Sports Med 2011; 41 (7): 523-539 0112-1642/11/0007-0523/$49.95/0
REVIEW ARTICLE
ª 2011 Adis Data Information BV. All rights reserved.
Influence of Exercise on Skill Proficiency in Soccer Mark Russell1 and Michael Kingsley1,2 1 Sport & Exercise Science, Swansea University, Singleton Park, Swansea, UK 2 Centre for Physical Activity Studies, Institute of Health and Social Science Research, CQUniversity, Rockhampton, Queensland, Australia
Contents Abstract. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Technical Demands of Soccer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Methods Currently Employed in the Evaluation of Technical Performances in Soccer . . . . . . . . . . . . 3.1 Tests that Measure Ball Control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2 Tests that Measure Ball Accuracy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3 Additional Issues Concerning the Use of Isolated Skills Tests . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. Simulating Soccer-Specific Exercise. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5. The Effects of Exercise on Soccer Skills. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.1 Dribbling Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2 Passing Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.3 Shooting Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6. Factors Affecting Technical Skills Executed during Exercise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.1 Aerobic Fitness . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.2 Hydration Status. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.3 Blood Glucose Concentrations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7. Conclusions and Future Research Recommendations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Abstract
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The ability to maintain technical performances (i.e. skills) throughout soccer match-play is considered to be crucial in determining the outcome of competitive fixtures. Consequently, coaches dedicate a large proportion of time to practicing isolated skills, such as passing, shooting and dribbling. Unlike other elements that contribute to team-sport performances, it is unusual for coaches to use methods other than observations to assess changes resulting from technical training. Researchers have employed various tests to measure isolated soccer skills; however, reliance on outcome measures that include number of contacts (ball juggling tasks), time (dribbling tasks) and points scored (criterion-based passing and shooting tests) means that the outcomes are difficult for coaches to interpret. Skill tests that use videoanalysis techniques to measure ball speed, precision and success of soccer skills offer valid and reliable alternatives. Although equivocal results are published, skill performances can be affected by assorted factors that threaten homeostasis, including match-related fatigue, dehydration and reductions in blood glucose concentrations. While acknowledging methodological
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constraints associated with using skill tests with limited ecological validity and cognitive demands, the effects of these homeostatic disturbances might vary according to the type of skill being performed. Shooting performances appear most susceptible to deterioration after exercise. Strategies such as aerobic training, fluid-electrolyte provision and acute carbohydrate supplementation have been found to improve proficiency in technical actions performed after soccer-specific exercise. However, mechanisms that cause deterioration in skill during soccer-specific exercise remain to be fully elucidated and strategies to optimize technical performance throughout match-play are warranted.
1. Introduction Performance during soccer match-play is dependent on a range of factors that include technical, tactical, mental, physical and physiological factors.[1] The quality of technical response (skill performance) is dependent on cognitive, perceptual and motor skills, which interact in rapidly changing environments.[2] Skilled performers receive information (e.g. movement of ball and targets), rapidly analyse information and execute appropriate responses with maximum certainty and minimum outlay of time and energy.[2] In comparison with the physiology of intermittent exercise, technical responses (i.e. the performance of skills, such as passing, shooting and dribbling) to the physical demands of team sports are not well understood. This is somewhat surprising considering that the proficiency of skilled performance is often responsible for determining the outcome of competitive fixtures in sports such as soccer, rugby (league and union), field hockey and basketball. A possible reason for the scarcity of literature regarding the influence of exercise on sports skills is the lack of exercise simulations that replicate, in a controlled and repeatable manner, the movement and technical demands of team sports. This review summarizes current research that evaluates technical response to exercise, using soccer as the main area of interest. Computerized literature searches were performed in PubMed, Google Scholar and SportDiscus databases between November 2009 and November 2010. The following keywords were used in different combinations: ‘soccer’, ‘football’, ‘skill’, ‘technical’, ‘passing’, ‘shooting’, ‘dribbling’ and ‘juggling’. ª 2011 Adis Data Information BV. All rights reserved.
Articles evaluating technical proficiency in ‘rugby’ were excluded. All titles were scanned and relevant articles were retrieved for review. In addition, the reference lists from both original and review articles retrieved were also reviewed. This review will (i) describe the frequency of soccer skills during match-play; (ii) discuss the methods used to simulate and evaluate the demands of match-play, with a particular focus on the measurement of soccer skills; (iii) discuss the influence of exercise on skills; and (iv) examine the factors that affect technical responses to exercise. 2. Technical Demands of Soccer Soccer is primarily aerobic in nature, where players have been observed to cover approximately 10 km during matches.[3-8] Nevertheless, success during soccer match-play is associated with increased high-intensity activity[9] and the quality of skilled actions, such as passing and shooting.[10] Considering that a disproportionate number of goals are scored in the last 15 minutes of a match,[11] the ability to maintain technical proficiency while engaged in prolonged highintensity intermittent exercise is a primary determinant of success in competitive fixtures. Although the main focus of notational analysis has been the quantification and classification of physical activities, this methodology has also revealed vital information about the frequency of occurrence of sports-specific motor skills.[12,13] Throughout a soccer match, each player completes between 50 and 110 technical involvements;[13-15] however, fullbacks have been reported to have a higher frequency of technical involvement than Sports Med 2011; 41 (7)
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all other positions.[13] In order to score a goal, a team must make between 16–30 attacks and take an average of ten shots,[16] whereas analysis of individual actions has revealed that dribbling and short passes are the most frequently performed skills during match-play.[15,17] Despite the number of skilled actions that occur throughout match-play being a consequence of aerobic fitness, positional role and the team’s league position,[13,18] relatively little information is available to evaluate the possible time-course of decay in the frequency and/or success of technical performances executed during match-play. Although half to half variations in the frequency of skilled performances have previously been reported,[18] no study has aimed to determine whether technical proficiency varies over smaller time intervals (e.g. every 15 minutes). This is surprising considering that it has been reported that lapses in concentration could partially explain the disproportionate number of goals scored in the latter stages of matchplay relative to all other times during a game.[11] Based on the technical demands of soccer, and the importance of skilled actions in defining success, it is not surprising that soccer players allocate a large proportion of their training time to improving skilled actions. Unlike other predictors of soccer success, such as a maximal aerobic capacity in excess of 60 mL/kg/min,[19] coaches do not regularly monitor the efficacy of training on technical performances using means other than empirical observations. Nevertheless, the growing interest in soccer skill among researchers has led to the development of various methods to evaluate the quality of skilled performances; however, soccer teams are yet to regularly incorporate such protocols in their testing batteries. 3. Methods Currently Employed in the Evaluation of Technical Performances in Soccer Global measures of soccer skills (such as match results) have strong ecological validity,1 but in-
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corporate too much variability to consistently identify changes associated with interventional research. For example, using the number of goals scored and conceded as outcome measures, Zeederberg et al.[22] concluded that carbohydrate supplementation did not improve motor skill performance during soccer match-play. In addition to challenging the appropriateness of this global outcome measure, similarities in the plasma glucose concentrations between the carbohydrate and placebo trials suggest that the supplementation strategy was not optimal. To overcome external factors that affect the repeatability of match-play (e.g. opponents activity profiles and success experienced throughout the season),[7,18] a number of tests have been devised that isolate the performance of soccer skills (table I).[23-33,35] These protocols can be categorized into tests that assess ball control and tests that measure ball accuracy. 3.1 Tests that Measure Ball Control
The ability of a player to control the ball during a soccer match, either when receiving a pass from a team mate or while running into an opponent’s territory, is an important skill; consequently, a number of authors have designed tests that aim to assess this facet of soccer skill performance.[23-25,29,30,32,33] A method that has been used to assess ball control is ball juggling, whereby the frequency of consecutive and successful (i.e. preventing the ball from touching the ground) ball touches are counted, and higher values are deemed to represent a greater level of skill. Figueiredo et al.[33] reported that performance on a reliable ball juggling task (coefficient of reliability: 0.77) was influenced by the sexual maturity of Portuguese junior soccer players as 13- to 14-year-olds outperformed their 11- to 12-year-old counterparts (69.5 vs 25.2 touches). However, although ball juggling is commonly observed on the training ground, empirical observations of competitive match-play seldom reveal ball juggling to be a frequently
1 Ecological validity can be defined as the degree to which congruence exists between the environment that the subject in an investigation experiences and the intended properties of the environment that the investigator assumes[20] or the extent to which research emulates the real world.[21]
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ª 2011 Adis Data Information BV. All rights reserved.
Table I. Summary of soccer skill tests that isolate specific technical actions Study (year)
Skill
Measurement
Assessment method
Outcome measures
Zelenka et al.[23] (1967)
Shooting
Accuracy
Criterion-based measure
Points scored
Dribbling
Ball control
Timing
Time
Reilly and Holmes[24] (1983)
McGregor et al.[25] (1999) Northcott et al.[26] (1999)
Ball juggling
Ball control
Frequency of successful touches
Number of touches
Dribbling
Ball control
Timing
Time
Wall volley
Ball control
Frequency of successful touches
Number of continuous touches
Shooting
Accuracy
Criterion-based measure
Points scored
Dribbling
Ball control
Timing
Time
Passing
Accuracy
Criterion-based measure
Points scored
Shooting
Accuracy
Criterion-based measure
Points scored
Cox et al.[27] (2002)
Shooting
Accuracy
Criterion-based measure
Points scored
Finnoff et al.[28] (2002)
Passing
Accuracy
Manual distance measurement
Distance
Ali et al.[29] (2007a)
Mirkov et al.[30] (2008)
Rostgaard et al.[31] (2008) Currell et al.[32] (2009)
Figueiredo et al.[33] (2010)
Russell et al.[35] (2010)
Accuracy and ball control
Criterion-based measure and timing
Time
Speed, accuracy, ball control
Radar speed gun, criterion-based measure, timing
Speed and points scored
Throw-in
Maximal upper body power
Manual distance measurement
Maximal distance
Kicking
Maximal lower body power
Manual distance measurement
Maximal distance
Dribbling
Ball control
Timing
Time
Passing
Accuracy
Criterion-based measure
Points scored Time
Dribbling
Ball control
Timing
Kicking
Accuracy
Criterion-based measure
Points scored
Heading
Maximal height
Height measurement
Maximal height
Ball juggling
Ball control
Frequency of successful touches
Number of continuous touches
Dribbling
Ball control
Timing
Time
Passing
Accuracy and ball control
Criterion-based measure
Points scored
Shooting
Accuracy
Criterion-based measure
Points scored
Shooting
Accuracy
Criterion-based measure
Points scored
Passing
Speed, accuracy, ball control
Video digitization
Ball speed, precision, success rate
Shooting
Speed, accuracy, ball control
Video digitization
Ball speed, precision, success rate
Dribbling
Speed, accuracy, ball control
Video digitization
Ball speed, precision, success rate
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Williams et al.[34] (2010)
Passing Shooting
Exercise and Soccer Skill
occurring skill. Therefore, as a marker of technical proficiency, the ecological validity of ball juggling is questionable compared with more match-specific actions such as dribbling. A 20 m timed sprint dribble identified that fluid abstinence caused a 5% reduction in dribbling performance when compared with a trial where fluid was provided.[25] Subsequent studies have incorporated similar tests;[36] however, the outcome measure from timed dribbling tasks is speed, with no measure of the quality of the skill (e.g. precision or success). Although some people would argue that a shorter time to complete such tests represents a more skilled action, this is not necessarily the case. For example, a skilled dribbler is able to keep the ball close to the desired position while travelling at high speed and a lack of ball control will increase the likelihood of losing possession of the ball. Consequently, the ability to quantify the actual ball position in relation to the desired position (precision) and the ability to complete the desired task without mistakes (success rate) are additional outcome measures that provide further information about the proficiency of this technical action. Recently, we have confirmed the validity and reliability of soccer skill tests that use video-analysis techniques to produce outcome measures of ball speed, precision and success rate for soccer dribbling, passing and shooting skills.[35] These tests require players to kick a moving ball to one of four randomly identified targets (passing and shooting) and to manoeuvre a ball as fast and as accurately as possible between cones (dribbling). In addition to providing outcomes with better absolute and relative reliability than comparable traditional criterionbased methods, these tests provide outcome measures with strong ecological validity that are easily interpreted by coaches, players and researchers. Therefore, authors of future research may wish to explore the use of such analysis methods when examining the technical response to exercise. 3.2 Tests that Measure Ball Accuracy
The precision of skill performances influences the winning and losing of possession during soccer match-play; therefore, it is not surprising that ª 2011 Adis Data Information BV. All rights reserved.
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the majority of soccer skill tests incorporate a measure of accuracy (table I). However, most skill tests in soccer research are those that produce accuracy outcomes from criterion-based measurements, whereby discrete (i.e. outcomes can only take certain values) as opposed to continuous (i.e. outcomes can take any value) data are produced. Consequently, conclusions drawn from the use of such tests are heavily influenced by the values assigned in the scoring criteria and may not necessarily reflect the relative difficulty of the tasks performed. For example, the Loughborough Soccer Shooting Test (LSST) allocated the greatest number of points to shots placed in the corners of a goal as this limits the chance of the goalkeeper saving the shot.[29] However, a similar shooting task devised by Currell et al.[32] assigned the lowest number of points when shots were placed towards the corners. Consequently, conclusions derived from tests that rely on criterion-based outcomes are heavily dependent on the scoring criteria used and limit the like-for-like comparison of data between different tests that aim to assess the same variables of skilled performance. The Loughborough Soccer Passing Test (LSPT), described by Ali et al.,[29] requires participants to aim passes towards coloured targets while negotiating a coned area. Performance is determined by the time taken to complete the task plus any additional penalty points accumulated. Although the LSPT has been used to examine the influence of a number of interventions on soccer passing performance in both male[37-39] and female players,[40] the outcome measure lacks ecological validity as the outcome of the test, which is designed to measure kicking accuracy and is expressed in time(s) rather than distance. Compared with outcomes derived from criterionbased soccer skill tests, relatively few authors have published data concerning the accuracy of skills involving kicking. Finnoff et al.[28] reported a median deviation of approximately 90 cm over a 6.1 m distance when ball impacts were measured manually, whereas Young et al.[41] implemented video-analysis procedures to yield deviations of 80–90 cm when Australian football players kicked a ball towards a target that was 16 m away. Sports Med 2011; 41 (7)
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The omission of match-specific cognitive processes (such as decision making and visual searching), where a ball is kicked towards a target in a pre-planned manner, and differences in the motor skills between football codes limit the application of these earlier studies to soccer research. However, video-analysis techniques have recently been used to quantify ball speed, precision and success rates in soccer skill tests that incorporate match-specific cognitive processes.[35] These methods demonstrated construct validity, where shooting and passing accuracy of youth players from a UK-based championship soccer team were superior to university-standard players. Therefore, alternative methods exist to the criterion-based outcome measures that have previously dominated soccer skill research.
Table II. Factors to consider when designing isolated skill tests Skill Clearance
Testing considerations Standardization of ball delivery Player movement at the start and throughout the test Outside interference when clearing the ball Position of ball clearance
Corner
Type of corner (e.g. cross, short) Speed, accuracy and success of outcome
Cross
Standardization of ball delivery Player movement at the start and throughout the test Outside interference when crossing the ball Speed, accuracy and success of outcome
Dribble
Standardization of ball delivery Player movement at the start and throughout the test Path covered (e.g. distance, directional, turns) Cessation of test (skill at the complete task, e.g. pass) Speed, accuracy and success of outcome
3.3 Additional Issues Concerning the Use of Isolated Skills Tests
While attempting to maintain experimental control through standardized test protocols, some researchers have designed skill tests that require the kicking of a static ball.[26] At the time of their development, these tests provided novel findings to support the use of selected ergogenic aids when aiming to maintain skilled performances; however, such tests focus on technique rather than skill because the use of a stationary ball fails to include cognitive aspects of matchplay (e.g. decision-making and visual searching processes).[2,29] The array of technical movements involved in match-play further complicates the practice of testing soccer skills in isolation; consequently, consideration should be given to various factors that influence isolated skill tests (table II). In addition, a range of environmental factors (e.g. location, wind and playing surface) should also be considered. Since the quality of a skill is dependent on the interaction between speed and accuracy of execution,[42] and given that success is a valuable outcome, information concerning these subcomponents of skilled actions could provide independent outcome measures that are of relevance to players, coaches and sports scientists. Criterion-based tests determine accuracy in terms of ª 2011 Adis Data Information BV. All rights reserved.
Free kick
Type of free kick (e.g. pass, shot, cross, position) Outside interference when taking the kick (e.g. defensive wall) Speed, accuracy and success of outcome
Header
Standardization of ball delivery Player movement at the start and throughout the test Outside interference when heading Type of header (e.g. towards opponents goal or team mate) Speed, accuracy and success of outcome
Pass
Standardization of ball delivery Player movement at the start and throughout the test Type of pass (e.g. foot, chest, head, long, short) Outside interference when passing Speed, accuracy and success of outcome
Penalty
Speed, accuracy and success of outcome
Shot
Standardization of ball delivery Player movement at the start and throughout the test Outside interference when shooting Type of shot (e.g. long or short range, power or placement) Speed, accuracy and success of outcome
Tackle
Standardization of ball delivery Player movement at the start and throughout the test Success of outcome
Throw-in
Type of throw (e.g. long, short, position of target) Ball trajectory on release Speed, accuracy and success of outcome
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total points scored and rarely determine speed; however, video-analysis techniques have been demonstrated to provide these outcome measures a soccer skill test battery with confirmed validity and reliability.[35] Therefore, future research in this field should employ analysis methods that quantify skilled performances in terms of continuous data (as opposed to discrete data) and provide outcome measures in ecologically valid units. 4. Simulating Soccer-Specific Exercise As a sport with worldwide participation and the most popular of the football codes,[43] the commercial value of findings from soccer research are potentially high; consequently, several exercise protocols have been developed that aim to replicate the demands of competition.[34,44-48] The primary reason for developing an exercise simulation is to control the movement requirements and thereby standardize the physiological demands. In doing so, the variation in responses that usually exist between matches is limited and the effects of exercise become repeatable. The most obvious benefit of simulation protocols is that they minimize external variation and allow for more prominent effects to be identified in sometimes subtle physiological changes that result from supplementation protocols, strength and conditioning regimes and/or other performancealtering interventions. Studies aiming to assess the validity of exercise protocols, which were designed to replicate the demands of soccer match-play, have generally compared simulation data with the results of notational analysis studies collected during match-play in a different subject pool. According to Drust et al.,[49] if an exercise simulation is to be validated against the demands of match-play, then a single group of participants would be required to undergo both experimental conditions (i.e. match-play and the simulation) and their responses subject to statistical analysis. However, few researchers have adopted this approach when assessing the validity of an exercise simulation. Thatcher and Batterham[48] demonstrated the comparability of physiological responses between ª 2011 Adis Data Information BV. All rights reserved.
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individuals participating in actual match-play and a non-motorized treadmill protocol. However, the lack of lateral and backwards movements performed in unidirectional treadmill protocols, limits the ecological validity of this protocol. The Loughborough Intermittent Shuttle Test (LIST) is a commonly employed intermittent exercise simulation that has been used to examine the effects of various ergogenic aids on exercise performance.[50-52] The LIST consists of 75 minutes of intermittent activity followed by a shuttle run to exhaustion. This free-running exercise simulation that replicated the movement demands of soccer was a valuable progression from unidirectional treadmill-based protocols.[44] However, the omission of a half-time period and the lack of game-specific skills, some of which have been previously found to have an energyconsuming consequence (e.g. dribbling),[53] reduces the ecological validity of the LIST and compromises the integrity of the physiological strain imposed by this protocol when compared with match-play. The inclusion of soccer skills during exercise protocols designed to replicate the demands of a soccer match was rare in early research. Although this might be surprising considering the influence that soccer skills have in defining success, players with lower skill might lack the ability to maintain skills throughout the exercise simulation, thereby compromising the overall exercise intensity. In a research field where the recruitment of large numbers of homogenous participants is already acknowledged as a major challenge, it is not surprising that the technical responses of soccer players have received relatively little attention; nevertheless, more recent studies have attempted to include soccer skills into exercise simulations. Soccer skills tests have been completed before and after exercise. In a study evaluating the effects of dehydration on soccer skill, participants performed a timed dribbling task before and after 90 minutes of soccer-specific exercise.[25] Similarly, Ali et al.[39] investigated the ergogenic potential of carbohydrate-electrolyte provision relative to a non-electrolyte placebo beverage on passing and shooting skills performed before and after a modified LIST protocol. Consequently, some Sports Med 2011; 41 (7)
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authors have investigated the effects of exercise and various ergogenic aids on the quality of skilled performances in soccer.[25,39] However, only assessing soccer skills at these timepoints does not examine the time-course of decay in technical proficiency throughout the duration of a match while players are simultaneously engaging in high-intensity intermittent exercise; furthermore, information concerning the skilled response when assessed at the end of 90 minutes of exercise is only applicable to players who are about to enter a period of extra time. More recent work has sought to rectify this problem by incorporating the performance of isolated soccer skills throughout exercise protocols.[32,34,37,38,54,55] For example, Ali and Williams[37] required fasted and previously glycogendepleted players to perform a criterion-based passing test (LSPT) every 15 minutes throughout a 90-minute modified LIST protocol, whereas Currell et al.[32] assessed kicking accuracy by means of a criterion-based shooting task on six occasions throughout a 90-minute exercise simulation. These protocols suggest that soccer skills decline during the second half of exercise; however, criterion-based outcomes limited the ecological validity of these findings. Difficulties in interpreting the results from these tests, particularly the magnitude of effect and the element of the skill that is influenced by fatigue, means that there is a need to utilize soccer-specific exercise simulations that include regular assessment of soccer skills throughout the duration of a match; furthermore, the skill tests should provide outcome measures that quantify the speed, precision and success rate of skill performance. 5. The Effects of Exercise on Soccer Skills The reduction in physical performance throughout match-play has been the focus of a number of research articles.[5,9,12,13,47,56,57] Challenges to homeostasis, such as core temperature changes[57] and the accumulated effects of match-related fatigue,[9,58] are generally thought to explain these performance decrements. However, considerably fewer articles have investigated the effects of exercise on technical performances involved in team ª 2011 Adis Data Information BV. All rights reserved.
sports, such as soccer. As mentioned previously in section 2, a disproportionate number of goals are scored in the last 15 minutes of a match;[11] therefore, it is plausible that a link exists between match-related fatigue and the technical proficiency of soccer players.[36] Rampinini et al.[18] reported that the number of involvements with the ball, short passes and successful short passes decreased from the first to the second halves in Italian Serie A matches. When these data were expressed as a function of the fatigue experienced during a game, using the decrement in high-intensity running throughout the match as an indicator of fatigue, the differences between halves were no longer evident. This finding suggests that fatigue reduces the quality of skills executed during match-play.[18] Similarly, game-related events such as kicking, heading and tackling have been observed to decrease by 11% in the second half when compared with the first half during Australian league matches.[14] These findings support the existence of an association between fatigue and soccer skill proficiency during match-play. Further attempts to elucidate the effects of exercise on soccer skills have used isolated skill tests, primarily incorporating tests of dribbling, passing and shooting. 5.1 Dribbling Performance
Dribbling is considered a valuable skill in soccer because players have the potential to advance deeper into an opponent’s territory while maintaining possession of the ball. Despite the importance of this skill, the effect of exercise on dribbling performance has received relatively little attention.[25,36,59] Using a 20 m timed sprintdribbling test, McGregor et al.[25] observed reductions in performance as a consequence of 90 minutes of soccer-specific exercise performed under conditions of fluid abstinence. However, when the same sprint-dribbling task was performed in a more ecologically valid scenario, where players consumed a fluid-electrolyte solution during exercise, skill was maintained. Consequently, dribbling speed is maintained throughout soccerspecific exercise scenarios that replicate the hydronutritional practices; however, no data exist to Sports Med 2011; 41 (7)
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evaluate the influence of fatigue on other aspects that affect the quality of dribbling (e.g. precision and success) during match-play or simulations of soccer. 5.2 Passing Performance
It has been reported that the top five teams in the Italian Serie A league complete more short passes (<37 m) than their less successful counterparts[18] and longer passing sequences are associated with an increased number of goals per possession in successful teams.[10] Additionally, an early study assessing passing proficiency in international competitions[60] found that 57% of goals were scored after a period of play that includes short passes; therefore, the maintenance of passing proficiency throughout the duration of a match probably contributes to the scoring of goals. However, studies examining the effects of exercise on isolated soccer passing performances have produced conflicting findings. McMorris et al.[61] investigated passing performance at rest and following cycle ergometry at moderate (70%) and high (100%) percentages of maximal power output. Results indicated that moderate-intensity exercise yielded improvements in passing performances, which exceeded all other intensities. In contrast, passing performance has been observed to decrease following a bout of high-intensity, lower-body resistance training.[62] Variations in the intensity of exercise, mode of exercise, and the interaction between exercise and cognitive processes (i.e. inverted U theory)[63] might explain the lack of agreement between authors. Consequently, the practical application of these findings are limited due to the likely differences that exist between the effects of fatigue induced by isolated bouts of high-intensity exercise compared with exercise that is similar to that encountered during match-play. With this in mind, other authors have used exercise protocols that simulate soccer matchplay to evaluate the influence of fatigue on passing performances;[39,40,64] however, equivocal findings exist – some researchers support this observation,[64] while others disagree.[39,40] Rampinini et al.[64] showed that the frequency and success of ª 2011 Adis Data Information BV. All rights reserved.
