Skip Navigation LinksHome » Articles » PRACTICAL APPROACHES TO IMPROVING NUTRITION AND ENERGY AVAILABILITY IN RED-S

PRACTICAL APPROACHES TO IMPROVING NUTRITION AND ENERGY AVAILABILITY IN RED-S

– Written by Nicole Farnsworth and Kathryn E. Ackerman, United States

 

 

INTRODUCTION

Participation in sport places significant demand on the body to sustain performance and support recovery. Nutrition provides the substrates needed for sport and to support normal physiological function. Inadequate nutrition creates a deficit in these substrates, which can negatively affect health and athletic performance. Correction of nutrient intake and balance can, in many cases, restore an athlete’s health status and support optimal athletic performance. 

 

ENERGY AVAILABILITY AND RELATIVE ENERGY DEFICIENCY IN SPORT (RED-S)

The human body requires nutrition in the form of calories and nutrients in order to perform the various processes needed to support survival and wellbeing. For the athlete, additional calories are needed to support the demands placed on the body during and following physical activity. The term energy availability (EA) refers to the calories ingested [energy intake (EI)] less the calories expended through exercise [exercise energy expenditure (EEE)], normalized for fat free mass (FFM) and expressed as kilocalories per kg of FFM per day (kcal/kg FFM/day). Adequate energy availability has been suggested in the literature to be 45 kcal/kg FFM/day1. Research has demonstrated that below 30 kcal/kg FFM/day, physiological changes alter the signaling of hormones, resulting in impaired function2. The Female Athlete Triad (Triad) describes the interplay among EA, bone mineral density (BMD) and menstrual function. While this model originally described the impact of LEA as disordered eating (DE), amenorrhea, and osteoporosis, it is now recognized as a spectrum disorder spanning from optimal EA to low EA (LEA) with or without an eating disorder (ED), optimal bone health to osteoporosis, and eumenorrhea to functional hypothalamic amenorrhea (FHA)3.

In 2014, the International Olympic Committee (IOC) published a consensus statement describing Relative Energy Deficiency in Sport (RED-S), a syndrome which details the effects of LEA on numerous body systems in both male and female athletes, including the endocrine system, metabolism, hematological system, growth and development, cardiovascular system, gastrointestinal system, immune system, and reproductive system. LEA additionally can affect and be affected by psychological conditions such as stress, anxiety, depression, or an EA4–6. The RED-S model also details the potential performance effects of LEA, including decreased endurance performance, increased injury risk, decreased training response, decreased glycogen stores, decreased muscle strength, impaired judgement, decreased coordination and concentration, irritability, and depression. (Figure 1)6. Surveying athletes has illustrated the high prevalence of LEA and the systemic health and performance effects that can occur8. The 2018 IOC RED-S update described the scientific progress that has been made in studying RED-S and the gaps in knowledge that remain, including assessment of EA and validated prevention measures9

 

PREVALENCE OF LEA AND RED-S IN SPORT

Prevalence of LEA varies across sports and between different athlete populations, with a higher prevalence found in those sports with a focus on weight and/or aesthetics. In athletics, prevalence of LEA and its subsequent complications varies across events, with higher prevalence seen in middle-to-long distance runners and jumping events10. In an examination of 40 elite female endurance athletes using food and exercise logs, Melin, et al found that 63% had low/reduced EA (<45 kcal/kg FFM/day)11. In female high school athletes participating in various sports, 36% had LEA as indicated by EA ≤ 45 kcal/kg FFM, with 6% < 30 kcal/kg FFM. EI was calculated using the results of 3-day food diaries and EEE was determined using the compendium of physical activities classification and included details regarding sport participation, exercise intensity, age, weight, and sex12,13. Elite sprinters assessed for EA were found to have a risk of LEA prevalence from pre-season (31%) to post-season (54%) by analysis of primary (amenorrhea, bone mineral density, follicle-stimulating hormone, luteinizing hormone, estradiol, resting metabolic rate, Low Energy Availability in Females Questionnaire (LEAF-Q) score) and secondary (fasting blood glucose, free triiodothyronine, ferritin, low-density lipoprotein cholesterol, fasting insulin, insulin-like growth factor-1, systolic blood pressure and diastolic blood pressure) LEA markers14. LEA has been examined in recreational athletes as well, with as many as 45% classified as “at risk” for LEA using the LEAF-Q15.

