Female Athlete Triad: Difference between revisions

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'''Original Editors '''- [[Pathophysiology of Complex Patient Problems|Students from Bellarmine University's&nbsp;Pathophysiology of Complex Patient Problems project.]]  
'''Original Editor '''[[User:Aarti Sareen|Aarti Sareen]]  
 
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= Introduction =
== Introduction ==
 
[[File:At risk Female athletic triad.jpeg|thumb|Ballet dancers at risk |alt=|300x300px]]
One of the major medical concerns for women in sports is that of the female athlete triad which was initially defined at the Traid Consensus Conference in 1992<ref>Yeager KK,Agostini R, Nattiv A, Drinkwater BL.The female athlete traid: disordered eating,amenorrhea,osteoporosis. [Commentary].Med. Sci Sports Exer 25:775-7,1993.</ref>.Also known simply as the Triad, this condition is seen in females participating in sports that emphasize leanness or low body weight<ref>Torstveit et al. 2005. ‘The Female Athlete Triad: Are Elite Athletes at Increased Risk?’ Medicine and Science in Sports and Exercise. vol. 37, no. 2. p. 184-93.</ref>.This behavious may lead to fatal consequences<ref>Hobart, Julie A. and Douglas R. Smucker. 2000. ‘The Female Athlete Triad.’ The American Academy of Family Physicians. &amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;lt; http://www.aafp.org/afp/20000601/3357.html&amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;gt; Retrieved on 2007-10-11</ref>. It is a syndrome which involve 3 distinct and interrelated conditions:<br>
The female athlete triad comprises three medical conditions, and is seen commonly in active teen girls:
 
#Disordered Eating (a range of poor nutritional behaviour)
#Amenorrhea (irregular or absent menstural periods)
#Osteoporosis (low bone mass and microarchitectural deterioration, which leads to weak bones and risk of fractures)
 
The problem of the&nbsp; of the female athlete traid collectively, as well as its indiviual components, have since been recognized as potentially serious problems for girls and women in sports worldwide.<ref>Nattive A,Agostini R,Drinkwater BL,Yeager KK; The female athlete traid: the inter-relatedness of disordered eating, amenorrhea and osteoporosis.Clin Sports Med 13:405-18,1994.</ref><ref>Otis CL,Drinkwater B, Johnson MD,et al:American College of Sports Medicine Position Stand on the Female Athlete Traid.Med Sci Sports Exer 29:i-ix,1997.</ref>A study by Burrows et al has suggested that the current triad components do not identify all at-risk women; rather, the authors suggest that criteria such as exercise-related menstrual alterations, disordered eating, and osteopenia may be more appropriate<ref>Burrows M, Shepherd H, Bird S, MacLeod K, Ward B. The components of the female athlete triad do not identify all physically active females at risk. J Sports Sci. Oct 2007;25(12):1289-97.</ref>.It is said to be interrelated as if an athlete is suffering from one element of the Triad, it is likely that they are suffering from the other two components of the triad as well<ref>"What is the Triad?". Female Athlete Triad Coalition. Retrieved 14 March 2012.</ref>. A Norwegian study of the prevalence of the triad found that fewer than 5% of elite female athletes met all the triad criteria and that this prevalence was comparable to that seen in normally active girls and young women<ref>Torstvcit MK, Sundgot-Borgen J. The female athlete traid exist in both elite athlets and controls;Med Sci Sports Exer.2005; 37(9) 1149 59.</ref>.When evaluating the presence of two of the components of the triad, prevalence ranged from 5.4% to 26.9% in the athletes. This implies that a Significant proportion of female athletes suffer from components of the triad rather than the triad itself and that this is not just confined to elite athletes, It has also been suggested that osteopenia is the likely effect of disordered eating on bone; osteoporosis is rare in this group of active women<ref>Khan KM,Liu-Ambrose T,Sran MM,Ashe MC,Donaldson MG,Wark JD.New criteria for 'female athlete traid'syndrome? Br J Sports Med 2002; 36; 10-13.</ref>.<br>
 
{{#ev:youtube|sASL7de5QWY|300}}<br>
 
= Etiology  =
 
There are basically 3 main reason purposed for female athlete triad:<br>
 
1. '''Low energy availability: T'''his syndrome is caused by an energy drain or caloric deficit (ie, the athlete’s energy expenditure exceeds her dietary energy intake).This low energy availability, whether subconscious or conscious, disrupts the hypothalamic-pituitary-ovarian axis, resulting in decreased gonadotropin-releasing hormone (GnRH) pulsatility and low luteinizing hormone (LH) and follicle-stimulating hormone (FSH) levels<ref>Loucks AB. Effects of exercise training on the menstrual cycle: existence and mechanisms. Med Sci Sports Exerc. Jun 1990;22(3):275-80.</ref>These changes eventually lead to decreased estrogen production, causing menstrual dysfunction. The decreased estrogen levels, in turn, affect calcium resorption and bone accretion, causing decreased bone health.<br>
 
2'''. Leptin Hormone:''' The hormone leptin, which is secreted by adipocytes, has also garnered increased interest. Leptin appears to influence the metabolic rate, and levels are proportional to body mass index (BMI). It may be a significant mediator of reproductive function, and many studies have demonstrated that low levels of leptin correlate positively with amenorrhea and infertility. Furthermore, leptin receptors have been found on hypothalamic neurons involved in the control of GnRH pulsatility and in bone, which may also affect osteoblastic function.<br>
 
3. '''Emotional stressors''' can also often be identified as inciting factors in athletes with the triad. The death of a coach or a family member, growth spurts, an illness that prevents training, and other events that an athlete cannot control often lead to disordered eating and excessive training—areas of life that the athlete can control.For many, moving to a university setting initiates the triad cascade. Some young women move far away from family and friends, and they may carry the added responsibilities of a sports scholarship and a demanding academic workload.<br>
 
= Epidemiology  =


The female athlete triad, though more common in the athletic population, can also occur in the nonathletic population.All female athletes are at risk for the female athlete triad or any of its components, sports that have an aesthetic component e.g.in ballet, figure skating, or gymnastics or are tied to a weight class (eg, tae kwon do, judo, or wrestling) have a higher prevalence of affected female athletes<ref>Nattiv A, Loucks AB, Manore MM, et al. American College of Sports Medicine position stand. The female athlete triad. Med Sci Sports Exerc. Oct 2007;39(10):1867-82.</ref><ref>Rosen LW, Hough DO. Pathogenic weight-control behavior of female college gymnasts. Phys Sportsmed. 1988;16(9):141-6.</ref><ref>Kiernan M, Rodin J, Brownell KD, Wilmore JH, Crandall C. Relation of level of exercise, age, and weight-cycling history to weight and eating concerns in male and female runners. Health Psychol. 1992;11(6):418-21.</ref>.Weight class sports associated with disordered eating, in athlets including males are,wresting,rowing.<br>
* Energy imbalance with or without an [[Eating Disorders|eating disorder]]
* [[Menstrual Cycle and Physical Activity|Menstrual disturbances]]
* Decreased [[Bone Density|bone mineral density]] with or without [[osteoporosis]]<ref name=":0">WebMD [https://teens.webmd.com/female-athlete-triad The Female Athlete Triad] Available:https://teens.webmd.com/female-athlete-triad (accessed 14.1.2023)</ref>
The components of the female athlete triad are interconnected:  


