Female Athlete Triad: Difference between revisions

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== Definition/Description  ==
== Introduction ==
[[File:At risk Female athletic triad.jpeg|thumb|Ballet dancers at risk |alt=|300x300px]]
The female athlete triad comprises three medical conditions, and is seen commonly in active teen girls:


The Female athlete triad was originally defined as an interrelation of amenorrhea, osteoporosis, and disordered eating that would exist simultaneously.<ref>Otis CL, Drinkwater B, Johnson M, Loucks A, Wilmore J. American College of Sports Medicine position stand: the Female Athlete Triad. ''Med Sci Sports Exerc''. 1997;29(5):i–ix </ref> More recently, it has been recognized that these 3 conditions exist on a spectrum and they have since been renamed menstrual dysfunction, low bone mineral density, and low energy availability with or without an eating disorder.<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> It is important to note that not all components of the triad need to be present to make the diagnosis; only one is needed.<ref name=":1" /><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> Timely prevention, recognition, and treatment are important at delaying the progression as any one of the 3 triad components puts the individual at a higher risk of incurring all 3.<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=":0">Nichols JF, Rauh MJ, Lawson MJ, Ji M, Barkai HS. Prevalence of the female athlete triad syndrome among high school athletes. Archives of pediatrics & adolescent medicine. 2006 Feb 1;160(2):137-42.</ref> Each component of the triad can have irreversible consequences,<ref name=":1" /> and the components can increase in severity.    <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:  


[[Image:Triad-diagram.jpg]]<ref name=":1" /><ref name=":10" />  
* 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 figure above depicts the female athlete triad spectrum.<ref name=":1" /> The black lines are representative of the spectrums of each of the 3 components and the red and green triangles show both of the extremes. The top right, green triangle, is desired and it is representative of a healthy athlete who has a good balance between energy intake and expenditure. Because of this, they have a normal menstruation cycle and a bone mineral density that is above average for the athlete’s age. The bottom left, red triangle, is undesired and it is representative of an athlete who does not have an appropriate balance between energy intake and expenditure, which may be the result of restrictive dieting and/or clinical eating disorders. Because of the lack of balance, they develop functional hypothalamic amenorrhea and osteoporosis (hormones, including estrogen, that promote the formation of bone are suppressed). 
== Epidemiology ==
== Prevalence  ==
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'''


The female athlete triad occurs in girls and women, especially if they are highly competitive athletes. The development of female athlete triad is also possible in those who are sedentary and recreationally active<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><ref>De Souza MJ, Toombs RJ, Scheid JL, O'Donnell E, West SL, Williams NI. High prevalence of subtle and severe menstrual disturbances in exercising women: confirmation using daily hormone measures. Human reproduction. 2010 Feb 1;25(2):491-503.</ref> but the prevalence rate is less than that of more competitive athletes.<ref name=":2">Hoch AZ, Pajewski NM, Moraski L, Carrera GF, Wilson CR, Hoffmann RG, Schimke JE, Gutterman DD. 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. 2009 Sep;19(5):421.</ref><ref name=":3">TORSTVEIT MK, SUNDGOT-BORGEN JO. The female athlete triad exists in both elite athletes and controls. Medicine & Science in Sports & Exercise. 2005 Sep 1;37(9):1449-59.</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>  
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" />  


Unfortunately, due to inconsistencies and limitations in definition criteria and experimental design,<ref name=":1" /><ref>De Souza MJ, Williams NI. Physiological aspects and clinical sequelae of energy deficiency and hypoestrogenism in exercising women. Human reproduction update. 2004 Sep;10(5):433-48.</ref> it is difficult to determine the prevalence of all three components of the Triad existing simultaneously. However, a lot of evidence exists looking at the prevalence of each individual component.<ref name=":4">Gibbs JC, Williams NI, De Souza MJ. Prevalence of individual and combined components of the female athlete triad. Medicine & Science in Sports & Exercise. 2013 May 1;45(5):985-96.</ref>
* 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>


