Sports Med 2011; 41 (5): 345-360 0112-1642/11/0005-0345/$49.95/0
CURRENT OPINION
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Exercise Guidelines in Pregnancy New Perspectives Gerald S. Zavorsky1,2 and Lawrence D. Longo3 1 Human Physiology Laboratory, Marywood University, Scranton, Pennsylvania, USA 2 The Commonwealth Medical College, Scranton, Pennsylvania, USA 3 Center for Perinatal Biology, School of Medicine, Loma Linda University, Loma Linda, California, USA
Abstract
In 2002, the American College of Obstetricians and Gynecologists published exercise guidelines for pregnancy, which suggested that in the absence of medical or obstetric complications, 30 minutes or more of moderate exercise a day on most, if not all, days of the week is recommended for pregnant women. However, these guidelines did not define ‘moderate intensity’ or the specific amount of weekly caloric expenditure from physical activity required. Recent research has determined that increasing physical activity energy expenditure to a minimum of 16 metabolic equivalent task (MET) hours per week, or preferably 28 MET hours per week, and increasing exercise intensity to ‡60% of heart rate reserve during pregnancy, reduces the risk of gestational diabetes mellitus and perhaps hypertensive disorders of pregnancy (i.e. gestational hypertension and pre-eclampsia) compared with less vigorous exercise. To achieve the target expenditure of 28 MET hours per week, one could walk at 3.2 km per hour for 11.2 hours per week (2.5 METs, light intensity), or preferably exercise on a stationary bicycle for 4.7 hours per week (~6–7 METs, vigorous intensity). The more vigorous the exercise, the less total time of exercise is required per week, resulting in ‡60% reduction in total exercise time compared with light intensity exercise. Light muscle strengthening performed over the second and third trimester of pregnancy has minimal effects on a newborn infant’s body size and overall health. On the basis of this and other information, updated recommendations for exercise in pregnancy are suggested.
1. Introduction Regular aerobic exercise is an important component for the maintenance of overall health. Exercise is especially important in pregnancy, as women of childbearing age are at increased risk of gestational diabetes mellitus (GDM), which has been strongly linked with obesity.[1,2] As more women tend to gain an excessive amount of weight during pregnancy, they also tend to retain the weight after delivery.[3,4] Gaining an excessive
amount of weight during pregnancy can result in obesity-associated co-morbidities, which are a major health concern in the US.[5] In 2002, the American College of Obstetricians and Gynecologists (ACOG) published exercise guidelines for pregnancy.[6] These suggested that in the absence of medical or obstetric complications, 30 minutes or more of moderate exercise a day on most, if not all, days of the week is recommended for pregnant women. These guidelines were based on the 1995 joint recommendations
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by the Centers of Disease Control and Prevention (CDC) and the American College of Sports Medicine (ACSM).[7] However, these were general public health recommendations, with no clarity on the definition of ‘moderate intensity’ exercise or the recommended amount of weekly physical activity energy expenditure. It has been 15 years since those initial CDC and ACSM recommendations were established, and 9 years since their adoption by ACOG. Since then, new science has emerged that has enhanced our understanding of the amount of physical activity expenditure per week required and the intensity of exercise needed to improve health outcome and quality of life. In 2007, updated physical activity recommendations were published by the ACSM and the American Heart Association (AHA).[8,9] These included definitions of ‘moderate’ and ‘vigorous’ exercise, and provided recommendations for muscle strengthening activities (table I). As such, we believe these updated 2007 recommendations should be used to establish new ACOG guidelines for pregnancy in the absence of medical or obstetric complications. Pregnancy is not a state of confinement, yet pregnant women spend less time performing vigorous exercise with less duration and frequency than non-pregnant women.[12] Indeed, women who maintain their exercise regimen during pregnancy continue to exercise at a higher intensity than those who stop.[13] Over time, these women gain less weight, deposit less fat, have increased fitness and have a lower cardiovascular risk profile in the perimenopausal period than women who cease to exercise in pregnancy.[13] Therefore, the purpose of this clinical opinion is 2-fold: (i) to provide evidence that increasing weekly physical activity expenditure while incorporating vigorous exercise provides the best health outcome for pregnant women and their infants; and (ii) to create new exercise guidelines for pregnancy that are relatively specific, and that
Table I. The American College of Sports Medicine (ACSM) and American Heart Association (AHA)’s physical activity recommendations for men and non-pregnant womena Aerobic activity
Muscle strengthening activity
Adults aged 18–65 y perform a minimum of 30 min moderate intensity exercise for 5 d/wk or 20 min vigorous intensity exercise 3 d/wkb
For adults aged 18–65 y, 8–12 repetitions each of 8–10 muscular strength exercises should be performed on 2 or more non-consecutive d/wk using the major muscle groups
For adults >65 y, moderate intensity = 12–14 on the Borg RPE 6–20 point scale; vigorous intensity = 15–16 on the Borg RPE 6–20 point scale[10]
For adults >65 y, 10–15 repetitions each of 8–10 exercises on 2 or more nonconsecutive d/wk using the major muscle groups with an effort level of 12–14 to 15–16 on the Borg RPE 6–20 point scale[10]
a
These are the 2007 updated ACSM and AHA recommendations from Haskell et al.[8] and Nelson et al.[9] Moderate intensity is now classified as activities that require 3–6 METs (10.5–21 mL/kg/min) and vigorous activity is classified as >6 METs (>21 mL/kg/min).[8] Moderate intensity exercise can be walking at 4.8 km/h, 3.3 METs); walking briskly at 6.4 km/h (5 METs); washing a car, garage, sweeping floors or washing windows (3 METs); slow to fast ballroom dancing (3–4.5 METs); badminton (4.5 METs); or swimming leisurely (6 METs).[11] Vigorous intensity can be walking at a very brisk pace at 7.2 km/h (6.3 METs); jogging at 8.0 km/h (8 METs); walking on a treadmill at 5.6 km/h (5% grade, 6.1 METs); swimming at a moderate/hard feeling of effort (8–11 METs).[11]
b
Moderate = 3–6 METs; vigorous >6 METs.
METs = metabolic equivalent tasks; RPE = rating of perceived exertion.
incorporate the emerging research findings over the past decade. 2. Increasing the Amount of Vigorous Intensity Exercise is an Important Goal for Pregnant Women, Especially Those Who are Overweight or Obese Obese women have an increased risk of fetal, neonatal and maternal morbidity;[14-24] therefore, prevention of excessive weight gain1 during pregnancy is important for the welfare of both mother and child.[16,26] Regular physical activity
1 Excessive weight gain during pregnancy is defined as ‡9.0 kg in overweight women (pre-pregnancy body mass index [BMI] = 25.0–29.9 kg/m2), or ‡5.9 kg in obese women (pre-pregnancy BMI ‡30 kg/m2). For pregnant women of normal pre-pregnancy bodyweight (BMI = 20.0–24.9 kg/m2), optimal weight gain during pregnancy is between 2.1 and 9.9 kg. For pregnant women whose pre-pregnancy BMI is <20 kg/m2, optimal weight gain during pregnancy is 4.1–9.9 kg.[25]
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performed before[1,25,27] and during pregnancy[1] has been shown to reduce the incidence of GDM, for example, by at least 30%, depending on the amount of weekly physical activity energy expenditure and intensity of exercise. Vigorous exercise is important to prevent weight gain in pregnancy and throughout life.2 Recent data demonstrate that skeletal muscle work efficiency changes dramatically when bodyweight is altered.[28] With weight gain from lack of physical activity, efficiency of skeletal muscle decreases,[28] which at the outset is fine as more calories are burned with heavier weight. However, weight gain from physical inactivity usually means an increase in fat mass, which, biochemically, has been found to decrease the body’s ability to gain future muscle due to the attenuation of anabolic processes;[29] therefore, an obese individual has an impeded ability to gain muscle. With weight loss through physical activity, caloric expenditure decreases, not just because muscles have less weight to carry around, but due to a reduction in the ratio of glycolytic to oxidative enzymes in muscle without significant changes in enzymatic activity related to fatty acid oxidation.[28] As such, with weight loss, significantly fewer calories are expended with physical activity,[28] and an increase in weight will occur once again. A programme of vigorous intensity exercise may stop the yo-yo effect of the weight gain/weight loss cycle.[30] Non-oxidative type IIb muscle fibres (which minimally burn fat) are increased in obese women,[31,32] and are directly related to body mass index (BMI). The larger the BMI, the more type IIb muscle fibres a woman possesses. In addition, the larger the BMI, the lower the percentage of type I oxidative (fat burning) fibres.[33] Weight loss by itself[34] or weight loss with physical activity[35,36] can, but not always,[28] improve muscle oxidative capacity in obese women with or without diabetes. If the muscle oxidative capacity is increased with physical activity, then the capacity to burn fat throughout the day is increased.
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Vigorous intensity exercise that increases the energy expenditure post-exercise compared with low-intensity exercise,[37,38] should limit weight gain in overweight and obese pregnant women. In fact, for a given energy expenditure, vigorous exercise programmes induce a greater loss of subcutaneous fat compared with a programme of moderate intensity.[39] Thus, we propose that higher intensity exercise may be an alternative means to improve oxidative capacity .and increase post-exercise oxygen consumption (VO2) so that body fat percentage is reduced to a greater extent compared with traditional low-intensity exercise, and weight gain is limited in overweight and obese pregnant women. Considerable evidence supports the use of higher intensity exercise to reduce body fat percentage. Specifically, in overweight individuals, a 14-week exercise programme consisting of moderate-intensity exercise (60–70% aerobic capacity) was compared with an exercise programme of high-intensity exercise (75–90% aerobic capacity). Both groups exercised three times per week, and both expended the same amount of calories.[40] The high-intensity group reduced their total body fat percentage from 27% to 22% (p < 0.05), while the moderate-intensity group did not see a reduction.[40] Another study demonstrated that moderate exercise intensity (40–55% of aerobic capacity) for 8 months did not reduce total fat mass (-2 – 3 kg) to the same extent as vigorous exercise (65–80% of aerobic capacity, -5 – 3 kg), even when controlled for the same weekly distance and the same total training time.[41] This has been shown elsewhere,[42] although, the exercise bouts were not isocaloric. Another compelling reason why pregnant women should perform vigorous exercise as tolerated, is that the duration of labour is inversely associated with aerobic capacity after adjusting for birthweight (p = 0.03).[43] Kardel and colleagues[43] investigated the effect of aerobic capacity on duration of labour in 40 nulliparous women (aged 30 – 4 years)
. 2 Vigorous exercise is defined by the ACSM as an oxygen consumption (VO2) of >21 mLO2/kg/min, which is taken to be >6-fold greater than the resting metabolic rate (>6 METs). However, this article shows that some . pregnant women are not able to exercise at that VO2. Therefore, the. definition of. vigorous exercise should be defined as ‡60% of heart rate reserve (HRR) [preferably] or ‡65% of VO2 reserve (VO2R). ª 2011 Adis Data Information BV. All rights reserved.
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who started labour spontaneously. Aerobic capacity was measured in these women (bodyweight = 77 – 9 kg) at 35–37 weeks of gestation. Duration of labour was defined as the time between 3 cm cervical dilation with regular uterine contractions and delivery. The mean aerobic capacity was 2.1 – 0.3 LO2/min and duration of labour 583 – 317 minutes. The potential determinants of the duration of labour, identified by a Pearson correlation were tested in a multivariate model. They concluded that increased aerobic fitness was associated with shorter labour in nulliparous women who started labour spontaneously. Other earlier research confirms Kardel’s study. Clapp[44] found that his well trained groups who exercised during pregnancy had a significant shorter first stage of labour by 118 minutes than a group who had stopped exercising before the end of the first trimester. Beckmann and Beckmann[45] found that nulliparous women who exercised regularly before becoming pregnant also had a significantly shorter labour (first and second stages) by ~8 hours in total compared with a non-exercising control group. The minimal threshold for independent living requires an aerobic capacity of approximately 15 (women) to 18 (men) mLO2/kg/min,[46,47] which is four to five metabolic equivalent tasks . (METs) [a value of one MET = resting VO2, or ~3.5 mLO2/kg/min]. Thankfully, only about 1% of women of childbearing age are at or below this minimum threshold.[48] Normal weight pregnant women in the second and third trimester (pre-pregnancy BMI = 23 kg/m2) have an aerobic capacity that ranges from 1.4 to 2.6 LO2/min, which equals about 27–39 mLO2/kg/min.[49-53] Unfit, overweight (pre-pregnancy BMI = 25.0 to 29.9 kg/m2) or obese pregnant women (pre-pregnancy BMI ‡30 kg/m2) who are unaccustomed to exercise have a low aerobic capacity relative to bodyweight (18–22 mLO2/kg/min).[50,54] Endurance-trained pregnant athletes have an aerobic capacity reported to be around 50 mLO2/kg/min.[55,56] Aerobic capacity in LO2/min remains quite stable between the second and third trimester; however, the aerobic capacity measured in mLO2/kg/min may decrease by 10% by the third trimester due to maternal weight gain.[52] ª 2011 Adis Data Information BV. All rights reserved.
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One way to incorporate vigorous exercise is the use of interval training, which incorporates . brief intense bouts of exercise (>80% of VO2 re. serve [VO2R]) with periods of rest. This has been found to be time efficient while improving oxidative capacity in skeletal muscle to the same extent as traditional low-intensity continuous exercise.[57,58] Interval training has been shown to. be safe and more effective in improving peak VO2 and left ventricular function in patients with coronary artery disease than the traditional method of continuous moderate exercise.[59-61] In 75-year-old subjects, which included overweight women with stable post-infarction heart failure, 12 weeks of interval training increased aerobic capacity by 46%, several heart function parameters by 20–30% and improved their quality of life.[61] These changes were significantly greater compared with 12 weeks of regular continuous training.[61] A major consideration is that if elderly overweight women with heart failure and/or coronary artery disease can successfully perform interval training, then this type of research should be implemented in pregnancy to establish the extent to which type of exercise periodic intense exercise is feasible, safe and results in appropriate exercise adherence. Interval training during pregnancy is an exciting new possibility. However, until further studies are performed, it is our opinion that pregnant women should build up to continuous, steady-state aerobic exercise of about ‡65% of aerobic capacity (vigorous exercise), which is ~60% of heart rate reserve (HRR) or ~70–75% of maximum heart rate (HRmax).[62] This recommendation is within the range of the recommendations from the Society of Obstetricians and Gynecologists of Canada (SOGC)/Canadian Society for Exercise Physiology.[63] 3. Increasing Weekly Physical Activity Energy Expenditure is an Important Goal for Pregnant Women Increasing weekly physical activity energy expenditure has been found to reduce the incidence of the metabolic syndrome,[64] GDM[25] and systemic inflammation,[65] while delaying ageing[66] and disability.[67] The risks of coronary heart Sports Med 2011; 41 (5)
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disease and cardiovascular disease also decrease linearly in association with increasing physical activity energy expenditure.[68] Johnson and colleagues[64] studied the effects of three different 6-month exercise programmes on components of the metabolic syndrome: low amount/moderate intensity (equivalent to jogging 19 km/wk at 40–55% of aerobic capacity), low amount/high intensity (equivalent to jogging 19 km/wk at 65–80% of aerobic capacity) or high amount/ vigorous intensity (equivalent to jogging 32 km/wk at 65–80% aerobic capacity). These investigators showed that the high-amount/vigorous-intensity group had improvement in the highest number of metabolic variables, compared with the other two groups and a control group.[64] This makes sense because insulin resistance is negatively related to caloric expenditure from a single bout of exercise (figure 1). From this study, the dose-response of energy expenditure in reducing the risk factors for metabolic syndrome were uncovered.[64] Reduced risk of GDM and pre-eclampsia is seen when women exercise between 3 months and 1 year before or during pregnancy.[1,25,27,70,71] During pregnancy, exercise programmes lasting at least several weeks[72] is the best way to reduce the fasting blood glucose level and to blunt the glycaemic response following a meal, whereas, single
bouts of exercise provided the fewest benefits.[73,74] Zhang and co-workers[25] conducted a prospective cohort study to assess whether the amount, type and intensity of pregravid physical activity are associated with GDM risk. The relative risks (RRs) of GDM decreased with total pregravid weekly physical activity (figure 2), such that 16 MET hours per week showed a 17% reduction in GDM risk, and 56 MET hours per week showed a ~30% reduction in GDM risk, compared with subjects who did not exercise. If the amount of pregravid weekly vigorous physical activity (figure 2) increased (vigorous exercise intensity ‡6 METs or ‡21 mLO2/kg/ min), the RR for GDM also decreased by 20% and 25% if 6 and 15 MET hours per week of vigorous physical activity is performed, respectively. Rudra et al.[27] demonstrated that those who exercised strenuously up to maximal exertion using the Borg rating of perceived exertion (RPE) scale in the year before pregnancy, showed a 43% decrease in the risk for GDM. Also, those that performed ‡30 MET hours per week of energy expenditure from physical activity in the year before pregnancy had a 50% decrease in the risk of GDM, compared with only a 34% decrease in GDM if the exercise expenditure was <14.9 MET hours per week.[27] Dempsey et al.[1] b 30
20
15 Change from rest (%)
Change from rest (%)
a 40
0 −20 −40
0 −15 −30 −45
−60
−60
−80 0
1.26 (300)
2.51 (600)
3.77 (900)
5.02 (1200)
6.28 (1500)
<3.77 (900)
* >3.77 (900)
Total energy expenditure during exercise, MJ (kcal) Fig. 1. Exercise-induced changes in (a) homeostasis model assessment of insulin resistance as a function of total energy expenditure during exercise; and (b) subjects who expended <900 or >900 (kcal) during the exercise bout. The data demonstrate that whole body insulin sensitivity from a single bout of exercise is improved only when the total energy expenditure is >900 kcal per session. Reproduced from Magkos et al.[69] with permission from Portland Press Ltd. * p < 0.05 compared with resting state.
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demonstrated that pregravid women who exercised ‡21.1 MET hours per week during the year before pregnancy reduced GDM risk by 74%, while women who were pregnant and expended ‡28 MET hours per week per week during pregnancy reduced GDM risk by 33% (figure 3). However, due to the large confidence intervals for the reduction in RR for GDM during pregnancy in the group that exercised ‡28 MET hours per week compared with no exercise (RR = 0.67; 95% CI 0.31, 1.43), statistical significance was not reached. Nonetheless, this does not negate the findings of how exercise during pregnancy can reduce GDM risk. Therefore, it is our opinion that there is a potential benefit for the adoption and continuation of an active lifestyle for women of reproductive age that is of vigorous intensity prior to and during pregnancy. To obtain energy expenditure in MET hours per week, one multiplies the number of METs required for the activity by the number of hours per day multiplied by the total number of days
per week performing the activity. For example, 5 METs · 0.95 hours per day · 6 days per week = 28.5 MET hours per week. Second, to convert MET hours per week into kcal/wk of energy expenditure, one multiples 28.5 MET hours per week by the resting metabolic rate of 3.5 mLO2/kg/min and by 60 min/h to get 5985 mLO2/kg/wk. Now, the bodyweight is needed. For this example, the bodyweight of an individual is 58.7 kg, therefore, 5985 mLO2/kg/wk · 58.7 kg = 351319.5 mLO2/wk or 351.2 LO2/wk consumed in total for physical activity. Since 5 kcal are yielded for every L of oxygen consumed, then 351.2 LO2/wk · 5 kcal/L = 1756.6 kcal/wk. The more vigorous the exercise, the less total time of exercise is required. For example, one can exercise 3 METs · 1.6 hours per day · 6 days per week = 28.8 MET hours per week; or one can exercise for less time at a higher intensity to achieve the same expenditure (e.g. 5 METs · 0.95 hours per day · 6 days per week = 28.5 MET hours per week). For a 54 kg woman, 28.5 MET hours per Total physical activity Vigorous activity
1.2
RR of GDM
1.0
0.8
0.6
0.4
0.2 8
16
24
32
40
48
56
MET h/wk Fig. 2. Relative risks (RRs) of gestational diabetes mellitus (GDM) according to total physical activity (solid line) and vigorous activity (dotted line) measured in metabolic equivalent task (MET) hours per week, continuous, prior to pregnancy. RRs are adjusted for age, race/ethnicity, cigarette smoking status (never, past or current), family history of diabetes in a first-degree relative (yes, no), parity (0, 1, 2, ‡3), alcohol intake (0.0, 0.1–5.0, 5.1–15.0 or >15.0 g/day), dietary factors (in quintiles of total energy, cereal fibre, glycaemic load and total fat) and body mass index before the pregnancy. The error bars illustrate the approximate 95% CI.[25]
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1.0
Adjusted RRs of GDM
0.9 0.8
(0.35, 1.47)
0.7 0.6
(0.31, 1.43)
(0.27, 1.21)
0.5 0.4 (0.10, 0.65)
0.3 0.2 0.1 0 <21.1
>21.1
Year before pregnancy in MET h/wk
<28.0
>28.0
During pregnancy in MET h/wk
Fig. 3. Adjusted relative risks (RRs) of gestational diabetes mellitus (GDM) according to the amount of physical activity energy expenditure performed in the year before and also during pregnancy, adjusted for maternal age, race, parity and pre-pregnancy body mass index. No physical activity was made to have a RR of 1.0. Physical activity before and during pregnancy reduces RR of GDM. The numbers in parentheses illustrate 95% CI.[1] MET = metabolic equivalent task.
week = approximately 1616 kcal/wk (or 269 kcal/day for 6 days). If one exercises 6 days in a 7-day cycle, then the energy expenditure in MET hours per week is calculated over 6 days of exercise. 4. Potential Risks of Exercise in Pregnancy 4.1 Cardiac Risks of Exercise
With regard to the frequency with which myocardial infarction is triggered by exertion, it is important to distinguish absolute from RR. The absolute risk of a 50-year-old non-smoking, non-diabetic individual having a myocardial infarction during a given 1-hour period, is approximately 1 in 1 million (0.0001%).[75,76] If an individual is habitually sedentary, but engaged in heavy physical exertion (>6 METs) during that hour, the risk would increase 100-fold over the baseline value, but the absolute risk during that hour still would be only 1 in 10 000 (0.01%). The research has shown that a single episode of vigorous physical exertion can increase the shortterm risk of myocardial infarction.[77] The paradox, however, is that increased frequencies of vigorous exercise at >6 METs is associated with a reduction in the long-term risk of coronary events. Individuals who exercise regularly not ª 2011 Adis Data Information BV. All rights reserved.
only have a lower baseline risk of myocardial infarction, they also have a lower RR that an infarction will be triggered by heavy physical exertion.[77] There is no reason to suggest that the maternal cardiac risk of exercise would be different during pregnancy. The number of sudden cardiac arrests or other cardiac events in the general population is one event per 565 000 hours of exercise.[78] For individuals with known heart disease, it is one event per 59 142 hours.[78] The absolute risk of sudden death during any episode of vigorous exercise equals about one death per 1.51 million episodes of exertion.[79] Thus, the risk of exercise in triggering cardiac events is very small. Compare the risk of triggering sudden cardiac events (which is about 0.01%) with the CDCs death rate for accidental deaths (unintentional injuries), which is about 0.04%.[80] As such, the risk of death from unintentional injuries in the US is higher than the risk of triggering cardiac events from exercise; therefore, the risks must be placed in perspective to a real-world context. The US death rate of all causes (accidents, homicides, suicides, diseases, cancer, infection, dying of old age, etc.) is about 0.8%,[80] so when compared with the risk of exercise, these other issues provide more risk to human health than a vigorous exercise session in sedentary pregnant women. 4.2 Risk of Regular Exercise Training Resulting in Small for Gestational Age Infants and Increased Risk of Preterm Birth
Small for gestational age (SGA), which is a birthweight that is in the 10th percentile or below for the gestational age of the infant, is usually a consequence of compromised intrauterine development, and is considered a risk of perinatal morbidity and mortality.[81] Regardless of whether a woman is sedentary or an endurance athlete, exercise during the first two trimesters has not been shown to affect birthweight.[82] However, female endurance athletes who exercise vigorously (‡6 · per week, >1 hour per session for 10 weeks, >50% of age predicted HRmax) into the third trimester, produce infants that are on average 212 g (95% CI 149, 276) smaller than active Sports Med 2011; 41 (5)
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controls (‡3 · per week, 30 minutes per session for 10 weeks, >50% of age-predicted HRmax), and 437 g (95% CI 268, 606) smaller than sedentary controls.[82] Nonetheless, a 200–400 g decrease in mean birthweight is not clinically meaningful for two reasons. First, this difference in weight is less than the 500 g difference between the 50th percentile and 10th percentile in recent published tables.[83] Second, SGA is an anthropometric characteristic that does not necessarily have adverse health implications, and is therefore commonly used (but not necessarily appropriately) as a proxy for the pathological outcomes believed to be associated with an inadequate rate of fetal growth[84] (i.e. the majority of SGA births are small for no demonstrative reason; an aetiology is not found in >50% of cases of SGA).[85] Third, more recent data published in 2010 with a larger sample size suggests no real clinically meaningful difference in birthweight of infants born to women who exercise during pregnancy for >5 hours per week compared with pregnant women who do not exercise.[86] In this study of ~80 000 infants, it was found that women who exercised during pregnancy had a decreased risk of having a SGA child or a large for gestational age child (birthweight greater than the 90th percentile for gestational age).[86] These data suggest that women who exercise >5 hours per week have smaller infants by only 11 g than those of non-exercisers;[86] therefore, differences may not be clinically meaningful. As a corollary, SGA-identified fetuses may not tolerate the mild diversion of cardiac output from the uterus to the skeletal muscles during exercise. Therefore, there is a slight chance of post-exercise bradycardia. This has occurred previously in a subsequently diagnosed growth-restricted fetus.[87] While there are many SGA fetuses who are not growth restricted, the clinician does not know which is which until after birth. As such, caution is advised against exercise in the growthrestricted fetus. In terms of preterm births, exercise during pregnancy actually reduces the risk of complications. Using data of over 85 000 births, >5 hours a week of exercise during pregnancy reduced the risk of preterm birth by 18% (RR 0.81; 95% CI 0.64, 1.04).[88] When calculating energy expenª 2011 Adis Data Information BV. All rights reserved.
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diture, pregnant women who exercised 10–15 MET hours per week (715–1071 kcal/wk for a 68 kg woman) experienced a 17% reduction in the risk of preterm births (RR 0.83; 95% CI 0.71, 0.96), and those who exercise for more than 15 MET hours per week (>1071 kcal/wk for a 68 kg woman) experienced a 12% reduction (RR 0.88; 95% CI 0.78, 1.00) in preterm births.[88] 4.3 Risks of Exercise Resulting in an Abnormal Fetal Heart Rate (HR) Response
A misconception about exercise in pregnancy is that fetal health may be compromised because uterine blood flow can decrease progressively with exercise intensity and duration (by up to ~20%).[89,90] However, several . compensatory mechanisms act to preserve fetal VO2 even during exhaustive exercise.[90,91] In sheep, the increased haemoglobin concentration from pregnancy maintains total oxygen delivery to the uterus and, . with increased uterine oxygen extraction, VO2 remains unaltered.[90] In humans, the measurement of fetal umbilical and maternal uterine pulsatility index (PI), which is the best noninvasive technique to assess changes in resistance to blood flow in those areas, was assessed in pregnant women (third trimester) immediately after strenuous exercise above the anaerobic threshold.[92] Compared with rest, there were modest changes in the right uterine PI without changes in umbilical artery PI or left uterine PI in pregnant women 2 minutes post-exercise.[92] However, by 5 minutes post-exercise, right uterine PI returned to baseline values.[92] Therefore, sheep and human data imply that limited strenuous exercise above the anaerobic threshold has minimal effects on total uterine and umbilical . oxygen delivery and VO2. Fetal heart rate (FHR) monitoring has been widely used to monitor fetal well-being before and after exercise. The earlier studies demonstrating fetal bradycardia (FHR <110 beats/minute for 10 seconds) during exercise[93-95] have been dismissed as representing motion artifact.[96,97] FHR is increased by about 20 beats/minute within 30 seconds of strenuous exercise stoppage.[98] By 10 minutes post-exercise, FHR is 0–10 beats/minute Sports Med 2011; 41 (5)
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higher, compared with pre-exercise after a bicycle test to maximal or near maximal exertion.[87,98,99] This suggests that brief intense exercise does not cause fetal distress. Furthermore, regular exercise training does not alter the fetal response.[100] More recently, researchers have demonstrated that FHR response to strenuous maternal exercise is not a predictor of fetal distress since the incidence did not vary with the level of fitness, maternal BMI or fetal weight.[98] 5. Developing New Exercise Guidelines in Pregnancy In 2003, the SOGC published guidelines that were somewhat more specific than the ACOG guidelines. The SOGC suggested that pregnant women should perform 15 minutes of continuous aerobic exercise 3 days per week, with progression to 30 minutes sessions four times per week in previously sedentary women.[63] For most pregnant women, the intensity of exercise is recommended to be 12–14 (out of 20) on the Borg RPE scale.[63] RPE is the perceived, subjective, overall effort of exertion and fatigue from 6 (no exertion) to 20 (maximal exertion). A rating of 6 = no exertion at all, 7–8 = extremely light, 9–10 = very light, 11–12 = light, 13–14 = somewhat hard, 15–16 = hard, 17–18 = very hard, 19 = extremely hard and 20 = maximal exertion. This scale scores the total, overall exertion and fatigue level of exercise. The more exertion, the less total time of exercise is required to reach the recommended weekly physical activity expenditure goal. Basal resting heart rate (HR) is increased by 10–15 beats/minute in pregnancy.[101-103] In turn, HRmax is blunted by 10–15 beats/minute, compared with the predicted HRmax of 220 minus age[50,54,103] (although not always[102]), the HRR is lowered. Thus, the target HR zones are modified in the SOCG guidelines. For example, the target HR zone for a non-obese pregnant woman 20–29 years of age is 135–150 beats per minute, 130–145 for a woman 30–39 years-of-age and 125–140 for a woman ‡40 years of age.[63] This equates to 71–79% of predicted HRmax for the
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20–39 years-of-age group combined. Nonetheless, developing an HR zone generalizable to pregnant populations may not be appropriate because of the individual variation of resting HR, and the large standard deviation of predicting HRmax from age (HRmax = 220 minus age), which is – 10–12 beats/minute.[104] To identify the optimal HR for a given intensity in a given individual, the HRR method was developed by Karvonen.[105] The HRR method essentially uses the difference between HRmax and resting HR (in which both should be measured directly and not predicted). The ‘reserve’ available is the difference between measured HRmax and measured resting HR. Then, a given intensity is provided, and the correct exercise prescription HR can be determined from the following formula: Prescription HR = % intensity · (HRmax that is measured from an aerobic capacity test - resting HR obtained from 5 minutes of sitting upright on a chair) + resting HR. HR zones are published for pregnant overweight or obese women.[54] However, since the minimum intensity for improving aerobic fitness was updated in 2002,[106] the HR zones provided for sedentary, overweight and pregnant women begin at an exercise intensity of 101 beats/minute, which is too low.[54] According to Swain and classified as havFranklin,[106] those individuals . ing low initial fitness (VO2max <40 mLO2/kg/min), based on a graded exercise test to maximum, will show improvements in aerobic. capacity only if the training intensity is ‡30% VO2R..3 For those with higher aerobic capacities (VO2max >40 mL/kg/min),. the minimal training intensity has to be ‡45% VO2R.[106] The percentage of HRR . (%HRR) is equal to the percentage of VO2R . (%VO2R) unless the woman is overweight, sedentary and pregnant. . In overweight, sedentary pregnant women, %VO2R is slightly higher. by about 5% compared with %HRR, until 70% VO2R after . which %VO2R and %HRR are about equal.[54] Prescribing exercise intensity based on %HRR provides the most accurate training prescription, especially when the patient’s resting and HRmax is
. . . . 3 Prescription VO2 = %intensity · (VO2max - resting VO2) + resting VO2. ª 2011 Adis Data Information BV. All rights reserved.
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Table II. Updated aerobic exercise recommendations during pregnancya . Gestational age (wk) %HRR %VO2R
RPE
Total target exercise energy expenditure (MET h/wk)
Previously sedentary and/or overweight/obese pregnant women unaccustomed to exercisea 1–3
35–39
40–45
12–14
‡16
3–6
45–55
50–60
13–15
28
6–9
60
65
15–16
28
10–26
60
65
15–16
28
27–40
45
50
13–14
16
Previously healthy and/or physically active pregnant womena 1–3
45–55
50–60
13–15
‡16
3–6
50–60
55–65
14–15
28
6–9
60
65
15–16
28
10–26
60
65
15–16
28
27–40
50
55
14–15
16
a
See table III for the estimated converted total amount of energy expenditure from physical activity in kcal/wk. The Borg RPE scale is from 6 (no exertion) to 20 (maximal exertion).[10] Some of the suggested programme shown in this table for exercise intensity is based on the American College of Sports Medicine[8,48] and elsewhere.[54] The target goal for the amount of physical activity per wk expended during pregnancy is based on the study by Dempsey et al.,[1] which shows a 33% risk reduction in GDM in women who exercise ‡28 MET h/wk during pregnancy. The complications are listed in table V.[6] These recommendations are for individuals without medical and obstetrical complications.
