. Estrogen carcinogenesis in breast cancer. N Engl J Med 2006; 354: 270-82 161. Hulley S, Furberg C, Barrett-Connor E, et al. Noncardiovascular disease outcomes during 6.8 years of hormone therapy: Heart and Estrogen/progestin Replacement Study follow-up (HERS II). JAMA 2002; 288: 58-66 162. Stauffer SR, Coletta CJ, Tedesco R, et al. Pyrazole ligands: structure-affinity/activity relationships and estrogen receptor-alpha-selective agonists. J Med Chem 2000; 43: 4934-47
Correspondence: Dr Peter M. Tiidus, Faculty of Science, Wilfrid Laurier University, Waterloo, ON, N2L 3C5, Canada. E-mail:
[email protected]
Sports Med 2010; 40 (1)
Sports Med 2010; 40 (1): 59-75 0112-1642/10/0001-0059/$49.95/0
REVIEW ARTICLE
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The Pathomechanics, Pathophysiology and Prevention of Cervical Spinal Cord and Brachial Plexus Injuries in Athletics Simon Chao, Marisa J. Pacella and Joseph S. Torg Department of Orthopaedic Surgery and Sports Medicine, Temple University School of Medicine, Philadelphia, Pennsylvania, USA
Contents Abstract. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. The Mechanism and Incidence of Cervical Spine Injuries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.1 Mechanism of Injury . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2 Methods of Data Collection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.3 Analysis of Data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Pathomechanics/Pathophysiology of Cervical Spine Cord Trauma and Guide to Management . . . . 2.1 Injuries at the C3–C4 Level . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2 The Axial Load Teardrop Fracture . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3 Spear Tackler’s Spine . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4 Cervical Cord Neurapraxia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Pathophysiology of Cervical Cord Injury as it Relates to the Principles of Cord Resuscitation and Clinical Application . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1 Clinical Correlation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. Brachial Plexus/Cervical Nerve Root Injuries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1 Mechanisms of Injury . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2 Chronic Burner Syndrome . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5. Recurrence and Return to Play . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Abstract
59 60 60 61 61 64 64 64 65 65 67 68 69 70 70 71 71
Cervical spinal cord injuries may occur with catastrophic sequelae (e.g. quadriplegia) in collision sport activities. The discovery was made that the head-down tackling technique in football straightens the spine into a position vulnerable for compression and, thus, is responsible for these incidents. This led to rule changes requiring head-up tackling, which in turn resulted in the reduction of the incidence of these injuries. However, the dramatic initial reduction in the occurrence – from 32 and 34 catastrophic injuries in 1975 and 1976, respectively, down to 12 in 1977 – has levelled off with ten and eight reported cases in 2006 and 2007, respectively. The football community has increased their efforts to prevent head-down tackling with additional rule changes. Brachial plexus injury prevention must rely on properly fitted shoulder pads and use of equipment such as ‘cowboy’ collars. Furthermore, physicians must take into consideration cervical cord neurapraxia, congenital stenosis and other risk factors in patients who wish to return to contact sports.
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Athletic traumas to the cervical spine resulting in cord injury are infrequent but potentially catastrophic events. Brachial plexus or cervical root injuries, known as ‘stingers’ or ‘burners’, occur much more frequently than spinal cord injuries but are not associated with catastrophic sequelae; however, they are a major problem because of their frequent occurrence. Recognition of the problems associated with these injuries has led to a series of field, clinical and basic research studies conducted over the past 35 years that have answered basic questions regarding the pathomechanics, pathophysiology and prevention of cervical cord injury. The purpose of this paper is to review current concepts regarding both cervical cord and brachial plexus injuries as they are applicable to athletic activity today. Our discussion of these injuries includes the effect of rule changes on the injury rates in contact sports, i.e. tackle football. The initial success in injury prevention involved rule changes to alter player technique, and it dramatically succeeded in reducing the number of catastrophic spinal cord injuries from 1976 to recent years. However, a cyclical pattern of incidences has been observed due to high player and coach turnover. Thus, there is renewed interest in the occurrence of cervical spine injuries as they relate to further altering the rules of the game and ensuring player safety. This push for change has resulted in a series of rule revisions and, most recently, a 2008 season rule to hopefully affect player safety. The clinical relevance of spinal cord injury research is 3-fold. First, identification of axial energy inputs resulting in buckling and failure of a segmented column, a previously unappreciated mechanism, has been translated into injury prevention measures. Second, clarification of both the pathomechanics and pathophysiology of cervical spine and cord trauma resulting from athletic activity has provided guidelines to assist clinical management decisions. Third, correlation of the clinical manifestations of cord trauma with deformation of in vitro axonal injury model both explains the variable response to injury and supports the case for spinal cord resuscitation. Additionally, the clinical relevance of brachial plexus and cervical root injuries known as ‘burners’ ª 2010 Adis Data Information BV. All rights reserved.
or ‘stingers’ is also discussed. There are two key mechanisms of injury: compression and traction. The resulting pain and weakness may last for only seconds in the mildest of cases or may be seasonending. This article comments on recurrence and return-to-play as well as potential risk factors. 1. The Mechanism and Incidence of Cervical Spine Injuries 1.1 Mechanism of Injury
Injuries resulting in spinal cord trauma have been associated with football, water sports, gymnastics, wrestling, rugby, trampolining and ice hockey. Traditionally, hyperflexion and hyperextension have been implicated as the primary mechanisms in cervical spine injuries based on post-injury radiograph interpretation. In 1972, Schneider[1] reported a series of cervical spine injuries occurring in tackle football that he attributed to striking of the head with a knee, acute cervical hyperextension, tackling by the face guard, forced hyperflexion and head-butting. He and others[2-23] concluded that the most serious cervical injuries in football and other sports occurred as a result of forced hyperflexion. Hyperextension has also received attention as a mechanism leading to cervical spinal cord injury.[24-29] While some authors recognized axial loading as a possible mechanism for cervical athletic injuries,[30-41] it was not generally accepted as the predominant mechanism in cervical spine injury producing cord damage prior to 1975. In the course of a contact activity, such as tackle football, the cervical spine is repeatedly exposed to potentially injurious, high-energy inputs.[42] Fortunately, most energy inputs are dissipated by controlled spinal motion through the cervical paravertebral muscles and the intervertebral discs.[43] With the neck in a neutral position, the cervical spine is actually extended due to the normal cervical lordosis. When the neck is flexed to 30 degrees, the cervical spine becomes straight. In this situation, the cervical spine assumes the physical characteristics of a segmented column, motion is precluded in response to axially Sports Med 2010; 40 (1)
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a
b
c
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d
e
Fig. 1. Biomechanically, the straightened cervical spine responds to axial loading forces like a segmented column. (a and b) Axial loading of the cervical spine first results in compressive deformation of the intervertebral disks. (c) As the energy input continues and maximum compressive deformation is reached, angular deformation and buckling occur. (d and e) The spine fails in a flexion mode, with resulting fracture, subluxation or dislocation. Compressive deformation leading to failure, with a resultant fracture, dislocation or subluxation occurs in as little as 8.4 ms (reproduced from Torg et al.,[45] with permission).
directed impacts, and the forces are directly transmitted to the spinal structures. This results in the cervical spine being compressed between the abruptly decelerated head and the force of the oncoming trunk.[44] When the maximum vertical compression is reached, the cervical spine fails and buckles in a flexion mode with fracture, subluxation or facet(s) dislocation occurring (figure 1). This observation is consistent with the accepted mechanical engineering principles of elastic instability and buckling or failure of a segmented column. Numerous biomechanical studies subsequently further supported this axial loading theory.[46-54] 1.2 Methods of Data Collection
An electronic bibliographic database search was performed to identify relevant articles for this literature review. The databases utilized include AccessMedicine, MDConsult, MEDLINE, Ovid SP and PubMed. Keyword searches were performed for phrases such as ‘cervical spine injuries’, ‘cervical neurapraxia’, ‘brachial plexus injuries’, ‘stingers’, ‘burners’ and ‘sports/athletic injuries’. A series of combination searches helped narrow down the articles to those with the greatest relevance (e.g. searching ‘cervical spine injuries’ AND ‘sports injuries’). Articles referª 2010 Adis Data Information BV. All rights reserved.
enced by authors online or articles with restricted full text online were found in hardcopy form in library archives. Rule changes for the high school, college and professional football leagues were found on their official websites. Data collected by The National Football Head and Neck Injury Registry (NFHNIR) and The National Center for Catastrophic Sports Injury Research provided additional resources on cervical spine injuries. The NFHNIR, established in 1975, collected data on over 1000 cervical spine injuries from 1971 to 1988.[45,55,56] The criteria for inclusion in the NFHNIR were injuries requiring hospitalization for more than 72 hours; those that required operations; and fractures, subluxations or dislocations resulting in neurological injury or death. Data were collected from the athlete, parent and school officials, radiographs, medical records and, when available, analysis of game films or videotapes. The National Center for Catastrophic Sports Injury Research was established in 1982 and has been publishing annual reports of cervical spine injuries since its inception. 1.3 Analysis of Data
The total number of football head and neck injuries was calculated retrospectively from 1971 Sports Med 2010; 40 (1)
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to 1975[55] and compared with the data compiled by Schneider[57] in a similar study during the period 1959–63. The results indicated both intracranial haemorrhages and deaths due to intracranial injuries had decreased by 66% and 42%, respectively, while the number of cervical spine fractures, subluxations and dislocations had increased 204%, and the number of cases of cervical quadriplegia had increased 116% (to 99 cases over 5 years, or approximately 20 cases per year). The majority of the permanent cervical quadriplegias occurring between 1971 and 1975 were determined to be due to so-called ‘spearing’ or direct compression when the player had made initial contact with the top of his helmet (figure 2). Documentation of axial loading as the responsible mechanism of injury in the production
Fig. 2. A college defensive back (dark jersey) is shown ramming an opposing ball carrier with his head, resulting in severe axial loading of his cervical spine. The defensive player suffered fractures of C4, C5 and C6 and was rendered quadriplegic (reproduced from Torg et al.,[58] with permission).
ª 2010 Adis Data Information BV. All rights reserved.
Chao et al.
of catastrophic football cervical spine injuries was obtained from stop-frame kinetic analysis of 60 game films and video tapes of actual injuries resulting in permanent quadriplegia.[45] The mechanism of injury was determined in 85% of the cases, and in all instances it was axial loading. Based on these findings, it was concluded that the improved protective capabilities of modern helmets accounted for the decrease in head injuries; however, it led to the development of playing techniques that used the top or crown of the helmet as the initial point of contact, placing the cervical spine at risk. In 1976, in response to these reports, the National Collegiate Athletic Association (NCAA) banned ‘spearing’ and tackling techniques using the helmet as the initial point of contact. The 1976 rule specified that the actions must be ‘‘deliberate’’ with an ‘‘attempt to punish an opponent,’’ done ‘‘deliberately’’ and ‘‘intentionally’’. Similar rule changes were also enacted at the high school level.[59-61] As a result of these changes, fractures, subluxations and dislocations of the cervical spine declined dramatically between 1976 and 1987 when the data were explicitly collected. In 1976, the injury rates for these conditions were 7.72/100 000 and 30.66/100 000 for high school and college athletes, respectively; they decreased to 2.31/100 000 and 10.66/100 000, respectively, by 1987. Cervical spine injuries resulting in quadriplegia also declined. In 1976, the injury rate for quadriplegia was 2.24/100 000 at the high school level and 10.66/100 000 at the college level. In 1977, 1 year after the rule changes, the injury rate for quadriplegia decreased to 1.30/100 000 and 2.66/100 000 for high school and college athletes, respectively. By 1984, the injury rates had decreased to 0.40/100 000 for high schools and 0/100 000 for colleges.[45,55,56] Boden et al.[62] reported a mean incidence for 1989–2002 as 0.52/100 000 (0.50/100 000 for high school and 0.82/100 000 for college) with the peak quadriplegia rate during the 1989–90 season. It should be noted that because of the greater number of participants in high school football programmes, more high school players suffer catastrophic Sports Med 2010; 40 (1)
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40 35
No. of injuries
30 25 20 15 10 5
1975 1976 1977 1978 1979 1980 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007
0
Year Fig. 3. The effect of the 1976 rule changes banning spearing and head impact playing techniques was a dramatic, sustained decrease in the occurrence of catastrophic cervical spine injuries (data from the National Football Head and Neck Injury Registry for 1975–1996[64] and Annual Survey of Catastrophic Football Injury 1977–2007[65]).
spinal injuries overall than individual college players, but incidence numbers also support the notion that college football players are at a greater risk for such injuries[63] (figure 3). According to these incidence rates, the 1976 rule change did diminish the occurrence of ‘spearing’ in tackle football; however, it didn’t completely eliminate it (table I). Heck[66] has shown that spearing still frequently occurs in every game. In one sample of high school games, the rule decreased the independent tackler spearing incidence from 1975 to 1990 but not the overall incidence of spearing. This suggests that some programmes are not enforcing the rules or teaching the proper tackling techniques to their young players. An estimated 21% of high school players still spear when they tackle.[67] The inclusion of the phrases ‘‘deliberately’’ and ‘‘intentionally strike a runner’’ apparently made referee reinforcement of the 1976 rule difficult and ambiguous. Both a 2005 NCAA and a 2006 National Federation of State High School Associations (NFHSA) alteration of the rule removed ‘‘deliberately’’ and ‘‘intentionally’’ from their definition of spearing but left the similarly questionable ª 2010 Adis Data Information BV. All rights reserved.
phrase ‘‘attempt to punish [an opponent].’’ Data on NCAA penalties supports the observation that this rule change did not increase referee reinforcement of the rules on spearing (figure 4). Table I. National Collegiate Athletic Association (NCAA) football rules and interpretations 1976 NCAA rule 1. Spearing is the deliberate use of the helmet in an attempt to punish an opponent 2. No player shall deliberately use his helmet to butt or ram an opponent 3. No player shall intentionally strike a runner with the crown or top of his helmet 2005 NCAA rule 1. Spearing is the use of the helmet (including the face mask) in an attempt to punish an opponent 2. No player shall use his helmet (including the face mask) to butt or ram an opponent or attempt to punish him 3. No player shall strike a runner with the crown or top of the helmet in an attempt to punish him 2008 NCAA rule 1. No player shall initiate contact and target an opponent with the crown (top) of his helmet. When in question, it is a foul 2. No player shall initiate contact and target a defenceless opponent above the shoulders. When in question, it is a foul
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2007
2006
2005
2004
2003
2002
2001
45 40 35 30 25 20 15 10 5 0 2000
No. of penalties
Spearing Butting/ramming Total
Year Fig. 4. The enforcement, or lack thereof, of the spearing rule according to penalties called during National Collegiate Athletic Association (NCAA) football games from 2000, before the 2005 rule update, to 2007, after the rule update (information obtained from the NCAA[68]).