While female athletes have been the focus of many EA studies, research in male athletes has increased in an effort to further understand how LEA presents in each sex. LEA in male athletes has been examined in cycling, distance running, rowing, and combat sports such as judo16–18. Male jockeys have low BMD and increased bone resorption, suggestive of hormonal changes due to the common practice of weight cycling in the sport19. Assessment of 108 recreationally-trained male athletes using the EA cut-points categorized in females (LEA < 30 kg/kg FFM, adequate EA≥45 kg/kg FFM) found that 47.2% were categorized as LEA and nearly 80% of the study participants were below adequate EA20

Specialists have additionally described the prevalence of LEA in the para-athlete population. A survey of 260 male and female para-athletes found that signs associated with Triad/RED-S, such as bone stress injuries, oligomenorrhea/amenorrhea, and an elevated Eating Disorder Examination Questionnaire (EDE-Q) score, were present in this population21. These findings are not consistent across studies, however, and more research is needed to fully characterize LEA in athletes with disabilities22,23.

 

ADDRESSING RED-S WITH NUTRITION

Assessment

When treating RED-S, experts recommend the coordination of an interdisciplinary team, including at least a sports medicine physician and registered dietitian (RD/RDN), and often a psychologist6,9. Nutrition is a critical component of EA and as such, an important point of intervention when working with athletes with RED-S and LEA. An RD/RDN, and preferably one specialized in sports dietetics, is a valuable provider for this population given their knowledge and experience in guiding athletes and understanding sport culture. Furthermore, a sports RD/RDN experienced in treating DE and EDs is ideal given the prevalence of eating pathology in athletes with RED-S. 

Nutrition management of RED-S begins with assessment of EA by gathering data on EI and EEE. There are numerous strategies for assessing EI and EEE, each with its own limitations with regards to accuracy24. Predictive equations can be utilized to calculate resting metabolic rate (RMR), and with the addition of physical activity expenditure can be used to estimate energy needs. If FFM data are available, the Cunningham-Sabo equation can be utilized25. Other popular predictive equations include Harris-Benedict and Mifflin St. Jeor26,27. These predictive equations were developed using the general population and therefore may underestimate an athlete’s RMR. Furthermore, these predictive equations may result in inaccuracies when calculating energy needs for those in an energy deficit28. The Cunningham and Harris-Benedict equations are considered the most accurate predictive equations available for assessment in athletes29

Assessment of EA necessitates a comparison between EI and energy expenditure. Collecting accurate energy and nutrient intake information poses challenges. Common strategies include 24-hour recalls, dietary records, food frequency questionnaires (FFQs), and food logs. Researchers commonly cite underreporting as a challenge when using 24-hour recalls and dietary records. FFQs may provide more accuracy when analyzing specific nutrients, but may not be able to capture the variability in intake that athletes often have30,31. Furthermore, the act of logging nutritional intake could influence food choices and behaviors, therefore making it difficult to analyze ad libitum intake32. Weight is not a dependable indicator of EA, as those with LEA can be weight stable due to the suppression in RMR33

Assessment of overall energy needs includes factoring in the expenditure of physical activity. This can be measured using pedometers, accelerometers, or GPS trackers, or estimated using metabolic equivalent of task (MET) or physical activity coefficients34,35. There is no standard method for assessing expenditure and there is no consensus in the literature regarding what constitutes EEE34. Additionally, many methods for assessing expenditure outside of a controlled research setting have the potential to inaccurately capture EEE. A study comparing various wearable devices to doubly-labelled water (DLW) found that these devices underestimated expenditure in free-living individuals by 69-590 calories36. Comparison of accelerometers and the energy-cost estimates via questionnaire in elite athletes found that EEE was 20-30% lower on accelerometer results37.

Given the challenges associated with calculating EA, a fully comprehensive assessment conducted by an inter-disciplinary team increases the likelihood that LEA will be detected. Analysis of reproductive function using labs and questionnaires has been found to be more accurate and objective than self-reported intake and estimations of EA24. Indirect or direct calorimetry can be used to assess RMR and determine if metabolic suppression has occurred38. Dual-energy X-ray absorptiometry (DXA), the modern gold standard for anthropometric assessment, provides information on BMD and FFM, which can be critical for assessing bone health and body composition in those suspected to have RED-S39,40.