GDM = gestational diabetes mellitus; MET = metabolic equivalent task; RPE = rating of perceived exertion; %HRR = percentage of heart rate . reserve; %VO2R = oxygen consumption reserve.
known (table II). The actual target HRs, which have been listed elsewhere,[50,54] are not provided in table II because each pregnant woman will have a different resting and HRmax. Let us consider an exercise HR for a sedentary overweight pregnant woman with GDM. At the beginning of the programme, the intensity would be ~35–39% HRR. If her resting HR is 90 beats/min (after sitting upright in a chair for 5 minutes), and measured HRmax (measured from . a graded exercise test to volitional exhaustion) [VO2max test] is 185 beats/minute, then 39% HRR = 0.39 (185–90) + 90 = 127 beats/minute. A HR of 127 beats/minute would be her prescription HR. Pregnant women can monitor their HR during pregnancy using a simple HR monitor (e.g. Polar FS1), which is relatively inexpensive. For those women who are not willing or able to purchase one, then pulse rates can be monitored from their wrists at intervals or the Borg RPE scale can be used (see table II). An additional consideration is that the definition of moderate intensity classified as physical activity requiring 3–6 METs (10.5–21 mLO2/kg/min), and vigorous activity classified as >6 METs (>21 mLO2/kg/min)[8] is
ª 2011 Adis Data Information BV. All rights reserved.
circumspect, because the definition of moderate and vigorous should be based on each individual’s own aerobic capacity. For example, some pregnant women have an aerobic capacity that approaches 46 mLO2/kg/min, which is 13 METs or 13-fold greater than the resting metabolic rate.[55] An activity level of 7 METs would be moderate rather than vigorous intensity for them, as . they would only be exercising at ~53% of VO2max. On the other hand, an unfit, sedentary, overweight pregnant woman may have an aerobic capacity of only 21 mLO2/kg/min or 6 METs.[54] An activity level of 6 METs would not be moderate . for her, as she would be exercising at 100% of VO2max, therefore, the terms ‘moderate’ and ‘vigorous’ are relative, depending on the fitness level of the pregnant woman. That is why exercise intensity based on %HRR and the Borg RPE scale are the best ways to prescribe exercise intensity in all individuals, including pregnant women with GDM, and for those who are sedentary or overweight. Given that obstetricians and gynecologists may wish to simplify exercise prescription by eliminating the use of HRR and its calculations, Sports Med 2011; 41 (5)
Updated Exercise Guidelines in Pregnancy
we understand the practicality of using the Borg RPE scale for exercise intensity, so we have added the scale in table II. Based on the woman’s weight prior to pregnancy, the amount of weekly physical activity energy expenditure in kcal/week during pregnancy is provided in table III. However, we also recognize that calculating the energy expenditure from exercise in a pregnant woman in kcal/week may not be user friendly for the patient or physician, so an estimated total time of exercise is also reported in table III (see footnotes). Muscle strengthening guidelines are reported in table IV for women who wish to supplement their aerobic exercise training periodically. Several physical activity questionnaires are suitable for obtaining an estimate of weekly energy expenditure during pregnancy. We suggest the use of a questionnaire that estimates previous energy expenditure, such as the 7-day physical activity recall,[107-109] the Kaiser Physical Activity Survey in Women[111,112] or the Pregnancy Physical Activity Questionnaire.[113] These questionnaires can be completed in a structured 15–20-minute interview. Nonetheless, for simplicity, we provide an estimated number of hours of physical activity needed per week based on two different modes of exercise that would allow a pregnant woman to achieve the target energy expenditure (this is listed in table III in the footnotes). 5.1 Exercise Testing to Determine Maximum HR (Peak HR and Aerobic Capacity)
Individualizing an exercise programme for pregnant women involves medical screening with the use of a physical activity readiness questionnaire for pregnancy,[114] an estimation of previous physical activity level and developing a programme specific to the woman’s situation. Informing the patient about limitations, contraindications and warning signs should also be performed (table V).[6] On the basis of numerous studies, exercise testing to maximum exercise capacity in pregnant women is safe for both the mother and the fetus.[43,87,92,98,99,103,115,116] Therefore, before an exercise programme is given to a woman, a graded exercise test using a cycle ergometer or treadmill would be an ideal scenario to obtain ª 2011 Adis Data Information BV. All rights reserved.
355
Table III. The minimum and target amount of energy expenditure recommended per wk from physical activity converted to kcal/wk and hours of activity per wk during pregnancy according to bodyweight at start of pregnancya Weight of woman at the start of pregnancy (kg)
Minimum energy expenditure of 16 MET h/wkb (kcal/wk)
Target energy expenditure of 28 MET h/wkc (kcal/wk)
45.2
759
1328
49.7
835
1461
54.2
911
1594
58.7
986
1726
63.2
1062
1859
67.8
1138
1992
72.3
1214
2125
76.8
1290
2258
81.3
1366
2390
85.8
1442
2523
90.3
1518
2657
94.9
1594
2789
99.4
1669
2921
103.9
1745
3054
108.4
1821
3187
112. 9
1897
3320
117.4
1973
3453
122.0
2049
3586
126.5
2125
3718
131.0
2201
3851
135.5
2276
3984
140.0
2352
4116
144.5
2428
4248
a
For every 4.5 kg increase in bodyweight, the weekly energy expenditure increases by about 76 kcal for the minimum required 16 MET h/wk category and 133 kcal/wk for the target 28 MET h/wk category. The minimum and target energy expenditure is based on recent data by Dempsey et al.[1] and Zhang et al.[25] To estimate the total weekly physical activity energy expenditure from vigorous exercise, a questionnaire such as the 7-day physical activity recall can be used.[107-109] However, for simplicity, the required number of h/wk of exercise is estimated here. This is based on two different modes of physical activity. As one can see, the more vigorous the exercise, the less total time of exercise is required per wk.
b
Light = approximately 6.4 h/wk walking (2.0 mph, 2.5 METs); vigorous = approximately 2.7 h/wk bicycling on a stationary bike (~6–7 METs).
c
Light = approximately 11.2 h/wk walking (2.0 mph, 2.5 METs); vigorous = approximately 4.7 h/wk bicycling on a stationary bike (~6–7 METs).
MET(s) = metabolic equivalent task(s); mph = miles per hour.
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Table IV. Muscle strengthening exercise guidelines during pregnancya For pregnant women aged 18–45 y, 8–10 muscular strength exercises can be performed over one to two sessions per wk (nonconsecutive days). One aerobic training session can be replaced by a muscle strengthening session in the weight room or at home Use lighter weights, more reps Heavy weights may overload joints already loosened by increased levels of the hormone relaxin during pregnancy. Thus, perhaps it would be wise to use lighter weights and do more repetitions instead. For example, if one usually performs leg presses with 15.8 kg for 8–12 reps, try 9.0 kg for 15–20 reps. Or, if one typically performs a chest press with 6.8 kg for 8–12 reps, try 3.6 kg for 15–20 reps Avoid walking lunges These may raise the risk of injury to connective tissue in the pelvic area Watch the free weights One should be careful with free weights as free weights may involve the risk of hitting the abdomen. Women can use resistance bands instead, which offer different amounts of resistance and varied ways to do weight training and should pose minimal risk to the stomach Try not to lift while flat on your back. In the second and third trimester, lying on your back may cause the uterus to compress a major vein, the inferior vena cava into which blood from the pregnant uterus flows. This increased pressure can be transmitted to the placenta, to compromise fetal blood flow in the gas exchange area, thereby limiting oxygen supply to the infant. An easy modification is to tilt the bench to an incline Try to avoid the valsalva manoeuver This manoeuver, which involves forcefully exhaling without actually releasing air, can result in a rapid increase in blood pressure and intra-abdominal pressure, and may decrease oxygen flow to the fetus. However, on rare occasions, the uterus can be displaced against the inferior vena cava, which can result in a decrease in blood pressure. Thus, a decrease in blood pressure can also occur with the valsalva manoeuver, but this is uncommon Listen to your body The most important rule is to pay attention to what is going on physically. If you feel muscle strain or excessive fatigue, modify the moves and/or reduce the frequency of the workouts. Pregnancy is not the time to perform heavy weightlifting but muscle strengthening according to these guidelines will burn calories and increase the resting metabolic rate a
Light muscle strengthening training (resistance exercise training) performed over the second and third trimester of pregnancy does not have a negative impact on the newborn infant’s body size and overall health.[110]
HRmax and current fitness. However, access to this type of testing is limited by the number of exercise physiologists, adequate equipment and/ or patient finances; as a result, exercise testing is impractical for a majority of pregnant women. As such, HRmax can be estimated by the formula 220 minus age; subsequently, the programme ª 2011 Adis Data Information BV. All rights reserved.
outlined in table II using %HRR would be appropriate. Should HR not be measured or recorded during exercise, the Borg RPE scale could be a substitute for determining exercise intensity. Exercises that stimulate large muscle groups such as stationary cycling, swimming, walking or jogging are recommended. A standard stationary bicycle can substitute for one that is recumbent. A pregnant woman who has just finished exercise should be aware of uterine contractions. Women should be informed that stimulation of the uterus (i.e. as it moves inside the body from exercise) will cause contractions or tightening. Women should seek medical advice when these contractions become increasingly painful and do not dissipate within a reasonable time frame after exercise. When monitoring fetal movements pre-, during or post-exercise, the National Institute for Health and Clinical Excellence recommends that health professionals should no longer suggest the routine counting of fetal movements in the second half of a woman’s pregnancy.[117] Nevertheless, pregnant women should continue to be aware of fetal movements throughout the day. Less than ten fetal movements in 12 hours is an indication that further investigation at a hospital is warranted.[117] 6. Conclusions The updated 2007 ACSM and AHA recommendations are used to help establish new guidelines for pregnancy, in the absence of medical or obstetric complications. These recommendations are based on recent findings that suggest increasing the amount of physical activity expenditure to at least ‡16 MET hours per week. To achieve the minimum expenditure of 16 MET hours per week, one could walk at 3.2 km per hour for 6.4 hours per week (2.5 METS, light intensity), or preferably exercise on a stationary bicycle for 2.7 hours per week (6.0–7.0 METS, more vigorous intensity). Incorporating vigorous exercise at about 60% HRR, obtained from the pregnant woman’s own resting and HRmax will provide the best health outcome. Use of these new aerobic exercise and muscle strengthening guidelines for pregnancy (tables II, III, IV), which Sports Med 2011; 41 (5)
Updated Exercise Guidelines in Pregnancy
Table V. Absolute and relative contraindications to aerobic exercise during pregnancy as well as warning signs to terminate exercise while pregnant (reproduced from the ACOG Committee opinion,[6] with permission from the American College of Obstetricians and Gynecologists) Absolute contraindications Haemodynamically significant heart disease Restrictive lung disease Incompetent cervix/cerclage Multiple gestation at risk for premature labour Persistent second or third trimester bleeding
357
Acknowledgements Gerald S. Zavorsky, PhD, holds a Certified Strength and Conditioning Specialist credential from the National Strength and Conditioning Association and a Certified Exercise Physiologist credential from the Canadian Society for Exercise Physiology. Lawrence D. Longo is an obstetrician-gynecologist with extensive expertise in exercise and pregnancy in both animal and human models. No sources of funding were used to assist in the preparation of the article. The authors have no conflicts of interests to declare that are directly relevant to the content of this article.
Placenta previa after 26-wk gestation Premature labour during the current pregnancy Ruptured membranes Pre-eclampsia/pregnancy-induced hypertension Relative contraindications Severe anaemia Unelevated maternal cardiac arrhythmia Chronic bronchitis Poorly controlled type 1 diabetes mellitus Extreme morbid obesity Extremely underweight (body mass index <12) History of extremely sedentary lifestyle Intrauterine growth restriction in current pregnancy Poorly controlled hypertension Orthopaedic limitations Poorly controlled seizure disorder Poorly controlled hyperthyroidism Heavy smoker Warning signs to terminate exercise while pregnant Vaginal bleeding Dyspnoea prior to exertion Dizziness Headache Chest pain Muscle weakness Calf pain or swelling (need to rule out thrombophlebitis) Preterm labour Decreased fetal movement Amniotic fluid leakage
are specific, safe for both mother and fetus and which incorporate the emerging research findings over the last decade, may result in a cohort of pregnant women with increased fitness and health, and infants with an enlarged prospect for a healthy and productive life. ª 2011 Adis Data Information BV. All rights reserved.
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66. Cherkas LF, Hunkin JL, Kato BS, et al. The association between physical activity in leisure time and leukocyte telomere length. Arch Intern Med 2008 Jan 28; 168 (2): 154-8 67. Chakravarty EF, Hubert HB, Lingala VB, et al. Reduced disability and mortality among aging runners: a 21-year longitudinal study. Arch Intern Med 2008 Aug 11; 168 (15): 1638-46 68. Williams PT. Physical fitness and activity as separate heart disease risk factors: a meta-analysis. Med Sci Sports Exerc 2001 May; 33 (5): 754-61 69. Magkos F, Tsekouras Y, Kavouras SA, et al. Improved insulin sensitivity after a single bout of exercise is curvilinearly related to exercise energy expenditure. Clin Sci (Lond) 2008 Jan; 114 (1): 59-64 70. Rudra CB, Williams MA, Lee IM, et al. Perceived exertion during prepregnancy physical activity and preeclampsia risk. Med Sci Sports Exerc 2005 Nov; 37 (11): 1836-41 71. Redden SL, Lamonte MJ, Freudenheim JL, et al. The association between gestational diabetes mellitus and recreational physical activity. Matern Child Health J. Epub 2010 Mar 6 72. Jovanovic-Peterson L, Durak EP, Peterson CM. Randomized trial of diet versus diet plus cardiovascular conditioning on glucose levels in gestational diabetes. Am J Obstet Gynecol 1989 Aug; 161 (2): 415-9 73. Avery MD, Walker AJ. Acute effect of exercise on blood glucose and insulin levels in women with gestational diabetes. J Matern Fetal Med 2001 Feb; 10 (1): 52-8 74. Lesser KB, Gruppuso PA, Terry RB, et al. Exercise fails to improve postprandial glycemic excursion in women with gestational diabetes. J Matern Fetal Med 1996 Jul-Aug; 5 (4): 211-7 75. Anderson KM, Odell PM, Wilson PW, et al. Cardiovascular disease risk profiles. Am Heart J 1991 Jan; 121 (1 Pt 2): 293-8 76. Anderson KM, Wilson PW, Odell PM, et al. An updated coronary risk profile: a statement for health professionals. Circulation 1991 Jan; 83 (1): 356-62 77. Mittleman MA, Maclure M, Tofler GH, et al. Triggering of acute myocardial infarction by heavy physical exertion: protection against triggering by regular exertion. Determinants of Myocardial Infarction Onset Study Investigators. N Engl J Med 1993 Dec 2; 329 (23): 1677-83 78. Fletcher GF, Froelicher VF, Hartley LH, et al. Exercise standards: a statement for health professionals from the American Heart Association. Circulation 1990 Dec; 82 (6): 2286-322 79. Albert CM, Mittleman MA, Chae CU, et al. Triggering of sudden death from cardiac causes by vigorous exertion. N Engl J Med 2000 Nov 9; 343 (19): 1355-61 80. Xu J, Kochanek KD, Murphy SL, et al. Deaths: final data for 2007. Natl Vital Stat Rep 2010 May 10; 58 (19): 1-136 81. Wilcox AJ, Skjaerven R. Birth weight and perinatal mortality: the effect of gestational age. Am J Public Health 1992 Mar; 82 (3): 378-82 82. Leet T, Flick L. Effect of exercise on birthweight. Clin Obstet Gynecol 2003 Jun; 46 (2): 423-31 83. Kramer MS, Platt RW, Wen SW, et al. A new and improved population-based Canadian reference for birth weight for gestational age. Pediatrics 2001 Aug; 108 (2): E35
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84. Altman DG, Hytten FE. Intrauterine growth retardation: let’s be clear about it. Br J Obstet Gynaecol 1989 Oct; 96 (10): 1127-32 85. Lee PA, Chernausek SD, Hokken-Koelega AC, et al. International Small for Gestational Age Advisory Board consensus development conference statement: management of short children born small for gestational age, April 24-October 1, 2001. Pediatrics 2003 Jun; 111 (6 Pt 1): 1253-61 86. Juhl M, Olsen J, Andersen PK, et al. Physical exercise during pregnancy and fetal growth measures: a study within the Danish National Birth Cohort. Am J Obstet Gynecol 2010 Jan; 202 (1): 63.e1-8 87. MacPhail A, Davies GA, Victory R, et al. Maximal exercise testing in late gestation: fetal responses. Obstet Gynecol 2000 Oct; 96 (4): 565-70 88. Juhl M, Andersen PK, Olsen J, et al. Physical exercise during pregnancy and the risk of preterm birth: a study within the Danish National Birth Cohort. Am J Epidemiol 2008 Apr 1; 167 (7): 859-66 89. Lotgering FK, Gilbert RD, Longo LD. Exercise responses in pregnant sheep: oxygen consumption, uterine blood flow, and blood volume. J Appl Physiol 1983 Sep; 55 (3): 834-41 90. Lotgering FK, Gilbert RD, Longo LD. Exercise responses in pregnant sheep: blood gases, temperatures, and fetal cardiovascular system. J Appl Physiol 1983 Sep; 55 (3): 842-50 91. Lotgering FK, Gilbert RD, Longo LD. Maternal and fetal responses to exercise during pregnancy. Physiol Rev 1985 Jan; 65 (1): 1-36 92. Kennelly MM, Geary M, McCaffrey N, et al. Exercise-related changes in umbilical and uterine artery waveforms as assessed by Doppler ultrasound scans. Am J Obstet Gynecol 2002 Sep; 187 (3): 661-6 93. Artal R, Romem Y, Paul RH, et al. Fetal bradycardia induced by maternal exercise. Lancet 1984 Aug 4; II (8397): 258-60 94. Jovanovic L, Kessler A, Peterson CM. Human maternal and fetal response to graded exercise. J Appl Physiol 1985 May; 58 (5): 1719-22 95. Dale E, Mullinax KM, Bryan DH. Exercise during pregnancy: effects on the fetus. Can J Appl Sport Sci 1982 Jun; 7 (2): 98-103 96. Paolone AM, Shangold M, Paul D, et al. Fetal heart rate measurement during maternal exercise: avoidance of artifact. Med Sci Sports Exerc 1987 Dec; 19 (6): 605-9 97. Paolone AM, Shangold MM. Artifact in the recording of fetal heart rates during material exercise. J Appl Physiol 1987 Feb; 62 (2): 848-9 98. Kennelly MM, McCaffrey N, McLoughlin P, et al. Fetal heart rate response to strenuous maternal exercise: not a predictor of fetal distress. Am J Obstet Gynecol 2002 Sep; 187 (3): 811-6 99. van Doorn MB, Lotgering FK, Struijk PC, et al. Maternal and fetal cardiovascular responses to strenuous bicycle exercise. Am J Obstet Gynecol 1992 Mar; 166 (3): 854-9 100. Barakat R, Ruiz JR, Rodriguez-Romo G, et al. Does exercise training during pregnancy influence fetal cardiovascular responses to an exercise stimulus? Insights from a randomised controlled trial. Br J Sports Med 2010 Aug; 44 (10): 762-4 101. Lotgering FK, Struijk PC, van Doorn MB, et al. Errors in predicting maximal oxygen consumption in pregnant women. J Appl Physiol 1992 Feb; 72 (2): 562-7
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102. Sady MA, Haydon BB, Sady SP, et al. Cardiovascular response to maximal cycle exercise during pregnancy and at two and seven months post partum. Am J Obstet Gynecol 1990 May; 162 (5): 1181-5 103. Heenan AP, Wolfe LA, Davies GA. Maximal exercise testing in late gestation: maternal responses. Obstet Gynecol 2001 Jan; 97 (1): 127-34 104. Londeree BR, Moeschberger ML. Effect of age and other factors on maximal heart rate. Res Q Exerc Sport 1982; 53: 297-303 105. Karvonen MJ, Kentala E, Mustala O. The effects of training on heart rate; a longitudinal study. Ann Med Exp Biol Fenn 1957; 35 (3): 307-15 106. Swain DP, Franklin BA. VO(2) reserve and the minimal intensity for improving cardiorespiratory fitness. Med Sci Sports Exerc 2002 Jan; 34 (1): 152-7 107. Blair SN, Haskell WL, Ho P, et al. Assessment of habitual physical activity by a seven-day recall in a community survey and controlled experiments. Am J Epidemiol 1985 Nov; 122 (5): 794-804 108. Washburn RA, Jacobsen DJ, Sonko BJ, et al. The validity of the Stanford Seven-Day Physical Activity Recall in young adults. Med Sci Sports Exerc 2003 Aug; 35 (8): 1374-80 109. Sallis JF, Haskell WL, Wood PD, et al. Physical activity assessment methodology in the Five-City Project. Am J Epidemiol 1985 Jan; 121 (1): 91-106 110. Barakat R, Lucia A, Ruiz JR. Resistance exercise training during pregnancy and newborn’s birth size: a randomised controlled trial. Int J Obes (Lond) 2009 Sep; 33 (9): 1048-57 111. Schmidt MD, Freedson PS, Pekow P, et al. Validation of the Kaiser Physical Activity Survey in pregnant women. Med Sci Sports Exerc 2006 Jan; 38 (1): 42-50 112. Ainsworth BE, Sternfeld B, Richardson MT, et al. Evaluation of the kaiser physical activity survey in women. Med Sci Sports Exerc 2000 Jul; 32 (7): 1327-38 113. Chasan-Taber L, Schmidt MD, Roberts DE, et al. Development and validation of a pregnancy physical activity questionnaire. Med Sci Sports Exerc 2004 Oct; 36 (10): 1750-60 114. CSEP. Physical activity readiness medical evaluation for pregnancy (PARmed-x for Pregnancy) 2002 [online]. Available from URL: http://www.csep.ca/english/view. asp?x=698 [Accessed 2011 Mar 21] 115. Jaque-Fortunato SV, Wiswell RA, Khodiguian N, et al. A comparison of the ventilatory responses to exercise in pregnant, postpartum, and nonpregnant women. Semin Perinatol 1996 Aug; 20 (4): 263-76 116. Soultanakis HN, Artal R, Wiswell RA. Prolonged exercise in pregnancy: glucose homeostasis, ventilatory and cardiovascular responses. Semin Perinatol 1996 Aug; 20 (4): 315-27 117. Hill-Smith I. Professional and patient perspectives of NICE guidelines to abandon maternal monitoring of fetal movements. Br J Gen Pract 2004 Nov; 54 (508): 858-61
Correspondence: Gerald S. Zavorsky, PhD, Director, Human Physiology Laboratory; Associate Professor, Marywood University, 2300 Adams Avenue, Scranton, PA 18509, USA. E-mail:
[email protected]
Sports Med 2011; 41 (5)
Sports Med 2011; 41 (5): 361-376 0112-1642/11/0005-0361/$49.95/0
REVIEW ARTICLE
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Athletic Osteitis Pubis Corey J. Hiti,1,2 Kathryn J. Stevens,3 Moira K. Jamati,1 Daniel Garza1 and Gordon O. Matheson1,2 1 Division of Sports Medicine, Department of Orthopaedic Surgery, Stanford University, Palo Alto, California, USA 2 Program in Human Biology, Stanford University, Palo Alto, California, USA 3 Department of Radiology, Stanford University, Palo Alto, California, USA
Contents Abstract. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Definition and Clinical Presentation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. Anatomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5. Incidence and Epidemiology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6. Aetiology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7. Differential Diagnosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8. Imaging . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9. Treatment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.1 Conservative Therapy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.2 Local Injections . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.3 Surgical Treatment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Abstract
361 362 362 362 363 365 365 366 367 369 370 371 372 373
Athletic osteitis pubis is a painful and chronic condition affecting the pubic symphysis and/or parasymphyseal bone that develops after athletic activity. Athletes with osteitis pubis commonly present with anterior and medial groin pain and, in some cases, may have pain centred directly over the pubic symphysis. Pain may also be felt in the adductor region, lower abdominal muscles, perineal region, inguinal region or scrotum. The pain is usually aggravated by running, cutting, hip adduction and flexion against resistance, and loading of the rectus abdominis. The pain can progress such that athletes are unable to sustain athletic activity at high levels. It is postulated that osteitis pubis is an overuse injury caused by biomechanical overloading of the pubic symphysis and adjacent parasymphyseal bone with subsequent bony stress reaction. The differential diagnosis for osteitis pubis is extensive and includes many other syndromes resulting in groin pain. Imaging, particularly in the form of MRI, may be helpful in making the diagnosis. Treatment is variable, but typically begins with conservative measures and may include injections and/or surgical procedures. Prolotherapy injections of dextrose, anti-inflammatory corticosteroids and a variety of surgical procedures have been reported in the literature with varying efficacies. Future studies of athletic osteitis pubis should attempt to define specific and
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reliable criteria to make the diagnosis of athletic osteitis pubis, empirically define standards of care and reduce the variability of proposed treatment regimens.
1. Introduction Groin pain is a common problem for many athletes, especially those who participate in sports that involve kicking, rapid accelerations and decelerations, and sudden directional changes.[1,2] The differential diagnosis for groin pain, however, is extensive and presents a significant diagnostic challenge to physicians.[3-5] Often listed amongst the many causes of groin pain in athletes is the condition osteitis pubis.[2,4] The condition was described as a complication of suprapubic surgery in 1924 by Beer and was first described in an athlete in 1932.[6-8] Definitions of osteitis pubis in the medical literature since these first publications have continued to be quite variable, with the term describing pain in the pubic bone as a result of vaginal birth, pelvic and perineal surgery, iatrogenic infection, urinary tract infection, idiopathic infection, rheumatoid arthritis and/or exercise.[5,9-16] However, most authors consider osteitis pubis in athletes to be etiologically distinct from osteitis pubis in non-athletes.[15,17-19] Efforts to differentiate osteitis pubis in athletes from other variants of osteitis pubis have resulted in additional terms, such as ‘pubic bone stress injury’,[20-22] ‘symphysis pubis stress injury’[19] and ‘traumatic osteitis pubis’, that describe similar clinical entities.[1,23] We present a review of the literature to examine current knowledge of athletic osteitis pubis, and to examine practices and future treatments for the optimal rehabilitation of athletes. 2. Methods The MEDLINE database was searched using the PubMed search engine and the combinations of keywords and MeSH terms listed in table I. Search results were limited to those written in English and published between 1 January 1989 and 16 July 2009. The search yielded a total of 217 hits. The abstracts of the corresponding reª 2011 Adis Data Information BV. All rights reserved.
search papers were then evaluated for their relevance to the research question: what are the best practices for diagnosing and treating athletes with osteitis pubis? Studies using patients who experienced osteitis pubis as a result of a prior surgical procedure, arthritis, postpartum complication, renal failure, bacterial infection or tuberculosis were excluded due to their limited role in the aetiology of the disease in athletic populations. Studies that addressed only fractures, stress fractures, dislocations, hernias, open-book injuries and apophyseal avulsion injuries were also excluded as they are pathologies distinct from the diagnosis of osteitis pubis. These criteria resulted in the exclusion of 131 search results. The remaining 86 search results corresponded to 59 individual studies. An additional 11 studies were located by examining the references of these 59 studies. 3. Definition and Clinical Presentation Athletic osteitis pubis is a chronic, painful overuse injury of the pubic symphysis and the adjacent parasymphyseal bone.[6,15,24,25] Patients with athletic osteitis pubis present to the clinic with anterior and medial groin pain. In some cases, pain is centered over the pubic symphysis and is tender to palpation.[17,21,26,27] Concomitant pain in the adductor musculature and tenderness of the superior pubic rami are also common symptoms, and may be present unilaterally or bilaterally.[17,21,23] In some cases, pain may be felt in the lower abdominal muscles, perineal region, inguinal region or scrotum.[2,13,23,28-30] The pain is aggravated by running, cutting, hip adduction (against resistance) or flexion, and eccentric loads to the rectus abdominis.[2,23,28,30-32] Other physical findings may include reduced external and internal range of motion at the hip joint,[1,2] sacroiliac joint dysfunction[2,19] and/or weakness of the abductor and adductor muscles.[2] In severe cases a waddling, antalgic gait may be present.[6,27,33,34] The onset of Sports Med 2011; 41 (5)
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Table I. The PubMed search queries and the limits used while searching, with the corresponding number of hits Search date
Search term
Search limits (English)
Hits
7/16/2009
Osteitis pubis (tw)
01/01/1989–7/16/2009
123
7/16/2009
Pubalgia (tw)
01/01/1989–7/16/2009
16
7/16/2009
Rehabilitation [MeSH] AND osteitis pubis (tw)
01/01/1989–7/16/2009
2
7/16/2009
Rehabilitation [MeSH] AND pubic symphysis [MeSH]
01/01/1989–7/16/2009
4
7/16/2009
Rehabilitation [MeSH] AND groin [MeSH]
01/01/1989–7/16/2009
14 19
7/16/2009
Athletic injuries [MeSH] AND pubic symphysis [MeSH]
01/01/1989–7/16/2009
7/16/2009
Athletic injuries [MeSH] AND pubic bone [MeSH]
01/01/1989–7/16/2009
18
7/16/2009
Cumulative trauma disorders [MeSH] AND ‘groin’ [MeSH]
01/01/1989–7/16/2009
6
7/16/2009
Cumulative trauma disorders [MeSH] AND ‘pubic symphysis’ [MeSH]
01/01/1989–7/16/2009
5
7/16/2009
Biomechanics [MeSH] AND pubic symphysis [MeSH]
01/01/1989–7/16/2009
5
7/16/2009
Models, biological [MeSH] AND pubic symphysis [MeSH]
01/01/1989–7/16/2009
5
Total
217
[MeSH] = MeSH keyword; (tw) = textword.
pain is usually gradual and can progress such that the athlete is unable to practice or compete.[35] 4. Anatomy The pubic symphysis is a nonsynovial amphiarthroidal joint situated at the confluence of the two pubic bones.[36] The two pubic bones are lined medially with hyaline cartilage and are separated by a thick fibrocartilaginous disc (figure 1). A thin physiological cleft known as the primary cleft is often found within the fibrocartilage disc.[36] Four ligaments bound the pubic symphysis. The inferior pubic or arcuate ligament forms a strong fibrous arch along the inferior aspect of the pubic symphysis, and blends with the inferior portion of the articular disc. The superior pubic ligament is less substantial and bridges the pubic tubercles, formed partly from the posterior rectus abdominis fascia. The fibres of the anterior pubic ligament blend with the rectus abdominis fascia and the thin posterior pubic ligament diffuses into the intrapelvic abdominal wall fascia.[36] Numerous tendons insert into the symphysis pubis, including the rectus abdominis superiorly and adductor longus tendon inferiorly, which merge anterior to the pubis to form a common structure that adheres to the underlying connective tissues (figures 1b and c). The prepubic connective tissues also act as an anchor point for ª 2011 Adis Data Information BV. All rights reserved.
the adjacent gracilis and adductor brevis tendons. These connective tissues and tendon insertions form the prepubic aponeurotic complex, which receives additional contributions from the transversus abdominis and internal oblique muscles. The prepubic aponeurotic complex has a fibrocartilage component inferiorly that blends with the underlying articular disc and pubic ligaments.[37] The symphysis is innervated with branches of the pudendal and genitofemoral nerves, and its blood supply is derived from branches of all major vessels in the area, including the obturator, internal pudendal, inferior epigastric and medial femoral circumflex arteries.[36] The pelvis and pubic symphysis are sexually dimorphic structures, as one would expect due to the demands of childbirth on the female anatomy. The inner dimensions of the pelvis as well as the fibrocartilaginous disc are wider in women, while the outer dimensions and vertical length of the pubic symphysis are larger in men.[36] The symphysis has 2–3 mm more mobility in women than men, a difference that can increase to 8–10 mm during the hormonal and mechanical changes of pregnancy.[36] The innominate bones function as arches, transferring the weight of the upright trunk from the sacrum to the hips.[36] The fibrocartilaginous disc serves to absorb and dissipate axial and shearing forces on the pubic symphysis.[37] The mobility of the pubic symphysis under normal physiological Sports Med 2011; 41 (5)
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a
b
P
Pect.