= Pathophysiology  =
* Disordered eating leads to inadequate nutrition.
* Inadequate nutrition affects the production of [[hormones]] such as [[estrogen]].
* Estrogen has an important role in [[bone]] development, low levels of estrogen leads to weakened bones and increasing the risk of injury.<ref name=":2">Womens sport foundation. [https://www.womenssportsfoundation.org/inspiration/the-female-athlete-triad/ The female athlete triad] Available:https://www.womenssportsfoundation.org/inspiration/the-female-athlete-triad/ (accessed 14.1.2023)</ref>
The below 2 minute video gives a good overview of the condition.{{#ev:youtube|v=zq6qhTP8i18|300}}<ref>Riverside. Female Athlete Triad Syndrome. Available from: https://www.youtube.com/watch?v=zq6qhTP8i18 [last accessed 14.1.2023]</ref>


The pathophysiology behind every triad is as follows:<br>  
== Epidemiology ==
Studies suggest that between 15-62% of the female athletic population exhibit disordered eating behaviours. Amenorrhea among female athletes range between 3-66%, depending on the definition that is used.<ref name=":2" />
[[File:Gymnasts at risk.jpeg|thumb|Gymnasts: risk group]]
'''Risk Factors'''


=== Disordered eating  ===
Those at greatest risk are girls involved in sports in which performance is scored subjectively, a low bodyweight is a focus, figure hugging clothing is required for competition, weight categories are used for participation and an immature body is seen as better for performance.<ref name=":2" />


Eating disorders are characterized by a serious disturbance in eating, such as restriction of intake or bingeing, as well as excessive concern about body shape or weight. The term disordered eating itself was coined to include pathologic eating behaviors that do not meet the strict ''Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition (DSM-IV)'' requirements for anorexia or bulimia; thus, it includes, but is not limited to, anorexia nervosa and bulimia nervosa.These eating behaviours lead to negative energy balance and reduce energy avalibility. For more information on Anorexia nervosa [http://www.physio-pedia.com/Anorexia_Nervosa click here] and for Bulimia Nervosa[http://www.physio-pedia.com/Bulimia_Nervosa click here]<br>  
* Categories of athletes at risk include: runner, dancers, gymnastics, figure skaters.<ref name=":0" />
* At greater risk are highly competitive athletes.<ref>De Souza MJ, Miller BE, Loucks AB, Luciano AA, Pescatello LS, Campbell CG, Lasley BL. High frequency of luteal phase deficiency and anovulation in recreational women runners: blunted elevation in follicle-stimulating hormone observed during luteal-follicular transition. The Journal of Clinical Endocrinology & Metabolism. 1998 Dec 1;83(12):4220-32.</ref>
* Younger individuals are greatly impacted by the non-reversible, long-term consequences of this syndrome. In fact, a study on animals found that low energy availability can decrease growth and hinder sexual development.<ref>Schneider JE, Wade GN. Inhibition of reproduction in service of energy balance. Reproduction in Context: Social and Environmental Influences on Reproductive Physiology and Behavior. 2000:35-82.</ref>


=== Menstrual Dysfunction<br>  ===
== Mechanisms ==
Becoming aware of how each component can develop and present itself will aid healthcare providers and other stakeholders in sport in the early recognition of the female athlete triad. The Three components comprise:


This includes includes luteal suppression, anovulation, oligomenorrhea, secondary amenorrhea and delayed menarche.<br>  
'''Low Energy Availability With or Without an Eating Disorder.''' A low energy availability (EA) can be due to decreased dietary energy intake and/or increased energy expended during exercise and, when EA is low, this leads to less energy available for body functions.
* Some athletes may participate in restrictive diets or use pills or laxatives.<ref name=":5">Beals KA, Hill AK. The prevalence of disordered eating, menstrual dysfunction, and low bone mineral density among US collegiate athletes. International journal of sport nutrition and exercise metabolism. 2006 Feb 1;16(1):1-23.</ref><ref name=":6">Beals KA, Manore MM. Disorders of the female athlete triad among collegiate athletes. International journal of sport nutrition and exercise metabolism. 2002 Sep 1;12(3):281-93.</ref><ref name=":7">Sundgot-Borgen J. Prevalence of eating disorders in elite female athletes. International Journal of Sport Nutrition and Exercise Metabolism. 1993 Mar 1;3(1):29-40.</ref><ref>Yager J, Devlin MJ, Halmi KA, Herzog DB, Mitchell JE, Powers PS, Zerbe KJ. Guideline watch: Practice guideline for the treatment of patients with eating disorders. Focus. 2005 Oct;3(4):546-51.</ref><ref>Johnson C, Powers PS, Dick R. Athletes and eating disorders: the National Collegiate Athletic Association study. International Journal of Eating Disorders. 1999 Sep;26(2):179-88.</ref><ref>Sundgot-Borgen J. Nutrient intake of female elite athletes suffering from eating disorders. International Journal of Sport Nutrition and Exercise Metabolism. 1993 Dec 1;3(4):431-42.</ref>
* Other athletes may have a diagnosis of an [[Eating Disorders|eating disorder]] (eg [[Anorexia Nervosa]], [[Bulimia Nervosa]], Binge Eating Disorder)<ref>American Psychiatric Association. Diagnostic and statistical manual of mental disorders (DSM-5®). American Psychiatric Pub; 2013 May 22.</ref> e Eating disorders can cause many problems, including dehydration, muscle fatigue and weakness, an erratic heartbeat, kidney damage, osteoporosis and hormone imbalances.<ref>Orthoinfo [https://orthoinfo.aaos.org/en/diseases--conditions/female-athlete-triad-problems-caused-by-extreme-exercise-and-dieting/ Female Athlete Triad: Problems Caused by Extreme Exercise and Dieting] Available:https://orthoinfo.aaos.org/en/diseases--conditions/female-athlete-triad-problems-caused-by-extreme-exercise-and-dieting/ (accessed 14.1.2023)</ref>
'''Menstrual Dysfunction: i'''nclude:
# Primary amenorrhea: pre-adolescent who hasn’t had a menstrual period by the age of 16 or has gone two years following the development of secondary sex characteristics without menarche. Eating disorders may be the cause.
# Secondary amenorrhea: menstruation ceases for three months or longer in a woman who has previously had normal menstruation. An integral part of anorexia nervosa.
# Oligomenorrhea: menstrual cycle occurs at irregular intervals.<ref name=":2" />
'''Low Bone Mineral Density:''' Bone is a dynamic structure, constantly being remodelled by osteoclasts and osteoblasts. Female athletes, functioning at a low estrogen state, have less  osteoblastic activity. Athletes require 5% to 15% higher bone mineral density than age-matched nonathlete, with reduced bone mineral density increases bone fragility and increase the risk of [[Stress Fractures|fractures]]. Stress fractures occurence is greater in amenorrheic athletes, and bone density has been shown to progressively decrease as the number of  menstrual cycles missed since menarche increases.<ref>Raj MA, Creech JA, Rogol AD. [https://www.ncbi.nlm.nih.gov/books/NBK430787/ Female Athlete Triad.] 2021 Aug 14. StatPearls. Treasure Island (FL): StatPearls Publishing. 2022.Available:https://www.ncbi.nlm.nih.gov/books/NBK430787/ (accessed 14.1.2023)</ref>