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short passes were reduced during the second half when compared with the first half of match-play. Conversely, Ali et al.[40] showed that participation in 90 minutes of a modified LIST protocol did not influence overall performance measures in the LSPT,[29] despite a 2.2% reduction in body mass (BM) in a fluid-abstinence trial. The use of analysis methods with greater application to onfield performances, in conjunction with the use of exercise simulations that better replicate the patterns of soccer activity, could improve our understanding of the technical response to exercise with respect to soccer passes performed throughout the duration of a match. 5.3 Shooting Performance
Shooting is arguably the most valuable skill because it directly determines the outcome of match-play. Empirical observations and research demonstrates that shooting is also the skill that exhibits the most variability, where coefficient of variance values have been found to exceed 20% in isolated shooting tasks that use a moving ball.[29,35,40] At first glance, this degree of variation appears to be high compared with generally accepted standards; however, even the most prolific of goal scorers exhibit considerable variation in goal scoring success between matches. Due to the dynamic nature of shooting, tests that incorporate decision-making and visual searching processes will incorporate more variation than tests that focus on technique alone;[29] however, the use of such tests are warranted by the enhanced ecological validity that they offer in relation to tests that incorporate a stationary ball. It has been consistently observed that shooting performances are reduced under conditions associated with physical fatigue. After 6 minutes of stepping exercise, reduced coordination between the upper and lower leg was proposed to cause a reduction in shot speed.[65] This finding has since been confirmed using a more sports-specific exercise protocol.[66] However, during soccer, the ball must be aimed towards areas within the goal that increase the chance of scoring.[29] Therefore, visual search and decision-making processes are vital contributors to success in soccer shooting; Sports Med 2011; 41 (7)
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unfortunately, such factors have not always been included in previous research.[65,66] The assessment of shot speed before and after 90 minutes of soccer-specific exercise led to initial reports that shooting performance was maintained following exercise.[39] However, the exclusion of shots that were slower than an arbitrary value resulted in significant reductions in shooting performance being observed. Unfortunately, no justification was provided for determining the threshold at which these shots were excluded and the number of shots remaining in subsequent analyses was not reported. Consequently, employing analysis methods that produce continuous rather than discrete data has the potential to extend earlier findings. For example, we have recently devised a shooting test that provides outcome measures to quantify precision, success rate and ball speed.[35] Therefore, the literature demonstrates that under physiological conditions that threaten homeostasis, a ‘speed-accuracy trade-off’[42] exists in skills that contribute to success in soccer. Similar responses have been observed in other high-intensity intermittent sports, such as tennis, where players alter specific subcomponents associated with skill execution in favour of preserving either accuracy or speed.[67] In summary, given the lack of research that documents absolute measures of technical proficiency, it is difficult to evaluate the skilled response to exercise. Nevertheless, it appears that the exercise-induced effects of fatigue vary according to the soccer skill. Shooting appears to be the most susceptible to modification by exercise-induced fatigue. Given the importance of skills during exercise and the evidence that exists concerning the decline in skilled sporting actions due to match-related fatigue, it is important that coaches account for factors that can affect the proficiency of technical performances throughout exercise. 6. Factors Affecting Technical Skills Executed during Exercise 6.1 Aerobic Fitness
It has previously been suggested that a maximal aerobic capacity in excess of 60 mL/kg/min is ª 2011 Adis Data Information BV. All rights reserved.
one of many physiological attributes that predicts success in elite soccer.[11,19] In addition to separating teams in terms of physical performances, aerobic fitness influences technical performances during soccer match-play, specifically during the latter stages. The decline in passing proficiency after a bout of high-intensity running has been correlated to aerobic fitness levels.[64] Although the physiological mechanisms of soccer fatigue remain unclear, and are likely to be multifaceted in origin, this study suggests that there is a role for sport-specific fitness training to reduce the decline in the quality of skilled performances that occurs during periods of the game where homeostasis is disturbed. This claim is further substantiated by the observation that a period of aerobic interval training increased involvement with the ball during match-play[68] and maintained passing performance following a period of high-intensity running.[69] Moreover, it has been reported that the aerobic fitness of soccer players fluctuate throughout a season.[70] Given the link that exists between aerobic fitness and the decline in skilled performances that result from fatigue, the efficacy of a mid-season aerobic training plan to counteract the decline in skill performance presents itself as a research opportunity. 6.2 Hydration Status
During exercise, metabolic heat produced via contracting musculature causes elevations in core temperature. This leads to increased sweat production and modified blood flow to the periphery for heat dissipation.[71] Even moderate hypohydration (1–2% BM loss) can impair exercise[72-74] and cognitive[73-75] performances, which are both crucial to high-intensity intermittent sports.[67] Similar magnitudes of hypohydration have been observed in soccer players who were free to voluntarily consume fluids during training and competition;[71] therefore, efforts to maintain euhydration are vital when aiming to optimize soccer performance as thirst alone is not a good enough indicator of fluid loss.[76] Despite the potential for dehydration in soccer, few studies have examined the effects of modified hydration status on the technical aspects of the Sports Med 2011; 41 (7)
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game; this is surprising considering that it is common practice for teams to seek more thermally challenging climates (i.e. increased daytime temperatures) to complete part of their pre-season preparations in which technical work will account for a large proportion of their training time. Nevertheless, the effects of fluid restriction on a timed dribbling task completed before and after intermittent running has been investigated.[25] The increased cardiovascular strain associated with dehydration resulted in the elevation of a number of physiological measures that are associated with thermal stress in the nofluid trial (i.e. serum osmolality, serum cortisol concentrations and heart rate). Moreover, 5% deterioration in dribbling performance occurred when players abstained from fluid intake. Additionally, shooting performances have been observed to reduce in fasted and previously glycogen-depleted players who exercised for 90 minutes while consuming a non-electrolyte placebo beverage.[39] Although the practical applications from these studies are difficult to interpret due to the limited ecological validity of the methods used to assess skill and the fluid-intake regimens employed, the link between hypohydration and impaired soccer performance is strengthened by the fact that attributes key to success in the game such as strength, power and anaerobic endurance are also compromised by hypohydration.[72,77,78] However, a recent study by Ali et al.[40] failed to substantiate these findings with respect to passing performances (assessed by the LSPT) in female soccer players. Baker and colleagues[74] examined the effects of hypohydration on basketball shooting drills. The authors concluded that gradual hypohydration impaired skilled performance, with the critical threshold at which a statistically significant decline in skills was achieved being 2% BM loss. Despite this study not being specific to soccer, both sports include intermittent bouts of highintensity activity repeated over a prolonged period of time while executing sports-specific skills. It is reasonable to assume that the effects of hypohydration observed by previous researchers in other multi-sprint sports (i.e. basketball)[73,74] could impact on skill performances in soccer. Consequently, ª 2011 Adis Data Information BV. All rights reserved.
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players should aim to limit water loss to within 2% BM and adhere to guidelines regarding hydration strategies during exercise.[71] 6.3 Blood Glucose Concentrations
Impaired blood glucose availability is considered to be a mechanism responsible for the deterioration of both cognitive[79-89] and physical[39,90-93] performances. Given that team sports such as soccer require the execution of sportsspecific skills while performing high-intensity intermittent exercise, and that the brain is primarily dependant on blood glucose for maintenance of cerebral function,[94] reductions in blood glucose concentrations during exercise probably influence performances in soccer; particularly with respect to the skills executed during match-play. A substantial body of evidence from nonexercise settings demonstrates that markers of cognitive function, including reaction time, arithmetical ability, verbal fluency, hand-eye coordination and visual scanning, are consistently impaired when blood glucose concentrations fall between 2.0 and 3.0 mmol/L.[80-83,86-88,95] Furthermore, complex cognitive tasks are more sensitive to reductions in blood glucose concentrations than simple tasks.[96] Although match-play has been demonstrated to reduce blood glucose concentrations,[97] the mean values of soccer players have not been reported to fall below 3.0 mmol/L. Nevertheless, serum glucose concentrations appears to be an important determinant of cognitive function before, at half-time and after soccer match-play in the heat,[98] where higher glucose concentrations were associated with faster visual discrimination, faster fine motor speed and faster psycho-motor speed. Soccer requires the simultaneous execution of cognitive, perceptual and motor skills in a rapidly changing environment.[2] Therefore, transient reductions in blood glucose could influence cognitive function and the performance of soccer-specific skills during a match, which could influence the outcome of the game. Although studies that induce hypoglycaemia have provided information concerning the influence of blood glucose concentration on cognitive performance, the stepped hyperinsulinaemic Sports Med 2011; 41 (7)
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glucose clamp technique enabled researchers to determine the threshold at which blood glucose concentrations impair cognitive function. In nondiabetic adults, almost immediate reductions in cognitive performance occur when blood glucose concentrations fall below 3.4 mmol/L;[79-83,86-89,95] concentrations which, although below average, have been reported to occur during soccer match-play.[97] As cognitive processes are crucial to skilled actions involved in competitive team sports,[67] and the role that blood glucose plays in maintaining cerebral function,[94] it is plausible that carbohydrate supplementation regimens could maintain selected soccer skills in the latter stages of a soccer match.[11,14,18] However, the influence of additional carbohydrates (either with or without simultaneous electrolyte provision) on the skilled performances during high-intensity intermittent sports has resulted in equivocal findings, where some studies support carbohydrate supplementation[26,32,36,39,73,90,91,99,100] and others do not.[22,101] Table III summarizes the studies that examine the effects of carbohydrate supplementation on technical aspects involved in the game of soccer. Contradictory findings currently exist concerning the effects of carbohydrate usage in attenuating a decline in aspects of technical performance. It is likely that early methods of skill evaluation such as the use of global measures of skilled performance (i.e. the number of goals scored or conceded during match-play) were too variable to consistently detect the subtle changes involved in supplementation research and this may account for the inconsistent findings.[22,102] Similarly, studies with self-perceived exercise intensities[26] and/or criterion-based outcome measures have also failed to agree on the effects of carbohydrate provision on various skills performed before, after and during exercise.[26,32,37,39] Ali and Williams[37] suggested that exogenous carbohydrate must be supplied at a minimum rate of 50 g/hour in order to improve motor skill performance. This statement was based on the findings of previous authors.[26,90] Interestingly, supplementing fasted and previously glycogendepleted participants with 52 g/hour of carbohydrates yielded no benefit to LSPT performance ª 2011 Adis Data Information BV. All rights reserved.
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when assessed before, after and during exercise.[37] This finding supports previous work from the same laboratory where passing was assessed before and after exercise and carbohydrates were supplied at a rate of 30 g/hour.[39] However, 30 g/hour of carbohydrate was beneficial to shooting performances post-exercise when compared with a non-electrolyte placebo trial. Although these results should be interpreted carefully due to methodological limitations regarding the skilled performance outcome measures and the hydronutritional status of the players pre-exercise (i.e. fasted and previously glycogen-depleted), the results suggest that the effects of carbohydrate provision can differ according to the type of skill being performed. Therefore, determining the critical blood glucose concentration at which skilled performance is challenged presents itself as a future research opportunity. It appears that the dose of carbohydrate is important when seeking to improve soccer skill performance. However, the optimal dose of carbohydrate has not been elucidated when seeking to maintain soccer skill proficiency in the latter stages of a match. Given that a dose-response relationship exists between carbohydrate provision and cognitive function in the non-exercise setting,[103] it remains to be determined whether higher doses of carbohydrates ingested during exercise will further increase the performance of skills. If so, caffeine, which has previously been reported to enhance the absorption[104] and oxidation[105] of co-ingested carbohydrates, might be of interest to team-sports players given the concomitant influence that this ergogenic aid has on the CNS. However, adding 3.7 mg/kg BM caffeine to a 6% carbohydrate-electrolyte solution did not improve performance in the LSPT.[55] The consumption of a high-glycaemic index carbohydrate in the hour before exercise can lower blood glucose levels 15–30 minutes after starting exercise.[106,107] Although the effects of exerciseinduced hypoglycaemia have been reported to reduce performance,[108] more recent research suggests that physical performance is not adversely influenced.[106,107] Studies involving non-exercising participants have demonstrated that almost immediate reductions in cognitive performance occur Sports Med 2011; 41 (7)
Subjects
Supplements
Timing (and dose) of supplements
Exercise protocol
Measurement of skill
Effect on skilled performance
Muckle[102] (1973)
NA
350–450 Kcal glucose syrup
30 min prior (NA)
90 min match
Frequency of ball contacts, goals scored or conceded, ball involvements per player
CHO › goals scored, CHO › defensive performances in last 30 min
Zeederberg et al.[22] (1996)
11 M
6.9% glucose polymer-electrolyte beverage or PL
15 min prior (5 mL/kg BM), half-time (5 mL/kg BM)
90 min match
Subjective evaluation of controlling, passing, dribbling, heading, tackling and shooting
No effects of CHO
Northcott et al.[26] (1999)
10 M
8% glucose-polymer or water PL
15 min prior (8 mL/kg BM), half-time (8 mL/kg BM)
90 min match simulation
CBM of various lengths of passing (10, 20 and 30 m) and shooting (15 m)
CHO › skill proficiency in last 15 min compared with PL
Ostojic and Mazic[36] (2002)
22 M
7% CHO-electrolyte beverage or plain water PL
Immediately prior (5 mL/kg BM), every 15 min during exercise (2 mL/kg BM)
90 min match
Timed dribbling test (see McGregor et al.[25])
CHO › dribbling performance compared with PL
Ali et al.[39] (2007b)
16 M
6.4% CHO-electrolyte beverage (Lucozade Sport) or a nonelectrolyte PL
Immediately prior (5 mL/kg BM), every 15 min during exercise (2 mL/kg BM)
90 min match simulation
CBM of passing and shooting
CHO › shooting performance compared with PL post-exercise No effect of exercise or CHO on passing
Ali and Williams[37] (2009)
17 M
6.4% CHO-electrolyte beverage (Lucozade Sport) or a nonelectrolyte PL
Immediately prior (8 mL/kg BM), every 15 min during exercise (3 mL/kg BM)
90 min match simulation
CBM of passing
No effects of CHO
Currell et al.[32] (2009)
11 M
7.5% maltodextrin beverage or PL
30 min prior (6 mL/kg BM), half-time (4 mL/kg BM), every 12 min during exercise (1 mL/kg BM)
90 min match simulation
Timed dribbling test, CBM of shooting and a maximum jump height heading task
CHO › dribbling and shooting performances in each trial
BM = body mass; CBM = criterion-based measure; CHO = carbohydrate; M = males; NA = data not available; PL = placebo; › indicates significant improvement (p £ 0.05).
535
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Study (year)
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ª 2011 Adis Data Information BV. All rights reserved.
Table III. The influence of acute carbohydrate supplementation on skilled performances of soccer players
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when blood glucose concentrations fall below 3.4 mmol/L;[79-83,86-89,95] furthermore, restoration of euglycaemia after a hypoglycaemic episode does not lead to immediate recovery of cognitive function, with delays of up to 90 minutes before cognitive function is restored to pre-hypoglycaemic levels.[95,109] It is, therefore, plausible that even transient reductions in blood glucose concentration might adversely affect decision making, other cognitive functions and ultimately the performance of skills. Nevertheless, the influence of reduced blood glucose concentrations on skill performance during high-intensity intermittent exercise remains to be evaluated. 7. Conclusions and Future Research Recommendations The purpose of this article was to provide the reader with current information concerning the frequency and type of skills performed during a soccer game, discuss the methods used to simulate and evaluate the demands of soccer matchplay (focusing on the measurement of soccer skills), explore the effects of exercise on these skills, and to examine the factors that influence skill proficiency during soccer-specific exercise. This article aims to inform researchers and coaches about soccer skill investigations and to initiate future research in this field. Nevertheless, it should be noted that the issues raised in this review are not exclusive to soccer and the application of these findings to other high-intensity intermittent sports is encouraged. The unpredictable nature of soccer limits the suitability of match-play as an exercise protocol when examining the effects of interventions on performance; consequently, a number of soccerspecific exercise simulations have been developed to elicit repeatable responses to exercise. Despite the frequent application of simulation protocols in scientific research, the ecological validity of these protocols is questionable. This problem is further complicated by the array of skilled movements involved in soccer and problems associated with performing such movements under controlled laboratory conditions. Thus, the majority of research in this field employs methods of skill ª 2011 Adis Data Information BV. All rights reserved.
assessment where the ball is aimed towards a target, with the performance judged and scored according to set criteria.[26,29,64,69] Although the use of skill tests that produce criterion-based outcome measures has overcome some of the problems associated with assessing skills throughout match-play, the results are difficult to interpret. Therefore, researchers are encouraged to incorporate skill tests with increased ecological validity and outcome measures of a continuous (as opposed to discrete) nature. Factors that contribute to the decline in physical performances in soccer (e.g. fitness, dehydration and hypoglycaemia) might also moderate skill proficiency during match-play, particularly in the latter stages. Early research, in combination with findings from other high-intensity intermittent sports, supports further investigation into interventions such as aerobic training, fluidprovision and carbohydrate-electrolyte supplementation to attenuate the decline in technical performance that is associated with fatigue. However, because the mechanism(s) responsible for the deterioration in skill performance remain unclear, more research is required to develop appropriate strategies to maintain skill proficiency throughout soccer match-play. 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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96. Warren RE, Frier BM. Hypoglycaemia and cognitive function. Diabetes Obes Metab 2005; 7: 493-503 97. Ekblom B. Applied physiology of soccer. Sports Med 1986; 3: 50-60 98. Bandelow S, Maughan R, Shirreffs S, et al. The effects of exercise, heat, cooling and rehydration strategies on cognitive function in football players. Scan J Med Sci Sports 2010; 20: 148-60 99. Vergauwen L, Brouns F, Hespel P. Carbohydrate supplementation improves stroke performance in tennis. Med Sci Sports Exerc 1998; 30: 1289-95 100. Bottoms LM, Hunter AM, Galloway SDR. Effects of carbohydrate ingestion on skill maintenance in squash players. Eur J Sport Sci 2006; 6: 187-95 101. Ferrauti A, Weber K, Struder HK. Metabolic and ergogenic effects of carbohydrate and caffeine beverages in tennis. J Sports Med Phys Fitness 1997; 37: 258-66 102. Muckle DS. Glucose syrup ingestion and team performance in soccer. Br J Sports Med 1973; 7: 340-3 103. Messier C, Pierre J, Desrochers A, et al. Dose-dependent action of glucose on memory processes in women: effect on serial position and recall priority. Brain Res Cogn Brain Res 1998; 7: 221-33 104. Van Nieuwenhoven MA, Brummer RM, Brouns F. Gastrointestinal function during exercise: comparison of water, sports drink, and sports drink with caffeine. J Appl Physiol 2000; 89: 1079-85 105. Yeo SE, Jentjens RL, Wallis GA, et al. Caffeine increases exogenous carbohydrate oxidation during exercise. J Appl Physiol 2005; 99: 844-50 106. Jentjens RL, Cale C, Gutch C, et al. Effects of pre-exercise ingestion of differing amounts of carbohydrate on subsequent metabolism and cycling performance. Eur J Appl Physiol 2003; 88: 444-52 107. Jentjens RL, Jeukendrup AE. Effects of pre-exercise ingestion of trehalose, galactose and glucose on subsequent metabolism and cycling performance. Eur J Appl Physiol 2003; 88: 459-65 108. Foster C, Costill DL, Fink WJ. Effects of preexercise feedings on endurance performance. Med Sci Sports 1979; 11: 1-5 109. Tallroth G, Lindgren M, Stenberg G, et al. Neurophysiological changes during insulin-induced hypoglycaemia and in the recovery period following glucose infusion in type 1 (insulin-dependent) diabetes mellitus and in normal man. Diabetologia 1990; 33: 319-23
Correspondence: Dr M. Kingsley, Sport and Exercise Science, Swansea University, Singleton Park, Swansea, SA2 8PP, UK. E-mail:
[email protected]
Sports Med 2011; 41 (7)
REVIEW ARTICLE
Sports Med 2011; 41 (7): 541-557 0112-1642/11/0007-0541/$49.95/0
ª 2011 Adis Data Information BV. All rights reserved.
Sex Differences in Proximal Control of the Knee Joint Jurdan Mendiguchia,1,2 Kevin R. Ford,1,3 Carmen E. Quatman,1,4 Eduard Alentorn-Geli5 and Timothy E. Hewett1,3,4,6 1 Sports Medicine Biodynamics Center and Human Performance Laboratory, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH, USA 2 Studies, Research and Sport Medicine Center, Government of Navarra CEIMD, Department of Physical Therapy, Pamplona, Spain 3 Department of Pediatrics, College of Medicine, University of Cincinnati, Cincinnati, OH, USA 4 The Ohio State University Sports Medicine Sports Health & Performance Institute, Departments of Physiology & Cell Biology, and Orthopaedic Surgery, Columbus, OH, USA 5 Department of Orthopaedic Surgery, Hospital del Mar i l’Esperanc¸a – IMAS, Barcelona, Spain 6 The Ohio State University, The School of Allied Medical Professions and The College of Medicine, Family Medicine and Biomedical Engineering, Columbus, OH, USA
Contents Abstract. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. The Concept of ‘Core Stability’ . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Sagittal Plane Evidence for Proximal Control of Knee-Joint Stability. . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1 Trunk Contributions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2 Hip Contributions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. Coronal Plane Evidence: Proximal Control of Knee Stability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1 Trunk Contributions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2 Hip Contributions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5. Transverse Plane Evidence for Proximal Control of Knee-Joint Stability . . . . . . . . . . . . . . . . . . . . . . . . . 5.1 Trunk Contributions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2 Hip Contributions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Abstract
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Following the onset of maturation, female athletes have a significantly higher risk for anterior cruciate ligament (ACL) injury compared with male athletes. While multiple sex differences in lower-extremity neuromuscular control and biomechanics have been identified as potential risk factors for ACL injury in females, the majority of these studies have focused specifically on the knee joint. However, increasing evidence in the literature indicates that lumbo-pelvic (core) control may have a large effect on knee-joint control and injury risk. This review examines the published evidence on the contributions of the trunk and hip to knee-joint control. Specifically, the sex differences in potential proximal controllers of the knee as risk factors for ACL injury are
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identified and discussed. Sex differences in trunk and hip biomechanics have been identified in all planes of motion (sagittal, coronal and transverse). Essentially, female athletes show greater lateral trunk displacement, altered trunk and hip flexion angles, greater ranges of trunk motion, and increased hip adduction and internal rotation during sport manoeuvres, compared with their male counterparts. These differences may increase the risk of ACL injury among female athletes. Prevention programmes targeted towards trunk and hip neuromuscular control may decrease the risk for ACL injuries.
1. Introduction The number of females participating in sports has increased by over 900% in high school and 500%[1] in collegiate athletics over the last few decades. This large increase in participation, combined with a 4- to 6-fold higher anterior cruciate ligament (ACL) injury rate in females[2-4] has led to a corresponding increase in ACL injuries. ACL ruptures lead to chronic knee pain and disability, a significantly greater risk of radiographically diagnosed knee osteoarthritis,[5-8] high costs for management,[9-12] loss of entire sports seasons, possible loss of scholarship funding and significantly lowered academic performance.[13,14] Sex differences in ACL injury rates may be explained by anatomical,[15-23] hormonal[4,7,24-30] and/or neuromuscular factors.[11,31-34] Even though anatomical and hormonal factors may contribute to an ACL injury, the implications of both factors are not yet clear.[35] Moreover, modification of these parameters would be both difficult and controversial. In contrast, neuromuscular adaptations are readily achievable and have been used extensively to lower ACL injury risk in female athletes.[7,33,36-38] There is increasing evidence that insufficient or abnormal neuromuscular control of the lower limbs during athletic movements, in particular over the knee joint, is a primary contributor to non-contact ACL injuries, especially in the female athlete.[39] The knee is not an isolated joint, but is part of the body in which the trunk, hips, knees and ankles constitute the body’s kinetic chain that controls lower-extremity movements. The proximal and distal segments of the body’s kinetic chain can have significant effects on knee-joint biomechanics.[35,37] The kinetic chain ª 2011 Adis Data Information BV. All rights reserved.
model refers to the body as a linked system of interdependent segments, often working in a proximal-to-distal sequence, to achieve the desired movement in an efficient manner.[40] Hence, considering the relationship between the trunk and the lower-extremity joints during a dynamic task, it is important to consider the effects of the trunk and hip on the control of the knee. Specifically, the trunk-to-hip system will be referred to as core, throughout the review. This review reports the existing evidence on the contributions of the trunk and hip to neuromuscular control of the knee joint. A systematic review of the literature was performed by utilizing an electronic database literature search in PubMed MEDLINE (1985–2009). The keyword selection was designed to capture all aspects of the contributions of the trunk and hip to neuromuscular control of the knee joint and the search terms included: ‘ACL prevention’, ‘ACL biomechanics’, ‘ACL and trunk’, ‘ACL and hip’, ‘non-contact ACL injuries’, ‘mechanisms of ACL injuries’ and ‘prevention non-contact ACL injuries’. The search was supplemented by a review of the bibliographies of retrieved articles, personal correspondence with authors of retrieved articles and hand searching of journals to identify any additional studies addressing this topic of interest. Articles included in this review were limited to those published in English. 2. The Concept of ‘Core Stability’ Despite the growing interest in the body’s core during the last decade, ‘core stability’ remains an often ambiguous or misused term. It has been incorrectly used synonymously and interchangeably Sports Med 2011; 41 (7)
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with core strength, hip strength, balance and spine stability. In this review, the term ‘core musculature’ will be referred to as those muscles that surround and insert into the lumbopelvic region. These muscles act synergistically to stabilize the trunk and hip and contribute to the stability of more distal joints, including the knee joint. The term ‘core stability’ is considered the ability of passive (ligaments and vertebral facets) and active stabilizers involved in the lumbopelvic region to maintain appropriate trunk and hip posture, balance and control during static and dynamic movements.[41] Neuromuscular control consists of sensory input (muscle spindles, Golgi tendon organs and receptors within the core ligaments),[42,43] CNS processing and motor (the neuromuscular signal) output. The output is targeted to the core musculature, thus optimal recruitment, strength and endurance of the 29 muscles attached to the pelvis are necessary to maintain and restore joint (core) homeostatic stability in response to internal or external forces from expected or unexpected perturbations in all planes of motion. The need for an adequate intermuscular coordination between such a large number of muscles shows the complex nature existing under the concept of core. Core stability, a critical component of the entire body kinetic chain, is especially important during unexpected dynamic situations, where insufficient control of the core may affect the control of other joints through the multi-segment system and possibly lead to injury at other joints in the system.[39] The concepts of ‘robustness’ and ‘performance’ are important for the proper investigation of dynamic stability of the core during athletic manoeuvres.[44] According to the definition of robustness of Reeves et al., the core is considered to be robust if it remains stable after perturbation.[44] In contrast, performance is defined as how close the disturbed trajectory of the core remains to the undisturbed and expected trajectory. Both concepts depend on the neuromuscular control of all the muscles that attach to the lumbopelvic region. The main function of the core during sports manoeuvres is to maintain the stability of the whole system and allow optimal production, transfer and control of force and motion to the terminal segment (proximal to distal) for integrated kinetic ª 2011 Adis Data Information BV. All rights reserved.
