REVIEW PAPER
Female athlete triad and relative energy deficiency in sport – endocrine changes and treatment in women
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1
Faculty of Medicine and Health Science, Andrzej Frycz Modrzewski Krakow University, Poland
2
Department of Basic Biomedical Science, Faculty of Pharmaceutical Sciences in Sosnowiec, Medical University of Silesia, Katowice, Poland
Submission date: 2021-10-14
Final revision date: 2022-03-29
Acceptance date: 2022-04-11
Online publication date: 2022-09-20
Corresponding author
Joanna Witkoś
Faculty of Medicine and Health Science, Andrzej Frycz Modrzewski Krakow University, G. Herlinga-Grudzińskiego 1, 30-705 Kraków, Poland.
Pol. Ann. Med. 2022;29(2):281-287
KEYWORDS
TOPICS
ABSTRACT
Introduction:
Female athlete triad (FAT) it is a syndrome of three tightly interrelated components: amenorrhea, eating disorder, and osteoporosis. FAT syndrome has been re-evaluated and re-defined and the International Olympic Committee introduced a new relative energy deficiency in sport (RED-S) syndrome.
Aim:
The aim of the study was to review the knowledge on the issues of endocrine changes occurring in FAT and RED-S, and treatment of those conditions on a basis of available literature.
Material and methods:
This article was based on a review of the literature search in the electronic databases Medline (PubMed), EBSCO, ClinicalKey, and Willey Online Library, using the terms: ‘female athlete triad,’ ‘relative energy deficiency in sport,’ ‘FAT and RED-S and endocrine changes,’ ‘low energy availability (LEA) and endocrine changes,’ ‘FAT and RED-S and treatment and women’.
Results and discussion:
LEA influences abnormal secretion of gonadotropin-releasing hormone (GnRH) and this leads to the disrupted follicle-stimulating hormone (FSH) and luteinising hormone (LH) secretion. Higher ghrelin levels inhibit secretion of GnRH and of adrenocorticotropic hormone (ACTH), growth hormone (GH), FSH and LH. A high peptide YY (PYY) results in a significant suppression of GnRH secretion. Hypercortisolemia occurring in athletes may directly affect reproductive functions. Lack of estrogen contributes both to disrupted mineralization of bones and to endothelial dysfunction.
Conclusions:
Low energy levels found in female athletes diagnosed with FAT or RED-S syndrome significantly influence hormonal pathways, disrupting the function of their reproductive system, and this noticeably affects the overall health of sportswomen, influencing endothelial dysfunctions and bone mineral density.
FUNDING
None declared.
CONFLICT OF INTEREST
None declared.
REFERENCES (44)
4.
Javed A, Kashyap R, Lteif AN. Hyperandrogenism in female athletes with functional hypothalamic amenorrhea: a distinct phenotype. Int J Women's Health. 2015;13(7):103–111.
https://doi.org/10.2147/ijwh.s....
5.
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.
https://doi.org/10.1210/jc.201....
7.
Horn E, Gergen N, McGarry KA. The female athlete triad. R I Med J. 2013;97(11):18–21.
8.
Williams NI, Statuta SM, Austion A. Female athlete triad future directions for energy availability and eating disorder research and practice. Clin Sports Med. 2017;36(4):671–686.
https://doi.org/10.1016/j.csm.....
9.
De Souza MJ, Koltun KJ, Etter CV, et al. Current status of the female athlete triad: Update and future directions. Curr Osteoporos Rep. 2017;15(6):577–587.
https://doi.org/10.1007/s11914....
13.
Hoch AZ, Lal S, Jurva JW, Gutterman DD. The female athlete triad and cardiovascular dysfunction. Phys Med Rehabil Clin N Am. 2007;18(3):385–400.
https://doi.org/10.1016/j.pmr.....
14.
Mountjoy M, Sundgot-Borgen J, Burke L, et al. IOC consensus statement on relative energy deficiency in sport (RED-S): 2018 update. Br J Sports Med. 2018;52(11):687–697.
https://doi.org/10.1136/bjspor....
15.
Sim A, Burns SF. Review: questionnaires as measures for low energy availability (LEA) and relative energy deficiency in sport (RED-S) in athletes. J Eat Disord. 2021;9(1):41.
https://doi.org/10.1186/s40337....
17.
Elliott-Sale KJ, Tenforde AS, Parziale AL, et al. Endocrine effects of relative energy deficiency in sport. Int J Nutr Exerc Metab. 2018;28(4):335–349.
https://doi.org/10.1123/ijsnem....
18.
Ackerman KE, Slusarz K, Guereca G, et al. Higher ghrelin and lower leptin secretion are associated with lower LH secretion in young amenorrheic athletes compared with eumenorrheic athletes and controls. Am J Physiol Endocrinol Metab. 2012;302(7):800–806.
https://doi.org/10.1152/ajpend....
19.
Corr M, De Souza MJ, Toombs RJ, Williams NI. Circulating leptin concentrations do not distinguish menstrual status in exercising women. Hum Reprod. 2011;26(3):685–694.
https://doi.org/10.1093/humrep....
20.
Donoso MA, Munoz-Calvo MT, Barrios V, Hawkins F, Argente J. Increased circulating adiponectin levels and decreased leptin/soluble leptin receptor ratio throughout puberty in female ballet dancers: Association with body composition and the delay in puberty. Eur J Endocrinol. 2010;162(5):905–911.
https://doi.org/10.1530/eje-09....
21.
