The term Relative Energy Deficiency in Sport was introduced by the International Olympic Committee in 2014. It refers to the potential health and performance consequences of inadequate energy for sport, emphasizing that there are consequences of low energy availability (EA; typically defined as <30 kcal·kg−1 fat-free mass·day−1) beyond the important and well-established female athlete triad, and that low EA affects populations other than women. As the prevalence and consequences of Relative Energy Deficiency in Sport become more apparent, it is important to understand the current knowledge of the hormonal changes that occur with decreased EA. This paper highlights endocrine changes that have been observed in female and male athletes with low EA. Where studies are not available in athletes, results of studies in low EA states, such as anorexia nervosa, are included. Dietary intake/appetite-regulating hormones, insulin and other glucose-regulating hormones, growth hormone and insulin-like growth factor 1, thyroid hormones, cortisol, and gonadal hormones are all discussed. The effects of low EA on body composition, metabolic rate, and bone in female and male athletes are presented, and we identify future directions to address knowledge gaps specific to athletes.
Endocrine Effects of Relative Energy Deficiency in Sport
Kirsty J. Elliott-Sale, Adam S. Tenforde, Allyson L. Parziale, Bryan Holtzman, and Kathryn E. Ackerman
Female Athlete Triad/Relative Energy Deficiency in Sport: A Perspective Interview With Professor Barbara Drinkwater
Barbara Drinkwater has been a lifelong champion of equality for women in many areas of life well before it was widely accepted. Her “walking the walk” of women breaking barriers in traditional male roles in administration and leadership is exemplified by her election as the first woman president of the American College of Sports Medicine in 1988. Some of the controversial areas in which Barbara was vocal in the arena of women in sport, besides triad/relative energy deficiency in sport, include increased opportunity and participation, total equality, acceptance of diversity, intolerance of harassment and abuse, and fairness with transgender athletes. She co-founded the evidence-based advocacy group on the international stage known as Women Sport International. As a physiologist, Barbara has had a major influence on attention to the health of the female athlete, and she produced the original pioneering work in the field. Her impactful study, “Bone mineral density after resumption of menses in amenorrheic athletes,” was published in the Journal of the American Medical Association in 1986. Since that time, the female athlete triad has set the stage for research and treatment to enhance women in physical activity at all levels.
International Olympic Committee (IOC) Consensus Statement on Relative Energy Deficiency in Sport (RED-S): 2018 Update
Margo Mountjoy, Jorunn Sundgot-Borgen, Louise Burke, Kathryn E. Ackerman, Cheri Blauwet, Naama Constantini, Constance Lebrun, Bronwen Lundy, Anna Melin, Nanna Meyer, Roberta Sherman, Adam S. Tenforde, Monica Klungland Torstveit, and Richard Budgett
Low Energy Availability Is Difficult to Assess but Outcomes Have Large Impact on Bone Injury Rates in Elite Distance Athletes
Ida A. Heikura, Arja L.T. Uusitalo, Trent Stellingwerff, Dan Bergland, Antti A. Mero, and Louise M. Burke
We aimed to (a) report energy availability (EA), metabolic/reproductive function, bone mineral density, and injury/illness rates in national/world-class female and male distance athletes and (b) investigate the robustness of various diagnostic criteria from the Female Athlete Triad (Triad), Low Energy Availability in Females Questionnaire, and relative energy deficiency in sport (RED-S) tools to identify risks associated with low EA. Athletes were distinguished according to benchmarks of reproductive function (amenorrheic [n = 13] vs. eumenorrheic [n = 22], low [lowest quartile of reference range; n = 10] versus normal testosterone [n = 14]), and EA calculated from 7-day food and training diaries (< or >30 kcal·kg−1 fat-free mass·day−1). Sex hormones (p < .001), triiodothyronine (p < .05), and bone mineral density (females, p < .05) were significantly lower in amenorrheic (37%) and low testosterone (40%; 15.1 ± 3.0 nmol/L) athletes, and bone injuries were ∼4.5-fold more prevalent in amenorrheic (effect size = 0.85, large) and low testosterone (effect size = 0.52, moderate) groups compared with others. Categorization of females and males using Triad or RED-S tools revealed that higher risk groups had significantly lower triiodothyronine (female and male Triad and RED-S: p < .05) and higher number of all-time fractures (male Triad: p < .001; male RED-S and female Triad: p < .01) as well as nonsignificant but markedly (up to 10-fold) higher number of training days lost to bone injuries during the preceding year. Based on the cross-sectional analysis, current reproductive function (questionnaires/blood hormone concentrations) appears to provide a more objective and accurate marker of optimal energy for health than the more error-prone and time-consuming dietary and training estimation of EA. This study also offers novel findings that athlete health is associated with EA indices.