The NFHSA eliminated the ‘‘attempt to punish’’ phrase in 2007, and the high school rule now states that ‘‘Spearing is an act by an offensive or defensive player who initiates contact against any opponent with the top of his helmet.’’ Finally, changes to the NCAA rules in the 2008 season not only eliminated the ambiguous phrasings but also added that ‘‘When in question, it is a foul.’’ Spearing will incur a 15-yard penalty with automatic first down and possibility of disqualification for flagrant offenders. Thus, these latest rule changes (NFHSA 2007, NCAA 2008) could help referees to better prohibit spearing, whether intentional or not, and to better protect both offensive and defensive players from spinal injury in upcoming years. 2. Pathomechanics/Pathophysiology of Cervical Spine Cord Trauma and Guide to Management 2.1 Injuries at the C3–C4 Level
Injuries at the C3–C4 level are rare in comparison with the other cervical vertebrae and are infrequently reported.[24,69,70] Injuries at this level accounted for only 25 (2.4%) of the NFHNIR documented 1062 injuries occurring between 1971 and 1988.[71,72] Axial loading was again the ª 2010 Adis Data Information BV. All rights reserved.
predominant injury mechanism. The specific injuries were acute intervertebral disc herniation, anterior subluxation, unilateral and bilateral facet dislocation, and C4 vertebral fracture. Injuries to the middle cervical segment are unique in that these lesions generally do not involve fracture and more favourable results were observed with prompt reduction of unilateral and bilateral facet dislocations. In two cases of unilateral facet dislocation reduced within 3 hours of injury, marked neurological recovery occurred compared with the remaining patients who were treated with delayed open reduction or closed skeletal traction and who remained quadriplegic. Four patients in whom a bilateral facet dislocation was reduced successfully with either closed or open methods had no neurological recovery, but all four patients survived. The three patients who did not have a successful reduction died.[70] 2.2 The Axial Load Teardrop Fracture
Schneider and Kahn[73] were the first to describe a triangular fracture fragment at the anteroinferior corner of a cervical vertebral body as a ‘teardrop’ fracture. Their description was made on the basis of analysis of lateral x-rays and they concluded that the fracture was caused by acute flexion. The terms ‘acute flexion’ and ‘teardrop’[39] have been recognized and accepted as the terms for vertebral body fractures with an antero-inferior corner fracture fragment. Others have described these fractures as burst[74] or compression fractures, or have used the terms ‘flexion teardrop’[75] and ‘burst’ interchangeably.[76-78] Because of the inconsistency in both terminology and injury mechanism, the neurological sequelae of each of the fracture patterns had not been clarified. Utilizing data from the NFHNIR, 55 patients with 58 teardrop fractures of C4, 5 and 6 were analysed.[79] In 51 of the 55 patients, axial compression was determined to be the mechanism of injury. Radiographically, only six patients had an isolated antero-inferior vertebral body fracture; in 49 patients, there was in addition a sagittal vertebral body fracture and fractures through the lamina. In this series, five of the six patients with an isolated antero-inferior corner fracture had Sports Med 2010; 40 (1)
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no serious neurological sequelae; one patient had posterior element fractures of the subjacent vertebra and was quadriplegic. Of the 49 patients with a documented three-part, two-plane injury, 44 (90%) were quadriplegic. These results identified two fracture patterns associated with the antero-inferior corner fracture (teardrop) fragment: the isolated fracture that is not associated with permanent neurological sequelae, and the three-part, two-plane fracture in which there is a sagittal vertebral body fracture and fracture of the posterior neural arch, which is usually associated with permanent neurological sequelae. The mechanism of injury for both fracture patterns is axial loading. 2.3 Spear Tackler’s Spine
Spear tackler’s spine is a clinical entity that constitutes an absolute contraindication to participation in tackle football and other collision activities that expose the cervical spine to axial energy inputs.[58] A subset of football players were identified who demonstrated: (i) developmental narrowing of the cervical canal (canal-vertebral body ratio <0.8); (ii) straightening or reversal of the normal cervical lordosis; (iii) post-traumatic radiographic abnormalities; (iv) video documentation of using spear tackling techniques; and (v) a history of cervical cord, nerve root or plexus neurapraxia. Fifteen cases of spear tackler’s spine meeting these criteria were identified by the NFHNIR between 1987 and 1990.[58] Eleven patients had complete neurological recovery from their injuries and four patients had permanent neurological deficits. Permanent neurological injury occurred as the result of axial loading of a persistently straightened cervical spine from use of head-impact playing techniques. On the basis of these observations, it was concluded that individuals who possess the aforementioned characteristics of spear tackler’s spine be precluded from participation in activities that expose the cervical spine to axially directed energy inputs. 2.4 Cervical Cord Neurapraxia
Neurapraxia of the cervical spinal cord with transient quadriplegia has been previously deª 2010 Adis Data Information BV. All rights reserved.
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scribed in both NFHNIR and clinical practice data.[80-82] The prevalence of cervical cord neurapraxia (CCN) has been estimated at 7 per 10 000 football participants. It involves an athlete who sustains an acute transient neurological episode of cervical spinal cord origin associated with sensory changes of burning pain, numbness, tingling or loss of sensation with or without motor changes of weakness or complete paralysis. The episode is transient, with complete recovery usually occurring in 10–15 minutes, although recovery may take up to 2 days. The cervical area is pain free at the time of injury and there is complete return of motor function and full range of motion. In athletes with diminution of the anteroposterior diameter of the spinal canal, the cord can, on forced hyperextension or hyperflexion, be compressed causing transient motor and sensory manifestations described as the ‘‘pincer mechanisms’’ by Penning.[83] To determine which athletes had a decreased anteroposterior diameter of the spinal canal, an objective measurement was devised that compares the spinal canal sagittal diameter to that of the vertebral body on the lateral radiograph (figure 5).[84] There is normally a 1 : 1 relationship. A spinal canal-vertebral body ratio of 0.80 or less was recorded at one or more levels in all patients who experienced CCN.[81]
b
a
Ratio = a b Fig. 5. The spinal canal/vertebral body ratio is the distance from the midpoint of the posterior aspect of the vertebral body to the nearest point on the corresponding spinolaminar line (a) divided by the anteroposterior width of the vertebral body (b) [reproduced from Torg et al.,[81] with permission].
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a 0.9
Probability of recurrence
0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0 6
7
8 9 10 11 12 13 MRI disc level canal diameter (mm)
14
15
b 0.9 0.8 Probability of recurrence
It should be noted that Herzog et al.,[85] studying a cohort of professional football players, pointed out that although the canal-vertebral body ratio has a high sensitivity for detecting cervical spinal stenosis, it has a poor positive predictive value. Questions regarding both the relationship of cervical sagittal spinal canal size and injury as well as the reliability of the canal-vertebral body ratio as an indicator of stenosis subsequently arose.[86,87] To answer these questions, Kang et al.[87] reported an association between severity of spinal cord injury and cord space, noting that patients with permanent cord damage had narrower sagittal diameters before their injuries. After comparing CT parameters in the cervical spine of cord-injured patients with those of normal controls, Matsuura et al.[88] concluded that the intrinsic dimensions and shape of the cervical spinal canal may contribute a predisposition to cord injury. To analyse the relationship of the spinal cord to the spinal canal, a computerized system was developed to analyse the MRIs using a graphics digitizer pad with a resolution of 0.01 mm. The disc-level canal diameter was measured as the shortest distance between the intervertebral disc and the bony posterior elements to quantify spondylolytic narrowing. The cord diameter was determined by measuring its transverse diameter. Graphic plots were constructed using logistic regression analysis of the percentage risk of recurrence versus the disclevel canal diameter and the spinal canal-vertebral body ratio (figures 6a and 6b). The overall average recurrence rate for those who returned to football was 56%. Specific risk of recurrence is inversely correlated to canal size, i.e. the smaller the canal, the greater the risk, and is clearly predictable. Individuals who experience uncomplicated CCN are not at risk of incurring permanent neurological sequelae; rather, the problem is recurrence of subsequent transient episodes.[90] To address the issues of canal size and cord injury, and to determine the relationship between a developmentally narrowed cervical spinal canal and reversible and irreversible injury, a classification system and an epidemiological study were created. The classification system of CCN[90] was developed based on clinical, radiographic and
0.7 0.6 0.5 0.4 0.3 0.2 0.1 0 0.3
0.4
0.5 0.6 0.7 0.8 0.9 1.0 1.1 1.2 x-Ray spinal canal/vertebral body ratio
1.3
Fig. 6. Graphs developed using logistic regression analysis in which the risk of recurrence can be plotted as a function of the disc level diameter measured on (a) MRI and (b) the spinal canal/ vertebral body ratio calculated on the basis of a radiograph. The construction of these plots is based on the result that increased risk of recurrence is inversely correlated with canal diameter. Future cervical cord neurapraxia patients can be counselled regarding their individual risk of recurrence based on the particular size of their spinal canal (reproduced from Torg et al.,[89] with permission).
MRI data. CCN was classified according to the degree of neurological deficit ranging from complete paralysis to only sensory deficit, graded according to length of neurological symptoms and defined by the anatomic distribution of the neurological symptoms. The epidemiological study was performed with the use of various cohorts of football players as well as a large control group.[90] They were: Sports Med 2010; 40 (1)
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Cohorts I and II: 227 college and 97 professional football players, respectively, who were asymptomatic without transient CCN. Cohort III: 45 high school, college and professional football players who had at least one episode of transient CCN. Cohort IV: 77 high school or college football players who were permanently quadriplegic. Cohort V: 105 control non-athlete male patients without a history of cervical spine injury or symptoms. The findings of this study demonstrated that (i) a ratio of 0.80 or less had a high sensitivity (93%) for transient neurapraxia and (ii) none of the 77 quadriplegic individuals (cohort IV) had had an episode of transient neurapraxia of the spinal cord before the catastrophic injury; none of the 45 high school, college and professional players who had had an episode of transient neurapraxia (cohort III) became quadriplegic despite narrowing of the cervical spinal canal. The data provided evidence that the occurrence of transient CCN and an injury associated with quadriplegia are unrelated (figure 7). It was concluded that developmental narrowing of the cervical spinal canal in the absence of in1 College 2 Professional 3 Transient 4 Quadraplegic 5 Control
Spinal canal diameter (mm)
19
4 5 1 2
5 4 1 2
1 4 2 5
2 1 4 5
18
17
16 3 3
15
3 3
C3
C4 C5 Cervical spine level
C6
Fig. 7. Profile plot of the mean diameter of the spinal canal measured in millimetres demonstrating a significantly smaller value for cohort III (transient neurapraxia) than all the other cohorts (p < 0.05). No significant difference was found among cohorts I, II, IV and V (reproduced from Torg et al.,[90] with permission).
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stability is neither a harbinger of nor a predisposing factor for permanent neurological injury.[90] Studies by Maroon et al.[91] and Bailes[92] reached similar conclusions. Maroon et al.[91] followed five athletes who had surgery for CNN secondary to herniated cervical discs, focal stenosis or compressive osteophytes, and the researchers found that neurologically intact players could safely return to play (though they wouldn’t necessarily recommend it) and that there was an increased risk of repeated disc herniation above or below the site of the fusion but there was not a greater risk of quadriplegia. Therefore, on the basis of available data, it appears that developmental narrowing of the cervical spinal canal without associated instability does not predispose an individual to permanent neurological injury. The major factor in the occurrence of cervical quadriplegia in football is a playing technique in which the head is used as the primary point of contact, with an axial energy input to, and subsequent failure of, the cervical spine. Although a controversial issue, and one about which many spine surgeons disagree, CCN should not necessarily preclude an athlete from participation in contact sports.[89,93-95] A clear understanding of the pathomechanics of cervical spine injury combined with a description of those specific injury patterns have aided in attempts to establish criteria for return to activity[93,96,97] (table II). 3. Pathophysiology of Cervical Cord Injury as it Relates to the Principles of Cord Resuscitation and Clinical Application Athletic injuries to the cervical spine have resulted in reversible, incompletely reversible and irreversible neurological deficits.[58,70,81,98] A possible explanation for the variable response to injury has been obtained from the study of the histochemical responses of an in vitro axon injury model to mechanical deformation.[99] The spinal cord is considered an element with a low modulus of rigidity in which compressive macroscopic deformations result in local elongation. With axial elongation of the cord, all elements experience Sports Med 2010; 40 (1)
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Table II. Guidelines for return to play by an athlete who sustained previous cervical cord neurapraxia (from Torg et al.)[64] No contraindication 1. Spinal canal/vertebral body ratio £0.8 in an asymptomatic individual Relative contraindication 1. Spinal canal/vertebral body ratio £0.8 with one episode of cervical cord neurapraxia 2. Documented episode of cervical cord neurapraxia associated with intervertebral disc disease or degenerative changes 3. Documented episode of cervical cord neurapraxia associated with MRI evidence of cord deformation Absolute contraindication 1. Documented episode of cervical cord neurapraxia associated with MRI evidence of cord defect or cord oedema 2. Documented episode of cervical cord neurapraxia associated with ligamentous instability, neurological symptoms lasting >36 hours and/or multiple episodes
stretch. With extension or flexion, the tension in the cord will vary across the diameter. Highly localized loading, such as shearing from subluxation or focal compression, results in elongation in the direction of the long axis of the cord. The giant axon of the squid was used as the tissue model to determine the effects of high strain and uniaxial tension to various degrees of stretch in concert with the neurophysiological changes.[99] The effects of mechanical deformation of the axon membrane lead to an alteration in membrane permeability that allows calcium to flow into the cell and results in membrane depolarization. These experiments demonstrated that the degree of mechanical injury to the axon influences the magnitude of the calcium insult and the time course of the recovery phase. A low rate of deformation produces a small reversible depolarization; the axon responds to the increased intracellular calcium by pumping it extracellularly without residual deficit. As the rate of loading increased, the magnitude of the depolarization and the recovery time to the original resting potential increased in a nonlinear fashion; the axon may or may not fully recover depending on the ability of the cell to pump calcium. With a large influx of calcium, intracellular calcium pumps may be overwhelmed resulting in irreversible injury. The excess intracellular calcium results in accumulation of proteins intracellularly. ª 2010 Adis Data Information BV. All rights reserved.
The resulting increased osmotic pressure causes the cell to swell and eventually rupture. In addition to the immediate and direct effect of mechanical deformation on the cytosolic calcium concentration within the axon, it has been shown that high strain rate elongation of isolated venous specimens elicits a spontaneous constriction. This mechanically induced vasospasm alters blood flow in various regions as a function of the level of vessel stretch. Ultimately, the outcome for the neural tissue will depend synergistically on the level of calcium introduced into the cytosol and the degree to which the metabolic machinery of the cell may be compromised by regional reduction in blood flow.[99] The clinical evidence of varying degrees of recovery to cervical spine injury correlate with the in vitro axon model. 3.1 Clinical Correlation
Cord neurapraxia and transient quadriplegia, a completely reversible cord lesion, are associated with developmental narrowing of the cervical spinal canal. Cord deformation occurs rapidly and is attributable to a hyperflexion or hyperextension mechanism. Disruption of cell membrane permeability leads to a small increase in intracellular calcium, but spinal stability and cell anatomy is not disturbed, and the deleterious effect of local anoxia secondary to venous spasm do not impede recovery of axonal function. Incomplete cord reversibility is often associated with instability whereby the cord undergoes maximal elastic deformation. It is proposed that a lack of full recovery is attributable to a prolonged duration of deformity with local anoxia inhibiting cell membrane function and a reduction of intracellular calcium concentrations. Irreversible cord injury with permanent quadriplegia results from an axial load mechanism, which causes a fracture or dislocation that renders the spine markedly unstable. The cord undergoes functional plastic deformation with anatomic disruption of axonal integrity. The literature supports the concept that acute spinal cord injury with concomitant subluxation and dislocation should be reduced promptly.[69,94,98,100-103] Similar to irreversible neurological Sports Med 2010; 40 (1)
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sequelae following closed head injuries, it is the secondary injury phenomena, cerebral hypoxia and ischaemia due to swelling, that is the major problem. It is well established in the neurosurgery literature that the release of excitotoxic substances, cell membrane depolarization, the rise in the intracellular calcium concentration and increased intracellular hydrostatic pressure results in increase neuronal pressure and rupture.[89,99] With regard to permanent neurological sequelae, it is proposed that the same pathophysiological mechanistical phenomena occur in acute spinal cord trauma. It is the secondary injury phenomenon to the cord caused by oedema, hypoxia and aberration of cell membrane potential that is largely responsible for the resultant neurological deficit. Admittedly based in part on clinical observations lacking scientific format, the concept of spinal cord resuscitation has been proposed for consideration as an attempt to reverse the secondary injury phenomena to obtain maximum neurological recovery. Such measures include support of both respiratory and haemodynamic function to facilitate spinal cord perfusion, prompt relief of cord defamation, administration of intravenous corticosteroids as recommended by Bracken et al.,[104] and early spinal stabilization. 4. Brachial Plexus/Cervical Nerve Root Injuries Due to the nature of contact sports such as football, wrestling and ice hockey, the brachial plexus is frequently subjected to physical trauma. A review of all sports-related peripheral nerve injuries shows that ‘burners’ are more frequent than any other single nerve lesion.[105] An estimated 49–65% of collegiate football players experience a ‘stinger’ at least once in their career,[106,107] with a recurrence rate of 87%.[107] Under-reporting is common because of the transience of milder cases. The variable severity of deficits in brachial nerve injuries, like the variable responses to spinal cord injuries, may be explained by the in vitro axon model described in section 3. The mildest and most common type of brachial plexus injury is termed neurapraxia. In neurapraxia, the nerves remain structurally ª 2010 Adis Data Information BV. All rights reserved.