SPR F
Add. B OE
P
Pect.
OI
Add L IT
c
R
*
P
Fig. 1. (a) Coronal T2-weighted MRI of the anterior pelvis demonstrates the pubic symphysis (open arrows) bounded superiorly by the superior pubic ligament and inferiorly by the inferior pubic (arcuate) ligament. The adductor longus (Add. L) tendon (white arrow) is seen arising from the inferior aspect of the body of the pubis (P). (b) Axial T1-weighted MRI demonstrating anatomy around the pubic symphysis (open arrow), with the Add. L tendon (white arrow) in close apposition to the prepubic aponeurotic complex (black arrow). (c) Paramedian sagittal T1-weighted MRI demonstrating anatomy around the P. The rectus abdominis (R) inserts into the pubic crest (white *), and fibres can be seen passing inferiorly to blend with fibres of the Add. L at the prepubic aponeurotic complex (arrows). The thick inferior pubic ligament (open arrow) can be seen along the inferior margin of the pubic symphysis. Add. B = adductor brevis; F = femoral head; IT = ischial tuberosity; OE = obturator externus; OI = obturator internus; Pect. = pectineus; SPR = superior pubic ramus.
conditions mainly involves vertical shear and anterior/posterior rotation, with resistance to bending being greater in the superior direction than the inferior direction and greater in the posterior direction than the anterior direction.[38] The relª 2011 Adis Data Information BV. All rights reserved.
atively thick inferior pubic ligament provides the majority of joint stability in day-to-day activities, while the muscle forces acting on the pubic symphysis have considerable influence on the stress patterns in the pelvic bone.[36,38,39] Sports Med 2011; 41 (5)
Athletic Osteitis Pubis
5. Incidence and Epidemiology The true incidence and prevalence of athletic osteitis pubis is unknown, since there have been no epidemiological studies to investigate the condition.[6,40] Some idea of the prevalence and incidence of athletic osteitis pubis may be gained from an epidemiological study of 16 Australian football teams, each with approximately 40 players, followed over the course of a 4-year period.[41] This study reported the prevalence of groin strain as 1.35% and the incidence as 3.3 injuries per club per season, while the prevalence of ‘other’ groin/ hip/thigh injuries was reported as 0.26% with an incidence of 0.7 per club per season. Athletic osteitis pubis would likely fall into the category of ‘other’ groin injuries in this study; however, the study did not list specific diagnoses for each category and thus it is unknown to what degree athletic osteitis pubis contributed to the values reported by these authors. Perhaps a more direct method of estimating the prevalence and incidence of athletic osteitis pubis is to examine case series of athletes experiencing chronic groin injury in which athletic osteitis pubis was considered as a possible diagnosis. In one study of 189 athletes experiencing groin pain, athletic osteitis pubis was found to be the primary cause of pain in 14% of the athletes and a secondary cause in an additional 6%.[42] A study utilizing MRI of 97 athletes with groin pain reported the prevalence of isolated athletic osteitis pubis as 9.3%, while athletic osteitis pubis with concomitant adductor microtear was found in 42.3% of patients.[43] These reports demonstrate that athletic osteitis pubis may be a rather prevalent source of groin injury in the athletic population; however, they also illustrate the limitation of this method – the significant variance between the values reported. This phenomenon is likely attributable to the current absence of standardized diagnostic criteria available for athletic osteitis pubis, as well as true variability between different sports. One reliable trend that has emerged from the available data is the much greater prevalence of athletic osteitis pubis in men than in women.[6,17,42] As postulated by Johnson[6] in his review, this ª 2011 Adis Data Information BV. All rights reserved.
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may be a result of a broader sex disparity in athletic participation rather than a susceptibility of men to the condition. Evidence for the latter, however, may derive from the aforementioned anatomical differences between the male and female pelvis that affect the mechanical properties of the joint;[38] although to what extent these anatomical differences influence the sex distribution of athletic osteitis pubis is unknown. Despite the paucity of data to accurately define the incidence and prevalence of athletic osteitis pubis, it has been identified as an important contributor to groin pain in the athletic population and especially in sports, such as soccer, rugby, Australian Rules football, running and skating, that require kicking, twisting and frequent lateral movements.[2,4,5,26,44] Thus, knowledge of the condition is essential for all health practitioners who treat athletes presenting with groin pain. 6. Aetiology Abnormal physical stresses at the pubic symphysis and parasymphyseal bone have been singled out as the likely cause of osteitis pubis in the athlete.[17,21,24,29,30] Yet, what generates these abnormal physical stresses is debated in the literature. As stated in section 4, the muscle forces acting on the pubic symphysis have considerable influence on the stress patterns in the pelvic bone.[36,38,39] Omar et al.[45] hypothesize that the antagonistic relationship between the adductor longus muscle, producing an anterior-inferior force on the pubic symphysis, and the rectus abdominis muscle producing a posterior-superior force on the pubic symphysis, is particularly influential on the biomechanics of the pubic symphysis. Thus, they believe that alterations in the load-bearing characteristics of either tendon can lead to alterations in the biomechanics of the joint and instability of the pubic symphysis.[45] Another theory has focused upon hip joint range of motion in athletes experiencing athletic osteitis pubis. In 1978, Williams[46] published a study that found that all athletes examined showed some loss of internal rotation of the hip. The study postulated that reduced internal motion of the hip joint led to shearing stress in the pelvis, which Sports Med 2011; 41 (5)
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in turn led to anteroposterior movement of one hemipelvis in relation to the other during extension, and proximo-distal movement in flexion. This hypothesis was further examined in a study by Verrall et al.[1] who found a significant association between the loss of both external and internal range of motion in athletes experiencing athletic osteitis pubis. Yet, as stated in the study by Verrall et al.,[1] it is unclear from these investigations whether reduced hip joint range of motion was a predisposing factor to the development of athletic osteitis pubis or a consequence of the injury itself. Other authors have investigated the association of sacroiliac abnormalities with athletic osteitis pubis. Harris and Murray[47] first postulated that instability of the sacroiliac joint may lead to a secondary stress reaction at the pubic symphysis resulting in athletic osteitis pubis. A more recent study by Major and Helms[19] found that 6 of 11 athletes with diagnosed athletic osteitis pubis had concomitant imaging findings indicative of sacroiliac abnormality. These studies theorize that the anatomy of the pelvic ring is such that stresses placed on it by abnormal motion at either the sacroiliac joints or the pubic symphysis can cause instability and lead to athletic osteitis pubis.[19] Whatever the cause of increased biomechanical stress at the pubic symphysis and parasymphyseal bone region, it is postulated that over time these biomechanical stresses lead to an overuse injury at the pubic symphysis and/or parasymphyseal bone. Evidence supporting this possibility comes from two histological studies examining bone and cartilage samples taken during surgical procedures on athletes being treated for athletic osteitis pubis. The first study, conducted by Verrall et al.,[15] examined bone biopsies taken from the superior pubic ramus/rami of Australian Rules football players diagnosed as having pubic bone stress injuries. Pathological examination of these specimens revealed the absence of inflammatory cells or signs of osteonecrosis. They did, however, demonstrate the formation of new woven bone with plump osteoblasts, neovascularization and stellate fibroblasts.[15] The authors concluded that these findings were consistent with the hypothesis ª 2011 Adis Data Information BV. All rights reserved.
that the pathological cause of their patients’ chronic groin pain was a bony stress response rather than an inflammatory process, and that avascular necrosis and venous congestion were unlikely to contribute to the aetiology of the disease. In a separate study by Radic and Annear,[25] cartilage samples taken from 15 athletes treated with curettage of the fibrocartilage disc and hyaline endplates of both pubic bodies, demonstrated evidence of degenerative cartilage and lacked significant inflammatory infiltrate. These studies, taken together, suggest that biomechanical overloading leads to a bony stress response in the parasymphyseal bone and/or degenerative changes in the cartilage of the pubic symphysis. Of particular interest in both of the above studies was the conspicuous absence of inflammatory findings, despite the widely published description of athletic osteitis pubis as a disease of inflammation.[14,23,32,35] These claims seem to stem from the histological findings of seven cases published by Coventry and Mitchell[48] in 1961. Their findings included evidence of marrow fibrosis, vascular areas, thin layers of new bone, significant numbers of polymorphonuclear leukocytes and bone with hyaline cartilage degeneration and resorption of bone.[6,48] The patient population used by Coventry and Mitchell,[48] however, did not include athletes and, instead, was composed of patients with a prior history of pelvic surgery and infection. It thus seems likely that their findings are not representative of the pathological process occurring in athletes experiencing athletic osteitis pubis.[6,17,48] Additional histological studies should be performed to replicate the findings of Verrall et al.[15] in patients experiencing the athletic variant of osteitis pubis and to further characterize the pathology of athletic osteitis pubis. 7. Differential Diagnosis It can be difficult to diagnose osteitis pubis, which often means that the diagnosis is missed, or is only made after a number of follow-up visits.[5,6,12,23,44] Osteitis pubis shares many of its symptoms with other groin injuries and thus must be differentiated from a number of other conditions Sports Med 2011; 41 (5)
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including adductor tendon dysfunction, injuries to the prepubic aponeurotic complex, stress fracture, incipient direct inguinal hernia (also termed prehernia complex or sportsperson’s hernia), posterior inguinal wall deficiency, intra-articular hip pathology, femoroacetabular impingement, iliopsoas injury and abnormality of the lower lumbar spine.[21,42,49-51] However, this is not to say that these other pathologies of the groin cannot co-occur with athletic osteitis pubis. In fact, the diagnosis of athletic osteitis pubis is often complicated by the co-occurrence of other groin injuries.[16,24,42] Perhaps the most important differential diagnosis of osteitis pubis is osteomyelitis of the pubis, as both present in a similar fashion and have been reported to occur spontaneously in athletes.[4,6,34] Osteomyelitis of the pubis can be differentiated from osteitis pubis based on the acute, atraumatic onset of symptoms mimicking osteitis pubis, accompanied by non-specific changes of raised levels of acute-phase proteins and mild leukocytosis due to its infectious aetiology.[6] This distinction is important to make, as their courses of treatment differ greatly. Positive provocation tests such as the ‘lateral compression test’, ‘squeeze test’, ‘cross-leg test’, ‘Patrick (FABER) test’ and ‘quadrant test’ can be helpful in differentiating osteitis pubis from other conditions.[22,27,28,35,52] However, the specificity of these tests for athletic osteitis pubis is unknown. Imaging studies are not pathognomonic, but are generally used to help confirm the diagnosis and exclude other pathologies of the groin.[16] 8. Imaging Osteitis pubis has historically been investigated using both standard anteroposterior radiographs and 99mTc-methylenediphosphonate triple-phase bone scans.[17,21,33] Positive bone scans in athletic osteitis pubis show increased tracer uptake in the region of the pubic symphysis and parasymphyseal bone, especially on the delayed images.[17,21,33] However, the degree of uptake is poorly correlated with the duration and severity of symptoms.[21] Standard anteroposterior radiographs may show widening of the symphysis, sclerosis or rarefacª 2011 Adis Data Information BV. All rights reserved.
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tion at the symphysis, cystic changes or marginal erosions in the subchondral bone (figures 1 and 2).[47,53] Often ‘flamingo view’ x-rays are taken to evaluate for pubic instability, defined as a vertical shift greater than 2 mm, or widening greater than 7 mm across the symphysis while standing on one leg.[17,26] However, these changes need to be correlated with the patient’s symptoms, as similar x-ray findings can be seen in asymptomatic athletes, or athletes experiencing different pathologies.[47] In addition, x-ray changes in the early or mild forms of the disease may be absent.[17,21,26,54] CT is used selectively, and may show marginal ‘stamp erosions’ of the parasymphyseal pubis, an insertional bony spur or periarticular microcalcifications better than MRI (figure 2).[55] MRI has become the diagnostic modality of choice when an advanced imaging technique is required, as it has superior visualization of softtissue abnormalities and changes within the bone marrow, as well as multiplanar imaging capabilities[6,50,55,56] (figures 2 and 3). MRI studies of patients presenting with anterior pelvic pain should include dedicated high-resolution imaging of the pubic symphysis and its musculotendinous attachments, as well as imaging of the entire pelvis using a larger field of view, which helps exclude abnormalities of the hips or other bony and soft tissue structures that can mimic osteitis pubis. MRI findings in athletic osteitis pubis of <6-months duration include bone marrow oedema, linear high T2 signal intensity in the parasymphyseal pubis and fluid within the pubic symphysis,[22,24,50] whereas subchondral sclerosis, subchondral resorption with bony irregularity and osteophytosis or pubic beaking is usually apparent in more chronic disease.[24] Bone marrow oedema in the pubic bones usually appears relatively symmetrical in athletic osteitis pubis.[16,57,58] There has been much debate in the literature regarding the clinical significance of bone marrow oedema. In 2001, Verrall et al.[21] proposed that bone marrow oedema might be directly related to athletic osteitis pubis after their experiment correlated the extent of pubic bone marrow oedema with the severity of clinical symptoms, and demonstrated that all symptomatic athletes displayed prominent bone marrow oedema within the pubis. Sports Med 2011; 41 (5)
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a
b
c
d
Fig. 2. (a) Anteroposterior radiograph of the pelvis demonstrating subtle sclerosis within the right parasymphyseal pubis (open arrow) in comparison to the left. (b) On the corresponding coronal T1-weighted image there is low T1 signal intensity within the right pubis corresponding to the sclerosis on the radiograph (open arrow). (c) Coronal; and (d) axial T2-weighted MRI with fat saturation demonstrate reactive bone marrow oedema around the pubic symphysis, most marked on the right. A secondary cleft sign is apparent on the right (arrow).
This finding was later discussed by Lovell et al.,[49] who found that all of the symptomatic athletes in their study demonstrated substantial marrow oedema within the pubic bone, but indicated that a proportion of asymptomatic athletes in both studies also presented with pubic bone marrow oedema. The bone marrow oedema ª 2011 Adis Data Information BV. All rights reserved.
seen within the pubic symphysis, therefore, most likely reflects a reaction of the bone to external stress, rather than necessarily being pathological. More recently, a distinct band of linear high T2 signal has been described in the parasymphyseal bone, paralleling the subchondral bone plate of the pubis.[22,50] This hyper-intense line is found in Sports Med 2011; 41 (5)
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the most symptomatic athletes, and may prove to be more clinically relevant than bone marrow oedema.[28] The secondary cleft sign is another finding that has been described on MRI in athletes with groin pain, corresponding to abnormal inferior extension of the cleft in the symphyseal fibrocartilage that is thought to reflect a microtear of the adductor enthesis[16,59,60] (figures 2c and d). In one study, a secondary cleft was present in four of six athletes with osteitis pubis.[58,60] A more recent study imaged 100 patients with groin pain, and 97 of these were attributed to pathology at the pubic symphysis, with 3 demonstrating pathology at other sites.[43] A secondary cleft sign was identified in 88 of the 97 patients. Bone marrow oedema was seen in 91 of the 100 patients; in 51 cases there was focal bone marrow oedema in the pubic tubercle at the adductor insertion, with 49 of these displaying an adductor microtear. Forty patients demonstrated a more diffuse pattern of bone marrow oedema considered secondary to osteitis pubis, but 31 of these also had evidence of an adductor tear. The study concluded that osteitis pubis and adductor dysfunction frequently coexist, and speculated that adductor dysfunction may precede the development of osteitis pubis. However, further research is still required to clarify the prognostic value of the secondary cleft sign.[60]
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all fail to rise above level 4 evidence.[32] With these limitations in mind, the current principles of treatment are examined below. a
b
[R]
[L]
c
9. Treatment Although athletic osteitis pubis typically improves with rest and has thus been described as a self-limiting process, it is clear that extended rest is not always feasible or desirable for highly competitive athletes.[2,6,17,18,61] An array of treatment approaches ranging from rest and rehabilitation, to a variety of injections and surgeries are reported in the literature. The trend is to initiate conservative treatment in the form of rest and/or supervised rehabilitation, resorting to the more invasive interventions only if outcomes are unsatisfactory.[10,18,23,61-64] Unfortunately, none of the studies examining the treatment of osteitis pubis directly compare treatment modalities, and ª 2011 Adis Data Information BV. All rights reserved.
[R]
[L]
Fig. 3. (a) Anteroposterior radiograph; and (b) axial CT of the pelvis demonstrate stamp erosions of the pubic symphysis on the left (arrow). (c) Axial T2-weighted image with fat saturation demonstrates prominent bone marrow oedema within the left pubis (arrow).
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9.1 Conservative Therapy
Studies examining the effectiveness of rehabilitation programmes for osteitis pubis are exceedingly rare in the literature. A literature search using PubMed and an examination of references cited by other articles identified three case series and one case report with data concerning the conservative treatment of osteitis pubis that met our inclusion criteria[22,35,65,66] (see table II). All of the studies propose treatment regimens that incorporate a graded or progressive approach in which less stressful and simple exercises precede more stressful and complex exercises. However, the interventions used were extremely variable between studies and, in some cases, were not standard for all athletes treated within a given study. It is not surprising that the variable treatments utilized among these studies produced widely
varying reports of success and time to recovery. While Rodriguez et al.[35] report athletes returning to asymptomatic participation as early as 3 days after initiating treatment and a 100% success rate in 35 soccer players by 10 weeks, the 27 male Australian football players in a study by Verrall et al.[22] were not even permitted to attempt running for a minimum of 12 weeks. At 5 months after the initial diagnosis of athletic osteitis pubis, only 41% of the athletes treated by Verrall et al. reported a symptom-free return to sport. After 2 years, 19% of athletes remained symptomatic with play and 26% were playing at a lower level of competition. A case series of four youth soccer players treated by Wollin and Lovell[66] reports 100% of athletes returning to play symptom free after 10–16 weeks of treatment, with no recurrence of symptoms on a 1-year follow-up. The absence of control groups and the variability in treatments utilized in these studies make
Table II. Conservative treatment studies of osteitis pubis Study
Study design (sample size)
Treatment
Time to pain-free return to play
Success rate (%)a
Rodriguez et al.[35]
Case series (n = 35)
Oral ibuprofen 800 mg three times daily for 14 d, daily application of therapeutic modalities (cryomassage, laser, ultrasound or electric stimulation) for 14 d, flexibility exercises emphasizing the adductors, strengthening exercises emphasizing both abductors and adductors and a progressive running programme
3 d to10 wk
100
Verrall et al.[22]
Case series (n = 27)
Non-weight-bearing exercises for 12 wk, followed by a non-standardized pelvic core stability programme 3–6 wk into the treatment period
5–24 mo
81
Wollin and Lovell[66]
Case series (n = 4)
Rehabilitation programme consisting of four modules, beginning with pain reduction, pelvic floor and transversus abdominis retraining with real-time ultrasound and isometric hip adduction. Modules 2–4 incorporated a progressive core stability, gluteal and adductor muscle conditioning, and two running programmes undertaken every second day. LIPUS was used for 20 min od over the area of bone marrow oedema, and patients used neoprene groin shorts during running programmes
10–16 wk
100
McCarthy and Vicenzino[65]
Case report (n = 1)
5 wk of supervised PT initiated 3 wk after injury. Rehabilitation consisted of a progression from static trunk, pelvic and hip stability exercises to more complex strength and stability work (increasingly dynamic and sport specific). Passive stretching was incorporated only after key muscle groups were well trained
5 wk
100
a
The success rate is given as the percentage of patients who returned to sport and were asymptomatic at the end of the recovery period listed. The beginning of the recovery period is based on the earliest report of success in that particular study. Sample sizes and success rates are based upon the number of patients who completed treatment.
LIPUS = low-intensity pulsed ultrasound; PT = physical therapy.
ª 2011 Adis Data Information BV. All rights reserved.
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Table III. Injection treatment studies of osteitis pubis Study
Study design (sample size)
Treatment
Time to pain-free return to play
Success rate (%)a
Holt et al.[23]
Case series (n = 12)
Nine athletes were treated with a prolonged rest period, oral NSAIDs, hip stretching exercises and a progressive impact programme. Eight of the athletes subsequently received corticosteroid injections into the pubic symphysis, while the ninth one was asymptomatic after the initial treatment. Three athletes in the latter part of the study received corticosteroid injections within 7–10 d of the onset of symptoms if conservative treatment during this interval failed to reduce symptoms
2–24 wk
91
O’Connell et al.[58]
Case series (n = 16)
Injection of 20 mg of methyprednisolone acetate and 1 mL of 0.5% bupivacaine hydrochloride into the symphyseal cleft followed by immediate mobilization
48 h to 6 mo
31
Batt et al.[12]
Case series (n = 2)
Initially treated with ice, local modalities, avoidance of aggravating activities and NSAIDs. Subsequently treated with betamethasone injection into and around the pubic symphysis as well as a course of oral indomethacin and an aggressive stretching routine. The corticosteroid injection was repeated in both cases
12 mo
0
Topol et al.[61]
Case series (n = 24)
Prolotherapy injection, consisting of 12.5% dextrose and 0.5% lidocaine, in eight separate sites on the pelvis until isometric contraction of abdominals and adductors was pain free. This was followed by a period of rest and progressive exercise allowances and re-injection at 4-wk intervals if still symptomatic
6–32 mo
83
Topol et al.[67]
Case series (n = 72)
Prolotherapy injection, consisting of 12.5% dextrose and 0.5% lidocaine, in eight separate sites on the pelvis until isometric contraction of abdominals and adductors was pain free. This was followed by a period of rest and progressive exercise allowances and re-injection at 4-wk intervals if still symptomatic
1–5 mo (mean 3)
89
a
The success rate is given as the percentage of patients who returned to sport and were asymptomatic at the end of the recovery period listed. The beginning of the recovery period is based on the earliest report of success in that particular study. Sample sizes and success rates are based upon the number of patients who completed treatment.
it difficult to meaningfully compare their relative efficacies. Furthermore, only Wollin and Lovell[66] present clear criteria for progression through their rehabilitation programme. Considered as a group, these studies suggest that prolonged rest and passive treatment correlate with delayed recovery and lingering symptoms. Common aims of treatment across studies included reducing loaded weight-bearing activities during the initial stages of treatment, improving hip range of motion, addressing biomechanical faults such as limitations of sacroiliac and lumbosacral movement and improving stability of the pelvic and core muscles. Future investigations should specify the nature of the intervention, and functional and clinical criteria for progression and successful treatment. ª 2011 Adis Data Information BV. All rights reserved.
9.2 Local Injections
Injections administered in the treatment of osteitis pubis may be generally classified as either anti-inflammatory or regenerative and have been reported in five separate studies[12,23,58,61,67] (table III). Three case series report favourable results relative to return to sport participation after injection of corticosteroid directly into the symphyseal cleft and surrounding tissues.[12,23,58] The two cases reported by Batt et al.[12] resulted in two football players returning to sport, but not without complication. Both players returned to participation and experienced a relapse in symptoms resulting in a repeat course of treatment, including rest and multiple injections. Despite successfully returning to participation for a second Sports Med 2011; 41 (5)
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time, both players continued to report persistent symptoms. Holt et al.[23] reported successful return to sport in 11 of 12 cases, with more rapid return in patients who had the procedure within the first 2 weeks of diagnosis. Other patients in this study with more chronic symptoms required multiple injections and up to 2 years to recover. O’Connell et al.[58] report that 14 of 16 patients experienced immediate relief of some symptoms and were able to return to sport within 48 hours of the procedure. However, at 6-month followup, only five patients remained symptom free. One of these five did not respond to the injection within the first 48 hours and symptom resolution at 6 months was attributed to rest following the procedure. These studies demonstrate similar limitations to the case series described in the conservative treatment section, including the lack of control subjects and the use of return to sport as the sole criterion for success. Additionally, the duration of the study significantly impacts the reported success of the treatment. For instance, if O’Connell et al.[58] had not conducted a 6-month follow-up, they would have reported a success rate of 87% in contrast to 31%. Two studies by Topol et al.[61,67] evaluate the use of regenerative injection therapy in osteitis pubis using dextrose. The authors theorize that osteitis pubis is a degenerative process, rather than a change induced by inflammation, and that injection of dextrose into the symphysis and surrounding tissues promotes tendon, ligament and cartilage repair. Their first paper reported that prolotherapy with local injection of dextrose was effective in 22 of 24 cases.[61] Of 24 patients (all male rugby and soccer players), two did not respond to the therapy; 22 patients were fully participatory in sports within 3 months and at follow-up (average 17.2 months), with 20 reporting no pain with full participation. In a second, more extensive case-control study, the authors demonstrated that 66 of 72 athletes were able to return to athletic participation in a mean time of <3 months (1–5 months) with an average of three prolotherapy treatments.[67] It is notable that all patients had not improved with conservative treatment before beginning treatment with prolotherapy. Post-treatment follow-up occurred anywhere ª 2011 Adis Data Information BV. All rights reserved.
from 6 to 73 months following the cessation of prolotherapy treatment (average of 23 months), and demonstrated a significant reduction in pain using both the visual analogue scale (82% improvement) and Nirschl pain phase scale (78% improvement). While none of the injection studies was experimental in design, all reported positive outcomes relative to return to sport participation. With localized anti-inflammatory injections, ongoing symptoms were reported by many patients treated despite returning to play. Additionally, the time between treatment and return to play was also extremely variable in the athletes studied. The limited literature regarding regenerative dextrose injections indicates that prolotherapy may be a novel and effective way to treat athletic osteitis pubis; however, the efficacy of dextrose prolotherapy and mechanism of action is contested in the literature.[68] It is important to note that a multitude of injection sites were utilized in these studies (including both the pubic symphysis and nearly all sites of muscle attachments into the ischiopubic rami) and, thus, no specific pathology is targeted. Further studies in this area by additional investigators should aim to replicate the success achieved by Topol et al.[61,67] with a controlled experimental design and more specific sites of injection. 9.3 Surgical Treatment
Surgical techniques utilized in the treatment of athletic osteitis pubis include curettage of the symphysis pubis with or without subsequent arthrodesis of this joint alone,[10,25,64] and a variety of procedures to reinforce or repair the abdominal and pelvic floor musculature, with or without a release of the adductor tendons.[18,62,63,69-71] A study by Williams et al.[64] utilized curettage with subsequent arthrodesis of the symphysis in seven rugby players, resulting in a return to full match fitness between 5 and 9 months, post-operatively (mean of 6.6 months). Complications included post-operative haemospermia for 6 weeks in one patient, intermittent scrotal swelling with exercise for 6 months in another patient and a stress fracture running through the arthrodesis of a patient Sports Med 2011; 41 (5)
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that necessitated a second attempt at arthrodesis. Mulhall et al.[10] reported successful return to play within 6 months following curettage of the symphysis alone in two male professional soccer players, while Radic and Annear[25] reported that 16 of 24 patients undergoing the same procedure returned to full activity in a range of 2.5–12 months. These authors felt that curettage without subsequent arthrodesis of the symphysis allowed their patients a more rapid return to activity, and avoided the attendant risks of internal fixation. Of the papers describing repair or reinforcement of the abdominal and pelvic soft tissues, it is unclear if an alternate diagnosis (i.e. hernia or damaged contractile tissue) was the precursor to the development of groin pain, and only one limited the subject pool to specific cases of osteitis pubis. Paajanen et al.[18] describe a procedure using an endoscopic extraperitoneal technique using a polypropylene mesh placed posterior to the pelvic tubercle. In a case series, the authors reported success with all five elite male athletes: all returned to sport 4–8 weeks after the procedure, and all reported absence of symptoms at 1-month and 1-year, post-operatively. They advocate the procedure for athletes without evidence of pelvic instability, and report a low morbidity with this minimally invasive approach. The mesh is thought to provide firm support while evenly distributing muscle pressure in this vulnerable area for athletes who train heavily. The surgical treatments for athletic osteitis pubis reported in the literature vary widely in their invasiveness, impact on pelvic biomechanics and recovery time frame. However, little evidence exists to support one surgical method over another or the necessity of surgery itself. Indeed, some authors suggest that surgical treatment should never be undertaken for athletic osteitis pubis.[17] The fact that the majority of patients treated surgically have been professional athletes may indicate that the average patient does not require surgical treatment.[10,64,71] The propensity of professional athletes to return to sport regardless of treatment outcomes further complicates the interpretation of studies using ‘return to sport’ as the sole criterion for assessing the sucª 2011 Adis Data Information BV. All rights reserved.
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cess of surgical procedures. Further studies are necessary to determine if and when surgical procedures are necessary for the treatment of athletic osteitis pubis. 10. Conclusions Athletic osteitis pubis is an overuse injury of the parasymphyseal pubic bone and/or pubic symphysis caused by mechanical overloading. It is an important pathology to consider in the differential diagnosis of chronic groin pain in athletes, especially those who participate in sports, such as soccer and Australian Rules football, which require kicking and cutting movements. Significant confusion exists in the literature due to the historical variability of pathologies described by the term, ‘osteitis pubis’. In this review, we have used the term ‘athletic osteitis pubis’ to make this historical connection to previous studies clear. However, given the mounting evidence describing the aetiology as a bony stress injury rather than a disease of inflammation, it is perhaps more accurate to describe the condition using the term ‘pubic bone stress injury’ than as a true ‘osteitis’. No standardized diagnostic criteria exist for athletic osteitis pubis, likely due to its extensive differential diagnosis and frequent co-occurrence with other pathologies of the groin. Symptoms typically include anterior and medial pelvic pain centered over the pubic symphysis, concomitant pain in the adductor musculature and/or tenderness of the superior pubic rami present unilaterally or bilaterally, as well as lower abdominal pain. Provocation tests, such as the ‘lateral compression test’, ‘squeeze test’, ‘cross-leg test’, ‘Patrick (FABER) test’ and ‘quadrant test’, have been used to help differentiate athletic osteitis pubis from other conditions. Standard anteroposterior radiographs and CT scans are useful for showing irregularities of the pubic bone including widening of the symphysis, sclerosis or rarefaction at the symphysis, cystic changes and marginal erosions in the subchondral bone. However, MRI is best for imaging osteitis pubis as it allows visualization of soft tissue abnormalities in multiple planes, and can also demonstrate changes in the Sports Med 2011; 41 (5)
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bone such as bone marrow oedema. Patient history, the results of physical examination and imaging findings are all important components for making the diagnosis. Treatment of osteitis pubis is variable but generally begins with physical therapy and other conservative measures, progressing to injections and finally to surgical intervention if necessary. Improving hip range of motion, addressing biomechanical faults such as limitations of sacroiliac and lumbosacral movement and improving stability of the pelvic and core muscles through progressive exercises are important components of a successful rehabilitation programme; however, future studies should focus on defining functional and clinical criteria for progression through conservative treatment programmes. Understanding athletic osteitis pubis as a bony stress response rather than an inflammatory process may help to explain the marginal results resulting from corticosteroid therapy. The use of dextrose prolotherapy has shown promising results in the treatment of athletic osteitis pubis; however, the lack of studies replicating these results cautions against implementing this treatment at the current time. Although a number of surgical treatments for recalcitrant osteitis pubis have been described in the literature, it is unclear at this time whether surgery should play a role in the treatment of athletic osteitis pubis. Future studies of athletic osteitis pubis should attempt to define specific and reliable criteria to make the diagnosis of athletic osteitis pubis, empirically define standards of care and reduce the variability of proposed treatment regimens. Acknowledgements The authors declare no conflicts of interest that are pertinent to the content of this review. No sources of funding were used to prepare this review.