A systematic review by Gibbs and colleagues (2013)<ref name=":4" /> compiled available evidence and identified 9 studies investigation prevalence of 3/3, 2/3, and 1/3 of the triad conditions in exercising women. Of the 9 included studies,<ref name=":5" /><ref name=":0" /><ref name=":2" /><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. Journal of sports sciences. 2007 Oct 1;25(12):1289-97.
== Mechanisms ==
</ref><ref>Hoch AZ, Stavrakos JE, Schimke JE. Prevalence of female athlete triad characteristics in a club triathlon team. Archives of physical medicine and rehabilitation. 2007 May 1;88(5):681-2.</ref><ref>Pollock N, Grogan C, Perry M, Pedlar C, Cooke K, Morrissey D, Dimitriou L. Bone-mineral density and other features of the female athlete triad in elite endurance runners: a longitudinal and cross-sectional observational study. International journal of sport nutrition and exercise metabolism. 2010 Oct 1;20(5):418-26.</ref><ref>Schtscherbyna A, Soares EA, de Oliveira FP, Ribeiro BG. Female athlete triad in elite swimmers of the city of Rio de Janeiro, Brazil. Nutrition. 2009 Jun 1;25(6):634-9.</ref><ref name=":3" /><ref>Vardar SA, Vardar E, Altun GD, Kurt C, Öztürk L. Prevalence of the female athlete triad in Edirne, Turkey. Journal of sports science & medicine. 2005 Dec;4(4):550.</ref> they found a prevalence of 0-15.9% for 3/3 conditions.<ref name=":4" /> When it came to determining the prevalence of the combination of any 2 components they found the following:
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:  
# Menstrual dysfunction (MD) and low bone mineral density (BMD) had a prevalence of 0-7.5%
# MD and disordered eating (DE) had a prevalence of 2.7-50%
# Low BMD and DE had a prevalence of 0.9 -3.2%
# MD and low energy availability (EA) had a prevalence of 17.5%, and
# Low BMD and low EA had a prevalence of 3.75%.<ref name=":4" />
To investigate the prevalence of individual components of the triad in exercising women, Gibbs and colleagues (2013)<ref name=":4" />  found that the prevalence ranged from 0-56% for primary amenorrhea, 1-60% for secondary amenorrhea, 0.9%-52.5% for oligomenorrhea, 7.1-89.2% for clinical and subclinical disordered eating, and 0-39.8% for low BMD (defined by z-score between -1.0 and -2.0).<ref name=":4" /> 