 

Treatment

Once RED-S has been diagnosed, an important step in treatment is to determine the cause of LEA. An athlete can develop RED-S due to a lack of knowledge about energy needs, limited dietary intake due to food allergies or gastrointestinal concerns, food insecurity, or DE or an ED6,9. The body undergoes acute hormonal changes following exercise – the suppression of leptin and suppression or maintenance of ghrelin – that can impair appetite and could lead to LEA if an athlete is not fueling properly following training41. This differs from the hormonal changes present in chronic LEA which included decrease leptin and increased ghrelin42. While those athletes exhibiting unawareness of nutritional needs may be able to amend their EA status through nutrition education, those with DE/ED will require nutrition counseling to address disordered thoughts and behaviors43. Therefore, understanding the contributors to LEA can help the provider determine the most appropriate, personalized approach.

Male and female athletes cite a lack of nutrition knowledge and contradictory sports nutrition information in scientific literature, anecdotal data, and articles written for the lay public make it difficult for athletes to determine how to best fuel for their sport44,45. Sports nutrition education provided in a group or individualized setting, has been shown to significantly improve nutrition behaviors and knowledge and self-efficacy46–48. Nutrition education should focus on the unique nutritional needs of the athlete and should connect to an individual athlete’s sport, when possible. 

For those athletes with DE/ED, nutri-tion counseling is warranted in order to support behavioral change and move the athlete towards adequate EA. Commonly used counseling modalities employed by dietitians working with DE/ED include cognitive-behavioral therapy (CBT), dialectical behavioral therapy (DBT), motivational interviewing (MI), family-based therapy (FBT), and acceptance and commitment therapy (ACT). The use of these differing techniques may depend on the eating behaviors that are present and the athlete’s stage of change43. Nutrition counseling and guidance is provided in conjunction with psychotherapy and possibly pharmacotherapy, and therefore consistent communication among mem-bers of the interdisciplinary team is recommended to ensure the athlete with DE/ED is supported while working towards normative eating behaviors and attitudes that will support adequate EA49

Therapeutic nutrition interventions for RED-S require an individualized approach and an assessment that indicates the contributors to LEA for an athlete. Nutritional interventions may require an increase in dietary intake, a decrease in exercise expenditure, or both to support adequate EA3,6,9. Athletes may need to adjust their dietary patterns by shifting their macronutrient intake or changing their nutrition timing. The provider should inform the athlete that improvement in RED-S signs and symptoms, including FHA and low BMD, can take months to years to improve, even once adequate EA is achieved3. For female athletes presenting with FHA, weight gain and fat mass gain may be warranted in order to support hormonal function, and improvement in EA does not ensure immediate resumption of menses50. In those who have achieved weight stabilization, it can take 6 to 12 months to resume menses51.

In many cases, weight gain is necessary in order to address LEA and promote optimal physiological function. Weight gain at a rate of 0.23 kg per week is manageable for most individuals and may require an increase in EI, and decrease in EEE, or both52,53. The amount of weight gain needed varies and research suggests that females may need to gain 2 kg more than the weight at which menses was lost in order to support menstrual restoration51,54. When low body fat is present as a result of LEA, increasing fat mass to essential levels is required to support the role of fat in metabolism, including bone health55,56. Weight gain in the form of fat mass gain is associated with proper hormonal functioning in those with FHA57. Observation of body fat distribution in females with anorexia nervosa has described the initial increase in fat mass distribution in the central region of the body and a subsequent redistribution of body fat once weight restoration has been maintained58,59. It is important to explain this phenomenon to those restoring body weight, as this initial increase in central mass can be psychologically distressing. 