In '''luteal suppression''' have luteal phase and a prolonged follicular phase in which estradiol levels decrease. The cycle length usually does not change; the athlete will continue to ovulate—although it may be later in the cycle—and usually has regular menstruation.'''Anovulation''' is marked by low levels of estradiol and progesterone, which deter follicular development, as well as by an absence of ovulation.'''Amenorrhea '''usually refers to secondary amenorrhea, though delayed menarche/primary amenorrhea can occur in young athletes. By consensus, secondary amenorrhea is defined as the “absence of menstrual cycles lasting more than 3 months after menarche has occurred.”'''Oligomenorrhea''' is defined as “greater than 35 days between cycles.” <br>  
== Manifestations (including systemic involvement)  ==
*Weight loss 
*Absent or irregular menstrual cycles (includes primary and secondary amenorrhea, as well as oligomenorrhea)
*Chronic fatigue
*Fractures without significant trauma (low force cause); most common location is the [[tibia]]<ref>Barrow GW, Saha S. Menstrual irregularity and stress fractures in collegiate female distance runners. The American journal of sports medicine. 1988 May;16(3):209-16.</ref><ref>Bennell KL, Malcolm SA, Thomas SA, Wark JD, Brukner PD. The incidence and distribution of stress fractures in competitive track and field athletes: a twelve-month prospective study. The American journal of sports medicine. 1996 Mar;24(2):211-7.</ref><ref>Iwamoto J, Takeda T. Stress fractures in athletes: review of 196 cases. Journal of Orthopaedic Science. 2003 May 1;8(3):273-8.</ref><ref>Shaffer RA, Rauh MJ, Brodine SK, Trone DW, Macera CA. Predictors of stress fracture susceptibility in young female recruits. The American journal of sports medicine. 2006 Jan;34(1):108-15.</ref>
*Compulsive exercise
*Increased infections and illnesses<ref name=":1">Nattiv A, Loucks AB, Manore MM, Sanborn CF, Sundgot-Borgen J, Warren MP; American College of Sports Medicine. American College of Sports Medicine position stand: the female athlete triad. Med Sci Sports Exerc. 2007;39(10):1867–1882</ref>
*Decreased ability to recovery from injuries (slower tissue repair)<ref>Manore MM, Kam LC, Loucks AB. The female athlete triad: components, nutrition issues, and health consequences. Journal of sports sciences. 2007 Dec 1;25(S1):S61-71.</ref>
*Anxiety<ref name=":9">Berga SL, Loucks TL. Use of cognitive behavior therapy for functional hypothalamic amenorrhea. Annals of the New York Academy of Sciences. 2006 Dec;1092(1):114-29.</ref><ref name=":19">Nappi RE, Facchinetti F. Psychoneuroendocrine correlates of secondary amenorrhea. Archives of women's mental health. 2003 Apr 1;6(2):83-9.</ref> and [[depression]]<ref name=":9" /><ref name=":20">Stice E, South K, Shaw H. Future directions in etiologic, prevention, and treatment research for eating disorders. Journal of Clinical Child & Adolescent Psychology. 2012 Nov 1;41(6):845-55.</ref>
*[[Nutrition|Nutrient]] deficits
*Esophagitis and oesophageal perforation if self-induced vomiting<ref name=":12">Mountjoy M, Sundgot-Borgen J, Burke L, Carter S, Constantini N, Lebrun C, Meyer N, Sherman R, Steffen K, Budgett R, Ljungqvist A. The IOC consensus statement: beyond the female athlete triad—Relative Energy Deficiency in Sport (RED-S). Br J Sports Med. 2014 Apr 1;48(7):491-7.</ref>
*Constipation<ref>Norris ML, Harrison ME, Isserlin L, Robinson A, Feder S, Sampson M. Gastrointestinal complications associated with anorexia nervosa: A systematic review. International Journal of Eating Disorders. 2016 Mar;49(3):216-37.</ref>
*Changes in thyroid function, appetite, decrease in [[insulin]], increase in cortisol, and resistance to growth hormones<ref name=":21">Ihle R, Loucks AB. Dose‐response relationships between energy availability and bone turnover in young exercising women. Journal of bone and mineral research. 2004 Aug;19(8):1231-40.</ref><ref>Loucks AB, Thuma JR. Luteinizing hormone pulsatility is disrupted at a threshold of energy availability in regularly menstruating women. The Journal of Clinical Endocrinology & Metabolism. 2003 Jan 1;88(1):297-311.</ref><ref>Allaway HC, Southmayd EA, De Souza MJ. The physiology of functional hypothalamic amenorrhea associated with energy deficiency in exercising women and in women with anorexia nervosa. Hormone molecular biology and clinical investigation. 2016 Feb 1;25(2):91-119.</ref><ref>Logue D, Madigan SM, Delahunt E, Heinen M, Mc Donnell SJ, Corish CA. Low energy availability in athletes: a review of prevalence, dietary patterns, physiological health, and sports performance. Sports Medicine. 2018 Jan 1;48(1):73-96.</ref><ref>Misra M. Neuroendocrine mechanisms in athletes. InHandbook of clinical neurology 2014 Jan 1 (Vol. 124, pp. 373-386). Elsevier.</ref>
*Increased [[Cardiovascular Disease|cardiovascular]] risk (including [[atherosclerosis]])<ref>O'Donnell E, Goodman JM, Harvey PJ. Cardiovascular consequences of ovarian disruption: a focus on functional hypothalamic amenorrhea in physically active women. The Journal of Clinical Endocrinology & Metabolism. 2011 Dec 1;96(12):3638-48.</ref> due to increase in bad lipids and [[Reticuloendothelial System|endothelial]] dysfunction<ref name=":16">Rickenlund A, Eriksson MJ, Schenck-Gustafsson K, Hirschberg AL. Amenorrhea in female athletes is associated with endothelial dysfunction and unfavorable lipid profile. The Journal of Clinical Endocrinology & Metabolism. 2005 Mar 1;90(3):1354-9.</ref>
*Decreased resting metabolic rate<ref>Melin A, Tornberg ÅB, Skouby S, Møller SS, Sundgot‐Borgen J, Faber J, Sidelmann JJ, Aziz M, Sjödin A. Energy availability and the female athlete triad in elite endurance athletes. Scandinavian journal of medicine & science in sports. 2015 Oct;25(5):610-22.</ref> and slowed growth<ref>Lantzouni E, Frank GR, Golden NH, Shenker RI. Reversibility of growth stunting in early onset anorexia nervosa: a prospective study. Journal of Adolescent Health. 2002 Aug 1;31(2):162-5.</ref><ref>Modan-Moses D, Yaroslavsky A, Novikov I, Segev S, Toledano A, Miterany E, Stein D. Stunting of growth as a major feature of anorexia nervosa in male adolescents. Pediatrics. 2003 Feb 1;111(2):270-6.</ref><ref>Modan-Moses D, Yaroslavsky A, Kochavi B, Toledano A, Segev S, Balawi F, Mitrany E, Stein D. Linear growth and final height characteristics in adolescent females with anorexia nervosa. PloS one. 2012;7(9).</ref>
*Impaired athletic performance and reduced muscle mass<ref>Fagerberg P. Negative consequences of low energy availability in natural male bodybuilding: A review. International journal of sport nutrition and exercise metabolism. 2018 Jul 1;28(4):385-402.</ref>
*Vaginal dryness<ref>Hammar ML, Hammar-Henriksson MB, Frisk J, Rickenlund A, Wyon YA. Few oligo-amenorrheic athletes have vasomotor symptoms. Maturitas. 2000 Mar 31;34(3):219-25.</ref>