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sound but focal demyelination causes a temporary conduction block with loss of sensation and/or motor function for from minutes up to possibly 6 weeks. Axonotmesis, the next grade up in plexopathies, involves a damaged axon and consequently Wallerian degeneration of the distal nerve end. Fortunately, the axon is able to slowly repair due to an intact epineurium layer, and complete recovery may be obtained in a few months. However, injury to the entire neuron (i.e. the axon and all of the surrounding connective tissue layers) may occur in the case of neurotmesis, recovery from which varies. If indicated, surgery should be performed in a timely manner to encourage nerve regeneration; however, even with timely surgery, the damage may still take a year to resolve, assuming function does indeed return.[108] The symptoms of axonotmesis include acute pain, burning or tingling, hence the name ‘burner’ or ‘stinger’. This pain is characteristically unilateral, radiating from one side of the neck or shoulder down possibly all the way to the fingertips. As the upper trunk of the brachial plexus (C5 and C6) is commonly involved in burners, predominant weakness may be expected in the deltoid, supraspinatous and coracobrachial muscles.[109] Knowing that extended symptoms last hours, days and up to weeks in 5–10% of brachial plexus cases, it is possible to overlook a more serious injury. Coaches, players and their trainers must be careful not to immediately rule out a cervical nerve root injury or spinal cord trauma.[110] Hinton and Torg (Hinton MA, Torg JS, unpublished data) report an exemplary case of an unstable cervical fracture that went undiagnosed for several days as the neurological deficit progressively worsened; fortunately, the player was removed from the game and practice and avoided potentially devastating ramifications (in this particular case, surgery was successful in reversing the motor and sensory losses though the player chose not to return to football). Researchers have used electrodiagnostic studies to try to locate the exact spot of these nerve lesions. These studies yielded conflicting conclusions with some reports pointing to the upper Sports Med 2010; 40 (1)
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trunk of the brachial plexus[106,111] and others to the nerve roots.[112,113] Wilbourn[114] even argues that such studies don’t allow differentiation between the two sites; therefore, physicians should not exclude roots and assign injuries to the plexus instead based on a lack of electrical evidence. However, it seems both conclusions are correct in that both upper trunk plexopathies and cervical radiculopathies cause burners. Each lesion has been classified with a specific mechanism of injury. 4.1 Mechanisms of Injury
The mechanisms identified to cause burners are compression (of the nerve root) and traction (of the plexus). Some studies have also included direct trauma to be a third mechanism.[109,110,115,116] Markey et al.[109] and Meyer et al.[117] both found that compression was the most common mechanism among their college-age subjects. Reilly and Torg[118] noted its association with older players in collegiate and professional leagues, especially players with stenosis, cervical disk disease, degeneration or other pre-existing conditions. Compression of the cervical nerves occurs with the shoulder pad pressing the nerves against the superior medial scapula in a point where they are vulnerable called Erb’s point.[109] Hyperextension of the neck combined with rotation may cause compression of the nerve roots by narrowing the foraminal canal diameter; the foraminal canal is another site of vulnerability due to the absence of epineurium and perineurium cushioning. Finally, axial loading along with the contrived head position from a tackle leads to compression. Traction, or stretch injury, results from pressure forcing the distal and proximal ends of the plexus in opposite directions. The shoulder (distal) is depressed while the head is being pushed toward the contralateral side. Younger players tend to have stretch stingers rather than compression stingers since these players have yet to develop predisposing spinal conditions.[108,110,119] Meyer et al.[117] reported that players with stretch stingers were able to return to football sooner than players with compression stingers. Direct trauma to the plexus at Erb’s point can also produce a burner. In football, the blow from ª 2010 Adis Data Information BV. All rights reserved.
an opponent’s helmet or shoulder pad may injure the nerve tissue between the player’s scapula and his own shoulder pads. Similarly, this may be seen in hockey or lacrosse if a player is hit on the shoulder with someone else’s stick.[109,110,115,116] 4.2 Chronic Burner Syndrome
Levitz et al.[120] define chronic burner syndrome as neurapraxia and/or axonotmesis episodes with prolonged weakness, time loss from practice and games, and recurrence. The mechanism of chronic injury involves neck extension with ipsilateral-lateral deviation. Chronic burner syndrome is also known as chronic, recurrent cervical nerve root neurapraxia. Due to CCN and its association with cervical canal stenosis, a similar association was sought for cervical nerve root neurapraxia and stenosis. Kelly et al.[121] reported smaller cervical spinal canal ratios in football players with a known history of burners than in players without such a history. The Levitz et al.[120] study, which defines chronic burner syndrome, also demonstrated an association with cervical canal stenosis, reversal of lordosis, disk disease, foraminal stenosis and a positive Spurling’s sign, suggesting that said alterations in pathomechanics may be leading to the compression mechanism of dorsal nerve roots within the intervertebral foramina. Two further studies are also of particular note. Meyer et al.[117] tested for the Torg ratio in college football players who had had stingers versus players who were asymptomatic. Using athletes as the control group accounted for enlarged vertebral bodies in athletes which might otherwise exaggerate cervical spinal stenoses. Meyer et al.[117] found a smaller mean Torg ratio in the stinger group for all cervical vertebrae which was statistically significant for C4, C5 and C6; the fact that these are the vertebrae most commonly linked to stingers is well supported by most authors. The researchers calculated the risk of stingers to be three times greater when stenosis (as determined by the Torg ratio) was present. Kelly et al.[119] conducted a similar study in high school players that tested for both cervical spinal and foraminal stenoses. High school athletes Sports Med 2010; 40 (1)
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wouldn’t yet have as enlarged vertebral bodies or as many degenerative changes as both symptomatic and asymptomatic collegiate players accumulate, thus avoiding confounding factors to the data. Significant spinal canal narrowing was found in their burner group. Kelly et al.[119] also found that foraminal stenosis was associated with their burner group; they suggest that as these players acquire degenerative changes in time, their risk for root injury may increase further. 5. Recurrence and Return to Play The 1976 rule change on spearing, in shifting tackling technique away from the head and toward the shoulder, may have inadvertently promoted burners via lateral flexion of the neck with contralateral shoulder depression.[106] This notion is supported by the fact that the estimate for burners increased from 49% in 1977 to 65% in 1992[106,107] as the incidence of quadriplegia decreased from 34 in 1976 to 6 in 1992.[68] However, since head-up tackling is necessary to avoid catastrophic spinal cord injuries, preventative measures for burners must rely on properly fitting shoulder pads, cervical orthosis and neck exercises.[116,122] Electromyography (EMG) should be used to help diagnose the injury. Athletes were found to have a higher percentage, about 50%, of abnormal EMG results than the average patient population when an EMG was ordered as a means to rule out nerve injury.[114] However, EMG is not an effective diagnostic tool for acute burners because abnormal EMG readings typically develop 3–5 weeks after the injury. Therefore, earlier EMG readings could be misleading. Furthermore, researchers do not recommend basing return-to-play decisions on EMG because clinical function of the muscles may return before the EMG returns to normal.[113,123] Bergfeld et al.[123] estimated that 80% of clinically normal patients still have an abnormal EMG for an average of up to 53 months, or 4.42 years, post-injury. There have been several attempts to devise return-to-play criteria. Watkins et al.[124] offer a set of guidelines for scoring an athlete’s condition and return-to-play eligibility. Similarly, Bailes ª 2010 Adis Data Information BV. All rights reserved.
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et al.[125] outline a classification system for who should and should not return, taking into account the transience of symptoms, physical examination, radiography and stability of the lesion. Decisions must be made on an individual case basis, taking into account a number of factors. Athletes should have regained full range of motion and should no longer be experiencing paraethesia. Spurling, brachial plexus stretch and axial compression tests should all be negative. Recovery of normal, symmetrical motor strength is also necessary.[126] This last criterion is strongly emphasized by most authors. Contraindications include unstable vertebral damage and loss of lordosis.[94,95,126] Despite the association of congenital stenosis with chronic burners, it has been argued that it is not an absolute contraindication for return to play,[94,95] whereas others believe that foraminal stenosis should elicit advice against a return to contact sports.[126] For those permitted to return to contact sports, a year-round exercise regimen should be undertaken to strength the neck muscles and the player’s ability to absorb the shock of tackles.[122] It is also recommended that they use a cervical orthosis in order to limit neck extension and lateral deviation (e.g. ‘cowboy’ collars).[109,116] All shoulder padding should be checked for proper fit, and player technique should be reviewed. 6. Conclusions The major contributions of these works have been: (i) implementation of an effective, nationally recognized injury prevention programme generated from within the orthopaedic community; (ii) the attempt to correlate the observed clinical pathomechanics with cellular pathophysiology in instances of cervical spine, spinal cord, brachial plexus and cervical nerve root trauma; and (iii) initiation of recognition of the importance of appropriate early intervention treatment regimens for catastrophic cervical cord injuries and burners. It is hoped that the updated rules on spearing will decrease the incidence of catastrophic spinal injuries, but ultimately this rule relies on more than just the players to succeed. Coaches, referees, Sports Med 2010; 40 (1)
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trainers and physicians working together can protect athletes from preventable injury. Coaches must teach proper tackling techniques; referees must penalize spear-tacklers; trainers must recognize the potential seriousness of an injury; and doctors must be able to evaluate return-to-play status. Stingers, or burners, present additional issues for catching these injuries due to their transient nature and for diagnosing them due to the limitations of EMG results. Particular attention should be played to looking out for athletes with chronic burner syndrome and its associated risk factors as this may influence return-to-play decisions. Acknowledgements No sources of funding were used to assist in the preparation of this review. The authors have no conflicts of interest that are directly relevant to the content of this review.
References 1. Schneider RC. Head and neck injuries in football: mechanisms, treatment, and prevention. Baltimore (MD): Williams and Wilkins, 1973 2. Dolan KD, Feldick HG, Albright JP, et al. Neck injuries in football players. Am Fam Physician 1975; 12: 86-91 3. Funk Jr FJ, Wells RE. Injuries of the cervical spine in football. Clin Orthop Relat Res 1975; 109: 50-8 4. Silver JR. Injuries of the spine sustained in rugby. BMJ 1984; 288: 37-43 5. Alexander Jr E, Davis Jr CH, Field CH. Hyperextension injuries of the cervical spine. Arch Neurol Psychiatry 1958; 19: 146-50 6. Ciccone R, Richman R. The mechanism of injury and the distribution of three thousand fractures and dislocations caused by parachute jumping. J Bone Joint Surg 1948; 30A: 77-100 7. Ellis WB, Green D, Holzaepfel NR, et al. The trampoline and serious neurological injuries: a report of five cases. JAMA 1960; 174: 1673-6 8. Hage P. Trampolines: an ‘attractive nuisance’. Physician Sportsmed 1982; 10: 118-22 9. Kravitz H. Problems with the trampoline: 1. Too many cases of permanent paralysis. Pediatr Ann 1978; 7: 728-9 10. Tator CH, Edmonds VE. National survey of spinal injuries to hockey players. Can Med Assoc J 1984; 130: 875-80 11. Tator CH, Ekong CEU, Rowed DA, et al. Spinal injuries due to hockey. Can J Neurol Sci 1984; 11: 34-41 12. Torg JS, Das M. Trampoline-related quadriplegia: review of the literature and reflections on the American Academy of Pediatrics’ position statement. Pediatrics 1984; 74: 804-12
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13. Carvell JE, Fuller DJ, Duthrie RB. Rugby football injuries to the cervical spine. BMJ 1983; 286: 49-50 14. McCoy GF, Piggot J, Macafee AL, et al. Injuries of the cervical spine in schoolboy rugby football. J Bone Joint Surg 1984; 66-B: 500-3 15. O’Carroll F, Sheenan M, Gregg TM. Cervical spine injuries in rugby football. Irish Med J 1981; 74: 377-9 16. Piggot J, Gordon DS. Rugby injuries to the cervical cord. BMJ 1979; 1: 192-3 17. Scher AT. Crashing the rugby scrum: an avoidable cause of cervical spinal injury. S Afr Med J 1982; 61: 919-20 18. Williams JPR, McKibbin B. Cervical spine injuries in rugby union football. Br Med J 1978; 2: 147-50 19. Gehweiler Jr JA, Clark WM, Schaaf RE, et al. Cervical spine trauma: the common combined conditions. Radiology 1979; 130: 77-86 20. MacNab I. Acceleration injuries of the cervical spine. J Bone Joint Surg 1964; 46-A: 1797-9 21. Wu WQ, Lewis RC. Injuries of the cervical spine in high school wrestling. Surg Neurol 1985; 23: 143-7 22. Leidholt JD. Spinal injuries in athletes: be prepared. Orthop Clin North Am 1973; 4: 691-703 23. Paley D, Gillespie R. Chronic repetitive unrecognized flexion injury of the cervical spine (high jumper’s neck). Am J Sports Med 1986; 14: 92-5 24. Burke DC. Hyperextension injuries of the spine. J Bone Joint Surg 1971; 53-B: 3-12 25. Carter OR, Frankel VH. Biomechanics of hyperextension injuries to the cervical spine in football. Am J Sports Med 1980; 8: 302-9 26. Edeiken-Monroe B, Wagner LK, Harris Jr JH. Hyperextension dislocation of the cervical spine. AJR Am J Roentgenol 1986; 146: 803-8 27. Forsyth HF. Extension injuries of the cervical spine. J Bone Joint Surg 1964; 46-A: 1792-7 28. Marar BC. Hyperextension injuries of the cervical spine. J Bone Joint Surg 1974; 56-A: 1655-62 29. Scher AT. Diversity of radiological features in hyperextension injury of the cervical spine. S Afr Med J 1980; 58: 27-30 30. Kazarian L. Injuries to the human spinal column: biomechanics and injury classification. Exerc Sport Sci Rev 1981; 9: 297-352 31. Kewalramani LS, Taylor RG. Injuries to the cervical spine from diving accidents. J Trauma 1975; 15: 130-42 32. Albrand OW, Corkill G. Broken necks from diving accidents. Am J Sports Med 1976; 4: 107-10 33. Albrand OW, Walter J. Underwater deceleration curves in relation to injuries from diving. Surg Neurol 1975; 4: 461-5 34. Maroon JC, Steele PB, Berlin R. Football head and neck injuries: an update. Clin Neurosurg 1979; 27: 414-29 35. Mennen U. Survey of spinal injuries from diving: a study of patients in Pretoria and Cape Town. S Afr Med J 1981; 59: 788-90 36. Rogers WA. Fractures and dislocations of the cervical spine: an end-result study. J Bone Joint Surg 1957; 39A: 341-76