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diagnosed as pubic bone stress injury. Am J Sports Med 2007 Mar; 35 (3): 467-74 Holt MA, Keene JS, Graf BK, et al. Treatment of osteitis pubis in athletes: results of corticosteroid injections. Am J Sports Med 1995 Sep-Oct; 23 (5): 601-6 Kunduracioglu B, Yilmaz C, Yorubulut M, et al. Magnetic resonance findings of osteitis pubis. J Magn Reson Imaging 2007 Mar; 25 (3): 535-9 Radic R, Annear P. Use of pubic symphysis curettage for treatment-resistant osteitis pubis in athletes. Am J Sports Med 2008 Jan; 36 (1): 122-8 Nelson EN, Kassarjian A, Palmer WE. MR imaging of sports-related groin pain. Magn Reson Imaging Clin N Am 2005 Nov; 13 (4): 727-42 Barry NN, McGuire JL. Acute injuries and specific problems in adult athletes. Rheum Dis Clin North Am 1996 Aug; 22 (3): 531-49 Braun P, Jensen S. Hip pain: a focus on the sporting population. Aust Fam Physician 2007 Jun; 36 (6): 406-8, 410-3 Lynch SA, Renstrom PA. Groin injuries in sport: treatment strategies. Sports Med 1999 Aug; 28 (2): 137-44 Shaker AM, Shaheen MA, O’Neel PJ. Traumatic aseptic osteitis pubis. Ann Saudi Med 1991 Mar; 11 (2): 205-8 O’Kane JW. Anterior hip pain. Am Fam Physician 1999 Oct 15; 60 (6): 1687-96 Choi H, McCartney M, Best TM. Treatment of osteitis pubis and osteomyelitis of the pubic symphysis in athletes: a systematic review. Br J Sports Med 2011; 45 (1) 57-64 Briggs RC, Kolbjornsen PH, Southall RC. Osteitis pubis, Tc-99m MDP, and professional hockey players. Clin Nucl Med 1992 Nov; 17 (11): 861-3 Pauli S, Willemsen P, Declerck K, et al. Osteomyelitis pubis versus osteitis pubis: a case presentation and review of the literature. Br J Sports Med 2002 Feb; 36 (1): 71-3 Rodriguez C, Miguel A, Lima H, et al. Osteitis pubis syndrome in the professional soccer athlete: a case report. J Athl Train 2001 Dec; 36 (4): 437-40 Gamble JG, Simmons SC, Freedman M. The symphysis pubis: anatomic and pathologic considerations. Clin Orthop Relat Res 1986 Feb; (203): 261-72 MacMahon PJ, Hogan BA, Shelly MJ, et al. Imaging of groin pain. Magn Reson Imaging Clin N Am 2009; 17 (4): 655-66 Li Z, Alonso JE, Kim JE, et al. Three-dimensional finite element models of the human pubic symphysis with viscohyperelastic soft tissues. Ann Biomed Eng 2006 Sep; 34 (9): 1452-62 Dalstra M, Huiskes R. Load transfer across the pelvic bone. J Biomech 1995 Jun; 28 (6): 715-24 Haider NR, Syed RA, Dermady D. Osteitis pubis: an important pain generator in women with lower pelvic or abdominal pain: a case report and literature review. Pain Physician 2005 Jan; 8 (1): 145-7 Orchard J, Seward H. Epidemiology of injuries in the Australian Football League, seasons 1997-2000. Br J Sports Med 2002 Feb; 36 (1): 39-44 Lovell G. The diagnosis of chronic groin pain in athletes: a review of 189 cases. Aust J Sci Med Sport 1995 Sep; 27 (3): 76-9 Cunningham PM, Brennan D, O’Connell M, et al. Patterns of bone and soft-tissue injury at the symphysis pubis in
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soccer players: observations at MRI. AJR Am J Roentgenol 2007 Mar; 188 (3): W291-6 Andrews SK, Carek PJ. Osteitis pubis: a diagnosis for the family physician. J Am Board Fam Pract 1998 Jul-Aug; 11 (4): 291-5 Omar IM, Zoga AC, Kavanagh EC, et al. Athletic pubalgia and ‘‘sports hernia’’: optimal MR imaging technique and findings. Radiographics 2008 Sep-Oct; 28 (5): 1415-38 Williams JG. Limitation of hip joint movement as a factor in traumatic osteitis pubis. Br J Sports Med 1978 Sep; 12 (3): 129-33 Harris NH, Murray RO. Lesions of the symphysis in athletes. Br Med J 1974 Oct 26; 4 (5938): 211-4 Coventry MB, Mitchell WC. Osteitis pubis: observations based on a study of 45 patients. JAMA 1961 Dec 2; 178: 898-905 Lovell G, Galloway H, Hopkins W, et al. Osteitis pubis and assessment of bone marrow edema at the pubic symphysis with MRI in an elite junior male soccer squad. Clin J Sport Med 2006 Mar; 16 (2): 117-22 Slavotinek JP, Verrall GM, Fon GT, et al. Groin pain in footballers: the association between preseason clinical and pubic bone magnetic resonance imaging findings and athlete outcome. Am J Sports Med 2005 Jun; 33 (6): 894-9 LeBlanc KE, LeBlanc KA. Groin pain in athletes. Hernia 2003 Jun; 7 (2): 68-71 Jansen JA, Mens JM, Backx FJ, et al. Diagnostics in athletes with long-standing groin pain. Scand J Med Sci Sports 2008 Dec; 18 (6): 679-90 Kneeland JB. MR imaging of sports injuries of the hip. Magn Reson Imaging Clin N Am 1999 Feb; 7 (1): 105-15, viii Pavlov H. Roentgen examination of groin and hip pain in the athlete. Clin Sports Med 1987 Oct; 6 (4): 829-43 De Paulis F, Cacchio A, Michelini O, et al. Sports injuries in the pelvis and hip: diagnostic imaging. Eur J Radiol 1998 May; 27 Suppl. 1: S49-59 Overdeck KH, Palmer WE. Imaging of hip and groin injuries in athletes. Semin Musculoskelet Radiol 2004 Mar; 8 (1): 41-55 Zajick DC, Zoga AC, Omar IM, et al. Spectrum of MRI findings in clinical athletic pubalgia. Semin Musculoskelet Radiol 2008 Mar; 12 (1): 3-12 O’Connell MJ, Powell T, McCaffrey NM, et al. Symphyseal cleft injection in the diagnosis and treatment of osteitis pubis in athletes. AJR Am J Roentgenol 2002 Oct; 179 (4): 955-9 Tuite MJ, DeSmet AA. MRI of selected sports injuries: muscle tears, groin pain, and osteochondritis dissecans. Semin Ultrasound CT MR 1994 Oct; 15 (5): 318-40 Brennan D, O’Connell MJ, Ryan M, et al. Secondary cleft sign as a marker of injury in athletes with groin pain: MR image appearance and interpretation. Radiology 2005 Apr; 235 (1): 162-7 Topol GA, Reeves KD, Hassanein KM. Efficacy of dextrose prolotherapy in elite male kicking-sport athletes with chronic groin pain. Arch Phys Med Rehabil 2005 Apr; 86 (4): 697-702 Ahumada LA, Ashruf S, Espinosa-de-los-Monteros A, et al. Athletic pubalgia: definition and surgical treatment. Ann Plast Surg 2005 Oct; 55 (4): 393-6
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63. Moyen B, Mainetti E, Sansone V, et al. Surgical treatment of pubic pain refractory to conservative treatment. Ital J Orthop Traumatol 1993; 19 (1): 43-9 64. Williams PR, Thomas DP, Downes EM. Osteitis pubis and instability of the pubic symphysis: when nonoperative measures fail. Am J Sports Med 2000 May-Jun; 28 (3): 350-5 65. McCarthy A, Vicenzino B. Treatment of osteitis pubis via the pelvic muscles. Man Ther 2003 Nov; 8 (4): 257-60 66. Wollin M, Lovell G. Osteitis pubis in four young football players: a case series demonstrating successful rehabilitation. Phys Ther Sport 2006; 7: 153-60 67. Topol GA, Reeves KD. Regenerative injection of elite athletes with career-altering chronic groin pain who fail conservative treatment: a consecutive case series. Am J Phys Med Rehabil 2008 Nov; 87 (11): 890-902 68. Rabago D, Best TM, Beamsley M, et al. A systematic review of prolotherapy for chronic musculoskeletal pain. Clin J Sport Med 2005 Sep; 15 (5): 376-80
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69. Paajanen H, Hermunen H, Karonen J. Pubic magnetic resonance imaging findings in surgically and conservatively treated athletes with osteitis pubis compared to asymptomatic athletes during heavy training. Am J Sports Med 2008 Jan; 36 (1): 117-21 70. Meyers WC, Foley DP, Garrett WE, et al. Management of severe lower abdominal or inguinal pain in high-performance athletes: PAIN (Performing Athletes with Abdominal or Inguinal Neuromuscular Pain Study Group). Am J Sports Med 2000 Jan-Feb; 28 (1): 2-8 71. Biedert RM, Warnke K, Meyer S. Symphysis syndrome in athletes: surgical treatment for chronic lower abdominal, groin, and adductor pain in athletes. Clin J Sport Med 2003 Sep; 13 (5): 278-84
Correspondence: Dr Gordon Matheson, MD, PhD, Sports Medicine Center, 341 Galvez Street, Stanford, CA 94305-6175, USA. E-mail:
[email protected]
Sports Med 2011; 41 (5)
Sports Med 2011; 41 (5): 377-400 0112-1642/11/0005-0377/$49.95/0
REVIEW ARTICLE
ª 2011 Adis Data Information BV. All rights reserved.
Comparison of Traditional and Recent Approaches in the Promotion of Balance and Strength in Older Adults Urs Granacher,1 Thomas Muehlbauer,1 Lukas Zahner,2 Albert Gollhofer3 and Reto W. Kressig4 1 2 3 4
Institute of Sport Science, Friedrich-Schiller University, Jena, Germany Institute of Exercise and Health Science, University of Basel, Basel, Switzerland Institute of Sport and Sport Science, University of Freiburg, Freiburg, Germany Basel University Hospital, Division of Acute Geriatrics, Basel, Switzerland
Contents Abstract. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Literature Search . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1 Search Strategy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2 Selection Criteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3 Quality Assessment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Balance Training in Older Adults . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1 Traditional Balance Training . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2 Perturbation-Based Balance Training . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3 Multitask Balance Training . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. Resistance Training in Older Adults . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1 Traditional Resistance Training . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2 Power or High-Velocity Resistance Training . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Abstract
377 378 379 379 379 379 380 380 387 389 391 392 392 395
Demographic change in industrialized countries produced an increase in the proportion of elderly people in our society, resulting in specific healthcare challenges. One such challenge is how to effectively deal with the increased risk of sustaining a fall and fall-related injuries in old age. Deficits in postural control and muscle strength represent important intrinsic fall risk factors. Thus, adequate training regimens need to be designed and applied that have the potential to reduce the rate of falling in older adults by countering these factors. Therefore, the purpose of this review is to compare traditional and recent approaches in the promotion of balance and strength in older adults. Traditionally, balance and resistance training programmes proved to be effective in improving balance and strength, and in reducing the number of falls. Yet, it was argued that these training protocols are not specific enough to induce adaptations in neuromuscular capacities that are specifically needed in actual balance-threatening situations (e.g. abilities to recover balance and to produce force explosively). Recent studies indicated that
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perturbation-based or multitask balance training and power/high-velocity resistance training have the potential to improve these specific capacities because they comply with the principle of training specificity. In fact, there is evidence that these specifically tailored training programmes are more effective in improving balance recovery mechanisms and muscle power than traditional training protocols. A few pilot studies have even shown that these recently designed training protocols have an impact on the reduction of fall incidence rate in older adults. Further research is needed to confirm these results and to elucidate the underlying mechanisms responsible for the adaptive processes.
1. Introduction The world population is increasingly becoming ‘old’. According to the United Nations, the proportion of older people aged ‡60 years in the world has grown from 8% to 10% between 1950 and 2000, and by 2050 the proportion of this population worldwide is expected to be as high as 22%.[1] A serious concern, particularly of developed countries, is that an older age structure would undermine the sustainability of the public healthcare system, since per capita health expenditures are five times higher for people older than 75 years of age than for those aged 25–34 years.[2] One reason for high medical treatment costs in the elderly seems to be an increased prevalence of sustaining falls and fall-related injuries:[3,4] 28–35% of individuals over the age of 65 years suffer at least one fall over a 1-year period,[5,6] and the occurrence increases to 32–42% in adults over the age of 75 years and to 56% of adults between the ages of 90 and 99 years.[7,8] About 20% of falls need medical attention; 15% of those result in severe injuries like joint dislocations, soft tissue bruises and contusions. The remaining 5% cause fractures, with femoral neck fractures occurring at a rate of 1–2% in community-dwelling older adults.[9] The aetiology of falls is generally considered to be multifactorial, involving extrinsic (environmental) and intrinsic (patient-related) circumstances.[10] Numerous epidemiological studies have identified a multitude of extrinsic and intrinsic risk factors for falling in older adults.[11-15] Extrinsic factors include loose rugs, obstructed walkways, inadequate handrails, etc.[16] In terms ª 2011 Adis Data Information BV. All rights reserved.
of intrinsic fall risk factors, impaired postural control under single (e.g. walking/standing) and particularly multitask conditions (e.g. walking/ standing while talking), and deficits in maximal and particularly explosive force production of lower extremity muscles, have most frequently been reported to increase the risk of falling in the elderly population.[17,18] Age-related changes in postural control can be attributed mainly to cognitive impairment,[19] visual, vestibular and proprioceptive dysfunctions[20] and muscle weakness.[21] The decline in maximal and explosive force production is primarily caused by a reduced excitability of efferent corticospinal pathways[22] resulting in lower levels of central muscle activation,[23] a gradual loss of spinal motoneurons due to apoptosis,[24] a subsequent decline in muscle fibre number and size (sarcopenia),[25] changes in muscle architecture[26] and decreases in tendon stiffness.[27] Given these detrimental effects of ageing, it is important to design and apply adequate intervention programmes that are able, for example, to delay or even reverse age-related constraints within the neuromuscular system. Recently, it was reported that postural control and strength are two independent neuromuscular capacities.[28] Thus, the authors suggested that the abilities to control posture and to produce force should be trained complementarily. This finding is reinforced by a recent meta-analysis, which provides evidence that, in particular, the combination of balance- and strength-promoting exercises has an impact on both intrinsic fall risk factors, such as deficits in postural control and muscle weakness, and on fall rate (up to 50% reduction).[29] In recent years, a trend towards more specifically Sports Med 2011; 41 (5)
Neuromuscular Performance in Seniors
designed balance and resistance training programmes has been noted in the literature. It is argued that perturbation-based or multitask balance training programmes as well as power or high-velocity strength training programmes are more effective than traditional balance or resistance training programmes in attenuating or even reversing intrinsic fall risk factors in old age.[30-38] Thus, the objective of this review is to describe and discuss traditional and particularly recent approaches in balance and resistance training regarding the effects of these training regimens on intrinsic fall risk factors, i.e. postural control and strength in older adults. 2. Literature Search 2.1 Search Strategy
Two reviewers performed systematic electronic searches on MEDLINE, PubMed, SportDiscus and Web of Science. The last search was performed on 25 June 2010. A search filter containing medical subject headings (MeSH) terms was applied. The primary search included permutations of keyword combinations for the following PICO (Patient/population and/or problem, Intervention, Comparison/control intervention and Outcome or effects)[39] categories: 1. Patient/population and/or problem: ‘aged’, ‘ageing’, ‘aging’, ‘elderly’, ‘geriatric’, ‘older adults’, ‘senior’. 2. Intervention: ‘balance training’, ‘sensorimotor training’, ‘perturbation exercise’, ‘step training’, ‘dual-task training’, ‘resistance training’, ‘strength training’, ‘high-velocity strength training’, ‘power training’, ‘weight training’. 3. Comparison/control intervention: ‘intervention versus no treatment’, ‘intervention versus usual care programme’, ‘traditional intervention versus recent intervention’. 4. Outcome: ‘balance’, ‘gait’, ‘walking’, ‘stance’, ‘standing’, ‘postural stability’, ‘postural control’, ‘body sway’, ‘strength’, ‘power’, ‘physical function’. The MeSH terms for each PICO category were connected using the ‘AND’ operator. Furthermore, we set limits on the types of article (i.e. ª 2011 Adis Data Information BV. All rights reserved.
379
randomized or clinical controlled trial, peerreviewed journal article), ages (i.e. ‡60 years), species (i.e. humans), text options (i.e. full text) and languages (i.e. English). Results of the initial search are summarized in figure 1. In a secondary search, articles from the reference list of included articles were screened using the same criteria as applied to the initial citation search. 2.2 Selection Criteria
Studies were included in the review if they (i) were randomized or clinical controlled trials published in peer-reviewed journals; (ii) had study participants who were aged ‡60 years (except otherwise stated due to a limited amount of studies available); and (iii) had incorporated at least one balance or strength outcome measure. Studies were excluded if they (i) did not meet the minimum requirements of an experimental study design (e.g. case reports); (ii) did not meet the minimum requirements regarding training design (e.g. volume, frequency or intensity statements); and (iii) were not written in English. Based on the inclusion and exclusion criteria, two independent reviewers screened citations of potentially relevant publications. If the citation showed any potential relevance, it was screened at the abstract level. When abstracts indicated potential inclusion, full text articles were reviewed for inclusion. A third-party consensus meeting was held if two reviewers were not able to reach agreement on inclusion of an article. 2.3 Quality Assessment
Two reviewers independently performed quality assessments of included studies, and disagreements were resolved during a consensus meeting or rating by a third assessor. Initially, methodological quality was assessed using the Physiotherapy Evidence Database (PEDro) scale[40] because it had previously shown good reliability.[41,42] This scale rates randomized controlled trials from 0 to 10. The PEDro scores are presented in tables I and II for the respective studies. Given that only a few but highly relevant perturbation-based and dual-task balance training studies are available, we decided to include articles in this review that Sports Med 2011; 41 (5)
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Potentially relevant papers identified and screened for retrieval concerning (...): Balance training (n = 72)
Duplicate papers excluded (n = 4)
Potentially relevant papers remaining (n = 68)
Papers excluded on basis of title or abstract (n = 31)
Papers retrieved for more detailed evaluation (n = 37)
Papers excluded on basis of eligibility criteria (n = 11)
Included papers (n = 26)
Resistance training (n = 109)
Duplicate papers excluded (n = 7)
Potentially relevant papers remaining (n = 102)
Papers excluded on basis of title or abstract (n = 27)
Papers retrieved for more detailed evaluation (n = 75)
Papers excluded on basis of eligibility criteria (n = 43)
Included papers (n = 32)
Fig. 1. Flowchart illustrating the different phases of the search and selection of the balance/resistance training studies.
do not fully meet the high standards of the PEDro scale. 3. Balance Training in Older Adults 3.1 Traditional Balance Training
Traditionally, balance training has been used to rehabilitate ankle and knee joint injuries. More recently, the application area of balance training was expanded to the geriatric population with the purpose of fall prevention. However, in contrast to resistance training, there are hardly any scientific guidelines concerning contents, optimal duration and intensity in balance training. Thus, there is a large variation in these parameters. With regard to content, even Tai Chi can be classified as balance training in the broadest sense. Yet, primarily static and dynamic exercises on stable and unstable surfaces during bipedal or monopedal stance with eyes open or closed represent the core of traditional balance training. ª 2011 Adis Data Information BV. All rights reserved.
Regarding optimal duration of balance training, reported training periods range from 2 days,[34] over 4 and 13 weeks[36,74] to 1 year.[75] A recent systematic review on balance training in healthy individuals clarifies this issue by indicating that balance training programmes performed at least 10 minutes per day, 3 days per week for 4 weeks have the potential to improve balance ability.[76] Training intensity often varies in balance training in terms of diverse conditions regarding the base of support (e.g. bipedal vs monopedal stance), the sensory input (e.g. eyes open vs eyes closed) and task complexity (e.g. single task balance training vs multitask balance training). In a recent position stand on exercise and physical activity for older adults, the American College of Sports Medicine[77] provided preliminary exercise prescription guidelines that included the following: 1. Progressively difficult postures that gradually reduce the base of support (e.g. two-legged stand, semi-tandem stand, tandem stand, one-legged stand). Sports Med 2011; 41 (5)
No. of subjects; sex; exercise group; age (y)
Training regimen; volume
Frequency
Intensity
Balance gain
PEDro score
Mynark and Koceja[34] (2002)
10; F (5), M (5); EG; ‡65
PBBT; 2 d
1 ·/d
NA
Improvements in regulation of the Hoffman reflex ( › 19–21%; p < 0.05) and in static sway area ( › 10%; p < 0.05)
3
Rogers et al.[43] (2003)
8; F (4), M (4); EG; ‡63
PBBT; 3 wk
2 ·/wk
53 trials each session
Improvements in step initiation time ( › 7–19%; p < 0.01), and in step completion time ( › 17–28%; p £ 0.05). No significant improvements in step length
2
Jo¨bges et al.[44] (2004)
14; F (8), M (6); EG; ‡41a
PBBT; 2 wk
2 ·/d
20 min each session
Improvements in length of compensatory steps ( › 88%; p < 0.001), step initiation time ( › 30%; p < 0.001), step length ( › 11%; p = 0.026), cadence ( › 9%; p = 0.03), gait velocity ( › 20%; p = 0.007) and in double support time ( › 48%; p = 0.046). No significant improvements in measures of static postural control
0
Shimadaet al.[45] (2004)
32; F (11), M (3); EG; F (14), M (4); TEG; ‡66
PBBT; 6 mo
1–3 ·/wk
600 min total sessions
Improvements in reaction time during unperturbed ( › 32%; p = 0.015) and perturbed walking ( › 34%; p = 0.007), in oneleg standing time ( › 60%; p = 0.017) and in FRT ( › 42%; p < 0.001)
3
Marigold et al.[46] (2005)
30; F (7), M (23); AG; 31; F (10), M (21); SWG; ‡50b
PBBT; 10 wk
3 ·/wk
60 min each session
Improvements in postural reflex onset latency ( › 4–17%; p £ 0.05), step reaction time ( › 16%; p = 0.005), BBS ( › 10%; p < 0.001) and in TUG ( › 17%; p < 0.001)
8
Silsupadol et al.[47] (2006)
3; F (2), M (1); EG; ‡82
MTBT; 4 wk
3 ·/wk
45 min each session
Improvements in BBS ( › 6–45%) in DGI ( › 10–17%) and in TUG ( › 8–25%)
1
Yang et al.[48] (2007)
25; F (5), M (7); CG; F (6), M (7); EG; range 45–80b
DTWT; 4 wk
3 ·/wk
30 min each session
Improvements in gait speed ( › 30%; p < 0.001), cadence ( › 15%; p < 0.001), stride time ( › 0.2%; p = 0.007) and stride length ( › 18%; p = 0.003)
6
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Study (y)
Neuromuscular Performance in Seniors
ª 2011 Adis Data Information BV. All rights reserved.
Table I. Studies examining the impact of perturbation-based and multitask balance training on balance performance in older adults
382
ª 2011 Adis Data Information BV. All rights reserved.
Table I. Contd Study (y)
No. of subjects; sex; exercise group; age (y)
Training regimen; volume
Frequency
Intensity
Balance gain
PEDro score
Sakai et al.[32] (2008)
43; F (26), M (19); EG; ‡68
PBBT; 1 d
1 ·/d
5 min
1
Silsupadol et al.[49] (2009)
21; F (7); ST; F (10), M (4); DT; ‡65
MTBT; 4 wk
3 ·/wk
45 min each session
Silsupadol et al.[36] (2009)
21; F (7); ST; F (10), M (4); DT; ‡65
MTBT; 4 wk
3 ·/wk
45 min each session
Improvements in the degree of body sway ( › 7%; p < 0.01), stride time ( › 3%; p < 0.01) and integral EMG ( › 5–13%; p < 0.01) of muscles compensating for the perturbation impulse. No significant improvements in the latency EMG of muscles compensating for the perturbation impulse No significant improvements in gait speed and stride length. Improvements in ankle joint inclination angle ( › 30–56%; p = 0.04) Improvements in single-task gait speed ( › 3–14%; p = 0.02) for ST and DT, in dualtask gait speed ( › 17–18%; p < 0.001) for DT, and in BBS ( › 10–15%; p < 0.001) for ST and DT
Brauer and Morris[50] (2010)
20; F (8), M (12); EG; ‡39b
MTBT; 1 d
1 ·/d
20 min
1
Granacher et al.[51] (2010)
11; F (7), M (4); EG; ‡67
MTBT; 6 wk
3 ·/wk
60 min each session
Mansfield et al.[52] (2010)
30; F (7), M (7); CG; 16; F (8), M (8); EG; 64–80
PBBT; 6 wk
3 ·/wk
30 min each session
Schwenk et al.[53] (2010)
49; F (18), M (11); CG; F (13), M (7); EG; ‡67c
DT; 12 wk
2 ·/wk
60 min each session
Improvements in single- ( › 13%; p < 0.001) and dual-task ( › 4–12%; p < 0.05) gait speed and in single- ( › 12%; p < 0.001) and dualtask ( › 5–16%; p < 0.01) step length Improvements in stride time variability during single- ( › 35%; p = 0.02) but not dual- and triple-task walking Improvements in frequency of multi-step reactions ( › 31%; p = 0.034) and foot collisions ( › 67%; p = 0.005) following surface translation and in grasping reactions ( › 19%; p = 0.004) following cable pull Changes in dual-task cost in gait speed ( › 38%; p = 0.086), cadence ( › 27%; p = 0.846), stride length ( › 98%; p = 0.074), stride time ( › 30%; p = 0.750) and single support ( › 32%; p = 0.459)
Patients with PD.
b
Patients with CS.
7
6
7
5
c Patients with dementia. ·/d = times per day; ·/wk = times per week; AG = agility exercise group; BBS = Berg balance scale; CG = control group; CS = chronic stroke; DGI = dynamic gait index; DP = dementia patients; DT = dual-task balance training group; DTWT = dual-task walking training; EG = exercise group containing physical therapy, stretching and gait training; EMG = electromyogram; F = female; FRT = functional reach test; M = males; MTBT = multitask balance training; NA = not available; PBBT = perturbation-based balance training; PD = Parkinson’s disease; PEDro = Physiotherapy Evidence Database; ST = single-task balance training group; SWG = stretching/weight-shifting exercise group; TEG = treadmill exercise group containing perturbed walking on a treadmill; TUG = timed up-and-go test; › indicates an increase in percentage change (e.g. from pre- to post-testing).
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Sports Med 2011; 41 (5)
a
5
Study (y)
No. of subjects; sex; age
Training regimen; volume (wk)
Frequency Intensity Sets; reps (·/wk) (%)a
Ha¨kkinen et al.[54] (1998)
21; F (10), M (11); ‡64
PT; 24
2
50–80
Ha¨kkinen et al.[55] (2000)
10; F (5), M (5); ‡62 PT; 24
2
Earles et al.[56] (2001)
18; F (11), M (7); ‡70
HVRT; 12
Izquierdo et al.[57] (2001)
11; M; ‡62
Fielding et al.[58] (2002)
Balance gain
PEDro score
3–4; 10–15 ND
Improvements in maximal isometric (M: › 36%; p < 0.001; F: › 57%; p < 0.001) and dynamic (M: › 21%; p < 0.001; F: › 30%; p < 0.001) leg extensor strength
2
50–80
3–4; 10–15 ND
Improvements in maximal isometric leg extension values ( › 23–29%; p < 0.001)
1
3
50–70
3; 10
Improvements in maximal leg press power ( › 22%; p = 0.004) and strength ( › 22%; p < 0.001)
5
PT; 16
2
50–80
3–4; 10–15 ND
Improvements in maximal isometric force ( › 26%; p < 0.001)
2
30; F; ‡72
HVRT; 16
3
70
3; 8–10
ND
Improvements in leg press 4 ( › 35%; p < 0.001) and knee extensor ( › 25%; p < 0.001) strength and leg press ( › 97%; p < 0.002) and knee extensor ( › 33%; p < 0.001) power
Miszko et al.[59] (2003)
39; F (9), M (6); CG; F (7), M (6); PG; F (6), M (5); SG; ‡65
PT; 16
3
50–80
3; 6–8
Improvements on the CS-PFP ( › 15%; p < 0.05)
No significant improvements in strength parameters
Sayers et al.[60] (2003)
15; F; ‡65
HVRT; 16
3
70
3; 8
ND Improvements in tandem walk ( › 8%; p = 0.03) and stair climb time ( › 9%; p < 0.001). No significant improvements in chairrise time and gait velocity
Improvements in gait velocity ( › 5%; p < 0.001). No significant improvements in 6-m walk distance and in singleleg stance time
3
3
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Strength gain
Neuromuscular Performance in Seniors
ª 2011 Adis Data Information BV. All rights reserved.
Table II. Studies examining the impact of power or high-velocity resistance training on balance and strength performance in older adults
384
ª 2011 Adis Data Information BV. All rights reserved.
Table II. Contd No. of subjects; sex; age
Training regimen; volume (wk)
Frequency Intensity Sets; reps (·/wk) (%)a
Balance gain
Strength gain
PEDro score
Bean et al.[61] (2004)
10; F; ‡70
HVRT; 12
3
NA
3; 10
Improvements chair rise time ( › 8%; p < 0.05). No significant improvements in gait speed and single-leg stance time
Improvements in leg press power ( › 12–36%; p < 0.05)
5
Kongsgaard et al.[62] (2004)
6; M; ‡65b
HVRT;12
2
80
4; 8
Improvements in maximal gait time ( › 14%; p < 0.01) and stair climbing time ( › 17%; p < 0.05)
Improvements in lower extremity strength ( › 15–37%; p < 0.01) and peak power ( › 19%; p < 0.01)
3
De Vos et al.[63] (2005)
112; F (68), M (44); PT; 8–12 ‡60
2
20, 50, 80
3; 8
ND
Improvements in muscle strength 6 ( › 13–20%; p £ 0.001) and muscle power ( › 14–15%; p £ 0.05) performance
Henwood and Taaffe[64] (2005)
25; F (17), M (8); ‡60
HVRT; 8
2
33, 55, 75
3; 6–8
Improvements in 6-m backward walk ( › 7%; p < 0.01), floor rise to standing ( › 10%; p < 0.05) and chair rise ( › 10%; p < 0.05) times
Improvements in upper ( › 29%; p £ 0.01) 4 and lower ( › 43%; p £ 0.01) extremity strength and lower knee extensor power ( › 17%; p £ 0.002)
Henwood and Taaffe[65] (2006)
23; F (14), M (9); ‡65
HVRT; 8
2
45, 60, 75
3; 8
Improvements in 6-m walk ( › 7%; p < 0.01) and chair rise ( › 12%; p < 0.05) times
5 Improvements in upper ( › 10–25%; p £ 0.05) and lower ( › 10–43%; p < 0.01) extremity strength
Holviala et al.[66] (2006)
22; W; ‡60
HVRT; 21
2
40–80
2–5; 8–15
Improvements in 6-m walk ( › 3%; p < 0.05)
Improvements in maximal isometric 3 force ( › 20%; p < 0.001) and rate of force development ( › 18–31%; p < 0.01)
Orr et al.[67] (2006)
12; F (68), M (44); ‡60
PT; 8–12
2
20, 50, 80
3; 8
Improvements in balance performance ( › 1–11%; p = 0.006)
Improvements in muscle strength ( › 13–20%; p < 0.004) and in muscle power ( › 14–15%; p < 0.004) performance
Bottaro et al.[68] (2007)
11; M; ‡60
HVRT; 10
2
60
3; 8–10
Improvements in 8-ft (2.4-m) upand-go test ( › 15%; p < 0.05) and in 30-sec chair stand test ( › 43%; p < 0.05)
Improvements in dynamic upper ( › 28%; 3 p < 0.05) and lower ( › 27%; p < 0.05) body strength and upper ( › 37%; p < 0.05) and lower ( › 31%; p < 0.05) body power
7
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Granacher et al.
Sports Med 2011; 41 (5)
Study (y)
No. of subjects; sex; age
Training regimen; volume (wk)
Frequency Intensity Sets; reps (·/wk) (%)a
Balance gain
Strength gain
PEDro score
Caserotti et al.[69] (2008)
65; W; 60–65 (old communitydwelling women [n = 40]); 80–89 (very-old communitydwelling women [n = 25])
HVRT; 12
2
75–80
4; 8–10
ND
60–65 y: improvements in peak force ( › 22%; p < 0.001), rate of force development ( › 18%; p = 0.003), and jumping height ( › 10%; p = 0.002); 80–89 y: improvements in peak force ( › 28%; p = 0.005), rate of force development ( › 51%; p = 0.005), and jumping height ( › 18%; p = 0.05)
2
Henwood et al.[70] (2008)
19; F (12), M (7); ‡65
PT; 24
2
40–75
3; ‡8
Improvements in the 6-m backwards walk ( › 16%; p £ 0.001), chair rise time ( › 13%; p = 0.004) and FRT ( › 9%; p < 0.05)
Improvements in upper ( › 19–21%; p £ 0.05) and lower ( › 35–125%; p £ 0.05) maximal strength and upper ( › 70–78%; p £ 0.05) and lower ( › 55–65%; p £ 0.005) peak power
4
Reid et al.[37] (2008)
23; F (12), M (11); ‡65
PT; 12
3
70
3; 8
ND
Improvements in maximal muscle knee extensor strength ( › 49%; p < 0.01) and power ( › 55%; p < 0.01)
5
Marsh et al.[71] (2009)
15; F (9), M (6); ‡65 PT; 12
3
40–70
3; 8–10
ND
Improvements in maximal knee 3 extension ( › 34%; p = 0.003) and leg press ( › 41%; p < 0.001) power, and knee extension ( › 20%; p = 0.02) and leg press ( › 22%; p = 0.03) strength
Nogueira et al.[72] (2009)
20; M; 60–76
PT + TRT; 3 10
40–60
3; 8–10
ND
Improvements in leg extensor strength (PT: › 27%; p < 0.05; TRT: › 27%; p < 0.05) and leg extensor power (PT: › 31%; p < 0.05; TRT: › 8%; p < 0.05)
Webber and Porter[73] (2010)
50; W; 70–88
PT; 12
80
3; 8–10
Changes in reaction time ( › 2%; p < 0.51) and movement time ( › 8%; p < 0.20)
Changes in dorsi flexor peak power 5 ( › 27%; p < 0.89) and plantar flexor peak power ( › 17%; p < 0.84)
a
Intensity is with 1RM unless otherwise stated.
b
Patients with chronic obstructive pulmonary disease.