=== Osteoporosis ===
== Screening ==
The 2014 Female Athlete Triad Coalition Consensus (Triad Coalition) Statement on Treatment and Return to Play of the Female Athlete Triad, by De Souza and colleagues (2014), identified the following 9 questions that adolescent females should be asked as part of the PPE to screen for the Triad:  
* "Have you ever had a menstrual period?"
* "How old were you when you had your first menstrual period?"
* "When was your most recent menstrual period?"
* "How many periods have you had in the past 12 months?"
* "Are you presently taking any female hormones (estrogen, progesterone, birth control pills)?"
* "Do you worry about your weight?"
* "Are you trying to or has anyone recommended that you gain or lose weight?"
* "Are you on a special diet or do you avoid certain types of foods or food groups?"
* "Have you ever had an eating disorder?"
* "Have you ever had a stress fracture?"
* "Have you ever been told you have low bone density ([[Osteopenia]] or [[Osteoporosis]])?"<ref name=":10">De Souza MJ, Nattiv A, Joy E, Misra M, Williams NI, Mallinson RJ, Gibbs JC, Olmsted M, Goolsby M, Matheson G, Panel E. 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 Feb 1;48(4):289-.</ref>
== Management  ==


Bone quality refers to factors related to bone turnover rates (eg, resorption versus formation, microarchitecture or trabeculae, time for maturation of the new bone matrix, and bone geometry and size).The WHO has established diagnostic criteria for postmenopausal osteoporosis using bone density measurements, however, there is no similar diagnostic crietria that have been established for girls or young women using bone density criterioa. The consequences of ostepenia and osteoporosis in the female athlete are great.Menstruating athletes gain approximately 2-4% of bone mass per year, whereas amenorrheic athletes tend to lose 2% of BMD per year. Thus, it is easy to see why athletes who are involved in high-impact sports can still be more susceptible to fractures than their nonathletic and menstruating athletic counterparts. These include a possible increase in risk for stress fractures, as well as the potential for hip, vertebral and wrist fractures later in life.<ref>Rencken M, Chesnut CH, Drinkwater BL:Decreased bone density at multiple skeletal sites in amenorrheic athletes.JAMA 276:238-40,1996.</ref><ref>Ireland M, Nattiv A. The Female Athlete. Saunders publication.</ref><br>  
When approaching the Triad with an affected athlete it is important to recognize this may be a sensitive topic. Treatment requires a multidisciplinary approach.<ref name=":1" /><ref>Zach KN, Machin AL, Hoch AZ. Advances in management of the female athlete triad and eating disorders. Clinics in sports medicine. 2011 Jul 1;30(3):551-73.</ref> The team may be comprised of various healthcare providers including a physician, registered dietitian, mental health practitioner, physiotherapist<ref name=":1" /><ref>Nazem TG, Ackerman KE. The female athlete triad. Sports Health. 2012 Jul;4(4):302-11.</ref><ref>Papanek PE. The female athlete triad: An emerging role for physical therapy. J Orthop Sports Phys Ther.</ref> (and/or athletic trainer or exercise physiologist), and coach.<ref name="p4">Stickler L, Hoogenboom BJ, Smith L. The Female Athlete Triad‐What Every Physical Therapist Should Know. International journal of sports physical therapy. 2015 Aug;10(4):563.</ref> While interventions can have both pharmacological and non-pharmacological components, non-pharmacological treatment methods are to be the initial course of action.<ref name=":10" /> Pharmacological interventions should be considered if there is no improvement after a year of non-pharmacological intervention and/or the athlete has a relevant history of fractures.<ref name=":10" />


For more information on osteoporosis[http://www.physio-pedia.com/Osteoporosis click here]<br>  
'''Pharmacological interventions:''' may include oral contraceptives, gonadal steroids (estrogen, progesterone, and testosterone), other bone restorative medications, recombinant parathyroid hormone, antidepressants. However pharmacological interventions should not be a first-line therapy. There is a lack of evidence to support them.<ref name=":10" />


= Signs &amp; Symptoms  =
'''Non-pharmacological interventions.''' Low energy availability (EA) is generally directly related to menstrual dysfunction and low bone mineral density (BMD) so it is addressed first and foremost.<ref name=":1" /><ref name=":12" /> Depending on the cause of low EA, the athlete should be referred to a sports dietitian for nutritional education and counselling. If there is suspicion of a clinical eating disorder, the athlete should be referred to a mental health professional for psychological treatment.<ref name=":1" /><ref>Temme KE, Hoch AZ. Recognition and rehabilitation of the female athlete triad/tetrad: a multidisciplinary approach. Current Sports Medicine Reports. 2013 May 1;12(3):190-9.</ref> Depending on the severity, inpatient treatment may be needed. Energy expenditure may also need to be altered by reducing or ceasing exercise.<ref>Mountjoy M, Sundgot-Borgen JK, Burke LM, Ackerman KE, Blauwet C, Constantini N, Lebrun C, Lundy B, Melin AK, Meyer NL, Sherman RT. IOC consensus statement on relative energy deficiency in sport (RED-S): 2018 update. British Journal of Sports Medicine. 2018 May 15.</ref> It is believed that normalizing body weight will promote the return of menses and improve bone health.<ref name=":1" /><ref name=":17">Committee on Sports Medicine and Fitness. Medical concerns in the female athlete. Pediatrics. 2000 Sep 1;106(3):610-3.</ref><ref>Arends JC, Cheung MY, Barrack MT, Nattiv A. Restoration of menses with nonpharmacologic therapy in college athletes with menstrual disturbances: a 5-year retrospective study. International journal of sport nutrition and exercise metabolism. 2012 Apr 1;22(2):98-108.</ref><ref>Misra M, Prabhakaran R, Miller KK, Goldstein MA, Mickley D, Clauss L, Lockhart P, Cord J, Herzog DB, Katzman DK, Klibanski A. Weight gain and restoration of menses as predictors of bone mineral density change in adolescent girls with anorexia nervosa-1. The Journal of Clinical Endocrinology & Metabolism. 2008 Apr 1;93(4):1231-7.</ref><ref>Audí L, Vargas DM, Gussinyé M, Yeste D, Martí G, Carrascosa A. Clinical and biochemical determinants of bone metabolism and bone mass in adolescent female patients with anorexia nervosa. Pediatric research. 2002 Apr;51(4):497-504.</ref> When it comes to low BMD, addressing low EA, increasing body weight, having a regular menstrual cycle, and ensuring adequate calcium and vitamin D are recommended.<ref name=":10" />


If a girl has risk factors for female athlete triad, she may already be experiencing some symptoms and signs of the disorder, such as:
== Role for Physical Therapy in Management  ==


*weight loss<br>  
A study by Pantano (2009)<ref name=":18">Pantano KJ. Strategies used by physical therapists in the US for treatment and prevention of the female athlete triad. Physical Therapy in Sport. 2009 Feb 1;10(1):3-11.</ref> involved 205 physiotherapists and found that 61% self-reported having knowledge of the triad and all 3 of its components. However, when actively assessed, only 21% knew the spectrum.<ref name=":18" /> Pantano (2009)<ref name=":18" /> concluded that physiotherapists need to play a larger role in the prevention of the triad. Physiotherapists possess the knowledge and skills to help prevent a condition from happening in the first place or increasing in severity. They also help maintain and restore function in those dealing with particular conditions. 
*no periods or irregular periods
*fatigue and decreased ability to concentrate
*stress fractures (fractures that occur even if a person hasn't had a significant injury)
*other injuries


Girls with female athlete triad often have signs and symptoms of eating disorders, such as:
Through presentations and discussions, physiotherapists can educate stakeholders in sport on the importance of adopting healthy behaviours and the role physiotherapy plays in preventing and treating the triad.<ref name=":18" /> As mentioned earlier on this page, screening athletes is very important. If there is suspicion of any triad component, the athlete should be referred onwards to a physician, dietitian, and/or mental health professional for further investigations. This may require the physiotherapist to advocate for their patients. 