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37. Scher AT. Diving injuries to the cervical spinal cord. S Afr Med J 1981; 59: 603-5 38. Scher AT. Injuries to the cervical spine sustained while carrying loads on the head. Paraplegia 1978; 16: 94-101 39. Scher AT. ‘Tear-drop’ fractures of the cervical spine: radiologic features. S Afr Med J 1982; 61: 355-9 40. Scher AT. The high rugby tackle: an avoidable cause of cervical spinal injury? S Afr Med J 1978; 53: 1015-8 41. Scher AT. Vertex impact and cervical dislocation in rugby players. S Afr Med J 1981; 59: 227-8 42. Burstein AH, Otis JC, Torg JS. Mechanisms and pathomechanics of athletic injuries to the cervical spine. In: Torg JS, editor. Athletic injuries to the head, neck, and face. Philadelphia (PA): Lea and Febiger, 1982: 139-54 43. Nightingale RW, McElhaney JH, Richardson WJ, et al. Experimental impact injury to the cervical spine: relating motion of the head and the mechanism of injury. J Bone Joint Surg 1996; 78-A: 412-21 44. Torg JS. Epidemiology, pathomechanics, and prevention of athletic injuries to the cervical spine. Med Sci Sports Exerc 1985; 17: 295-303 45. Torg JS, Vegso JJ, O’Neill MJ, et al. The epidemiologic, pathologic, biomechanical, and cinematographic analysis of football-induced cervical spine trauma. Am J Sports Med 1990; 18: 50-7 46. Mertz HJ, Hodgson VR, Murray TL, et al. An assessment of compressive neck loads under injury-producing conditions. Physician Sportsmed 1978; 6: 95-106 47. Hodgson VR, Thomas LM. Mechanisms of cervical spine injury during impact to the protected head. In: Proceedings of the Twenty-Fourth Stapp Car Crash Conference. Warrendale (PA): Society of Automobile Engineers, 1980: 15-42 48. Sances Jr A, Myklebust JB, Maiman DJ, et al. Biomechanics of spinal injuries. Crit Rev Biomed Eng 1984; 11: 1-76 49. Gosch HH, Gooding E, Schneider RC. An experimental study of cervical spine and cord injuries. J Trauma 1972; 12: 570-6 50. Maiman DJ, Sances Jr A, Myklebust JB, et al. Compression injuries of the cervical spine: a biomechanical analysis. Neurosurg 1983; 13: 254-60 51. Roaf R. Experimental investigations of spinal injuries. J Bone Joint Surg 1959; 41-B: 855 52. White AAI, Punjabi MM. Clinical biomechanics of the spine. Philadelphia (PA): JB Lippincott, 1978 53. Roaf R. A study of the mechanics of spinal injuries. J Bone Joint Surg 1960; 42-B: 810-23 54. Bauze RJ, Ardran GM. Experimental production of forward dislocation in the human cervical spine. J Bone Joint Surg 1978; 60-B: 239-45 55. Torg JS, Quedenfeld TC, Burstein AH, et al. National Football Head and Neck Injury Registry: report on cervical quadriplegia 1971 to 1975. Am J Sports Med 1979; 7: 127-32 56. Torg JS, Truex Jr RC, Quedenfeld TC, et al. The National Football Head and Neck Injury Registry: report and conclusions 1978. JAMA 1979; 241: 1477-9 57. Schneider RC. Serious and fatal neurosurgical football injuries. Clin Neurosurg 1966; 12: 226-36
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58. Torg JS, Sennett B, Pavlov H, et al. Spear tackler’s spine: an entity precluding participation in tackle football and collision activities that expose the cervical spine to axial energy inputs. Am J Sports Med 1993; 21: 640-9 59. National Collegiate Athletic Association. Football rules and interpretations. Indianapolis (IN): National Collegiate Athletic Association, 1976 60. National Collegiate Athletic Association. Football rules and interpretations. Indianapolis (IN): National Collegiate Athletic Association, 2005 61. National Collegiate Athletic Association. Football rules and interpretations. Indianapolis (IN): National Collegiate Athletic Association, 2008 62. Boden BP, Tacchetti RL, Cantu RC, et al. Catastrophic cervical spine injuries in high school and college football players. Am J Sports Med 2006; 34: 1223-32 63. Cantu RC, Mueller FO. Catastrophic spine injuries in American football, 1977-2001. Neurosurgery 2003; 53: 358-63 64. Torg JS, Guille JT, Jaffe S. Injuries to the cervical spine in American football players. J Bone Joint Surg Am 2002; 84: 112-122 65. Mueller FO, Cantu RC. Annual survey of catastrophic football injury 1977–2007 [online]. Available from URL: http://www.unc.edu/depts/nccsi/FootballCatastrophic.pdf [Accessed 2009 Oct 14] 66. Heck JF. The incidence of spearing during a high school’s 1975 and 1990 football seasons. J Athletic Training 1996; 31: 31-7 67. Drake GA. Research provides more suggestions to reduce serious football injuries. Natl Fed News 1994 Nov/Dec; 18-21 68. Heck JF, Clarke KS, Peterson TR, et al. National Athletic Trainers’ Association position statement: head-down contact and spearing in tackle football. J Athletic Training 2004; 39 (1): 101-11 69. Bohlman HH. Acute fractures and dislocations of the cervical spine: an analysis of three hundred hospitalized patients and review of the literature. J Bone Joint Surg 1979; 61-A: 1119-42 70. Torg JS, Sennett B, Vegso JJ, et al. Axial loading injuries to the middle cervical spine segment: an analysis and classification of twenty-five cases. Am J Sports Med 1991; 19: 6-20 71. Torg JS, Sennett B, Vegso JJ. Spinal injury at the level of the third and fourth cervical vertebrae resulting from the axial loading mechanism: an analysis and classification. Clin Sports Med 1987; 6: 159-83 72. Torg JS, Truex Jr RC, Marshall J, et al. Spinal injury at the level of the third and fourth cervical vertebrae from football. J Bone Joint Surg Am 1977; 59-A: 1015-9 73. Schneider RC, Kahn EA. Chronic neurological sequelae of acute trauma to the spine and spinal cord. Part I: the significance of the acute-flexion or ‘‘tear-drop’’ fracture dislocation of the cervical spine. J Bone Joint Surg Am 1956; 38-A: 985-97 74. Mawk JR. C7 burst fracture with initial ‘‘complete’’ tetraplegia. Minn Med 1983; 66: 135-8
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75. Kim KS, Chen HH, Russell EJ, et al. Flexion teardrop fracture of the cervical spine: radiographic characteristics. AJR Am J Roentgenol 1989; 152: 319-26 76. Woodford MJ. Radiography of the acute cervical spine. Radiography 1987; 53: 3-8 77. Allen BL, Ferguson RL, Lehmann TR, et al. A mechanistic classification of closed, indirect fractures and dislocations of the lower cervical spine. Spine 1982; 7: 1-27 78. Lee C, Kim KS, Rogers LF. Sagittal fracture of the cervical vertebral body. AJR Am J Roentgenol 1982; 139: 55-60 79. Torg JS, Pavlov H, O’Neill MJ, et al. The axial load teardrop fracture: a biomechanical, clinical, and roentgenographic analysis. Am J Sports Med 1991; 19: 355-64 80. Torg JS, Pavlov H, Genuario SE. Cervical spinal stenosis with cord neurapraxia and transient quadriplegia in athletes. Surg Rounds Orthop 1987; 9-19 81. Torg JS, Pavlov H, Genuario SE, et al. Neurapraxia of the cervical spinal cord with transient quadriplegia. J Bone Joint Surg Am 1986; 68: 1354-70 82. Torg JS. Cervical spinal stenosis with cord neurapraxia and transient quadriplegia. Clin Sports Med 1990; 9: 279-96 83. Penning L. Some aspects of plain radiography of the cervical spine in chronic myelopathy. Neurology 1962; 12: 513-9 84. Pavlov H, Torg JS, Robie B, et al. Cervical spine stenosis: determination with vertebral body ratio method. Radiology 1987; 164: 771-5 85. Herzog RJ, Wiens JJ, Dillingham MF, et al. Normal cervical spine morphometry and cervical spinal stenosis in asymptomatic professional football players: plain film radiography, multiplanar computed tomography, and magnetic resonance imaging. Spine 1991; 16 (6 Suppl.): S178-86 86. Eismont FJ, Clifford S, Goldberg M, et al. Cervical sagittal spinal canal size in spine injury. Spine 1984; 9 (7): 663-6 87. Kang JD, Figgie MP, Bohlman HH. Sagittal measurements of the cervical spine in subaxial fractures and dislocations: an analysis of two hundred and eighty-eight patients with and without neurological deficits. J Bone Joint Surg Am 1994; 76: 1617-28 88. Matsuura P, Waters RL, Adkins RH, et al. Comparison of computerized tomography parameters of the cervical spine in normal control subjects and spinal cord-injured patients. J Bone Joint Surg Am 1989; 71 (2): 183-8 89. Torg JS, Corcoran TA, Thibault LE, et al. Cervical cord neurapraxia: classification, pathomechanics, morbidity, and management guidelines. J Neurosurg 1997; 87: 843-50 90. Torg JS, Naranja Jr RJ, Pavlov H, et al. The relationship of developmental narrowing of the cervical spinal canal to reversible and irreversible injury of the cervical spinal cord in football players. J Bone Joint Surg Am 1996; 78: 1308-14 91. Maroon JC, El-Kadi H, Abla AA, et al. Cervical neurapraxia in elite athletes: evaluation and surgical treatment. J Neurosurg Spine 2007; 6: 356-63 92. Bailes JE. Experience with cervical stenosis and temporary paralysis in athletes. J Neurosurg Spine 2005; 2 (1): 11-6 93. Torg JS, Glasgow SG. Criteria for return to contact activities following cervical spine injury. Clin J Sports Med 1991; 1: 12-6
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94. Torg JS. Management guidelines for athletic injuries to the cervical spine. Clin Sports Med 1987; 6: 53-60 95. Torg JS, Ramsey-Emrhein JA. Management guidelines for participation in collision activities with congenital, developmental, or postinjury lesions involving the cervical spine. Sports Med Arthoscopy Rev 1997; 5: 226-42 96. Torg JS, Vermiel R, Torg E. Prevent paralysis: don’t hit with your head [video]. Philadelphia (PA): University of Pennsylvania, 1992 97. Torg JS, Vegso JJ, Torg E. Cervical quadriplegia resulting from axial loading injuries: cinematographic radiographic, kinetic and pathologic analysis. Chicago (IL): American Academy of Orthopaedic Surgeons Audio-Visual Library, 1987 98. Bohlman HH, Anderson PA. Anterior decompression and arthrodesis of the cervical spine: long-term motor improvement. J Bone Joint Surg Am 1992; 74: 671-82 99. Torg JS, Thibault L, Sennett B, et al. The Nicolas Andry Award: the pathomechanics and pathophysiology of cervical spinal cord injury. Clin Orthop Relat Res 1995; 321: 259-69 100. Chiles BW, Cooper PR. Acute spinal injury. N Engl J Med 1996; 334: 514-20 101. Delamarter RB, Sherman J, Carr JE. Pathophysiology of spinal cord injury; recovery after immediate and delayed decompression. J Bone Joint Surg Am 1995; 77: 1042-9 102. Forsyth HF, Alexander Jr E, Davis Jr C, et al. The advantages of early spine fusion in the treatment of fracturedislocations of the cervical spine. J Bone Joint Surg Am 1959; 41-A: 17-36 103. Slucky AV, Eismont FJ. Treatment of acute injury of the cervical spine. Instr Course Lect 1995; 44: 67-80 104. Bracken MD, Shepard MJ, Collins WF, et al. A randomized, controlled trial of methylprednisolone or naloxone in the treatment of acute spinal cord injury. N Engl J Med 1990; 322: 1405-11 105. Krivickas LS, Wilbourn AJ. Sports and peripheral nerve injuries: report of 190 injuries evaluated in a single electromyography laboratory. Muscle Nerve 1998; 21: 1092-4 106. Clancy Jr WG, Brand RL, Bergfield JA. Upper trunk brachial plexus injuries in contact sports. Am J Sports Med 1977; 5: 209-16 107. Sallis RE, Jones K, Knopp W. Burners: offensive strategy for an underreported injury. Physician Sportsmed 1992; 20 (11): 47-55 108. Olsen DE, McBroom SA, Nelson BD, et al. Unilateral cervical nerve injuries: brachial plexopathies. Curr Sports Med Rep 2007; 6: 43-9 109. Markey KL, Di Benedetto M, Curl WW. Upper trunk brachial plexopathy: the stinger syndrome. Am J Sports Med 1993; 21 (5): 650-5 110. Safran MR. Nerve injury about the shoulder in athletes, part 2: long thoracic nerve, spinal accessory nerve, burners/stingers, thoracic outlet syndrome. Am J Sports Med 2004; 32: 1063-76 111. Robertson WC, Eichman PL, Clancy WG. Upper trunk brachial plexopathy in football players. JAMA 1979; 241: 1480-2
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112. Poindexter DP, Johnson EW. Football shoulder and neck injury: a study of the ‘‘stinger.’’ Arch Phys Med Rehabil 1984; 65: 601-2 113. Speer KP, Bassett III FH. Prolonged burner syndrome. Am J Sports Med 1990; 18 (6): 591-4 114. Wilbourn AJ. Electrodiagnostic testing of neurologic injuries in athletes. Clin Sports Med 1990; 9 (2): 229-45 115. DiBennedetto M, Markey K. Electrodiagnostic localization of traumatic upper trunk brachial plexopathy. Arch Phys Med Rehabil 1984; 65 (1): 15 116. Koffler KM, Kelly IV JD. Neurovascular trauma in athletes. Orthop Clin N Am 2002; 33: 523-4 117. Meyer SA, Schulte KR, Callaghan JJ, et al. Cervical spinal stenosis and stingers in collegiate football players. Am J Sports Med 1994; 22 (2): 158-66 118. Reilly PJ, Torg JS. Athletic injury to the cervical nerve roots and brachial plexus. Oper Tech Sports Med 1993; 1 (3): 231-5 119. Kelly IV JD, Aliquo D, Sitler MR, et al. Association of burners with cervical canal and foraminal stenosis. Am J Sports Med 2000; 28: 214-7 120. Levitz CL, Reilly PJ, Torg JS. The pathomechanics of chronic, recurrent, cervical nerve root neurapraxia. Am J Sports Med 1997; 25 (1): 73-6
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121. Kelly IV JD, Clancy M, Marchetto PA, et al. The relationship of transient upper extremity paresthesias and cervical stenosis. Orthop Trans 1992; 16: 732-8 122. Bland JH. Helping athletes avoid neck injuries. J Musculoskel Med 1996; 13: 30-8 123. Bergfeld JA, Hershman E, Wilbourn A. Brachial plexus injuries in sports: a 5-year follow-up. Orthop Trans 1988; 12: 734-44 124. Watkins RG, Dillin W, Maxwell J. Cervical spine injuries in football players. Spine: State of Art Reviews 1990; 4 (2): 391-408 125. Bailes JE, Hadley MN, Quigley MR, et al. Management of athletic spine and spinal cord injuries. Neurosurgery 1991; 29: 491-7 126. Cantu RC. Stinger, transient quadriplegia, and cervical spinal stenosis: return to play criteria. Med Sci Sports Exerc 1997; 29: S233-5
Correspondence: Dr Joseph S. Torg, Temple University Hospital, 6th Floor OPB, 3401 N. Broad Street, Philadelphia, PA 19140, USA. E-mail:
[email protected]
Sports Med 2010; 40 (1)
Sports Med 2010; 40 (1): 77-90 0112-1642/10/0001-0077/$49.95/0
REVIEW ARTICLE
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Mountain Biking Injuries in Children and Adolescents Kylee B. Aleman1 and Michael C. Meyers1,2 1 Human Performance Research Laboratory, Department of Sports and Exercise Sciences, West Texas A&M University, Canyon, Texas, USA 2 Montana State University, Bozeman, Montana, USA
Contents Abstract. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. Events and Requirements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Injuries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1 Incidence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2 Head and Neck Injuries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3 Thoraco-Abdominal Injuries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4 Upper Extremity Injuries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.5 Trunk Injuries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.6 Lower Extremity Injuries. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.7 Fatal Injuries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Aetiology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1 Overuse and Fatigue . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2 Age, Skill Level and Experience . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3 Equipment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4 Musculoskeletal Immaturity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.5 Excessive Speed . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.6 Environmental Conditions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.7 Conditioning and Fitness Status . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.8 Behaviour. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.9 Challenges in Medical Care . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. Limitations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5. Prevention . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.1 Education and Instruction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2 Equipment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.3 Training and Conditioning . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.4 Environmental Management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Abstract
77 78 79 79 80 81 81 81 82 83 83 83 83 84 84 84 85 85 85 85 86 87 87 87 87 88 88
Over the last decade, the sport of mountain biking has experienced extensive growth in youth participation. Due to the unpredictable nature of outdoor sport, a lack of rider awareness and increased participation, the number of injuries has unnecessarily increased. Many believe that the actual incidence of trauma in this sport is underestimated and is just the ‘tip of the
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iceberg’. The most common mechanism of injury is usually attributed to downhill riding and forward falling. Although rare, this type of fall can result in serious cranial and thoraco-abdominal trauma. Head and neck trauma continue to be documented, often resulting in concussions and the possibility of permanent neurological sequelae. Upper limb injuries range from minor dermal abrasions, contusions and muscular strains to complex particular fracture dislocations. These are caused by attempting to arrest the face with an outstretched hand, leading to additional direct injury. Common overuse injuries include repeated compression from the handlebars and vibration leading to neurovascular complications in the hands. Along with reports of blunt abdominal trauma and lumbar muscle strains, lower extremity injuries may include various hip/pelvic/groin contusions, patellofemoral inflammation, and various muscle strains. The primary causes of mountain biking injuries in children and adolescents include overuse, excessive fatigue, age, level of experience, and inappropriate or improperly adjusted equipment. Additional factors contributing to trauma among this age group involve musculoskeletal immaturity, collisions and falls, excessive speed, environmental conditions, conditioning and fitness status of the rider, nonconservative behavioural patterns, and inadequate medical care. The limited available data restrict the identification and understanding of specific paediatric mountain biking injuries and injury mechanisms. Education about unnecessary risk of injury, use of protective equipment, suitable bikes and proper riding technique, coupled with attentive and proper behaviour, are encouraged to reduce unnecessary injury. This article provides information on the causation and risk factors associated with injury among young mountain bikers, and recommendations to minimize trauma and enhance optimal performance and long-term enjoyment in this outdoor sport.