Low RMRratio as a Surrogate Marker for Energy Deficiency, the Choice of Predictive Equation Vital for Correctly Identifying Male and Female Ballet Dancers at Risk
Sarah Staal, Anders Sjödin, Ida Fahrenholtz, Karen Bonnesen, and Anna Katarina Melin
Ballet dancers are reported to have an increased risk for energy deficiency with or without disordered eating behavior. A low ratio between measured ( m ) and predicted ( p ) resting metabolic rate (RMRratio < 0.90) is a recognized surrogate marker for energy deficiency. We aimed to evaluate the prevalence of suppressed RMR using different methods to calculate p RMR and to explore associations with additional markers of energy deficiency. Female (n = 20) and male (n = 20) professional ballet dancers, 19–35 years of age, were enrolled. m RMR was assessed by respiratory calorimetry (ventilated open hood). p RMR was determined using the Cunningham and Harris–Benedict equations, and different tissue compartments derived from whole-body dual-energy X-ray absorptiometry assessment. The protocol further included assessment of body composition and bone mineral density, blood pressure, disordered eating (Eating Disorder Inventory-3), and for females, the Low Energy Availability in Females Questionnaire. The prevalence of suppressed RMR was generally high but also clearly dependent on the method used to calculate p RMR, ranging from 25% to 80% in males and 35% to 100% in females. Five percent had low bone mineral density, whereas 10% had disordered eating and 25% had hypotension. Forty percent of females had elevated Low Energy Availability in Females Questionnaire score and 50% were underweight. Suppressed RMR was associated with elevated Low Energy Availability in Females Questionnaire score in females and with higher training volume in males. In conclusion, professional ballet dancers are at risk for energy deficiency. The number of identified dancers at risk varies greatly depending on the method used to predict RMR when using RMRratio as a marker for energy deficiency.
Male Flat Jockeys Do Not Display Deteriorations in Bone Density or Resting Metabolic Rate in Accordance With Race Riding Experience: Implications for RED-S
George Wilson, Dan Martin, James P. Morton, and Graeme L. Close
Despite consistent reports of poor bone health in male jockeys, it is not yet known if this is a consequence of low energy availability or lack of an osteogenic stimulus. Given the rationale that low energy availability is a contributing factor in low bone health, we tested the hypothesis that both hip and lumbar bone mineral density (BMD) should progressively worsen in accordance with the years of riding. In a cross-sectional design, male apprentice (n = 17) and senior (n = 14) jockeys (matched for body mass and fat-free mass) were assessed for hip and lumbar spine BMD, as well as both measured and predicted resting metabolic rate (RMR). Despite differences (p < .05) in years of race riding (3.4 ± 2 vs. 16.3 ± 6.8), no differences were apparent (p > .05) in hip (−0.9 ± 1.1 vs. −0.8 ± 0.7) and lumbar Z-scores (−1.3 ± 1.4 vs. −1.5 ± 1) or measured RMR (1,459 ± 160 vs. 1,500 ± 165 kcal/day) between apprentices and senior jockeys, respectively. Additionally, years of race riding did not demonstrate any significant correlations (p > .05) with either hip or lumbar spine BMD. Measured RMR was also not different (p > .05) from predicted RMR in either apprentice (1,520 ± 44 kcal/day) or senior jockeys (1,505 ± 70 kcal/day). When considered with previously published data examining underreporting of energy intake and direct assessments of energy expenditure, we suggest that low BMD in jockeys is not due to low energy availability per se but rather the lack of an osteogenic stimulus associated with riding.
Markers of Bone Health, Bone-Specific Physical Activities, Nutritional Intake, and Quality of Life of Professional Jockeys in Hong Kong
Eric Tsz-Chun Poon, John O’Reilly, Sinead Sheridan, Michelle Mingjing Cai, and Stephen Heung-Sang Wong
Weight-making practices, regularly engaged in by horse racing jockeys, have been suggested to impair both physiological and mental health. This study aimed to assess bone health markers, nutritional intake, bone-specific physical activity (PA) habits, and quality of life of professional jockeys in Hong Kong (n = 14), with gender-, age-, and body mass index-matched controls (n = 14). Anthropometric measurements, serum hormonal biomarkers, bone mineral density, bone-specific PA habits, nutritional intake, and quality of life were assessed in all participants. The jockey group displayed significantly lower bone mineral density at both calcanei than the control group (left: 0.50 ± 0.06 vs. 0.63 ± 0.07 g/cm2; right: 0.51 ± 0.07 vs. 0.64 ± 0.10 g/cm2, both ps < .01). Thirteen of the 14 jockeys (93%) showed either osteopenia or osteoporosis in at least one of their calcanei. No significant difference in bone mineral density was detected for either forearm between the groups. The current bone-specific PA questionnaire score was lower in the jockey group than the control group (5.61 ± 1.82 vs. 8.27 ± 2.91, p < .05). Daily energy intake was lower in the jockeys than the controls (1,360 ± 515 vs. 1,985 ± 1,046 kcal/day, p < .01). No significant group difference was found for micronutrient intake assessed by the bone-specific food frequency questionnaire, blood hormonal markers, and quality of life scores. Our results revealed suboptimal bone conditions at calcanei and insufficient energy intake and bone-loading PAs among professional jockeys in Hong Kong compared with healthy age-, gender-, and body mass index-matched controls. Further research is warranted to examine the effect of improved bone-loading PAs and nutritional habits on the musculoskeletal health of professional jockeys.