*continued dieting in spite of weight loss
Physiotherapists can play a role in assessing, modifying and monitoring an athlete’s activity, such that they can help place less focus on cardiovascular training.<ref name=":18" /> Case studies have shown improvements in bone health after athletes with amenorrhea gained some weight,<ref>Zanker CL, Cooke CB, Truscott JG, Oldroyd B, Jacbos HS. Annual changes of bone density over 12 years in an amenorrheic athlete. Medicine & Science in Sports & Exercise. 2004 Jan 1;36(1):137-42.</ref><ref>Fredericson M, Kent K. Normalization of bone density in a previously amenorrheic runner with osteoporosis. Medicine & Science in Sports & Exercise. 2005 Sep 1;37(9):1481-6.</ref> but it is not likely that this will restore BMD by itself.<ref name=":10" /> Resistance exercises,<ref>Martyn-St James M, Carroll S. Progressive high-intensity resistance training and bone mineral density changes among premenopausal women. Sports Medicine. 2006 Aug 1;36(8):683-704.</ref><ref>Wallace BA, Cumming RG. Systematic review of randomized trials of the effect of exercise on bone mass in pre-and postmenopausal women. Calcified Tissue International. 2000 Jul 1;67(1):10-8.</ref> including weight-training, should also be incorporated 2-3 days a week.<ref>Martyn-St James M, Carroll S. Effects of different impact exercise modalities on bone mineral density in premenopausal women: a meta-analysis. Journal of bone and mineral metabolism. 2010 May 1;28(3):251-67.</ref> While simple low-impact weight-bearing exercise has been shown to increase BMD during menopause, it is likely not enough for younger athletes.<ref>Papanek PE. The female athlete triad: an emerging role for physical therapy. Journal of Orthopaedic & Sports Physical Therapy. 2003 Oct;33(10):594-614.</ref> Additionally, high-impact sports, including running, may increase an athlete’s risk of developing stress fractures if they do not have adequate BMD to withstand the repeated forces. Lastly, it is also important to note that physiotherapists have the knowledge and skills to recognize and manage stress fractures and osteoporosis. See [https://www.researchgate.net/publication/8204880_American_College_of_Sports_Medicine_Position_Stand_physical_activity_and_bone_health/link/53d848530cf2e38c633171cd/download American College of Sports Medicine Position Stand: Physical Activity and Bone Health.] 
*preoccupation with food and weight  
*frequent trips to the bathroom during and after meals
*using laxatives
*brittle hair or nails
*dental cavities because in girls with bulimia tooth enamel is worn away by frequent vomiting
*sensitivity to cold
*low heart rate and blood pressure
*heart irregularities and chest pain<br><br>


= Diagnosis  =
As part of a multidisciplinary team, physiotherapists will work closely with others to determine an athlete’s readiness to return-to-play. If the athlete is not ready to fully return-to-play it is recommended athletes receive a written contract from the physician. The physician will work with each multidisciplinary team member to develop treatment goals and a plan that will allow the athlete to progress. Prior to 2014, there were no guidelines on clearing an athlete, but something like the Clearance and Return-to-Play Guidelines by Medical Risk Stratification, or the Decision-Based Return-to-Play model<ref name=":10" /> could be incorporated. [https://www.researchgate.net/publication/269957752_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_Inter Click here to access the article and resources for return-to-play.]


= Resources<br>  =
== Prevention ==
Preventing the triad requires proper education. Coaches, athletic trainers, parents and athletes need to be informed about the female athlete triad.


http://www.femaleathletetriad.org/<br>  
* Mandate annual screening of the triad for female athletes/dancers
* Mandate preseason education
* Mandate education for parents of athletes who are 18 years of age or younger
* Mandate education for coaches and athletic trainers
* Promote healthy stress-management behaviors and tactics
* Promote community awareness of the triad through educational programs<ref name=":2" />


== Recent Related Research (from Pubmed)  ==
== More Resources    ==
<div class="researchbox"><rss>http://www.ncbi.nlm.nih.gov/entrez/eutils/erss.cgi?rss_guid=1bMp6-Tj_k-Tp3SHckuSwmk295VvEN0Zoxm7MyTLE-v7rkPM-e|charset=UTF-8|short|max=10</rss></div>
= References  =


<references /><br>  
{{#ev:youtube|HgqLiwfU3yE|300}}<ref>The AMSSM. Understanding Female Athlete Triad: Evaluation, Diagnosis and Treatment | AMSSM MSIG Webinar. Available from: http://www.youtube.com/watch?v=HgqLiwfU3yE [last accessed 31/5/2022]</ref>
== References  ==
<references />  


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[[Category:Pelvis - Conditions]]
[[Category:Conditions]]

Latest revision as of 04:56, 14 January 2023

Original Editors - Students from Bellarmine University's Pathophysiology of Complex Patient Problems project.

Top Contributors - James Chad Cissell, Michelle Walsh, Ethan Adams, Aarti Sareen, Lucinda hampton, Wanda van Niekerk, Regan Haley, Kim Jackson, Elaine Lonnemann, Nicole Hills, 127.0.0.1, Oyemi Sillo, WikiSysop, Adam Vallely Farrell, Rishika Babburu and Claire Knott  

Introduction[edit | edit source]

Ballet dancers at risk

The female athlete triad comprises three medical conditions, and is seen commonly in active teen girls:

The components of the female athlete triad are interconnected:

  • Disordered eating leads to inadequate nutrition.
  • Inadequate nutrition affects the production of hormones such as estrogen.
  • Estrogen has an important role in bone development, low levels of estrogen leads to weakened bones and increasing the risk of injury.[2]

The below 2 minute video gives a good overview of the condition.

[3]

Epidemiology[edit | edit source]

Studies suggest that between 15-62% of the female athletic population exhibit disordered eating behaviours. Amenorrhea among female athletes range between 3-66%, depending on the definition that is used.[2]

Gymnasts: risk group

Risk Factors

Those at greatest risk are girls involved in sports in which performance is scored subjectively, a low bodyweight is a focus, figure hugging clothing is required for competition, weight categories are used for participation and an immature body is seen as better for performance.[2]

  • Categories of athletes at risk include: runner, dancers, gymnastics, figure skaters.[1]
  • At greater risk are highly competitive athletes.[4]
  • Younger individuals are greatly impacted by the non-reversible, long-term consequences of this syndrome. In fact, a study on animals found that low energy availability can decrease growth and hinder sexual development.[5]

Mechanisms[edit | edit source]

Becoming aware of how each component can develop and present itself will aid healthcare providers and other stakeholders in sport in the early recognition of the female athlete triad. The Three components comprise:

Low Energy Availability With or Without an Eating Disorder. A low energy availability (EA) can be due to decreased dietary energy intake and/or increased energy expended during exercise and, when EA is low, this leads to less energy available for body functions.