Since its inception over 30 years ago, individuals have been drawn to the fast-paced, outdoor sport of mountain biking (MTB).[1-4] During the 1990s, the participation in MTB increased from 4.6 million to over 10 million riders, with growth consistent throughout North America and Europe.[5-7] Since then, mountain bikes have outsold all other bicycles.[1-3,7-9] Due to the unpredictable nature of outdoor sport, a lack of rider awareness and increased participation, the number of injuries in MTB has unnecessarily increased.[5,9] Since its inception as an Olympic sport, youth spend a greater number of hours training and competing than ever before. As with many outdoor sports,[10-12] male mountain bikers participate more than females; however, some studies suggest that female mountain bikers are at an increased risk for trauma.[4,9,13,14] The unpredictable nature of terrain coupled with ª 2010 Adis Data Information BV. All rights reserved.
excessive speed results in significant injury to the developing musculoskeletal system. Injury will not only have implications for healing but also for future growth and maturation.[1,4,9,15-17] Unfortunately, the limited available data restrict the identification and understanding of specific paediatric MTB injuries and injury mechanisms. Therefore, based on the perceived increase in trauma among this active age group, it is imperative to glean the limited and diverse information available to confirm and develop strategies that may minimize unnecessary predisposition to trauma, optimize performance and provide long-term enjoyment in this growing outdoor activity. 1. Events and Requirements Mountain biking is a multifaceted sport that involves various types of competitive and Sports Med 2010; 40 (1)
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recreational challenges. In the US, the National Off-Road Bicycle Association (NORBA) offers six different competitions nationwide throughout the year. These six events are referred to as the National Championship Series, enabling riders to earn points and qualify for such competitions as the World Championships, organized by Union Cycliste Internationale (UCI).[1,8,14,17-19] Another prestigious challenge, the World Cup Series, consists of ten cross-country and six downhill races.[20] Both UCI and NORBA recognize different levels involving Pro/Elite, Expert, Sport and Beginner, and are separated into Junior (age 12–18 years), Senior (age 19–34 years), Veteran (age 35–44 years), and Master (age ‡45 years) groups.[17-20] Additional growth and worldwide popularity have also resulted in MTB becoming an Olympic sport in 2000.[1,5,21] There are currently several categories of mountain bike competitions: Olympic cross-country, hill climb/uphill, downhill, four cross and free, dual slalom, mountain cross, point-to-point racing, stage races, observed trials, ultraendurance events, and the short track race.[1,8,17,18,20] One of the longer and most energy-depleting of the five challenges, Olympic cross-country racing is composed of laps around varying terrain,[8,18,20] often lasting >2 hours, with competitors reaching heart rates up to 90% of their maximum heart rate (HR . max) and 84% of their maximal oxygen uptake (VO2max).[1,8] Hill climb/uphill events are timed races up steep inclines, whereas downhill racing requires precise attention, reaching speeds up to 112 km/h (70 mph).[1,18,20] Considered the most dangerous of all the races, because of the greater potential for trauma, professional mountain bikers are actually more often injured in downhill events than are amateur athletes.[1,14,15,17,19] Interestingly, crosscountry racing has become less prevalent, with downhill racing now the premiere event.[17] Both four cross and dual slalom racing consist of all-out brawls to the finish line along man-made trails.[1] UCI recently introduced a race similar to the dual slalom, named ‘The Dual’, where both riders race to the finish on a single course rather than on two separate courses.[17] Similarly, the mountain cross contains four competitors on a single course, and, similar to alpine skiing contests, these events ª 2010 Adis Data Information BV. All rights reserved.
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contain slalom gates with the winner determined by the lowest time.[17,18,20] Point-to-point races are where riders start in a mass group and travel from a designated point ‘A’ to a designated point ‘B’. Stage racing differentiates itself from other mountain bike competitions since it is broken up into a designated amount of phases over several days. Observed trials are technical contests where handling ability of the mountain bike is graded and the distance is short, whereas ultraendurance events involve no technical component, may extend over a 24-hour period, and usually involve distances of 120 km (75 miles) or more.[18,20] Although these races do not always require high speeds, the risk for collisions and falls is very high.[1] NORBA also offers a short track race where laps are completed for typically 30 minutes.[17] Regardless of the event, MTB racing requires high levels of physical fitness, the ability to defy gravity on steep climbs, and the strength to stabilize the bicycle on rocky terrain.[8] The excessive speed and surprises along courses contribute to injury, regardless of the cyclist’s experience level.[5] In actuality, with increasing experience mountain bikers sustain more joint injuries than less experienced riders.[15] 2. Injuries 2.1 Incidence
With the increase in participants combined with a more progressive style of MTB, the incidence of injury has been rising steadily among younger age groups. Similar to other youth sports, many believe that the actual incidence of trauma among young mountain bikers is underestimated or is just the ‘tip of the iceberg’, due to the tendency for injuries to go unreported, especially among the teenage sector.[10,22,23] Documentation of the incidence of injury among this population has also been hampered by numerous limitations, not only from a lack of injury awareness or under-reporting, but also from missing data, poor injury recall, a delay in subject response and subsequent treatment, and a multiplicative array of reporting sources.[10,22] Although information on injuries in children and adolescents in MTB is relatively limited, the type of Sports Med 2010; 40 (1)
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trauma is similar to cases reported among adult mountain bikers and on-road cyclists.[1,4,15,24] The aetiology of trauma, however, often remains unique to the young competitor. As previously stated, the increase in mountain bike enthusiasts worldwide has presented an increase in injuries, ranging from minor injuries to fatalities.[15] From 1992 to 2002, Kim et al.[4] and others[9,15,17,25] reported a 300% increase in MTB injuries correlating with the growth in participation. As many as 85% of riders will experience some form of trauma during the season, a fact that is consistent across all forms of cycling.[4,9] As expected, several studies have also revealed a seasonal increase in MTB trauma during the summer with increasing rider activity.[9,13] Compared with on-road biking, children on mountain bikes are particularly exposed to a higher risk for trauma, resulting in more fractures, dislocations, concussions and a greater risk for hospitalization due to off-road crashes.[26-29] Although the specific numbers of youth cases are not always specifically defined, it is estimated that during the course of 1 year, a mountain biker will experience one injury per 1000 hours of competing or training.[15] In 1998, approximately 19 000 MTB injuries were treated at various trauma centres across Austria, primarily consisting of minor injuries with minimal complications.[6] More recently, a New Zealand insurance company reported that MTB injuries made up 14% of total claims and were implicated in 14.8 out of 1000 claimants.[30] Since its introduction in the US, MTB injuries account for ~500 000 visits to the ER throughout the year, with a cost exceeding approximately $US1 billion each year.[16,28,31] Along with minor complications, orthopaedic injuries of the extremities – including fractures, sprains and dislocations – are likely to occur,[4,9,32] with fractures the second most common injury following basic soft tissue wounds among young mountain bikers.[3,5,13,14,17,19,20,25] Although ambiguous due to a lack of available information, there have been reported cases of femoral, tibia-fibula, radio-ulnar and humoral fractures, craniocervical trauma and organ rupture, comprising approximately 20% of all MTB injuries.[5] Due to the limited available data, ª 2010 Adis Data Information BV. All rights reserved.
however, further longitudinal studies are needed to confirm these findings. Because of the prevalence of major injuries, high surgical rates have been reported in up to 66% of total cases.[4] 2.2 Head and Neck Injuries
It is unclear to what extent head and neck injuries occur in young riders; however, due to several underlying factors, i.e. fitness level and behaviour, it has been stated that children involved in cycling activities are at an extremely high risk for cranial trauma, comprising approximately 85% of fatalities.[1,33,34] Injuries may range from minor contusions, lacerations and abrasions to serious trauma involving concussions with concomitant traumatic brain injury, head or neck fracture, and dental trauma.[9,15] Although concussions may be relatively uncommon,[15,20,25] specific cranial trauma, reportedly associated with MTB injuries, bleeding and contusion of the cerebral cortex, cerebellum and brain stem, and dislocation of the incus into the external auditory meatus with subsequent intercranial haemorrhage, do occur.[1,4,9,13,17,25,35] Reports indicate that young cyclists are more likely to experience vomiting, seizures or retrogressive behaviour after just mild head trauma than adults, although the reason for this is disputed in the literature.[4,34,36] The nature of MTB allows many opportunities for numerous facial injuries.[1,14,15,20,35,37] Falling over the handlebars can lead to both soft tissue disruptions and fractures to the face.[1,4] There is the potential for dentoalveolar injuries involving chipped teeth, mandibular alveolar mucosa lacerations, and degloving injuries of the oral mucosa from falling over the handlebars.[1,38-40] Typically under-reported, the cervical spine and associated musculature are one of the most commonly injured areas of the body in off-road cycling, with cervical trauma ranging from muscle strain to fracture, possibly depending on the type of fall sustained.[1,5,17,41-43] Cervical strain may simply occur through increased extension of the neck over a prolonged period.[44] Vertebral fractures and dislocations – with concomitant spinal cord trauma leading to associated neurological Sports Med 2010; 40 (1)
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deficit and paraplegia, regardless of age – have been mentioned.[1,4,5,45] Because of musculoskeletal immaturity, the potential for spinal cord trauma is greater among children than adults; however, the literature regarding this topic is sparse.[46-48] The mechanism of craniocervical trauma typically results from falling forward, usually over the handlebars onto the top of the helmet, as opposed to falls in other directions.[1,3,15,17,45] Although highly recommended, helmets, with or without facial shields, do not always prevent these injuries from occurring.[17,38] For example, Jacobson et al.[27] reported that off-road riders up to 9 years of age had the highest rate of head injuries, whether or not they were helmeted. 2.3 Thoraco-Abdominal Injuries
Trauma to the thoraco-abdominal region has not been extensively documented in children and adolescent riders. The spleen and the liver are the two most commonly injured intra-abdominal organs among all sports.[49] The liver, which is especially susceptible to injury among the paediatric population, is commonly injured because of its abdominal location, as well as its large size.[49] As documented in many traditional bicycle accidents in youths, the spleen and liver are anatomically susceptible to blunt force trauma from handlebars during falls.[6,17] Intrathoracoabdominal cases have involved renal trauma, haemothorax, splenic ruptures, anterior subscapular haematomas of the liver, and diaphragmatic rupture.[1,4-6,49-52] Although the majority of cases are managed conservatively, in a limited number of MTB cases, trauma to the spleen and liver has required surgical intervention 26% and 17% of the time, respectively.[4] Spinal cord injuries may either be partial or comprise cord injuries due to transection, compression or a cord syndrome.[4] Additional injuries to a nerve root may also occur in isolation. These may result in partial injuries or comprise neurological deficit depending on the nature and location of the injury. Scapular fractures occur due to the rider falling to one side, sparing the head and taking the force from the face either to the blade of the scapula or the point of the ª 2010 Adis Data Information BV. All rights reserved.
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shoulder.[3,14,17,25] Contusions and acute muscle strains of the back and abdominal regions is a concern in children because of lower muscle mass and total body strength.[3,14,15,17,49] The potential for chronic lumbar pain has also been reported, with intervertebral disc herniation reported in some cases.[17,25,42-44] 2.4 Upper Extremity Injuries
Upper limb injuries range from either minor dermal abrasions, contusion and muscular strains to complex periarticular fracture dislocations.[4,5,15,25,32,51] These are caused by attempting to arrest the face with an outstretched hand leading to additional direct injury.[1,14,17,53] This trauma can occur regardless of upper body protection.[17] Unfortunately, with the exception of helmet wear, limited recommendations for upper body protection, body armour or wrist protectors have been found in the MTB literature. The majority of suggestions focus on equipment selection such as larger diameter handlebars with modified end/peg attachments, and/or additional MTB padding to minimize potential trauma.[1,6,17,50-52] Common overuse injuries include reported compression from the handlebars and vibration leading to neurovascular complications in the hands.[1,54] These overuse injuries are commonly described as hypothenar hammer syndrome or ulnar artery occlusion, with wrist pain, digital numbness and tingling occurring in 19–35% of cyclists.[1,25,54] Ulnar neuropathy, commonly referred to as ‘handlebar neuropathy’, occurs as a result of ulnar pressure in the canal of Guyon, and is attributed to numbness and weakness in the digits and the palms.[44] Although ulnar neuropathies may exacerbate into permanent nerve damage without immediate treatment, cessation of symptoms has been observed with proper riding technique and bike adjustments.[44] 2.5 Trunk Injuries
Direct friction against the bicycle seat during prolonged MTB activity can lead to perineal complaints such as chafing, perineal folliculitis and furuncles, subcutaneous perineal nodules and urethritis.[2,28,44,55] Infected perineal follicles Sports Med 2010; 40 (1)
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and furuncles, commonly referred to as saddle sores, are the result of obstructed skin glands.[44] Excessive MTB activity may result in skin tag nodules (known as ‘accessory testicles’) and are typically presented posterior to the scrotum.[2,28] The mechanism of injury – repeated microtraumatization to the perineum in conjunction with inadequate shocks and padding on the bicycle – remains the same for both male and female groin trauma.[1,2,16,20,28,56] Based solely on palpation, the incidence of scrotal anomalies among all ages has been reported to account for 45–46% of cases.[2,28] These abnormalities may include scrotal calculi, epididymal cysts, epididymal calcifications, testicular calcifications, hydrocoeles, left-sided varicocoeles, testicular microlithiasis, and inflammation of the tunica vaginalis with concomitant torsion of the appendix testis.[1,16,28] Hydrocoeles are among the most common palpable testicular masses found in male youths.[57] Testicular torsion occurs from the twisting of the testis between the thigh and bike saddle as the leg is moving up and down; if left untreated, it can result in testis loss.[57] Often under-reported, compression of the pudendal nerve may lead to neuropathy with numbness and erectile dysfunction and impotence.[1,16,17,44,57,58] Trauma is not limited to the male population, with female adolescent riders presenting with labial contusions, perineal chafing or dermatitis, and unilateral vulval hypertrophy.[1,16,44,56] 2.6 Lower Extremity Injuries
As with adult competitors, contusions, abrasions, lacerations, gluteal strains, dislocations and fractures may occur among the younger population.[3,16] Although the mechanism of injury dictates the type of injury (i.e. forward falls or overuse), falls off the side of the mountain bike remain the primary mechanism in many cases.[1,17] More serious trauma that evokes immediate attention involves injuries to the pelvis, with external artery occlusion reported in a young adult female mountain biker following repeat pelvic microtrauma.[59,60] This phenomenon can occur regardless of sex in any long-duration activity. ª 2010 Adis Data Information BV. All rights reserved.
Hip and thigh injuries range from minor quadriceps and hamstring strains to more serious fractures.[3,5,14,15,17,61] Failing to disengage the foot from either the clips or pedals can result in a lateral compression force, producing femoral neck, head, pelvic and acetabular fractures.[1,59] Although anecdotal evidence has indicated various injuries to the knee in young mountain bikers, the incidence of specific knee injury among youth in this sport is relatively undocumented in the literature. Again, the choice of reporting system and analyses results in confounded data combining all age groups, which is an area of research concern in this sport. However, patellofemoral pain syndrome, a phenomenon commonly referred to as ‘biker’s knee’, has been observed in both males and females.[44,62-64] This condition may involve anterior knee pain syndrome, patellofemoral malalignment, or chondromalacia patella.[44,63] Irritation of the soft tissues around the front of the knee, with a strained patellar tendon, is fairly common. Often, the condition may be due to patella malalignment, with vigorous biking resulting in excessive stress, wear and breakdown of the cartilage of the patella (chondromalacia patella). Prodromal pain in the underlying bone, inflammation of associated tissues, and synovial membrane irritation are associated with this syndrome.[44,62,63] Additional concerns include the potential for iliotibial band friction syndrome.[44,63] Contributing factors among both sexes include ill-fitted bikes, overuse, muscle-tendon overload from wrong gear selection, inadequate stretching, muscle strength imbalance and, commonly mentioned in female cases, a wider iliotibial band width resulting in increased stress to the tuberosities that the iliotibial band encompasses.[44,63,65] Lacerations, abrasions,[1] calf strains,[14,15,17] and open and closed tibial fractures of the lower leg are typically reported, reflective of the physical challenges faced in this sport.[3,17,25] Although rare, the possibility of compartment syndrome following lower leg impact must be considered as a part of any diagnosis, and aggressively treated in order to prevent nerve and vessel damage to the leg.[65] Foot and ankle trauma, however, is extremely rare among young mountain bikers, although paraesthesia can occur from overly tight toe straps Sports Med 2010; 40 (1)
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and ill-fitting shoes,[15,63] as well as the potential for fracture dislocations of the midfoot due to inability to release the foot during a fall (e.g. Carmont[1]). 2.7 Fatal Injuries
Although reports of fatalities have been mentioned in print media, the overall incidence of fatalities among youth participating in MTB has not been clearly established and may be vastly under-reported.[17] Of those mentioned in the literature, craniocervical injuries and blunt liver trauma remain the leading causes of death, especially among young males.[4,6,15,26,66] 3. Aetiology The primary causes of MTB injuries among children and adolescents include overuse, excessive fatigue, age, skill level, level of experience, and inappropriate or improperly adjusted equipment. Additional factors contributing to trauma among this age group involve musculoskeletal immaturity, excessive speed, environmental conditions, conditioning and fitness status, nonconservative behavioural patterns, and inadequate medical care.[24,37] Although the type and severity of the injury is a function of the rider’s biomechanical efficiency, velocity and trail conditions, it must be stressed that a multiplicative array of intrinsic and extrinsic factors usually simultaneously contribute to trauma.[67-69] 3.1 Overuse and Fatigue
Although approximately 45–90% of all adult mountain bikers will experience overuse and fatigue symptoms, the extent to which they specifically occur among young MTB riders is unknown.[17,20,42,43] The common factor in many overuse cases, however, is simply repeated microtrauma caused by vibration or motions.[20] Fatigue is a contributing factor to injury, resulting in compromised athletic performance and increased predisposition to injury.[10,70] Sports that particularly involve a high degree of eccentric movement, such as MTB, enhance the early onset of fatigue and subsequent musculoskeletal ª 2010 Adis Data Information BV. All rights reserved.