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chain activities in order to achieve the maximum efficiency.[45] Kibler et al.[45] demonstrated that >50% of the total kinetic energy and total force generated in the tennis serve is generated by the lower legs, hip and trunk. The proximal to distal muscle firing sequence has been shown in running and kicking activities, with the hip flexors being the main contributor muscles to achieve the highest velocities.[40,46] Growing evidence for decreased neuromuscular control of the core as an underlying cause of injury[41,47-53] justifies the increased use of current trunk or core neuromuscular training as a central tenet of rehabilitation treatments and prevention.[54-59] However, some of these studies observed a reduction of force output at the hip, which may consequently result in an increased risk of lowerextremity injury. Although the hip is part of the core, measures of hip strength should not be wholly defined as, or generalized to, core stability. It is not known how isolated hip strength functions to stabilize the core. If quantitative analysis is accurate, for daily living, 10% of maximal voluntary contraction or even less of abdominal co-contraction may be sufficient to achieve spine stability. Moreover, given the relationship observed between stiffness and stability, the majority of spine stability may be achieved in the first 25% of the maximum contraction level.[60] Hence, neural control, motor firing patterns or muscular endurance are likely to be of greater importance than strength in determining overall core stability. Further studies and the use of core models that include all the muscles that attach to the pelvis are needed to elucidate the influence of each of these control components on total core stability. Ireland[61] speculated about a possible relationship between the trunk and hip with ACL injuries. The videographic sequence analyses of sports knee injuries formed the basis of the authors’ proposed ‘position of no return’ model for a non-contact ACL injury.[61] However, the link between proximal control strategies and abnormal knee-joint loading and motions specifically related to sex differences remains unclear. In the remainder of this review, we evaluate the current evidence into the three planes of movement (sagittal, coronal and transverse) in Sports Med 2011; 41 (7)
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order to create a working construct to better understand the current evidence for the connection between the proximal core neuromuscular controllers and distal knee-joint stability. Although trunk and hip are part of the core, both regions were reviewed in separate sections for didactic reasons. In summary: Core musculature is referred to as those muscles that surround and insert into the lumbopelvic region. These muscles act synergistically to stabilize the trunk and hip and contribute to the stability of more distal joints, including the knee joint. Core stability is considered the ability of passive and active stabilizers of the lumbopelvic region to achieve the minimum neuromuscular control needed, in order to maintain appropriate trunk and hip posture, balance and control during static and dynamic movements. The link between proximal control strategies and abnormal knee-joint loading and motions specifically related to sex differences remains unclear. 3. Sagittal Plane Evidence for Proximal Control of Knee-Joint Stability 3.1 Trunk Contributions
Knee flexion-extension may be influenced by the trunk and hip proximal musculature. The trunk, arms and head comprise approximately 60% of the body mass.[62] Increases in height of the centre of mass during puberty may result in more challenging trunk neuromuscular control, especially during high-speed athletic manoeuvres.[63] Trunk, arms and head position relative to hip, knee and ankle may influence ground reaction force (GRF), energetics and knee load from a landing or cutting manoeuvre.[64] An understanding of the biomechanical relationship between the trunk and knee may be used to reduce GRF and energetic demands of passive and dynamic restraints and thus decrease the likelihood of knee injury. Recently, Blackburn and Padua studied trunk, hip and knee biomechanics during two landing tasks, a natural landing strategy (preferred) and a ª 2011 Adis Data Information BV. All rights reserved.
landing that involved active trunk flexion upon landing (flexed). Peak trunk flexion angle was 47% greater for the flexion group compared with the preferred landing group.[65] The authors demonstrated that trunk flexion during landing produced concomitant increases in knee (22) and hip flexion (31) angles. An increase in knee flexion may result in decreased anterior shear forces and GRF, with a subsequent decrease in ACL load. Hamstrings lengthening and the increase in passive tension imposed by greater hip flexion may also account for the decreased tension induced by knee flexion. Coronal and transverse plane knee kinematics did not differ significantly between preferred and flexed landings. In addition, the authors did not find sex differences in landing forces and quadriceps electromyographic activity depending on trunk flexion.[66] Flexing the trunk forward or moving the mass of the upper body anterior towards the knees may result in a reduced external knee flexion and internal quadriceps moments with concomitant increase in internal hamstrings moments during landing. This may be explained by a reduction in the quadriceps moment arm (decreasing shear forces) between trunk and knee, and an increase in the hamstrings hip extensor activity.[64] Synergistically, trunk flexion in a standing position may increase posterior shear forces and enhance hamstrings activation, which can potentially decrease forces on the ACL.[67,68] This mechanical advantage can be altered by reduced stiffness derived by excessive length and laxity of hamstrings muscles. Increased laxity may reduce muscle reflex activity and fibre shortening velocity.[69,70] Both would increase latencies, decrease joint stiffness and potentially decrease dynamic knee stability.[31,69-76] Generalized joint laxity, which has been reported to be higher in female athletes, and anterior–posterior knee-joint laxity have been associated with an increased risk of non-contact ACL injury for both males and females.[77-80] The absence of trunk control may increase ACL load and predispose one to an injury, especially with knee angles near full extension.[81-87] Altered weighting of the trunk may have direct effects on loading of the knee joint. Kulas et al.[88] recently reported lower-extremity biomechanics Sports Med 2011; 41 (7)
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during drop landings with added load (10% of bodyweight) to the trunk. The study subjects were divided into either a trunk flexor or trunk extensor landing style. The trunk extensor group increased knee and ankle extensor efforts over 20% and 14–15% during landing, respectively. In contrast, the trunk flexor group did not exceed a 10% increase in either the ankle or knee extensor moments after weighting. The trunk extensor group showed an 11–18% decrease in hip extensor efforts, while flexor group increase 14–19%. These findings are in agreement with Farrokhi et al.,[89] who reported similar relationships during a lunge manoeuvre. Studies have reported that females demonstrated more erect landings postures[90-93] and less hip absorption compared with males,[90] which may be related to the decrease in hip extensor activity reported by Kulas et al.[88] From these data, it may be concluded that an increase in flexion of the trunk would be an appropriate strategy to reduce ACL injury risk. The resultant increase in hip and knee flexion alone would support this statement. However, the referred studies did not clarify whether or not the behaviour is the same for both sexes. Furthermore, the reported trunk flexion angles do not usually correspond to those angles seen in athletic manoeuvres. Excessive trunk flexion and concomitant hip flexion may influence the gluteus medius and gluteus maximus muscles attachment leading to decreased hip abduction and extension strength. This may in turn result in undesirable joint angles and moments at the knee during dynamic motion, potentially decreasing proximal control.[94] A recent injury mechanism description in the literature, based on video analysis of basketball players, reported greater hip and knee flexion angles in female players who suffered a valgus collapse with ACL injury compared with males.[93] The description of the trajectory of the trunk during landing (performance) as well as the sudden reaction movement of the trunk following the perturbation created from the GRF (robustness) may be useful to find sex differences in trunk behaviour and stability. Neuromuscular control of the trunk is likely different between males and females.[94] Abdominal activation patterns may differ between sexes during ª 2011 Adis Data Information BV. All rights reserved.
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double-leg landings, though they may be reliable for prediction of ACL injuries in females.[34] Specific local abdominal activation strategies (tranversus and internal oblique abdominal muscles) used by males during landing may be safer than general abdominal muscles activation used by females.[94] Although local activation strategies are beneficial for injury prevention,[95-98] the general activation of other muscles is also important for core stability. All the torso muscles, acting harmoniously, likely play a critical role in securing spinal stability and reacting against external perturbations.[99-103] However, further research is needed in this area to know if there are different abdominal patterns between sexes (e.g. muscle patterns that occur in the quadriceps, hamstrings, or gluteus) and how these patterns affect trunk motion and, consequently, knee load. 3.2 Hip Contributions
Increased trunk flexion during landing produced concomitant increases in knee and hip flexion compared with a more erect/extended trunk posture in a drop jump.[65] An increase in hip flexion could result in reduced shear forces and increased hip extensor effort and energy absorption.[88,104] The gluteus maximus is an important controller of trunk flexion,[105-108] and contributes to hip absorption at landing.[90] Females may land more erect compared with males,[90,91,93,109] thus decreasing the hip absorption and, consequently, increasing knee and ankle loads.[90] Eccentric hip extensor contraction can absorb over 20% of the body’s total kinetic energy in females during soft, compared with stiff, landings.[64] Hence, the trunk and hip flexor/extensor musculatures are an important contributor to loads at the knee, and may influence the GRF from a landing. However, the relative contribution of each joint to energy absorption is poorly understood. Females have lower gluteus maximus activation[110,111] and hip extension strength compared with males.[20,112-114] This may indicate the crucial role posterior hip muscles play in preventing knee injuries. However, these data must be taken with caution because these studies did not control the influence of the trunk flexion in gluteus medius activation[94,115] nor the correlation Sports Med 2011; 41 (7)
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between strength and electromyography. The potential for increased hip flexion to change the moment arm of the gluteus medius and gluteus maximus could negatively affect neuromuscular control at the hip and in consequence, at the knee. Hewett et al., in a prospective study conducted with 205 female athletes, observed a greater peak external hip flexion moment during drop landings coupled with a tendency to lower maximum knee flexion angles (10.5 less) in the group that sustained ACL injury compared with the uninjured athletes.[34] Differences between sagittal plane knee flexion-extension moments and ACL injury status were not reported. However, since the sagittal plane may not be considered a primary predictor of ACL injury in females, it was speculated that the knee and hip joint are better prepared to act as a hinge in this plane. Thus, the musculature that limits sagittal plane trunk, hip and knee motion dissipates sagittal plane knee loads more effectively than coronal plane loads. Similar to those findings reported by Hewett et al.,[34] Kernozek et al.[112] found no significant differences in hip flexion angles, hip extensor moments (internal) and knee moments and angles between males and females also following a drop jump. However, females demonstrated greater vertical and posterior GRF than males. This finding is in agreement with the stiffer landing style in females postulated by Decker et al.[90] Conversely, Salci et al.[116] reported decreased hip and knee flexion in female volleyball players during block and spike landings compared with males. Similar results were found by Schmitz et al.[117] in single-leg drop landings tasks, where females exhibited decreased hip and knee flexion angles compared with males. In contrast, Hewett et al.[118] did not find differences in hip sagittal plane kinetics and kinematics during single-leg horizontal hops, reinforcing the ‘hinge’ mechanism theory for sagittal plane. Theoretically, decreased hip and knee flexion may increase anterior shear forces and therefore ACL load.[81-86,119] Decreased hip flexion angles may inhibit hip extensor muscles, increasing quadriceps extensor torques. Greater GRF in combination with greater quadriceps force may increase the anterior translation force to the tibia excessively, especially near full ª 2011 Adis Data Information BV. All rights reserved.
knee extension,[81,82,84,85,119,120] where the ACL is at higher risk of injury.[31] Only a few studies have examined sex differences in the biomechanics of the hip and knee exclusively in the sagittal plane during the cutting manoeuvre. McLean et al.[120] reported less hip and knee flexion angles in females compared with males in a side-cut manoeuvre with opposition. In contrast, Landry et al.[121] reported decreased hip flexion angles and smaller hip flexion moments in females compared with males, but no differences in knee flexion angles and moments during unanticipated side-cut manoeuvres. Yu et al.[122] and Chappell et al.[123] reported decreased hip flexion with decreased knee flexion angles in females compared with males during vertical stop jumps. Although Yu et al.,[122] based on hip and knee angular velocities, suggested that GRF are more related to the motion than to the hip and knee angles, the role of joint positions in the risk of ACL injury has been well established, as joint angles may not only influence GRF but also force vectors of muscles. Controversially, Krosshaug et al.[93] reported greater hip and knee flexion in female basketball players than males at initial contact and at initial contact during landing tasks. Females demonstrated a 5.3-fold higher relative risk of sustaining a valgus collapse.[93] This increase in hip flexion has been previously related with greater knee valgus positions in females.[124,125] In summary: Trunk, arms and head position relative to hip, knee and ankle may influence GRF, energetics and knee load from a landing or cutting manoeuvre. The gluteus maximus is an important controller of trunk flexion, and contributes to hip absorption at landing. Females may land more erect compared with males, thus decreasing the hip absorption and, consequently, increasing knee and ankle loads. 4. Coronal Plane Evidence: Proximal Control of Knee Stability 4.1 Trunk Contributions
Minimal evidence exists regarding the influence of the trunk on the hip, knee and ankle. The Sports Med 2011; 41 (7)
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video evidence of ACL injuries reported by Hewett et al.[125] shows that the female trunk usually moves lateral to the ACL-injured limb as the knee abducts, while this is not a common observation in males (figure 1). A possible close relationship between the position of the trunk and lower limb has been established by Dempsey et al.[124] The authors recently reported that sidestep cutting techniques influence peak valgus and internal rotation moments in healthy young male athletes (around 21 years old). A foot position away from the midline with the GRF lateral to the knee-joint centre and trunk leaning and rotating to the opposite direction with respect to the cut (displacing the centre of mass away from the plantar surface of the foot) may significantly increase lower-extremity valgus and internal rotation loads at the knee joint during the weight acceptance phase. Moreover, ipsilateral trunk lean may be a sign of weak hip abductors as it moves the centre of mass closer to the stance limb to reduce demand on the weak abductors,[126] therefore considerably affecting core stability and robustness. Pollard et al.[127] speculated that females lean the trunk over the stance limb and agreed with the results of Dempsey et al.[124] who observed a displaced foot at initial contact among females who presented with greater external knee abduction during side cutting. Knee valgus has been found to be one of the strongest predictors of ACL injury in female athletes.[34] During single-leg
Fig. 1. Photograph of an athlete sustaining an anterior cruciate ligament injury event, which illustrates a common mechanism of injury in female athletes, with trunk movement lateral to and away from the body’s midline as the knee collapses toward the midline.
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landing and cutting, the entire body mass must be balanced over one lower extremity. Because the trunk, head and arms comprise greater than half of the body’s mass, lateral trunk motion increases GRF and knee abduction load. Therefore, technique modification and feedback would be an important element to include in prevention programmes to decrease knee valgus torque in sports involving side-step cutting.[126] Zazulak et al.[128] reported that lateral displacement was a strong predictor of knee ligament injuries. Trunk displacement, proprioception and history of low back pain predicted knee ligament injury with 91% sensitivity and 68% specificity, and specific ACL injuries with 91% accuracy in female athletes. Low back pain may decrease force,[129-131] hip strength[132] and endurance,[133,134] and may alter activation patterns (preactivation and delayed reflex activation),[135-140] postural control,[141,142] trunk proprioception,[143-145] side-to-side weightbearing symmetry[146] and gluteal activation.[147-149] Thus, low back pain may decrease the capability to react against a movement and may reduce trunk equilibrium and robustness. This may unexpectedly move the centre of mass and potentially excessively load the knee joint. Zazulak et al.[128] employed open kinetic chain movements to detect proprioceptive deficits at the trunk. Most sport manoeuvres of the lower extremity are performed through closed kinetic chain movements, during which ACL injuries likely occur. Studies incorporating more functional tasks are needed to confirm these findings. However, the role of lateral trunk flexion in ACL injury risk remains controversial. Zeller et al.[150] reported that female athletes had a decreased amount of lateral trunk flexion in a kinematic study during single-legged squat compared with their male counterparts. This was related to a greater knee valgus angle presented during the same task in females. Thus, core stability in the coronal plane may have a profound influence on distal joints. Deficits in neuromuscular control of the trunk during cutting and landing may lead to uncontrolled lateral trunk motion that may increase knee abduction motion and torque through mechanical (lateral GRF motion)[127,151] and neuromuscular Sports Med 2011; 41 (7)
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(increased hip adductor torque)[34] mechanisms, consequently increasing strain on the ACL and leading to injury via either one or both of these mechanisms. Disturbances in trunk motions may increase the ACL injury risk by altering transmission of forces distally and by inducing deleterious joint positions. Core stability may be a crucial component of prevention programmes,[148] although further research is needed to better understand the exact role of coronal plane trunk biomechanics in the genesis of ACL injuries. 4.2 Hip Contributions
The contributions of the hip musculature to knee abduction have been studied in running, landing, squatting and side-step cutting manoeuvres. Female recreational athletes were found to have greater peak hip adduction angles with greater peak knee abduction angles when running compared with their male counterparts.[123,152] In contrast, hip moments may not differ between sexes for running actions.[123] During the landing preparation of a stop-jump task, Chappell et al.[123] found decreased hip abduction (also decreased hip flexion and hip external rotation) in female compared with male athletes. During the landing task itself, Blackburn and Padua[65] did not observe coronal plane biomechanical changes at hip and knee joints after increased trunk flexion during landing. A correlation between hip adduction moment and knee abduction moments in ACL-injured subjects (R = 0.69) was noted in females who subsequently injured their ACL.[34] An external hip abduction moment created by the GRF moving lateral to the centre of the femoral head is counterbalanced internally by hip adductor torque. Ford et al.[153] reported an increase in coronal excursion of the hip and knee after a single drop landing of approximately 13 cm, both medially and laterally, for females compared with males. In contrast, no sex differences for hip abduction at initial contact, maximum hip abduction or maximum hip adduction were reported. These results agree with findings of Pappas et al.,[154] who found less hip adduction in unilateral (one-legged) compared with bilateral (two-legged) landings despite similar ending ª 2011 Adis Data Information BV. All rights reserved.
position at the time of peak knee flexion. These authors did not observe differences between sexes in hip kinematics during single-legged landings. Significant correlations between coronal plane hip and knee initial contact angles during both types of landings were observed for females but not for males.[155] Considering all the presented data, hip and trunk excursions and trajectory may be more informative than the final position. Hewett et al. also assessed sex differences on hip kinetics and kinematics in single-legged landings.[155] The landing task consisted of three consecutive horizontal single-leg hops holding the position after the last one. Females demonstrated greater hip adduction angles at initial contact. The maximal adduction angles and external adduction moments at the hip were significantly greater for the first and second but not for the third hop. Landing sex differences were also reported by Jacobs et al.[156] during a more complex and functional task that mimics a high-risk posture for ACL injury. The task consisted of a double-legged, broad-jump landing on a single leg. Females had lower hip abduction compared with males, and moderate correlations were shown between hip abduction strength and knee valgus kinematics for females, but not for males.[156] In contrast, Padua et al.[157] examined the relationship between hip strength measured by hand-held dynamometer and joint kinematics during a drop jump task in 63 males and 54 females. The authors reported decreased gluteus medius and gluteus maximus strength that were related to greater knee valgus at initial contact and greater peak knee valgus. Therefore, hip abduction strength assessment may be a potential method to identify those subjects at risk of ACL injury at landing. Also, hip abduction strength programmes may decrease the risk of sustaining an ACL tear at landing. Overall, female soccer players were found to have a significant side-to-side disparity in hip abductor strength not present in males.[158] In single-legged squat kinematics, Zeller et al.[150] reported that female athletes had an increased amount of hip adduction (with concomitant increase in knee valgus) when compared with males. In contrast, Nguyen[20] only found a trend toward Sports Med 2011; 41 (7)
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more hip adduction in females, but no statistically significant sex differences were demonstrated in single-legged squat. Most of the data indicate that females have difficulties with hip control and also show the potential importance of gluteus medius strength and activation in order to stabilize the pelvis in single-leg, weight-bearing sport activities. Studies have reported a significant increase in hip adduction moments in females concomitantly with greater knee valgus moments compared with males during side-step cutting.[121,159] Sigward and Powers[160] investigated the hip coronal plane kinematics in a group of females divided by the magnitude of external moment knee valgus during side-step cutting. Contrary to their primary hypothesis, females with excessive knee valgus moment demonstrated significantly larger hip abduction position at initial contact compared with the females with a normal valgus moment. The authors argued that more hip abduction angles may translate the centre of pressure laterally to the centre of mass of the tibia increasing the valgus moment. This may be understood as a dependent task strategy for side stepping to increase the foot width at initial contact, showing that foot positions may influence the kinetics and kinematics of proximal joints.[126,161] Despite speculating on the impact of the trunk on knee position, the position of the trunk was not analysed in their study.[160] Coronal plane hip biomechanics are not only affected by the task itself, but also by the situation in which the task is performed. Houck et al.[161] found that the unanticipated side-step movement was performed with greater hip adduction compared with the anticipated situation. However, the authors included male and female subjects within a single study group, thus, conclusions on sex differences are not possible. Imwalle et al.[162] investigated the lower-extremity motions in females also assessing the unanticipated cutting manoeuvres with running actions at an angle of 45 or 90. The authors found that hip adduction was the only significant predictor of knee abduction for both situations. Hip abduction torque differences between females and males have been observed in some studies,[49,114,157,163] but not in others.[113,164] Sex differences in hip abduction torques may explain ª 2011 Adis Data Information BV. All rights reserved.
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the higher injury incidence in females. Intervention strategies that target sex differences hip adduction torques (increasing hip abduction strength) may optimize ACL injury prevention programmes, specifically for female athletes.[148] It has yet to be definitively determined whether there is a relationship between hip abduction strength and lower-extremity valgus positioning. Proper functioning (strength and recruitment) of the posterior-lateral hip musculature is essential to provide proximal stability for lower-extremity motion during functional activities. Little to no correlation has been found between hip abduction torque[20,111,163,164] and gluteus medius activation[108,109] with knee valgus during different tasks. Measurement methods may explain these findings. Hip abductor strength is measured using isokinetic and hand-held dynamometer devices during open chain tasks, which differs from what occurs in athletic manoeuvres. Moreover, these studies did not control the influence of the trunk flexion in gluteus medius activation, which could influence the obtained results. Therefore, neuromuscular control of the hip in the coronal plane is required not only to stabilize the trunk and pelvis, but also the knee joint. In summary: Females and males have significantly different trunk and hip movements in the coronal plane during landing, squatting and side-step tasks. Specifically, females appear to exhibit movement patterns at the trunk that increase knee abduction. Studies indicate that abduction at the knee joint predicts risk for ACL injury. Deficits in neuromuscular control of the trunk and hip during cutting and landing may lead to uncontrolled lateral trunk motion. Targeted neuromuscular training of the trunk and hip to reduce movements that contribute knee abduction may decrease injury risk. 5. Transverse Plane Evidence for Proximal Control of Knee-Joint Stability 5.1 Trunk Contributions
Investigations about the influence of transverse plane movements on the risk of ACL injury Sports Med 2011; 41 (7)
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are scarce. Dempsey et al.[124] recently reported that placing the foot away from the midline while the trunk is leaning and rotating to the opposite direction to the cut significantly increased knee abduction and internal rotation loads at the knee in the weight acceptance phase. The rotation of the trunk transfers transverse plane motions to the hip through the pelvis, potentially producing hip adduction and internal rotation that may in turn induce knee abduction. These data coincide with the ‘position of no return’ described by Ireland[61] to explain a non-contact ACL injury mechanism and where Ireland warned against flexion and rotation to the opposite side of the trunk. In contrast, Blackburn and Padua[65] found no influence of trunk flexion at the hip and knee position in the transverse plane. No studies examining sex differences in the transverse plane trunk motions were found; therefore, further research is needed in this area. 5.2 Hip Contributions
Transverse plane hip contributions to knee biomechanics have been investigated in running, side-step cutting, and landing manoeuvres. Ferber et al.[151] reported significantly greater hip internal rotation angles and hip negative work in the transverse plane during running in female recreational athletes compared with males. However, Landry et al.[121] found that females produced a greater overall hip external rotation moment than did male subjects during the early stance phase of the unanticipated straight run. Position of the foot at initial contact may explain these contradictory data. The contribution of the hip musculature during side-step cutting is supported by findings of McLean et al.,[159] who showed that the peak knee abduction moment was more sensitive to initial hip internal rotation and knee abduction position (R = 0.76) in females compared with males. These findings are in agreement with those reported by Sigward and Powers[160] who found significantly greater hip internal rotation and greater internally rotated foot at initial contact in the excessive valgus moment compared with a normal valgus group during side-step cutting. ª 2011 Adis Data Information BV. All rights reserved.
During the same manoeuvre, Pollard et al.[149] reported that female athletes demonstrated significantly greater hip internal rotation angles at early deceleration compared with male athletes. In contrast, Landry et al.[121] reported that female subjects sustained a larger hip external rotation moment than male subjects during the early stance phase of an unanticipated side-cutting manoeuvre. However, the moment magnitudes were much smaller than the maximal moments reached later in midstance phase. It remains unclear if these moment differences at the smaller magnitudes during early stance serve as potential risk factors for ACL injury. For landing tasks, Lephart et al.[164] found that females exhibited significantly lower leg internal rotation maximum angular displacement for both single-leg landing and forward hop. Specifically, for the single-leg land, females had significantly greater hip internal rotation maximum angular displacement, and less lower leg internal rotation time to maximum angular displacement compared with males.[164] For the forward hop, females had significantly greater hip rotation time to maximum angular displacement than males.[164] Surprisingly, Pollard et al.[149] reported changes in the hip, but not in the knee, after in-season neuromuscular training. Interestingly, the authors demonstrated how hip internal rotation may be decreased after an adequate neuromuscular training, as they found 6.2 decreases in hip internal rotation and 2.8 greater hip abduction angles during the early deceleration phase of landing following the season, without differences in knee valgus and flexion angles. Although the authors did not assess sex differences in hip contributions to knee-joint motions, these results point out the relevance of prevention programmes to decrease the risk of ACL injury. During vertical stop jump tasks, Chappell et al.[123] found decreased hip external rotation and increased knee internal rotation angles in females compared with males at landing. In contrast, Nguyen[20] did not observe significantly greater hip internal excursion in females compared with males during a single-leg squat, although differences in the assessed task may explain differing results. Sex differences in hip or trunk contribution to knee-joint motions are likely task-dependent. Sports Med 2011; 41 (7)
Sex Differences in Proximal Control of the Knee Joint
The gluteus maximus and gluteus medius act synergistically to stabilize the pelvis in all planes of motion and control rotation at the hip, especially in single-leg stance. While the gluteus medius is the primary abductor of the hip, the gluteus maximus functions primarily as an extensor and, secondarily, as an external rotator of the hip. Decreased activation of proximal stabilizing muscles may lower load-bearing capacity of the knee joint and predispose it to injury. Zazulak et al.[108] found decreased gluteus maximus electromyographic activity at landing in female soccer, basketball and volleyball players compared with males. Gluteal muscles are able to change their functions depending on the hip position.[91] Therefore, it would be desirable to monitor and provide information about hip and trunk position when considering the activation of these musculatures. Females demonstrated decreased values in hip external rotation strength compared with males measured with a hand-held dynamometer.[49,165] In contrast, Claiborne et al.[111] did not find differences in hip musculature strength measured with isokinetics when normalized to body mass. Weakness or poor neuromuscular control in hip external rotators in females may increase the injury risk of the lower extremity, as reported by Leetun et al.[49] Core stability was used synonymously with isometric hip strength.[49] To affirm this contention, information and interrelation of all components involved in neuromuscular control of the core would be necessary. Lawrence et al.[165] studied hip external rotation strength on kinematic and kinetic variables during single-leg drop landings in females. The authors stratified the group of females according to ‘strong’ or ‘weak’ hip external rotation strength with a hand-held dynamometer. The ‘strong’ group demonstrated significantly lower peak vertical GRF and external knee flexor moment. The ‘weak’ group had significantly greater external knee adduction moment, net knee anterior shear joint reaction force and a greater hip external adduction moment. Therefore, this study demonstrated that hip strength may be related to high-risk landing strategies and highlights the importance of the hip external rotators at potentially preventing ACL ª 2011 Adis Data Information BV. All rights reserved.
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injuries.[165] However, caution must be taken when interpreting these results due to the limitations of hand-held dynamometry with open kinetic chain measurements. In summary: The rotation of the trunk transfers transverse plane motions to the hip through the pelvis, potentially producing hip adduction and internal rotation that may in turn induce knee abduction. There is minimal evidence examining sex differences in the transverse plane trunk motions. Peak knee abduction moment appears to be more sensitive to initial hip internal rotation and knee abduction position in females. Weakness or poor neuromuscular control in hip external rotators in females may increase the injury risk of the lower extremity. 6. Conclusions This review has focused on the contributions of proximal controllers of the trunk and hip- to knee-joint motions. Sex differences in the biomechanics of trunk and hip in sagittal, coronal and transverse planes have been identified and discussed. We have used this approach to better understand the neuromuscular imbalances and the higher incidence of ACL injury observed in female athletes. Considering the increased risk of radiographically diagnosed knee osteoarthritis following ACL injury, regardless of whether the ligament is reconstructed or not, prevention is currently the only effective treatment for this devastating athletic injury. Based on the presented evidence, the following conclusions can be generated regarding sex-based differences in the proximal control of the knee joint: The risk of ACL injury likely results from a combination of disturbances in all three planes of motion. Females may land with less trunk and hip flexion compared with males, which results in decreased energy absorption capacity of the musculoskeletal system. GRF (normalized) at landing may be higher in females compared with males. Greater reaction forces with the hip and knee flexion angles Sports Med 2011; 41 (7)
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near extension may overload the ACL and place it at high risk of injury. The lateral displacement of the trunk centre of mass away from the knee joint may increase knee valgus and can potentially increase ACL injury risk. Females may show greater hip adduction while performing sport manoeuvres (running, landing, squatting and cutting), which may increase knee valgus and hip internal rotation and place the ACL at increased risk of rupture. Hip strength training may decrease the risk of ACL injury by modifying high-risk positions about the knee. The influence of transverse plane trunk biomechanics on the knee joint needs to be further studied, as little evidence has been reported in the literature. Significantly greater hip internal rotation has been reported among females compared with males during running, side-step cutting and landing, and is related to knee abduction in female athletes. Proximal control of the knee joint is sex and task dependent. Prevention programmes targeted towards trunk and hip neuromuscular control may help decrease the risk of ACL injuries in athletes, especially female athletes.
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Acknowledgements The authors acknowledge funding support from National Institutes of Health/NIAMS Grants R01-AR049735, R01AR05563, R01-AR056259 and R03-AR057551. The authors have no conflicts of interest that are directly relevant to the content of this review.
