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== Definition/Description  ==
== Introduction ==
 
[[File:At risk Female athletic triad.jpeg|thumb|Ballet dancers at risk |alt=|300x300px]]
Female Athlete Triad is a syndrome that evolves from the interrelationships among energy availability, bone mineral density, and menstrual function. The clinical manifestations include eating disorders, functional hypothalamic amenorrhea, and osteoporosis. Not all clinical signs must be present to diagnose Female Athlete Triad.<ref name="1">The Female Athlete Triad. Medicine &amp;amp;amp;amp; Science In Sports &amp;amp;amp;amp; Exercise [serial on the Internet]. (2007, Oct), [cited March 27, 2017]; 39(10): 1867-1882. Available from: Academic Search Complete.</ref>&nbsp;Female Athlete Triad commonly occurs in adolescent or highly competitive female athletes. This syndrome is most common in Adolescent athletes largely due to their skeletal immaturity and naturally low Bone Mineral Density (BMD) being more susceptible to physical and metabolic stressors. Along with health care providers, all coaching staff members of high level and high school women’s sports teams should be highly aware of signs of this disease in order to manage the health of their players.<ref name="2">Mukherjee S, Chand V, Wong X, Choong P, Lau V, Ng K, et al. Perceptions, awareness and knowledge of the Female Athlete Triad amongst coaches—Are we meeting the expectations for athlete safety?. International Journal Of Sports Science &amp;amp;amp;amp; Coaching [serial on the Internet]. (2016, Aug), [cited March 27, 2017]; 11(4): 545-551. Available from: PsycINFO.</ref>&nbsp;It is also recommended that all female athletes are screened for Female Athlete Triad on a yearly basis.<ref name="3">Thein-Nissenbaum J. Long term consequences of the female athlete triad. Maturitas [serial on the Internet]. (2013, June), [cited March 27, 2017]; 75(2): 107-112. Available from: MEDLINE.</ref> Early signs of the Female Athlete Triad include weight changes, repeated fractures, and decreased energy.Longterm effects of Female Athlete Triad include low peak BMD, Osteoporosis, Thoughts of suicide during long term disease process, and kidney and liver dysfunction.<ref name="3" /><br>
The female athlete triad comprises three medical conditions, and is seen commonly in active teen girls:
 
[[Image:Triad-diagram.jpg]]<ref name="1" /><ref name="4">Stickler L, Hoogenboom B, Smith L. THE FEMALE ATHLETE TRIAD-WHAT EVERY PHYSICAL THERAPIST SHOULD KNOW. International Journal Of Sports Physical Therapy [serial on the Internet]. (2015, Aug), [cited March 27, 2017]; 10(4): 563-571. Available from: MEDLINE.</ref>
 
== Prevalence  ==
 
Due to inconsistencies and limitations in criteria defining Female Athlete Triad, study methodology, and experimental design there is an evident discrepancy in the literature when determining the prevalence of the triad. The chances of all three conditions of the triad presenting simultaneously are low, ranging from 0% to 16%. The odds of two conditions presenting at the same time range from 3% to 27%. Generally, most common to just have one of the conditions present with the odds ranging from 16% to 60%.<ref name="5">Gibbs J, Williams N, De Souza M. Prevalence of individual and combined components of the female athlete triad. Medicine And Science In Sports And Exercise [serial on the Internet]. (2013, May), [cited March 27, 2017]; 45(5): 985-996. Available from: MEDLINE.</ref> Since a diagnosis for Female Athlete Triad is possible without having all three components of the triad, it is possible for sedentary and normally active females to be diagnosed with the syndrome at rates that are only slightly less than competitive female athletes.<ref name="6">Hoch A, Pajewski N, Moraski L, Carrera G, Wilson C, Gutterman D, et al. Prevalence of the female athlete triad in high school athletes and sedentary students. Clinical Journal Of Sport Medicine: Official Journal Of The Canadian Academy Of Sport Medicine [serial on the Internet]. (2009, Sep), [cited March 27, 2017]; 19(5): 421-428. Available from: MEDLINE.</ref><ref name="7">Torstveit M, Sundgot-Borgen J. The female athlete triad exists in both elite athletes and controls. Medicine And Science In Sports And Exercise [serial on the Internet]. (2005, Sep), [cited March 27, 2017]; 37(9): 1449-1459. Available from: MEDLINE.</ref><br><br>
 
== Characteristics/Clinical Presentation  ==
 
*Weight loss
*Absent or irregular periods
*Fatigue
*Stress fractures
*Restrictive dieting
*Binge eating
*Induced vomiting
*Excessive exercise<br>


== Associated Co-morbidities  ==
* 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:


Due to the loss in bone mineral density the primary comorbidity associated with female athlete triad is osteoporosis. Female athlete triad generally occurs in the primary age range for storing and depositing calcium in the bones. Slowing or reversing this possess will result in the potential to increase the risk of fractures later in life even after resolving the issues leading to a diagnosis of female athlete triad.  
* 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>


Systemically low Bone MIneral Density, low blood estrogen level, and menstrual dysfunction has been linked to Endothelial Dysfunction in endurance athletes. Endothelial Dysfunction is directly related to the bodies ability to constrict or dilate blood vessels. If Endothelial Dysfunction is present (indicated by Brachial Artery flow-mediated dilation) the risk for Cardiovascular Events, poor blood flow mediation, and athrosclerotic disease are all increased significantly.<ref name="8">Weiss Kelly A, Hecht S. The Female Athlete Triad. Pediatrics [serial on the Internet]. (2016, Aug), [cited March 27, 2017]; 138(2): e1-e10. Available from: Academic Search Complete.</ref><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'''