Gibbs and colleagues (2013)<ref name=":4" /> also found literature that concluded an increased prevalence of the triad components in lean sport athletes.<ref name=":3" /><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>Byrne S, McLean N. Elite athletes: effects of the pressure to be thin. Journal of science and medicine in sport. 2002 Jun 1;5(2):80-94.</ref><ref>Nichols JF, Rauh MJ, Barrack MT, Barkai HS, Pernick Y. Disordered eating and menstrual irregularity in high school athletes in lean-build and nonlean-build sports. International journal of sport nutrition and exercise metabolism. 2007 Aug 1;17(4):364-77.</ref><ref>Reinking MF, Alexander LE. Prevalence of disordered-eating behaviors in undergraduate female collegiate athletes and nonathletes. Journal of athletic training. 2005 Jan;40(1):47.</ref><ref>Rosendahl J, Bormann B, Aschenbrenner K, Aschenbrenner F, Strauss B. Dieting and disordered eating in German high school athletes and non‐athletes. Scandinavian journal of medicine & science in sports. 2009 Oct;19(5):731-9.</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>Torstveit MK, Rosenvinge JH, Sundgot‐Borgen J. Prevalence of eating disorders and the predictive power of risk models in female elite athletes: a controlled study. Scandinavian journal of medicine & science in sports. 2008 Feb;18(1):108-18.</ref><ref>Torstveit MK, Sundgot-Borgen J. The female athlete triad: are elite athletes at increased risk?. Medicine & Science in Sports & Exercise. 2005 Feb 1;37(2):184-93.</ref> Lean sports are ones that emphasize endurance, aesthetic/physique, and/or antigravitation; non-lean sports are ones that are more technical, power-focused, and/or ball-related.<ref name=":3" /> Torstveit and Sundgot-Borgen (2005)<ref name=":3" /> found that the prevalence of DE and MD in lean sport athletes was nearly 2 times more likely than in non-lean sport athletes. This supports the notion that DE can lead to MD, which then leads to decreased BMD.<ref name=":4" />
'''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>  
== Mechanisms    ==
* 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>
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.
'''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.  
=== '''Low Energy Availability With or Without an Eating Disorder''' ===
# Secondary amenorrhea: menstruation ceases for three months or longer in a woman who has previously had normal menstruation. An integral part of anorexia nervosa.  
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" /><ref name=":6" /><ref name=":7" /><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 disorder including [[Anorexia Nervosa]], [[Bulimia Nervosa]], Binge Eating Disorder, or Other Specified or Unspecified Feeding or Eating Disorders.<ref>American Psychiatric Association. Diagnostic and statistical manual of mental disorders (DSM-5®). American Psychiatric Pub; 2013 May 22.</ref> 
# 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>
Low EA can lead to menstrual dysfunction and low BMD. 
 
EA = dietary energy intake (calories in) – energy expended during exercise (calories out) 
 
=== '''Menstrual Dysfunction''' ===
As shown in the female athlete triad spectrum, menstrual function will range from eumenorrhea to functional hypothalamic amenorrhea. Where eumenorrhea is a menstrual cycle occurring after 28 +/- 7 days and amenorrhea is the absence of a menstrual cycle for more than 90 days.<ref name=":1" /> Amenorrhea can be primary, meaning there is a delay in age of the first occurrence of menstruation (15 years or older or within 5 years of breast tissue development), or secondary, meaning it occurs after the individual has begun menstruation.<ref name=":1" /> Oligomenorrhea is an irregularity somewhere in between the two extremes on the spectrum; it is defined as intervals of more than 35 days between menstrual cycles.<ref name=":1" />
 
Functional hypothalamic amenorrhea (FHA), which is most relevant in the Triad, can be a primary or secondary amenorrhea caused by low EA and it is classified into the following 3 categories: weight loss-related, stress-related, and exercise-related amenorrhea.<ref>Meczekalski B, Katulski K, Czyzyk A, Podfigurna-Stopa A, Maciejewska-Jeske M. Functional hypothalamic amenorrhea and its influence on women’s health. Journal of endocrinological investigation. 2014 Nov 1;37(11):1049-56.</ref> FHA affects gonadotropin-releasing hormone<ref name=":8">Gordon CM. Functional hypothalamic amenorrhea. New England Journal of Medicine. 2010 Jul 22;363(4):365-71.</ref> and luteinizing hormone,<ref>Meczekalski B, Podfigurna-Stopa A, Warenik-Szymankiewicz A, Genazzani AR. Functional hypothalamic amenorrhea: current view on neuroendocrine aberrations. Gynecological Endocrinology. 2008 Jan 1;24(1):4-11.</ref> which leads to estrogen deficiency. The low EA, resulting in hypoestrogenism and other metabolic disturbances, can cause anovulation and infertility,<ref>Hind K. Recovery of bone mineral density and fertility in a former amenorrheic athlete. Journal of sports science & medicine. 2008 Sep;7(3):415.</ref> miscarriage or preterm birth,<ref>Easter A, Treasure J, Micali N. Fertility and prenatal attitudes towards pregnancy in women with eating disorders: results from the Avon Longitudinal Study of Parents and Children. BJOG: An International Journal of Obstetrics & Gynaecology. 2011 Nov;118(12):1491-8.</ref> low BMD and fractures,<ref>Lambrinoudaki I, Papadimitriou D. Pathophysiology of bone loss in the female athlete. Annals of the New York Academy of Sciences. 2010 Sep;1205(1):45-50.</ref><ref>Misra M. What is the best strategy to combat low bone mineral density in functional hypothalamic amenorrhea?. Nature Clinical Practice Endocrinology & Metabolism. 2008 Oct;4(10):542-3.</ref> coronary artery disease,<ref>Friday KE, Drinkwater BL, Bruemmer B, CHESNUT 3rd C, Chait A. Elevated plasma low-density lipoprotein and high-density lipoprotein cholesterol levels in amenorrheic athletes: effects of endogenous hormone status and nutrient intake. The Journal of Clinical Endocrinology & Metabolism. 1993 Dec 1;77(6):1605-9.</ref><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> diabetes mellitus, 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>
 