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151. Ferber R, McClay Davis I, Williams III DS. Gender differences in lower extremity mechanics during running. Clin Biomech (Bristol, Avon) 2003 May; 18 (4): 350-7 152. Chumanov ES, Wall-Scheffler C, Heiderscheit BC. Gender differences in walking and running on level and inclined surfaces. Clin Biomech (Bristol, Avon) 2008 Dec; 23 (10): 1260-8 153. Ford KR, Myer GD, Smith RL, et al. A comparison of dynamic coronal plane excursion between matched male and female athletes when performing single leg landings. Clin Biomech 2006; 21 (1): 33-40 154. Pappas E, Hagins M, Sheikhzadeh A, et al. Biomechanical differences between unilateral and bilateral landings from a jump: gender differences. Clin J Sport Med 2007 Jul; 17 (4): 263-8 155. Hewett TE, Ford KR, Myer GD, et al. Gender differences in hip adduction motion and torque during a single leg agility maneuver. J Orthop Res 2006; 24 (3): 416-21 156. Jacobs CA, Uhl TL, Mattacola CG, et al. Hip abductor function and lower extremity landing kinematics: sex differences. J Athl Train 2007 Jan-Mar; 42 (1): 76-83 157. Padua DA, Marshall SW, Beutler AI, et al. Predictors of knee valgus angle during a jump-landing task. Med Sci Sports Exerc 2005; 37 (5): S398 158. Brophy RH, Chiaia TA, Maschi R, et al. The core and hip in soccer athletes compared by gender. Int J Sports Med 2009 Sep; 30 (9): 663-7 159. McLean SG, Huang X, van den Bogert AJ. Association between lower extremity posture at contact and peak knee valgus moment during sidestepping: implications for ACL
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Correspondence: Dr Timothy E. Hewett, PhD, The Ohio State University, 2050 Kenny Road, Suite 3100, Columbus, OH 43221-3502, USA. E-mail:
[email protected]
Sports Med 2011; 41 (7)
Sports Med 2011; 41 (7): 559-585 0112-1642/11/0007-0559/$49.95/0
REVIEW ARTICLE
ª 2011 Adis Data Information BV. All rights reserved.
Carbohydrate Ingestion during Team Games Exercise Current Knowledge and Areas for Future Investigation Shaun M. Phillips, John Sproule and Anthony P. Turner Institute of Sport, Physical Education and Health Studies, University of Edinburgh, Edinburgh, UK
Contents Abstract. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 559 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 560 2. Methodology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 561 3. Carbohydrate Supplementation Immediately before and during Prolonged Intermittent Exercise . 562 3.1 Early Laboratory Work . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 562 3.2 Team Game-Specific Laboratory and Field Work . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 564 3.3 Mental Function and Skill Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 568 3.4 Physiological and Metabolic Responses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 572 3.5 Summary. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 573 4. Mechanisms of Enhancement with Carbohydrate Supplementation during Prolonged Intermittent, High-Intensity Exercise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 573 4.1 Intermittent Exercise Capacity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 573 4.2 Sprint Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 574 4.3 Mental Function and Skill Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 575 5. Modulators of Carbohydrate Efficacy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 575 5.1 Fluid Volume and Solution Composition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 576 5.1.1 Fluid Volume . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 576 5.1.2 Carbohydrate Concentration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 576 5.1.3 Carbohydrate Composition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 576 5.1.4 Solution Osmolality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 577 5.1.5 Recommendations. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 577 5.2 Fluid and Carbohydrate Ingestion Pattern . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 577 5.3 Glycaemic Index of Pre-Exercise Meals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 578 5.4 Fluid Temperature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 578 5.5 Carbohydrate Mouthwash . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 579 5.6 Ambient Temperature. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 579 5.7 Populations. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 579 6. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 580
Abstract
There is a growing body of research on the influence of ingesting carbohydrate-electrolyte solutions immediately prior to and during prolonged intermittent, high-intensity exercise (team games exercise) designed to replicate field-based team games. This review presents the current body of knowledge in this area, and identifies avenues of further research. Almost all early work supported the ingestion of carbohydrate-electrolyte solutions during prolonged
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intermittent exercise, but was subject to methodological limitations. A key concern was the use of exercise protocols characterized by prolonged periods at the same exercise intensity, the lack of maximal- or high-intensity work components and long periods of seated recovery, which failed to replicate the activity pattern or physiological demand of team games exercise. The advent of protocols specifically designed to replicate the demands of field-based team games enabled a more externally valid assessment of the influence of carbohydrate ingestion during this form of exercise. Once again, the research overwhelmingly supports carbohydrate ingestion immediately prior to and during team games exercise for improving time to exhaustion during intermittent running. While the external validity of exhaustive exercise at fixed prescribed intensities as an assessment of exercise capacity during team games may appear questionable, these assessments should perhaps not be viewed as exhaustive exercise tests per se, but as indicators of the ability to maintain high-intensity exercise, which is a recognized marker of performance and fatigue during field-based team games. Possible mechanisms of exercise capacity enhancement include sparing of muscle glycogen, glycogen resynthesis during lowintensity exercise periods and attenuated effort perception during exercise. Most research fails to show improvements in sprint performance during team games exercise with carbohydrate ingestion, perhaps due to the lack of influence of carbohydrate on sprint performance when endogenous muscle glycogen concentration remains above a critical threshold of ~200 mmol/kg dry weight. Despite the increasing number of publications in this area, few studies have attempted to drive the research base forward by investigating potential modulators of carbohydrate efficacy during team games exercise, preventing the formulation of optimal carbohydrate intake guidelines. Potential modulators may be different from those during prolonged steady-state exercise due to the constantly changing exercise intensity and frequency, duration and intensity of rest intervals, potential for team games exercise to slow the rate of gastric emptying and the restricted access to carbohydrateelectrolyte solutions during many team games. This review highlights fluid volume, carbohydrate concentration, carbohydrate composition and solution osmolality; the glycaemic index of preexercise meals; fluid and carbohydrate ingestion patterns; fluid temperature; carbohydrate mouthwashes; carbohydrate supplementation in different ambient temperatures; and investigation of all of these areas in different subject populations as important avenues for future research to enable a more comprehensive understanding of carbohydrate ingestion during team games exercise.
1. Introduction The ergogenic effects of ingesting carbohydrateelectrolyte solutions prior to and during prolonged (‡45 min) moderate to. high-intensity (>75% maximal oxygen uptake [VO2max])[1] steady-state exercise (sub-maximal exercise requiring a constant power output and a stable heart rate [HR] and ª 2011 Adis Data Information BV. All rights reserved.
. oxygen uptake [VO2])[2] have been known for several decades.[1,3] During steady-state cycling, exogenous carbohydrate ingestion appears to maintain euglycaemia and high carbohydrate oxidation rates, and during steady-state running it has been demonstrated to reduce net muscle glycogen breakdown in type I muscle fibres.[1] Carbohydrate ingestion can improve both exercise performance, Sports Med 2011; 41 (7)
Carbohydrate and Team Games Exercise
defined as distance covered in a set time or the time to complete a set distance/amount of work,[4] and exercise capacity, defined as time to exhaustion at a fixed exercise intensity.[5] The mean whole-game exercise intensity during adult field-based team games (soccer, rugby and . field hockey) has been estimated at 70–80% VO2max, similar to prolonged steady-state exercise,[1,6] and appears sufficient to promote significant muscle glycogen depletion,[7] although this is not a consistent finding.[8] Muscle glycogen availability during prolonged intermittent, highintensity exercise (hereafter referred to as ‘team games exercise’) can influence work output, distance covered and sprinting frequency, particularly in the later stages of exercise.[7,9] Therefore, ingesting carbohydrate-electrolyte solutions during field-based team games may prove beneficial by attenuating performance decrements that can occur towards the end of a game. In their earlier review on fluid and carbohydrate replacement during intermittent exercise, Shi and Gisolfi[10] provided recommendations for the optimal carbohydrate concentration, composition and osmolality of a carbohydrate-electrolyte solution for use before and during team games exercise. Since this review, a large number of publications have specifically addressed the ingestion of carbohydrateelectrolyte solutions immediately prior to and during team games exercise, and an updated synthesis of current knowledge in this field is required. The aim of this review is to present the current state of knowledge on carbohydrate ingestion immediately prior to and during laboratory and field exercise typical of field-based team games. Suggestions are provided for further research that would increase knowledge in this area in both breadth and depth. 2. Methodology To locate articles focusing on the effect of carbohydrate supplementation on team games exercise performance and capacity, searches in MEDLINE (PubMed) were performed using the terms ‘carbohydrate prolonged intermittent exercise’, ‘carbohydrate intermittent exercise’, ‘carbohydrate team games’, ‘carbohydrate endurance ª 2011 Adis Data Information BV. All rights reserved.
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exercise’, ‘carbohydrate exercise capacity’ and ‘carbohydrate sprint performance’. For the influence of carbohydrate supplementation on mental function and skill performance, the following MEDLINE (PubMed) searches were performed: ‘carbohydrate skill team games’, ‘carbohydrate shooting passing performance’, ‘carbohydrate skill performance’, ‘carbohydrate mental function team games’, ‘carbohydrate cognitive function exercise’, ‘carbohydrate effort perception exercise’. The ‘related citations’ service in PubMed was explored for each highlighted abstract to locate additional relevant articles. The reference list of each article was also hand searched for other appropriate studies. These searches yielded a total of 36 articles for the influence of carbohydrate on team games exercise performance and capacity, and 25 articles for mental function and skill performance. Searches were not date limited, as the total research output in this area is manageable without using this limitation and the authors wanted to retrieve the earliest papers in the field. Only studies related to soccer, rugby and field hockey were incorporated, leading to the exclusion of 27 articles. Studies using additional supplementations (i.e. carbohydrate with caffeine, carbohydrate with protein) that did not include a direct comparison between a carbohydrateelectrolyte solution and a placebo solution were excluded. Discussion of these articles would have shifted the focus of the review, which is solely on the effect of carbohydrate supplementation. Using this exclusion criterion, four articles were removed. This review focuses on the acute effects of carbohydrate supplementation in team games; therefore, studies that supplemented the first bolus of carbohydrate >1 hour prior to the start of exercise were discounted. As a result, three articles were removed. Articles investigating the influence of carbohydrate on immune function during team games exercise were incorporated into the discussion of the physiological and metabolic responses to team games exercise with carbohydrate supplementation, but the influence on immune function was not discussed. A sufficiently in-depth review of this literature is outside the aims of this article. Based on these criteria, a total of 21 articles were included in the discussion Sports Med 2011; 41 (7)
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of team games exercise performance and capacity, and 11 in the discussion of mental function and skill performance. 3. Carbohydrate Supplementation Immediately before and during Prolonged Intermittent Exercise The following sections discuss early research that supplemented carbohydrate during prolonged intermittent exercise atypical of team games activity, followed by the more recent body of work that attempted to utilize team games-specific protocols and practices. The influence of carbohydrate supplementation on mental function and skill performance, and on physiological and metabolic responses during team games exercise is also discussed. 3.1 Early Laboratory Work
All studies in this section were placebo controlled and are summarized in table I. This initial body of work demonstrated that (i) consuming carbohydrate-electrolyte solutions during prolonged intermittent exercise can significantly improve exercise performance and capacity; (ii) consuming carbohydrate-electrolyte solutions may significantly attenuate muscle glycogen utilization during prolonged intermittent exercise; (iii) solid carbohydrate is not significantly different from a carbohydrate-electrolyte solution in improving intermittent exercise capacity; and (iv) the efficacy of carbohydrate-electrolyte solutions during prolonged intermittent exercise may be influenced by the intensities at which exercise is performed. However, prevalent methodological issues must be discussed prior to interpreting these conclusions. Murray et al.[11] and Coggan and Coyle[12] were among the first to study the effects of carbohydrate supplementation during prolonged intermittent exercise. It is unclear why Murray et al.[11] conducted their study in a high ambient temperature. A thermoneutral trial should have been included for comparison due to the possibility of increased glycogen breakdown in high ambient temperatures.[16-18] Although both protocols were intermittent, neither was consistent with the activity pattern or physiological demand of intermitª 2011 Adis Data Information BV. All rights reserved.
tent exercise ‘in the field’ due to the nature of the recovery provided, the lack of a maximal- or highintensity component, the structured and prolonged duration of the workloads and the use of a cycle ergometer. However, at this early stage of study, the authors may have been more concerned with establishing a baseline of data using controlled research designs rather than maximizing external validity. Research by Murray et al.[13] and Yaspelkis et al.,[14] while again supporting carbohydrate supplementation, is subject to similar methodological issues. The regimented and specifically timed exercise intensities, with no maximal work and long periods of seated recovery, did not accurately reflect the physiological demand of team games. Additionally, exercise performance and capacity was assessed using steady-state rather than intermittent exercise. Yaspelkis et al.[14] did not provide body mass (BM)-standardized volumes of the carbohydrate or placebo solutions, meaning subjects of lower BM received a larger relative carbohydrate intake. Furthermore, muscle biopsy data were not collected during the solid carbohydrate trial, preventing full data interpretation and hindering the ability to understand the mechanisms behind the improvement in exercise capacity. The lack of improvement in intermittent exercise capacity with carbohydrate supplementation shown by Nassis et al.[15] is in contrast with the literature discussed to this point. As the authors stated, the protocol probably made large demands on muscle glycogen stores; therefore, it would be expected that carbohydrate ingestion would have improved exercise capacity. However, while the volume of fluid ingested during exercise was similar to most related studies (2 mL/kg BM), the lower pre-exercise bolus (3 mL/kg BM) facilitated a lower overall carbohydrate intake during the protocol than most related work. The total amount of carbohydrate ingested during the trial (~36 g/hour) was above the minimum intake of 16 g/hour that is required for performance enhancement,[1] but was notably lower than the recommended intake for maximizing carbohydrate delivery (60–70 g/hour).[19] Furthermore, the lower volume of fluid entering the stomach may have Sports Med 2011; 41 (7)
No. of subjects and training level
Protocol
Supplementation
Significant findings
Limitations
Murray et al.[11]
13 untrained
5 · 15 min cycle at 55–65% . VO2max, 480 rev TT (33C)
5% glucose polymer solution 6% glucose/fructose solution 7% glucose polymer/fructose solution 2 mL/kg BM during each recovery period
Similar physiological function between trials Significantly faster TT with 6% and 7% solutions
No thermoneutral trial Design of study protocol is not externally valid to demands of team sports training or competition
Coggan and Coyle[12]
7 endurancetrained cyclists
Alternating 15 min cycle at . 65% and ~85% VO2max to exhaustion
50% CHO (1 g/kg BM) solution at 10 min, 20% CHO (0.6 g/kg BM) solution every 30 min thereafter
Significantly higher intensity during third h of exercise 18% longer time to fatigue 19% more work completed
Design of study protocol is not externally valid to demands of team sports training or competition
Murray et al.[13]
12 (5 F) untrained
3 · 20 min cycle at 65% . VO2max, 1200 rev TT
6%, 8% and 10% sucrose solution 2.5 mL/kg BM before exercise and during each recovery
Similar physiological function between trials Significantly faster TT with 6% solution
Design of study protocol is not externally valid to demands of team sports training or competition
Yaspelkis et al.[14]
7 endurancetrained cyclists
3.3 h intermittent (45–80% . VO2max) cycle: . 30 min at 45% VO2max 6 · 16 min (8 min at 75%, . 8 min at 45% VO2max) 12 min seated rest 5 min at 45%, 5 min at 60% . VO2max 9 · 6 min (3 min at 75%, . 3 min at 45% VO2max) 12 min seated rest . cycle at 80% VO2max to exhaustion
Two trials: 180 mL of 10% CHO polymer solution every 20 min 25 g CHO bar every 30 min
Significantly reduced muscle glycogen use with CHO solution Significant increase in time to exhaustion in both trials No difference between liquid and solid CHO
Design of study protocol is not externally valid to demands of team sports training or competition Solutions not standardized to BM Muscle biopsies not taken during solid CHO trial
Nassis et al.[15]
9 endurancetrained runners
Repeated 15 sec run at 80% . VO2max for 60 min, 85% . VO2max for 60–100 min, . 90% VO2max from 100 min to exhaustion, separated by 10 sec slow running
6.9% CHO-E solution 3 mL/kg BM prior to exercise 2 mL/kg BM every 20 min during exercise
Similar physiological function between trials No difference in time to exhaustion
Design of study protocol is not externally valid to demands of team sports training or competition Volume of CHO ingested may be insufficient for improving exercise capacity Intensity of exercise during final period of exercise may have been too intense
a
All studies were placebo controlled. . BM = body mass; CHO-E = CHO-electrolyte; F = females; rev = revolutions; TT = time trial; VO2max = maximal oxygen uptake.
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Table I. Summary of early laboratory studies on the effects of carbohydrate (CHO) supplementation immediately before and during prolonged intermittent exercise on the exercise performance and capacity of adultsa
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resulted in a suboptimal rate of gastric emptying (GE), possibly further attenuating the delivery of carbohydrate to the intestine. Therefore, carbohydrate may not have been systemically present in sufficient amounts to alter metabolism. This is supported by no significant between-trials difference in blood glucose concentration (with the exception of one timepoint), blood lactate concentration or respiratory exchange ratio (RER). However, due to the variable intensities of the protocol, RER may not have been a valid method of assessing metabolism. Buffering of H+ ions produced during the high-intensity periods of the protocol leads to greater production of CO2 requiring removal at the lungs, thereby over-inflating RER.[15] It is also possible that the exercise . intensity in the final part of the protocol (90% VO2max) was too intense, possibly causing fatigue to occur as a result of factors other than glycogen availability, such as phosphocreatine depletion.[20,21] If so, this negates the goal of the study and may help to explain the result being somewhat out of step with other research in the area. 3.2 Team Game-Specific Laboratory and Field Work
All studies discussed in this section are summarized in table II. Leatt and Jacobs[22] attempted to expand the research base by investigating, for the first time, the effect of carbohydrate ingestion on muscle glycogen depletion during an exhibition soccer match. Unfortunately, in an independent study design comprising two groups, only five subjects per group were used, placing the rigour of any statistical analyses under question. The authors attempted to control the between-groups physical demand of the game by using players from the same positions on the field. However, significant variations in exercise intensity and distance covered and, hence, muscle glycogen utilization, could have occurred between groups due to factors including team tactics, the activity profile of the opposing team[37] and the score in the game. This could have influenced the reported efficacy of the carbohydrateelectrolyte solution. However, Leatt and Jacobs[22] attempted to control the influence of team tactics ª 2011 Adis Data Information BV. All rights reserved.
and activity profile by analysing an intra-squad match. A time-motion analysis of each player would have been useful to confirm the physical demand experienced. Solutions were administered in a single-blind fashion, suggesting the potential for experimenter bias. However, the investigators had no direct contact with subjects during the match. All subjects consumed 0.5 L of the carbohydrate (containing 35 g carbohydrate) or placebo solution rather than a volume matched to individual BM. The authors stated that post-match blood samples and muscle biopsies were taken within 20 minutes and 45 minutes of the match ending, respectively. If these tests were administered at different times between subjects, the reliability of the results could have been affected due to intersubject differences in lactate dynamics[38] and the onset of rapid glycogen resynthesis, particularly in the carbohydrate group.[39,40] While this may be speculative, it would have been beneficial to standardize these measurements. It may also have been prudent to collect some performance measures during the match to investigate whether glycogen sparing in the carbohydrate trial facilitated any improvement or maintenance of performance compared with placebo. In a defining study, Nicholas et al.[23] demonstrated, for the first time, a 33% improvement in intermittent exercise capacity when a carbohydrateelectrolyte solution was consumed immediately prior to and during the Loughborough Intermittent Shuttle Test (LIST), a protocol specifically designed to replicate the physiological demand of soccer.[41] Carbohydrate supplementation did not significantly improve sprint performance during the protocol. Solutions were prescribed relative to BM and in a double-blind, counterbalanced fashion, ensuring equal fluid and carbohydrate (0.90 g/kg BM) intake across all subjects. These strengths are in direct comparison to the issues highlighted in section 3.1. Most subsequent research investigating carbohydrate supplementation during team games exercise employed the LIST protocol or a slight modification of it. Almost without exception, this research demonstrates that carbohydrate supplementation improves intermittent exercise capacity[24,26,27,30,32,33] or promotes physiological Sports Med 2011; 41 (7)
No. of subjects and training level
Protocol
Supplementation
Significant findings
Limitations
Leatt and Jacobs[22]
10 highly trained soccer players
90 min outdoor friendly soccer match, 10 min interval Treatment (n = 5) and PLA (n = 5) group
7% glucose polymer solution 0.5 L ~10 min before match and at half-time
~39% reduction in muscle glycogen use with CHO ingestion
Low subject numbers Single-blind design Solutions not standardized to BM Variable timing of post-match blood and muscle samples No performance measurements made
Nicholas et al.[23]
9 trained games players
Standard LIST Double-blind design
6.9% CHO-E solution 5 mL/kg BM prior to exercise 2 mL/kg BM every 15 min during exercise
33% longer time to exhaustion Sprint performance unchanged
No notable limitations
Davis et al.[24]
10 active
Standard LIST Double-blind design
20% CHO solution 20% CHO + BCAA solution 5 mL/kg BM 1 h and 10 min before exercise 2 mL/kg BM every 15 min during exercise (CHO only)
Significant increase in time to exhaustion (52% CHO, 42% CHO + BCAA) No difference between treatments
Sprint performance not assessed
Nicholas et al.[25]
6 trained games players
Extended LIST (part A only, 90 min duration)
6.9% CHO-E solution 5 mL/kg BM prior to exercise 2 mL/kg BM every 15 min during exercise
Sprint performance unchanged 22% reduction in muscle glycogen use
Exercise capacity not assessed Blinding procedures used were not stated
Davis et al.[26]
8 active
Standard LIST Double-blind design
6% CHO-E solution 5 mL/kg BM 10 min before exercise 2 mL/kg BM every 15 min during exercise
32% longer time to exhaustion
Sprint performance not assessed
Welsh et al.[27]
10 (5 F) trained games players
Modified LIST: 4 · modified part A, with a 20 min recovery between the second and third set Modified part A: 3 · 20 m walking 2 vertical jumps at 80% maximum height 1 · 20 m sprint . 3 · 20 m run at 120% VO2max 2 vertical jumps at 80% maximum height
18% and 6% CHO-E solution 5 mL/kg BM prior to exercise 3 mL/kg BM every 15 min (6% only) 5 mL/kg BM at half-time (18% only)
37% longer time to exhaustion Significantly faster sprint performance during final 15 min Similar physiological function between trials
No validity or reliability testing of modified LIST protocol
Continued next page
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Table II. Summary of team games-specific laboratory and field studies on the effects of carbohydrate (CHO) supplementation immediately before and during team games exercise on the intermittent exercise performance and capacity of adultsa
Study
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Table II. Contd No. of subjects and training level
Protocol
Supplementation
Significant findings
Limitations
. 3 · 20 m jogging at 55% VO2max Double-blind design Motor skill, jumping, cognitive and emotion tests undertaken before, during, and after protocol 9 active
Modified LIST in 30C heat: 5 · part A, followed by 60 sec run/60 sec rest until exhaustion
6.5% CHO-E solution 6.5 mL/kg BM prior to exercise 4.5 mL/kg BM every 15 min during exercise
No difference in sprint performance or time to exhaustion Similar physiological function between trials
Subjects were not acclimatized to exercise in the heat An order effect was reported for distance run Very low number of subjects completed the protocol Blinding procedures used were not stated
Winnick et al.[28]
20 (10 F) active
Modified LIST: 4 · 15 min modified part A, 5 min interval after set 1 and 3, 20 min interval after set 2 Modified part A, see Welsh et al.[27] Double-blind design Motor skill, jumping, force sensation, cognitive and emotion tests undertaken before, during and after protocol
6% CHO-E solution 5 mL/kg BM prior to exercise and at beginning of 20 min interval 3 mL/kg BM beginning of each 5 min interval, 10 min into 20 min interval, and immediately after fourth set
Significantly faster sprint performance during final 15 min Similar physiological function between trials
No validity or reliability testing of modified LIST protocol
Ali et al.[29]
16 trained games players
Extended LIST (part A only, 90 min duration) following glycogen-depleting exercise Shooting and passing tests undertaken before and after exercise
6.4% CHO-E solution 5 mL/kg BM prior to exercise 2 mL/kg BM every 15 min during exercise
Significantly faster mean sprint performance during protocol
Exercise capacity was not assessed Blinding procedures used were not stated
Patterson and Gray[30]
7 trained games players
Standard LIST Double-blind design
CHO gel 0.89 mL/kg BM prior to exercise 0.35 mL/kg BM every 15 min during exercise
45% longer time to exhaustion Similar physiological function between trials
CHO gel was compared with a PLA solution, rather than a PLA gel
Continued next page
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Sports Med 2011; 41 (7)
Morris et al.[18]
No. of subjects and training level
Protocol
Supplementation
Significant findings
Limitations
Clarke et al.[31]
12 trained games players
Soccer-specific motorized treadmill protocol (2 · 45 min with 15 min recovery)
6.9% CHO-E solution 7 mL/kg BM prior to exercise and during recovery (trial 1) Same total volume as trial 1 at 15 min intervals (trial 2)
Similar physiological function and metabolic response between trials Significant attenuation in gut fullness in trial 2
No performance variables measured
Davison et al.[32]
10 untrained
Modified LIST: Part A for 60 min followed by incremental run to exhaustion Double-blind design
6% CHO-E solution 8 mL/kg BM 15 min before exercise
8% longer time to exhaustion
CHO was not ingested during exercise
Foskett et al.[33]
6 active games players
Modified LIST: Part A for 90 min, and then continuously to exhaustion Double-blind design
6.4% CHO-E solution 8 mL/kg BM prior to exercise 3 mL/kg BM every 15 min during exercise
21% longer time to exhaustion Sprint performance unchanged Similar physiological function between trials
Low subject number
Abbey and Rankin[34]
10 trained games players
5 · 15 min intermittent exercise: . 2 · 55 m jogging at 55% VO2max 2 · 55 m running at 120% . VO2max 2 · 55 m walking 4 · 55 m sprinting Agility and shooting tests performed during exercise
6% CHO-E solution 8.8 mL/kg BM 30 min prior to exercise and at half-time
No difference in time to exhaustion No difference in sprint performance
CHO intake regimen may not have enabled performance improvement CHO availability may not have been a limiting factor in CHO or PLA trial Blinding procedures used were not stated
Ali and Williams[35]
17 trained games players
Extended LIST (part A only, 90 min duration) following glycogen-depleting exercise Passing test performed before, every 15 min during and after exercise
6.4% CHO-E solution 8 mL/kg BM prior to exercise 3 mL/kg BM every 15 min during exercise
No difference in sprint performance Similar physiological function between trials
Exercise capacity was not assessed Blinding procedures used were not stated
Roberts et al.[36]
8 trained games players
BURST test
9% CHO-E solution 1 h before exercise and 21, 46, and 77 min during exercise Volume ingested: 1.2 g/kg BM/h
No difference in sprint performance Similar physiological function between trials
Protocol design based on activity profile data of Rugby Union forwards only Blinding procedures used were not stated
a
All studies were PLA controlled.
BCAA = branched-chain amino acids; BM . = body mass; BURST = Bath University Rugby Shuttle Test; CHO-E = carbohydrate-electrolyte; F = females; LIST = Loughborough Intermittent Shuttle Test; PLA = placebo; VO2max = maximal oxygen uptake.
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Table II. Contd
568
and metabolic alterations that infer greater performance and/or capacity.[25,31] Improvements in intermittent exercise capacity with carbohydrate ingestion during part B of the non-modified LIST range between 32% and 52%, with effect sizes ranging from d = 0.44–2.69.[23,24,26,30] The validity of this performance measure should be considered, as team games athletes are rarely required to continue running to exhaustion during training or competition. However, the intermittent run to exhaustion should perhaps not be viewed as an exhaustive exercise test per se, but rather as an assessment of the ability to maintain high-intensity exercise, which is a recognized marker of performance and fatigue during field-based team games.[37] Despite this, the fixed workloads of most team games protocols (e.g. part A of the LIST protocol) do not permit the subject to alter their work rate; therefore, the influence of carbohydrate on self-governed work rate during team games exercise cannot be quantified. Future protocols, such as that proposed by Ali et al.[42] should address this. The influence of carbohydrate supplementation on sprint performance during team games exercise is contentious, with only three studies showing any form of improvement[27-29] (see section 4.2). Abbey and Rankin[34] found no effect of carbohydrate supplementation on exercise performance or capacity during a team games protocol. However, the different protocol and tests of sprint performance and exercise capacity from those discussed above, along with less frequent carbohydrate ingestion, may help to explain this. Morris et al.[18] found no performance or capacity benefits with carbohydrate ingestion during a slightly modified LIST in 30C heat. Lack of performance enhancement was attributed to carbohydrate availability not being a limiting factor in the unacclimatized subjects. As the authors must have recognized this prior to the study, it raises the question of why they failed to account for it by, for example, acclimatizing the subjects. The rate of rise in rectal temperature was greatest in the carbohydrate and placebo trials compared with the flavoured water trial. The authors suggested this was indicative of greater thermal strain due to impaired fluid delivery with ingestion of the carbohydrate-electrolyte solution. However, this ª 2011 Adis Data Information BV. All rights reserved.