2
3
·/wk = times per week; 1RM = one-repetition maximum; BW = bodyweight; CG = control group; CS-PFP = Continuous Scale Physical Functional Performance; F = female; FRT = functional reach test; HVRT = high-velocity resistance training; M = males; NA = not available; ND = no data; PEDro = Physiotherapy Evidence Database; PEG = power exercise group; PT = power training; reps = repetitions; SEG = strength exercise group; TRT = traditional resistance training; › indicates an increase in percentage change (e.g. from pre- to post-testing).
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Study (y)
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Table II. Contd
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between the ages of 60 and 80 years. Recently, the effects of a 16-week Tai Chi programme (one training session per week) on measures of postural control and walking ability were investigated in older community-dwelling older adults with a mean age of 69 years.[82] Postural sway under different task conditions (e.g. standing on the floor or on a foam mat) and choice stepping reaction time, i.e. the ability to step as quickly as possible on one of four randomly illuminated rectangular panels, were significantly improved in the Tai Chi group after training but not in the control group. Given the potential of balance training and Tai Chi in old age to counteract a large number of intrinsic fall risk factors, it can be expected that these training regimens have a significant effect on fall incidence rate in older adults. In fact, Madureira et al.[75] investigated the impact of a 1-year balance training programme (static and dynamic exercise) with one session per week on their performance in different functional mobility Change per study Mean change of all studies 18 15 12 Change in gait speed (%)
2. Dynamic movements that perturb the centre of gravity (e.g. tandem walk, circle turns). 3. Stressing postural muscle groups (e.g. heel stands, toe stands). 4. Reducing sensory input (e.g. standing with eyes closed). Despite the wide variety of contents, training duration and intensity in balance training, convincing results were obtained over recent years regarding the effects of balance training on both intrinsic fall risk factors (e.g. deficits in postural control and muscle strength) and the reduction of fall incidence rate.[74,75,78] In this regard, Steadman et al.[79] reported that 6 weeks of balance training with two training sessions per week improved the performance in clinical balance and mobility tests in elderly subjects aged ‡60 years. Granacher et al.[80] examined the effects of a 13-week balance training programme (three training sessions per week) for men between the ages of 60 and 80 years and its effects on performance in clinical balance tests (functional reach test, tandem walk test) and on the ability to compensate for medio-lateral perturbation impulses while standing on a two-dimensional balance platform. After training, performance in the clinical balance tests was significantly improved and summed oscillations of the balance platform were significantly reduced together with an improved activation of muscles compensating for the perturbation impulse. In a more functional approach, Granacher et al.[74] investigated the impact of a 13-week balance training programme (three training sessions per week) in elderly men on the ability to compensate for decelerating gait perturbations while walking on a treadmill. Balance training resulted in a decrease in onset latency and an enhanced reflex activity in the prime mover compensating for the decelerating perturbation impulse. Furthermore, Rochat et al.[81] reported that 10 weeks of low-intensity balance training (one training session per week) produced significant improvements in gait speed, stride length and falls efficacy in older adults who were fearful of falling (figure 2). In another study, Granacher et al.[78] were able to show that 13 weeks of balance training (three training sessions per week) improved maximal and explosive force production capacity of the leg extensors in a cohort of healthy elderly men
9 6 3 0 −3 −6 −9 Traditional BT
Recent BT
Training mode Fig. 2. Percentage of change in gait speed following traditional or recent approaches in balance training (BT). For clarity, more circles and triangles are plotted than there are studies in which gait speed was measured because a number of studies involved the assessment of more than one intervention (see table I).
Sports Med 2011; 41 (5)
Neuromuscular Performance in Seniors
tests (e.g. Berg balance scale [BBS], timed upand-go test [TUG]) as well as on the rate of falling in women aged ‡65 years. After training, the intervention group showed improvements in functional mobility in terms of a significantly higher BBS score and a reduced time to complete the TUG. Notably, this enhancement was paralleled by a significant reduction in the number of falls in the intervention compared with the control group. In terms of Tai Chi, Li et al.[83] reported that a 6-month Tai Chi programme performed three times per week, is effective in decreasing the number of falls, risk for falling and fear of falling in physically inactive persons aged ‡70 years. Only scarce information is available regarding adaptive mechanisms following balance training in old age, which is why results from different age groups have to be consulted. In his 2003 publication, Gollhofer[84] assumed that adaptive processes following balance training take place mainly at a spinal level due to the high intermuscular activation frequencies observed during stabilization tasks on unstable platforms. Recently, Taube et al.[85] investigated cortical and spinal adaptations in young adults following 4 weeks of balance training (three training sessions per week) by means of Hoffmann reflex stimulation, transcranial magnetic stimulation, and conditioning of the Hoffmann reflex by transcranial magnetic stimulation. After training, the authors observed an improved postural stability accompanied by a decrease in motorevoked potentials during stance perturbation on a treadmill. At the same time, Hoffmann reflexes were decreased despite an unchanged background EMG during the performance of a balance task. This could imply that balance training induced changes in the regulation of human erect posture in terms of a shift from cortical to subcortical areas. Thus, supraspinal rather than spinal mechanisms seem to be responsible for the training-induced postural improvement.[85] In other words, after balance training, less neural effort might be required for the regulation of posture due to increased task automatization. However, further research is necessary to clarify whether the training-induced adaptive processes responsible for improvements in postural control ª 2011 Adis Data Information BV. All rights reserved.
387
observed in young adults can be transferred to elderly adults. 3.2 Perturbation-Based Balance Training
Recently, more specifically designed balance training programmes – so-called ‘perturbationbased training regimens’ – have begun to receive attention.[33] This approach is based on the fact that slips and trips account for 30–50% of falls in community-dwelling older adults.[86,87] Thus, compensatory strategies for recovery of equilibrium play a vital functional role in preventing falls. The successful recovery of balance demands the centre of mass to remain within the boundaries of the base of support. This compensatory mechanism can be achieved by different movement strategies (ankle, hip and step strategy).[88] In an actual fall situation, in-place strategies such as the ankle and hip strategy could be insufficient to recover balance, which is why a step is used to bring the support base back into alignment under the centre of mass. These change-in-support reactions (step strategy) can provide a much larger degree of stabilization, compared with in-place reactions where the base of support does not change.[89] It has been reported that neural control of change-in-support reactions evoked by postural perturbation differ in some fundamental way from volitional limb movements.[89] Given that recovery strategies are not under direct volitional control, it is not possible to train this specific capacity through voluntary exercises alone. However, since most balance training programmes include voluntarily controlled exercises only, it was suggested that adequate training regimens should comply with the principle of training specificity and involve the use of perturbation-based exercises.[31] The principle of training specificity requires that a person should experience training conditions (e.g. perturbation exercises) that match real-life conditions (e.g. balance recovery situations) as closely as possible. This fundamental principle of successful exercise prescription applies to anyone regardless of sex, level of physical activity or health status.[90] Recently, Sakai et al.[32] were able to show that a short-term perturbation-based training Sports Med 2011; 41 (5)
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programme (one session with 20 perturbation impulses) on a treadmill produced acute adaptations in terms of significant decreases in postural sway during slip-perturbed gait in a cohort of community-dwelling elderly subjects with a mean age of 71 years. This finding was paralleled by an improved activation of muscles compensating for the perturbation impulse. In an earlier study, Mynark and Koceja[34] investigated whether subjects older than 65 years of age show acute adaptations in the soleus muscle Hoffman reflex following short-term (2 days) perturbation-based balance training. After the first day of training, a significant down-regulation of the Hoffman reflex was observed (19%). On day 2, the Hoffman reflex was decreased by 21% in elderly subjects, indicating that the potential to functionally modulate reflex output persists despite the effects of ageing. In addition to the changes observed in Hoffman-reflex amplitude, the down-training of the Hoffman reflex also seemed to have a functional impact on the static balance of elderly subjects resulting in a significant 10% decrease in the area of static sway from pre- to post-test. Perturbation-based balance training programmes were not only applied in short-term exercise regimens but also in long-term training programmes. Marigold et al.[46] determined the effect of two different community-based group exercise programmes on functional balance (e.g. BBS), mobility (e.g. TUG), postural reflexes (e.g. step reaction time, onset latency following platform translations), and falls in older adults (mean age 68 years) with chronic stroke. Participants were randomly assigned to an agility exercise group (e.g. standing in various postures, walking with various challenges, standing perturbations, etc.) or a stretching/weight-shifting exercise group (e.g. low-impact stretching, Tai Chi-like movements). Both groups exercised three times a week for 10 weeks. For both types of exercise programmes, training improved functional balance and mobility, and led to shorter latencies in postural reflexes and to faster step reaction time. Notably, the agility group demonstrated greater improvement in step reaction time and postural reflex onset latency, as well as a trend toward greater improvement in the TUG. In addition, the total ª 2011 Adis Data Information BV. All rights reserved.
Granacher et al.
number of falls experienced during platform translations was reduced to a larger extent in the agility than the stretching/weight-shifting group after the interventions. Jo¨bges et al.[44] scrutinized the impact of compensatory step training in outpatients with Parkinson’s disease (mean age 61 years) on the ability to compensate for unexpected perturbation impulses while standing, as well as on various gait parameters. Training was conducted for 2 weeks with two training sessions per day (weekends were excluded), and consisted of repetitive pulls to the patient’s back and pushes to the person’s right and left side applied by a physiotherapist. The strength of the pulls and pushes was adapted to the degree of the patient’s individual postural instability. After training, a significant increase in length of compensatory steps was observed, which was accompanied by a significantly shorter step initiation time. In addition, significant training-induced increases in gait velocity and step length, as well as decreases in double support time, i.e. time in which both feet contact the floor during walking, were found during normal walking. In another study with healthy older adults (mean age 70 years), Rogers et al.[43] showed that a 3-week period (two training session per week) of either voluntary or waist-pull-induced step training significantly reduced step initiation time, i.e. the time interval from the onset of a reaction stimulus cue until the vertical ground reaction force under the stepping limb equals zero at foot lift-off. Moreover, compared with voluntary step practice, the waist-pull-induced step training resulted in a significantly greater improvement in reaction time stepping. In a comparative approach, Shimada et al.[45] investigated the effects of two types of exercise programmes (perturbed walking on a treadmill and exercise containing physical therapy, stretching and gait training) on the ability to compensate for gait perturbations, on functional reach performance and on fall rate in long-term care facility residents and outpatients aged 66–98 years. After 6 months of training (one to three training sessions per week), significant improvements in reaction time during perturbed walking and in Sports Med 2011; 41 (5)
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389
functional reach performance were seen in the perturbed walking group but not in the exercise group with physical therapy, stretching and gait training. The number of falls occurring in the treadmill exercise group was 21% lower than that in the multi-component exercise group (odds ratio for falls 0.4). However, this difference was not significant, possibly due to the small sample size utilized in this study (n = 18 treadmill group vs 14 multi-component group). Recently, it was suggested to conduct a water-based balance training programme that includes perturbation exercises to improve stepping responses.[91] Water seems to provide a safe environment for perturbation exercises and may thus reduce the occurrence of exercise-induced fear of falling, which could be present during exercising on land. For therapists and practitioners, a schematic illustration of progression in perturbation-based balance training is presented in figure 3. 3.3 Multitask Balance Training
In accordance with the principle of training specificity, effective fall-prevention programmes should not only include balance-recovery reactions but also multitask balance exercises, because gait instability, and thus risk of falling, increases even when shared attention or dual-tasks
(e.g. walking while talking) are performed.[18] In this regard, Brauer and Morris[50] investigated the impact of a 20-minute dual-task walking training session on acute adaptations in gait characteristics of people with Parkinson’s disease. Participants performed a series of 10-m walking trials under seven conditions: gait only, and with six different added tasks varying by task type (e.g. motor, cognitive), domain (e.g. postural, manual manipulation, language, calculation, auditory, visuospatial) and difficulty level. Following training, step length increased when performing five of the six added tasks, indicating that transfer of dual-task training when walking occurred across task types and domains. Improvements in gait speed were present in three of the six added tasks (figure 2). When other gait variables were examined, such as step length variability, few improvements with training were found. Thus, dual-task training has the potential to induce acute improvements in specific gait characteristics of people with Parkinson’s disease. Regarding long-term training effects, Granacher et al.[51] investigated the impact of a 6-week balance training programme in healthy older adults with an age range of 65–80 years on the variability of their walking pattern both with and without dual and triple tasking, while concurrently performing a cognitive (backward
Progression 1. Weak perturbation: → ankle strategy
Com
Instructor
ComCom
Patient
2. Medium perturbation: → hip strategy
Com
Com om
Instructor
Patient
3. Large perturbation: → step strategy
Com
Instructor
Com Com
Patient
Fig. 3. Schematic illustration of progression in perturbation-based balance training. Com = centre of mass (the three different arrow thicknesses indicate an increase in the applied severity of the perturbation).
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390
counting) and/or motor interference task (holding two interlocked sticks in front of the body). Balance training was conducted three times a week and training intensity was intensified by including additional motor interference tasks (e.g. catching and throwing a ball while performing a balance exercise) and by increasing the number of sets and/or the duration of single exercise sets. Balance training resulted in statistically significant reductions in stride time variability under single- (only walking) but not dual- (walking + cognitive/motor interference) or triple-task walking (walking + cognitive + motor interference). In addition, significant improvements in the motor interference task, but not in the cognitive interference task, were found while walking. Findings showed that improved performance during single-task walking did not transfer to walking under dual- or triple-task conditions, suggesting multiple-task balance training as an alternative training modality. Improvement of the secondary motor but not cognitive task may indicate the need for the involvement of motor, and particularly cognitive, tasks during balance training. Silsupadol et al.[36] investigated the effects of single-task versus dual-task balance training with fixed-priority instructions and dual-task balance training with variable-priority instructions on gait speed under single- (only walking) and dualtask conditions (walking while concurrently performing an arithmetical task) in elderly adults. Single-task balance training involved the performance of balance exercises only (e.g. standing with eyes closed, tandem standing). The participants receiving dual-task balance training with fixed-priority instructions practiced balance tasks while simultaneously performing cognitive tasks (e.g. naming objects), and were instructed to maintain attention on both postural and cognitive tasks at all times. Participants in the dual-task balance training with variable-priority instructions performed the same exercises as the fixed instruction dual-task balance training group, but spent half the session focused on balance and half focused on cognitive task performance. Training lasted for 4 weeks with three training sessions a week. Gait speed was obtained at baseline, in the ª 2011 Adis Data Information BV. All rights reserved.
Granacher et al.
second week, at the end of training and in the twelfth week after the end of training. Following training, participants in all exercise groups significantly improved performance on single-task gait speed (figure 2). However, dual-task training (fixed and variable-priority instruction) was superior to single-task training in improving walking under dual-task conditions. In fact, only participants who received dual-task training walked significantly faster after the training when simultaneously performing a cognitive task. In addition, only dual-task balance training with variable-priority instructions resulted in a dualtask training effect in the second week and maintained the training effect at the 12-week follow-up. These findings suggest that older adults are able to improve their walking performance under dual-task conditions only when specific types of training, i.e. dual-task training, are performed. Furthermore, it seems that training balance under single-task conditions may not generalize to balance control in dual-task contexts.[36] This finding further strengthens the principle of training specificity when designing fall-preventive interventions. In fact, Oddsson et al.[92] followed this principle when introducing a concept for balance training that incorporates voluntary exercises as well as perturbation and dual-task exercises to improve balance control. The programme is performed on five different levels where levels 1–4 focus on the skill to maintain balance (voluntary control) and level 5 adds perturbation exercises that focus on the skill to recover balance (automatic postural corrections), as well as dual-task exercises providing a cognitive load during the execution of a balance task. The feasibility of the concept has been demonstrated in elderly fallers.[93] For therapists and practitioners, a schematic illustration of progression in multitask balance training is presented in figure 4. A detailed list of studies that conducted perturbation-based or multitask balance training is given in table I. In summary, our outlines indicate that studies following the traditional or recent approach in balance training are heterogeneous in terms of training volume, training frequency and training intensity. Nevertheless, most of these studies were Sports Med 2011; 41 (5)
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Progression 1. Single task
2. Dual task
3. Triple task Blue Yellow Green
635 632 611
Com
Com
Com
Patients Fig. 4. Schematic illustration of progression in multitask balance training. Com = centre of mass (arrows indicate displacements of the Com).
effective in inducing acute or long-term adaptations in the postural control system. However, there is evidence that perturbation-based balance training is even more effective than traditional balance training in improving balance recovery mechanisms following perturbation impulses. Furthermore, it seems plausible to argue that multitask conditions should be applied in balance training because only multitask and not singletask balance training improves performance in multitask walking. Since training volume, frequency and intensity were rather heterogeneous in both traditional and recent approaches in balance training, it appears that training specificity in particular could be the major determinant responsible for the enhanced effectiveness of perturbation-based and multitask balance training over traditional balance training. 4. Resistance Training in Older Adults Currently, resistance training programmes in the geriatric context mainly comprise three major methodological approaches: (i) high-intensity resistance training conducted at moderate movement speed, with loads corresponding to 70–80% of one-repetition maximum (1RM)[94,95] – the 1RM is defined as the load that can be lifted only ª 2011 Adis Data Information BV. All rights reserved.
once; (ii) high-velocity or power training conducted at maximum speed during the concentric phase and released at moderate speed during the eccentric phase of the exercise, with loads of 20–80% of 1RM;[37,58] and (iii) eccentric resistance training (also called negative resistance training) conducted at moderate movement speed with high mechanical loads.[96,97] It has been argued that negative work intervention programmes are particularly suited for elderly people because high mechanical loads can be produced at low energetic costs. In fact, LaStayo et al.[98] reported that the energy cost of eccentric work is approximately four times less than that of concentric work at a comparable external load. For a review on this topic see Roig et al.[99] However, the implementation of eccentric resistance training as an intervention programme for elderly people is hard to realize because the performance of resistance training in isolated eccentric contraction mode requires special training equipment (e.g. an isokinetic device). Further, intense guidance during training is mandatory and demands highly qualified personnel as well as a personnel-intense therapist-to-participant ratio. This is why eccentric resistance training was mainly applied in a scientific context and to a lesser extent in large-scale intervention programmes. Sports Med 2011; 41 (5)
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Due to these exercise-specific limitations of eccentric resistance training, we decided to focus our review on high-intensity resistance training and high-velocity or power training, which can be applied in large-scale intervention programmes and group exercises. 4.1 Traditional Resistance Training
The specific effects of resistance training in the elderly have been explored scientifically for many years. Early research from the 1970s and the 1980s was methodologically limited and quite conservative in terms of the intensity of the exercise prescription. At that time, it was assumed that resistance training for older adults could only induce neural adaptations but not muscle hypertrophy (for a review see Porter and Vandervoort[100]). However, in the late 1980s and early 1990s, new insights were gained regarding the real potential of resistance training for older adults, partly due to improved testing equipment, but also because of a better understanding of dose-response relations. Frontera et al.[101] and Fiatarone et al.[94] were among the first to prove that high-intensity resistance training conducted at 80% of 1RM is a feasible, safe and effective means to induce large increases in muscle strength (up to 227% increase in lower extremity strength)[101] and function (48% higher tandem gait speed).[94] CT scans indicated significant increases in muscle mass of the quadriceps (9.3%) following 12 weeks of training with three training sessions a week.[101] Today, it is well known that resistance training using heavy loads (>70% of 1RM) is more effective than low-intensity training in terms of strength gains and increases in muscle mass.[102] It was reported that heavyresistance strength training leads to gains in muscle cross-sectional area ranging between 5–12% in elderly individuals as evaluated by MRI or CT scanning.[103] In addition, neural factors – such as an increased activation of the prime movers (improved recruitment pattern, discharge rate and synchronization of motor units), an improved coactivation of the synergists and a reduced coactivation of the antagonist muscles – have been discussed as potential adaptive mechanisms ª 2011 Adis Data Information BV. All rights reserved.
following resistance training in older adults.[104] Changes in muscle architecture in terms of an increased fascicle length and pennation angle[105] as well as increased tendon stiffness[106] may also account for an enhanced strength performance following resistance training in older adults. Yet, it seems that resistance training increases strength but has less-clear effects on balance abilities. Recently, it was shown that 13 weeks of heavyresistance strength training with three training sessions per week had an impact on maximal and explosive force production[95] in elderly men but not on the ability to compensate for platform[95] or gait perturbation impulses.[74] A recent systematic review of randomized controlled trials on the efficacy of resistance training on balance performance in older adults found similar results.[107] In addition, Latham et al.[102] could not find a clear effect of resistance training on various measures of standing balance among 789 participants (effect size = 0.11). This rather limited adaptive potential of traditional resistance training restricted to variables of strength could be the reason why, to the authors’ knowledge, no clear fall-preventive effect could be shown for resistance training alone.[108] Due to the well documented impact of resistance training on bone mineral content in the elderly,[109-112] it could be speculated that resistance training does not influence the risk of sustaining a fall in old age but does influence the risk of sustaining a fallrelated fracture. Further research is necessary to prove this hypothesis. 4.2 Power or High-Velocity Resistance Training
The ability to generate force rapidly in advancing age declines more precipitously than maximal strength[113] and is, in a fall-threatening situation, more relevant for preventing a fall than the capacity to produce maximal strength.[114] In an actual fall risk situation (e.g. unexpected stop during standing in a driving bus/train), the time taken to produce maximal strength is too long to recover successfully from the balance threat. In fact, there is evidence that lower extremity muscle strength and power are predictors of the risk of falling.[115,116] Therefore, it is of paramount Sports Med 2011; 41 (5)
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importance to apply resistance training programmes that have the potential to specifically enhance explosive force production capacity. It has been suggested that high-velocity and power training have a greater impact on explosive force production in the elderly than heavy-resistance strength training.[38] Fielding et al.[58] were among the first to investigate the impact of a 16-week high- versus low-velocity resistance training regimen on variables of muscle strength (1RM) and power (force · velocity) of the knee and leg extensors in elderly women with self-reported disability. Both training groups exercised three times per week at an intensity of 70% of 1RM. After training, both groups improved their leg extensor 1RM strength (high velocity 35%; low velocity 33%) and knee extensor 1RM strength (high velocity 45%; low velocity 41%) to a similar extent. However, those in the high-velocity strength training group experienced significantly greater improvements in leg press peak muscle power than those participants in the low-velocity training group (high velocity 97%; low velocity 45%). Improvements in knee extensor peak power were not significantly different between the high- (33%) and low-intensity (25%) groups. In a similar study design, Henwood et al.[70] investigated the impact of a 24-week high-velocity or constant-velocity resistance training regimen conducted twice a week on measures of dynamic and isometric muscle strength and peak muscle power. Participants in the high-velocity strength training group performed three sets with eight repetitions using maximal movement velocity. The first set was conducted at 45% of 1RM, the second set at 60% of 1RM, and the third set at 75% of 1RM. The constant-velocity resistance training group performed three sets with eight repetitions at 75% of 1RM using moderate movement velocity. Following training, the average change in dynamic muscle strength (across six exercises) amounted to 51% for the high-velocity, and 48% for the constant-velocity resistance training group. Maximal isometric strength significantly increased in the high-velocity group (30%) and in the constant-velocity group (24%). Significant training-induced increases in peak ª 2011 Adis Data Information BV. All rights reserved.
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muscle power were observed for both exercise groups (high velocity 51%; constant velocity 34%). Overall, no significant differences between exercise groups emerged following training. Yet, it is important to note that these gains in muscle strength and power occurred for the high-velocity group using a reduced total workload per exercise session compared with the constant-velocity group. Thus, these findings support the efficiency of using high-velocity varied resistance training protocols in older adults as a means to enhance muscle strength and power. Recently, it was shown that older adults aged 60–65 years, and particularly those aged 80–89 years, benefit from 12 weeks of power training (two training sessions per week) in terms of large increases in the rate of force development (21% and 51%, respectively) and muscle power of the leg extensors (12% and 28%, respectively).[69] Miszko et al.[59] scrutinized the effects of a 16-week power or strength training programme with three training sessions a week on maximal strength and peak anaerobic power of the leg extensors as well as physical function in communitydwelling older adults (mean age 73 years). Intensity in strength training progressed from 50% to 70% of 1RM by week 8, and then remained at 80% of 1RM for weeks 9–16. Intensity in power training was the same as in strength training for the first 8 weeks. After 8 weeks, the programme was altered to increase muscle power. Each subject performed three sets of 6–8 repetitions at 40% of 1RM value as fast as possible. Miszko et al.[59] found that power training was more effective than strength training for improving whole-body physical function on the continuous scale physical functional performance test, which assesses 16 everyday tasks with components for the lower body, the upper body, balance, coordination and endurance. In addition, results indicated that both programmes were equally effective for improving maximal strength. The strength training group were significantly stronger than the control group following training; however, there were no significant differences between the exercise groups. In a recently conducted study,[37] high-velocity power training and traditional slow-velocity progressive resistance training yielded similar increases Sports Med 2011; 41 (5)
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ª 2011 Adis Data Information BV. All rights reserved.
velocity regimen might be particularly well suited for the promotion of balance in older adults. However, the question regarding the most effective training intensity in power training with older adults is still under debate. The American College of Sports Medicine, for instance, recommended that healthy older adults should perform one to three sets using light to moderate resistance (40–60% of 1RM) for six to ten repetitions with high-movement velocity. In contrast to these recommendations, it was reported that 8–12 weeks of power training with high loads (80% of 1RM) induced larger gains in muscle power, strength and endurance than power training with medium (50% of 1RM) and low loads (20% of 1RM).[63] It has to be mentioned that the risk of sustaining an injury during training was greater in the highintensity group than that of the medium- and low-intensity groups. This has to be put into perspective though, since the rate of adverse Change per study Mean change of all studies 18 15 12 Change in gait speed (%)
of lower extremity power in older adults with mobility limitations. It is of interest to note that after 12 weeks of training (three training sessions a week), no significant changes in total leg lean mass assessed by dual-energy x-ray absorptiometry occurred over the course of the intervention in any group. Thus, the authors hypothesized that neuromuscular adaptations rather than muscle hypertrophy may account for the investigated gains in muscle strength and power.[37] Similarly, Fielding et al.[58] suggested that changes in motor unit recruitment and activation seem to be primarily responsible for increased peak power following 16 weeks of high-velocity resistance training (three training sessions per week). Returning to the results of Miszko et al.[59] regarding the impact of power or resistance training on measures of physical function, Henwood and Taafe[64] confirmed these results by demonstrating that 8 weeks of high-velocity resistance training (two training sessions per week) produced larger improvements in tests of physical performance, i.e. the floor rise to standing test, the 6-m walk test, the repeated chair rise test, and the lift and reach test than traditional strength training. In a later study, however, Henwood et al.[70] reported that 24 weeks of high-velocity or constant resistance training (two training sessions per week) resulted in similar improvements in the 6-m fast walk, chair rise, stair climbing and functional reach task. From a functional point of view, it is of interest to know whether power training has an impact on balance in older adults, since balance control is an important component of physical performance. In this regard, Orr et al.[67] investigated the effects of a 10-week power training (two sessions per week) programme at one of three intensities (20%, 50% and 80% of 1RM) on balance performance in sedentary healthy older adults. Irrespective of training intensity, significant improvements were observed in peak power, strength and endurance of lower extremity muscles. Notably, in the low-intensity group (20% of 1RM) training-induced improvements in balance were significantly higher than in the high (80% of 1RM) and medium (50% of 1RM) exercise groups, indicating that a low-load high-
9 6 3 0 −3 −6 −9 Traditional RT
Recent RT
Training mode Fig. 5. Percentage of change in gait speed following traditional or recent approaches in resistance training (RT). For clarity, more circles and triangles are plotted than there are studies in which gait speed was measured because a number of studies involved the assessment of more than one intervention (see table II).[117-127]
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395
One repetition 1. Starting position
2. Concentric action
Load
3. Eccentric action
Load
Load
A
80% 1RM
A
80% 1RM
A
80% 1RM
B
20% 1RM
B
20% 1RM
B
20% 1RM
High-velocity movement speed
Moderatevelocity movement speed
Fig. 6. Schematic description of power or high-velocity resistance training. 1RM = one-repetition maximum.
events for strength testing (16 events, 4711 strength tests [0.34%]) and power training (four events, 1633 training sessions [0.25%]) was rather low.[63] In another study, the effects of a heavyresistance training with explosive concentric contractions in elderly men with chronic obstructive pulmonary disease was investigated on muscle strength, power and physical performance.[62] Following 12 weeks of training (two training sessions per week), significant improvements in isometric (14%) and isokinetic (18%) knee extension strength, leg extension power (19%), quadriceps cross-sectional area (4%), maximal gait speed (14%) and stair climbing time (17%) were observed (figure 5). Notably, no training-related injuries were reported in this cohort of elderly men suffering from chronic disease. For therapists and practitioners, a schematic illustration of training load and contraction mode in power/high-velocity resistance training is presented in figure 6. A detailed list of studies that conducted power/high-velocity resistance training is given in table II. In summary, our review indicates that highintensity resistance training and power or high-velocity resistance training are effective in improving muscle strength/power and functional capacity even though major determinants of the respective study designs (e.g. training volume, frequency, intensity) were rather heterogeneous across the traditional and recent approaches. ª 2011 Adis Data Information BV. All rights reserved.