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damage.[10,70,71] This type of muscle damage can also occur in the young mountain biker who suddenly increases the magnitude or intensity of his or her workload or activity.[10,70] Fatigue may result in serious injury, especially in the upper extremities, where repetitive fatigue often causes the cyclist to lose control, release the handlebars due to loss of grip strength, and experience a forward fall.[17] Furthermore, as the sport continues to explode in popularity, the number of young competitors and competitions geared toward youth has increased, further decreasing the amount of time spent recovering between events. Lastly, non-sport-specific conditioning programmes, as well as improper rehabilitation regimens following trauma – may enhance the probability of an overuse injury occurring, as they may be either aggressive or not aggressive enough for the young competitor.[72] This may be especially true when the rehabilitation specialist is unaware of the stresses involved within the specific sport and event.[72] In summary, however, the influence that these factors have on injury has yet to be fully determined among young mountain riders. 3.2 Age, Skill Level and Experience
Age, skill level and experience are major factors in this extremely technical sport. Participants must attain the technical skills at a much younger age in order to adequately control the bike across unpredictable trails.[8,17] With the development of specialized bikes to meet the demands of various events in off-road cycling, it is essential that the young rider be familiar with techniques that optimize what the bike was specifically built for.[18] Other related factors that lead to injury are simple errors in judgment, incorrect riding technique, incorrect braking manoeuvres, and riding on a trail too difficult for one’s level.[9,12,17,20] These factors, along with a higher centre of mass, lead to decreased stability and an increased likelihood of falls among young riders.[12] Unrealistic assessment of actual ability, and inattention to safety and fundamentals of riding, are common among this age group, predisposing the individual to avoidable injury and unnecessary medical attention.[17,20] Sports Med 2010; 40 (1)
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Limited forethought among adolescents tends to cloud judgement, leading to limited use of recommended preventative measures.[10] In addition, with increasing age/maturation associated with physical strength gains and increasing independence, the number of injuries among adolescents compared with children may escalate. There is also an erroneous mindset among adolescents that skill proficiency carries over from one sport to another, e.g. skiing and skateboarding to MTB riding. Inhibitions are therefore decreased, resulting in a possible greater incidence of injury.[10] 3.3 Equipment
The lack of adequate equipment, as well as existing equipment designs, poses challenges among young participants. Handlebars have been the cause of the majority of youth blunt abdominal trauma documented in MTB cases.[50-52,73] Bar ends that are attached to the handlebars for increased comfort and decreased energy expenditure can be extremely dangerous and cause life-threatening intraabdominal injuries.[1,6,20,74] Typically, the tip of the handlebar remains quite small, which concentrates the force and increases the risk of severe lacerations, especially when bar end protection is not maintained.[50-52] The opportunity for direct contact during a fall is increased when straight bar ends are used.[1,15] Researchers have suggested the use of bent and foam-covered bar ends to decrease the risk of liver damage among all forms of cycling.[6,50,51,74] Improper saddle padding, inadequate shock absorbers, and lack of an adequate suspension system enhance the severity of both acute and chronic pelvic/hip trauma.[16,28] Research involving saddle improvement, however, has developed differing designs for male and female riders, encompassing wider widths for females, more pliable cushioning and cutouts.[55] Improper suspension exacerbates the incidence of overuse symptoms in the upper extremity and cervical regions, with sensory pathology in the toes usually attributed to ill-fitting shoes or overly tight toe straps.[9,17,42] The fact that helmet use is lowest among youth across most cycling activities continues to evoke ª 2010 Adis Data Information BV. All rights reserved.
great concern.[9,26,36,75,76] With studies indicating that young cyclists typically wear helmets only half of the time,[9,76] predisposing youth to cranial trauma with concomitant neurological sequelae and death,[63] helmet use remains an important issue within the medical community. Unfortunately, helmets do not always prevent craniofacial injuries.[17,26,38,77] Not surprisingly, any number of standard mechanical problems may occur at a given time, culminating in trauma.[1,3,17,19,26,38] Mechanical failure of brakes, chains, forks, handlebars, pedals, cranks, suspension parts, as well as the tyres, rims and spokes are possible.[9,14,17] Since the sport has grown to encompass several types of events, attempting to perform on a bike not designed for the specific demands of the event is not recommended, but it is often observed, leading to frame and component failure.[17] 3.4 Musculoskeletal Immaturity
The musculoskeletal immaturity of children puts them at a distinct disadvantage and predisposes them to injury, with approximately 15% of clinical sport injuries in children being attributed to inadequate bone growth, skeletal development and musculoskeletal imbalance.[7,10,12,53,78] Although MTB activity in moderation may provide a positive stress to the musculoskeletal system, increasing both muscle and bone mass, the forces acting on the skeleton during the growth stages are already significant and, with the addition of muscle contractile forces during intense physical activity, the exponential combination of stressors acting on the young skeleton, often accentuates the potential for injury.[79] 3.5 Excessive Speed
Excessive speed, unreliable terrain and steep slopes ultimately enhance the probability of loss of control and subsequent falls with little time to react, regardless of experience level.[5,8,15,17] With the higher speeds sustained while riding downhill, the magnitude of force also increases the severity of trauma following a fall.[15,17] Further research is warranted to determine what specific role increased speed, as a result of a more forward Sports Med 2010; 40 (1)
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centre of gravity in combination with rapid deceleration, contributes to the incidence and severity of trauma.[3,4,14,17,20] 3.6 Environmental Conditions
Environmental conditions, such as new or slippery terrain, continually challenge the rider throughout the course.[9,15] Sharp curves, manmade structures such as stairs, and unexpected obstacles such as scree, uneven surfaces and simply water test a cyclist’s steadiness to maintain control and prevent mistakes.[1,9,15,18,20] Although these obstacles are a hallmark of the sport and contribute to its thrilling nature, whether the young rider can properly manage these conditions largely determines the potential and severity of injury.[17] 3.7 Conditioning and Fitness Status
Limited research has been focused on the conditioning and fitness requirements of this sport, especially among young riders.[17] However, a lack of upper body strength in young and, obviously, untrained participants as documented in numerous other sport studies predisposes the individual to a higher prevalence of injury.[10,17,80] Prepubescent riders exhibit little to no gender differences in physical capacity, somatotype, strength or oxygen female riders, transport ability.[64] Postpubertal . however, exhibit a lower VO2max than males, even when adjusted for bodyweight. This decreased aerobic capability is due to less muscle mass and subsequent lower number of mitochondria. Therefore, excessive fatigue and low initial muscle strength due to inadequate conditioning in females may precipitate the potential for musculoskeletal trauma.[64] The distinct events in MTB require specific physical skills and an understanding of training to meet event-specific demands.[8] Primarily, this sport requires both aerobic and anaerobic capacities, and overall body strength and flexibility.[18] The absence of any of these factors will increase injury risk. Prior to high altitude riding and competition, regardless of fitness level, off-road mountain cyclists should consider a period of acclimatization to minimize potential injurycausing effects of acute mountain sickness.[20] ª 2010 Adis Data Information BV. All rights reserved.
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Lastly, regarding injury exposure, an increase in the number of injuries is directly correlated with the number of hours competing or training.[9,17,19] A 1993 study revealed that athletes who rode 7.8 versus 6.3 h/wk were more likely to be seriously injured.[9] In most studies, however, the relationship between training time and incidence of injury in MTB has not been adequately addressed. 3.8 Behaviour
Maladaptive behaviour among young cyclists continues to be a challenge. Younger cyclists are less likely to wear helmets because peer pressure leads them to believe they are ‘uncool’, and therefore young riders have consistently been shown to be less likely to wear protective headgear.[9,26,27,29,36,75] Lack of attention, loss of control, indecisiveness and an unrealistic appraisal of ability are considered to cause the majority of cycle accidents.[9,15,20] Lack of knowledge about proper riding technique, improper landing technique and excess brake application exacerbate the potential for forward falls.[3,17] As observed in other sport activities, inadequate proprioception, slow reaction and response time, and lack of agility are indices of an undeveloped neuromuscular system typically observed with preadolescent mountain bikers.[10,12] Male adolescent riders may select descent routes or tracks beyond their experience level or may engage in unhealthy behaviours such as drinking alcohol or smoking marijuana.[9,17] Male riders tend to comprise the majority of trauma cases because they are more likely to be aggressive, demanding and daring in their sport activities than females.[4,33,81] On the other hand, males participating in outdoor sports, such as MTB, are more likely to attain higher levels of concentration, motivation, self-confidence and proprioception than females, possibly enhancing performance.[81] 3.9 Challenges in Medical Care
The phenomenon of delayed symptoms in children with traumatic injuries is of concern. Often, the lack of appreciation of the severity of Sports Med 2010; 40 (1)
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the specific trauma leads to insufficient medical care by both the attending physician and the patient. One study reported that several young BMX riders were sent home following incomplete medical checks, resulting in serious increased pain, vomiting and collapse.[73] In addition, among all trauma cases, preventable deaths are attributed to overlooking maxillofacial injury leading to airway obstruction and blunt abdominal patterns leading to intra-abdominal bleeding – two common events in MTB activities.[46,52] With reference to scrotal injury, mild and severe injuries usually present similarly, and delayed presentation may occur due to the patient’s reluctance to seek medical attention.[82] Interestingly, of those initially seeking medical attention, only half of injured cyclists attend a follow-up examination following their initial injury.[15] 4. Limitations Despite extensive efforts to provide a comprehensive picture of the aetiology of injury among young mountain bike enthusiasts, data collection challenges do exist and continue to be a concern in most MTB injury studies. Even more disconcerting are the limitations found in most MTB studies with children that severely hamper the ability to fathom the totality of trauma actually occurring.[22] These limitations include inaccurate delineation of age and sex, a participant’s lack of injury awareness, data collection criteria and source, and predisposing factors prior to injury. As previously mentioned, limited data have been collected on children and adolescents, and of those published, there has been little effort in delineating youth trauma from adult cases. The issue of sex also causes great concern, as females are extremely under-represented in many studies.[3,5,8,15,17,37] Although young males consistently experience more injury than young females,[26,29,33,34,36,53] female riders are automatically predisposed to injury in this sport because of lighter bodyweight, the possibility of lower bone mineral density, and lower upper body strength than males.[1,9,14,15,64] The increased likelihood of injuries in females may also be attributed to their lower level of experience[18,83] and ª 2010 Adis Data Information BV. All rights reserved.
increased likelihood of loss of control.[14,17] Compared with males, females are two times more likely to experience trauma and four times more likely to sustain a fracture.[14,17] Variations in somatotype and build – i.e. leg length discrepancy, pelvic width and tibial torsion – may also predispose an individual to injury.[44,65] Females, with a wider pelvis, increased knee valgus and hip varus angles, as well as decreased shoulder width, are thought to be at an anatomical disadvantage because of the increased likelihood of overuse injury occurring.[64] The source of injury data has been of concern within the last few years as researchers attempt to understand the intricacies that define and lead to unnecessary trauma. Little effort has been focused on when injury precisely occurs with this sport.[1,84,85] Compounding the challenge are the continual incidences of self-treatment and subsequent nonreporting.[1] This has resulted in questionable under-reporting, the inability to monitor trauma patterns, incomplete or ambiguous data, debatable accuracy of diagnosis, and patients lost to follow-up.[1] To remedy these challenges, a few studies have incorporated various forms of follow-up procedures such as telephone interviews and mailed questionnaires. However, as injury recall time increases, memory and consequently validity and reliability of data declines, especially when dealing with parental recall.[1,3,85-87] Other inconsistencies include the definition of injury, the clarification of the terms ‘off-road’ and ‘mountain biking’, and more accurate delineation between recreational and competitive MTB.[1,17,22,26,27] Interestingly, the most under-reported incidence of all may be fatalities.[88] From a sport science standpoint, very few articles have been published on the physiology and nutritional requirements of MTB,[8] with studies primarily focused on older competitors. In addition, the lack of adequate nutrition and hydration, when combined with extremely dry conditions, may also lead to injury due to perceived inconvenience during long races.[8] In summary, although specific indices associated with injuries have been addressed in the literature, prior studies have indicated the limitations in attempting to isolate the extensive array of Sports Med 2010; 40 (1)
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intrinsic and extrinsic factors that predispose the young mountain cyclist to injury. The full scope of the effect that MTB has on children, however, cannot be adequately understood until specific studies are conducted on this growing sport population. 5. Prevention 5.1 Education and Instruction
When revealing injury causation in any sport, one must keep in mind that without risk, the potential for trauma decreases. In the absence of risk, however, there would be little exhilaration and challenge. To achieve a reasonable balance, prior studies have suggested that young or beginner off-road cyclists should attend an educational course taught by a certified mountain bike instructor.[4] Although any educational efforts may only minimize but not eliminate trauma, understanding how injuries occur and proper riding technique is crucial in helping to decrease serious injury,[3,16,17,26] with some stressing education as early as in kindergarten children.[29,89,90] These prevention programmes should encompass helmet use, protective equipment, basic bike maintenance prior to riding, and selecting the trail best suited to the level of ability.[1,4,17,29,44,75] Australia has implemented laws within the last decade that require helmet use among on- and off-road cyclists alike.[27] Parents, however, should be educated as well, since parental involvement is crucial to adherence of youth to safety.[26,29] 5.2 Equipment
While many studies indicate that helmets offer significant protection against catastrophic injury, studies indicate that serious trauma still occurs despite helmet use.[4,9,13,25,36] The majority, however, recommend that some form of approved headgear be required at all levels of mountain biking. When used correctly, a helmet with the addition of a face shield decreases the incidence of craniofacial trauma and death.[1,13,15,17,26,35,38,66,76] In addition, mouthguard use may also reduce the risk of dental injury.[10] Despite recommendations, ª 2010 Adis Data Information BV. All rights reserved.