Phillips et al.
is confused when it is noted that mean rectal temperature at the end of the protocol was not significantly different between the three trials. Furthermore, impaired fluid delivery with carbohydrate ingestion is dependent on multiple factors that were not measured in this study (section 5.1), and this does not explain the similar rate of rise in rectal temperature in the placebo trial. An order effect was reported for the total distance run (19% increase in trial 3 compared with trial 1), despite a randomized and counterbalanced approach to trial ordering. This may reflect a learning and/or, possibly, an acclimatization effect across the three trials. Finally, only four of the nine subjects completed the full protocol in the flavoured water trial, three in the placebo trial and only one in the carbohydrate trial. This invalidates any statistical tests carried out on the data. As a result of these issues, the findings of this study should be interpreted with extreme caution. 3.3 Mental Function and Skill Performance
All studies in this section are summarized in table III. Carbohydrate intake during team games exercise has been associated with significantly better maintenance of whole-body motor skills and mood state,[27,28] and reduced perception of exertion,[29] fatigue[27] and force production[28] in the latter stages of exercise. Carbohydrate intake does not appear to influence cognitive function during team games exercise.[27,28] Roberts et al.[36] found no influence of carbohydrate on the same motor skills test used by Welsh et al.[27] and Winnick et al.[28] and attributed this to the different protocol used in their study. The lack of influence of carbohydrate on agility in the study of Abbey and Rankin[34] may have been due to carbohydrate not being a limiting factor in the exercise protocol. Findings on the influence of carbohydrate on mental function during exercise may be influenced by the assessment procedure used, with Backhouse et al.[46] suggesting the Profile of Mood States test may not be sensitive enough to detect treatment effects on psychological responses to exercise. Using the Felt Arousal Scale, a subjective measure of perceived arousal, the authors demonstrated a significantly better maintenance of perceived arousal Sports Med 2011; 41 (7)
No. of subjects and training level
Protocol
Supplementation
Significant findings
Limitations
Zeederberg et al.[43]
22 trained games players
90 min outdoor competitive soccer game Tackling, heading, dribbling, shooting, passing and ball control performance recorded throughout game
6.9% CHO-E solution 5 mL/kg BM 15 min prior to match and at half-time
No significant effect on tackling, heading, dribbling, shooting, passing or ball control ability
Confounding factors associated with soccer performance in the field Blinding procedures used were not stated
Northcott et al.[44]
10 active games players
90 min circuit designed to replicate soccer, 15 min interval Passing and shooting tests undertaken every 15 min during protocol
8% CHO-E solution 8 mL/kg BM 15 min prior to exercise and at half-time
Significantly better maintenance of passing and shooting performance in last 15 min of exercise
No validity or reliability data regarding the exercise protocol, shooting or passing tests Blinding procedures used were not stated
Ostojic and Mazic[45]
22 trained games players
90 min outdoor soccer match, 15 min interval. Treatment (n = 11) and PLA (n = 11) group Dribbling, precision, coordination and power tests undertaken after the match
7% CHO-E solution 5 mL/kg BM immediately prior to match 2 mL/kg BM every 15 min during match
Significant improvement in dribbling performance and precision scores No difference in coordination or power
Confounding factors associated with soccer performance in the field Blinding procedures used were not stated Skill measures only taken after soccer match
Welsh et al.[27]
10 (5 F) trained games players
Modified LIST: 4 · modified part A, with a 20 min recovery between the second and third set Modified part A: 3 · 20 m walking 2 vertical jumps at 80% maximum height 1 · 20 m sprint . 3 · 20 m run at 120% VO2max 2 vertical jumps at 80% maximum height . 3 · 20 m jogging at 55% VO2max Double-blind design Motor skill (hopscotch), jumping, cognitive (SCWT) and mood (POMS) tests undertaken before, during and after protocol
18% and 6% CHO-E solution 5 mL/kg BM prior to exercise 3 mL/kg BM every 15 min (6% only) 5 mL/kg BM at half-time (18% only)
Significantly better maintenance of motor skill in last 15 min Significantly lower sensation of fatigue at exhaustion No difference in cognitive function
No validity or reliability testing of modified LIST protocol
Continued next page
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Table III. Summary of team game-specific laboratory and field studies on the effects of carbohydrate (CHO) supplementation immediately before and during team games exercise on mental function and skill performance in adultsa
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ª 2011 Adis Data Information BV. All rights reserved.
Table III. Contd No. of subjects and training level
Protocol
Supplementation
Significant findings
Limitations
Winnick et al.[28]
20 (10 F) active games players
Modified LIST: 4 · 15 min modified part A, 5 min interval after set 1 and 3, 20 min interval after set 2 Modified part A, see Welsh et al.[27] Double-blind design Motor skill (hopscotch), jumping, force sensation (perception of force at wrist extensors), cognitive (SCWT) and mood (external POMS) tests undertaken before, during and after protocol
6% CHO-E solution 5 mL/kg BM prior to exercise and at beginning of 20 min interval 3 mL/kg BM beginning of each 5 min interval, 10 min into 20 min interval and immediately after fourth set
Significantly better motor skills during final 30 min Significantly improved mood during final 15 min Significantly reduced force sensation No influence on cognitive function
No validity or reliability testing of modified LIST protocol
Ali et al.[29]
16 trained games players
Extended LIST (part A only, 90 min duration) following glycogen-depleting exercise LSST and LSPT undertaken before and after exercise
6.4% CHO-E solution 5 mL/kg BM prior to exercise 2 mL/kg BM every 15 min during exercise
Significant reduction in RPE during final 15 min of exercise Significantly better maintenance of shooting performance No difference in passing performance
Blinding procedures used were not stated
Backhouse et al.[46]
17 trained games players
Extended LIST (part A only, 90 min duration) Measures of pleasure-displeasure (scale) and perceived arousal (felt arousal sale) recorded throughout exercise
6.4% CHO-E solution 8 mL/kg BM prior to exercise 3 mL/kg BM every 15 min during exercise
Significantly greater perceived activation in last 30 min Trend for attenuation of RPE in last 30 min of exercise
Blinding procedures used were not stated No performance measures were made
Abbey and Rankin[34]
10 trained games players
5 · 15 min intermittent exercise: . 2 · 55 m jogging at 55% VO2max . 2 · 55 m running at 120% VO2max 2 · 55 m walking 4 · 55 m sprinting Agility and shooting tests performed during exercise
6% CHO-E solution 8.8 mL/kg BM 30 min prior to exercise and at half-time
No significant difference in agility No significant difference in passing performance
CHO intake regimen may not have enabled performance improvement CHO availability may not have been a limiting factor in CHO or PLA trial Blinding procedures used were not stated
Ali and Williams[35]
17 trained games players
Extended LIST (part A only, 90 min duration) following glycogen-depleting exercise LSPT performed before, every 15 min during and after exercise
6.4% CHO-E solution 8 mL/kg BM prior to exercise 3 mL/kg BM every 15 min during exercise
No difference in passing performance
Blinding procedures used were not stated
Continued next page
Phillips et al.
Sports Med 2011; 41 (7)
Study
All studies were PLA controlled. a
8 trained games players Roberts et al.[36]
ª 2011 Adis Data Information BV. All rights reserved.
BM = body mass; BURST = Bath University Rugby Shuttle Test; CHO-E = carbohydrate electrolyte; F = females; LIST = Loughborough Intermittent Shuttle Test; LSPT = Loughborough Soccer. Passing Test; LSST = Loughborough Soccer Shooting Test; PLA = placebo; POMS = Profile of Mood States; RPE = rating of perceived exertion; SCWT = Stroop Colour Word Test; VO2max = maximal oxygen uptake.
9% CHO-E solution 1 h before exercise and 21, 46 and 77 min during exercise Volume ingested: 1.2 g/kg BM/h
No different in motor skills throughout protocol
Protocol design based on activity profile data of Rugby Union forwards only Blinding procedures used were not stated
571
BURST test Motor skill (hopscotch) test performed before, during and after exercise
Blinding procedures used were not stated Significant improvement in dribbling, agility and shooting performance No significant difference in heading performance 7.5% CHO-E solution 6 mL/kg BM 30 min prior to exercise 4 mL/kg BM at half-time 1 mL/kg BM every 12 min during exercise 11 trained games players Currell et al.[47]
10 · 6 min exercise: 10 sec walk, 10 sec jog, 10 sec cruise, 10 sec jog, 10 sec cruise, 15 sec walk, 5 sec sprint, 15 sec jog, 5 sec sprint Exercise pattern repeated four times per 6 min exercise block Tests of agility, dribbling, kicking and heading performed during exercise
No. of subjects and training level Study
Table III. Contd
Protocol
Supplementation
Significant findings
Limitations
Carbohydrate and Team Games Exercise
during the final 30 minutes of the LIST with carbohydrate ingestion, along with a non-significant attenuation in the rating of perceived exertion (RPE). Exercise performance and capacity were not assessed, making it impossible to observe whether increased arousal influenced these measures. Zeederberg et al.[43] found no effect of a carbohydrate-electrolyte solution on aspects of skill performance in two teams during two outdoor soccer matches. The ability to successfully complete these actions was determined according to set criteria defined by the authors. For example, passing performance was governed by the criterion ‘‘a player kicks the ball to a team-mate without interception by the opposition or over the sideline for a defensive clearance.’’ This does not account for the possibility that the player miskicked the ball (e.g. in attempting a shot on goal and the ball happened to reach a team-mate). It also does not quantify the quality of the pass, which may have been successful due to poor positioning of the opposition players rather than passing accuracy. Hypoglycaemia may inhibit performance of skills requiring sensory-visual information, small and precise postural changes and tactical thinking and inter-player cooperation,[29,43] providing a rationale for carbohydrate ingestion to improve skill performance. However, the absence of post-match hypoglycaemia in either trial in the Zeederberg et al.[43] study suggests carbohydrate availability was not an issue, possibly negating the requirement for carbohydrate ingestion. The conflicting results reported by Ostojic and Mazic[45] (table III) may be due to differences in the tests administered or the degree of test familiarization the subjects were given. Additionally, Ostojic and Mazic[45] conducted their tests after a soccer match, and therefore presented no evidence that carbohydrate ingestion modulated skill aspects during soccer. As both studies were conducted in the field, the extraneous factors that can affect field-based soccer performance (section 3.2) could have also influenced the measures of skill in both studies.[29] Northcott et al.[44] found a significantly better maintenance of passing and shooting performance with carbohydrate ingestion. However, no information was provided on the validity or reliability of the shooting and passing tests, or the exercise Sports Med 2011; 41 (7)
Phillips et al.
572
protocol. Distance covered increased significantly during the first and second 45-minute periods of the protocol in the carbohydrate trial. This may have been independent of the solution consumed, possibly representing a protocol reliability issue. The recent development and validation of specific laboratory tests of soccer shooting accuracy and passing performance[48] has enabled a more objective quantification of the influence of carbohydrate supplementation on these variables. Carbohydrate ingestion before and during team games exercise has been demonstrated to significantly improve or maintain shooting accuracy in glycogen depleted[29] and non-glycogen depleted[47] subjects, with no significant influence on passing performance.[29,34,35] However, the observation that the performance of a dribbling test is significantly better maintained during the last 30 minutes of the LIST when a non-carbohydrate fluid is consumed compared with no fluid ingestion,[49] suggests that the relative influence of fluid and carbohydrate intake on skill performance in team games should be quantified. This will determine whether one is more important than the other with regard to skill performance, and whether an additive effect is evident when fluid and carbohydrate are co-ingested. 3.4 Physiological and Metabolic Responses
Ingestion of carbohydrate-electrolyte solutions does not appear to directly influence . VO2, HR, core temperature (Tcore), plasma volume (PV) or fluid loss during team games exercise.[11,13-15,22-25,27-29,31,35,36,43,45,46,50] Some authors have reported a significantly lower HR throughout exercise with carbohydrate ingestion,[24,26] attributed to a trend for better maintenance of PV. However, other work has reported non-significantly greater PV losses with carbohydrate supplementation without a significant alteration in HR response.[23] Yaspelkis et al.[14] reported a significantly higher HR at exhaustion with carbohydrate supplementation, which may reflect an increased ability to continue exercise due to carbohydrate-mediated central and/or peripheral alterations (section 4.1). The significantly . higher VO2 with carbohydrate supplementation ª 2011 Adis Data Information BV. All rights reserved.
reported by Ali et al.[29] and Coggan and Coyle[12] could relate to an augmented work rate (section 4.2). Ostojic and Mazic[45] found a significantly lower BM loss after a soccer match, attributed to larger sweat and urine losses in the placebo trial. However, sweat rate and urine loss were not measured in the study. Furthermore, the limitations associated with using BM loss as a measure of hydration status should be considered.[51] Extraneous factors associated with conducting the study in the field, such as possible differences in exercise intensity both within and between teams, as well as differences in the timing of BM measurement between players before, during and after the match, may also have contributed to the different BM losses, independent of carbohydrate intake. Carbohydrate ingestion alters the metabolic response to team games exercise, with a significant increase in blood glucose concentration found either periodically,[11,12,14,15,23,26,29,31,33,35,36,46,50,52] or throughout exercise.[13,24,45] Studies that have not recorded increased blood glucose concentration may have been hampered by infrequent blood sampling opportunities[22,43] or a small sample size.[25] Significant increases in blood insulin concentration may also occur with carbohydrate supplementation,[12,14,31,33] but this is not consistently observed. Significantly greater carbohydrate oxidation rates are recorded with carbohydrate ingestion,[12,14,29,31,35] along with a strong trend for attenuated blood free fatty acid (FFA) levels[12,14,24,26,31,33,35] and fat oxidation rates,[31,35] although this is not consistent.[23,25,29,36,45] Nassis et al.[15] found no increase in carbohydrate oxidation rates with carbohydrate intake, but this may be due to protocol issues (section 3.1). RER appears to be significantly higher during prolonged intermittent exercise when carbohydrate is ingested.[12-14] Ali et al.[29] did not find a between-trials difference in RER during the LIST, despite a higher rate of carbohydrate oxidation in the carbohydrate trial. This highlights the issues associated with using RER to quantify metabolic responses to intermittent exercise (section 3.1). The blood lactate response to prolonged intermittent exercise is largely unaffected by carbohydrate ingestion,[11-13,23,24,26,27,29,33,35,36,45] except Sports Med 2011; 41 (7)
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at exhaustion, where it has been reported to be significantly higher.[14,15] This may reflect the ability to continue exercising to a higher intensity, as previously discussed in this section and section 4.1. However, if this is the case, blood lactate concentration is not a reliable marker of this phenomenon, as numerous studies have described enhanced intermittent exercise capacity without a significant increase in blood lactate concentration. It is also worth noting that blood lactate concentration only reflects activities undertaken a few minutes prior to sampling, and the balance between lactate movement into and out of the blood.[53,54] 3.5 Summary
Early research was almost unanimous in supporting the consumption of carbohydrate-electrolyte solutions during prolonged intermittent exercise for maintaining and/or improving exercise performance and capacity. However, the studies presented significant methodological concerns that limit their applicability to actual team games. A key concern is the failure to use protocols that accurately replicate the physiological demands of team games. Contemporary research constructed methodologies and protocols more representative of the activities and physiological demands of team games and was almost unequivocal in its support for the efficacy of carbohydrate supplementation in improving intermittent exercise capacity. Most research shows no benefit of carbohydrate supplementation on sprint performance. The minority of research showing no influence of carbohydrate supplementation on intermittent exercise capacity displays methodological issues that could significantly impact the findings. Therefore, this work should be interpreted with caution. Carbohydrate supplementation may elicit alterations in effort perception and mood state, which could facilitate improvements in exercise performance or capacity late in the exercise bout. The presence and extent of any such influence of carbohydrate will likely depend on factors including pre-exercise muscle glycogen status, the intensity and duration of the exercise bout and ª 2011 Adis Data Information BV. All rights reserved.
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the amount and timing of carbohydrate ingestion. More work is required using appropriate evaluative tools to confirm the presence of such an effect, as well as its influence on exercise performance and/or capacity. Carbohydrate supplementation may facilitate a better maintenance of shooting accuracy during team games, with negligible support for improvements in passing, dribbling, tackling or heading. Again, these studies may be influenced by such factors as preexercise glycogen concentration; the existing skill level of subjects; the validity and reliability of and ability to compare between the various skill tests employed; the extent of test familiarization; and the type, intensity and duration of exercise. Further work using consistent, well controlled protocols and a uniform battery of standardized tests will enable greater understanding of the influence of carbohydrate on skill performance. Carbohydrate ingestion does not directly alter the physiological response to prolonged intermittent exercise. Any alterations that may occur are likely due to carbohydrate-mediated augmentations in work rate. The general metabolic response to prolonged intermittent exercise with carbohydrate supplementation is an increase in blood glucose concentration and significantly greater carbohydrate oxidation rates, along with attenuated blood FFA levels and fat oxidation rates. 4. Mechanisms of Enhancement with Carbohydrate Supplementation during Prolonged Intermittent, High-Intensity Exercise 4.1 Intermittent Exercise Capacity
It appears that carbohydrate supplementation extends intermittent exercise capacity via reduced muscle glycogen utilization in the first ~75 minutes of exercise.[23,24,26] Nicholas et al.[25] seemed to confirm this by showing a combined 22% reduction in type I and II muscle fibre glycogen utilization with carbohydrate ingestion during 90 minutes of the LIST. This was attributed to factors including exogenous carbohydrate oxidation sparing endogenous stores, greater activity of the pyruvate dehydrogenase complex due to Sports Med 2011; 41 (7)
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hyperinsulinaemia and lower blood lactate concentration and glycogen resynthesis in type II fibres due to elevated blood glucose and insulin levels. Other studies support the hypotheses of carbohydrate-mediated muscle glycogen sparing and/or glycogen resynthesis during team games exercise due primarily to observations of increased blood glucose and/or blood insulin concentrations during exercise.[14,18,23,24,26] However, only Yaspelkis et al.[14] measured muscle glycogen concentration, finding a 25% greater concentration at the end of exercise in type I muscle fibres in the carbohydrate trial. This suggests sparing of muscle glycogen rather than its synthesis during exercise, which is suggested to occur in type II muscle fibres.[25] Supporting evidence for greater pyruvate dehydrogenase activity with carbohydrate supplementation is lacking. However, work into the mechanisms of carbohydrate efficacy should continue when it is considered that only a small amount of exogenous carbohydrate appears to be oxidized, or made available for oxidation, in the first hour of exercise regardless of whether carbohydrate exerts an ergogenic effect[55] or not.[56] The potential influence of carbohydrate on perceptual responses to exercise may enable enhanced intermittent exercise capacity (see section 3.3).[29,46,57] While this hypothesis requires more work, as the relationship between carbohydrate ingestion, RPE and performance during team games exercise has not been clearly established, it does appear that carbohydrate may modify the perception of effort during team games. The significantly lower HR reported by some authors[24,26] during team games exercise when carbohydrate is ingested (section 3.4) infers reduced stress on the cardiovascular system and an ability to exercise at a higher intensity for a given HR, and may possibly contribute to improved intermittent exercise capacity. However, the common observation that carbohydrate exerts no influence on PV or HR during team games exercise suggests that altered HR response is not a plausible or consistent ergogenic mechanism of carbohydrate supplementation. Furthermore, Ali et al.[29] found a trend for a higher HR with carbohydrate ingestion during the LIST; however, ª 2011 Adis Data Information BV. All rights reserved.
this may have been due to the faster sprint times reported in the carbohydrate trial (section 4.2). 4.2 Sprint Performance
Improved sprint performance during team games exercise following ingestion of a carbohydrate-electrolyte solution has been attributed to maintenance of blood glucose levels,[27,29] which may enable greater muscle and cerebral metabolism,[29] thereby maintaining central nervous system (CNS) function and allowing better maintenance of power output or muscle glycogen sparing.[28] These hypotheses are debatable, as blood glucose concentration did not reach hypoglycaemic levels in the carbohydrate or placebo trial in the studies of Ali et al.[29] or Welsh et al.,[27] and muscle glycogen levels were not measured by Winnick et al.[28] It should be stated that the subjects in the Ali et al.[29] study began exercise with depleted glycogen stores. This may explain the improved sprint performance with carbohydrate supplementation in this study, as short-duration, maximal-intensity exercise can be attenuated if muscle glycogen levels fall below a critical threshold (~200 mmol/kg dry weight).[58,59] Therefore, ingestion of carbohydrate may have provided a sufficient supply of glucose to the muscle to enable greater sprint performance in the glycogen-depleted state compared with placebo. However, the extent of glycogen depletion was not quantified; therefore, this hypothesis is speculative. Furthermore, Foskett et al.[33] and Ali and Williams[35] reported a significant attenuation of sprint performance during the LIST protocol in the carbohydrate and placebo trials when subjects began exercise in a glycogen-depleted state. However, the extent of glycogen depletion was not reported. It also does not explain the improved sprint performance documented by Welsh et al.[27] or Winnick et al.,[28] as subjects in these studies were not glycogen depleted prior to exercise. When glycogen availability is not compromised, phosphocreatine concentration and its rate of resynthesis rather than carbohydrate availability is more related to short-duration sprint performance,[60] perhaps helping to explain the lack of effect of carbohydrate on sprint performance in most studies. However, it should be considered Sports Med 2011; 41 (7)
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that, while phosphocreatine availability is the determining factor when short sprints are interspersed with adequate passive recovery, during team games, subjects are required to jog, run and walk between each sprint. In this situation, phosphocreatine resynthesis may not be complete enough to contribute fully to each sprint, particularly in the later stages of the protocol. If this were the case, other substrates, notably carbohydrate and fat, would become more prevalent fuels during the sprints.[61] Therefore, carbohydrate supplementation may be important for maintaining sprint performance during the later stages of team games exercise. This may be particularly pertinent when pre-exercise muscle glycogen stores are not optimal,[29] but may also help to explain the findings of Welsh et al.[27] and Winnick et al.[28] who found a significant improvement in sprint performance in the late stages of exercise only. It may also help to explain the non-significant between-trials difference in sprint performance observed in most studies. However, this requires further investigation. 4.3 Mental Function and Skill Performance
Studies confirming improved mood, force output and effort perception with carbohydrate supplementation during team games exercise have implicated carbohydrate-mediated alterations in brain chemistry, particularly attenuated serotonin production,[62,63] as a potential mechanism.[27,28,46] However, none of the studies collected data that could directly confirm this, instead inferring increased brain glucose uptake based on significantly elevated blood glucose concentrations in the carbohydrate trial.[64] Cerebral glucose uptake begins to decline when blood glucose concentration falls below ~3.6 mmol/L,[65] which did not happen in the placebo trial in the studies of Backhouse et al.[46] or Welsh et al.[27] and, in the Winnick et al.[28] study, blood glucose levels were not measured. It is therefore difficult to accept this explanation. Furthermore, the concept of CNS fatigue remains unclear and difficult to experimentally isolate and confirm, particularly from a mechanistic perspective.[66] It is also extremely difficult to differentiate central from peripheral effects ª 2011 Adis Data Information BV. All rights reserved.
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when carbohydrate is ingested during exercise.[67] Work needs to be conducted that is sensitive enough to resolve the nature of the influence of carbohydrate on mental function during team games exercise, yet using tests that are externally valid to team games performance. The significantly improved, or better maintained, performance of certain skills reported by some authors has also been largely attributed to carbohydrate-mediated alterations in CNS function that enable better motor control and hence skill performance.[27-29,47] However, the issues with this are discussed above. Ali et al.[29] suggested an augmentation of neuromuscular function with carbohydrate supplementation that may also enable greater motor control, but this was not supported with data. Maintenance of blood glucose concentration, sparing of muscle glycogen and therefore, possibly, attenuation of muscle fatigue and, perhaps, better performance of the anaerobic component of the skill test have also been postulated.[27-29,44,45] However, no muscle glycogen measurements were taken,[27,29] and some studies did not measure blood glucose concentration.[28,44,45] Furthermore, hypoglycaemia did not occur in any of the other studies,[27,29] and Ali and Williams[35] failed to show a significant improvement in passing performance with carbohydrate supplementation despite very similar betweentrial blood glucose responses to their 2007 study. However, the possible effects of low blood glucose concentration on skill performance have not been elucidated.[29] Further work must attempt to quantify the mechanisms responsible for improvements in skill performance during team games exercise when carbohydrate is ingested. 5. Modulators of Carbohydrate Efficacy Research supporting the use of carbohydrateelectrolyte solutions during team games exercise generally focuses on supplementation of an approximate 6% carbohydrate-electrolyte solution of similar composition. The current research output does not provide a sufficient thesis on factors that modulate the efficacy of carbohydrate supplementation during team games exercise. Potential modulators may be different from those during Sports Med 2011; 41 (7)
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prolonged steady-state exercise due to the constantly changing exercise intensity and frequency, duration and intensity of rest intervals, the potential for team games exercise to slow the rate of GE[68] and restricted access to carbohydrateelectrolyte solutions during many team games. Work must be undertaken to further understanding in this area, and ultimately lead to the formulation of clear guidelines for the optimal ingestion of carbohydrate during team games exercise. Some of these important modulators are discussed in sections 5.1–5.7. 5.1 Fluid Volume and Solution Composition
If carbohydrate-electrolyte solutions are consumed during exercise, then fluid and carbohydrate intake are interdependent and should not be considered in isolation. Therefore, the following discussion on fluid volume, carbohydrate concentration, carbohydrate composition and solution osmolality is presented as one topic. 5.1.1 Fluid Volume
Mild dehydration increases Tcore, RPE and BM loss, and impairs skill performance during team games exercise.[49,69,70] Team games athletes should maintain adequate hydration status in order to maximize performance. This can be achieved by replacing the same amount of fluid that is lost during exercise and is a recommended practice for team games athletes.[10,71-75] Failure to ingest an appropriate volume of fluid during exercise may prevent the athlete from maximizing their performance even when ingesting carbohydrate. More specific fluid ingestion recommendations are difficult due to the numerous factors that can influence fluid requirements, such as BM, exercise intensity, individual sweat rates and environmental conditions. Section 5.2 further discusses fluid intake strategies for team games. 5.1.2 Carbohydrate Concentration
Only three studies have employed different carbohydrate concentrations during prolonged intermittent exercise.[11,13,27] Unfortunately, the use of different carbohydrate compositions,[11] relatively small increases in carbohydrate ingesª 2011 Adis Data Information BV. All rights reserved.
tion between solutions[13] and different carbohydrate concentrations within the same trial,[27] limit the usefulness of the results. Ingesting too little carbohydrate may not meet energy requirements during exercise (section 3.1). However, consuming too much carbohydrate can attenuate GE rate, cause gastrointestinal distress and impair intestinal fluid absorption (section 5.1.4).[68,76,77] A 5–7% carbohydrate-electrolyte solution is currently recommended for team games,[10] along with the recommendation of Jeukendrup and Jentjens[19] for an optimal carbohydrate intake of ~1.0–1.1 g/min. However, neither of these recommendations have been thoroughly tested using externally valid team games protocols. 5.1.3 Carbohydrate Composition
Carbohydrate oxidation rate depends on multiple factors, one of which is the composition of ingested carbohydrate.[19] This suggests that different carbohydrate compositions may have different efficacies during exercise. Ingestion of multiple transportable carbohydrates, typically glucose and fructose in a ratio of ~2 : 1, appears beneficial during prolonged steady-state exercise for increasing GE rate,[78] intestinal carbohydrate and water absorption (section 5.1.4)[78,79] and exogenous carbohydrate oxidation rates,[79-82] although the latter is not universally found.[83] In the only study to manipulate carbohydrate composition during prolonged intermittent exercise,[11] it was not possible to discern between effects due to changes in carbohydrate concentration and composition (section 5.1.2). Therefore, the effect of alterations in carbohydrate composition during team games exercise should receive close attention in future work. Recently, the first study investigating the effect of a carbohydrate gel during team games exercise reported a 45% improvement in intermittent exercise capacity compared with a placebo solution,[30] analogous to the effect of carbohydrate solutions (section 3.2). This is supported by evidence of a similar time-course of carbohydrate oxidation and peak carbohydrate oxidation rate between carbohydrate gels and drinks of the same composition.[84] This represents a step forward for the research base by investigating carbohydrate deSports Med 2011; 41 (7)
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livery in essentially a different medium. Although initial findings are positive, more research is required. 5.1.4 Solution Osmolality
Following ingestion of isocaloric carbohydrate solutions of differing composition and osmolality, less than 5% of the variance in GE rate is due to differences in osmolality.[85] Similar findings have been replicated numerous times at rest and during exercise.[86-90] Solution osmolality often increases in proportion to caloric content, indicating that the inhibition of GE originally attributed to osmolality[91,92] may have been confused with the influence of increased caloric density.[93] Significant negative correlations between carbohydrate content and GE rate with ingestion of iso-osmotic carbohydrate solutions, and positive correlations between solution caloric content and the half-time of GE, have been reported.[94,95] Calbet and MacLean[95] confirmed that caloric content explained 92% of the variance in GE rate. This, along with the observation of a similar GE rate when solutions with the same carbohydrate concentrations but significantly different osmolalities are consumed,[94,96] suggests that carbohydrate content and caloric density are more important than solution osmolality in modulating GE rate. Rapid fluid and carbohydrate delivery to the systemic circulation is crucial for exercise performance. The osmolality of a carbohydrateelectrolyte solution appears inversely related to the rate of water absorption in the small intestine,[97-101] with conflicting findings[86,96,102-105] attributed to the activity and number of intestinal solute transporters, alterations in osmolality over the length of the small intestine, and solution composition.[10,106,107] Increasing the carbohydrate concentration of a carbohydrate-electrolyte solution can increase osmolality, and therefore attenuate the rate of intestinal water absorption,[108] when carbohydrate concentration reaches ~8%.[103] This should be considered when manipulating the concentration of carbohydrate-electrolyte solutions (section 5.1.2), as increasing carbohydrate concentration may allow increased absorption of carbohydrate, but could attenuate GE rate and ª 2011 Adis Data Information BV. All rights reserved.