  • Some athletes may participate in restrictive diets or use pills or laxatives.[6][7][8][9][10][11]
  • Other athletes may have a diagnosis of an eating disorder (eg Anorexia Nervosa, Bulimia Nervosa, Binge Eating Disorder)[12] e Eating disorders can cause many problems, including dehydration, muscle fatigue and weakness, an erratic heartbeat, kidney damage, osteoporosis and hormone imbalances.[13]

Menstrual Dysfunction: include:

  1. Primary amenorrhea: pre-adolescent who hasn’t had a menstrual period by the age of 16 or has gone two years following the development of secondary sex characteristics without menarche. Eating disorders may be the cause.
  2. Secondary amenorrhea: menstruation ceases for three months or longer in a woman who has previously had normal menstruation. An integral part of anorexia nervosa.
  3. Oligomenorrhea: menstrual cycle occurs at irregular intervals.[2]

Low Bone Mineral Density: Bone is a dynamic structure, constantly being remodelled by osteoclasts and osteoblasts. Female athletes, functioning at a low estrogen state, have less osteoblastic activity. Athletes require 5% to 15% higher bone mineral density than age-matched nonathlete, with reduced bone mineral density increases bone fragility and increase the risk of fractures. Stress fractures occurence is greater in amenorrheic athletes, and bone density has been shown to progressively decrease as the number of menstrual cycles missed since menarche increases.[14]

Manifestations (including systemic involvement)[edit | edit source]

  • Weight loss
  • Absent or irregular menstrual cycles (includes primary and secondary amenorrhea, as well as oligomenorrhea)
  • Chronic fatigue
  • Fractures without significant trauma (low force cause); most common location is the tibia[15][16][17][18]
  • Compulsive exercise
  • Increased infections and illnesses[19]
  • Decreased ability to recovery from injuries (slower tissue repair)[20]
  • Anxiety[21][22] and depression[21][23]
  • Nutrient deficits
  • Esophagitis and oesophageal perforation if self-induced vomiting[24]
  • Constipation[25]
  • Changes in thyroid function, appetite, decrease in insulin, increase in cortisol, and resistance to growth hormones[26][27][28][29][30]
  • Increased cardiovascular risk (including atherosclerosis)[31] due to increase in bad lipids and endothelial dysfunction[32]
  • Decreased resting metabolic rate[33] and slowed growth[34][35][36]
  • Impaired athletic performance and reduced muscle mass[37]
  • Vaginal dryness[38]

Screening[edit | edit source]

The 2014 Female Athlete Triad Coalition Consensus (Triad Coalition) Statement on Treatment and Return to Play of the Female Athlete Triad, by De Souza and colleagues (2014), identified the following 9 questions that adolescent females should be asked as part of the PPE to screen for the Triad:  

  • "Have you ever had a menstrual period?"
  • "How old were you when you had your first menstrual period?"
  • "When was your most recent menstrual period?"
  • "How many periods have you had in the past 12 months?"
  • "Are you presently taking any female hormones (estrogen, progesterone, birth control pills)?"
  • "Do you worry about your weight?"
  • "Are you trying to or has anyone recommended that you gain or lose weight?"
  • "Are you on a special diet or do you avoid certain types of foods or food groups?"
  • "Have you ever had an eating disorder?"
  • "Have you ever had a stress fracture?"
  • "Have you ever been told you have low bone density (Osteopenia or Osteoporosis)?"[39]

Management[edit | edit source]

When approaching the Triad with an affected athlete it is important to recognize this may be a sensitive topic. Treatment requires a multidisciplinary approach.[19][40] The team may be comprised of various healthcare providers including a physician, registered dietitian, mental health practitioner, physiotherapist[19][41][42] (and/or athletic trainer or exercise physiologist), and coach.[43] While interventions can have both pharmacological and non-pharmacological components, non-pharmacological treatment methods are to be the initial course of action.[39] Pharmacological interventions should be considered if there is no improvement after a year of non-pharmacological intervention and/or the athlete has a relevant history of fractures.[39]

Pharmacological interventions: may include oral contraceptives, gonadal steroids (estrogen, progesterone, and testosterone), other bone restorative medications, recombinant parathyroid hormone, antidepressants. However pharmacological interventions should not be a first-line therapy. There is a lack of evidence to support them.[39]

Non-pharmacological interventions. Low energy availability (EA) is generally directly related to menstrual dysfunction and low bone mineral density (BMD) so it is addressed first and foremost.[19][24] Depending on the cause of low EA, the athlete should be referred to a sports dietitian for nutritional education and counselling. If there is suspicion of a clinical eating disorder, the athlete should be referred to a mental health professional for psychological treatment.[19][44] Depending on the severity, inpatient treatment may be needed. Energy expenditure may also need to be altered by reducing or ceasing exercise.[45] It is believed that normalizing body weight will promote the return of menses and improve bone health.[19][46][47][48][49] When it comes to low BMD, addressing low EA, increasing body weight, having a regular menstrual cycle, and ensuring adequate calcium and vitamin D are recommended.[39]

Role for Physical Therapy in Management[edit | edit source]

A study by Pantano (2009)[50] involved 205 physiotherapists and found that 61% self-reported having knowledge of the triad and all 3 of its components. However, when actively assessed, only 21% knew the spectrum.[50] Pantano (2009)[50] concluded that physiotherapists need to play a larger role in the prevention of the triad. Physiotherapists possess the knowledge and skills to help prevent a condition from happening in the first place or increasing in severity. They also help maintain and restore function in those dealing with particular conditions. 

Through presentations and discussions, physiotherapists can educate stakeholders in sport on the importance of adopting healthy behaviours and the role physiotherapy plays in preventing and treating the triad.[50] As mentioned earlier on this page, screening athletes is very important. If there is suspicion of any triad component, the athlete should be referred onwards to a physician, dietitian, and/or mental health professional for further investigations. This may require the physiotherapist to advocate for their patients. 

Physiotherapists can play a role in assessing, modifying and monitoring an athlete’s activity, such that they can help place less focus on cardiovascular training.[50] Case studies have shown improvements in bone health after athletes with amenorrhea gained some weight,[51][52] but it is not likely that this will restore BMD by itself.[39] Resistance exercises,[53][54] including weight-training, should also be incorporated 2-3 days a week.[55] While simple low-impact weight-bearing exercise has been shown to increase BMD during menopause, it is likely not enough for younger athletes.[56] Additionally, high-impact sports, including running, may increase an athlete’s risk of developing stress fractures if they do not have adequate BMD to withstand the repeated forces. Lastly, it is also important to note that physiotherapists have the knowledge and skills to recognize and manage stress fractures and osteoporosis. See American College of Sports Medicine Position Stand: Physical Activity and Bone Health. 