Yet, there is preliminary evidence that power training with particularly high loads is more effective/efficient in increasing power than traditional resistance training. Further, it seems that power training compared with resistance training is more beneficial in improving measures of physical function. More specifically, there is evidence that especially low-intensity power training is well suited to enhance balance in older adults. Given the heterogeneity in study designs across traditional and recent approaches in resistance training, it appears that the specificity of the contraction mode (moderate vs high velocity) may represent an important determinant for producing substantial gains in muscle power and functional capacity. This result complies with the principle of training specificity and suggests that ballistic contractions should be incorporated in resistance training for older adults. 5. Conclusions During the last 30 years, intense research efforts have been undertaken regarding the effects of balance and resistance training on measures of postural control and strength in older adults. In general, these training regimens appear to be feasible, safe and effective. There is evidence that traditional balance training has an impact on postural control, physical function, and strength and fall rate in older adults. Based on preliminary Sports Med 2011; 41 (5)
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data, it seems plausible to argue that specific types of balance training (perturbation-based and multitask) are particularly effective in promoting balance recovery mechanisms and variables of postural control under single and multitask conditions. This could indirectly imply that these training regimens may have a larger impact on fall rate than traditional balance training programmes. However, this important issue needs to be confirmed in future studies. Traditional approaches have proven that resistance training particularly enhances strength performance but has limited effect on physical function. Thus, recent studies focused on the impact of power or high-velocity strength training and found that this training regimen seems to have larger effects on explosive force production and physical function than traditional resistance training. However, clear dose-response relations need to be established for power training. Additional verification is needed regarding the underlying neuromuscular mechanisms responsible for training-induced adaptive processes following perturbation-based/multitask balance training and power/high-velocity resistance training. 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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89. Maki BE, McIlroy WE. The role of limb movements in maintaining upright stance: the ‘‘change-in-support’’ strategy. Phys Ther 1997; 77 (5): 488-507 90. Reilly T, Morris T, Whyte G. The specificity of training prescription and physiological assessment: a review. J Sports Sci 2009; 27 (6): 575-89 91. Melzer I, Elbar O, Tsedek I, et al. A water-based training program that include perturbation exercises to improve stepping responses in older adults: study protocol for a randomized controlled cross-over trial. BMC Geriatr 2008; 8: 19 92. Oddsson LIE, Boissy P, Melzer I. How to improve gait and balance function in elderly individuals: compliance with principles of training. Eur Rev Aging Phys Act 2007; 4 (1): 15-23 93. Boissy P, Yurkow J, Chopra A, et al. Balance training in the elderly using Swiss ball: a pilot study [abstract]. Arch Phys Med Rehabil 2000; 81 (10): 1463 94. Fiatarone MA, Marks EC, Ryan ND, et al. High-intensity strength training in nonagenarians: effects on skeletal muscle. JAMA 1990; 263 (22): 3029-34 95. Granacher U, Gruber M, Gollhofer A. Resistance training and neuromuscular performance in seniors. Int J Sports Med 2009; 30 (9): 652-7 96. LaStayo PC, Ewy GA, Pierotti DD, et al. The positive effects of negative work: increased muscle strength and decreased fall risk in a frail elderly population. J Gerontol A Biol Sci Med Sci 2003; 58 (5): 419-24 97. Mueller M, Breil FA, Vogt M, et al. Different response to eccentric and concentric training in older men and women. Eur J Appl Physiol 2009; 107 (2): 145-53 98. LaStayo PC, Reich TE, Urquhart M, et al. Chronic eccentric exercise: improvements in muscle strength can occur with little demand for oxygen. Am J Physiol 1999; 276 (2): 611-5 99. Roig M, O’Brien K, Kirk G, et al. The effects of eccentric versus concentric resistance training on muscle strength and mass in healthy adults: a systematic review with metaanalysis. Br J Sports Med 2009; 43 (8): 556-68 100. Porter MM, Vandervoort AA. High-intensity strength training for the older adult: a review. Topics Geriatr Rehabil 1995; 10 (3): 61-74 101. Frontera WR, Meredith CN, O’Reilly KP, et al. Strength conditioning in older men: skeletal muscle hypertrophy and improved function. J Appl Physiol 1988; 64 (3): 1038-44 102. Latham NK, Bennett DA, Stretton CM, et al. Systematic review of progressive resistance strength training in older adults. J Gerontol A Biol Sci Med Sci 2004; 59 (1): 48-61 103. Aagaard P, Suetta C, Caserotti P, et al. Role of the nervous system in sarcopenia and muscle atrophy with aging: strength training as a countermeasure. Scand J Med Sci Sports 2010; 20 (1): 49-64 104. Ha¨kkinen K. Ageing and neuromuscular adaptation to strength training. In: Komi PV, editor. Strength and power in sport. Oxford: Blackwell Publishing, 2003: 409-25 105. Seynnes OR, de Boer M, Narici MV. Early skeletal muscle hypertrophy and architectural changes in response to
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high-intensity resistance training. J Appl Physiol 2007; 102 (1): 368-73 Reeves ND, Narici MV, Maganaris CN. Strength training alters the viscoelastic properties of tendons in elderly humans. Muscle Nerve 2003; 28 (1): 74-81 Orr R, Raymond J, Fiatarone SM. Efficacy of progressive resistance training on balance performance in older adults: a systematic review of randomized controlled trials. Sports Med 2008; 38 (4): 317-43 Latham NK, Anderson CS, Lee A, et al. A randomized, controlled trial of quadriceps resistance exercise and vitamin D in frail older people: the Frailty Interventions Trial in Elderly Subjects (FITNESS). J Am Geriatr Soc 2003; 51 (3): 291-9 McMurdo ME, Mole PA, Paterson CR. Controlled trial of weight bearing exercise in older women in relation to bone density and falls. BMJ 1997; 314 (7080): 569 Wolff I, van Croonenborg JJ, Kemper HC, et al. The effect of exercise training programs on bone mass: a meta-analysis of published controlled trials in pre- and postmenopausal women. Osteoporos Int 1999; 9 (1): 1-12 Liu-Ambrose TY, Khan KM, Eng JJ, et al. Both resistance and agility training increase cortical bone density in 75- to 85-year-old women with low bone mass: a 6-month randomized controlled trial. J Clin Densitom 2004; 7 (4): 390-8 Suominen H. Muscle training for bone strength. Aging Clin Exp Res 2006; 18 (2): 85-93 Skelton DA, Greig CA, Davies JM, et al. Strength, power and related functional ability of healthy people aged 65-89 years. Age Ageing 1994; 23 (5): 371-7 Suetta C, Magnusson SP, Beyer N, et al. Effect of strength training on muscle function in elderly hospitalized patients. Scand J Med Sci Sports 2007; 17 (5): 464-72 Perry MC, Carville SF, Smith IC, et al. Strength, power output and symmetry of leg muscles: effect of age and history of falling. Eur J Appl Physiol 2007; 100 (5): 553-61 Shigematsu R, Rantanen T, Saari P, et al. Motor speed and lower extremity strength as predictors of fall-related bone fractures in elderly individuals. Aging Clin Exp Res 2006; 18 (4): 320-4 Judge JO, Underwood M, Gennosa T. Exercise to improve gait velocity in older persons. Arch Phys Med Rehabil 1993; 74 (4): 400-6 Judge JO, Lindsey C, Underwood M, et al. Balance improvements in older women: effects of exercise training. Phys Ther 1993; 73 (4): 254-62 Sipila S, Multanen J, Kallinen M, et al. Effects of strength and endurance training on isometric muscle strength and walking speed in elderly women. Acta Physiol Scand 1996; 156 (4): 457-64 Buchner DM, Cress ME, de Lateur BJ, et al. The effect of strength and endurance training on gait, balance, fall risk, and health services use in community-living older adults. J Gerontol A Biol Sci Med Sci 1997; 52 (4): 218-24 Singh NA, Clements KM, Fiatarone MA. A randomized controlled trial of progressive resistance training in depressed elders. J Gerontol A Biol Sci Med Sci 1997; 52 (1): 27-35
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122. Schlicht J, Camaione DN, Owen SV. Effect of intense strength training on standing balance, walking speed, and sit-to-stand performance in older adults. J Gerontol A Biol Sci Med Sci 2001; 56 (5): 281-6 123. Tyni-Lenne R, Gordon A, Jensen-Urstad M, et al. Aerobic training involving a minor muscle mass shows greater efficiency than training involving a major muscle mass in chronic heart failure patients. J Card Fail 1999; 5 (4): 300-7 124. Englund U, Littbrand H, Sondell A, et al. A 1-year combined weight-bearing training program is beneficial for bone mineral density and neuromuscular function in older women. Osteoporos Int 2005; 16 (9): 1117-23 125. Judge JO, Whipple RH, Wolfson LI. Effects of resistive and balance exercises on isokinetic strength in older persons. J Am Geriatr Soc 1994; 42 (9): 937-46
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126. Topp R, Mikesky A, Wigglesworth J, et al. The effect of a 12-week dynamic resistance strength training program on gait velocity and balance of older adults. Gerontologist 1993; 33 (4): 501-6 127. Topp R, Mikesky A, Dayhoff NE, et al. Effect of resistance training on strength, postural control, and gait velocity among older adults. Clin Nurs Res 1996; 5 (4): 407-27
Correspondence: Prof. Dr Urs Granacher, Institute of Sport Science, Friedrich-Schiller-University, Seidelstr. 20, 07749 Jena, Germany. E-mail: urs.granacher@uni-jena-de Dr Thomas Muehlbauer, Institute of Sport Science, FriedrichSchiller-University, Seidelstr. 20, 07749 Jena, Germany. E-mail:
[email protected]
Sports Med 2011; 41 (5)
Sports Med 2011; 41 (5): 401-411 0112-1642/11/0005-0401/$49.95/0
REVIEW ARTICLE
ª 2011 Adis Data Information BV. All rights reserved.
Is the ‘Athlete’s Heart’ Arrhythmogenic? Implications for Sudden Cardiac Death Thomas Rowland Baystate Medical Center, Springfield, Massachusetts, USA
Contents Abstract. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. The Pathological Model . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Ventricular Remodelling in Athletes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Electrophysiological Changes with Exercise Training . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. Frequency of Ventricular Dysrhythmias in Athletes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5. Sudden Death and the ‘Athlete’s Heart’ . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6. Hypertrophic Cardiomyopathy – or Not? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7. Right Ventricular Cardiomyopathy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Abstract
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Whether the ventricular hypertrophic response to athletic training can predispose to fatal ventricular dysrhythmias via mechanisms similar to that of pathological hypertrophy is controversial. This review examines current information regarding the metabolic and electrophysiological differences between the myocardial hypertrophy of heart disease and that associated with athletic training. In animal studies, the biochemical and metabolic profile of physiological hypertrophy from exercise training can largely be differentiated from that of pathological hypertrophy, but it is not clear if the former might represent an early stage in the spectrum of the latter. Information as to whether the electrical remodelling of the athlete’s heart mimics that of patients with heart disease, and therefore serves as a substrate for ventricular dysrhythmias, is conflicting. If ventricular remodelling associated with athletic training can trigger fatal dysrhythmias, such cases are extraordinarily rare and thereby impossible to investigate by any standard experimental approach. Greater insight into this issue may come from a better understanding of the electrical responses to both acute bouts of exercise and chronic training in young athletes.
Henschen considered the cardiomegaly he detected in cross-country skiers by chest percussion in 1899 to be an adaptive phenomenon, a feature of the ‘athlete’s heart’ that represented ‘‘a physiologic enlargement of the heart due to the ath-
letic activity.’’ ‘‘The large heart,’’ he concluded presciently, ‘‘will win the race.’’[1] Others were not so convinced. The fact that the ventricular hypertrophy and chamber enlargement of the highly trained endurance athlete, which was later verified
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by radiological and ultrasound studies and mimicked many aspects of heart disease, was not lost on early clinicians. They expressed concern that the ‘athlete’s heart’ might bear pathological significance, both in terms of sudden cardiovascular collapse and chronic functional deterioration, and cautioned against excessive athletic training.[1-3] The recent development of diagnostic tools that have more precisely delineated pathological from physiological cardiac findings in athletes have largely dispelled such concerns.[1] Even more important in supporting the innocent nature of the morphological and electrocardiographical findings of the ‘athlete’s heart’ has been the ‘natural experiment’ in which an apparently benign course has been observed in many thousands of highly trained competitors. This debate has persisted, however, fueled by information suggesting that the myocardial hypertrophy related to both athletic training and pathological conditions may serve as a substrate for ventricular tachyarrhythmias.[4-7] By extension, this evidence implies that ventricular remodelling in response to participation in endurance sports might, in extremely rare individuals, serve as a predisposing factor for sudden death during athletic competition and training.[7-9] If so, such a risk would bear importance in designing strategies targeted at preventing sudden unexpected death during sports play – tragedies that have traditionally been considered manifestations of pre-existing, occult heart disease. This review will address current information examining (i) the similarities and differences between characteristics of the hypertrophy of the athlete’s heart and that of pathological conditions; and, more specifically, (ii) whether the documented predisposition created by pathological hypertrophy for life-threatening ventricular dysrhythmias in patients with heart disease is mimicked by the hypertrophic responses triggered by endurance athletic training. Published articles were obtained through a computer search between the years 1950 and 2010, using the terms ‘athlete’, ‘athletic training’, ‘sudden death’, ‘myocardial hypertrophy’ and ‘arrhythmias’. In addition, articles were accumulated from personal literature files, and reference lists from published reports. It should be ª 2011 Adis Data Information BV. All rights reserved.
recognized that this article does not constitute an exhaustive review of all materials published on these topics. Instead, previous reports were selected by the author that are pertinent to the separate portions of the review and which provide a balanced view of these issues. To any extent that the hypertrophy of the athlete’s heart can be demonstrated to enhance arrhythmogenicity, the corollary that such dysrhythmias can be considered responsible for cases of sudden death in athletes remains problematic. Indeed, such a conclusion is currently surrounded by considerable controversy. For example, citing Hart, ‘‘For most trained athletes the cardiac consequences of their activity would appear to be adaptive, benign and probably reversible. However, intensive athletic training is associated with a small but finite risk of sudden death, which may be a consequence of the cellular electrical changes of mild-to-moderate hypertrophy.’’[8] Other authorities have failed to agree. Maron and Pelliccia concluded, to the contrary, that ‘‘There is no evidence at present showing that athlete’s heart remodeling leads to long-term disease progression, cardiovascular disability, or sudden cardiac death.’’[10] 1. The Pathological Model Myocardial hypertrophy (an increase in ventricular mass by non-mitotic growth of cardiac myocytes) is an adaptive response to the demands of augmented heart work. According to the classic model proposed by Grossman et al.,[11] the pattern of this remodelling in patients with heart disease is dictated by the nature of the haemodynamic load. When the ventricle is required to expel stroke volume at greater levels of pressure (as with aortic valve stenosis or systemic hypertension), the wall thickness increases with a constant or reduced chamber volume. This concentric hypertrophy reflects the addition of sarcomeres in parallel, increasing the myocyte cross-sectional area. On the other hand, in pathological conditions in which a larger volume must be ejected per beat with enlargement of ventricular size, as in patients with aortic or mitral valve insufficiency, the resulting increase in wall stretch triggers sarcomere Sports Med 2011; 41 (5)
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growth in series, resulting in increased myocyte length.[12] The resulting eccentric hypertrophy is more modest in degree and serves to maintain a constant chamber wall thickness : internal volume relationship ratio, thereby stabilizing wall tension according to the law of Laplace.[13] These patterns of concentric and eccentric hypertrophy are initially adaptive and compensatory in the early stages of the natural course of cardiac disease, maintaining stroke volume in the face of increased pressure and volume work, respectively. Given sufficient duration and severity, however, myocardial systolic and diastolic function deteriorates and eventuates in congestive heart failure, characterized histologically by myocyte fibrosis, apoptosis and attenuated vascularization.[14] In recent years, a constellation of genetic transcription processes, biochemical agents and metabolic changes have been described that characterize this hypertrophic adaptive process in response to wall shear stress and/or stretch, and its eventual dysfunctional outcome. In pathological hypertrophy, these neurohormonal signalling pathways involve, principally, angiotensin II, endothelin and catecholamines. As function deteriorates, oxidative metabolism shifts to glycolytic, and a-myosin heavy chain is replaced by the more fetal form b-myosin heavy chain.[15,16] Myocardial hypertrophy in patients with heart disease clearly increases the risk for life-threatening ventricular tachyarrhythmias and sudden death.[17] Ghali et al.[18] described a graded relationship between ventricular rhythm disturbances and ventricular hypertrophy in 49 hypertensive adults without coronary artery disease. For every 1 mm increase in ventricular wall thickness, they found a 2- to 3-fold increase in both the frequency and complexity of ventricular arrhythmias. In addition, pathological hypertrophy typically occurs in the context of cardiovascular disease[18] (such as diminished perfusion from coronary artery disease), which can contribute to an increased arrythmogenic state of the myocardium. The principal expression of pathological ventricular hypertrophy on the electrical properties of the myocardium is an enhanced action potential duration and repolarization time, as indicated ª 2011 Adis Data Information BV. All rights reserved.
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by an increased QT interval.[19,20] These changes reflect alterations in the balance of inward and outward transmembrane ion channels. The genes that control such currents are sensitive to mechanical stress and are activated in direct proportion to the extent of hypertrophy.[21] This electrical remodelling occurs early in the hypertrophic response and appears to be independent of structural remodelling or ventricular function.[22] The electrophysiological alterations occurring with myocardial hypertrophy result in heterogeneity (both spatial and temporal) of ventricular repolarization within the heart. These changes predispose to early after-depolarizations, which increase vulnerability to re-entrant ventricular tachyarrhythmias.[23,24] As an index of this electrical remodelling, the QT-interval duration on the standard body surface ECG has been reported in several studies to be directly related to left ventricular hypertrophy.[25] The beat-to-beat variability of the QT-interval duration increases with electrical remodelling, which predisposes to dysrhythmias. A measure of this variability has been proposed as a possible marker for patients at risk.[26] Analogous to genetic ‘channelopathies’ (e.g. prolonged QT syndrome), these electrophysiological changes explain at least a part of the susceptibility of patients with pathological hypertrophy to fatal ventricular rhythm disturbances. Hypertrophy-related changes in connexin, critical to electrical conduction in the gap junction of cardiac myocytes, might also influence susceptibility to ventricular rhythm disturbances.[27] 2. Ventricular Remodelling in Athletes Myocardial hypertrophy is an essential feature of the cardiac responses to the repetitive heart work of sustained athletic training. Similar to pathological hypertrophy, the pattern of ventricular remodelling in the highly trained athlete depends upon the haemodynamic demands imposed by the particular sport involved. As Morganroth et al.[28] first proposed in 1975, training in endurance sports, such as distance running, triggers an increase in blood volume as a central feature of an expansion of the cardiovascular Sports Med 2011; 41 (5)
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system. The myocardial stretch created by the enlarged left ventricular volume stimulates commensurate myocardial hypertrophy to maintain a constant wall stress according to the law of Laplace (eccentric hypertrophy). On the other hand, power athletes, such as weightlifters, experience repeated bouts of blood pressure elevation in their training. This affects a remodelling response of increased wall thickness without chamber enlargement, or concentric hypertrophy. Sports that involve a combination of strength and endurance, such as cycling and rowing, are expected to demonstrate a combination of these features. The validity of such a model has been questioned (particularly concerning hypertrophy in power athletes[1,29]), but empiric echocardiographical studies of trained athletes have generally supported this construct.[29] However, a sufficient number of exceptions have been observed to suggest that other factors (such as repetitive sympathetic stimulation and genetic predisposition) may be involved in cardiac remodelling in athletes.[30] The parallels of this construct in athletes with the pattern of hypertrophic response in patients with heart disease are obvious. It is not unreasonable to assume, therefore, that the mechanical triggers responsible for increasing myocyte mass, as well as the subsequent forms of ventricular remodelling, are similar in both the physiological and pathological hypertrophy of the athlete. Much attention has focused on the next question of whether the nature of the hypertrophic response to such triggers of chronic myocardial stretch and wall tension differs in the two processes. Many have argued that the metabolic, biochemical and physiological ‘fingerprint’ of the ventricular hypertrophy of the athlete is, in fact, distinct from that of pathological hypertrophy (see references[15,16,31] for reviews and discussions). To begin with, the idea that these represent different physiological processes is suggested by their divergent natural courses. The hypertrophy associated with athletic training is beneficial, permitting an enhanced level of cardiac performance in sports competition. Pathological hypertrophy, on the other hand, although initially adaptive, is characterized by progressive ª 2011 Adis Data Information BV. All rights reserved.
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fibrosis, apotosis, diminished diastolic and systolic function, and ultimate clinical congestive heart failure. The obvious difference between the two situations, however, is that the work stress confronted by the myocardium of the athlete is discontinuous, not more than several hours per day at most, with abundant time for recovery. In contrast, pathological hypertrophy reflects a continuous rate of working without rest, 24 hours a day, for the lifespan of the heart disease. In this regard, extended periods of intense athletic competition, such as participation in ultra marathons, are accompanied by indicators of transient myocardial fatigue.[32] It is intriguing to postulate that if athletic training was conducted continuously for many years (i.e. temporally analogous to pathological hypertrophy), a natural history of declining myocardial function would be observed, which would mimic that of patients with heart disease. Such an idea is not entirely conjectural, as myocardial hypertrophy in conditions of chronic heart overwork not associated with structural heart disease (such as morbid obesity) are, in fact, characterized by progressive systolic and diastolic dysfunction leading to congestive heart failure.[33] Recent studies have identified a number of biochemical and molecular pathways that appear to distinguish the physiological hypertrophy of exercise training from pathological hypertrophy.[15,16,31] For example, in experimental animals, pathological hypertrophy is uniquely characterized by shifts of cardiac gene expression to the fetal state (e.g. transition to b-myosin heavy chain and atrial natriuretic peptide), and activation of signalling pathways for actions of angiotensin II and endothelin 1. Conversely, the insulin growth factor phosphatidylinisitol-3 kinase/protein kinase B pathway is particularly important for adaptations of physiological hypertrophy. Metabolically, a shift from oxidative to glycolytic pathways is observed in pathological hypertrophy, while augmented oxidative capacity with mitochondrial biogenesis is observed in the hypertrophy of exercise training. Such observations have led some to conclude that ‘‘the mechanisms leading to hypertrophy during pathological and physiological states are Sports Med 2011; 41 (5)
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distinct.’’[15] However, because of certain concerns regarding the classic study model, such conclusions would appear to be premature. The comparisons noted in this section have been performed almost uniquely in rodents, with considerable inter-species variability in the findings.[34] Moreover, there is no assurance that findings in small animals can be transferred to humans. The study model of pathological hypertrophy has involved creation of a chronic pressure overload by aortic constriction or induction of hypertension, while ‘physiological hypertrophy’ has been produced by endurance exercise (typically rodents forced to swim or run), which does not mimic the physiological stimulus occurring with voluntary exercise training in humans. It has been assumed, on no clear evidence, that such different models of pressure and volume overload effect identical triggers to hypertrophy, and that the haemodynamic loads of intermittent (exercise training) and chronic work (ventricular hypertension) are qualitatively and quantitatively similar. Such caveats limit confidence in considerations of any possible biochemical and metabolic differentiation between the ventricular hypertrophy of the human athlete and the patient with heart disease. The animal evidence suggests that distinct differences do exist between physiological exercise hypertrophy and longstanding pathological hypertrophy. However, whether physiological hypertrophy represents an early stage in a continuum of a single hypertrophic process, which eventuates in the markers observed in chronic pathological overwork, remains uncertain.
3. Electrophysiological Changes with Exercise Training More central to this discussion, is the following question: does the ventricular hypertrophy of the athlete’s heart share electrical properties that are characteristic of pathological hypertrophy? Insights into electrophysiological features of hypertrophy of the athlete are understandably limited, and the scant information available has been obtained in animals. ª 2011 Adis Data Information BV. All rights reserved.
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Tibbits et al.[35] reported that following 12 weeks of treadmill running training, the ventricular muscle fibres of rats demonstrated a significant prolongation of action potential duration. These authors noted the ‘‘strikingly similar’’ adaptations in their exercise model compared with previous findings described after aortic constriction. Similarly, Gwathmey et al.[36] described a 37% prolongation of action potential duration in nonhypertrophied right ventricular muscle with exercise training in rats. Some have argued, however, that studies in these animal models are not ‘‘electrophysiologically relevant’’ to humans.[9] Lacking an opportunity to directly measure such electrical features in humans, researchers have examined findings on the surface ECG of the athlete. Most of the attention has focused on the QT interval as an indicator of ventricular conduction and repolarization velocity and, therefore, of vulnerability to ventricular tachyarrhythmias. Such studies have produced mixed results. A number have demonstrated a significantly greater QT-interval duration corrected for heart rate (corrected QT [QTc]) in trained versus untrained subjects, despite values remaining within the normal range.[37-41] In one of these reports, Palatini et al.[38] could find no association between frequency of ventricular ectopy and length of the QTc interval. Others have reported similar QTc intervals in athletes and non-athletes.[42-47] Hart[20] suggested that failure to demonstrate a greater QT interval on the surface ECG, despite delayed cellular action potentials in hypertrophied hearts, could be explained by the heterogeneous rates of depolarization and repolarization in individual myocytes. Because of this altered regional distribution ‘‘cardiac hypertrophy may result in little overall prolongation of the QT interval, even though it is a ‘long QT’ syndrome at the level of most (but not all) of the ventricular myocytes.’’ To assess this proposed asymmetry, several investigators have examined QT-interval dispersion, or the variability of the QT interval, in athletes. This measure is considered an index of heterogeneity, or regional differences, in ventricular repolarization and an increased in pathological hypertrophy associated with coronary artery Sports Med 2011; 41 (5)
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disease, hypertension and hypertrophic cardiomyopathy.[47] Studies of small groups of highly trained athletes have often indicated no differences in QT-interval dispersion,[47-50] and in the report by Halle et al.,[48] a significant negative relationship was observed between left ventricular mass and QT-interval dispersion. However, some investigators have described greater QTinterval dispersion in trained athletes;[44,51-53] Tanriverdi et al.[53] reported a positive correlation between left ventricular mass index and QTinterval dispersal among athletes. Perhaps instructive in deciphering these conflicting data are two particular reports. Jordaens et al.[44] found that QT-interval dispersal in 13 athletes with symptomatic ventricular tachycardia (but no underlying heart disease) was greater than any of the three control groups (road cyclists, basketball players and non-athletic individuals) all without dysrhythmias. Tanriverdi et al.[53] reported that among 56 endurance athletes, QT-interval dispersal was greater than in non-athletic subjects, but this was dependent on angiotensin-converting enzyme I/D polymorphism. These reports suggest that (i) heterogeneity of ventricular repolarization in athletes may be linked to disposition for ventricular dysrhythmias; and (ii) this association may be genetically controlled. To summarize, although far from conclusive, evidence exists that the repolarization characteristics of heart muscle may be different in highly trained athletes compared with non-athletes, and these features may mimic those associated with heart disease. However, that such features in athletes are (i) linked to ventricular hypertrophy; and/or (ii) predisposed to fatal ventricular dysrhythmias, remains to be demonstrated. 4. Frequency of Ventricular Dysrhythmias in Athletes The rate of sudden unexpected death in young athletes is approximately 3-fold greater than that of the general population.[54] The proposal that arrhythmias generated from the hypertrophy of the athlete’s heart can be responsible for such tragedies would be strengthened if, in fact, ª 2011 Adis Data Information BV. All rights reserved.
trained athletes could be demonstrated to have greater frequency of ventricular ectopy. On this point, however, the research data are not clear. Twenty-four hour ECG recordings in small groups of endurance athletes have disclosed ventricular ectopy in 40–70%, a frequency similar to that of untrained subjects.[55-59] In these reports, ectopy has generally been limited to isolated premature ventricular beats, and advanced forms of dysrhythmia (couplets, ventricular tachycardia) have been rare. In one study of 40 highly trained endurance athletes, Palatini et al.[38] found that complex forms of ventricular ectopy (multifocal beats, couplets, tachycardia) were significantly more common than in sedentary subjects (25% vs 5%, respectively). Patano and Oriel[60] found that 21% of runners had ventricular ectopy on maximal treadmill testing, but on a monitored field run that frequency rose to 60%. This apparently benign picture can be contrasted, however, with other reports of groups of selective elite-level competitors with dysrhythmias, often symptomatic, and evaluated in specialized sports medicine centres. These indicate a more serious aspect of ventricular ectopy in athletes. The role that the possible usage of doping agents (e.g. sympathetic agents such as amphetamines) might play in these findings is uncertain. Biffi et al.[61] described 70 highly trained athletes who, on 24-hour ECG monitoring, had frequent and complex premature ventricular contractions as well as least one burst of nonsustained ventricular tachycardia. Twenty-one (30%) had a structural cardiovascular abnormality (arrhythmogenic right ventricle, mitral valve prolapse, myocarditis, dilated cardiomyopathy). In two-thirds of the athletes, ectopy disappeared during or immediately following exercise testing, and of the 24 who underwent electrophysiological testing, sustained ventricular tachycardia could be provoked in only one. After a 5-month period of detraining, 71% of these athletes with dysrhythmias demonstrated a significant reduction in ectopy (<500 premature ventricular contractions over 24 hours and no ventricular tachycardia).[62] No complications were observed on resumption of training and during an average 8-year follow-up.[63] It was concluded that ventricular Sports Med 2011; 41 (5)
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dysrhythmias in trained athletes without cardiovascular abnormalities ‘‘appear benign and probably do not require alteration in athletic lifestyle.’’[61] Conversely, this experience appears to indicate clearly that athletic training in a healthy heart can provoke significant ventricular dysrhythmias. Whether or not this is specifically related to ventricular hypertrophy of the athlete’s heart is not clear. In another study of 175 elite-level athletes, Biffi et al.[61] could find no evidence of a relationship between frequency of ectopy and extent of left ventricular wall thickness. However, as the authors identified, true ventricular hypertrophy was not present in these athletes, with an average wall thickness of approximately 9.0 – 0.5 mm, and in no athlete did the septal or posterior wall exceed 13 mm. Palatini et al.[6] performed a 5-year follow-up of 52 professional endurance athletes who were found to have ventricular ectopy on an initial 24-hour ECG recording. Among those who were still training, frequency of complex ventricular ectopy had decreased from 21.7% at baseline to 13.1% at follow-up. In those who had ceased training, complex ectopy was observed in 21% at baseline but had subsequently disappeared in all athletes. While hypertrophy by ECG had diminished in the latter group, no relation was observed between wall thickness changes and disappearance of complex ectopy. Furlanello et al.[4] described findings among 766 young competitive athletes who underwent evaluation for symptoms and dysrhythmias over a 17-year period. This included eight cases of sudden death, 16 with aborted sudden death from ventricular fibrillation, and seven with induced ventricular tachyarrhythmia during electrophysiological testing. In all of these 31 cases, the athletes were found to have underlying structural heart disease or genetic electrical disorder (arrhythmogenic right ventricle cardiomyopathy [RVC], mitral valve prolapse, Wolff-ParkinsonWhite syndrome, long QT syndrome). However, in a subset of 74 elite international athletes referred for documented or suspected dysrhythmias, 60% had no underlying heart abnormality, a proportion similar to that observed in the total group. ª 2011 Adis Data Information BV. All rights reserved.
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While hypertrophic responses to athletic training might prove arrhythmogenic, cardiac autonomic neural remodelling with training can be expected to be protective against life-threatening rhythm disturbances. Endurance training is associated with augmented parasympathetic activity, which, in animals, has been demonstrated to reduce the risk of ventricular fibrillation induced by myocardial ischaemia.[64] 5. Sudden Death and the ‘Athlete’s Heart’ Recently, concern has been raised that certain clinical and autopsy findings assumed to indicate cardiac disease, particularly hypertrophic cardiomyopathy (HCM) and RVC, might, in fact, represent changes connected with athletic training.[4-7] Such observations, again, raise the possibility that cardiac remodelling in response to sports training per se might serve as a substrate for fatal ventricular tachyarrhythmias. 6. Hypertrophic Cardiomyopathy – or Not? HCM is a genetic disease characterized by a dramatic increase in chamber wall thickness, particularly involving the ventricular septum. Sports participation in patients with this disease is disallowed, since HCM carries a risk for sudden death, which is often associated with physical activity.[65] Although rare, HCM has been considered the leading cause of sudden unexpected death in young athletes in the US, mainly because it is difficult to detect on routine history and physical examination.[66] HCM shares overlapping features of ventricular hypertrophy with that which is seen in extreme cases of the condition in the athletes heart, and guidelines have been proposed to clinically distinguish the two.[67] However, as previously proposed for cases of sudden death in athletes, HCM may have been incorrectly diagnosed at autopsy and ventricular hypertrophy per se has been the trigger for fatal ventricular dysrhythmia.[7] This conclusion was based on the observation that demographical features of athletes dying of supposed HCM are not consistent with those typically seen in this Sports Med 2011; 41 (5)
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disease in the general population. Moreover, these features share a common propensity for ventricular hypertrophy as follows: Virtually all reported cases of HCM-related deaths in athletes have been in males, which cannot be explained by differential sports participation rates. In one report, males accounted for 55 of 56 cases of HCM or ‘probable’ HCM.[68] At the same time, there is no sex predilection for HCM in the general population. In addition, it is recognized that highly trained female athletes demonstrate less relative ventricular hypertrophy than their male counterparts.[69] HCM is not a common cause of sudden unexpected death during exercise in non-athletic populations. For instance, in a study of sudden death in a large number of American military recruits, only two cases of HCM were found among 17 subjects who had died during exertion.[70] African Americans account for a disproportionate number of deaths during athletic play from presumed HCM.[71] A greater propensity for ventricular hypertrophy in patients with cardiovascular disease is observed among Blacks. However, there is no racial predisposition for HCM in the general population. These observations suggest that at least some of the deaths in athletes attributed to HCM have represented, instead, the influence of recognized triggers for ventricular hypertrophy (athletic training, androgenic hormonal effects and African American race). 7. Right Ventricular Cardiomyopathy A similar story surrounds RVC, which is the most common cause of sudden death in young athletes reported in the Veneto region of Northern Italy.[54] RVC is characterized by right ventricular enlargement with replacement of myocardium by fat and fibrous tissue, a processes predisposing to fatal ventricular tachyarrhythmias. This is an inherited disease, and a positive family history can be obtained in about half of the cases. Highly trained athletes can also demonstrate significant right ventricular enlargement and, in a parallel ª 2011 Adis Data Information BV. All rights reserved.
fashion to HCM, criteria have been suggested to discriminate the athlete’s heart from RVC.[72] Heidbuchel et al.[5] described a group of 46 athletes, mostly cyclists, who were evaluated at cardiac centres with findings of complex ventricular arrhythmias (including >1 run of ventricular tachycardia). Two-thirds of the athletes demonstrated global or regional right ventricular dilatation. In 80% of the athletes, ventricular arrhythmias had left-bundle, branch-block morphology, indicating a right ventricular origin. Twenty-seven athletes (59%) satisfied standard diagnostic criteria for RVC, but only one had a family history of RVC. HCM and coronary artery abnormalities were present in <5%. Fat infiltration of the right ventricular wall detected by MRI, a central feature of RVC, was present in only 2 of 28 subjects. Nine died in follow-up, 0.5–9.3 years after the evaluation. The authors suggested that these findings indicated that endurance sports training per se can stimulate right ventricular morphological and electrical remodelling, predisposing to potentially fatal tachyarrhythmias. Thus, there is some support for the idea that anatomical and electrophysiological features of both HCM and RVC may be simulated by athletic training. This lends credence to the argument that in rare cases this training-induced remodelling might place athletes at risk for sudden death. 8. Conclusions This review has addressed evidence surrounding a causal chain consisting of the following: athletic training, which leads to ventricular hypertrophy, which produces to electrophysiological remodelling, which creates vulnerability to ventricular tachyarrhythmias, which predisposes to sudden death. The strength of the evidence supporting each of these associations varies. The data indicating that ventricular hypertrophy is associated with sports training are incontrovertible. For other associations, the data are conflicting, and one can marshall evidence to support or refute the validity of these outcomes. However, it is the final and most crucial association for which there exists the most uncertainty. Sports Med 2011; 41 (5)
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If the final association is true (i.e. ventricular arrhythmias from training-induced electrical remodelling in athletes predisposes to sudden death), then such occurrences must be extraordinarily rare. If one considers all the cases of sudden death among young athletes in the US that are related to ventricular hypertrophy (HCM, idiopathic ventricular wall thickening), the greatest incidence, or risk, of such events would approximate one case in half a million athletes.[66] The central question would be, therefore, if, in extremely rare cases, ventricular responses to training can trigger fatal arrhythmias, what is unique about that unfortunate athlete? A particular pattern of ventricular morphological or electrical remodelling? A genetically-created risk for hypertrophy-related fatal arrhythmias? Differences in sympathetic-cardiac interactions during exercise? Many cases of sudden cardiac death in athletes do not occur with intense exercise but rather during low-grade play, warm-up, or even following bouts of training or competition. This observation led Varro and Baczko[9] to conclude that these fatal events were not ischaemic in nature but were rather explained by arrhythmias generated by sympathetic stimulation of a predisposed myocardium (i.e. with heterogeneity of ventricular repolarization). These authors suggested that sudden death via this scenario might largely reflect simply ‘bad luck’. ‘‘On the level of the individual, as a contributing factor, misfortune should be emphasized as the most important factor, since in case the trigger extrasystole [from sympathetic stimulation] occurs even a fraction of a millisecond prior to or later than the vulnerable period, serious cardiac arrhythmia will not develop.’’ This suggested scenario mimics that seen in young athletes who have died after being struck in the chest by a ball or blunt object (commotio cordis), where fatal ventricular arrhythmias have occurred at the same time (by chance) as the impact itself, during a narrow vulnerable portion of the cardiac cycle.[73] It can also be suggested that such fatal events occurring by chance might reflect predisposing conditions such as a myocardium sensitized by viral infection, alcohol consumption or drugs. ª 2011 Adis Data Information BV. All rights reserved.