Due to the systemic effects of LEA, certain nutrients – namely calcium and vitamin D – become particularly critical when addressing RED-S. Calcium and vitamin D are both important for bone health, therefore nutrition treatment should ensure that intake is adequate60. Adults and children need 1,000mg/day of calcium, while pre-adolescents and adolescents require 1,300mg/day. While dietary intake of calcium is preferred, due to its increased bioavailability, supplementation with calcium citrate or calcium carbonate is also appropriate. Because calcium is most bioavailable at or below 500 mg, calcium should be ingested multiple times per day to achieve daily requirements40. The United States Department of Agriculture (USDA) recommends 600-800 international units (IUs) of vitamin D daily to support bone health, but research suggests that higher doses are needed to support vitamin D levels >30 ng/mL, which is what is recommended for adequate vitamin D in athletes61,62. Vitamin D needs can be met through 15-30 minutes of sun exposure/day, fortified foods, and supplementation40. Vitamin D3 supplements are more bioavailable than vitamin D263.

Athletes with RED-S may present with suboptimal iron stores as well, which can become inadequate due to restricted intake of iron-containing foods64. A high amount of repetitive weight-bearing contact – like that seen with running – can also compromise iron levels through foot-strike hemolysis65. Exercise can also impair iron absorption through the upregulation of hepcidin66,67 Dietary interventions for iron include consuming sources of heme iron and pairing sources of non-heme iron with vitamin C-rich foods for optimal absorption68. Supplementation is recommended for athletes with iron depletion in order to prevent anemia40

 

CONCLUSION

RED-S has varying impacts on individual athletes but can have a profound effect on health and performance. Nutrition plays a key role in correcting LEA and treating RED-S. Further research is needed to determine the best strategies for assessing EA in the clinical setting. Understanding the nutritional, psychological, and physiological contributors of RED-S can determine the most appropriate treatment approach. 

 

 

Nicole Farnsworth M.S., R.D., C.S.S.D., L.D.N., C.P.T. 

Sports Dietitian

Female Athlete Program

Boston Children's Hospital

Harvard Medical School

 

Kathryn E. Ackerman M.D., M.P.H.

Medical Director

Female Athlete Program

Boston Children's Hospital

Associate Professor of Medicine, Harvard Medical School

 

Boston, USA

 

Contact: 

kathryn.ackerman@childrens.harvard.edu

 

 

 

References

1.              Ihle R, Loucks AB. Dose-response relationships between energy availability and bone turnover in young exercising women. J Bone Miner Res Off J Am Soc Bone Miner Res. 2004;19(8):1231-1240. doi:10.1359/JBMR.040410

2.              Loucks AB, Thuma JR. Luteinizing Hormone Pulsatility Is Disrupted at a Threshold of Energy Availability in Regularly Menstruating Women. J Clin Endocrinol Metab. 2003;88(1):297-311. doi:10.1210/jc.2002-020369

3.              Souza MJD, Nattiv A, Joy E, et al. 2014 Female Athlete Triad Coalition Consensus Statement on Treatment and Return to Play of the Female Athlete Triad: 1st International Conference held in San Francisco, California, May 2012 and 2nd International Conference held in Indianapolis, Indiana, May 2013. Br J Sports Med. 2014;48(4):289-289. doi:10.1136/bjsports-2013-093218

4.              Thein-Nissenbaum JM, Rauh MJ, Carr KE, Loud KJ, McGuine TA. Associations Between Disordered Eating, Menstrual Dysfunction, and Musculoskeletal Injury Among High School Athletes. J Orthop Sports Phys Ther. 2011;41(2):60-69. doi:10.2519/jospt.2011.3312

5.              Torstveit MK, Fahrenholtz IL, Lichtenstein MB, Stenqvist TB, Melin AK. Exercise dependence, eating disorder symptoms and biomarkers of Relative Energy Deficiency in Sports (RED-S) among male endurance athletes. BMJ Open Sport Exerc Med. 2019;5(1):e000439. doi:10.1136/bmjsem-2018-000439

6.              Mountjoy M, Sundgot-Borgen J, Burke L, et al. The IOC consensus statement: beyond the Female Athlete Triad—Relative Energy Deficiency in Sport (RED-S). Br J Sports Med. 2014;48(7):491-497. doi:10.1136/bjsports-2014-093502

7.              Constantini N. Medical Concerns of the Dancer. Book of Abstracts, XXVII FIMS World Congress of Sports Medicine. Budapest, Hungary; 2002:151.