Chou SH, Chamberland JP, Liu X, et al. Leptin is an effective treatment for hypothalamic amenorrhea. PNAS. 2011;108(16):6585–6590.
https://doi.org/10.1073/pnas.1....
22.
Scheid JL, Williams NI, West SL, VanHeest JL, De Souza MJ. Elevated PYY is associated with energy deficiency and indices of subclinical disordered eating in exercising women with hypothalamic amenorrhea. Appetite. 2010;52(1):184–192.
https://doi.org/10.1016/j.appe....
23.
Russell M, Stark J, Nayak S, et al. Peptide YY in adolescent athletes with amenorrhea, eumenorrheic athletes and non-athletic controls. Bone. 2009;45(1):104–109.
https://doi.org/10.1016/j.bone....
24.
Scheid JL, De Souza MJ. Menstrual irregularities and energy deficiency in physically active women: The role of ghrelin, PYY and adipocytokines. Med Sport Sci. 2010;55:82–102.
https://doi.org/10.1159/000321....
25.
De Souza, MJ, Van Heest J, Demers LM, Lasley BL. Luteal phase deficiency in recreational runners: Evidence for a hypometabolic state. J Clin Endocrinol Metab. 2003;88(1):337–346.
https://doi.org/10.1210/jc.200....
26.
Lawson EA, Donoho DA, Blum JI, et al. Decreased nocturnal oxytocin levels in anorexia nervosa are associated with low bone mineral density and fat mass. J Clin Psychiatry. 2011;72(11):1546–1551.
https://doi.org/10.4088/jcp.10....
27.
Lawson EA, Ackerman, KE, Estella NM, et al. Nocturnal oxytocin secretion is lower in amenorrheic athletes than nonathletes and associated with bone microarchitecture and finite element analysis parameters. Eur J Endocrinol. 2013;168(3):457–464.
https://doi.org/10.1530/eje-12....
28.
Lawson EA, Ackerman KE, Slattery M, Clarke H, Misra M. Oxytocin secretion is related to measures of energy homeostasis in young amenorrheic athletes. J Clin Endocrinol Metab. 2014;99(5):E881–E885.
https://doi.org/10.1210%2Fjc.2....
29.
Schaal K, Van Loan MD, Casazza GA. Reduced catecholamine response to exercise in amenorrheic athletes. Med Sci Sports Exerc. 2011;43(1):34–43.
https://doi.org/10.1249/mss.0b....
30.
Schorr M, Lawson EA, Dichtel LE, Klibanski A, Miller KK. Cortisol measures across the weight spectrum. J Clin Endocrinol Metab. 2015;100(9):3313–3321.
https://doi.org/10.1210/jc.201....
31.
Ackerman KE, Patel KT, Guereca G, Pierce L, Herzog DB, Misra M. Cortisol secretory parameters in young exercisers in relation to LH secretion and bone parameters. Clin Endocrinol. 2013;78(1):114–119.
https://doi.org/10.1111/j.1365....
32.
Misra M, Miller KK, Herzog DB, et al. Growth hormone and ghrelin responses to an oral glucose load in adolescent girls with anorexia nervosa and controls. J Clin Endocrinol Metab. 2004;89(4):1605–1612.
https://doi.org/10.1210/jc.200....
33.
Estour B, Germain N, Diconne E, et al. Hormonal profile heterogeneity and short-term physical risk in restrictive anorexia nervosa. J Clin Endocrinol Metab. 2010;95(5):2203–2210.
https://doi.org/10.1210/jc.200....
34.
Williams NI, Mallinson RJ, De Souza MJ. Rationale and study design of an intervention of increased energy intake in women with exercise-associated menstrual disturbances to improve menstrual function and bone health: The REFUEL study. Contemp Clin Trials Commun. 2019;14:100325.
https://doi.org/10.1016/j.conc....
35.
Richard N, Palmer C, Adams HP. Female athlete triad: Low energy availability, menstrual dysfunction, altered bone mineral density. Physician Assist Clin. 2018;3(3):313–324.
https://doi.org/10.1016/j.cpha....
36.
Misra M, Katzman D, Miller KK, et al. Physiologic estrogen replacement increases bone density in adolescent girls with anorexia nervosa. J Bone Miner Res. 2011;26(10):2430–2438.
https://doi.org/10.1002/jbmr.4....
37.
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.
https://doi.org/10.1210/jc.200....
38.
Papageorgiou M, Dolan E, Elliott-Sale KJ, Sale C. Reduced energy availability: Implications for bone health in physically active populations. Eur J Nutr. 2017;57(3):847–859.
https://doi.org/10.1007/s00394....
39.
Lanser EM, Zach KN, Hoch AZ. The female athlete triad and endothelial dysfunction. AAPM&R. 2011;3(5):458–465.
40.
Hoch AZ, Papanek P, Szabo A, Widlansky ME, Schimke JE, Gutterman DD. Association between the female athlete triad and endothelial dysfunction in dancers. Clin J Sport Med. 2011;21(2):119–125.
https://doi.org/10.1097/jsm.0b....
41.
Klein DA, Paradise SL, Reeder RM. Amenorrhea: A systematic approach to diagnosis and management. Am Fam Physician. 2019;100(1):39–48.
42.
Lebrun CM. The female athlete triad: What's a doctor to do? Curr Sports Med Rep. 2007;6(6):397–404.
44.
Thomas DT, Erdman KA, Burke LM. American College of Sports Medicine Joint Position Statement. Nutrition and Athletic Performance. Med Sci Sports Exerc. 2016;48(3):543–568.
https://doi.org/10.1249/mss.00....