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The question of arrythmogenicity of the athlete’s heart and its possible connection to sudden death in young athletes remains unresolved. Unfortunately, the extreme rarity of such cases does not lend itself to any conventional experimental approach. Answers may come from a better understanding of the electrophysiological responses to acute and repetitive exercise, as well as insights into the role of sympathetic stimulation as a triggering factor. In addition, the role that genetic influences might play in susceptibility to arrhythmic sudden death in athletes needs to be explored. Acknowledgements No sources of funding were used to conduct this review or prepare this manuscript. The author has no conflicts of interest that are directly relevant to the content of this review.
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35. Tibbits GF, Barnard RJ, Baldwin KM, et al. Influence of exercise on excitation-contraction coupling in rat myocardium. Am J Physiol 1981; 240: H472-80 36. Gwathmey JK, Slawsky MT, Perreault CL, et al. Effect of exercise conditioning on excitation-contraction coupling in aged rats. J Appl Physiol 1990; 69: 1366-71 37. Hanne-Paparo N, Drory Y, Schoenfeld Y, et al. Common ECG changes in athletes. Cardiology 1976; 61: 267-78 38. Palatini P, Maraglino G, Sperti G, et al. Prevalence and possible mechanisms of ventricular arrhythmias in athletes. Am Heart J 1985; 110: 560-7 39. Sharma S, Whyte G, Elliott P, et al. Electrocardiographic changes in 1000 highly trained junior athletes. Br J Sports Med 1999; 33: 319-24 40. Stolt A, Kujala UM, Karjalainen J, et al. Electrocardiographic findings in female endurance athletes. Clin J Sport Med 1997; 7: 85-9 41. Van Ganse W, Versee L, Eylenbosch W, et al. The electrocardiogram of athletes: comparison with untrained subjects. Br Heart J 1970; 32: 160-4 42. George KP, Wolfe LA, Burggraf GW, et al. Electrocardiographic and echocardiographic characteristics of female athletes. Med Sci Sports Exerc 1995; 27: 1362-70 43. Heinz L, Sax A, Robert F, et al. T-wave variability detects abnormalities in ventricular repolarization: a prospective study comparing healthy persons and Olympic athletes. Ann Noninvasive Eectrocardiol 2009; 14: 276-9 44. Jordaens L, Missault L, Pelleman G, et al. Comparison of athletes with life-threatening ventricular arrhythmia with two groups of healthy athletes and a group of normal control subjects. Am J Cardiol 1994; 74: 1124-8 45. Langdeau JB, Blier L, Turcotte H, et al. Electrocardiographic findings in athletes: the prevalence of left ventricular hypertrophy and conduction defects. Can J Cardiol 2001; 17: 655-9 46. Rajappan K, O’Connell C, Sheridan DJ. Changes in QT interval with exercise in elite male rowers and controls. Int J Cardiol 2003; 87: 217-22 47. Zoghi M, Gurgun C, Yavuzgil O, et al. QT dispersion in patients with different etiologies of left ventricular hypertrophy: the significance of QT dispersion in endurance athletes. Int J Cardiol 2002; 84: 153-9 48. Halle M, Huonker M, Hohnloser SH, et al. QT dispersion in exercise-induced ventricular hypertrophy. Am Heart J 1999; 138: 309-12 49. Mayet J, Kanagarantnam P, Shahi M. QT dispersion in athletic left ventricular hypertrophy. Am Heart J 1999; 137: 678-81 50. Turkmen M, Barutcu I, Esen AM, et al. Assessment of QT interval duration and dispersal in athlete’s heart. Int J Med Res 2004; 32: 626-32 51. Lawan A, Ali MA, Bauchi SSD. QT dispersion in dynamic and static group of athletes. Nig J Physiol Sci 2006; 21: 5-8 52. Munir DF, Love NWA, McCann GP, et al. Athletic ventricular hypertrophy is associated with increased QT dispersion [abstract]. Am Heart J 1999; 33 Suppl. A: 2 53. Tanriverdi H, Kaftan HA, Evrengul H, et al. QT dispersion and left ventricular hypertrophy in athletes: relationship with angiotensin-converting enzyme I/D polymorphism. Acta Cardiol 2005; 60: 387-93
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54. Corrado D, Basso C, Rizzoli G, et al. Does sports activity enhance the risk of sudden death in adolescents and young adults. JAMA 2003; 42: 1959-63 55. Bjornstad H, Storstein L, Meen HD, et al. Ambulatory electrocardiographic findings in top athletes, athletic students and control subjects. Cardiology 1994; 84: 42-50 56. Campbell RWF. Ventricular arrhythmias in normal individuals and athletes. Eur Heart J 1988; 9 Suppl. G: 113-7 57. Pilcher GF, Cook J, Johnston BL, et al. Twenty-four hour continuous electrocardiography during exercise and free activity in 80 apparently healthy runners. Am J Cardiol 1983; 52: 859-61 58. Talan DA, Bauernfeind RA, Ashley WW, et al. Twenty-four hour continuous ECG recordings in long-distance runners. Chest 1982; 82: 19-24 59. Viitsalo M, Kala R, Eisalo A. Ambulatory electrocardiographic recording in endurance athletes. Br Heart J 1982; 47: 213-20 60. Pantano JA, Oriel RJ. Prevalence and nature of cardiac arrhythmias in apparently normal well-trained runners. Am Heart J 1982; 104: 762-8 61. Biffi A, Maron BJ, Di Giacinto B, et al. Relation between training-induced left ventricular hypertrophy and risk for ventricular tachyarrhythmias in elite athletes. Am J Cardiol 2008; 101: 1792-5 62. Biffi A, Maron BJ, Verdile L, et al. Impact of physical deconditioning on ventricular tacharrhythmias in trained athletes. J Am Coll Cardiol 2004; 44: 1053-8 63. Biffi A, Pelliccia A, Verdile L, et al. Long-term clinical significance of frequent and complex ventricular tachyarrhythmias in trained athletes. J Am Coll Cardiol 2002; 40: 446-52 64. Billman GE. Cardiac autonomic neural remodeling and suspectibility to sudden cardiac death: effect of endurance
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Correspondence: Dr Thomas Rowland, MD, Department of Pediatrics, Baystate Medical Center, Springfield, MA 01199, USA. E-mail:
[email protected]
Sports Med 2011; 41 (5)
Sports Med 2011; 41 (5): 413-432 0112-1642/11/0005-0413/$49.95/0
REVIEW ARTICLE
ª 2011 Adis Data Information BV. All rights reserved.
Strength Testing and Training of Rowers A Review Trent W. Lawton,1,2 John B. Cronin2,3 and Michael R. McGuigan1,2,3 1 New Zealand Academy of Sport, Performance Services - Strength and Conditioning, Auckland, New Zealand 2 Sport Performance Research Institute New Zealand, AUT University, Auckland, New Zealand 3 School of Biomedical and Health Sciences, Edith Cowan University, Joondalup, Western Australia, Australia
Contents Abstract. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Search Strategy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Evaluation of Quality of Current Evidence Base . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. Measuring Rowing Strength . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5. How Strong are Elite Rowers? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6. Reliability of Strength, Power and Endurance Tests . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7. Validity of Strength, Power and Endurance Tests . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.1 Peak Forces (Maximal Strength) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.2 Sustained Forces (Strength Endurance) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.3 Scaling of Strength and Endurance Data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.4 Alternative Applications of Strength Testing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8. The Effects of Strength Training on Rowing Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.1 Strength Training and Rowing Injuries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9. Future Research . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Abstract
413 414 415 415 417 418 418 419 419 421 422 423 423 428 429 429
In the quest to maximize average propulsive stroke impulses over 2000-m racing, testing and training of various strength parameters have been incorporated into the physical conditioning plans of rowers. Thus, the purpose of this review was 2-fold: to identify strength tests that were reliable and valid correlates (predictors) of rowing performance; and, to establish the benefits gained when strength training was integrated into the physical preparation plans of rowers. The reliability of maximal strength and power tests involving leg extension (e.g. leg pressing) and arm pulling (e.g. prone bench pull) was high (intra-class correlations 0.82–0.99), revealing that elite rowers were significantly stronger than their less competitive peers. The greater strength of elite rowers was in part attributed to the correlation between strength and greater lean body mass (r = 0.57–0.63). Dynamic lower body strength tests that determined the maximal external load for a one-repetition maximum (1RM) leg press (kg), isokinetic leg extension peak force (N) or leg press peak
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power (W) proved to be moderately to strongly associated with 2000-m ergometer times (r = -0.54 to -0.68; p < 0.05). Repetition tests that assess muscular or strength endurance by quantifying the number of repetitions accrued at a fixed percentage of the strength maximum (e.g. 50–70% 1RM leg press) or set absolute load (e.g. 40 kg prone bench pulls) were less reliable and more time consuming when compared with briefer maximal strength tests. Only leg press repetition tests were correlated with 2000-m ergometer times (e.g. r = -0.67; p < 0.05). However, these tests differentiate training experience and muscle morphology, in that those individuals with greater training experience and/or proportions of slow twitch fibres performed more repetitions. Muscle balance ratios derived from strength data (e.g. hamstring-quadriceps ratio <45% or knee extensor-elbow flexor ratio around 4.2 – 0.22 to 1) appeared useful in the pathological assessment of low back pain or rib injury history associated with rowing. While strength partially explained variances in 2000-m ergometer performance, concurrent endurance training may be counterproductive to strength development over the shorter term (i.e. <12 weeks). Therefore, prioritization of strength training within the sequence of training units should be considered, particularly over the non-competition phase (e.g. 2–6 sets · 4–12 repetitions, three sessions a week). Maximal strength was sustained when infrequent (e.g. one or two sessions a week) but intense (e.g. 73–79% of maximum) strength training units were scheduled; however, it was unclear whether training adaptations should emphasize maximal strength, endurance or power in order to enhance performance during the competition phase. Additionally, specific on-water strength training practices such as towing ropes had not been reported. Further research should examine the onwater benefits associated with various strength training protocols, in the context of the training phase, weight division, experience and level of rower, if limitations to the reliability and precision of performance data (e.g. 2000-m time or rank) can be controlled. In conclusion, while positive ergometer timetrial benefits of clinical and practical significance were reported with strength training, a lack of statistical significance was noted, primarily due to an absence of quality long-term controlled experimental research designs.
1. Introduction Depending on crew size, boat type and weather conditions, an Olympic 2000-m rowing event lasts somewhere between 5:19.85 and 7:28.15 minutes, based on 2009 world best times. A relatively high energy cost with sculling (two oars) or rowing (single oars), was attributed to drag created by wind and water resistance.[1] Subsequently, elite rowers have developed better technique, demonstrating a more efficient recovery phase (particularly in the timing of forces at the catch), a faster stroke rate and a stronger, more consistent and effective propulsive stroke.[1-8] All other factors remaining equal, rowers who sustain greater net ª 2011 Adis Data Information BV. All rights reserved.
propulsive forces (or strength) achieve faster boat speeds.[3,7] From this relatively simplistic description, and with consideration of the impulses required to change boat inertia on starting or over the finishing burst of 2000-m racing, it would appear that rowing requires muscle strength, endurance and power. For the purposes of this review, strength was broadly defined as the amount of force produced in a specific task or activity. Irrespective of the mode of assessment or the duration required, the peak or greatest force achieved in any task has commonly been defined as the ‘maximum strength’.[9] ‘Strength endurance’ (or muscle endurance) on the other hand, was defined as the total Sports Med 2011; 41 (5)
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concentric work produced over a number of repetitions, often within a designated time interval.[10] A rower who performed an equal quantity of work more quickly was more powerful; therefore, a third and equally important measure of strength was muscle ‘power’.[11] Given these demands and that on-water performance could not be predicted precisely from any single test, including ergometer time trials,[7,10,12-16] testing and training of various strength parameters have been incorporated into the physical preparation of rowers. The reliability and relevance of such practice in the context of the physical preparation of the rower provided the focus for this review. Therefore, the purpose of this review was 2-fold: to identify strength tests that were reliable and valid correlates (predictors) of rowing performance; and, to establish the benefits gained when strength training was integrated into the physical preparation plans of rowers. 2. Search Strategy This review evaluated and interpreted the current evidence base to provide coaches, sport scientists and rowers alike, with an understanding of the rationale and application of strength testing and training principles to rowing. The conclusions of this article were drawn from either peer-reviewed journal publications or conference proceedings. Books or association journals were excluded in the analysis, but cited where of value for understanding the concepts of rowing or the training of rowers. Google Scholar and the EBSCO Host search engines with varying combinations of the keywords ‘strength’, ‘power’ and/or ‘endurance’ with the term ‘rowing’ or ‘oarsmen/women’ were used to filter relevant research from electronic databases such as MEDLINE, CINAHL, Biomedical Reference Collection: Basic, PubMed and SPORTDiscus. Bibliographical referral was an equally important search strategy. Studies were included in the analysis if the investigation utilized dynamometry to assess muscle strength (including tests using electromyography (EMG), rowing ergometers or on-water analysis, which were considered measures of rowing force) ª 2011 Adis Data Information BV. All rights reserved.
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or strength training interventions (excluding resisted inspiration studies). For inclusion, a project must have recruited rowers with at least 1 year of experience. For the purposes of this review, the level of rower was defined by the level of competition experience (where identified). An ‘elite’ subject sample utilized rowers who participated in open-age international competition (Class A), such as the World Cup regattas or World Championships. A ‘sub-elite’ sample recruited junior or under23 age competitors with international experience, or open-age rowers of national ranking or competition experience. Finally, ‘non-elite’ rowers participated in club or university rowing events. 3. Evaluation of Quality of Current Evidence Base In total, the search process recovered 53 papers. Around half (n = 27) used rowers classified as subelite or elite. The authors were unable to find any scientific paper that incorporated a measure of strength into a model of on-water rowing performance (i.e. race ranking or 2000-m times) because models utilizing on-water results have limitations primarily due to large standard error of the estimates of data.[16] Therefore, discussion was limited to the relevance of strength testing and training as part of the physiological preparation and reduction of injury risk associated with competitive rowing. The majority of studies (n = 35) were descriptive investigations that used strength testing to characterize differences between rowers (e.g. non-elite and elite) with non-rower populations. Less than one-third (n = 17) of the recovered research was intervention based, of which ten papers involved strength training along with a preand post-measure of rowing performance (i.e. ergometer time trial) and strength (e.g. one-repetition maximum [1RM] leg press). The methodological quality of this experimental research was assessed using the qualitative evaluation criteria proposed by Brughelli and colleagues.[17] Their method used a 10-item scale to rate the quality of the research design overcoming the harsh Delphi, PEDro and Cochrane scales ratings of most strength and conditioning research due to the lack of blinding Sports Med 2011; 41 (5)
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Table I. Methodological rating of the quality of intervention studies incorporating strength testing, training and rowing performance Itema
Bell duManoir Ebben Gallagher Haykowsky Kennedy Kramer et al.[18] et al.[19] et al.[20] et al.[21] et al.[22] and Bell[23] et al.[24]
Syrotuik et al.[25]
Tse Webster et al.[26] et al.[27]
Inclusion criteria were clearly stated
1
2
1
2
2
1
1
1
2
1
Rowers were randomly allocated to groups
2
0
2
2
0
0
0
1
1
0
Intervention was clearly defined
1
1b
2
1
1b
1b
2
2b
1
1
Groups were tested for similarity at baseline
1
1
2
0
1
1
2
1
2
1
Use of a control group
0
0
0
2
0
0
1
1
1
0
Outcome variables were clearly defined
2
2
2
1
2
2
2
2
2
2
Assessments were practically useful
2
2
1
1
2
2
2
2
2
2
Duration of intervention was practically useful
1
1
1
1
1
1
1
1
1
1
Between-group statistical analysis was appropriate
2
2
2
2
2
2
2
2
2
2
Point measures of variability
1
1
1
1
1
1
1
1
2
1
Rating (out of 20)
13
12
14
13
12
11
14
13
16
11
a
The score for each criterion was as follows: 0 = clearly no; 1 = maybe; and 2 = clearly yes.
b
Strength training intervention was not the primary independent variable of interest.
and randomization of intervention treatments. However, most of the ‘quasi-experimental’ interventions reviewed lacked use of either a crossover research design, control group and/or randomization allocation of rowers to treatment interventions. Subsequently, many papers rated poorly when the Brughelli et al.[17] evaluation criteria were used (see table I). Nonetheless, these descriptive research interventions reported positive performance outcomes of clinical[26,28] and practical significance[20,21] from the short-term inclusion of strength training that warranted discussion within the relevant sections of this review. There were also constraints to the relevance and applicability of some data when reviewed in the context of contemporary rowing practices. For example, over the past 30 years, training volumes have increased by >20% in many countries, with medal winners now training between 1100 and 1200 hours a year.[29] Such volumes of endurance training are far greater than the 4 days (or around 6 hours) a week deployed in the referenced research. Additionally, this review synª 2011 Adis Data Information BV. All rights reserved.
thesized data from research spanning over 40 years (1968–2010). After allowing for a population trend of increasing height of 0.03 m, the 21st century elite rower is some 0.06 m taller at 1.94 – 0.05 m and 1.81 – 0.05 m (male and females, respectively), and about 6.4 kg and 12.1 kg heavier at 94.3 – 5.9 kg and 76.6 – 5.2 kg than Olympic rowers of just over two decades earlier.[30] Given the significant influence of height and lean body mass on 2000-m performance,[30-35] the divergent characteristics of rowing populations must not be overlooked in review of the data. Finally, 2000-m ergometer times of <328 seconds and 374 seconds, respectively, for heavy and lightweight males (379 seconds and 407 seconds, respectively, for females) were recently proposed as benchmarks for a medal placing in the A-Finals for small boat categories (e.g. single or double sculls) at the 2007 World Championships.[16] While not the definitive measure of an elite rower, such benchmarks were considerably faster than average ergometer times of rowers reviewed in this article. Thus, it would appear warranted to revisit many of the Sports Med 2011; 41 (5)
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past experimental themes in future research. In particular, with consideration of the increased professionalism, endurance training volumes and general changes in anthropometrical build, the testing and training of strength parameters within the distinct phases of physical preparation of the champion elite warrant investigation. Stronger experimental research designs (e.g. use of control groups or crossover designs) over periods of longer intervention (e.g. more than 12 weeks) were also required (regardless of the experience of the population examined). Finally, where standard errors with modelling data permit, the common variances shared between changes in strength and on-water performance data should be explored. 4. Measuring Rowing Strength Without doubt, the most valid and specific measure of rowing strength is to assess the force vectors produced during 2000-m racing. Hartmann et al.[36] reported that peak force significantly decreased during maximal free rating 6-minute rowing ergometry. From the first stroke to the last stroke, peak forces after the initial and most
forceful ten strokes (around 1350 N for men and 1020 N for women) did not exceed more than 65–70% of maximum force thereafter. As the level of force declined, rowers substituted both an increase in stroke speed and rate in order to sustain mechanical power assessed at the flywheel. Similar results have been reported during onwater racing, the level of force up to 1000 N and 1500 N for the start; thereafter, speed was maintained with peak rowing forces between 500 and 700 N for the 210–230 strokes performed over 6 minutes.[37] Relatively modest forces produced at fast movement speeds accentuate the importance of stroke-to-stroke consistency, stroke smoothness and a high mean propulsive stroke power in order to achieve fast boat speeds.[3,6,7] Forces measured at the oar-pin during the drive phase[6,7] from catch (i.e. oar-blade entry into the water) to finish (i.e. oar-blade exit from the water) rise then fall producing a bell-shaped propulsive impulse (see figure 1). When disaggregated to examine the timing and relative contribution of the main body segments involved in the propulsive stroke, analysis showed that the leg drive (i.e. knee extension)
Drive 2
Drive 3
Drive 1
Force (N) Release Catch
Time (sec) Recovery (pre-entry to catch)
Fig. 1. Schema of the main phases and force-time characteristics of the propulsive rowing stroke.
ª 2011 Adis Data Information BV. All rights reserved.
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produced just under half, the trunk swing (i.e. hip and trunk extension) almost one-third and the arms (i.e. elbow flexion and shoulder adduction) less than one-fifth of total stroke power.[5,38] Subsequently, strength tests of these main body segments have been used to compare the differences between elite and non-elite rowers, irrespective of rowing experience or skill. For example, stronger non-elite oarswomen produced greater leg extension power across a spectrum of loads (e.g. 17.5% greater power at 50% 1RM) compared with weaker controls[11] and stronger sub-elite oarsmen sustained greater power (849.4 W) in 30 seconds of arm cranking than club level (610.2 W) rowers.[39] Similarly, isokinetic leg flexion strength tests proved useful for the early identification of individuals with the physiological potential to excel at rowing,[13] while also having been used to identify possible training interventions to bridge the gap between slower and faster rowers of equivalent skill.[40] 5. How Strong are Elite Rowers? Internationally successful rowers are taller, heavier, of greater sitting height and lower fatmass than their less successful peers.[30-34,41] They have some of the highest absolute aerobic power . (e.g. maximum oxygen uptake [VO2max] values over 6.0 L/min and 4.0 L/min for males and females, respectively) reported of any competitive sport.[2,37,42] Rowers are also relatively strong when comparisons of strength are made with other endurance athletes.[2,43-45] The comparison of greatest interest to rowers and coaches alike is: how strong are the fastest rowers? Elite male rowers generated a force of more than 2000 N in an isometric simulated-row position[46] and forces over 4000 N at 120 knee extension.[47] They can produce forces of around 300 N at 1.05 radians per second during isokinetic leg extension,[13,48,49] and cable or bench row 1RM loads of around 90 kg.[50,51] Based on the strength training data of elite male rowers, strength targets (expressed as a factor relative to body mass) for 1RM dead lift (1.9), back squat (1.9) and bench row (1.3) have been suggested.[52] Elite female rowers produce a force of around ª 2011 Adis Data Information BV. All rights reserved.
200 N at 1.05 radians per second during leg extension.[13,53] Strength targets expressed as a factor relative to body mass for 1RM dead lift (1.6), back squat (1.6) and bench row (1.2) have also been reported based on the strength data of elite female rowers.[52] Other useful data can be interpreted from the substantial literature that has investigated novice and sub-elite rowers. In summary, male non-elite rowers leg press around 290 kg for a 1RM[19,23,27,54,55] (168 kg for women[10,23,24,27]) and bench row around 80 kg for a 1RM.[55] Subelite rowers might perform over 100 repetitions with a load of approximately 50 kg (or about 50% of a 1RM) for a bench pull task over 6 minutes.[55,56] 6. Reliability of Strength, Power and Endurance Tests Comparisons between the strength of novices and elite rowers are interesting but potentially meaningless if the reliability and validity of such tests to rowing performance is questionable. Hopkins[57] argued, when selecting tests to monitor the progression of an athlete, that it is important to take into account the uncertainty or noise in the test result, ideally, for the specific population of interest. The precision of testing is important particularly if an attempt is made to replicate the data of previous research, or when the tests are used to assess different sample populations. The reliability for a range of strength and power measures commonly used with rowers appears quite robust. Intra-class correlations (ICC) for isokinetic leg extension peak torque range from 0.82 to 0.94.[18,58,59] The coefficient of variations (CV) for concentric power using a linear encoder on a seated cable row ranged from 3% to 5%.[50] Also, the reliability of tests using the leg press or prone bench pull exercise trialled with rowers appear as robust as reliability trials using the same exercises but with inexperienced middle-aged men (reported ICCs of 0.99, or typical [standard] error of the mean expressed as a CV [log transformed] of 3.3%).[18,60] The authors were unable to ascertain the reliability for typical upper and lower body (e.g. leg pressing or arm rowing) repetition endurance Sports Med 2011; 41 (5)
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tests typically used by rowers from previous literature. It is likely that they are less robust compared with maximal strength assessments, given the need to standardize lifting tempos, test durations and qualitative technical criteria to assess in the determination of test data (i.e. completed repetitions). Isometric measures of strength endurance of the abdominal core of the body appear reasonably stable, but again, like repetition tests, the duration of the test and qualitative assessment to determine test completion reduce the precision and reliability of the measures with reported ICCs ranged from 0.76 to 0.89 for right and left side static holds over 90 seconds, 0.88 for a spine extension test lasting 2 minutes on average and 0.93 for a spine flexor test lasting almost 3 minutes.[61] However, ICCs ranging between 0.97 and 0.99 for the same tests with rowers of similar age, experience and build (height and lean body mass) have also been reported.[26] 7. Validity of Strength, Power and Endurance Tests Strength data, while offering satisfactory precision, needs to be a relevant and valid measure of rowing ability. One form of validity can be inferred when strength significantly differentiates rowers of varying ability (e.g. novice and elite). Alternatively, the validity of strength data can be evaluated using correlation and regression analysis in an attempt to explain variances in rowing performance (e.g. 2000-m ergometer time trial). The estimation of correlation coefficients is dependent on a number of statistical criteria, namely the assumption of normality, linearity and homoscedasticity of data and a sample size adequate for the number of variables included in the analysis. Many of the studies reviewed do not report or violate one or all of these assumptions. This may be of little concern given that the strength of the relationship is often of interest within the unique population selected. However, the risk here is that often these predictor data are used to model performance outcomes and the relationships between data are ignored. At this ª 2011 Adis Data Information BV. All rights reserved.
419
point, it should be noted that a curvilinear regression between leg extension power (W) and ergometer time (seconds) provided a better fit (r2 = 41%) to the explained variance in rowing performance than linear regression (r2 = 38%).[62] In practical terms, this may mean relatively small increases in strength are associated with relatively large improvements in rowing performance changes for weaker rowers, whereas, relatively large increases in strength may be associated with comparatively small, although significant, improvements in rowing performance for stronger rowers. 7.1 Peak Forces (Maximal Strength)
The earliest tests of strength in rowers used strain gauges to assess isometric muscle forces of body segments at specific joint angles.[12,39,46] However, these isometric strength tests did not appear in any precise way to discriminate between levels of rowing performance. For example, a simulated rowing position differentiated the strength between world class rowers and national champions and between national champion and senior rowers;[46] however, multiple regression analysis found that the rank of a rower for crew selection was weakly explained (r = 0.577; p < 0.05) by isometric strength and experience compared with rowing ergometer trials (r = 0.895; p < 0.05).[12] Furthermore, maximal isometric force did not correlate with power or force production during modified ergometer rowing (albeit small sample sizes).[47] Dynamic muscle strength and power tests more effectively discriminate between performance abilities.[63,64] Highly ranked elite rowers perform better in isokinetic leg strength[13,40,49] and arm cranking power tests.[39] Those strength tests with superior discriminative ability involve bi-lateral recruitment of large muscle mass, such as the leg press exercise (see table II). However, maximal dynamic tests involving smaller muscle mass, such as the upper body, provide ambiguous insight into ergometer performance (see table III). In reviewing the literature, it was not obvious whether advances in strength testing technology provided any superior precision, reliability or validity of data to rowing performance. In terms of the interrelationships amongst these tests, some Sports Med 2011; 41 (5)
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ª 2011 Adis Data Information BV. All rights reserved.
Table II. Leg strength assessment and ergometer performance Strength test
Rowers (n)
Phase, mean strength and ergometer results (– SD)
Main findings
Chun-Jung et al.[54]
45 incline leg press (knee flexion ~90), Cybex (USA) 1RM (kg)
Non-elite (17)
Non-competitive: Males (n = 10) 1RM: 154.6 – 26.9 kg 2000 m (C2): 452.2 – 25.3 sec Females (n = 7) 1RM: 130.5 – 15.3 kg 2000 m (C2): 521.4 – 19.2 sec
Pooled 1RM (144.7 – 25.4 kg) correlated with (r = –0.536; p < 0.05) 2000-m time (481 – 41.4 sec)
Ju¨rima¨e et al.[55]
45 incline leg press (knee flexion ~90), unstated manufacturer. 1RM and continuous max. reps with 50%. 1RM in 7 min (reps)
Non-elite males (12)
Competitive: 1RM: 252.3 – 44.3 kg max. reps: 173.5 – 11.8 2000 m (C2): 417.2 – 14.3 sec
Max. reps correlated with 2000-m time (r = -0.677; p < 0.05), but not 1RM
Kramer et al.[10]
45 incline leg press (knee flexion ~100), Champion Barbell Company (USA). 1RM and max. reps at 28 reps/min with 70%. 1RM in 7 min (J)
Non-elite females (16), sub-elite females (4)
Non-competitive: 1RM: 172.6 – 33.0 kg max. reps: 13 932 – 5335 J 2500 m (C2): 591 – 41 sec
1RM and max. reps correlated with 2500-m time (r = -0.57 and -0.51, respectively; p < 0.05)
Kramer et al.[59]
Unilateral leg extension, Kin-Com (USA). Peak and average torque (Nm) of 3 reps at 160/sec
Non-elite lightweight males (15)
Competitive: PT: 202 – 24 Nm AT: 171 – 19 Nm 2000 m (C2): 412.5 – 11.5 sec
Oarside significantly stronger than non-oarside (~6%; p < 0.01). Poor correlations between oarside and non-oarside strength measures and 2000-m times (ranged from 0.32 to -0.42; p > 0.05)
Kramer et al.[10]
Unilateral leg extension, Kin-Com (USA). Peak torque at 180/sec from sum of highest 5 concentric reps for each leg
Non-elite females (16), sub-elite females (4)
Non-competitive: PT: 279 – 44 Nm 2500 m (C2): 591 – 41 sec
No significant correlation between isokinetic leg extension with ergometer time (range, r = -0.27 to -0.37; p > 0.05). Isokinetic strength high correlation with 1RM 45 leg press (r = 0.75)
Russell et al.[15]
Bilateral leg extension, Cybex (USA). Peak torque at 1.05 radians/sec of 3 reps
Sub-elite males (19)
Non-competitive: PT: 268 Nm (SD not stated) 2000 m (C2): 403 – 16.2 sec
Isoinertial
Isokinetic
Continued next page
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Sports Med 2011; 41 (5)
. VO2max (r = -0.43), body mass (r = -0.41) and leg extensor strength (r = -0.40) were the major significant (p < 0.05) predictors of rowing ergometer performance
ª 2011 Adis Data Information BV. All rights reserved.