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cyclists find excuses such as the high cost and uncomfortable nature of helmets to deter use.[38,75] Others have observed, as noted in other sports, that protective equipment use would actually increase tactically aggressive behaviour among athletes, resulting in higher velocity impact than present equipment designs could absorb.[10,91,92] Further research efforts are recommended to determine the efficacy and development of a MTBspecific helmet, equipped with a facial shield, at a reasonable price.[17,26] Since handlebars have been implicated in many thoraco-abdominal injuries in youth biking accidents,[50,51] it has been suggested that largediameter handlebars be manufactured with durable rubber grips over the metal, and bent away from the rider.[6,17,50-52] Handlebar end attachments (i.e. pegs) are discouraged and, if used, should have adequate padding and be curved away from the young rider.[1,17,52] To minimize groin and pelvic trauma, a proper saddle and short padding should be worn.[28] Padded gloves and shin guards have also been recommended.[1,20,26,44] Bicycles should be fitted properly, and the saddle should be adjusted to the proper height and angle for the young competitor.[1,28] To prevent impingement of the pudendal nerve, saddles should be engineered to reduce perineal pressure.[1] As previously mentioned, shock-absorbers should be checked and adjusted throughout the season, with full suspension bikes highly recommended.[2,28] Since tyre failure is most commonly associated with injury, both front and back tyres should be checked and monitored before and at various stops throughout the ride.[17] In summary, the use of protective equipment and a suitable mountain bike can reduce the incidence and severity of injuries. Coupled with attention to bike maintenance and reasonable behaviour, MTB can be an enjoyable sport for youth. 5.3 Training and Conditioning
Before attempting the sport of MTB, the fitness status of the individual should be assessed prior to initiating a sport-specific conditioning programme, especially to determine the status of Sports Med 2010; 40 (1)
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the musculoskeletal system.[15,80] Strength-building and coordination exercises are highly recommended before engaging in MTB.[15] A regular training regimen that builds endurance, strengthens the upper body and develops core capacity is crucial to a mountain biker’s ability to stabilize his or her bike and avoid trauma.[14,17] Since mountain bikers commonly participate in activities above the lactate threshold for hours at a time, depending on the skill and age level, a high level of training intensity may be required.[1,8] In addition to focusing on optimal hydration, a balanced diet with adequate protein, as well as feeding throughout long events, is essential to meet the demands of recovery as well as ensure the nutritional requirements of the growing child and adolescent.[8] Additional youth-specific research efforts in training, conditioning and nutrition have been recommended to provide a realistic opportunity to successfully participate with minimal potential for trauma.[8,14,17] 5.4 Environmental Management
It has been recommended that trails be rated according to level of difficulty, while being closely monitored for optimal safety.[4,17] When designing trails, attention should be directed toward an optimal environment that balances performance enhancement with adequate safety. As with other sports, a challenging course can still be reasonably safe. However, the ultimate responsibility lies in the hands of both parents and the cyclist, since it would be impossible for every trail to be monitored at all times.[17] 6. Conclusion The number of youth participants has dramatically increased in MTB. With an increasing number of participants in any sport, a concomitant potential for injury is likely to occur. Although injury is eminent among children and adolescents, incorporating MTB education, proper instruction and equipment, and an adequate level of fitness and training are recommended to decrease the prevalence of trauma. It is hoped that future research efforts will be focused toward recreational ª 2010 Adis Data Information BV. All rights reserved.
riders, as they comprise the majority of participants. In addition, a clearer and more comprehensive approach to injury reporting and efforts toward research specifically directed towards young riders will improve the opportunity to adequately understand the scope and severity of youth MTB injuries, as well as enhance optimal performance and long-term enjoyment in this outdoor sport. Acknowledgements Financial support for this review was provided by the McNair Scholars Program at West Texas A&M University, which is funded by the US Department of Education. The authors have no conflicts of interest that are directly relevant to the content of this review.
References 1. Carmont MR. Mountain biking injuries: a review. Br Med Bull 2008; 85: 101-12 2. Frauscher F, Klauser A, Hobisch A, et al. Subclinical microtraumatisation of the scrotal contents in extreme mountain biking. Lancet 2000; 356 (9239): 1414 3. Chow TK, Kronisch RL. Mechanisms of injury in competitive off-road bicycling. Wilderness Environ Med 2002; 13: 27-30 4. Kim PTW, Jangra D, Ritchie AH, et al. Mountain biking injuries requiring trauma centre admission. J Trauma 2006; 60: 312-8 5. Jeys LM, Cribb G, Toms AD, et al. Mountain biking injuries in rural England. Br J Sports Med 2001; 35: 197-9 6. Nehoda H, Hochleitner K, Hourmont K, et al. Central liver hematomas caused by mountain-bike crashes. Injury 2001; 32 (4): 285-87 7. Bicycle Wholesale Distributors Association. Sales report. Washington, DC: Bicycle Federation of America, 1990 8. Impellizzeri FM, Marcora SM. The physiology of mountain biking. Sports Med 2007; 37 (1): 59-71 9. Chow T, Bracker M, Patrick P. Acute injuries from mountain biking. West J Med 1993; 156 (2): 145-8 10. Meyers MC, Laurent Jr CM, Higgins RW, et al. Downhill ski injuries in children and adolescents. Sports Med 2007; 37 (6): 485-99 11. USA Cycling. Colorado Springs (CO): USA Cycling, 2001 12. Fountain JL, Meyers MC. Skateboarding injuries. Sports Med 1996; 22 (6): 360-6 13. Rivara FP, Thompson DC, Thompson RD, et al. Injuries involving off-road cycling. J Fam Pract 1997; 44 (5): 481-5 14. Kronisch RL, Pfeffier RP, Chow TK, et al. Gender differences in acute mountain bike racing injuries. Clin J Sport Med 2002; 12 (3): 158-64 15. Gaulrapp H, Weber A, Rosemeyer B. Injuries in mountain biking. Knee Surg Sports Traumatol Arthrosc 2001; 9: 48-53
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Mountain Biking Injuries in Youth
16. Mitterberger M, Pinggera GM, Neuwirt H, et al. Do mountain bikers have a higher risk of scrotal disorders than on-road cyclists? Clin J Sport Med 2008; 18 (1): 49-54 17. Kronisch RL, Pfeiffer RP. Mountain biking injuries: an update. Sports Med 2002; 32: 523-7 18. Pfeiffer RP. Off-road bicycle racing injuries: the NORBA pro/elite category. Clin Sports Med 1994; 13 (1): 201-17 19. Kronisch RL, Pfeiffer RP, Chow TK. Acute injuries in cross country and downhill off-road bicycle racing. Med Sci Sports Exerc 1996; 28 (11): 1351-5 20. Pfeiffer RP, Kronisch RL. Off-road cycling injuries: an overview. Sports Med 1995; 19 (5): 311-25 21. International Olympic Committee. The Games of the XXXVIII Olympiad mountain bike official results book. Lausanne: International Olympic Committee, 2000 22. Van Mechelen W, Hlobil H, Kemper HCG. Incidence, severity, aetiology and prevention of sports injuries: a review of concepts. Sports Med 1992; 14 (2): 82-99 23. Walter SD, Sutton JR, McIntosh JM, et al. The aetiology of sports injuries: a review of methodologies. Sports Med 1985; 2 (1): 47-58 24. Wilkins KE, Aroojis AJ. The present status of children’s fractures. In: Beaty JH, Kasser JR, editors. Rockwood and Wilkins’ fractures in children. Philadelphia (PA): Lippincott, Williams and Wilkins, 2001: 13-5 25. Kronisch RL, Rubin AL. Traumatic injuries in off-road bicycling. Clin J Sport Med 1994; 4: 240-4 26. Acton CHC, Thomas S, Nixon JW, et al. Children and bicycles: what is really happening? Studies of fatal and non-fatal bicycle injury. Inj Prev 1995; 1 (2): 86-91 27. Jacobson GA, Blizzard L, Dwyer T. Bicycle injuries: road trauma is not the only concern. Aust NZ J Public Health 1998; 22 (4): 451-5 28. Frauscher F, Klauser A, Stenzl A, et al. US findings in the scrotum of extreme mountain bikers. Radiology 2001; 219 (2): 427-31 29. Cushman R, Down J, MacMillan N, et al. Bicycle-related injuries: a survey in pediatric emergency department. Can Med Assoc J 1990; 143 (2): 108-12 30. Bentley T, Macky K, Edwards J. Injuries to New Zealanders participating in adventure tourism and adventure sports: an analysis of Accident Compensation Corporation (ACC) claims. NZ Med J 2006; 119 (1247): U2359 31. Sacks JJ, Holmgreen P, Smith SM, et al. Bicycle-associated head injuries and deaths in the United States from 1984 through 1988: how many are preventable? JAMA 1991; 266: 3016-8 32. Rajapaske BN, Horn G, Devane P. Forearm and wrist fractures in mountain bike riders. N Z Med J 1996; 109 (1020): 147-8 33. Kelly KD, Lissel HL, Rowe BH, et al. Sport and recreationrelated head injuries treated in the emergency department. Clin J Sports Med 2001; 11 (2): 77-81 34. Ivan LP, Choo SH, Ventureyra EC. Head injuries in childhood: a 2-year survey. Can Med Assoc J 1983; 128: 281-4 35. Chow TK, Corbett S, Farstad D. Do conventional helmets provide adequate protection in mountain biking? Wilderness Environ Med 1995; 6: 385-90
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36. O’Rourke NA, Costello F, Yelland JDN, et al. Head injuries to children riding bicycles. Med J Aust 1987; 146: 619-21 37. Gassner RJ, Jackl W, Tuli T, et al. Differential profile of facial injuries among mountainbikers compared with bicyclists. J Trauma 1999; 47 (1): 50-4 38. Revuelta R, Sandor GKB. Degloving injury of the mandibular mucosa following an extreme sport accident: a case report. J Dent Child 2005; 72 (3): 104-6 39. Dula DJ, Leicht MJ, Moothart WE. Degloving injury of the mandible. Ann Emerg Med 1984; 13: 630-2 40. Shockledge R, Mackie I. Oral soft tissue trauma: gingival degloving. Endod Dent Traumatol 1996; 12 (2): 109-11 41. Allen Jr BL, Ferguson RL, Lehmann TR, et al. A mechanistic classification of closed, indirect fractures and dislocations of the lower cervical spine. Spine 1982; 7 (1): 1-27 42. Frobose I, Lucker B, Wittman K. Overuse symptoms in mountainbikers: a study with an empirical questionnaire [in German]. Dtsch Z Sportmed 2001; 52 (11): 311-5 43. Dingerkus ML, Martinek V, Kolzow I, et al. Mountainbike related injuries and overuse syndromes [in German]. Dtsch Z Sportmed 1998; 49 (8): 242-4 44. Baker A. Cycling. In: Garrett Jr WE, Kirkendall DT, Squire DL, editors. Principles and practice of primary care in sports medicine. Philadelphia (PA): Lippincott, Williams and Wilkins, 2001: 453-70 45. Aspingi S, Dussa CU, Soni BM. Acute cervical spine injuries in mountain biking. Am J Sports Med 2006; 34: 487-9 46. Jaffe D, Wesson D. Emergency management of blunt trauma in children. N Engl J Med 1991; 243 (21): 1477-82 47. Kewalaramani LS, Kraus JF, Sterling HM. Acute spinal cord lesions in a pediatric population: epidemiological and clinical features. Paraplegia 1980; 18 (3): 206-19 48. Hubbard DD. Injuries of the spine in children and adolescents. Clin Orthop 1974; 100: 56-65 49. Chang CJ, Lin HC, Pryde JA. Abdominal injuries. In: Garrett Jr WE, Kirkendall DT, Squire DL, editors. Principles and practice of primary care in sports medicine. Philadelphia (PA): Lippincott, Williams and Wilkins, 2001: 353-72 50. Acton CH, Thomas S, Clark R, et al. Bicycle accidents in children: abdominal trauma and handlebars. Med J Aust 1994; 160: 344-6 51. Clarnette TD, Beasely SW. Handlebar injuries in children: patterns and prevention. Aust NZ J Surg 1997; 67: 338-9 52. Winston FK, Shaw KN, Kreshak AA, et al. Hidden spears: handlebars as injury hazards to children. Pediatrics 1998; 102 (3): 596-601 53. Maffulli N, Baxter-Jones AD. Common skeletal injuries in young athletes. Sports Med 1995; 19 (2): 137-49 54. Applegate KE, Speigel PK. Ulnar artery occlusion in mountain bikers. J Sports Med Phys Fit 1995; 35: 232-4 55. Potter JJ, Sauer JL, Weisshaar CL, et al. Gender difference in bicycle saddle pressure distribution during seated cycling. Med Sci Sports Exerc 2008; 40 (6): 1126-34 56. Humphries D. Unilateral vulval hypertrophy in competitive female cyclists. Br J Sports Med 2002; 36: 463-4 57. Nichols AW. Genital injuries in sports. In: Garrett Jr WE, Kirkendall DT, Squire DL, editors. Principles and practice
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of primary care in sports medicine. Philadelphia (PA): Lippincott, Williams and Wilkins, 2001: 373-80 Oberpenning F, Roth S, Leusmann DB, et al. The Alcock syndrome: temporary penile insensitivity due to compression of the pudendal nerve within the Alcock canal. J Urol 1994; 151: 423-5 Barnett B. More on mountain biking [letter]. West J Med 1993; 159 (6): 708 Korsten-Reck U, Rocker K, Schmidt-Trucksass A, et al. External iliac artery occlusion in a young female cyclist. J Sports Med Phys Fit 2007; 47: 91-5 Habernek H, Schmid L, Frauenschuh E. Sport related proximal femur fracture: a retrospective review of 31 cases treated in an eight year period. Br J Sports Med 2000; 34: 54-8 Hughston JC, Walsh WM, Puddu G. Patellar subluxation and dislocation. Philadelphia (PA): WB Saunders, 1984 Mellion MD. Common cycling injuries: management and preventions. Sports Med 1991; 11 (1): 52-70 Nattiv A, Arendt EA, Hecht SS. The female athlete. In: Garrett Jr WE, Kirkendall DT, Squire DL, editors. Principles and practice of primary care in sports medicine. Philadelphia (PA): Lippincott, Williams and Wilkins, 2001: 93-113 Whiting WC, Zernicke RF, editors. Biomechanics of musculoskeletal injury. Champaign (IL): Human Kinetics, 2008 McDermott FT. The effectiveness of bicyclists’ helmets: a study of 1710 casualties. J Trauma 1993; 34 (6): 834-45 Natri A, Johnson RJ. Skiing. In: Garrett Jr WE, Kirkendall DT, Squire DL, editors. Principles and practice of primary care in sports medicine. Philadelphia (PA): Lippincott, Williams and Wilkins, 2001: 553-61 Gissane C, White J, Kerr K, et al. An operational model to investigate contact sports injuries. Med Sci Sports Exerc 2001; 33 (12): 1999-2003 Meeuwisse WH. Assessing causation in sports injury: a multifactorial model. Clin J Sports Med 1994; 4: 166-70 Appell HJ, Soares JM, Duarte JA. Exercise, muscle damage, and fatigue. Sports Med 1992; 13: 108-15 Watson AWS. Sports injuries: incidence, causes, and prevention. Phys Ther Rev 1997; 27: 315-22 Haas JC, Meyers MC. Rock climbing injuries. Sports Med 1995; 20 (3): 199-205 Sparnon A, Ford W. Bicycle handlebars in children. J Pediatr Surg 1986; 21 (12): 118-9 Alvarez-Segui M, Castello-Ponce A, Verdu-Pascual F. A dangerous design for a mountain bike. Int J Legal Med 2001 Dec; 115: 165-6 Weiss B. Bicycle helmet use by children. Pediatrics 1986; 77 (5): 677-9
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76. Wasserman RC, Ruccini RV. Helmet protection from head injuries among recreational bicyclists. Am J Sports Med 1990; 18: 96-7 77. Thompson DC, Nunn ME, Thompson RS, et al. Effectiveness of bicycle safety helmets in preventing serious facial injury. JAMA 1996; 276 (24): 1974-5 78. Kozin SH. Fractures and dislocations along the pediatric thumb ray. Hand Clin 2006; 22 (1): 19-29 79. Daly RM, Stenevi-Lundgren S, Linden C, et al. Muscle determinants of bone mass, geometry and strength in prepubertal girls. Med Sci Sports Exerc 2008; 40 (6): 1135-41 80. Kibler WB, Chandler TJ, Uhi T, et al. A musculoskeletal approach to the preparticipation physical examination. Am J Sports Med 1989; 17 (4): 525-31 81. Trafton Jr TA, Meyers MC, Skelly WA. Psychological characteristics of the telemark skier. J Sport Behav 1997; 20 (4): 465-76 82. Bhatt S, Dogra VS. Role of US in testicular and scrotal trauma. Radiographics 2008; 28 (6): 1616-29 83. Pfeiffer RP. Injuries in NORBA pro/elite category off-road bicycle competitors. Cycling Sci 1993; 5 (1): 21-4 84. Noyes FR, Lindenfeld TN, Marshall MT. What determines an athletic injury (definition)? Who determines an injury (occurrence)? Am J Sports Med 1988; 16 Suppl. 1: S65-8 85. Harel Y, Overpeck MD, Jones D, et al. The effects of recall on estimating annual nonfatal injury rates for children and adolescents. Am J Public Health 1994; 84: 599-605 86. Junge A, Dvorak J. Influence of definition and data collection on the incidence of injuries in football. Am J Sports Med 2000; 28 (5): S40-6 87. Pless CE, Pless IB. How well they remember: the accuracy of parental reports. Arch Pediatr Adolesc Med 1995; 149: 553-8 88. Baker SP, O’Neill B, Karpf R. The injury fact book. Toronto (ON): Lexington Books, 1984 89. Fife D, Davis J, Tate L, et al. Fatal injuries to bicyclists: the experience of Dade County, Florida. J Trauma 1983; 23 (8): 745-55 90. Howland J, Sargent J, Weltzman M, et al. Barriers to bicycle helmet use among children. Am J Dis Child 1989; 143: 741-4 91. Parkkari J, Kujala UM, Kannus P. Is it possible to prevent sports injuries? Review of controlled clinical trials and recommendations for future work. Sports Med 2001; 31 (14): 985-95 92. Hagel BE, Meeuwisse W. Risk compensation: a side effect of sport injury prevention? Clin J Sports Med 2004; 14: 193-6
Correspondence: Kylee B. Aleman, 4700 Easely Place, Amarillo, TX 79119, USA. E-mail:
[email protected]
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CORRESPONDENCE
Sports Med 2010; 40 (1): 91-94 0112-1642/10/0001-0091/$49.95/0