=== '''Low Bone Mineral Density''' ===
Low BMD is classified as a z-score between -1.0 and -2.0 and osteoporosis is classified as a z-score of less than or equal to -2.0 along with the presence of a secondary risk factor such as low EA, hypoestrogenism, or a previous history of fractures.<ref name=":1" /> Athletes engaging in weight-bearing sports have been shown to have a BMD that is 5-15% higher than those who are not engaging in any sports at all.<ref>Fehling PC, Alekel L, Clasey J, Rector A, Stillman RJ. A comparison of bone mineral densities among female athletes in impact loading and active loading sports. Bone. 1995 Sep 1;17(3):205-10.</ref><ref>Risser WL, Lee EJ, LeBlanc AD, Poindexter HB, Risser JM, Schneider VI. Bone density in eumenorrheic female college athletes. Medicine and science in sports and exercise. 1990 Oct;22(5):570-4. </ref><ref>NICHOLS, D. L., and C. F. SANBORN. Female Athlete and Bone. In: Nutrition for Sport and Exercise, J. R. Berning and S. N. Steen. Gaithersburg, Md.: Aspen Publishers, pp. 205–215, 1998.</ref><ref>Robinson TL, Snow‐Harter C, Taaffe DR, Gillis D, Shaw J, Marcus R. Gymnasts exhibit higher bone mass than runners despite similar prevalence of amenorrhea and oligomenorrhea. Journal of Bone and Mineral Research. 1995 Jan;10(1):26-35.</ref> Furthermore, a z-score of -1.0 or less in athletes should lead to more tests regardless of what secondary risk factors are present at the time.<ref name=":1" /> Approximately half of an individual’s peak bone mass (PBM) is formed during puberty<ref>Juul A, Hagen CP, Aksglaede L, Sørensen K, Mouritsen A, Frederiksen H, Main KM, Mogensen SS, Pedersen AT. Endocrine evaluation of reproductive function in girls during infancy, childhood and adolescence. InPediatric and Adolescent Gynecology 2012 (Vol. 22, pp. 24-39). Karger Publishers.</ref> and, additionally, hormones and nutrition are thought to contribute 40-60%.<ref name=":8" /> Low EA plays a big role in BMD—as evidenced by a randomized controlled trial that found bone formation in exercising women declined shortly after EA was reduced to less than 30kcal/kg.<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> A low EA can lead to estrogen deficiency, which plays a key role in bone formation. A loss in BMD may be irreversible so it is important to identify it as early as possible to minimize the risks of stress fractures and [[osteoporosis]].