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intestinal water absorption, and result in suboptimal hydration status. Carbohydrate type can also influence solution osmolality and, therefore, intestinal water absorption[10] when carbohydrate concentration is >6%.[103] Incorporating multiple transportable carbohydrates into a solution can offset the effect of high osmolality on intestinal water absorption[109] by activating a greater number of intestinal solute transport mechanisms. This could enable a high volume of carbohydrate delivery while maintaining adequate intestinal water absorption. For a more detailed discussion on this topic, the reader is referred to the review of Shi and Passe.[110] 5.1.5 Recommendations
Future work must study the effects of altering fluid volume, carbohydrate concentration, composition and solution osmolality, independently and in an integrated fashion. This will enable discovery of the optimal composition of a carbohydrate-electrolyte solution for maximizing intestinal fluid and carbohydrate absorption during team games exercise. 5.2 Fluid and Carbohydrate Ingestion Pattern
Fluid may take ~40–60 minutes from the time of ingestion to be transported around the systemic circulation and become physiologically useful.[111,112] This, coupled with the potential attenuation of GE due to the intensity of team games exercise[68,76] and the addition of carbohydrate to a solution,[90,113] and the insufficient opportunities to ingest fluid at regular intervals during team games,[31] casts doubt on the efficacy of consuming consistent amounts of fluid and carbohydrate throughout team games exercise. Coyle[111] suggests that it may be beneficial to drink larger volumes early in exercise, ingest fluid throughout exercise to ensure gastric volume is high after 40 minutes, and then ingest little fluid thereafter to minimize gastric volume towards the end of exercise, and thereby minimize the volume of fluid present that cannot aid, and may inhibit, performance by adding weight and perhaps causing gastrointestinal discomfort. It would be interesting to compare the ‘standard’ intake regimen Sports Med 2011; 41 (7)
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employed in most team games research (see table II) with one that provides greater volumes of fluid in the early stages of exercise and then progressively less as exercise continues. Clarke et al.[31] investigated the effect of consuming a carbohydrate-electrolyte solution in a team games-specific fashion (a large bolus prior to and at 45 minutes during exercise) compared with more frequent ingestion during a team games exercise protocol. Exercise performance and capacity were not assessed but the overall metabolic response to exercise – quantified by measurement of blood glucose, insulin, non-esterified fatty acids, glycerol and adrenaline concentrations – was similar between trials. This suggests that ingestion of carbohydrate-electrolyte solutions before a game and at half-time is a practical alternative for fluid and carbohydrate provision.[31] However, this is not supported by the study of Abbey and Rankin.[34] More work is required in this area. 5.3 Glycaemic Index of Pre-Exercise Meals
This review will not discuss the glycaemic index in detail, and the interested reader is referred to the recent review by O’Reilly et al.[114] Manipulating the glycaemic index of a meal consumed several hours before team games exercise does not significantly affect sprint performance or intermittent exercise capacity,[115,116] despite increased fat oxidation rates with a low-glycaemic index meal.[116] Lack of effect may be due to the requirement for high-intensity efforts throughout team games protocols, which would be dependent on phosphocreatine and carbohydrate metabolism.[60,61] Ingesting a carbohydrate-electrolyte solution before and during steady-state endurance exercise negates the proposed benefits of a pre-exercise lowglycaemic index meal[117,118] by minimizing potential differences in metabolic response or substrate oxidation between low- and high-glycaemic index meals.[117,118] Chryssanthopoulos and Williams[119] reported a significant improvement in steadystate running capacity when ingestion of a preexercise carbohydrate meal was combined with carbohydrate ingestion during exercise. Howª 2011 Adis Data Information BV. All rights reserved.
ever, a low- to high-glycaemic index meal comparison was not made. No research has investigated the interaction between pre-exercise meals of differing glycaemic index and ingestion of a carbohydrate-electrolyte solution before and during team games exercise. This should be carried out in order to quantify the optimal pre- and during exercise nutritional strategy for team games athletes.[114] 5.4 Fluid Temperature
Provision of cold fluid (4–5C) encourages greater fluid ingestion during exercise in mild and high ambient temperatures,[120,121] and may also enable significantly greater steady-state endurance cycling performance[122] and capacity[121,123] in the heat compared with ingestion of warm fluid (16–38C). Cold fluid may act as a heat sink, attenuating the rise in body heat storage and, possibly, Tcore.[123] However, endurance capacity has been improved with cold fluid ingestion without significant changes in Tcore.[121,122] Cold fluid intake may significantly reduce skin temperature[122,124] and attenuate skin blood flow and sweat rate[125] during exercise in temperate and hot environments. This may represent a redistribution of cardiac output from the skin to the exercising muscles and may enable improved endurance performance/capacity.[122] However, this requires further investigation as skin temperature, blood flow and exercise performance/capacity have not yet been measured in the same study. The influence of cold fluid ingestion on steadystate cycling capacity in moderate environmental conditions appears negligible.[123,126] The studies discussed above were conducted using similar exercise protocols (steady-state recumbent or. upright cycling for ~50–120 minutes at 50–66% VO2max). No work has used prolonged running as a modality; furthermore, no prolonged intermittent cycling or running protocols have been employed. Variable intensity cycling in high ambient temperatures may significantly increase heat storage, the rate of rise in Tcore, wholebody sweat rate and dehydration, and significantly reduce forearm blood flow compared with steady-state cycling.[127] This, along with the Sports Med 2011; 41 (7)
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current recommendation for a fluid temperature of 15–21C[73] and the acknowledgement that preferred fluid temperature varies greatly between individuals,[73] provides a rationale for investigating the effects of fluid temperature during team games exercise. This should be conducted using fluid with and without carbohydrate, to observe whether alterations in the temperature of a carbohydrateelectrolyte solution provide an additional effect over and above that of carbohydrate or fluid alone. 5.5 Carbohydrate Mouthwash
Insufficient opportunities exist for regular fluid ingestion during field-based team games, and any opportunities that do arise may be brief and not afford the athlete the time to ingest the optimal volume of fluid or carbohydrate. Furthermore, evidence of an attenuated GE rate and, possibly, increased gastrointestinal discomfort with ingestion of carbohydrate-electrolyte solutions during team games exercise,[77] along with the recent suggestion by Edwards and Noakes[128] that the degree of sweat loss and associated dehydration commonly encountered during soccer is not crucial to performance, suggests that a carbohydrate-based ergogenic aid that can be rapidly utilized and has no tolerance issues may be useful for team games players. In recent years, the use of carbohydrate mouthwashes has been shown to enhance running and cycling performance lasting ~30–60 minutes.[129-132] Other work has failed to show a benefit of carbohydrate mouthwashes,[133,134] possibly due to study differences in solution blinding, the influence of dehydration and endogenous muscle glycogen availability. The apparent mechanisms for enhancement with carbohydrate mouthwashes revolve around modification of central drive and motivation and/or activation of reward and motor control centres in the brain rather than a metabolic cause.[129,131] These alterations may elicit a more favourable perception of effort during exercise.[129,130] For more information on the enhancement mechanisms of carbohydrate mouthwashes, see Chambers et al.[131] All previous studies of carbohydrate mouthwashes used steady-state protocols. The potential ª 2011 Adis Data Information BV. All rights reserved.
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of carbohydrate mouthwashes during team games exercise is strong, particularly in allowing easier and more rapid supplementation than carbohydrateelectrolyte solutions and limiting possible gastrointestinal distress associated with fluid and carbohydrate ingestion.[133] Research needs to quantify this potential benefit, particularly regarding whether a carbohydrate mouthwash is sufficient to enhance team games performance in the presence of significant muscle glycogen depletion. 5.6 Ambient Temperature
The effect of carbohydrate supplementation during prolonged exercise in the heat is equivocal. If exercise is terminated due to attainment of a critical Tcore – a concept that, while having some empirical support,[135,136] is not universally accepted[137-139] – carbohydrate is not beneficial to performance.[140] However, if subjects do not terminate exercise due to hyperthermia, ingestion of a 6% sucrose/glucose solution has been shown to improve prolonged cycling performance in the heat.[140] During prolonged exercise in a cool environment, a 7% carbohydrate solution is also able to improve exercise capacity.[141] However, these findings apply to prolonged steady-state exercise. Only two studies have investigated carbohydrate supplementation during prolonged intermittent exercise in the heat.[11,18] The major limitations of these studies (see sections 3.1 and 3.2) prevent confident interpretation and application of the findings. Therefore, there is a large scope for focused and well conducted research into the effect of carbohydrate supplementation during team games exercise in different ambient temperatures. 5.7 Populations
No research into carbohydrate supplementation during team games exercise has focused exclusively on adult female subjects. Females generally oxidize less carbohydrate and more fat during exercise than do males,[142,143] with less muscle glycogen utilization recorded during steady-state running[144] but not cycling.[145] It would be interesting to observe whether carbohydrate supplementation during team games exercise enabled any performance and/or capacity improvements in Sports Med 2011; 41 (7)
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females and, if so, whether mechanisms behind these improvements were different from those behind improvements in male subjects. A large number of children and adolescents actively participate in organized team games.[146,147] However, the research base investigating the physiological responses of this population to this form of exercise, as well as investigating fatigue mechanisms and avenues of performance enhancement is sparse. This is likely due to the many problems faced when conducting research in young people such as recruitment and retention, gaining parental consent, child assent and ethical approval to undertake all necessary experimental procedures,[148,149] ensuring subjects understand and fulfil all procedural requirements of a study and adequately controlling for the influence of biological maturation, which is often hampered by ethical and consensual restrictions.[150] Adolescents appear to exhibit a maturationdependent exercising metabolic response involving greater fat and lower carbohydrate oxidation than adults;[151] however, the large number of potentially confounding factors involved in the study of developmental changes in energy metabolism make a firm consensus extremely difficult.[152,153] They also appear able to oxidize significantly more exogenous carbohydrate during moderateintensity steady-state cycling than adults.[154] Additionally, a significant improvement in steadystate exercise cycling capacity with carbohydrate supplementation has been observed in 10- to 14-year-old males.[155] This provides a rationale for the study of carbohydrate supplementation during team games exercise in these subjects. We recently demonstrated, for the first time, that ingestion of a 6% carbohydrate-electrolyte solution immediately before and during a modified LIST protocol significantly improved the intermittent exercise capacity of trained 12- to 14-yearold team games players by 24% compared with a placebo.[156] Neither sprint performance nor physiological responses to exercise were affected by carbohydrate supplementation, except at exhaustion, where subjects elicited a significantly higher peak HR in the carbohydrate trial, but with no significant difference in RPE compared with the placebo trial. This was attributed to carbohyª 2011 Adis Data Information BV. All rights reserved.
drate supplementation enabling participants to continue working to a higher intensity via better maintenance of muscle metabolism (section 4.1), or the influence of carbohydrate on perceptual responses to exercise (section 3.3). Further work is required to confirm these mechanisms in this population. These positive findings provide a platform from which to investigate other factors associated with carbohydrate supplementation during team games exercise in adolescents, such as those discussed in sections 5.1–5.6, in order to widen and strengthen the research base in this area. 6. Conclusions Most early research investigating carbohydrate supplementation during prolonged intermittent exercise was subject to methodological limitations that restricted both its scientific rigour and its applicability to actual sporting activity. The development of team game-specific exercise protocols enabled a more focused investigative approach to this topic. The findings of this review into carbohydrate supplementation immediately prior to and during team games exercise are as follows: 1. Carbohydrate supplementation significantly improves intermittent exercise capacity in adults. Possible mechanisms include muscle glycogen sparing or resynthesis during low-intensity periods and altered effort perception during exercise. More research into the mechanisms of carbohydrate efficacy is required. 2. Initial findings suggest that carbohydrate supplementation significantly improves intermittent exercise capacity in adolescent team games players. Enhancement mechanisms may be, at least partially, centrally mediated. Future work should investigate this further. 3. Carbohydrate supplementation has a negligible effect on sprint performance in adults and adolescent team games players. Carbohydrate efficacy may depend on endogenous muscle glycogen availability. 4. Carbohydrate supplementation may elicit alterations in effort perception and mood state that could improve performance in the later stages Sports Med 2011; 41 (7)
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of team games exercise and may enable better maintenance of shooting accuracy during team games, with negligible support for improvements in passing, dribbling, tackling or heading. Improvements with carbohydrate intake are attributed to improved cerebral glucose uptake, greater CNS function and motor control. More work is required in these areas. 5. Carbohydrate ingestion does not directly alter physiological responses to prolonged intermittent exercise, with any alterations likely due to an augmented work rate via carbohydrate supplementation. Carbohydrate supplementation usually increases blood glucose and insulin concentrations either periodically or throughout exercise, increases carbohydrate oxidation rates and RER, and attenuates blood FFA levels and fat oxidation rates. 6. It has been suggested that a 5–7% carbohydrateelectrolyte solution containing multiple transportable carbohydrates and sodium, and with an osmolality of 250–370 mOsm/kg may be optimal before and during team games exercise. However, very little subsequent work has attempted to empirically test these recommendations, as well as other potential modulators of carbohydrate efficacy, during team games exercise. 7. Several key areas need to be addressed by future research. These include manipulations in ingested fluid volume, carbohydrate concentration, carbohydrate composition and solution osmolality, both independently and in an integrated fashion; the influence of the glycaemic index of pre-exercise meals with and without carbohydrate supplementation; alterations to fluid and carbohydrate ingestion patterns and fluid temperature; the influence of carbohydrate mouthwash supplementation; carbohydrate supplementation in different ambient temperatures; and the investigation of all of these areas in different populations. Acknowledgements No funding was provided for the preparation of this review. All authors declare that they have no conflicts of interest regarding the content of this paper. The authors wish to thank Dr Shirley Gray and Mr Mark Sanderson for their valued assistance in the preparation of this review.
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Correspondence: Mr Shaun Phillips, Institute of Sport, Physical Education and Health Studies, University of Edinburgh, St Leonards Land, Holyrood Road, Edinburgh, EH8 8AQ, UK. E-mail:
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Obstacles in the Optimization of Bone Health Outcomes in the Female Athlete Triad Gaele Ducher,1,2 Anne I. Turner,1 Sonja Kukuljan,1 Kathleen J. Pantano,3 Jennifer L. Carlson,4 Nancy I. Williams2 and Mary Jane De Souza2 1 Centre for Physical Activity and Nutrition Research, School of Exercise and Nutrition Sciences, Deakin University, Burwood, VIC, Australia 2 Department of Kinesiology, Pennsylvania State University, State College, PA, USA 3 Cleveland State University, Physical Therapy Program, Department of Health Sciences, Cleveland, OH, USA 4 Division of Adolescent Medicine, Department of Pediatrics, Lucile Packard Children’s Hospital at Stanford, Palo Alto, CA, USA
Contents Abstract. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Current Clinical Knowledge, Attitudes and Management of the Female Athlete Triad . . . . . . . . . . . 3. Management of Bone Health Issues Related to the Female Athlete Triad. . . . . . . . . . . . . . . . . . . . . . . 3.1 Assessment of Bone Health . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1.1 Dual-Energy X-Ray Absorptiometry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1.2 Three-Dimensional Imaging Techniques . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1.3 Bone Turnover Markers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1.4 Specific Considerations in the Growing Athlete. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2 Pharmacological Treatments and Current Issues . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.1 Estrogen Therapy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.2 Bisphosphonates and Other Anti-Osteoporotic Therapies . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.3 Other Pharmacological Therapies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3 Non-Pharmacological Approaches . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3.1 First-Line Strategy: Increasing Energy Availability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3.2 Other Non-Pharmacological Strategies to Improve Bone Health . . . . . . . . . . . . . . . . . . . . 3.3.3 Specific Considerations for Stress Fractures. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. Conclusions and Perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Abstract
587 588 589 590 590 590 592 593 594 595 595 597 597 597 597 598 599 600
Maintaining low body weight for the sake of performance and aesthetic purposes is a common feature among young girls and women who exercise on a regular basis, including elite, college and high-school athletes, members of fitness centres, and recreational exercisers. High energy expenditure without adequate compensation in energy intake leads to an energy deficiency, which may ultimately affect reproductive function and bone health. The combination of low energy availability, menstrual disturbances and low bone mineral
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density is referred to as the ‘female athlete triad’. Not all athletes seek medical assistance in response to the absence of menstruation for 3 or more months as some believe that long-term amenorrhoea is not harmful. Indeed, many women may not seek medical attention until they sustain a stress fracture. This review investigates current issues, controversies and strategies in the clinical management of bone health concerns related to the female athlete triad. Current recommendations focus on either increasing energy intake or decreasing energy expenditure, as this approach remains the most efficient strategy to prevent further bone health complications. However, convincing the athlete to increase energy availability can be extremely challenging. Oral contraceptive therapy seems to be a common strategy chosen by many physicians to address bone health issues in young women with amenorrhoea, although there is little evidence that this strategy improves bone mineral density in this population. Assessment of bone health itself is difficult due to the limitations of dual-energy X-ray absorptiometry (DXA) to estimate bone strength. Understanding how bone strength is affected by low energy availability, weight gain and resumption of menses requires further investigations using 3-dimensional bone imaging techniques in order to improve the clinical management of the female athlete triad.
1. Introduction For a growing number of female athletes, the desire for athletic success can be associated with a high drive for thinness that may lead to the development of low energy availability, menstrual dysfunction, and low areal bone mineral density (aBMD), a condition collectively referred to as the ‘female athlete triad’.[1] Alone or in combination, the disorders of the female athlete triad can have a negative impact on health and athletic performance.[2] This condition not only affects high-level female athletes but more generally exercising girls and women. Low energy availability can be caused by high energy expenditure associated with physical exercise and training, inadequate energy intake, or a combination of both. Energy availability is defined as dietary energy intake minus exercise energy expenditure.[1] Energy availability is considered adequate when energy intake is sufficient to maintain normal routine physiological functions in addition to exercise training. When energy availability is too low, the body tends to reduce the amount of energy that is used for physiological functions such ª 2011 Adis Data Information BV. All rights reserved.
as cellular maintenance, thermoregulation, growth and reproduction.[3] Energy conservation, which tends at restoring energy balance, could explain why stable body weight has been reported in amenorrhoeic athletes.[4-7] Low energy availability triggers the disruption of the hypothalamo-pituitary-gonadal axis, which leads to menstrual disturbances including amenorrhoea.[1,2,8-14] Amenorrhoea is defined as having no menses for a minimum period of 3 months.[15] Functional hypothalamic amenorrhoea (FHA) is diagnosed by exclusion of situations (e.g. pregnancy) or medical conditions (e.g. hyperprolactinoma, thyroid diseases) that typically cause the absence of menses.[15,16] Athletic amenorrhoea is a form of FHA observed in athletes who display low energy availability. Amenorrhoea represents the most severe menstrual disturbance along a continuum of abnormalities ranging from luteal phase defects, anovulatory cycles, oligomenorrhoea (irregular and inconsistent menstrual cycles lasting from 36 to 90 days[17]) and amenorrhoea.[9] Irregular menses in athletes (oligo- or amenorrhoea) have been associated with a 2- to 4-fold greater incidence of Sports Med 2011; 41 (7)
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stress fractures[18] and low aBMD, particularly at the spine.[19-26] The prevalence of oligomenorrhea and amenorrhoea in adult athletes across multiple sports has been reported to range from 12% to 79%.[27-29] In adolescents (<18 years), a high prevalence of oligomenorrhea and amenorrhoea (45–50%) has been reported in sports that emphasize a lean physique, such as ballet dancing and running.[27,30,31] However, regardless of age and type of sports participation, approximately 1 in 5 to 1 in 4 active women present with some form of menstrual disturbance.[32-35] Notably, the prevalence of oligomenorrhoea and amenorrhoea is more difficult to determine in adolescents since menstrual cycle intervals of >35 days are encountered in 65% of girls during the first 12 months following menarche.[36] Indeed, ovulatory status and menstrual cycle lengths are highly variable for about 5 years in post-menarcheal girls.[37] Menstrual cycles and ovulation are much less variable and cycles are more consistent in length for approximately 20 years in young reproductively mature adults. As women approach menopause, cycle length and ovulatory status become highly variable again for about 10 years.[38,39] Persistent, irregular menstrual cycles are a warning sign that warrant further medical attention, but may not be perceived as such by athletes. Athletes who display low energy availability, even when accompanied by irregular or absent menses, may not seek medical support until a more obvious symptom, such as a stress fracture, is sustained.[40] In addition, clinicians may not feel confident in treating athletes presenting with amenorrhoea[41-43] and the use of pharmacological therapies still remains very controversial in this population.[1,41,44] The objective of this review is to investigate current issues in the management of the bone health concerns associated with the female athlete triad. 2. Current Clinical Knowledge, Attitudes and Management of the Female Athlete Triad Little is known about the clinical management of the female athlete triad, particularly related to ª 2011 Adis Data Information BV. All rights reserved.
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bone health concerns. Published investigations are limited to those conducted in the US. The first survey on the clinical management of athletic amenorrhoea (1995) revealed that oral contraceptive use and other hormonal therapeutic regimens were endorsed by 92% of physicians surveyed,[42] despite a paucity of data demonstrating their efficacy in preserving bone mass.[45-47] Ten years later (2006), another survey revealed that clinicians, including paediatricians and gynaecologists, did not feel confident in treating athletes with conditions of the female athlete triad,[43] despite the position stand published by the American College of Sports Medicine (ACSM) in 1997.[48] One of the most recent surveys to date (2007) reported that almost 80% of clinicians believed there were insufficient guidelines for the management of the female athlete triad, more specifically for the evaluation of amenorrhoea, the use of bone density scans, and the prescription of estrogen therapy and other treatment modalities.[41] Reported use of estrogen therapy was very heterogeneous,[41] which is not surprising given the contradictory reports concerning its efficacy in improving bone health in premenopausal women with amenorrhoea.[49] The treatment strategies that have been reported to be used most frequently in amenorrhoeic athletes are calcium and vitamin D supplementation, followed by advice to change body weight and diet (figure 1).[41] Clinicians’ attitudes towards the female athlete triad also vary according to medical specialty.[43,50] For example, although orthopaedic surgeons reportedly suspected eating disorders in 59% of their patient-athletes, discussion of these issues occurred only with 31% of the involved patients.[50] In contrast, family physicians suspected eating disorders in 84% of their patientathletes and reportedly discussed the problem with 80% of the involved patients.[50] Physical therapists play an important role in identifying athletes at risk and in managing the female athlete triad due to their expertise in musculoskeletal health and exercise prescription, but their knowledge of the female athlete triad may be lacking.[51] A recent survey (2009) conducted in 205 physical therapists in the US[52] showed that 50% of the survey respondents had Sports Med 2011; 41 (7)
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% Patients 0 <25 26−50 51−75 >75 70
60
% Clinicians
50
40
30
20
10
0 Calcium
Vit D
Body weight
Diet
Exercise
Estrogen
Fig. 1. Preferred strategies for the management of amenorrhoea in athletes. The graph presents the strategies reported by clinicians for the management of athletic amenorrhoea in adolescent and young adult women (note: clinicians include medical doctors [n = 126] who reported specialty training in paediatrics [63%], family medicine [17%], adolescent medicine [16%], internal medicine [13%] and sports medicine [3%]. Some participants reported specialty training in more than one category). The numbers on the y-axis represent the percentage of clinicians who used the particular intervention strategy indicated on the x-axis. The bars correspond to the percentage of patients that clinicians reported as having received this intervention (for example, the first strategy used is calcium (Ca2+) supplementation: 70% of clinicians used Ca2+ supplementation in >75% of patients with athletic amenorrhoea) [reproduced from Carlson et al.,[41] with permission from Elsevier]. Body weight = maintenance or increase in body weight; Calcium = Ca2+ supplementation; Diet = increase in energy intake; Estrogen = estrogen therapy; Exercise = reduction in training volume; Vit D = vitamin D supplementation.
treated female athletes for conditions related to the female athlete triad (e.g. stress fractures), yet <25% could accurately list all three components of the syndrome, or had been involved in screening athletes for female athlete triad symptoms. The study concluded that physical therapy curriculums in the US need to better educate physical therapists about the detection, treatment and prevention of the female athlete triad in the future.[52] Updated clinical guidelines have been published by the ACSM[1] and the Medical Commission of the International Olympic Committee (IOC);[44] however, it is not clear whether these guidelines have been well disseminated in the medical and healthcare community. Furthermore, an international coalition with representatives from major organizations dedicated to active women and athletes, the Female Athlete ª 2011 Adis Data Information BV. All rights reserved.