As part of a multidisciplinary team, physiotherapists will work closely with others to determine an athlete’s readiness to return-to-play. If the athlete is not ready to fully return-to-play it is recommended athletes receive a written contract from the physician. The physician will work with each multidisciplinary team member to develop treatment goals and a plan that will allow the athlete to progress. Prior to 2014, there were no guidelines on clearing an athlete, but something like the Clearance and Return-to-Play Guidelines by Medical Risk Stratification, or the Decision-Based Return-to-Play model[39] could be incorporated. Click here to access the article and resources for return-to-play.

Prevention[edit | edit source]

Preventing the triad requires proper education. Coaches, athletic trainers, parents and athletes need to be informed about the female athlete triad.

  • Mandate annual screening of the triad for female athletes/dancers
  • Mandate preseason education
  • Mandate education for parents of athletes who are 18 years of age or younger
  • Mandate education for coaches and athletic trainers
  • Promote healthy stress-management behaviors and tactics
  • Promote community awareness of the triad through educational programs[2]

More Resources[edit | edit source]

[57]

References[edit | edit source]

  1. ↑ 1.0 1.1 WebMD The Female Athlete Triad Available:https://teens.webmd.com/female-athlete-triad (accessed 14.1.2023)
  2. ↑ 2.0 2.1 2.2 2.3 2.4 Womens sport foundation. The female athlete triad Available:https://www.womenssportsfoundation.org/inspiration/the-female-athlete-triad/ (accessed 14.1.2023)
  3. ↑ Riverside. Female Athlete Triad Syndrome. Available from: https://www.youtube.com/watch?v=zq6qhTP8i18 [last accessed 14.1.2023]
  4. ↑ De Souza MJ, Miller BE, Loucks AB, Luciano AA, Pescatello LS, Campbell CG, Lasley BL. High frequency of luteal phase deficiency and anovulation in recreational women runners: blunted elevation in follicle-stimulating hormone observed during luteal-follicular transition. The Journal of Clinical Endocrinology & Metabolism. 1998 Dec 1;83(12):4220-32.
  5. ↑ Schneider JE, Wade GN. Inhibition of reproduction in service of energy balance. Reproduction in Context: Social and Environmental Influences on Reproductive Physiology and Behavior. 2000:35-82.
  6. ↑ Beals KA, Hill AK. The prevalence of disordered eating, menstrual dysfunction, and low bone mineral density among US collegiate athletes. International journal of sport nutrition and exercise metabolism. 2006 Feb 1;16(1):1-23.
  7. ↑ Beals KA, Manore MM. Disorders of the female athlete triad among collegiate athletes. International journal of sport nutrition and exercise metabolism. 2002 Sep 1;12(3):281-93.
  8. ↑ Sundgot-Borgen J. Prevalence of eating disorders in elite female athletes. International Journal of Sport Nutrition and Exercise Metabolism. 1993 Mar 1;3(1):29-40.
  9. ↑ Yager J, Devlin MJ, Halmi KA, Herzog DB, Mitchell JE, Powers PS, Zerbe KJ. Guideline watch: Practice guideline for the treatment of patients with eating disorders. Focus. 2005 Oct;3(4):546-51.
  10. ↑ Johnson C, Powers PS, Dick R. Athletes and eating disorders: the National Collegiate Athletic Association study. International Journal of Eating Disorders. 1999 Sep;26(2):179-88.
  11. ↑ Sundgot-Borgen J. Nutrient intake of female elite athletes suffering from eating disorders. International Journal of Sport Nutrition and Exercise Metabolism. 1993 Dec 1;3(4):431-42.
  12. ↑ American Psychiatric Association. Diagnostic and statistical manual of mental disorders (DSM-5®). American Psychiatric Pub; 2013 May 22.
  13. ↑ Orthoinfo Female Athlete Triad: Problems Caused by Extreme Exercise and Dieting Available:https://orthoinfo.aaos.org/en/diseases--conditions/female-athlete-triad-problems-caused-by-extreme-exercise-and-dieting/ (accessed 14.1.2023)
  14. ↑ Raj MA, Creech JA, Rogol AD. Female Athlete Triad. 2021 Aug 14. StatPearls. Treasure Island (FL): StatPearls Publishing. 2022.Available:https://www.ncbi.nlm.nih.gov/books/NBK430787/ (accessed 14.1.2023)
  15. ↑ Barrow GW, Saha S. Menstrual irregularity and stress fractures in collegiate female distance runners. The American journal of sports medicine. 1988 May;16(3):209-16.
  16. ↑ Bennell KL, Malcolm SA, Thomas SA, Wark JD, Brukner PD. The incidence and distribution of stress fractures in competitive track and field athletes: a twelve-month prospective study. The American journal of sports medicine. 1996 Mar;24(2):211-7.
  17. ↑ Iwamoto J, Takeda T. Stress fractures in athletes: review of 196 cases. Journal of Orthopaedic Science. 2003 May 1;8(3):273-8.
  18. ↑ Shaffer RA, Rauh MJ, Brodine SK, Trone DW, Macera CA. Predictors of stress fracture susceptibility in young female recruits. The American journal of sports medicine. 2006 Jan;34(1):108-15.
  19. ↑ 19.0 19.1 19.2 19.3 19.4 19.5 Nattiv A, Loucks AB, Manore MM, Sanborn CF, Sundgot-Borgen J, Warren MP; American College of Sports Medicine. American College of Sports Medicine position stand: the female athlete triad. Med Sci Sports Exerc. 2007;39(10):1867–1882
  20. ↑ Manore MM, Kam LC, Loucks AB. The female athlete triad: components, nutrition issues, and health consequences. Journal of sports sciences. 2007 Dec 1;25(S1):S61-71.
  21. ↑ 21.0 21.1 Berga SL, Loucks TL. Use of cognitive behavior therapy for functional hypothalamic amenorrhea. Annals of the New York Academy of Sciences. 2006 Dec;1092(1):114-29.
  22. ↑ Nappi RE, Facchinetti F. Psychoneuroendocrine correlates of secondary amenorrhea. Archives of women's mental health. 2003 Apr 1;6(2):83-9.
  23. ↑ Stice E, South K, Shaw H. Future directions in etiologic, prevention, and treatment research for eating disorders. Journal of Clinical Child & Adolescent Psychology. 2012 Nov 1;41(6):845-55.
  24. ↑ 24.0 24.1 Mountjoy M, Sundgot-Borgen J, Burke L, Carter S, Constantini N, Lebrun C, Meyer N, Sherman R, Steffen K, Budgett R, Ljungqvist A. The IOC consensus statement: beyond the female athlete triad—Relative Energy Deficiency in Sport (RED-S). Br J Sports Med. 2014 Apr 1;48(7):491-7.
  25. ↑ Norris ML, Harrison ME, Isserlin L, Robinson A, Feder S, Sampson M. Gastrointestinal complications associated with anorexia nervosa: A systematic review. International Journal of Eating Disorders. 2016 Mar;49(3):216-37.
  26. ↑ Ihle R, Loucks AB. Dose‐response relationships between energy availability and bone turnover in young exercising women. Journal of bone and mineral research. 2004 Aug;19(8):1231-40.