1RM = one-repetition maximum; AT = average torque; C2 = Concept2 rowing ergometer; max. = maximum; NS = not specified; PP = peak power; PT = peak torque; reps = repetitions.
Absolute leg press power correlated with ergometer time (r = -0.52; p < 0.001), but not when expressed relative to bodyweight (r = -0.21; p > 0.05) NS PP: 2300 – 379 W 2000 m (C2): 426 – 14.9 sec Horizontal bilateral leg press, Anaeropress (Japan). Peak power (W) from average of best two efforts of five trials Yoshiga and Higuchi[35]
Non-elite males (78)
Ergometer time related to height (r = -0.48; p < 0.001), body mass (r = -0.73; p < 0.001), fatfree mass (r = -0.76; p < 0.001) and leg press power (r = -0.62; p < 0.001) NS PP: 2260 – 367 W 2000 m (C2): 425 – 20 sec Non-elite males (332) Horizontal bilateral leg press, Anaeropress (Japan). Peak power (W) from average of best two efforts of five trials Yoshiga and Higuchi[62]
NS PP: 2241 – 286 W 2000 m (C2): 409.3 – 12.2 sec Non-elite males (16) Horizontal bilateral leg press, Anaeropress (Japan). Peak power (W) from average of best two efforts of five trials Shimoda et al.[65]
Accommodating resistance
Phase, mean strength and ergometer results (– SD) Strength test Study
Table II. Contd
421
Rowers (n)
Main findings
. Ergometer time correlated with VO2max (r = -0.61; p = 0.012), leg press power (r = -0.68; p = 0.004) and stroke power consistency (r = 0.69; p = 0.003)
Rowing Strength Testing and Training
researchers found that isokinetic leg strength data were strongly correlated with isoinertial leg strength data (r = 0.75; p < 0.05).[10] Therefore, either maximal isoinertial leg strength (kg)[10,54] or power (W)[35,62,65] or peak isokinetic quadriceps strength data (N)[10,15] can be used to provide valid physiological measures and predictors of non-elite and sub-elite rowers’ ergometer performance. It should be noted that this relationship has not been tested with elite-level rowers. Acknowledging limitations with single factor performance models,[15] the greater strength of elite rowers can in part be attributable to a larger . muscle mass.[30-34] Along with VO2max greater lean body mass was a significant attribute of champion elite rowers[30-32] and strongly correlated with ergometer performance (r = -0.77 to -0.91).[34,35] Maximal strength was also strongly associated with muscle mass and cross-sectional area (r = 0.57–0.63).[48,49,53,66] It appears likely that a more valid strength test to rowing, targets those body segments more critical to the development of rowing power (i.e. anterior thigh, posterior chain complex and erector spinae muscle groups of the legs and trunk).[38] 7.2 Sustained Forces (Strength Endurance)
Given a large aerobic energy contribution (approximately 70–85%) in racing 2000 m,[1,2,37,67] it was not surprising that tests of local muscle strength endurance (i.e. repetition endurance tests) have been investigated. Strength endurance has been assessed as the maximum repetitions achieved with a load of approximately 50% of 1RM,[51,68-70] or calculated from the quantity of work achieved based on distance and repetitions executed using a load of 70% of 1RM.[10,24] A lifting tempo and time constraint for the test is typical for this type of assessment. However, the number of repetitions completed in these tests remains much less than the number of strokes completed during 2000 m of rowing. These tests also overlook important kinematic data that may prove useful in the analysis of performance differences (e.g. time and velocity of concentric muscle actions). Nonetheless, strength endurance tests using a leg press, report strong to modest Sports Med 2011; 41 (5)
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Table III. Arm strength and ergometer performance Study
Strength test (isoinertial)
Rowers (n)
Phase, mean strength and ergometer results (–SD)
Main findings
Chun-Jung et al.[54]
Inverted rows performed in a squat rack, MF Athletic Corp. (USA). Max. reps with bodyweight
Non-elite (17)
Non-competitive: Males (n = 10) max. reps: 13.9 – 4.0 2000 m (C2): 452.2 – 25.3 sec Females (n = 7) max. reps: 3.9 – 3.4 2000 m (C2): 521.4 – 19.2 sec
Pooled max. reps data (9.8 – 6.3) correlated with ergometer time (r = -0.624; p < 0.05)
Ju¨rima¨e et al.[55]
Prone bench pull, unstated manufacturer. 1RM and continuous max. reps with 50%. 1RM in 7 min
Non-elite males (12)
Competitive: 1RM: 82.0 – 12.6 kg max. reps: 122.6 – 17.7 2000 m (C2): 417 – 14.3 sec
1RM and max. reps not significantly correlated with ergometer time (correlation not reported)
Kramer et al.[10]
Prone bench pull, Universal Inc., (USA). 1RM and max. reps at 28 reps/min with 70%. 1RM in 7 min (J)
Non-elite females (16), sub-elite females (4)
Non-competitive: 1RM: ~48.7 – 7.1 kg max. reps: 5528 – 2511 J 2500 m (C2): 591 – 41 sec
1RM, but not max. reps, significant relationship with ergometer time (r = -0.52; p < 0.05; and r -0.25; p > 0.05, respectively)
1RM = one-repetition maximum; C2 = Concept2 rowing ergometer; max. = maximum; reps = repetitions.
correlations with ergometer time (r = -0.68 and -0.51, respectively; p < 0.05).[10,55] In contrast, non-significant correlations are associated with upper body repetition tests (e.g. bench pull) and ergometer times (see table III). Furthermore, a 6-minute bench pull repetition endurance test using a 41 kg load correlated poorly with on-water power during a simulated race (104.8 – 26.75 repetitions; r = 0.21; p > 0.05).[56] Unlike maximal strength assessments, the validity to rowing performance of upper body repetition endurance tests appears questionable. This is somewhat surprising given the logical validity of muscle endurance testing to endurance performance and warrants discussion. The number of repetitions completed using a set percentage of 1RM varies according to the quantity of muscle groups utilized as well as the training history and sex of the rower.[71-73] At an equal percentage of maximal ability, the number of repetitions attained with an upper body activity will be lower than that of a lower body activity. Ju¨rima¨e et al.[55] found that the number of repetitions performed in leg pressing at 50% 1RM was closer (repetitions = 173.5 – 11.8) to the number of average strokes taken to complete a 2000-m time trial (n = 194.2 – 19.5) than bench pulling (repetitions = 122.6 – 17.7) at 50% 1RM, thus explaining the significant and strong correlations ª 2011 Adis Data Information BV. All rights reserved.
found for leg pressing. Arguably, a lower percentage of 1RM was required for bench pulling; however, such a contention remains untested. It may be that repetition endurance tests, whether isokinetic or isoinertial, provide data better used to differentiate training experience and muscle morphology. That is, at a fixed percentage of 1RM, individuals with greater endurance training experience, proportions and hypertrophy of slow-twitch fibres perform a greater number of repetitions at sub-maximal loads.[66,71,74,75] Internationally, successful rowers have significantly greater proportions (e.g. 70–85%) and hypertrophy of slow-twitch fibres of the quadriceps muscle than lesser ranked national rowers (e.g. 66.1%)[2,37,49,53] and, subsequently, perform better in repetition endurance tests of the legs.[2,53] Whereas relatively similar variances in rowing performance may be shared with repetition endurance tests involving the legs, given a relatively smaller muscle mass and limited contribution to rowing power,[5,38] it would appear repetition endurance tests of the arms have little common variance with rowing performance. 7.3 Scaling of Strength and Endurance Data
To account for differences in body size (height and weight), it is common practice to normalize Sports Med 2011; 41 (5)
Rowing Strength Testing and Training
data by dividing the result by body mass (also known as ratio scaling) or by first raising body mass using a power exponent based on the theory of geometric symmetry (known as allometric scaling).[76-78] Ratio and allometric scaling of strength data reduces observed differences between males and females or between elite athletes participating in endurance sports. When allometric scaling was used to normalize ergometer 2000-m times, the resultant data provided a stronger model to predict on-water performance.[14] To our knowledge, neither ratio nor allometric scaling of strength data have been used to examine relationships with on-water performance. Given somatotype differences[30-32] and body mass constraints, allometric or ratio scaling of strength data might prospectively explain variances in on-water performances between heavyweight and lightweight, male and female, or novice and elite rowers. 7.4 Alternative Applications of Strength Testing
Apart from quantifying the physiological capacity of a rower, strength testing has also proved useful for the refinement of an optimal rowing technique. For example, past isometric strength testing established that the strongest rowing action was one where the elbows were kept at 180 during the leg driving phase, and where the arms were adducted and hands held at umbilicus height during the arm pulling phase of the rowing stroke.[79] Such strength tests may also prove useful as feedback to assist a rower to establish and refine their rowing technique. Strength tests may also provide data that is equally useful for evaluating musculo-skeletal conditions associated with pain or injury when rowing. For example, non-elite rowers with poor hamstring strength relative to the extensor muscles of the knee (e.g. ratio less than 45%) reported more frequent occurrences of low back pain affecting their participation in rowing.[28] Sub-elite rowers with a past rib-stress fracture occurrence were found to have lower knee extensor to elbow flexor strength ratios (i.e. 4.2 – 0.22 to 1) when matched to non-injured controls (i.e. 4.8 – 0.16 to 1; p < 0.05).[80] In addition, elite rowers were reª 2011 Adis Data Information BV. All rights reserved.
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ported to have greater strength and better symmetry (i.e. 1 : 1 ratios) between trunk flexor and extensors than weaker control non-rowers, more akin to the imbalances observed in low back pain populations.[81] The asymmetry of muscle development and strength associated with pain pathology, particularly of the legs and back observed in novice rowers, may be attributable to the asymmetrical rotation of trunk during the sweep-oar rowing technique.[82] For example, unilateral strength tests show that the oarside leg of nonelite lightweight oarsmen was significantly stronger (around 6%; p < 0.05) than the non-oarside leg;[59] however, such differences were not observed amongst more experienced sub-elite oarsmen.[82] It may therefore be that the interpretation of strength test data and the utilization of subsequent musculo-skeletal interventions differ between novice and elite rowers. 8. The Effects of Strength Training on Rowing Performance This review thus far has highlighted that muscle strength data significantly explains much of the variance in ergometer performance. Therefore, the efficacy of various strength training interventions on rowing performance warranted investigation. The purpose of this section is to examine whether strength training offers any benefits or performance edge over and above that attainable by rowing itself. Strength training improves muscle function by inducing neuromuscular adaptations (e.g. improved muscle recruitment, rate and synchronicity of fibre contractions) with long-term benefits ultimately attributable to (selective) hypertrophy of muscle fibres, vascular proliferation and expansion of energy substrates within the muscle.[83] In terms of increasing maximal strength, RM loading ranging from 1–12RM for up to three to four sessions a week, are thought optimal loading parameters for intermediate training (individuals with 6 months of consistent exercise history).[9] More frequent strength training may be required for experienced athletes (up to 6 days each week) where muscle-group training is divided over two sessions in order to limit the total duration of Sports Med 2011; 41 (5)
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exercise as training volumes approach up to eight sets for each muscle group.[84] The acute training objective is to progressively increase the intensity of the exercise (determined as a proportion of maximum ability), rather than increase the volume of repetitions to increase muscle fatigue.[85] Indeed, strategies to reduce fatigue significantly increase the rate of muscle work (i.e. power), thus, improve the quality of training and rate of muscular adaptation.[86,87] There is some contention about the efficacy and utility of various strength training modalities, particularly for advanced endurance athletes. Concurrent maximal strength and aerobic endurance training appears counterproductive to strength development.[88] It has been proposed that the acute fatigue of muscle fibres from endurance training compromises the intensity of the training required for strength development. It was also proposed that adaptations induced at the muscle level from endurance exercise are antagonistic to the hypertrophy response required to optimize strength (for reviews see Docherty and Sporer[89] and Leveritt et al.[90]). From this literature, it seems that the successful integration of strength training may be difficult for endurance athletes. However, short-term resistance strength training interventions (e.g. 5–10 weeks) with highly trained endurance cyclists and distance runners provided evidence that a performance edge was gained when units of strength training were scheduled in place of, and not in addition to, endurance exercise.[91,92] If it is decided that strength training is to be utilized in an athlete’s preparation, a rower’s first challenge is to decide how to successfully integrate and sequence endurance and strength training units. Irrespective of whether the objective is to build or maintain maximal strength, strength training should be scheduled after a rower has had opportunity to recover. Any preceding endurance exercise should consist of lowintensity continuous exercise, avoiding the use of the glycolytic energy system.[93] However, often time constraints mean this may not be practicable. Therefore, an alternative integration strategy is to sequence phases of physiological preparation (known as periodization) and to prioritize strength ª 2011 Adis Data Information BV. All rights reserved.
Lawton et al.
training during the non-competition phase.[94,95] A typical prioritized strength phase ranged between 9 and 10 weeks (refer table IV). On average, a little less than 5 hours of endurance exercise was scheduled, distributed over three to four sessions each week. Strength training was normally performed on alternate days to the endurance exercise, with between two and four sessions scheduled each week. Such periodized training sequences allowed non-elite and sub-elite rowers to achieve significant average weekly strength gains of around 2.5% a week.[19,22-25,27] At the end of the training phase, significant improvements in 2000-m ergometer performance times were also reported (table IV). However, as noted section 3, the reader needs to be aware of the limitations of research in this area. That is, it is inconclusive whether any performance edge was attributable to strength gains in examination of the standardized effect sizes due to the absence of any control groups or crossover research designs. Nonetheless, emphasizing strength training over an off-season would appear to be an effective strategy to promote strength development without loss of endurance or performance gains. After a period of prioritization over the offseason, a rower may have little time or sufficient energy to commit to further strength gains. General strength training might be ceased and replaced with specific on-water practices such as towing ropes to increases boat drag, thus providing resistance to promote muscle strength. To our knowledge, there is no evidence regarding the efficacy of such strategies. What is apparent from the literature is that intensive on-water training is unlikely to achieve the mechanical, metabolic and hormonal stimuli required to maintain maximal strength. For example, the isokinetic leg strength of elite oarsmen declined 12–16% by the end of a competition period once strength training was ceased.[48] In contrast, at sufficient intensity (i.e. 73.0–79.3% of predicted 1RM), oarswomen were able to maintain maximal strength over a 6-week competition period whether one or two resistance sessions were performed each week.[18] Therefore, some element of off-water strength training to maintain maximal strength appears warranted all year round. Sports Med 2011; 41 (5)
Rower’s level; sex (n); age; height; weighta,b
Phase and strength training intervention
Strength tests and rowing performance assessmentc
Main findings
Bell et al.[18]
Non-elite; F (20); 20.4 – 1.5 y; 170.7 – 9 cm; 64.9 – 8.8 kg
Non-competitive: 10 wk concurrent strength (~4–5 sets · ~6 reps at 64–81% 1RM, 3 d) and ergometer endurance training (<2 h/wk). Then, for 6 wk, group 1 performed one strength session each wk (~3–4 · ~6 reps at 73–79% 1RM) while group 2 performed two strength sessions each wk as endurance training steadily increased (<4 h/wk, 4 d). Descriptive study, no control group for strength intervention
Pre- and post-tests used to calculate total load (i.e. weight · reps) based on 6–11RM for all strength exercises prescribed (e.g. inclined leg press.d Change in 7-min row power (Gjessing Ergorow, Oslo Norway). Average power: 176.7 – 26.6 W
After 10 wk, strength increased for all exercises (p < 0.05, ES not calculated) as did average power for 7-min rowing ergometer test (ES = 0.51, p < 0.05). Inclined leg press strength results were maintained for a further 6-wk phase whether one or two sessions a week at sufficient intensity (e.g. 73–79% 1RM) were performed (ES not calculated)
duManoir et al.[19]
Non-elite; M (10); 31.2 – 12.1 y; 184.4 – 4 cm; 79.2 – 9.0 kg
Non-competitive: 10 wk concurrent strength (2–6 sets · 4–10 reps, 3 d) and endurance training (<4 h/wk, 3 d). Descriptive study, no control group for strength intervention
Pre- and post-strength tests: 1RM 45 leg press (90 knee flexion): 339.2 – 44.4 kg. Change 2000-m (C2) time: 436.1 – 18.2 sec
Significant improvements (p < 0.05) in 1RM leg press (2.83% per wk, ES = 1.14) and 2000-m time (20.7-sec faster, ES = 0.67)
Ebben et al.[20]
Non-elite and sub-elite; F (26); 20.0 – 1.0 y; 170.0 – 6 cm; 71.0 – 7.0 kg
Non-competitive: 8 wk concurrent high-load (3 · 12–5RM) or high-rep (2 · 15–32RM) strength (3 d) and endurance training.d Descriptive study, no control group for strength intervention
No strength tests: average total volume (i.e. kg · reps) calculated for all strength exercises prescribed. Change 2000-m (C2) time: non-elite: 509 – 26 sec; sub-elite: 476 – 19 sece
Average total volume for strength cycle was 105 003 kg for high rep and 84 744 kg for high load. Both high-load and high-rep groups improved 2000-m time regardless of strength protocol (p < 0.001; ES = 0.36–0.35 and 0.60–0.20, respectively). Greater positive effects noted for high-rep training for non-elite and high load for sub-elite (ES not stated)
Gallagher et al.[21]
Non-elite; M (18); 20.2 – 0.87 y; 188.0 – 8 cm; 82.4 – 33.3 kg
Non-competitive: 8 wk concurrent strength (2 d) and endurance training (<2 h, 2 d), as well as regular on-water training.d Intervention design for high-rep (2–3 sets · 15–30RM) or high-load (3–5 sets · 1–5RM) strength training with control group (no strength training, but 2 h less training each week)
No strength tests: change in total volume (i.e. kg · reps) calculated for all strength exercises prescribed. Change 2000-m (C2) time: control 418.3 – 5.4 high rep 386.2 – 4.4 high load 403.3 – 4.7
High rep increased total volume by 9.44% and high load by 2.02%. All 2000-m times improved, however, no differences between control, high rep and high load (p < 0.96, ES = 3.28, 2.48 and 2.22 respectively). However, practical significance of improvements between high load (3.5% or 15 sec), high rep (3.1% or 12 sec) and control (2.8% or 11 sec) argued to equal one boat-length over 2000 m Continued next page
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ª 2011 Adis Data Information BV. All rights reserved.
Table IV. Intervention studies involving strength testing, training and rowing performance
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Table IV. Contd Rower’s level; sex (n); age; height; weighta,b
Phase and strength training intervention
Strength tests and rowing performance assessmentc
Main findings
Haykowsky et al.[22]
Non-elite rowers (n = 25); M (8); 23.0 – 6.1 y; 1.83 – 8 cm; 78.1 – 12.5 kg F (17); 22.7 – 5.0 y; 170.6 – 8 cm; 65.8 – 9.8 kg
Non-competitive: 10 wk concurrent strength (3–6 sets · 2–6 reps, 2 d) and endurance (<5 h/wk, 4 d) training. Descriptive study, no control group for strength intervention
Pre- and post-strength tests: average group 1RM 45 leg press (90 knee flexion): 306.0 – 58.0 kg. Average group change 2500-m (C2) time: 577.0 – 34.7 sec
Significant (p < 0.05) improvement in 1RM leg press (2.76% per wk, ES = 1.50) and 2500-m time (20.3-sec faster, ES = 0.50)
Kennedy et al.[23]
Non-elite rowers (n = 38) M (19); 25.1 – 4.8 y; 179.8 – 7cm; 79.3 – 8.2 kg F (19); 25.2 – 4.6 y; 169.2 – 6 cm; 68.0 – 11.5 kg
Non-competitive: 10 wk concurrent strength (2–6 sets · 4–12 reps, 2 d) and endurance (<4 h/wk, 4 d) training. Descriptive study, no control group for strength intervention
Pre- and post-strength tests: estimated 1RM 45 leg press (90 knee flexion): M 347.8 – 57.9 kg, F 186.5 – 50.5 kg. Change 2000-m (C2) time: M 426.3 – 20.0 sec, F 495.9 – 29.7 sec
Significant improvement (p < 0.05) in estimated 1RM (M 1.60% per wk, ES = 1.11 and F 2.28% per wk, ES = 0.61) and 2000-m time (M 31.8-sec faster, ES = 1.04, and F 43.5-sec faster, ES = 1.03)
Kramer et al.[24]
Sub-elite and non-elite; F (24); 19.3 – 1.0 y; 180 – 10 cm; 75.0 – 6.0 kg
Non-competitive: 9 wk concurrent endurance (<4 h/wk, 4 d) and strength (3–5 sets · 4–12 reps, 3 d) or strength with plyometric training (i.e. plus 80–310 jumps). Intervention design for plyometric training with control group
Pre- and post-strength tests: 1RM 45 leg press (100 knee flexion): control 164.2 – 24.9 kg, plyometric 162.4 – 36.1 kg. Change 2500-m (C2) time: control 606 – 48 sec, plyometric 614 – 61 sec
Both control and plyometric groups improved strength (p < 0.01; 1.61% per wk, ES = 0.57 and 1.66% per wk, ES = 0.90, respectively) and 2500-m time (p < 0.05; 19-sec faster, ES = 0.40 and 22-sec faster, ES = 0.33, respectively) but no differences in change due to plyometric training (p > 0.05)
Syrotuik et al.[25]
Non-elite rowers (n = 22); M (12), F (10); 23.0 y; 176.3 m; 76.8 kgf
Non-competitive: 9 wk concurrent strength (3–4 sets · 10RM, 2 d) and endurance training (31–37 km/wk, dispersed over 4 d). Intervention design for creatine monohydrate supplementation with control group. No control for descriptive strength intervention
Pre- and post-strength tests: estimated 1RM 45 leg press (90 knee flexion), creatine 337.7 – 96.4 kg. Control 300.9 – 100 kg. Change 2000-m (C2) time: creatine 458.2 – 42.4 sec, control 461.4 – 38.2 sec
Both creatine and control groups improved (p < 0.05) estimated 1RM strength (3.37% per wk, ES = 1.23 and 2.04% per wk, ES = 0.59) and 2000-m time (18.2-sec faster, ES = 0.39 and 15.3-sec faster, ES = 0.33, respectively). Creatine no beneficial effect on either test measures (p > 0.05)
Tse et al.[26]
Non-elite; M (34); 20.1 – 1.0 y; 175 – 6 cm; 67.3 – 5.8 kg
Competitive: Concurrent strength (2 sets · 12–15 reps, 2 d) and endurance training.d Intervention design for abdominal core training (n = 14) of 30–40 min of muscle transverse abdominus activation endurance (2 d), with control group (n = 20)
Pre- and post-strength tests: isometric abdominal endurance test (60 flexion): control 215.5 – 62.7 sec, core 176.2 – 48.9 sec. Change in 2000-m (C2) time: control 442.1 – 9.5 sec, core 452.4 – 9.8 sec
After 8 wk, no improvement (p > 0.05) in isometric abdominal endurance test for either control or core training groups (ES = 0.09 and 0.16, respectively) nor 2000-m time (1.4-sec faster, ES = 0.13 and 2.1-sec faster, ES = 0.18, respectively). Programme too short, tests too unrefined and improvements in incident rate of low back pain overlooked Continued next page
Lawton et al.
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Significant difference (p = 0.002). e
C2 = Concept2 rowing ergometer; ES = effect size (pre-, post-test data/SD pre-test data); F = female; M = male; max. = maximum; RM = repetition maximum; rep(s) = repetition(s).
Load not stated. d
Mean – SD unless otherwise stated. b
c All data is post-testing.
Sample only (refer to original paper for further details). a
Non-elite rowers (n = 31) M (12); 21.3 – 2.7 y; 184.3 – 6.6 cm; 81.5 – 7.8 kg F (19); 22.8 – 5.8 y; 173.4 – 7.2 cm; 70.9 – 9.7 kg Webster et al.[27]
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f Data for the Syrotuik et al.[25] study are presented in mean values.
Pre- and post-strength tests: 1RM 45 leg press (90 knee flexion): M 274.3 – 80.7 kg, F 172.8 – 49.0 kg. Change 2000-m (C2) time: M 444.8 – 29.7 sec, F 501.3 – 32.0 sec
All rowers significantly (p < 0.05) increased strength (1.8% per wk, ES = 0.55) and 2000-m time (22-sec faster, ES = 0.65). Duration (i.e. time) and not sex positively affect performance
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Non-competitive: 8 wk concurrent strength (2–6 sets · 4–12 reps, 2 d) and endurance (<4 h/wk, 4 d) training. Descriptive study, no control group for strength intervention
Rower’s level; sex (n); age; height; weighta,b Study
Table IV. Contd
Phase and strength training intervention
Strength tests and rowing performance assessmentc
Main findings
Rowing Strength Testing and Training
An alternative periodization model was to shift the off-season emphasis from maximal strength to local muscle endurance adaptation as a competition phase approaches. Lighter loads (i.e. 40–60% 1RM) coupled with higher repetitions (i.e. ‡15) lead to greater local endurance adaptation, without significant muscle hypertrophy.[83] Such adaptations may be preferable for lightweight rowers who need to be cautious of excessive body mass. Local muscle endurance training provides a suitable complement or substitute for endurance rowing, particularly for unskilled novice or injured rowers as very high repetition bench pull and leg press exercise at low intensities (e.g. 50–125 repetitions using a 40% of 1RM load) developed blood lactate levels ranging between 6.9 – 2.2 mmol/L and up to 11.2–11.8 – 2.5–2.3 mmol/L, respectively,[55,69,70] with mean and peak heart-rate responses (r = 0.71–0.77; p < 0.05), and perceived exertion (r = 0.76; p < 0.05) of leg pressing comparable to 2000-m ergometer rowing.[55] After 10 weeks, concurrent strength training and endurance exercise increased left ventricle diastole (10.6%), wall thickness (11.3%) and mass (17.5%), which was contended to be a unique and plausibly favourable anatomical adaption of the heart rate amongst rowing populations.[19,22] The effects of maximal strength and local muscle endurance exercise on 2000-m ergometer performance has been compared using novice and sub-elite rowers over 8 weeks of non-competition phase training.[20,21] Maximal strength training has consisted of 12RM loads, which were progressively increased to heavier 5RM loads,[20] or 5RM loads, which were progressively increased to sets varying in load between 1RM and 5RM.[21] In contrast, strength endurance training utilized loads ranging between 15RM and 32RM. Ebben et al.[20] concluded that rowers with more training experience achieved a greater benefit from maximal strength training, while novice rowers benefited more from strength endurance training; however, the lack of control group or crossover research designs again makes the interpretation of effect sizes and application of findings problematic (see tables I and IV). Gallagher et al.[21] found that no significant short-term performance improvements were gained from the inclusion of either low- or Sports Med 2011; 41 (5)
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high-load strength training, nor were any detrimental outcomes observed when compared with endurance only controls. However, a lack of statistical power (low subject numbers), imprecise assessment of changes in strength and strength endurance, and unequal training volumes between control and intervention groups (extra 2 hours exercise per week) again make the interpretation of effect sizes difficult (see tables I and IV). Although not statistically significant, the practical significance of the short-term differences in performance improvements between groups (i.e. high load 3.5% or 15 seconds faster; low load 3.1% or 12 seconds faster and control 2.8% or 11 seconds faster) were noteworthy and equivalent to almost a boat length over a 2000-m race. Nonetheless, longer-term interventions are required to clarify any beneficial prescription of strength training methods and performance outcomes between novice and elite rowers. To date, strength training research has primarily focused on the effect of maximal strength training on rowing performance. However, explosive power exercise may be more relevant over the competition phase when peak physical fitness performance needs are tuned to the specifics of racing. Compared with off-season maximal strength training, lighter isoinertial loads used for local muscle endurance exercise (40–60% of 1RM) enables the attainment of a faster movement velocity during exercise. While isokinetic strength training gains are specific to the velocity with which training is performed,[96] moderate and fast velocities with isoinertial loads enhance both strength and motor performance gains more effectively.[9] Significant performance benefits from the integration of short-term explosive low-fatigue strength exercise have been reported for highly trained endurance cyclists (e.g. 8.7% increase in 1 km power and 8.1% increase in 4 km power[97] and 7.1% increase in average power over a 1-hour time-trial performance[98]) and middle-distance runners (e.g. improved running economy ranging from 4.1–8.1%[92]). Izquierdo-Gabarren et al.[86] also found that by reducing the volume of strength exercise (i.e. five repetitions at 75% 1RM) to eliminate fatigue and sustain greater movement velocity, greater strength and power gains were realized than ª 2011 Adis Data Information BV. All rights reserved.
Lawton et al.
when repetition failure occurred (i.e. ten repetitions at 75% 1RM). Furthermore, significantly greater improvements in average power over ten strokes (3.6–5.0% gain) and 20 minutes (7.6–9.0% gain) were achieved during fixed-seat ergometer rowing (Concept 2, model D; Morrisville, VT, USA) for the non-fatigue exercise group compared with traditional strength training and control groups. There is a paucity of research, however, that has examined the effects of explosive power training on rowing performance. Neither sub-elite nor novice rowers achieved any additional performance advantage over traditional strength training after 9 weeks of lower body plyometric training was incorporated into the training programme.[24] Again, the findings of this research are problematic as total training volumes were not equivalent between groups and overtraining may have negated any ergometer performance benefits attributable to the addition of explosive leg exercise. 8.1 Strength Training and Rowing Injuries
As mentioned previously in section 7.4, strength testing may provide a means to assess musculoskeletal conditions commonly associated with rowing. Most injuries associated with rowing appear to be related to chronic overuse syndromes affecting soft tissues of the lower back, shoulders, knees and wrists.[2] However, a less than desirable rowing technique, such as increased posterior tilt during the leg drive action or excessive flexion and rotation of the thoracic spine at the catch,[99] may lead to imbalances in muscle development and an associated increase in pain or injury. While acknowledging limitations with past research, strength training has been used to correct muscle imbalances, which, in specific cases, appeared useful in the reduction of pain associated with rowing. For example, the number of training days lost due to low back pain was reduced once the relatively excessive quadriceps strength (i.e. a knee flexion to extension ratio less than 45%) was addressed by a specific hamstring strengthening programme over 6–8 months.[28] In addition, 8 weeks of specific strengthening of the deep abdominal and low back stabilizers of the Sports Med 2011; 41 (5)
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pelvis and spine, while having no effect on rowing performance, purportedly reduced the incidence of painful rowing for those rowers with a history of low back pain.[26] However, it was unclear whether changes in muscle imbalances led to a subsequent improvement in rowing technique, or whether similar outcomes could have been achieved by allocating an equivalent time to practice of a revised rowing technique. 9. Future Research On the basis of the evidence reviewed, the clinical relevance and practical significance of positive benefits associated with various strength training modalities cannot be ignored. Importantly, no negative performance outcomes were attributed to the inclusion of various strength-training protocols. However, while the integration of strength training appeared relatively simple, there was an absence of research that clarified the type of overload stimulus required for each distinct phase of preparation of the competition year (i.e. noncompetition or competition phase) that was of relevance to various divisions (light or heavyweight) and experience levels (novice or elite). Additionally, few definitive recommendations could be made with respect to essential programme variables of strength programme design. For example, it was unclear what rowing performance advantages were gained when three or more strength sessions a week were integrated over a training phase, whether changes in 2000-m times were attributable to lower or upper body strength development, or in emphasizing one over the other, or whether any particular exercises such as the lateral pulldown, shoulder press or dead-lifts were potentially more beneficial than others. What was apparent was that year-round monitoring, as part of longer-term investigations, rather than intermittent episodic interventions of <10 weeks, was required to better understand performance benefits attributable to various strength-training protocols. Of note, such benefits should be examined in the context of models that incorporate on-water performance data (e.g. 2000-m times or rank of rower) if limitations to the reliability and precision of such data can be overcome. ª 2011 Adis Data Information BV. All rights reserved.
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10. Conclusions While strength explained much of the variances in 2000-m ergometer performance and muscle balance assessments derived from strength data appeared useful in the pathological assessment of low back pain or rib injury history associated with competitive rowing, the clinical and practical significance of positive benefits associated with strength training lacked statistical significance, primarily due to an absence of quality long-term controlled experimental research designs. Acknowledgements This review was made possible due to funds awarded through a Prime Minister’s Scholarship 2010 (a New Zealand Government grant). The authors have no conflicts of interest that are directly relevant to the content of this review.
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Correspondence: Mr Trent Lawton, SPRINZ – AUT University, Private Bag 92006, Auckland 1142, New Zealand. E-mail:
[email protected]
Sports Med 2011; 41 (5)