Triad Coalition (www.femaleathletetriad.org), has been formed to foster education, research and advocacy with regard to the female athlete triad. 3. Management of Bone Health Issues Related to the Female Athlete Triad 3.1 Assessment of Bone Health 3.1.1 Dual-Energy X-Ray Absorptiometry
First introduced in the late 1980s, dual-energy X-ray absorptiometry (DXA) is the most available and widely used densitometry technique.[53] The ACSM recommends DXA scans for premenopausal women in any of the following situations: (i) oligomenorrhoea or amenorrhoea, present for ‡6 months; (ii) disordered eating or an eating disorder present for ‡6 months; and (iii) the presence of stress fracture or other fracture Sports Med 2011; 41 (7)
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from minimal trauma.[1] According to the recommendations from the International Society for Clinical Densitometry (ISCD), the appropriate skeletal sites to scan are the lumbar spine and hip in adults,[54,55] with a re-evaluation of aBMD after 12 months, if the aforementioned symptoms persist.[1] Although aBMD at the hip may well be within normal range in athletes engaged in activities inducing repetitive loading on the lower limbs (e.g. running, ballet dancing),[19,23,24,26,56-58] athletes with menstrual disturbances may display low aBMD at the lumbar spine[19-26,56,59,60] and distal forearm.[61,62] The longer the duration of menstrual dysfunction, the larger the aBMD deficits at non-weight-bearing sites (figure 2).[19] The lumbar spine and forearm should be monitored carefully because they are rich in trabecular bone and submitted to little or no weightbearing.[63] Not only do amenorrhoeic athletes present with lower aBMD than their eumenorrheic counterparts (which might indicate they did not maximize their exercise-induced skeletal
benefits), they can also present with lower aBMD than sedentary women.[19,20,46,63,64] The prevalence of low aBMD (£ -1 standard deviation [SD] compared with the norm in young adults) has been reported to range between 1.4–50% in athletic populations who are considered to be at risk for developing the female athlete triad.[65] Prospective cohort studies in postmenopausal women indicate that the risk of fracture increases by a factor of 1.4–2.6 for each decrease in aBMD by 1 SD.[66] This result suggests that amenorrhoeic athletes who have low aBMD during adolescence or young adulthood are likely to be at higher risk of osteoporotic fracture later in life. Notably, DXA measures are based on a 2dimensional projection of a 3-dimensional structure.[67] Because aBMD is the ratio between bone mineral content (BMC, a 3-dimensional parameter) and bone area (a 2-dimensional parameter), it is confounded by body size. For example, at the lumbar spine, BMC is scaled proportionately to bone area to the power of 1.5; a better estimate of true volumetric BMD would be BMC/bone = <40 mo = >40 mo
1.25 1
Non-weight-bearing sites
Weight-bearing sites * *
0.75 0.5
Z-score
0.25 LS
Head
Arms
Ribs
0 FN
Troch
−0.25 −0.5 −0.75 −1
* *** ** ***
−1.25 Fig. 2. Z-scores for areal bone mineral density (aBMD) at the weight-bearing and non-weight-bearing sites in dancers with oligomenorrhoea of <40 and >40 months duration (adapted from Pearce et al.,[19] with kind permission of Springer Science and Business Media). FN = femoral neck; LS = lumbar spine; Troch = trochanter aBMD; * p < 0.05; ** p < 0.01; *** p < 0.001 compared with zero.
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Vol-BMD (g/cm3)
BMC (g)
Area (cm2)
aBMD (g/cm2)
1/2 cm
1
1/8
1/4
1/2
1 cm
1
1
1
1
Fig. 3. Effect of skeletal size on dual-energy X-ray absorptiometrybased measures of areal bone mineral density (aBMD) [reproduced from Leonard and Zemel,[69] with permission from Elsevier]. BMC = bone mineral content; Vol-BMD = volumetric bone mineral density.
area1.5.[68] When scanning two bones with different dimensions but similar volumetric BMD, DXA-derived aBMD is typically shown to be lower in smaller bones (figure 3).[67,69] The fact that aBMD values are lower in smaller bones implies that DXA tends to underestimate volumetric BMD in petite individuals. In addition, DXA-derived aBMD is based on the assumption that mass and composition (percentage fat content) of the covering soft tissue are homogeneous in the body.[70] Not only do the thickness of soft tissue and its fat content vary throughout the body, but they are also affected by changes in body weight.[71] Therefore, aBMD results can be affected by body weight loss or body weight gain. For example, an average weight loss of 11.3 – 6.9 kg over a year in 34 obese subjects was associated with an apparent, but false, 1–2% reduction in spinal aBMD.[72] Little is known about how smaller changes in body weight and/or body composition affect the DXA outcomes; therefore, the error of measurement cannot be predicted. Health professionals must be aware of this issue when interpreting DXA scans in female athletes who may be gaining or losing weight. 3.1.2 Three-Dimensional Imaging Techniques
Bone geometry, volumetric BMD, and most importantly bone strength, cannot be assessed accurately by DXA because this technique fails to provide a 3-dimensional image. Using 3-dimensional imaging technologies is important for populations undergoing bone growth because minor increases in bone size can significantly affect bone strength, despite minor changes in aBMD or bone mass.[73] MRI has been used previously in athletes to investigate the effects of repetitive ª 2011 Adis Data Information BV. All rights reserved.
loading,[74-79] but it does not measure bone mineral mass and therefore needs to be coupled with DXA.[74,75,77,78] Axial quantitative computed tomography (QCT) and peripheral QCT (pQCT) have the capacity to measure not only bone geometry, but also bone mass and volumetric BMD, specific to trabecular and cortical bone. Studies using axial QCT in amenorrhoeic athletes showed that hypoestrogenism has a detrimental effect on the athlete’s spinal volumetric BMD.[59,80,81] The pQCT measures the same parameters as the QCT, but in the peripheral skeleton only, thereby keeping the radiation dose very low (1.5–4 mSv per scan vs >50 mSv for spinal QCT).[82] However, since the pQCT is used mostly in research settings, it has limited availability. The ability of pQCT to predict bone strength of the radius and tibia was found to be similar,[83,84] or slightly higher,[85-87] than DXA; 75–85% of the variance in failure load can be predicted using pQCT parameters.[83-86,88,89] This technique has been used in anorexic patients[90-93] who displayed Z-scores for BMC, total or trabecular volumetric BMD ranging between -0.8 and -1.2 SD at the distal radius.[91,93] More recently, the pQCT was used to clarify the geometric adaptations and changes in volumetric BMD induced by gymnastics training, a discipline typically associated with marked increases in aBMD.[94] Although retired elite artistic gymnasts had greater bone mass, size and strength than sedentary women of similar age,[94] a history of amenorrhoea seemed to have compromised some of the skeletal benefits associated with high-impact gymnastics training.[95] Greater trabecular volumetric density and bone strength in the distal radius and tibia were found in former gymnasts without a history of menstrual dysfunction, but not in those who reported a history of either primary or secondary amenorrhoea. Similar findings were obtained with DXA at the spine,[95] suggesting a detrimental effect of hypoestrogenism on trabecular bone. Different mechanisms underpin exercise-induced changes in bone strength during growth (figure 4). Bone strength depends on material properties that are difficult to measure in vivo, and structural properties that change dramatically during growth. Sports Med 2011; 41 (7)
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Change in bone dimensions
Change in bone shape
Change in trabecular volumetric BMD
Fig. 4. Potential changes in bone mass and shape that underpin the exercise-induced increase in bone strength in children and adolescents. The different mechanisms depicted are not mutually exclusive and in many instances are combined. Changes in bone dimensions and bone shape are the preferential mechanisms in long bone shafts in response to exercise during growth. In long bone ends that are rich in trabecular bone, the increase in bone size is limited, and thus, exercise alternatively promotes an increase in trabecular volumetric bone mineral density (trabecular volumetric BMD) [reproduced from Ducher et al.,[96] with permission of the American Society for Bone and Mineral Research].
More specifically, cross-sectional bone size is a strong determinant of bone strength, because the resistance of bone to bending or torsional forces is related to its diameter to the fourth power.[97] The impact of low energy availability on the mechanisms underlying exercise-induced changes in bone strength remains unknown. Importantly, both the DXA and quantitative computed tomography techniques (QCT and pQCT) measure the inorganic component of the bone matrix, i.e. the hydroxyapatite crystals made of calcium and phosphate that give the skeleton its stiffness. The organic component of the bone matrix, which is composed of ~90% of type I collagen and gives the skeleton its flexibility, also affects bone strength.[98] However, current imaging techniques that are applicable in vivo non-invasively do not provide information on the organic component of the bone matrix. 3.1.3 Bone Turnover Markers
Bone turnover markers have been used in clinical settings to monitor responses to antiosteoporotic treatment. Whereas the minimum time interval to perform two consecutive DXA scans is usually 12 months in adults[55] and 6 months in children,[99] bone markers can reveal ª 2011 Adis Data Information BV. All rights reserved.
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a change in overall bone metabolism within a few days,[100] even a few hours.[101] Common markers of bone turnover are given in table I. Major limitations to widespread clinical use of biomarkers are the cost of the biochemical assays and the variability of the markers (diurnal variability and inter-subject variability). Previous cross-sectional studies in athletes with amenorrhoea or oligomenorrhea showed no change[26] or a reduction[20,60,102-105] in bone formation markers when compared with eumenorrhoeic athletes or sedentary controls. Findings on markers of bone resorption are more contradictory, with either reduced,[102,103] unchanged[26,60] or elevated[105] bone resorption markers reported in amenorrhoeic athletes (table I). Results from crosssectional studies should be viewed with caution, however, because bone turnover markers are generally more meaningful when serial measurements are undertaken in the same subject.[106,107] Bone markers can also be used to measure the balance between bone resorption and formation by calculating a ‘coupling index’.[100] The difference in Z-scores between the marker of resorption and the marker of formation matters more than the absolute value of each marker. A shortterm trial conducted in sedentary premenopausal women who completed a supervised exercise protocol showed that bone formation markers were reduced when energy availability fell below 30 kcal/kg of lean body mass/day (a 33% shortterm energy deficiency, with 45 kcal/kg lean body mass/day representing a balanced energy availability), whereas bone resorption markers were only increased when energy availability fell to 10 kcal/kg of lean body mass/day (78% energy deficiency), an indication of the uncoupling between bone resorption and formation.[100] Changes in bone formation markers were mirrored by changes in metabolic hormones, such as insulin, tri-iodothyronine and insulin-like growth factor (IGF)-1, whereas changes in bone resorption markers were mirrored by changes in estradiol.[100,108] The foregoing observations suggest that bone formation might be more sensitive to a state of energy deficiency than bone resorption. Estimated average energy availability ranging between 12–29 kcal/kg of fat-free mass/day has Sports Med 2011; 41 (7)
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Table I. Biochemical markers of bone turnover in athletic amenorrhoeaa Amenorrhoeica compared with eumenorrhoeic athletes
Amenorrhoeica compared with healthy controls
Alkaline phosphatase (ALP)
Unchanged[26] Reduced[102,103]
Unchanged[26] Reduced[102]
Osteocalcin (bone GLA protein)
Unchanged[26] Reduced[60,102-104] b
Unchanged[26] Reduced[102,104] b
Procollagen type 1 Carboxyl terminal-propeptide (PICP)
Reduced[102]
Reduced[102]
Procollagen type 1 nitrogen terminal-propeptide (PINP)
Reduced[105]
Reduced[20] b
Markers Bone formation
Bone resorption Hydroxyproline (HOP)
Unchanged[60]
Deoxypyridinoline (DPYRX)
Unchanged[26] Reduced[102,103]
Unchanged[26] Reduced[102]
Pyridinoline (Pyr)
Reduced[102]
Reduced[102] Reduced[20] b
N telopeptide (NTX) C telopeptide (CTX)
Elevated
a
Some studies also included oligomenorrhoeic athletes.
b
Studies in adolescent athletes.[20,104]
[105]
been reported in adult athletes with and without amenorrhoea,[109] which places them at risk of impaired bone turnover. If low energy availability persists over a longer period, irreversible reductions in aBMD may be observed.[100] A recent cross-sectional study found similar rates of bone formation and resorption in energy-replete women, regardless of their estrogen status, whereas the rate of bone formation was lower, the rate of bone resorption was higher, and aBMD was lower in women who were deficient in both energy and estrogen.[105] 3.1.4 Specific Considerations in the Growing Athlete
Assessing bone health is even more challenging in adolescents because of the constant change in bone mass, size and shape.[110] DXAderived hip assessment in children and adolescents is not reliable due to significant variability in skeletal development and the lack of reproducible regions of interest.[99] Thus, scans at the spine are preferred.[99] Evaluation of aBMD at the whole body (less the head) is recommended by the ISCD because it has been shown to be associated with fracture risk in children.[111] However, whole body less head aBMD is likely to be normal in young athletes because higher aBMD at ª 2011 Adis Data Information BV. All rights reserved.
loaded sites may mask possible lower aBMD at unloaded sites. In contrast, the distal forearm, for which reference data exist in children,[112-114] might be a useful site for testing. It is the most common site of fracture in adolescents and it is not loaded in activities such as running or jumping, which account for a significant proportion of children’s physical activity.[115-117] In children and adolescents aged 5–19 years, ‘low bone mass’ has been defined by the ISCD as a Z-score £-2.0 SD for BMC or aBMD adjusted for age, gender, body size.[99] It can also be helpful to determine if a growth spurt occurred without weight gain, which constitutes a relative weight loss[118] and the assessment of bone age can give an indication of the maturational delay and remaining growth.[118] Normal bone growth can be compromised by a range of diseases but also, to an unknown extent, energy deficiency and hypoestrogenism. Depending upon the age at which bone growth becomes compromised, deficits may occur in limb dimensions (pre-puberty), spine dimensions (early puberty) or volumetric BMD by interfering with mineral accrual (late puberty).[119] Before DXA scans in growing children or adolescents are interpreted, it is essential to Sports Med 2011; 41 (7)
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adjust the outcomes to account for differences in body size.[99] Experiments conducted in 150 healthy individuals aged 6–21 years showed that normalizing whole-body DXA bone area for height and BMC for height provided the best measures of bone dimensions and strength as determined by pQCT.[120] DXA BMC for age and aBMD for age were only moderately correlated with pQCT-derived bone strength.[120] Therefore, comparing a child’s whole-body BMC to heightmatched reference data provided by the DXA manufacturer is a better approach than looking at the absolute values of aBMD.[99] Adjusting for height implies that a child who is scanned around the growth spurt may lie below the 50th percentile as peak height velocity is achieved 6–12 months earlier than peak in bone mass accrual (i.e. bones grow in length first and increases in bone diameter and bone mineralization lag behind).[121] The different rates of linear growth of bone and bone mineralization cause a relative skeletal fragility around the growth spurt, a time that coincides with the peak incidence of fractures during adolescence.[122] Concentrations of bone turnover markers in adolescents vary depending on sex, Tanner stage (pubertal stage), height velocity, as well as skeletal mass and rate of bone mineral accrual, which makes the interpretation of the results difficult.[123] Preliminary findings in young athletes with amenorrhoea have been reported in cross-sectional studies[20,104] (table I) and therefore must be viewed with caution. In summary, despite its limitations, DXA remains the standard method for assessing bone health in amenorrhoeic athletes. Keeping in mind that genetic factors account for 60–80% of the individual variances in aBMD,[124] clinicians can expect aBMD in amenorrhoeic athletes to be higher than the norm or within normal range at loaded skeletal sites, and lower than the norm at non-loaded or moderately loaded sites containing a high proportion of trabecular bone (spine, distal forearm). Growing athletes should be carefully monitored as low energy availability can impact their skeletal development and compromise the attainment of peak bone mass. Increase in skeletal mass slows down at the lumbar spine and femoral neck at 15–16 years in female adolesª 2011 Adis Data Information BV. All rights reserved.
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cents.[125] This cut-off point may not apply to young girls whose skeletal maturation has been delayed. Several case studies have reported increases in aBMD after 20 years or even 30 years of age.[21,24,40] However, full recovery in bone strength might not be achieved because bone mineralization in young adults (after completion of longitudinal growth) usually results in increased BMD, not increased bone size. Therefore, the long-term consequences for bone health may be irreversible. Periods of amenorrhoea or oligomenorrhoea during adolescence have been associated with a lower aBMD in adult women[126] and a greater incidence of osteoporosis in postmenopausal women.[127] History of menstrual dysfunction has also been associated with a greater risk of hip fractures[128] and wrist fractures.[129] These findings have not been confirmed in populations of retired athletes[130] and require further investigations, particularly in athletes who typically present with low spinal aBMD, such as runners and ballet dancers. 3.2 Pharmacological Treatments and Current Issues
A recent literature review investigated the different pharmacological strategies that have been used to treat impaired bone health in women with FHA.[131] The most common intervention consists of treating the hypoestrogenism, either with the oral contraceptive pill (OCP) or other forms of estrogen therapies. 3.2.1 Estrogen Therapy
In 1989, the American Academy of Pediatrics recommended that estrogen supplementation in amenorrhoeic adolescents should only be considered if the individual is 3-years post-menarche and older than 16 years of age.[132] This position has been endorsed by other authors and organizations.[1,118,133] Some state that supplementation could be permitted at a younger age if the athlete has previously sustained a stress fracture.[134] However, the use of OCP and other forms of estrogen therapy in adolescent females and adults with anorexia nervosa and FHA remains controversial.[49,135-137] Longitudinal cohort studies Sports Med 2011; 41 (7)
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have reported either an increase in aBMD[138-140] or a reduction of bone loss[141] in athletes taking OCP (0.020–0.035 mg of ethinyl estradiol + a progestogen) when compared with athletes not taking OCP. In the only large randomized controlled trial ever conducted, the effects of 2 years of OCP treatment (0.030 mg ethinyl estradiol and 0.3 mg norgestrel) on aBMD in both oligo/ amenorrhoeic runners and eumenorrheic runners were inconclusive.[45] The results of this study were confounded by the fact that the women who dropped out from the OCP group were more likely to be amenorrhoeic and to practice disordered eating.[45] Anecdotal evidence from case studies,[21,40,142] and small prospective or retrospective studies (n < 10),[23,143] have also provided contradictory findings on the effects of OCP in amenorrhoeic athletes. Two randomized trials failed to detect an effect on aBMD in 24 amenorrhoeic ballet dancers[47] and 34 oligo/amenorrhoeic runners, when given low doses of estrogens.[46] Many studies that incorporate OCP as a form of treatment are limited by high withdrawal rates,[46] noncompliance to treatment,[45] weight gain during treatment[21,40,45] and spontaneous resumption of menses in controls,[45,46] making it difficult to draw definitive conclusions regarding the effects of estrogen therapies on aBMD in amenorrhoeic athletes.[131] Similarly, the efficacy of estrogen treatment in preventing stress fractures in athletes remains unknown. A stress fracture is a partial or complete bone fracture that is caused by repetitive loading and consequent microtraumas to the bone. Although the magnitude of stress applied to the bone is lower than the stress required to fracture the bone in a single loading, repeated microtraumas can eventually result in bone fracture if microtraumas accumulate faster than they heal.[144] Three prospective cohort studies, one in athletes,[145] and two in military recruits,[146,147] failed to show any protective effect of OCP on the incidence of stress fractures in active women, while a cross-sectional study[148] and a casecontrol study[149] reported a lower use of OCP in athletes who had sustained a stress fracture. In the only randomized controlled trial conducted, randomization to OCP tended to be associated ª 2011 Adis Data Information BV. All rights reserved.
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with a lower incidence of stress fractures – 18 stress fractures occurred over 2 years, 6 stress fractures were sustained by runners randomized to OCP and 12 stress fractures were sustained by control runners.[45] The evidence supporting the use of estrogen treatment for stress fracture prevention in athletes remains inconclusive. Current studies are limited in their findings due to the use of self-reported non-documented stress fractures,[148] potential confounders such as body weight or training volume,[148] small sample size,[149] a relatively low number of stress fractures[45,145,148,149] and poor compliance to placebo or treatment with OCP.[45] Importantly, oligo/amenorrhoea was not an inclusion criterion in most of these studies.[45,145-147,149] Different factors could explain the lack of efficacy of estrogen therapy on aBMD and stress fractures risk. Estrogen therapy is used in postmenopausal women to prevent the hypoestrogenism-induced increase in bone resorption.[150-152] Estrogen replacement has also been shown to have positive effects on aBMD in young women with primary ovarian insufficiency.[153] However, bone resorption is not necessarily elevated in amenorrhoeic athletes (table I), in which case estrogen therapy is unlikely to have any further anti-resorptive effects.[137] Amenorrhoea in athletes is associated with a range of disturbances in hormones and nutrients including a decrease in total tri-iodothyronine, leptin, insulin, IGF-1/IGF-binding protein-1, glucose, luteinizing hormone pulsatility, folliclestimulating hormone, estradiol and progesterone, as well as an increase in growth hormone and cortisol.[59,61,102,103,154,155] Estrogen therapy is unlikely to normalize the metabolic factors that impair bone formation, which might explain its lack of efficacy in improving aBMD or reducing bone loss. Specific concerns have also been raised regarding exogenous estrogen administration in athletes with amenorrhoea. In women with FHA, OCP use might have a detrimental effect on androgen secretion,[156] and this could ultimately be detrimental for aBMD.[156] In growing athletes, exogenous estrogen may induce premature closure of the epiphyses[1] and compromise the attainment of full length of long bones.[92,157] Sports Med 2011; 41 (7)
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3.2.2 Bisphosphonates and Other Anti-Osteoporotic Therapies
Bisphosphonates, which markedly reduce bone turnover, have emerged as one of the leading effective treatments for postmenopausal and other forms of osteoporosis.[158] Bisphosphonates adhere to the bone surface, impair osteoclast function and induce apoptosis by inhibiting a key enzyme in the mevalonate pathway.[159] Using bisphosphonates for preventing[160] or treating[161] stress fractures in female athletes has also been studied. Findings indicated that risedronate did not reduce the incidence of stress fractures in military recruits, but the study suffered from a 60–70% dropout rate.[160] In another trial using bisphosphonates as a treatment for stress fracture, a weekly dose of intravenous pamidronate over a 5-week period permitted four of five athletes with tibial stress fractures to return to their previous training regimen within 1 week of initiating the intervention, but fracture recurrence was not reported.[161] Most importantly, long-term effects of bisphosphonates are unknown and side effects (stomach pain and bloating) have been reported in athletes.[142] The Medical Commission of the IOC does not approve of the use of bisphosphonates in premenopausal women[44] due to the long half-life of bisphosphonates in bones (up to 10 years) and their potential teratogenic effect on the fetus during future pregnancies.[13,134] 3.2.3 Other Pharmacological Therapies
Other therapies, including recombinant human IGF-1 (rhIGF-I)[162-164] and androgens[165,166] have been tested in amenorrhoeic women with anorexia nervosa.[131] Due to the less extreme pathophysiology of the female athlete triad,[167] these treatments have not been tested in female athletes with amenorrhoea. Recombinant human leptin (rhLeptin) may improve markers of bone formation in women with FHA.[168] Although calcium and vitamin D supplementation are frequently prescribed for amenorrhoeic athletes,[41] these nutrient supplements have never been prospectively assessed as an intervention using aBMD as an outcome variable. Currently there is no consensus as to the appropriate dosage and form of calcium and vitamin D suppleª 2011 Adis Data Information BV. All rights reserved.
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mentation for this population. The Medical Commission of the IOC recommends a calcium intake of at least 1500 mg/day,[44] whereas the ACSM guidelines indicate 1000–1300 mg/day.[1] Low levels of vitamin D are a concern worldwide.[169,170] The criterion to define vitamin D deficiency varies, although serum 25-hydroxyvitamin D concentrations below 50 mmol/L (20 ng/mL) are commonly used.[170] This threshold is largely debated and some experts have suggested that serum 25-hydroxyvitamin D levels above 75 nmol/L (30 ng/mL) maximize the health benefits of vitamin D.[169,171] Athletes engaged in indoor sports are at greater risk of vitamin D deficiency,[172] which may affect their muscle function, bone strength and performance.[173-175] An appropriate dose of vitamin D is 400 IU[176] to 800 IU per day, which combined with an adequate calcium dosage, may aid in the reduction of stress fractures.[147] In summary, none of the pharmacological strategies have demonstrated efficacy in correcting bone health abnormalities, including low aBMD in oligo- and amenorrhoeic athletes.[1] Although low-dose oral contraceptive (<35 mg of estrogen per day) has been suggested to be an appropriate treatment in amenorrhoeic athletes,[177] evidence to support such a conclusion is weak.[140] The criteria for initiating estrogen therapy, the optimal mode of therapy (estrogen alone or combined with a progestogen) and dosing schedule have not been defined.[177] Further studies are needed to clarify the potential risks and benefits of estrogen therapy in amenorrhoeic athletes. More research is also needed to define optimal vitamin D levels and to quantify the best combinations of calcium and vitamin D dosages necessary to achieve a protective effect on bone health. 3.3 Non-Pharmacological Approaches 3.3.1 First-Line Strategy: Increasing Energy Availability
The recommended first-line treatment strategy for athletes with oligo- and amenorrhoea consists in increasing energy availability by increasing dietary intake, decreasing energy expenditure, or both.[1] The strongest evidence that supports bone health improvements resulting from implementing this strategy comes from longitudinal Sports Med 2011; 41 (7)
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data obtained in girls or women with anorexia nervosa.[131] Both components of recovery (body weight gain, resumption of menses) are thought to have independent and additive effects on bone health.[136,178-183] For instance, a 38% increase in body weight over 3 months was associated with significant increases in aBMD in anorexic women, despite persistence of amenorrhoea (+2.6% and +1.1% at the hip and spine, respectively). Increases in spinal aBMD were found to be conditional on resumption of menses,[181] whereas hip aBMD was found to be more responsive to weight gain.[181,184] Similar studies looking at partial or full recovery (body weight gain and/or resumption of menses) in female athletes are scarce. A 2-year follow-up in five amenorrhoeic dancers showed that in the first year the increase in spinal aBMD was correlated to the increase in caloric intake and in the second year, spinal aBMD increase was correlated to weight gain.[185] The two dancers who had the largest increases in spinal aBMD during the first year (+18.8 and +20%) also had weight gain (+4.1 and +3.6 kg) and three menses during the year.[185] A study in runners showed that when an injury or illness forced athletes to decrease their mileage and participate in activities other than running, the athletes’ menses resumed and weight gain (+1.9 kg) occurred. When the athletes were reassessed at 15.5 months, spinal aBMD had increased by 6.3% compared with baseline (p < 0.01).[186] Even though aBMD may increase with weight gain and/or resumption of menses after 20[21,24] and 30 years of age,[40] athletes may fail to normalize aBMD.[25,62,142,185] In a study that included both dancers and nondancers (n = 50; 19 with amenorrhoea), the seven participants who resumed menses over the 2-year follow-up showed a 17% increase in spinal aBMD (vs 4% in those who remained amenorrhoeic), but their aBMD remained below aBMD in the eumenorrhoeic participants.[62] Further investigations using 3-dimensional imaging techniques are needed as DXA-derived outcomes are influenced by changes in body weight and body composition. Two studies provide preliminary data on the effectiveness of an intervention to increase energy availability in small groups of athletes (n = 4–7).[187,188] A decrease in training load by ª 2011 Adis Data Information BV. All rights reserved.