  27. ↑ Loucks AB, Thuma JR. Luteinizing hormone pulsatility is disrupted at a threshold of energy availability in regularly menstruating women. The Journal of Clinical Endocrinology & Metabolism. 2003 Jan 1;88(1):297-311.
  28. ↑ Allaway HC, Southmayd EA, De Souza MJ. The physiology of functional hypothalamic amenorrhea associated with energy deficiency in exercising women and in women with anorexia nervosa. Hormone molecular biology and clinical investigation. 2016 Feb 1;25(2):91-119.
  29. ↑ Logue D, Madigan SM, Delahunt E, Heinen M, Mc Donnell SJ, Corish CA. Low energy availability in athletes: a review of prevalence, dietary patterns, physiological health, and sports performance. Sports Medicine. 2018 Jan 1;48(1):73-96.
  30. ↑ Misra M. Neuroendocrine mechanisms in athletes. InHandbook of clinical neurology 2014 Jan 1 (Vol. 124, pp. 373-386). Elsevier.
  31. ↑ O'Donnell E, Goodman JM, Harvey PJ. Cardiovascular consequences of ovarian disruption: a focus on functional hypothalamic amenorrhea in physically active women. The Journal of Clinical Endocrinology & Metabolism. 2011 Dec 1;96(12):3638-48.
  32. ↑ Rickenlund A, Eriksson MJ, Schenck-Gustafsson K, Hirschberg AL. Amenorrhea in female athletes is associated with endothelial dysfunction and unfavorable lipid profile. The Journal of Clinical Endocrinology & Metabolism. 2005 Mar 1;90(3):1354-9.
  33. ↑ Melin A, Tornberg ÅB, Skouby S, Møller SS, Sundgot‐Borgen J, Faber J, Sidelmann JJ, Aziz M, Sjödin A. Energy availability and the female athlete triad in elite endurance athletes. Scandinavian journal of medicine & science in sports. 2015 Oct;25(5):610-22.
  34. ↑ Lantzouni E, Frank GR, Golden NH, Shenker RI. Reversibility of growth stunting in early onset anorexia nervosa: a prospective study. Journal of Adolescent Health. 2002 Aug 1;31(2):162-5.
  35. ↑ Modan-Moses D, Yaroslavsky A, Novikov I, Segev S, Toledano A, Miterany E, Stein D. Stunting of growth as a major feature of anorexia nervosa in male adolescents. Pediatrics. 2003 Feb 1;111(2):270-6.
  36. ↑ Modan-Moses D, Yaroslavsky A, Kochavi B, Toledano A, Segev S, Balawi F, Mitrany E, Stein D. Linear growth and final height characteristics in adolescent females with anorexia nervosa. PloS one. 2012;7(9).
  37. ↑ Fagerberg P. Negative consequences of low energy availability in natural male bodybuilding: A review. International journal of sport nutrition and exercise metabolism. 2018 Jul 1;28(4):385-402.
  38. ↑ Hammar ML, Hammar-Henriksson MB, Frisk J, Rickenlund A, Wyon YA. Few oligo-amenorrheic athletes have vasomotor symptoms. Maturitas. 2000 Mar 31;34(3):219-25.
  39. ↑ 39.0 39.1 39.2 39.3 39.4 39.5 39.6 De Souza MJ, Nattiv A, Joy E, Misra M, Williams NI, Mallinson RJ, Gibbs JC, Olmsted M, Goolsby M, Matheson G, Panel E. 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 Feb 1;48(4):289-.
  40. ↑ Zach KN, Machin AL, Hoch AZ. Advances in management of the female athlete triad and eating disorders. Clinics in sports medicine. 2011 Jul 1;30(3):551-73.
  41. ↑ Nazem TG, Ackerman KE. The female athlete triad. Sports Health. 2012 Jul;4(4):302-11.
  42. ↑ Papanek PE. The female athlete triad: An emerging role for physical therapy. J Orthop Sports Phys Ther.
  43. ↑ Stickler L, Hoogenboom BJ, Smith L. The Female Athlete Triad‐What Every Physical Therapist Should Know. International journal of sports physical therapy. 2015 Aug;10(4):563.
  44. ↑ Temme KE, Hoch AZ. Recognition and rehabilitation of the female athlete triad/tetrad: a multidisciplinary approach. Current Sports Medicine Reports. 2013 May 1;12(3):190-9.
  45. ↑ Mountjoy M, Sundgot-Borgen JK, Burke LM, Ackerman KE, Blauwet C, Constantini N, Lebrun C, Lundy B, Melin AK, Meyer NL, Sherman RT. IOC consensus statement on relative energy deficiency in sport (RED-S): 2018 update. British Journal of Sports Medicine. 2018 May 15.
  46. ↑ Committee on Sports Medicine and Fitness. Medical concerns in the female athlete. Pediatrics. 2000 Sep 1;106(3):610-3.
  47. ↑ Arends JC, Cheung MY, Barrack MT, Nattiv A. Restoration of menses with nonpharmacologic therapy in college athletes with menstrual disturbances: a 5-year retrospective study. International journal of sport nutrition and exercise metabolism. 2012 Apr 1;22(2):98-108.
  48. ↑ Misra M, Prabhakaran R, Miller KK, Goldstein MA, Mickley D, Clauss L, Lockhart P, Cord J, Herzog DB, Katzman DK, Klibanski A. Weight gain and restoration of menses as predictors of bone mineral density change in adolescent girls with anorexia nervosa-1. The Journal of Clinical Endocrinology & Metabolism. 2008 Apr 1;93(4):1231-7.
  49. ↑ Audí L, Vargas DM, Gussinyé M, Yeste D, Martí G, Carrascosa A. Clinical and biochemical determinants of bone metabolism and bone mass in adolescent female patients with anorexia nervosa. Pediatric research. 2002 Apr;51(4):497-504.
  50. ↑ 50.0 50.1 50.2 50.3 50.4 Pantano KJ. Strategies used by physical therapists in the US for treatment and prevention of the female athlete triad. Physical Therapy in Sport. 2009 Feb 1;10(1):3-11.
  51. ↑ Zanker CL, Cooke CB, Truscott JG, Oldroyd B, Jacbos HS. Annual changes of bone density over 12 years in an amenorrheic athlete. Medicine & Science in Sports & Exercise. 2004 Jan 1;36(1):137-42.
  52. ↑ Fredericson M, Kent K. Normalization of bone density in a previously amenorrheic runner with osteoporosis. Medicine & Science in Sports & Exercise. 2005 Sep 1;37(9):1481-6.
  53. ↑ Martyn-St James M, Carroll S. Progressive high-intensity resistance training and bone mineral density changes among premenopausal women. Sports Medicine. 2006 Aug 1;36(8):683-704.
  54. ↑ Wallace BA, Cumming RG. Systematic review of randomized trials of the effect of exercise on bone mass in pre-and postmenopausal women. Calcified Tissue International. 2000 Jul 1;67(1):10-8.
  55. ↑ Martyn-St James M, Carroll S. Effects of different impact exercise modalities on bone mineral density in premenopausal women: a meta-analysis. Journal of bone and mineral metabolism. 2010 May 1;28(3):251-67.
  56. ↑ Papanek PE. The female athlete triad: an emerging role for physical therapy. Journal of Orthopaedic & Sports Physical Therapy. 2003 Oct;33(10):594-614.
  57. ↑ The AMSSM. Understanding Female Athlete Triad: Evaluation, Diagnosis and Treatment | AMSSM MSIG Webinar. Available from: http://www.youtube.com/watch?v=HgqLiwfU3yE [last accessed 31/5/2022]
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