8.              Ackerman KE, Holtzman B, Cooper KM, et al. Low energy availability surrogates correlate with health and performance consequences of Relative Energy Deficiency in Sport. Br J Sports Med. 2019;53(10):628-633. doi:10.1136/bjsports-2017-098958

9.              Mountjoy M, Sundgot-Borgen JK, Burke LM, et al. IOC consensus statement on relative energy deficiency in sport (RED-S): 2018 update. Br J Sports Med. 2018;52(11):687-697. doi:10.1136/bjsports-2018-099193

10.           Melin AK, Heikura IA, Tenforde A, Mountjoy M. Energy Availability in Athletics: Health, Performance, and Physique. Int J Sport Nutr Exerc Metab. 2019;29(2):152-164. doi:10.1123/ijsnem.2018-0201

11.           Melin A, Tornberg ÅB, Skouby S, et al. Energy availability and the female athlete triad in elite endurance athletes. Scand J Med Sci Sports. 2015;25(5):610-622. doi:10.1111/sms.12261

12.           Hoch AZ, Pajewski NM, Moraski L, et al. PREVALENCE OF THE FEMALE ATHLETE TRIAD IN HIGH SCHOOL ATHLETES AND SEDENTARY STUDENTS. Clin J Sport Med Off J Can Acad Sport Med. 2009;19(5):421-428. doi:10.1097/JSM.0b013e3181b8c136

13.           Ainsworth BE, Haskell WL, Leon AS, et al. Compendium of physical activities: classification of energy costs of human physical activities. Med Sci Sports Exerc. 1993;25(1):71-80. doi:10.1249/00005768-199301000-00011

14.           Sygo J, Coates AM, Sesbreno E, Mountjoy ML, Burr JF. Prevalence of Indicators of Low Energy Availability in Elite Female Sprinters. Int J Sport Nutr Exerc Metab. 2018;28(5):490-496. doi:10.1123/ijsnem.2017-0397

15.           Slater J, McLay-Cooke R, Brown R, Black K. Female Recreational Exercisers at Risk for Low Energy Availability. Int J Sport Nutr Exerc Metab. 2016;26(5):421-427. doi:10.1123/ijsnem.2015-0245

16.           Burke LM, Close GL, Lundy B, Mooses M, Morton JP, Tenforde AS. Relative Energy Deficiency in Sport in Male Athletes: A Commentary on Its Presentation Among Selected Groups of Male Athletes. Int J Sport Nutr Exerc Metab. 2018;28(4):364-374. doi:10.1123/ijsnem.2018-0182

17.           Wheeler GD, Singh M, Pierce WD, Epling WF, Cumming DC. Endurance Training Decreases Serum Testosterone Levels in Men without Change in Luteinizing Hormone Pulsatile Release. J Clin Endocrinol Metab. 1991;72(2):422-425. doi:10.1210/jcem-72-2-422

18.           Kyröläinen H, Karinkanta J, Santtila M, Koski H, Mäntysaari M, Pullinen T. Hormonal responses during a prolonged military field exercise with variable exercise intensity. Eur J Appl Physiol. 2008;102(5):539-546. doi:10.1007/s00421-007-0619-0

19.           Dolan E, McGoldrick A, Davenport C, et al. An altered hormonal profile and elevated rate of bone loss are associated with low bone mass in professional horse-racing jockeys. J Bone Miner Metab. 2012;30(5):534-542. doi:10.1007/s00774-012-0354-4

20.           Lane AR, Hackney AC, Smith-Ryan A, Kucera K, Registar-Mihalik J, Ondrak K. Prevalence of Low Energy Availability in Competitively Trained Male Endurance Athletes. Medicina (Mex). 2019;55(10). doi:10.3390/medicina55100665

21.           Brook EM, Tenforde AS, Broad EM, et al. Low energy availability, menstrual dysfunction, and impaired bone health: A survey of elite para athletes. Scand J Med Sci Sports. 2019;29(5):678-685. doi:10.1111/sms.13385

22.           Shimizu Y, Mutsuzaki H, Tachibana K, Hotta K, Wadano Y. Investigation of the Female Athlete Triad in Japanese Elite Wheelchair Basketball Players. Med Kaunas Lith. 2019;56(1). doi:10.3390/medicina56010010