== Manifestations (including systemic involvement)  ==
== Manifestations (including systemic involvement)  ==
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*Absent or irregular menstrual cycles (includes primary and secondary amenorrhea, as well as oligomenorrhea)  
*Absent or irregular menstrual cycles (includes primary and secondary amenorrhea, as well as oligomenorrhea)  
*Chronic fatigue  
*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>    
*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  
*Compulsive exercise  
*Increased infections and illnesses<ref name=":1" />  
*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>  
*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" /><ref name=":19" />  
*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>
*Depression<ref name=":9" /><ref name=":20" />
*[[Nutrition|Nutrient]] deficits
*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>
*Esophagitis and oesophageal perforation if self-induced vomiting<ref name=":12" />
*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>
*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" /><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>
*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 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 endothelial dysfunction<ref name=":16" />  
*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>  
*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>
*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>
*Impaired athletic performance  
*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>
*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 and Risk Factor Stratification ==
== Screening ==
Screening for female athlete triad should occur for all female high school and college athletes<ref name=":10" /> as part of the [[Pre-participation Screening|Pre-Participation Physical Evaluation (PPE),]]<ref>Rumball JS, Lebrun CM. Preparticipation physical examination: selected issues for the female athlete. Clinical Journal of Sport Medicine. 2004 May 1;14(3):153-60.</ref><ref>Rumball JS, Lebrun CM. Use of the preparticipation physical examination form to screen for the female athlete triad in Canadian interuniversity sport universities. Clinical Journal of Sport Medicine. 2005 Sep 1;15(5):320-5.</ref><ref>Ljungqvist A, Jenoure P, Engebretsen L, Alonso JM, Bahr R, Clough A, De Bondt G, Dvorak J, Maloley R, Matheson G, Meeuwisse W. The International Olympic Committee (IOC) Consensus Statement on periodic health evaluation of elite athletes March 2009. British journal of sports medicine. 2009 Sep 1;43(9):631-43.</ref> at annual check-ups,<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>Nattiv A, Agostini R, Drinkwater B, Yeager KK. The female athlete triad. The inter-relatedness of disordered eating, amenorrhea, and osteoporosis. Clinics in sports medicine. 1994 Apr;13(2):405-18.</ref><ref>Otis CL. American College of Sports Medicine position stand. The Female Athlete Triad. Med. Sci. Sports Exerc.. 1997;29(5):1669-71.</ref>  as well as during evaluation for the signs and symptoms related to the triad (e.g., stress fractures, menstrual dysfunction).<ref name=":1" /> Physiotherapists are often the first clinical encounter for many athletes. Physiotherapists have the ability to refer their patients onwards to undergo further investigations, which may require some advocating. Furthermore, having knowledge of the triad and the ability to screen for it is compulsory in primary and secondary prevention. Screening questions can be incorporated into the subjective portion of physiotherapy assessments and treatments.<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>   
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:    
 
Despite a number of validated tools that detect disordered eating, a tool does not currently exist which detects low energy availability (EA). Considering that evidence supports the role low EA plays in menstrual dysfunction and poor bone health, a screening tool to identify the triad in its earlier stages would help to minimize the risk of long-term consequences. An observational study by Melin and colleagues (2014)<ref name=":11">Melin A, Tornberg ÅB, Skouby S, Faber J, Ritz C, Sjödin A, Sundgot-Borgen J. The LEAF questionnaire: a screening tool for the identification of female athletes at risk for the female athlete triad. Br J Sports Med. 2014 Apr 1;48(7):540-5.</ref> tested a questionnaire’s ability to detect athletes at risk of developing the female athlete triad. These researchers created the LEAF-Q; a 25-item, self-report questionnaire with a sensitivity of 78% and a specificity of 90% for detecting low EA, menstrual dysfunction, and poor bone health.<ref name=":11" /> Unfortunately, this tool does not seem to be readily accessible online. 
 
