Triathlon

Athlete Triad: An Update

by Alex Coates on January 21, 2013
This article originally appeared on Alex's personal website.

This past week Kyla and I had to present a seminar on a topic of our choice for two 1 hour class sessions. The first day was meant to be basic lecture-style, and the second day was supposed to be more hands-on. We chose to do our seminar on an updated take of the Female Athlete Triad. The first day we explained the model that some people know (very few actually… out of the 4th+ year kinesiology students in our class, only three knew all three components of the model when we quizzed them at the beginning of our presentation), explained gaps and problems with old model, and what causes the triad. The second day we broke up into groups and worked on a hypothetical case study of an Olympic hopeful athlete with triad symptoms from either the perspective of a dietician, a coach, or a physiotherapist. I personally thought it was an awesome seminar :)

I thought I’d post a summary of what Kyla and I talked about on here, since it pertains to triathletes (Not Just Women!!!!)! It isn’t cited all the way through, as this is just what we talked about in class. The references are all at the bottom though, just in case. 
Female Athlete Triad
The Common Model

The common depiction of the female athlete triad is a triangle symbol of three entities: eating disorders/energy deficiency, menstrual disturbances/amenorrhea, and osteoporosis/bone loss. This model is meant to show the extremes of the condition, and it is supposed to be understood that an athlete can be anywhere on the spectrum for all three aspects.  The female athlete triad is most often seen in sports that emphasize leanness, be it in sports where skinnier is faster, for weight class sports, or for appearance-based sports such as in gymnastics and dance. Although disordered eating is very prevalent in sport compared to the general population, there are also many cases where the athletes are unintentionally calorie deficient simply because they are training so much. 

In the common model, low energy availability is generally considered the cause of this syndrome. Low energy, or not enough caloric intake to exceed the recovery demands of the sport, causes energy to go towards survival rather than growth and reproductive functions. The basic model states, not unfairly, but not comprehensively either, that the low energy causes a decrease in estrogen production which causes amenorrhea (not having a period). Not having a period essentially means the woman is infertile. This drop in estrogen also causes loss of bone mineral density because estrogen is needed to limit bone resorption, stimulate calcitonin and increase renal calcium retention. As most of you know, peak bone mass is laid down before a person is twenty, slightly later for boys, and there can be some increase up to 30 years old. After 6 months of amenorrhea, bone mass will have already dropped significantly, sometimes down to post-menopausal level, and is not often recoverable.

Kyla and I first became interested in the female athlete triad and its confusing nature a couple of years ago. We always had been told that only female athletes with very low body fat (below 20%, or 15%…) would develop amenorrhea. As you may know, Kyla and I train with the national triathlon centre. We realized over time that every single female we trained with had menstrual disturbances, usually amenorrhea, and even the girls with significant enough body fat, who you would assume had enough energy stores to offset this, also had amenorrhea.

This put into question the body fat hypothesis, as although we trained hard, not many of the girls fell into the sub 15% body fat range. Also the fact that every single girl had menstrual disturbances demonstrates the extensive nature of this problem.  We have wanted to do a project on this topic for a long time because of how incredibly prevalent it is within elite endurance sport such as triathlon, and because it seems as though most doctors, coaches, and kinesiologists don’t realize this.

Prevalence and Relevance

In one Australian study it was found that only 10% (n=180) of active Australian women could identify the three components of the triad. Only 45% knew that amenorrhea could affect bone mineral density, and 22% of the women who were in sports that emphasized leanness said they would do nothing if they had amenorrhea. This shows how little the public actually knows about this disorder.

Here are some more important statistics:
•       Reported disordered eating behaviour in 15-62% of college athletes, and amenorrhea in up to 69% of female athletes versus 2-5% of women in the general population (Hobart & Smucker, 2000) (Nazem & Ackerman, 2012)
•       Prevalence of osteopenia ranging from 22-50% in athletes vs. 12% in the general population.
•       Majority of bone mass is acquired between ages 11- 19, with some gain up to age 30, and weight bearing exercise does not always compensate for the effects of hormonal irregularities on the skeleton (Oleson, Busconi, & Baran, 2002)
•       Up to 70% of elite athletes in weight class sports (male and female) are dieting and have some type of disordered eating pattern (Nazem & Ackerman, 2012).
•       Osteoporosis occurs in up to 13% of athletes vs. 2.3% in the general population
•       Premature osteoporosis and osteopenia puts athletes at risk for stress fractures and more serious fractures in hips and vertebral column. Loss of bone density may be irreplaceable, especially after three years of amenorrhea (Hobart & Smucker, 2000) 
•       Once menses returns post amenorrhea, bone density may increase an average of 6% for the first 14 months, and then 3% following this until a plateau occurs, which is generally much lower than the norm – i.e.. Bone density is not recovered. (Hobart & Smucker, 2000)

Definitions
•       Osteoporosis: Bone Mineral Density more than 2.5 standard deviations below mean of young adults (Khan et al., 2002).
•       Osteopenia: BMD Between 1 and 2.5 standard deviations below mean of young adults (Khan et al., 2002).
•       Functional Hypothalamic Amenorrhea: amenorrhea resulting from changes in energy availability.
•       Oligomenorrhea: infrequent menses, longer cycle duration
•       Amenorrhea: Primary and Secondary
•       Primary: No menses by age 14 and no development of secondary sex characteristics or no menses by age 16 and otherwise normal development
•       Secondary: 3 month absence of menses in women with primary regular menses (Miller, Kukuljan, Turner, van der Plight, & Ducher, 2012).