23.           Blauwet CA, Brook EM, Tenforde AS, et al. Low Energy Availability, Menstrual Dysfunction, and Low Bone Mineral Density in Individuals with a Disability: Implications for the Para Athlete Population. Sports Med Auckl NZ. 2017;47(9):1697-1708. doi:10.1007/s40279-017-0696-0

24.           Heikura IA, Uusitalo ALT, Stellingwerff T, Bergland D, Mero AA, Burke LM. Low Energy Availability Is Difficult to Assess but Outcomes Have Large Impact on Bone Injury Rates in Elite Distance Athletes. Int J Sport Nutr Exerc Metab. 2018;28(4):403-411. doi:10.1123/ijsnem.2017-0313

25.           Cunningham JJ. A reanalysis of the factors influencing basal metabolic rate in normal adults. Am J Clin Nutr. 1980;33(11):2372-2374. doi:10.1093/ajcn/33.11.2372

26.           Harris JA, Benedict FG. A Biometric Study of Human Basal Metabolism. Proc Natl Acad Sci U S A. 1918;4(12):370-373.

27.           Mifflin MD, St Jeor ST, Hill LA, Scott BJ, Daugherty SA, Koh YO. A new predictive equation for resting energy expenditure in healthy individuals. Am J Clin Nutr. 1990;51(2):241-247. doi:10.1093/ajcn/51.2.241

28.           Leibel RL, Rosenbaum M, Hirsch J. Changes in Energy Expenditure Resulting from Altered Body Weight. N Engl J Med. 1995;332(10):621-628. doi:10.1056/NEJM199503093321001

29.           Thompson J, Manore MM. Predicted and Measured Resting Metabolic Rate of Male and Female Endurance Athletes. J Am Diet Assoc. 1996;96(1):30-34. doi:10.1016/S0002-8223(96)00010-7

30.           Thompson FE, Subar AF, Loria CM, Reedy JL, Baranowski T. Need for Technological Innovation in Dietary Assessment. J Am Diet Assoc. 2010;110(1):48-51. doi:10.1016/j.jada.2009.10.008

31.           Rebro SM, Patterson RE, Kristal AR, Cheney CL. The effect of keeping food records on eating patterns. J Am Diet Assoc. 1998;98(10):1163-1165. doi:10.1016/S0002-8223(98)00269-7

32.           Bingham SA, Gill C, Welch A, et al. Comparison of dietary assessment methods in nutritional epidemiology: weighed records v. 24 h recalls, food-frequency questionnaires and estimated-diet records. Br J Nutr. 1994;72(4):619-643. doi:10.1079/bjn19940064

33.           Loucks AB, Kiens B, Wright HH. Energy availability in athletes. J Sports Sci. 2011;29 Suppl 1:S7-15. doi:10.1080/02640414.2011.588958

34.           Burke LM, Lundy B, Fahrenholtz IL, Melin AK. Pitfalls of Conducting and Interpreting Estimates of Energy Availability in Free-Living Athletes. Int J Sport Nutr Exerc Metab. 2018;28(4):350-363. doi:10.1123/ijsnem.2018-0142

35.           Ferguson T, Rowlands AV, Olds T, Maher C. The validity of consumer-level, activity monitors in healthy adults worn in free-living conditions: a cross-sectional study. Int J Behav Nutr Phys Act. 2015;12(1):42. doi:10.1186/s12966-015-0201-9

36.           Murakami H, Kawakami R, Nakae S, et al. Accuracy of Wearable Devices for Estimating Total Energy Expenditure: Comparison With Metabolic Chamber and Doubly Labeled Water Method. JAMA Intern Med. 2016;176(5):702-703. doi:10.1001/jamainternmed.2016.0152

 

37.           Frączek B, Grzelak A, Klimek AT. Analysis of Daily Energy Expenditure of Elite Athletes in Relation to Their Sport, the Measurement Method and Energy Requirement Norms. J Hum Kinet. 2019;70(1):81-92. doi:10.2478/hukin-2019-0049

38.           Koehler K, Williams NI, Mallinson RJ, Southmayd EA, Allaway HCM, De Souza MJ. Low resting metabolic rate in exercise-associated amenorrhea is not due to a reduced proportion of highly active metabolic tissue compartments. Am J Physiol-Endocrinol Metab. 2016;311(2):E480-E487. doi:10.1152/ajpendo.00110.2016

39.           Zabriskie HA, Currier BS, Harty PS, Stecker RA, Jagim AR, Kerksick CM. Energy Status and Body Composition Across a Collegiate Women’s Lacrosse Season. Nutrients. 2019;11(2). doi:10.3390/nu11020470

40.           Karpinksi C, Rosenbloom CA. Sports Nutrition: A Handbook for Professionals. 6th Edition. Academy of Nutrition and Dietetics; 2017.