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),<ref name=":10" /> identified the following 9 questions that adolescent females should be asked as part of the PPE to screen for the Triad:<ref name=":10" />    
* "Have you ever had a menstrual period?"
* "Have you ever had a menstrual period?"
* "How old were you when you had your first menstrual period?"
* "How old were you when you had your first menstrual period?"
Line 85: Line 72:
* "Have you ever had an eating disorder?"
* "Have you ever had an eating disorder?"
* "Have you ever had a stress fracture?"
* "Have you ever had a stress fracture?"
* "Have you ever been told you have low bone density ([[Osteopenia]] or [[Osteoporosis]])?"
* "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>
The De Souza and colleagues (2014)<ref name=":10" /> also created a Cumulative Risk Assessment that classifies athletes into high risk, moderate risk, or low-risk groups, which directly correlate with how much sport activity they should participate in. To find out the Cumulative Risk Score, risk factors are added together. Full clearance for participation requires 0-1 points, provisional/limited clearance requires 2-5 points, and restricted from training and competition requires 6 or more points.<ref name=":10" /> [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 the Cumulative Risk Assessment.]    
== Management  ==


Around the same time, the International Olympic Committee (IOC) Consensus group<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> created an updated term for the triad, called the Relatively Energy Deficiency in Sport (RED-S). Mountjoy and colleagues (2014)<ref name=":12" /> believe RED-S is more suitable because it is not actually a triad, but a syndrome associated with numerous physiological impairments that affect health and performance. The RED-S Clinical Assessment tool can be readily accessed at the following link: [https://bjsm.bmj.com/content/bjsports/49/7/421.full.pdf RED-S Clinical Assessment Tool for the Evaluation of Athletes]. With the tool, athletes can be classified into high risk, moderate risk, or low-risk groups, which also correlate with how much sport activity they should participate in. Additionally, the RED-S risk assessment<ref name=":12" /> also has a stepwise approach for determining an athlete’s readiness to return-to-play. 
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" />


Koltun and colleagues (2019)<ref name=":13">Koltun KJ, Strock NC, Southmayd EA, Oneglia AP, Williams NI, De Souza MJ. Comparison of Female Athlete Triad Coalition and RED-S risk assessment tools. Journal of sports sciences. 2019 Nov 2;37(21):2433-42.</ref> compared the Triad Coalition<ref name=":10" /> and RED-S<ref name=":12" /> tools and how they classified an athlete’s level of risk and recommendation for return-to-play using the same 166 individuals. Using the Triad Coalition tool, 25.3% of subjects were fully cleared, 62.0% were provisionally cleared, and 12.7% were restricted.<ref name=":13" /> In comparison, using the RED-S tool, 71.7% were fully cleared, 18.7% were provisionally cleared, and 9.6% were restricted.<ref name=":13" /> Furthermore, both of the tools differ quite significantly in that the Triad Coalition tool was more conservative and the RED-S tool was more liberal.<ref name=":13" /> Koltun and colleagues (2019)<ref name=":13" /> conclude that this should not be concerning since the main differences seem to be in deciding whether an athlete should return-to-play fully or provisionally. 
'''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" />


Holtzman and colleagues (2019)<ref name=":14">Holtzman B, Tenforde AS, Parziale AL, Ackerman KE. Characterization of Risk Quantification Differences Using Female Athlete Triad Cumulative Risk Assessment and Relative Energy Deficiency in Sport Clinical Assessment Tool. International journal of sport nutrition and exercise metabolism. 2019 Nov 1;29(6):569-75.</ref> performed another study comparing the 2 tools. The study involved 1000 athletes. The researchers found, using the Triad Coalition tool, 54.7% were moderate and 7.9% were high risk and, using the RED-S tool, 63.2% were moderate and 33% were high.<ref name=":14" /> Holtzman and colleagues (2019)<ref name=":14" /> conclude that the tools agree upon which athletes are at some level of risk, but not necessarily the exact level. 
'''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" />