== Medications  ==
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" />


Antidepressants are often used to treat associated concomitant depression and anxiety disorders. They are also used following weight restoration for bulimia nervosa and anorexia nervosa. Research has show mixed results for improving BMD or restoring menstrual cycles when using hormone replacement therapy (HRT) or oral contraceptive pill (OCP). While BMD may not be improved by using OCP, it may help to reduce further loss in BMD in athletes under the age of 16.Young women with functional hypothalamic amenorrhea should not use bisphosphonates that are approved for the treatment of postmenopausal osteoporosis due to their unproven efficacy in women of childbearing age. Also since the medication tend to linger in the bones for many years they have the potential to cause harm to a developing fetus is the patient becomes pregnant later in life.Ovulation inducing agents such as clomiphene citrate and exogenous gonadotropins are indicated if the aim of therapy is to restore fertility.<ref name="1" /> Nutritional therapy has the best evidence for successfully treating female athlete triad due to its ability to in increase energy availability.<ref name="9">Javed A, Tebben P, Fischer P, Lteif A. Female athlete triad and its components: toward improved screening and management. Mayo Clinic Proceedings [serial on the Internet]. (2013, Sep), [cited March 27, 2017]; 88(9): 996-1009. Available from: MEDLINE.</ref><br><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>


== Diagnostic Tests/Lab Tests/Lab Values  ==
== 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:


Athletes most commonly show signs of 1 or 2 components of Female Athlete Triad.&nbsp;If suspected due to pain, recurrent fractures, recurrent sprains, Low BMI (&lt;85% expected weight), poor eating habits, or other, use the following questions to see if there is cause for concern.<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>


[[Image:Triad_Table1.png]]<ref name="10" /><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>


== 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  ==


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" />


Table 1 from (10)
'''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" />


Table2 from (10)
'''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" />


<u>Risk Factors</u>(8,10, 11,)<u></u>
== Role for Physical Therapy in Management  ==


Non-Modifiable:  
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. 


*Female Gender
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. 
*Age 12-19 (10)


Modifiable:  
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.] 


*Early age sport specialization
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.]
*Low BMI (Z-score less than or equal to -1)
*Overtraining
*Engaging in sports with endurance, aesthetic, and weight class components
*Severe Dieting
*Family Dysfunction
*Abuse


<u>Energy Availability (EA)</u>
== Prevention ==
Preventing the triad requires proper education. Coaches, athletic trainers, parents and athletes need to be informed about the female athlete triad.


*&nbsp;Energy Intake should be at least 45 kcal/kg of fat-free mass (FFM)<ref name="8" />
* Mandate annual screening of the triad for female athletes/dancers
*&lt; 30kcal/kg FFM disrupts bone mineralization and menstruation<ref name="8" />
* Mandate preseason education
*5 days or more of &lt; 30kcal/kg decreases luteinizing hormone availability in the body<ref name="8" />
* 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" />


Triggers for disordered eating may include: Prolonged dieting, weight fluctuations, changes in coaching, injury, and social attention to weight.
== More Resources    ==


<u>Bone Mineral Density</u><br>In women, about 90% of bone formation should be complete by 18 years old<ref name="3" />, with bone density peaking between 20-30 years old. Poor Bone Mineral density is correlated with being &lt;85% expected weight for height and age. A Z-score at or below -1.0 is cause for concern.&nbsp;Long Distance Running is a highest risk sport for negatively impacting BMD<br>BMD Screenings such as for celiacs disease<ref name="10">Payne J, Kirchner J. Should you suspect the female athlete triad?. The Journal Of Family Practice [serial on the Internet]. (2014, Apr), [cited March 27, 2017]; 63(4): 187-192. Available from: MEDLINE.</ref><br>Menstruation<br>Disorders in menstrual function can be as mild as anovulation and luteal dysfunction to Oligomenorrhea and Amenorrhea<br>Menstrual disturbances are common in all adolescents (~21%), but more common in adolescent athletes (~54%)<ref name="8" />
{{#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>
 
*-Anovulation - ovaries do not release an oocyte and ovulation doesn’t occur. (few overt symptoms)
*-Luteal Deficiency - low concentration of blood progesterone and or Luteal phase lasting less than 11 days (few overt symptoms)
*-Oligomenorrhea - menstrual cycles lasting longer than 35 days
*-primary Amenorrhea is the “absence of menarche by the age of 15 years.”<ref name="8" />
*-secondary Amenorrhea is absence of menstruation for greater than or equal to 3 consecutive months after menarche<br><br>
 
== Etiology/Causes  ==
 
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== Systemic Involvement  ==
 
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== Medical Management (current best evidence)  ==
 
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== Physical Therapy Management (current best evidence)  ==
 
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== Differential Diagnosis  ==
 
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== Case Reports/ Case Studies  ==
 
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== Resources <br>  ==
 
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== Recent Related Research (from [http://www.ncbi.nlm.nih.gov/pubmed/ Pubmed])  ==
 
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Latest revision as of 04:56, 14 January 2023

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)
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  22. Nappi RE, Facchinetti F. Psychoneuroendocrine correlates of secondary amenorrhea. Archives of women's mental health. 2003 Apr 1;6(2):83-9.
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  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.
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  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.
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  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.
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  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]