Negative Consequences of Low Energy Availability in Natural Male Bodybuilding: A Review
Energy availability (EA) is a scientific concept describing how much energy is available for basic metabolic functions such as reproduction, immunity, and skeletal homeostasis. Carefully controlled studies on women have shown pathological effects of EA < 30 kcal/kg fat-free mass (FFM), and this state has been labeled low EA (LEA). Bodybuilding is a sport in which athletes compete to show muscular definition, symmetry, and low body fat (BF). The process of contest preparation in bodybuilding includes months of underfeeding, thus increasing the risk of LEA and its negative health consequences. As no well-controlled studies have been conducted in natural male bodybuilders on effects of LEA, the aim of this review was to summarize what can be extrapolated from previous relevant research findings in which EA can be calculated. The reviewed literature indicates that a prolonged EA < 25 kcal/kg FFM results in muscle loss, hormonal imbalances, psychological problems, and negatively affects the cardiovascular system when approaching the lower limits of BF (∼4%–5%) among males. Case studies on natural male bodybuilders who prepare for contest show muscle loss (>40% of total weight loss) with EA < 20 kcal/kg FFM, and in the study with the lowest observed BF (∼4 kg), major mood disturbance and hormonal imbalances co-occurred. Studies also underline the problem of BF overshoot during refeeding after extremes of LEA among males. A more tempered approach (EA > 25 kcal/kg FFM) might result in less muscle loss among natural male bodybuilders who prepare for contest, but more research is needed.
Pitfalls of Conducting and Interpreting Estimates of Energy Availability in Free-Living Athletes
Louise M. Burke, Bronwen Lundy, Ida L. Fahrenholtz, and Anna K. Melin
The human body requires energy for numerous functions including, growth, thermogenesis, reproduction, cellular maintenance, and movement. In sports nutrition, energy availability (EA) is defined as the energy available to support these basic physiological functions and good health once the energy cost of exercise is deducted from energy intake (EI), relative to an athlete’s fat-free mass (FFM). Low EA provides a unifying theory to link numerous disorders seen in both female and male athletes, described by the syndrome Relative Energy Deficiency in Sport, and related to restricted energy intake, excessive exercise or a combination of both. These outcomes are incurred in different dose–response patterns relative to the reduction in EA below a “healthy” level of ∼45 kcal·kg FFM−1·day−1. Although EA estimates are being used to guide and monitor athletic practices, as well as support a diagnosis of Relative Energy Deficiency in Sport, problems associated with the measurement and interpretation of EA in the field should be explored. These include the lack of a universal protocol for the calculation of EA, the resources needed to achieve estimates of each of the components of the equation, and the residual errors in these estimates. The lack of a clear definition of the value for EA that is considered “low” reflects problems around its measurement, as well as differences between individuals and individual components of “normal”/“healthy” function. Finally, further investigation of nutrition and exercise behavior including within- and between-day energy spread and dietary characteristics is warranted since it may directly contribute to low EA or its secondary problems.
Relative Energy Deficiency in Sport in Male Athletes: A Commentary on Its Presentation Among Selected Groups of Male Athletes
Louise M. Burke, Graeme L. Close, Bronwen Lundy, Martin Mooses, James P. Morton, and Adam S. Tenforde
Low energy availability (LEA) is a key element of the Female Athlete Triad. Causes of LEA include failure to match high exercise energy expenditure (unintentional) or pathological behaviors of disordered eating (compulsive) and overzealous weight control programs (misguided but intentional). Recognition of such scenarios in male athletes contributed to the pronouncement of the more inclusive Relative Energy Deficiency in Sport (RED-S) syndrome. This commentary describes the insights and experience of the current group of authors around the apparently heightened risk of LEA in some populations of male athletes: road cyclists, rowers (lightweight and open weight), athletes in combat sports, distance runners, and jockeys. The frequency, duration, and magnitude of the LEA state appear to vary between populations. Common risk factors include cyclical management of challenging body mass and composition targets (including “making weight”) and the high energy cost of some training programs or events that is not easily matched by energy intake. However, additional factors such as food insecurity and lack of finances may also contribute to impaired nutrition in some populations. Collectively, these insights substantiate the concept of RED-S in male athletes and suggest that a specific understanding of a sport, subpopulation, or culture may identify a complex series of factors that can contribute to LEA and the type and severity of its outcomes. This commentary provides a perspective on the range of risk factors that should be addressed in future surveys of RED-S in athletic populations and targeted for specific investigation and modification.