De Souza and colleagues (2020)<ref name=":15">De Souza MJ, Williams NI, Koltun KJ, Strock NC. Female Athlete Triad Coalition risk assessment tool is an evidenced-based tool that is reliable and well-described. Journal of Sports Sciences. 2020 May 2;38(9):996-9.</ref> addressed the differences in results found by Koltun and colleagues (2019)<ref name=":13" /> and Holtzman and colleagues (2019).<ref name=":14" /> De Souza and colleagues (2020)<ref name=":15" /> attributed them to the variability between the users, which stemmed from the lack of “explicit, well-defined risk factors and scoring instructions”<ref name=":15" /> for the RED-S tool. De Souza and colleagues (2020)<ref name=":15" /> recommend that the RED-S team implement revisions. However, they also noted that some limitations exist with the Triad Coalition tool, despite it having a more clearly defined scoring system for risk stratification.<ref name=":15" /> For example, The Triad Coalition tool requires access to dual-energy X-ray absorptiometry and presents difficulty identifying low energy availability.<ref name=":15" /> In a recent article, Koltun and colleagues (2020)<ref>Koltun KJ, Williams NI, De Souza MJ. Female Athlete Triad Coalition Cumulative Risk Assessment Tool: Proposed alternative scoring strategies. Applied Physiology, Nutrition, and Metabolism. 2020 Jun 5(ja).</ref> proposed ways to address the limitations with the Triad Coalition tool,<ref name=":10" /> which included, amongst other things, substituting a delayed menarche for low bone mineral density (BMD) and incorporating self-report questionnaires for low energy availability.   
== Investigations  ==
If there is suspicion that the athlete may have 1 of the triad components, investigations should be performed by the appropriate members of the multidisciplinary healthcare team.<ref name=":1" /><ref name=":10" /> A healthcare provider should measure height, weight, and vital signs,<ref name=":22">BECKER, A. E., S. K. GRINSPOON, A. KLIBANSKI, and D. B. HERZOG. Eating disorders. N. Engl. J. Med. 340:1092–1098, 1999.</ref><ref>Rome ES, Ammerman S, Rosen DS, Keller RJ, Lock J, Mammel KA, O’Toole J, Rees JM, Sanders MJ, Sawyer SM, Schneider M. Children and adolescents with eating disorders: the state of the art. Pediatrics. 2003 Jan 1;111(1):e98-108.</ref> as well as check for poorly circulated hands and feet, lanugo hair, and enlargement of the parotid gland.<ref name=":22" />
Athletes with disordered eating or low energy availability may undergo the following laboratory tests:<ref name=":22" /><ref>American Academy of Pediatrics. Identifying and treating eating disorders. Pediatrics. 2003 Jan;111(1):204.</ref><ref name=":23">Practice Committee of the American Society for Reproductive Medicine. Current evaluation of amenorrhea. Fertility and sterility. 2004 Sep 1;82:33-9.</ref><ref>Practice Committee of the American Society for Reproductive Medicine. Current evaluation of amenorrhea. Fertility and sterility. 2006 Nov 1;86(5):S148-55.</ref> 
* Electrolytes
* Chemistry profile
* Complete blood count
* Erythrocyte sedimentation rate
* Thyroid function tests
* Urinalysis
Dietary logs (3-day, 4-day, 7-day, 24-hour dietary recall or food-frequency questionnaires)<ref>Heaney S, O’Connor H, Gifford J, Naughton G. Comparison of strategies for assessing nutritional adequacy in elite female athletes’ dietary intake. International journal of sport nutrition and exercise metabolism. 2010 Jun 1;20(3):245-56.</ref> should also be used by dietitian's to gauge an athlete's dietary energy intake.
Energy expenditure can be measured with heart rate monitors and accelerometers.<ref>Loucks AB. Low energy availability in the marathon and other endurance sports. Sports Medicine. 2007 Apr 1;37(4-5):348-52.</ref> Self-report can also be used and the [https://www.researchgate.net/publication/51226666_2011_Compendium_of_Physical_Activities_A_Second_Update_of_Codes_and_MET_Values 2011 Compendium of Physical Activities] can be used to carry out the calculation (exercise expenditure in kcal= metabolic equivalents of task x weight in kilograms x duration of activity in hours).<ref>Ainsworth BE, Haskell WL, Herrmann SD, Meckes N, Bassett Jr DR, Tudor-Locke C, Greer JL, Vezina J, Whitt-Glover MC, Leon AS. 2011 Compendium of Physical Activities: a second update of codes and MET values. Medicine & science in sports & exercise. 2011 Aug 1;43(8):1575-81.</ref>