41.           Holtzman B, Ackerman KE. Measurement, Determinants, and Implications of Energy Intake in Athletes. Nutrients. 2019;11(3). doi:10.3390/nu11030665

42.           Elliott-Sale KJ, Tenforde AS, Parziale AL, Holtzman B, Ackerman KE. Endocrine Effects of Relative Energy Deficiency in Sport. Int J Sport Nutr Exerc Metab. 2018;28(4):335-349. doi:10.1123/ijsnem.2018-0127

43.           Herrin M, Larkin M. Nutrition Counseling in the Treatment of Eating Disorders. 2nd ed. Routledge; 2013.

44.           Burke LM, Hawley JA, Jeukendrup A, Morton JP, Stellingwerff T, Maughan RJ. Toward a Common Understanding of Diet-Exercise Strategies to Manipulate Fuel Availability for Training and Competition Preparation in Endurance Sport. Int J Sport Nutr Exerc Metab. 2018;28(5):451-463. doi:10.1123/ijsnem.2018-0289

45.           Torres-McGehee TM, Pritchett KL, Zippel D, Minton DM, Cellamare A, Sibilia M. Sports Nutrition Knowledge Among Collegiate Athletes, Coaches, Athletic Trainers, and Strength and Conditioning Specialists. J Athl Train. 2012;47(2):205-211. doi:10.4085/1062-6050-47.2.205

46.           Abood DA, Black DR, Birnbaum RD. Nutrition Education Intervention for College Female Athletes. J Nutr Educ Behav. 2004;36(3):135-139. doi:10.1016/S1499-4046(06)60150-4

47.           Valliant MW, Pittman Emplaincourt H, Wenzel RK, Garner BH. Nutrition Education by a Registered Dietitian Improves Dietary Intake and Nutrition Knowledge of a NCAA Female Volleyball Team. Nutrients. 2012;4(6):506-516. doi:10.3390/nu4060506

48.           Rossi FE, Landreth A, Beam S, Jones T, Norton L, Cholewa JM. The Effects of a Sports Nutrition Education Intervention on Nutritional Status, Sport Nutrition Knowledge, Body Composition, and Performance during Off Season Training in NCAA Division I Baseball Players. J Sports Sci Med. 2017;16(1):60-68.

49.           Yager J, Devlin MJ, Halmi KA, et al. Guideline Watch (August 2012): Practice Guideline for the Treatment of Patients With Eating Disorders, 3rd Edition. FOCUS. 2014;12(4):416-431. doi:10.1176/appi.focus.120404

50.           Łagowska K, Kapczuk K, Friebe Z, Bajerska J. Effects of dietary intervention in young female athletes with menstrual disorders. J Int Soc Sports Nutr. 2014;11(1):21. doi:10.1186/1550-2783-11-21

51.           Gordon CM, Ackerman KE, Berga SL, et al. Functional Hypothalamic Amenorrhea: An Endocrine Society Clinical Practice Guideline. J Clin Endocrinol Metab. 2017;102(5):1413-1439. doi:10.1210/jc.2017-00131

52.           Dueck CA, Matt KS, Manore MM, Skinner JS. Treatment of athletic amenorrhea with a diet and training intervention program. Int J Sport Nutr. 1996;6(1):24-40. doi:10.1123/ijsn.6.1.24

53.           Kopp-Woodroffe SA, Manore MM, Dueck CA, Skinner JS, Matt KS. Energy and nutrient status of amenorrheic athletes participating in a diet and exercise training intervention program. Int J Sport Nutr. 1999;9(1):70-88. doi:10.1123/ijsn.9.1.70

54.           Golden NH, Jacobson MS, Schebendach J, Solanto MV, Hertz SM, Shenker IR. Resumption of menses in anorexia nervosa. Arch Pediatr Adolesc Med. 1997;151(1):16-21. doi:10.1001/archpedi.1997.02170380020003