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The Central Governor Model Cannot be Adequately Tested by Observing its Components in Isolation In a recent issue of Sports Medicine, a current opinion article was published entitled ‘‘Is it Time to Retire the ‘Central Governor’?’’ in which the author Roy Shephard concluded that, based on a lack of experimental evidence, the Central Governor Model (CGM) should be treated with scepticism.[1] In the opening few pages of the article Shephard provides a concise overview of CGM before claiming that the CGM is ‘‘y hampered by the absence of a systematic and clearly enunciated listing of its inherent correlates.’’ Although this statement is to some extent true, it should be pointed out that the apparent lack of detailed evidence to which Shephard refers is perhaps a reflection of CGM ‘complexity’, which, in fairness to Noakes and his colleagues, is something that they have repeatedly acknowledged.[2-5] The complexity of CGM, involving feed forward muscular control derived from the integration of numerous afferent peripheral signals, presents considerable methodological challenges that, for the time being at least, leaves Noakes in the rather difficult scientific position of having to defend his model with only partial and inconclusive evidence. Attempts to discredit the CGM, which are summarized in Shephard’s article, have largely been deduced from empirical observations of component physiological systems that, despite being isolated from the CNS, exhibit self-limiting functions. However, we should be cautious about rejecting the CGM based upon such deductions because this approach essentially disregards the complex physiological, neurological and psychological interactions that model proposes and therefore does not constitute a sufficiently rigorous test. For instance, one of the claims made by Shephard is that a central governor is not needed because of
a study[6] that showed gradual rather than catastrophic reduction in the force production of locally stimulated soleus muscles. In fact, all that can really be interpreted from this study is that locally stimulated muscles gradually fatigue. The study does not provide any definitive evidence to rule out the existence of a central governor further up the neurological chain since the lack of attenuation of efferent command when a locally stimulated muscle becomes fatigued could be explained by the absence of other afferent signals that are usually present during ‘whole body’ exercise to represent changes in temperature, oxygen uptake, substrate availability and pH to name a few. Under such circumstances it is of no surprise that the efferent signal was not attenuated since the failure of single locally stimulated muscle does not really threaten overall homeostasis of the body and therefore does not test what Noakes et al. have proposed is the main purpose of the central governor.[2-5] In other words, the apparent normality of isolated CGM components should not be used as evidence against the model because it does not reflect the inherent complexity of Noakes’ model that, with time and methodological advances, might yet be proved correct. Another approach to oppose CGM that has been recently adopted is to draw on the evidence of evolutionary studies. Shephard suggests that there is little evidence for selective pressures that would lead to the evolution of a ‘central governor’ in humans. He suggests that hunting skills are acquired during adult life, and that this would mitigate against the genetic transmission of skills since reproduction occurs early in adult life. Of course, no acquired characteristics can be genetically transmitted, irrespective of when in life their acquisition takes place. Abilities are genetically transmitted, not skills, which are always learnt, and in our own recent work we have shown the importance of how experience and learning help athletes to make sense of present events and pace themselves appropriately in order to avoid premature fatigue during exercise.[7] To state that a central governor could not have evolved because the associated phenotype is often not present until later life
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represents a contradiction to the theory of evolution by natural selection. Shephard also suggests that certain bushmen survive despite working for only 2.2 days a week, and that, therefore, an individual with characteristics that are poorly adapted to their environment could survive by increasing the proportion of the week that they engage in hunting activities. Prey and, therefore, hunting opportunities may not be abundant, however, and so a poorly adapted individual may find himself out-competed for the available resources. The poorly adapted individual may also find mating opportunities more difficult to come by as a result of selection by potential mates. Either by lower survival rates due to less hunting success or by reduced mating opportunities, a process of differential reproduction will take place that over generations could lead to the eradication of even small differences that convey a disadvantage to individual organisms. Neuroscience provides evidence for the evolution of afferent neural pathways in primates that are absent in sub-primates and that are especially developed in humans, which provide a mechanism for enhanced awareness of bodily processes and their homeostatic control.[8,9] Since this pathway exists in primates only we can infer that evolutionary selective pressures that have led to physical structures for enhanced interoception must have existed and that these structures must contribute to the survival of the organisms possessing them. In a recent commentary, Duhamel (Amann et al.[10]) reminds us that it is imperative that exercise physiologists employ an integrative biology approach to characterize peripheral as well as central fatigue processes, rather than resort to reductionism, and only by considering the behaviour of the whole organism can we hope to gain an understanding of the limitations to human performance. Shephard’s article constitutes an interesting development in the ongoing debate about fatigue during exercise, although, for the reasons we have outlined in this letter, the CGM should not be retired until new and compelling integrative neurophysiological evidence is forthcoming to suggest otherwise. ª 2010 Adis Data Information BV. All rights reserved.
Letter to the Editor
Dominic Micklewright and David Parry Department of Biological Sciences, University of Essex, Colchester, Essex, UK
Acknowledgements The authors have no conflicts of interest that are directly relevant to the content of this letter.
References 1. Shephard RJ. Is it time to retire the ‘Central Governor’? Sports Med 2009; 39 (9): 709-21 2. Noakes TD, St Clair Gibson A, Lambert EV. From catastrophe to complexity: a novel model of integrative central neural regulation of effort and fatigue during exercise in humans: summary and conclusions. Br J Sports Med 2006; 39: 120-4 3. St Clair Gibson A, Noakes TD. Evidence for complex system integration and dynamic neural regulation of skeletal muscle recruitment during exercise in humans. Br J Sports Med 2004; 38: 797-806 4. Lambert EV, St Clair Gibson A, Noakes TD. Complex systems model of fatigue: integrative homeostatic control of peripheral physiological systems during exercise in humans. Br J Sports Med 2005; 39: 52-62 5. Noakes TD, St Clair Gibson A, Lambert EV. From catastrophe to complexity: a novel model of integrative central neural regulation of effort and fatigue during exercise in humans. Br J Sports Med 2004; 38: 511-4 6. Garland SJ, McComas A. Reflex inhibition of human soleus muscle during fatigue. J Physiol 1990; 429: 17-27 7. Micklewright D, Papadopoulou E, Swart J, et al. Previous experience influences pacing during 20-km time trial cycling. Br J Sports Med. Epub 2009 Apr 12 8. Craig AD. How do you feel? Interoception: the sense of the physiological condition of the body. Nature Neurosci 2002; 3: 655-66 9. Craig AD. A new view of pain as a homeostatic emotion. Trends Neuosci 2003; 26 (6): 303-7 10. Amann M, Marcora SM, Nybo L, et al. Commentaries on viewpoint. Fatigue mechanisms determining exercise performance: integrative physiology is systems physiology. J App Physiol 2008; 104: 1543-6
The Author’s Reply I would like to thank Drs Micklewright and Parry for their interest in my recent comments on the ‘Central Governor’ hypothesis.[1] In my brief article, I had noted the current absence of Sports Med 2010; 40 (1)
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represents a contradiction to the theory of evolution by natural selection. Shephard also suggests that certain bushmen survive despite working for only 2.2 days a week, and that, therefore, an individual with characteristics that are poorly adapted to their environment could survive by increasing the proportion of the week that they engage in hunting activities. Prey and, therefore, hunting opportunities may not be abundant, however, and so a poorly adapted individual may find himself out-competed for the available resources. The poorly adapted individual may also find mating opportunities more difficult to come by as a result of selection by potential mates. Either by lower survival rates due to less hunting success or by reduced mating opportunities, a process of differential reproduction will take place that over generations could lead to the eradication of even small differences that convey a disadvantage to individual organisms. Neuroscience provides evidence for the evolution of afferent neural pathways in primates that are absent in sub-primates and that are especially developed in humans, which provide a mechanism for enhanced awareness of bodily processes and their homeostatic control.[8,9] Since this pathway exists in primates only we can infer that evolutionary selective pressures that have led to physical structures for enhanced interoception must have existed and that these structures must contribute to the survival of the organisms possessing them. In a recent commentary, Duhamel (Amann et al.[10]) reminds us that it is imperative that exercise physiologists employ an integrative biology approach to characterize peripheral as well as central fatigue processes, rather than resort to reductionism, and only by considering the behaviour of the whole organism can we hope to gain an understanding of the limitations to human performance. Shephard’s article constitutes an interesting development in the ongoing debate about fatigue during exercise, although, for the reasons we have outlined in this letter, the CGM should not be retired until new and compelling integrative neurophysiological evidence is forthcoming to suggest otherwise. ª 2010 Adis Data Information BV. All rights reserved.
Letter to the Editor
Dominic Micklewright and David Parry Department of Biological Sciences, University of Essex, Colchester, Essex, UK
Acknowledgements The authors have no conflicts of interest that are directly relevant to the content of this letter.
References 1. Shephard RJ. Is it time to retire the ‘Central Governor’? Sports Med 2009; 39 (9): 709-21 2. Noakes TD, St Clair Gibson A, Lambert EV. From catastrophe to complexity: a novel model of integrative central neural regulation of effort and fatigue during exercise in humans: summary and conclusions. Br J Sports Med 2006; 39: 120-4 3. St Clair Gibson A, Noakes TD. Evidence for complex system integration and dynamic neural regulation of skeletal muscle recruitment during exercise in humans. Br J Sports Med 2004; 38: 797-806 4. Lambert EV, St Clair Gibson A, Noakes TD. Complex systems model of fatigue: integrative homeostatic control of peripheral physiological systems during exercise in humans. Br J Sports Med 2005; 39: 52-62 5. Noakes TD, St Clair Gibson A, Lambert EV. From catastrophe to complexity: a novel model of integrative central neural regulation of effort and fatigue during exercise in humans. Br J Sports Med 2004; 38: 511-4 6. Garland SJ, McComas A. Reflex inhibition of human soleus muscle during fatigue. J Physiol 1990; 429: 17-27 7. Micklewright D, Papadopoulou E, Swart J, et al. Previous experience influences pacing during 20-km time trial cycling. Br J Sports Med. Epub 2009 Apr 12 8. Craig AD. How do you feel? Interoception: the sense of the physiological condition of the body. Nature Neurosci 2002; 3: 655-66 9. Craig AD. A new view of pain as a homeostatic emotion. Trends Neuosci 2003; 26 (6): 303-7 10. Amann M, Marcora SM, Nybo L, et al. Commentaries on viewpoint. Fatigue mechanisms determining exercise performance: integrative physiology is systems physiology. J App Physiol 2008; 104: 1543-6
The Author’s Reply I would like to thank Drs Micklewright and Parry for their interest in my recent comments on the ‘Central Governor’ hypothesis.[1] In my brief article, I had noted the current absence of Sports Med 2010; 40 (1)
Letter to the Editor
experimental evidence supporting the hypothesis and I had pointed out that several likely correlates of any such governor were lacking. I thus suggested that it might be appropriate to halt the plethora of papers that one laboratory was writing to promote the hypothesis – at least until some definitive evidence was adduced to support their views. This, surely, is the method of science – the formulation of a plausible and testable hypothesis, with early proof or rejection by an appropriately designed experiment. I am reminded of an incident I witnessed at the British Physiological Society during the early 1950s. Members of that august body can voice brief (9.9 minute) communications to the Society on a topic of their choice, but the members of the Society then spend 5 minutes in public debate, deciding whether to accept and publish or to reject a brief abstract of the presentation. At the meeting in question, a member of the Society advanced a rather dubious hypothesis, and an elderly Scottish professor quickly took the floor at the end of his talk. ‘‘Sir,’’ he roared, ‘‘You have every right to believe that the moon is made of blue cheese if you so choose, but until you have gathered proof of this, you should not waste the time of this Society with your hypothesis.’’ He was perhaps taking an extreme view. Most of us welcome new ideas, including the ‘Central Governor’ hypothesis, as a challenge to our experimental ingenuity. But 13 or 14 years after its promulgation, I sense a similar need for hard evidence to support continued discussion of the ‘Central Governor’ hypothesis. I would agree with Micklewright and Parry that the identification of specific centres within the CNS is no easy matter. Nevertheless, the painstaking experimental work of neurophysiologists has been successful in identifying both the location and the mechanics of centres regulating vital functions such as respiration. If there is indeed a ‘Central Governor’, could it not be similarly identified and located by the application of such techniques as the micro-stimulation and/or ablation of various brain regions in experimental animals? I am somewhat puzzled by the importance that Micklewright and Parry attribute to afferent information. One or two other recent papers on the ª 2010 Adis Data Information BV. All rights reserved.
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‘Central Governor’ have also begun to stress the issue of afferent input; indeed, I wonder if the ‘Central Governor’ is not about to undergo another chameleon-like metamorphosis? In its original version, the hypothesis suggested that the brain had an intrinsic knowledge of a ‘safe’ level of physical activity, presumably gained through the evolutionary demise of those members of a species lacking an appropriate level of regulatory ability. The system of protection proposed in the original ‘Central Governor’ hypothesis involved a feed-forward control of physical activity, rather than any reflex response to peripheral signals. In regard to likely physiological correlates of a ‘Central Governor’, I thought it useful to draw together and weigh some of the main pieces of secondary evidence advanced by those supporting the hypothesis. I would agree with Micklewright and Parry that, with the possible exception of the absence of cardiac output and oxygen consumption plateaus during maximal effort,[2] none of the potential correlates are in themselves adequate either to prove or to disprove the hypothesis. My comments on the evolutionary perspective were necessarily brief, but have been developed in detail elsewhere.[3-5] The exercise component of the International Biological Programme, which I coordinated, had as its main thrust an examination of genetically isolated populations. It was hypothesized (but largely disproved) that such isolation might allow the emergence of specific genotypes, giving the population concerned an unusual level of physical ability and thus permitting it to colonize a challenging habitat. Nevertheless, it was also recognized that such inherent physical abilities were honed by a life-time learning of particular hunting and/or agricultural skills. In this context, Micklewright and Parry are correct to underline that the primary determinant of success in athletic competition is an acquired skill in pacing, rather than the promptings of any ‘Central Governor’.[6] The letter suggests ‘‘we should be cautious about rejecting the CGM based upon such deductions y (this) does not constitute a sufficiently rigorous test.’’ I fully agree. More Sports Med 2010; 40 (1)
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Letter to the Editor
importantly, such evidence is inadequate to accept the CGM. We now have a clear enunciation of the hypothesized properties of the ‘Central Governor’, and an adequate period has elapsed for the emergence of convincing experimental proof. In its absence, I am tempted to suggest that the hypothesis be consigned to a bottom drawer for future reference. In the parlance of my North American colleagues, the time may now be ripe for proponents of the hypothesis to ‘‘Put up or shut up.’’ Roy J. Shephard Faculty of Physical Health and Education, University of Toronto, Toronto, Ontario, Canada
ª 2010 Adis Data Information BV. All rights reserved.
References 1. Shephard RJ. Is it time to retire the ‘Central Governor’? Sports Med 2009; 39: 709-21 2. Shephard RJ. Is the measurement of maximal oxygen intake passe´? Br J Sports Med 2009; 43: 83-5 3. Shephard RJ. Human physiological work capacity. London: Cambridge University Press, 1978 4. Shephard RJ. Work physiology and activity patterns. In: Milan FA, editor. The human biology of circumpolar populations. Cambridge: Cambridge University Press, 1980: 305-38 5. Shephard RJ, Rode A. The health consequences of ‘modernization’: evidence from circumpolar peoples. London: Cambridge University Press, 1996 6. Micklewright D, Papadoulos E, Swart J, et al. Previous experience influences pacing during 20-km time trial cycling. Br J Sports Med. Published on-line 12 Apr 2009
Sports Med 2010; 40 (1)