A diagnosis of functional hypothalamic amenorrhea is made by excluding other causes of amenorrhea (those that are not weight loss-related, stress-related, or exercise-related amenorrhea).<ref name=":23" /><ref>Hall JE, Nieman LK, editors. Handbook of diagnostic endocrinology. Springer Science & Business Media; 2003 Jan 22.</ref><ref>Speroff L, Fritz MA, editors. Clinical gynecologic endocrinology and infertility. lippincott Williams & wilkins; 2005.</ref><ref>Warren MP, Hagey AR. The genetics, diagnosis and treatment of amenorrhea. Minerva ginecologica. 2004 Oct;56(5):437-55.</ref> This may involve a pregnancy test and other tests to rule out endocrinopathies.
De Souza and colleagues (2014)<ref name=":10" /> recommend dual-energy x-ray absorptiometry (DXA) to assess an athlete's BMD if they meet the following criteria:
* ≥1 high risk factors: 1) history of diagnosed eating disorder, 2) body mass index (BMI) ≤17.5kg/m^2, <85% of estimated weight, or ≥10% weight loss in 1 month, 3) menarche ≥16 years of age, 4) history of <6 menses over 12 months, 5) 2 previous stress fractures or non-traumatic fracture, 6) z-score of <-2.0 measured at least 1 year ago
* ≥2 moderate risk factors: 1) history of disordered eating for ≥6 months, 2) BMI of 17.5-18.5, <90% of estimated weight, or 5-10% weight loss in 1 month, 3) menarche between 15 and 16 years of age, 4) history of 6-8 menses over 12 months, 5) history of 1 fracture without significant trauma, 6) z-score between -1.0 and -2.0 measured at least 1 year ago
* Athletes using medications for ≥6 months that may have negative effects on bone health should also be considered for DXA.
Repeat DXA investigations depend on the athlete's status.<ref name=":10" /> It is recommend that an athlete undergoes DXA again 1-2 years after the initial one.<ref name=":10" />
== 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" /> 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" />
=== Pharmacological interventions ===
Pharmacological interventions may include oral contraceptives, gonadal steroids (estrogen, progesterone, and testosterone), other bone restorative medications, recombinant parathyroid hormone, antidepressants. However, as previously mentioned, pharmacological interventions should not be a first-line therapy. There is a lack of evidence to support them.<ref name=":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" /><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" /> 
== Role for Physical Therapy in Management  ==
== Role for Physical Therapy in Management  ==


Line 134: Line 87:
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. 
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. 


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, JACOBS 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.] 
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.] 


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.]<br>
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.]
== More Resources    ==


Female Athlete Triad Coalition - http://www.femaleathletetriad.org/
== Prevention ==
Preventing the triad requires proper education. Coaches, athletic trainers, parents and athletes need to be informed about the female athlete triad.


APTA - http://www.moveforwardpt.com/symptomsconditionsdetail.aspx?cid=0ca4bf2e-6d14-4b90-b1ec-ed8ebe13069e
* 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" />


NCAA -&nbsp;http://www.ncaa.org/health-and-safety/sport-science-institute/female-athlete-body-project
== More Resources    ==


{{#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  ==
<references />  
<references />  
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[[Category:Pelvis - Conditions]]  
[[Category:Pelvis - Conditions]]  
[[Category:Conditions]]
[[Category:Conditions]]
[[Category:One Page Project]]

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, Nicole Hills, Elaine Lonnemann, Oyemi Sillo, WikiSysop, Adam Vallely Farrell, 127.0.0.1, Claire Knott and Rishika Babburu  

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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