55.           Gilsanz V, Chalfant J, Mo AO, Lee DC, Dorey FJ, Mittelman SD. Reciprocal Relations of Subcutaneous and Visceral Fat to Bone Structure and Strength. J Clin Endocrinol Metab. 2009;94(9):3387-3393. doi:10.1210/jc.2008-2422

56.           Ayton A. The Importance of Restoring Body Fat Mass in the Treatment of Anorexia Nervosa: An Expert Commentary. J Popul Ther Clin Pharmacol J Ther Popul Pharmacol Clin. 2019;26(3):e9-e13. doi:10.15586/jptcp.v26i3.629

57.           Mallinson RJ, Williams NI, Olmsted MP, Scheid JL, Riddle ES, De Souza MJ. A case report of recovery of menstrual function following a nutritional intervention in two exercising women with amenorrhea of varying duration. J Int Soc Sports Nutr. 2013;10:34. doi:10.1186/1550-2783-10-34

58.           El Ghoch M, Calugi S, Lamburghini S, Dalle Grave R. Anorexia Nervosa and Body Fat Distribution: A Systematic Review. Nutrients. 2014;6(9):3895-3912. doi:10.3390/nu6093895

59.           Mayer L, Walsh BT, Pierson RN, et al. Body fat redistribution after weight gain in women with anorexia nervosa. Am J Clin Nutr. 2005;81(6):1286-1291. doi:10.1093/ajcn/81.6.1286

60.           Papageorgiou M, Dolan E, Elliott-Sale KJ, Sale C. Reduced energy availability: implications for bone health in physically active populations. Eur J Nutr. 2018;57(3):847-859. doi:10.1007/s00394-017-1498-8

61.           2015-2020 Dietary Guidelines | health.gov. Accessed June 22, 2020. https://health.gov/our-work/food-nutrition/2015-2020-dietary-guidelines/guidelines/

62.           Institute of Medicine (US) Committee to Review Dietary Reference Intakes for Vitamin D and Calcium. Dietary Reference Intakes for Calcium and Vitamin D. (Ross AC, Taylor CL, Yaktine AL, Del Valle HB, eds.). National Academies Press (US); 2011. Accessed June 24, 2020. http://www.ncbi.nlm.nih.gov/books/NBK56070/

63.           Lehmann U, Hirche F, Stangl GI, Hinz K, Westphal S, Dierkes J. Bioavailability of Vitamin D2 and D3 in Healthy Volunteers, a Randomized Placebo-Controlled Trial. J Clin Endocrinol Metab. 2013;98(11):4339-4345. doi:10.1210/jc.2012-4287

64.           Goldstein E, Fukuda DH. Connecting Energy Availability and Iron Deficiency with Bone Health: Implications for the Female Athlete. Strength Cond J. 2020;Publish Ahead of Print. doi:10.1519/SSC.0000000000000474

65.           Telford RD, Sly GJ, Hahn AG, Cunningham RB, Bryant C, Smith JA. Footstrike is the major cause of hemolysis during running. J Appl Physiol. 2003;94(1):38-42. doi:10.1152/japplphysiol.00631.2001

66.           Peeling P, Dawson B, Goodman C, et al. Effects of exercise on hepcidin response and iron metabolism during recovery. Int J Sport Nutr Exerc Metab. 2009;19(6):583-597. doi:10.1123/ijsnem.19.6.583

67.           Peeling P, Sim M, Badenhorst CE, et al. Iron Status and the Acute Post-Exercise Hepcidin Response in Athletes. PLOS ONE. 2014;9(3):e93002. doi:10.1371/journal.pone.0093002

68.           Hallberg L, Brune M, Rossander-Hulthén L. Is there a physiological role of vitamin C in iron absorption? Ann N Y Acad Sci. 1987;498:324-332. doi:10.1111/j.1749-6632.1987.tb23771.x

 

 

 

Header image by Confederated Tribes of Warm Springs, Oregon (Cropped)

Switch Language: list thumbnails
Bookmark and Share

Category

Sports Science

Volume 10
Targeted Topic - Sports Nutrition
view all articles in this issue

Article Images

Copyright © Aspetar Sports Medicine Journal 2021