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43% in four amenorrhoeic female runners resulted in a 5% increase in body weight, increased estradiol levels to within normal range, resumption of menses, and a 6% increase in spinal aBMD over 15 months.[188] The three other participants who did not decrease their training load remained amenorrhoeic.[188] Although adding a day of rest in the training schedule sounds like a reasonable treatment approach in active amenorrhoeic athletes, it was found that the benefits may be offset by an increase in training volume on alternate days.[187] This study, where the intervention combined a reduction in energy expenditure and an increase in energy intake, did not include bone status as a means to validate treatment outcomes in amenorrhoeic athletes.[187] Experiments in female monkeys showed that the number of days required for amenorrhoeic exercising monkeys to resume menses was directly proportional to the number of extra calories consumed per day. For example, animals that ate more daily calories recovered menses more quickly.[189] Further trials on larger samples are needed to determine the relationship between the increase in energy availability and the timing in which menses and bone restoration may return. It is important to mention that poor diet quality (deficiencies in minerals and vitamins, e.g. iron and vitamin D, respectively) often results from low energy availability. This aspect should not be overlooked when strategies to increase energy availability are employed. 3.3.2 Other Non-Pharmacological Strategies to Improve Bone Health
Instructing an athlete to participate in resistance training by changing a work-out routine from cardiovascular to weight-training is one of the recommended strategies reported by American Physical Therapy Association to treat the female athlete triad in an effort to reduce energy expenditure and increase aBMD.[51,52] Progressive high-intensity resistance training in premenopausal women was shown to increase absolute aBMD at the lumbar spine[190,191] and at the total forearm (although exercises with impacts might be more beneficial at that skeletal site).[192] Part of these skeletal adaptations are due to the fact that Sports Med 2011; 41 (7)
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a new form of exercise such as resistance training introduces variety in the loading pattern of the skeleton, which is beneficial for bone strength. The effects of resistance training alone or as part of a multidisciplinary exercise programme have been investigated in anorexic girls[193] and women.[194-197] Overall, resistance training improved body composition, muscle strength and psychological well-being, but the effects on aBMD were not investigated. Resistance training has been suggested as an alternative to weight-bearing exercises for stress fracture prevention in athletes participating in high-impact sports.[52] Resistance exercise programmes to improve bone health typically include three sets of 8–12 repetitions of 6–10 exercises at ~80% one-repetition maximum (1RM: maximum weight that can be lifted once), with 1–2 minutes of rest between exercises and a progressive increase in intensity. The recommended frequency of performing resistance exercises is three times/week, as resistance training programmes performed only 1–2 times/week[198,199] have been shown to be less effective in premenopausal women. Plyometric exercises, characterized by highintensity, explosive muscular contractions, are another form of exercise that can be substituted to usual training routines to improve bone health. Interventions including various jumping exercises have been shown to improve aBMD at the hip and spine in girls.[200,201] The osteogenic effects varied with stages of puberty, and may sometimes be masked by the overwhelming effect of growth on aBMD. In adults, studies have reported positive effects of plyometrics on aBMD at the hip after only 6 months of training,[202] or hip and spine after 18 months of training.[203] To target non-weightbearing skeletal sites that do not benefit from jumping exercises,[203] upper body plyometric exercises can be performed (e.g. throwing).[204] The main limitation of plyometrics is that these exercises are not recommended when returning from a stress fracture injury. Plyometrics can be combined with resistance training to maximize skeletal benefits.[205] 3.3.3 Specific Considerations for Stress Fractures
Experience has shown that convincing athletes to increase their energy intake and/or reduce their ª 2011 Adis Data Information BV. All rights reserved.
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training volume can be very challenging. A common training error is failing to incorporate training periodization, the allowance of active rest cycles during a weekly training regimen.[51] This training error can lead to stress fractures. The stress fracture rate in athletes/military recruits with menstrual dysfunction is 2- to 4-fold higher than in athletes/military recruits with normal menstrual cycles.[18] Due to the role of estrogen receptor alpha in mechanotransduction,[206] hypoestrogenism may impair the capacity of the osteocytes to respond to repetitive loading, inducing an accumulation of microdamage, stress reaction and eventually stress fracture.[207,208] The adverse effects on bone may not always translate to findings of low aBMD on a DXA scan because long-term repetitive loading may compensate for the negative effect of hypoestrogenism.[19] Findings are contradictory as to whether a relationship between stress fractures and low aBMD exists.[209-215] Bone geometry and estimates of bone strength, rather than aBMD, might be more relevant parameters when assessing stress fracture risk.[213,216-220] For example, individuals with ‘slender bones’ might be more susceptible to stress fractures when long bones are subjected to extreme loading, such as in military training.[221] The incidence of stress fractures may also be affected by poor muscle strength[18] and training-induced muscle fatigue.[222] Diminished muscular support surrounding the joints may cause increased tensile forces and shear stresses on the bone and joint surfaces, which can potentially, over time, lead to injury. Finally, alterations in trabecular bone microarchitecture, possibly caused by hypoestrogenism, have been reported in fractured female athletes[223] and might contribute to the aetiology of stress fractures. Amenorrhoeic athletes who have sustained a stress fracture need to recognize the time allowance that is required for proper tissue healing and the avoidance of future bone fractures. A restriction in the amount and intensity of exercise necessary to heal bone may be a potential source of frustration and depression for the athlete.[51,52,224] To avoid focusing on activity restriction, athletes can be directed to perform Sports Med 2011; 41 (7)
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non-weight-bearing activities,[224] and resistive, balance or coordination exercises using variations in the applied mechanical loads.[224,225] Cross-training, i.e. replacing a training session in the athlete’s specialty (e.g. running) with a dissimilar mode of exercise (e.g. cycling), can provide physiological and psychological benefits to the athlete while reducing or modifying the biomechanical demand placed on the musculoskeletal system, and perhaps, the energetic demand, depending on the exercise volume of the session.[51,52] A reduction in energy expenditure without reducing the number of training sessions can also be achieved by having the athlete work on technical and tactical skills, video analysis of sport skills and performance, sport visualization and cognitive techniques. 4. Conclusions and Perspectives The female athlete triad has drawn much attention from the research community in the past 30 years. Low energy availability and menstrual dysfunction place female athletes at greater risk for sustaining stress fractures, as well as osteoporotic fractures later in life. Evidence regarding the efficacy of treatment to prevent fractures is lacking because conducting trials with bone fracture as a major outcome typically requires large sample sizes and long-term follow-up studies. Previous studies in anorexic girls/women and female athletes indicate that an increase in energy availability through refeeding and/or decreasing energy expenditure is sometimes accompanied by positive outcomes for aBMD, i.e. the maintenance or increase in aBMD. This strategy should prevail over pharmacological therapies whose efficacy has not been proven. Evaluation of bone health in exercising women has relied on the measurement of aBMD by DXA, which has inherent limitations particularly in growing subjects. Further investigations using 3-dimensional imaging techniques are needed to clarify the effects of low energy availability on bone strength, and the capacity to recover bone strength with weight gain and/or resumption of menses. Advancing research and knowledge in bone health related to the female athlete triad is ª 2011 Adis Data Information BV. All rights reserved.
essential to ensure that all women can receive the physical and psychological benefits that are associated with exercise participation. Acknowledgements No funding was used to assist in the preparation of the manuscript. The authors have no conflict of interest.
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Correspondence: Dr Gaele Ducher, 123 Noll Laboratory, Department of Kinesiology, Penn State University, University Park, PA 16802, USA. E-mail:
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CORRESPONDENCE
ª 2011 Adis Data Information BV. All rights reserved.
Comments on ‘Expert Performance in Sport and the Dynamics of Talent Development’ It is always good to see reviews, such as the recent article by Phillips et al.,[1] which challenge the extant, simplistic, mono-disciplinary approaches to talent identification and development that are still common in the literature.[2,3] We are also completely in accord with the complex systems approach espoused; indeed, as coauthors and collaborators of one of the first papers to suggest this approach,[4] we are clearly supporters. We do have concerns, however, that relate to the limited scope of the paper. One of the most positive features of the complex systems approach is its consideration of interactions between contributory factors. All the more surprising, therefore, to find the factors highlighted by Phillips et al. are limited to those below the neck, despite a growing literature on the importance of psycho-behavioural constructs in the evolution of talent.[5-11] In a typical study, Van Yperen[5] demonstrates the predictive validity of psycho-behavioural constructs to success in professional football, even when initial performance level is controlled. In simple terms, these characteristics seem to be the driving force that underpins the developing performer’s exploitation of the various environmental factors and physical gifts they experience. In short, this represents a way in which the ‘intrinsic dynamics’[12] of the individual can best be exploited or, sometimes, even overcome. The closest Phillips et al. get to acknowledging this important contribution is their suggestion that the pathway ‘‘requires complimentary cognitive attributes (e.g. confidence, sacrifice, dedication and perseverance)’’ [p 279].[1] As such, we would suggest that their view is somewhat beheaded, or at the very least lobotomized. A similar issue relates to the social environment in which development takes place; the authors’ use of environment seems much more related to
the practice ‘conditions’ than to the wider context. Once again, there is a broad literature on the impact of the social setting for talent development, encompassing the environment itself,[13] social support available[14] and the promotion of individual characteristics.[8] Such factors surely underpin the ‘Wagga effect’[15] and the birth place effect,[16] both of which are cited but seemingly mechanistically unconsidered by the authors. The social impact is also missed as a critical qualifier of cited findings. For example, the paper cites Durand-Bush and Salmela[17] as reporting that all experts undergo the stages of Coˆte´ and Hay’s[18] ‘‘developmental model of sports participation,’’ namely ‘‘sampling, specialization and investment,’’ in their pathway to the top. Once again, more recent research[19] is suggesting that these stages may be socially specific, with few if any British athletes exhibiting a specialization stage in their pathway to high-level performance. In summary, the excellent coverage otherwise provided by Phillips et al.[1] seems to miss the psychosocial factors that, we suggest, play a crucial role in the realization of talent. Indeed, it may be that these factors could be considered as ‘‘generic emergenics’’ (cf. Simonton[20]), in that they seem to facilitate the emergence of superior expertise pan domain.[21,22] It may be that, as Phillips et al. claim, ‘‘Dynamical systems theory and the complexity sciences might provide the basis of an interactionist perspective on expertise acquisition in sports’’ (p 280).[1] However, we would suggest that it is more generically and psychosocially driven than the purported and essentially individualistic chaos that complex systems approaches may espouse. Dave Collins and Aine MacNamara Institute of Coaching and Performance, University of Central Lancashire, Preston, UK
Acknowledgements The authors have no conflicts of interest that are directly relevant to the content of this letter.
References 1. Phillips E, Davids K, Renshaw I, et al. Expert performance in sport and the dynamics of talent development. Sports Med 2010; 40 (4): 271-83
610
2. Hoare DG, Warr C. Talent identification and women’s soccer: an Australian experience. J Sports Sci 2000; 18: 751-8 3. Mohamed H, Vaeyens R, Matthys S, et al. Anthropometric and performance measures for the development of a talent detention and identification model in youth handball. J Sports Sci 2009; 27: 257-66 4. Abbott A, Button C, Pepping G-J, et al. Unnatural selection: talent identification and development in sport. Nonlin Dynam Psychol Life Sci 2005; 9 (1): 61-88 5. Van Yperen NW. Why some make it and others do not: identifying psychological factors that predict career success in professional adult soccer. The Sport Psychologist 2009; 23: 317-29 6. Abbott A, Collins D. Eliminating the dichotomy between theory and practice in talent identification and development: considering the role of psychology. J Sports Sci 2004; 22 (5): 395-408 7. MacNamara A´, Button A, Collins D. The role of psychological characteristics in facilitating the pathway to elite performance. Part 1: identifying mental skills and behaviours. The Sport Psychologist 2010; 24: 52-73 8. MacNamara A´, Button A, Collins D. The role of psychological characteristics in facilitating the pathway to elite performance. Part 2: examining environmental and stage related differences in skills and behaviours. The Sport Psychologist 2010; 24: 74-96 9. Toering T, Elferink-Gemser M, Jordet G, et al. Self-regulation and performance level of elite and non-elite youth soccer players. J Sports Sci 2009; 27 (14): 1509-17 10. Baker J, Horton S. A review of primary and secondary influences on sport expertise. High Ability Studies 2004; 15: 211-28 11. Ward P, Hodges N, Williams A, et al. Deliberate practice and expert performance: defining the path to excellence. In: Williams AM, Hodges NJ, editors. Skill acquisition in sport: research, theory and practice. London: Routledge, 2004: 231-58 12. Thelen E. Motor development: a new synthesis. Am Psychol 1995; 50 (2): 79-95 13. Martindale RJJ, Collins D, Daubney J. A critical review of talent development and implications for sport. Quest 2005; 57: 353-75 14. Holt N, Dunn JG. Towards a grounded theory of the psychosocial competencies and environmental conditions associated with soccer success. J Appl Sport Psychol 2004; 16: 199-219 15. Abernethy B. Sport expertise: from theory to practice. In: Farrow D, editor. Proceedings of the Applied Sport Expertise and Learning Workshop; 2005 [CD1]; Canberra (ACT): Australian Institute of Sport, 2005 16. Coˆte´ J, Macdonald DJ, Baker J, et al. When ‘‘where’’ is more important than ‘‘when’’: birthplace and birthdate effects on the achievement of sporting expertise. J Sports Sci 2006; 24 (10): 1065-73 17. Durand-Bush N, Salmela J. The development and maintenance of expert athletic performance: perceptions of world and Olympic champions. J Appl Sport Psychol 2002; 14 (3): 154-71 18. Coˆte´ J, Hay J. Children’s involvement in sport: a developmental perspective. Boston (MA): Allyn and Bacon, 2002 19. Bailey R, Toms M, Collins D, et al. Models of young player development in sport. In: Bailey R, Stafford I, editors.
ª 2011 Adis Data Information BV. All rights reserved.
Letter to the Editor
Coaching children in sport. London: Routledge, 2011: 38-56 20. Simonton DK. Talent and its development: an emergenic and epigenetic model. Psychol Rev 1999; 106 (3): 435-57 21. MacNamara A´, Holmes P, Collins D. Negotiating transitions in musical development: the role of psychological characteristics of developing excellence. Psychol of Music 2008; 36: 335-52 22. MacNamara A´, Collins D. The role of psychological characteristics in managing the transition to university. Psychol Sport and Exerc 2010; 11: 353-62
The Authors’ Reply In our article entitled Expert Performance in Sport and the Dynamics of Talent Development,[1] we provided a multidisciplinary theoretical framework for expertise in sport and talent development, arguing that the most relevant focus of study concerns the performer-environment relationship, not a separate focus on each of these factors.[1,2] This article complemented our other work that proposed how performer-environment relations frame a comprehensive understanding of skill acquisition and problem-solving processes in neurobiology.[3,4] In these articles, we highlighted the clear weaknesses of approaches that display what Dunwoody[5] termed an ‘organismic asymmetry’ – a fixation with performer-based explanations for emergent behaviours (see also Davids and Arau´jo[6]). This critical point should not pass over the heads of readers. Expertise in sport emerges from the continuous interaction of a multitude of constraints and does not solely or separately emanate from environmental or personal factors, as we discussed in our article. This ecological dynamics theoretical orientation should not be confused with an environmentalist stance, a misconception of our theoretical position and a misunderstanding of the term ‘ecology’, which emphasizes the relations between organisms and their environments (for an example of this misconception see comments by Gagne´[7]). For sports science to move beyond description and improve theoretical understanding of key concepts such as skill, transfer, expertise and talent development, we have advocated[1,5-7] the need to avoid a biased fixation on a single category of constraint alone. Understanding the interSports Med 2011; 41 (7)
Letter to the Editor
action of psycho-social constraints with physical and environmental constraints on behaviour is indeed an important challenge for scientists, but one that requires an emphasis on ‘embodied cognition’,[8] a different ‘headspace’ to that proposed by Collins and MacNamara.[9] This proposal is completely harmonious with the ideas of Van Yperen,[10] who observed that success in sport was not just shaped by psycho-behavioural constructs but also ‘‘influenced by a variety of additional psychological, physical, social, and organizational factors’’ (p 326). Elissa Phillips,1 Keith Davids,2 Duarte Araujo,3 Ian Renshaw2 and Marc Portus4 1 Institute of Sport, Exercise and Active Living & School of Sport and Exercise Science, Victoria University, Melbourne, VIC, Australia 2 Institute for Health and Biomedical Innovation & School of Human Movement Studies, Queensland University of Technology, Brisbane, QLD, Australia 3 Faculty of Human Movement Science, Technical University of Lisbon, Lisbon, Portugal 4 Sport Science Sport Medicine Unit, Cricket Australia Centre of Excellence, Brisbane, QLD, Australia
ª 2011 Adis Data Information BV. All rights reserved.
611
Acknowledgements The authors have no conflicts of interest that are directly relevant to the content of this letter.
References 1. Phillips E, Davids K, Renshaw I, et al. Expert performance in sport and the dynamics of talent development. Sports Med 2010; 40 (4): 271-83 2. Phillips E, Davids K, Renshaw I, et al. Developmental trajectories of fast bowling experts in Australian cricket. Tal Dev Excel 2010; 2: 137-48 3. Arau´jo D, Davids K. What exactly is acquired during skill acquisition? J Conscious Stud 2011; 18: 7-23 4. Davids K, Arau´jo D. Perception of affordances in multiscale dynamics as an alternative explanation for equivalence of analogical and inferential reasoning in animals and humans. Theory Psychol 2010; 20: 125-34 5. Dunwoody PT. The neglect of the environment by cognitive psychology. J Theor Phil Psychol 2006; 26: 139-53 6. Davids K, Arau´jo D. The concept of ‘Organismic Asymmetry’ in sport science. J Sci Med Sport 2010; 13: 633-40 7. Gagne´ F. ‘‘Some’’ equity through meritocracy: a rejoinder to 32 comments. Tal Dev Excel 2011; 3: 131-63 8. Chemero A. Radical embodied cognitive science. Cambridge: MIT Press, 2009 9. Collins D, MacNamara A. Comments on ‘Expert performance in sport and the dynamics of talent development’ [letter]. Sports Med 2011; 41 (7): 609-10 10. Van Yperen NW. Why some make it and others do not: identifying psychological factors that predict career success in professional adult soccer. The Sport Psychologist 2009; 23: 317-29
Sports Med 2011; 41 (7)
Sports Med 2011; 41 (7): 609-611 0112-1642/11/0007-0609/$49.95/0
CORRESPONDENCE
ª 2011 Adis Data Information BV. All rights reserved.
Comments on ‘Expert Performance in Sport and the Dynamics of Talent Development’ It is always good to see reviews, such as the recent article by Phillips et al.,[1] which challenge the extant, simplistic, mono-disciplinary approaches to talent identification and development that are still common in the literature.[2,3] We are also completely in accord with the complex systems approach espoused; indeed, as coauthors and collaborators of one of the first papers to suggest this approach,[4] we are clearly supporters. We do have concerns, however, that relate to the limited scope of the paper. One of the most positive features of the complex systems approach is its consideration of interactions between contributory factors. All the more surprising, therefore, to find the factors highlighted by Phillips et al. are limited to those below the neck, despite a growing literature on the importance of psycho-behavioural constructs in the evolution of talent.[5-11] In a typical study, Van Yperen[5] demonstrates the predictive validity of psycho-behavioural constructs to success in professional football, even when initial performance level is controlled. In simple terms, these characteristics seem to be the driving force that underpins the developing performer’s exploitation of the various environmental factors and physical gifts they experience. In short, this represents a way in which the ‘intrinsic dynamics’[12] of the individual can best be exploited or, sometimes, even overcome. The closest Phillips et al. get to acknowledging this important contribution is their suggestion that the pathway ‘‘requires complimentary cognitive attributes (e.g. confidence, sacrifice, dedication and perseverance)’’ [p 279].[1] As such, we would suggest that their view is somewhat beheaded, or at the very least lobotomized. A similar issue relates to the social environment in which development takes place; the authors’ use of environment seems much more related to
the practice ‘conditions’ than to the wider context. Once again, there is a broad literature on the impact of the social setting for talent development, encompassing the environment itself,[13] social support available[14] and the promotion of individual characteristics.[8] Such factors surely underpin the ‘Wagga effect’[15] and the birth place effect,[16] both of which are cited but seemingly mechanistically unconsidered by the authors. The social impact is also missed as a critical qualifier of cited findings. For example, the paper cites Durand-Bush and Salmela[17] as reporting that all experts undergo the stages of Coˆte´ and Hay’s[18] ‘‘developmental model of sports participation,’’ namely ‘‘sampling, specialization and investment,’’ in their pathway to the top. Once again, more recent research[19] is suggesting that these stages may be socially specific, with few if any British athletes exhibiting a specialization stage in their pathway to high-level performance. In summary, the excellent coverage otherwise provided by Phillips et al.[1] seems to miss the psychosocial factors that, we suggest, play a crucial role in the realization of talent. Indeed, it may be that these factors could be considered as ‘‘generic emergenics’’ (cf. Simonton[20]), in that they seem to facilitate the emergence of superior expertise pan domain.[21,22] It may be that, as Phillips et al. claim, ‘‘Dynamical systems theory and the complexity sciences might provide the basis of an interactionist perspective on expertise acquisition in sports’’ (p 280).[1] However, we would suggest that it is more generically and psychosocially driven than the purported and essentially individualistic chaos that complex systems approaches may espouse. Dave Collins and Aine MacNamara Institute of Coaching and Performance, University of Central Lancashire, Preston, UK
Acknowledgements The authors have no conflicts of interest that are directly relevant to the content of this letter.
References 1. Phillips E, Davids K, Renshaw I, et al. Expert performance in sport and the dynamics of talent development. Sports Med 2010; 40 (4): 271-83
610
2. Hoare DG, Warr C. Talent identification and women’s soccer: an Australian experience. J Sports Sci 2000; 18: 751-8 3. Mohamed H, Vaeyens R, Matthys S, et al. Anthropometric and performance measures for the development of a talent detention and identification model in youth handball. J Sports Sci 2009; 27: 257-66 4. Abbott A, Button C, Pepping G-J, et al. Unnatural selection: talent identification and development in sport. Nonlin Dynam Psychol Life Sci 2005; 9 (1): 61-88 5. Van Yperen NW. Why some make it and others do not: identifying psychological factors that predict career success in professional adult soccer. The Sport Psychologist 2009; 23: 317-29 6. Abbott A, Collins D. Eliminating the dichotomy between theory and practice in talent identification and development: considering the role of psychology. J Sports Sci 2004; 22 (5): 395-408 7. MacNamara A´, Button A, Collins D. The role of psychological characteristics in facilitating the pathway to elite performance. Part 1: identifying mental skills and behaviours. The Sport Psychologist 2010; 24: 52-73 8. MacNamara A´, Button A, Collins D. The role of psychological characteristics in facilitating the pathway to elite performance. Part 2: examining environmental and stage related differences in skills and behaviours. The Sport Psychologist 2010; 24: 74-96 9. Toering T, Elferink-Gemser M, Jordet G, et al. Self-regulation and performance level of elite and non-elite youth soccer players. J Sports Sci 2009; 27 (14): 1509-17 10. Baker J, Horton S. A review of primary and secondary influences on sport expertise. High Ability Studies 2004; 15: 211-28 11. Ward P, Hodges N, Williams A, et al. Deliberate practice and expert performance: defining the path to excellence. In: Williams AM, Hodges NJ, editors. Skill acquisition in sport: research, theory and practice. London: Routledge, 2004: 231-58 12. Thelen E. Motor development: a new synthesis. Am Psychol 1995; 50 (2): 79-95 13. Martindale RJJ, Collins D, Daubney J. A critical review of talent development and implications for sport. Quest 2005; 57: 353-75 14. Holt N, Dunn JG. Towards a grounded theory of the psychosocial competencies and environmental conditions associated with soccer success. J Appl Sport Psychol 2004; 16: 199-219 15. Abernethy B. Sport expertise: from theory to practice. In: Farrow D, editor. Proceedings of the Applied Sport Expertise and Learning Workshop; 2005 [CD1]; Canberra (ACT): Australian Institute of Sport, 2005 16. Coˆte´ J, Macdonald DJ, Baker J, et al. When ‘‘where’’ is more important than ‘‘when’’: birthplace and birthdate effects on the achievement of sporting expertise. J Sports Sci 2006; 24 (10): 1065-73 17. Durand-Bush N, Salmela J. The development and maintenance of expert athletic performance: perceptions of world and Olympic champions. J Appl Sport Psychol 2002; 14 (3): 154-71 18. Coˆte´ J, Hay J. Children’s involvement in sport: a developmental perspective. Boston (MA): Allyn and Bacon, 2002 19. Bailey R, Toms M, Collins D, et al. Models of young player development in sport. In: Bailey R, Stafford I, editors.
ª 2011 Adis Data Information BV. All rights reserved.
Letter to the Editor
Coaching children in sport. London: Routledge, 2011: 38-56 20. Simonton DK. Talent and its development: an emergenic and epigenetic model. Psychol Rev 1999; 106 (3): 435-57 21. MacNamara A´, Holmes P, Collins D. Negotiating transitions in musical development: the role of psychological characteristics of developing excellence. Psychol of Music 2008; 36: 335-52 22. MacNamara A´, Collins D. The role of psychological characteristics in managing the transition to university. Psychol Sport and Exerc 2010; 11: 353-62
The Authors’ Reply In our article entitled Expert Performance in Sport and the Dynamics of Talent Development,[1] we provided a multidisciplinary theoretical framework for expertise in sport and talent development, arguing that the most relevant focus of study concerns the performer-environment relationship, not a separate focus on each of these factors.[1,2] This article complemented our other work that proposed how performer-environment relations frame a comprehensive understanding of skill acquisition and problem-solving processes in neurobiology.[3,4] In these articles, we highlighted the clear weaknesses of approaches that display what Dunwoody[5] termed an ‘organismic asymmetry’ – a fixation with performer-based explanations for emergent behaviours (see also Davids and Arau´jo[6]). This critical point should not pass over the heads of readers. Expertise in sport emerges from the continuous interaction of a multitude of constraints and does not solely or separately emanate from environmental or personal factors, as we discussed in our article. This ecological dynamics theoretical orientation should not be confused with an environmentalist stance, a misconception of our theoretical position and a misunderstanding of the term ‘ecology’, which emphasizes the relations between organisms and their environments (for an example of this misconception see comments by Gagne´[7]). For sports science to move beyond description and improve theoretical understanding of key concepts such as skill, transfer, expertise and talent development, we have advocated[1,5-7] the need to avoid a biased fixation on a single category of constraint alone. Understanding the interSports Med 2011; 41 (7)
Letter to the Editor
action of psycho-social constraints with physical and environmental constraints on behaviour is indeed an important challenge for scientists, but one that requires an emphasis on ‘embodied cognition’,[8] a different ‘headspace’ to that proposed by Collins and MacNamara.[9] This proposal is completely harmonious with the ideas of Van Yperen,[10] who observed that success in sport was not just shaped by psycho-behavioural constructs but also ‘‘influenced by a variety of additional psychological, physical, social, and organizational factors’’ (p 326). Elissa Phillips,1 Keith Davids,2 Duarte Araujo,3 Ian Renshaw2 and Marc Portus4 1 Institute of Sport, Exercise and Active Living & School of Sport and Exercise Science, Victoria University, Melbourne, VIC, Australia 2 Institute for Health and Biomedical Innovation & School of Human Movement Studies, Queensland University of Technology, Brisbane, QLD, Australia 3 Faculty of Human Movement Science, Technical University of Lisbon, Lisbon, Portugal 4 Sport Science Sport Medicine Unit, Cricket Australia Centre of Excellence, Brisbane, QLD, Australia
ª 2011 Adis Data Information BV. All rights reserved.
611
Acknowledgements The authors have no conflicts of interest that are directly relevant to the content of this letter.
References 1. Phillips E, Davids K, Renshaw I, et al. Expert performance in sport and the dynamics of talent development. Sports Med 2010; 40 (4): 271-83 2. Phillips E, Davids K, Renshaw I, et al. Developmental trajectories of fast bowling experts in Australian cricket. Tal Dev Excel 2010; 2: 137-48 3. Arau´jo D, Davids K. What exactly is acquired during skill acquisition? J Conscious Stud 2011; 18: 7-23 4. Davids K, Arau´jo D. Perception of affordances in multiscale dynamics as an alternative explanation for equivalence of analogical and inferential reasoning in animals and humans. Theory Psychol 2010; 20: 125-34 5. Dunwoody PT. The neglect of the environment by cognitive psychology. J Theor Phil Psychol 2006; 26: 139-53 6. Davids K, Arau´jo D. The concept of ‘Organismic Asymmetry’ in sport science. J Sci Med Sport 2010; 13: 633-40 7. Gagne´ F. ‘‘Some’’ equity through meritocracy: a rejoinder to 32 comments. Tal Dev Excel 2011; 3: 131-63 8. Chemero A. Radical embodied cognitive science. Cambridge: MIT Press, 2009 9. Collins D, MacNamara A. Comments on ‘Expert performance in sport and the dynamics of talent development’ [letter]. Sports Med 2011; 41 (7): 609-10 10. Van Yperen NW. Why some make it and others do not: identifying psychological factors that predict career success in professional adult soccer. The Sport Psychologist 2009; 23: 317-29
Sports Med 2011; 41 (7)