Basic Model Treatments

The most current treatment options that doctors give to athletes who are suffering from female athlete triad syndrome are to:
1)    train less and eat more. Guess what happens if you tell an Olympic potential type-A girl to eat more and train less? You guessed it… Not much!
2)    The second step in the basic treatment is to put the girls on the birth control pill. This increases their estrogen, which increases their bone density and voila! Problem solved! Type A crazy girls like this solution. Take pills, problems go away right? There is actually very low evidence that estrogen-progesterone supplementation helps to increase bone mineral density (We will go further into this in a minute.)
3)    Finally, in the case of anorexia or other extreme cases of disordered eating there is recommended nutrition and psychological counseling, which is understandable and important.

Here is the last basic model treatment: Do nothing! Think about it – if a woman is training for the Olympics, and stops having her period, how do you think she feels about that? Happy! This is where the problems with the model begin, which is what we will look at next.

Gaps of the Basic Model

I’m going to start this slide off with a quote:

According to Title IX of the Educational Assistance Act, any college that accepts federal funding must provide equal opportunities for women and men to participate in athletic programs. Last year marked the 25th anniversary of the passage of Title IX legislation, which dramatically increased the number of women who participate in sports at all competitive levels. Increased participation in exercise can result in a myriad of proven short- and long-term benefits. However, potential adverse health consequences are associated specifically with the overzealous female athlete” (Hobart, & Smucker, 2000, italics mine).

How do you feel about that last sentence? Personally I feel as though this puts the onus on the athlete, making her out to be crazy for trying to be an elite athlete. This stigmatizes female athletes, and doesn’t recognize that men can have the same problems as females.

Therefore, the first obvious gap in the model is the lack of male presence. Basically there is a general sense that men don’t have to worry, and can train as much as they want. However, if you have been around endurance sport, you will know that although maybe not quite as common, men do get stress fractures quite frequently. We’ll talk more about that in a bit.

The second gap is the assumption that only people with very low body fat or eating disorders can have the athlete triad. This means that larger girls are being missed in the FAT diagnosis. An interesting study was done in 1999 on obese women who had surgical reductions of stomach volume so that they could no longer consume adequate amounts of energy. It showed that three months post surgery, although the women were still obese (BMI over 35), they had developed amenorrhea.

Another assumption that is made when one is learning about the Female Athlete Triad model is that amenorrhea is necessary for there to be a decrease in bone density. However, one study showed females with oligomenorrhea had a 1.5 times the stress fracture risk as their eumenorrheic counterparts, and another study showed that even in women with eumenorrhea there can be a drop in bone density with athletics.

Another gap is with estrogen supplementation. There is actually very little evidence that estrogen-progesterone supplementation, (the birth control pill), actually has an effect on bone mineral density. Some studies have showed it does nothing, whereas others show a slight slowing in bone mineral loss, but by no means a solution for the problem. There is also an increase in cortisol (which is catabolic) with estrogen supplementation, and so that could make the problem worse. On the flip side, with straight progesterone supplementation there can be decreases in bone density because of the estrogen inhibiting effects of progesterone.

Lack of awareness of other hormones and their relation to bone mineral density is also important. Progesterone is needed for decreasing bone resorption and increasing bone formation, and testosterone is needed for increasing bone size, which is why males generally have larger bone mass than females. It also isn’t mentioned that glucocorticoids released during periods of stress (or exercise) decrease bone mass over time and that a lack of protein in the diet also does this.

Finally as I mentioned in previous slides, there is a general apathy towards the Female Athlete Triad. Athletes take it as something that comes with being an athlete, and coaches don’t care so long as the athlete can do the work. When athletes get stress fractures, the protocol is to take 6 weeks off in the boot, up calcium intake, and get back atter. This is not a good solution to a problem that will have life-long effects if it is not addressed.

Male Athlete Triad

Cases of the Triad in male athletes rarely come to the attention of physicians because men do not perceive its reproductive effects. Its prevalence is also lower than in female athletes, because fewer male athletes practice diet and exercise regiments that severely reduce energy availability. In men, a low energy availability occurs most often in weight-class sports such as wrestling, in endurance sports such as long-distance running, and in soldiers during military training. In runners, most reproductive effects occur beyond a training volume threshold of 100 km ·week−1 (De Souza et al., 1994). When energy availability is severely reduced, alterations in metabolic hormones are similar to those seen in female athletes; testosterone is suppressed and sperm count, mobility, and morphology is reduced.

There has been very little research done on the effects of athlete triad on men. However, despite the weight bearing nature of most sports, bone loss does occur, especially in endurance sports like running.  Research points to low testosterone, low estradiol, and high glucocorticoids as the causes.

What’s Going On?

Chronic energy deficiency ( ie calories in < calories out. Not taking in enough calories to recover from training and not having an excess to go towards normal body functioning) causes a cascade of metabolic shifts that acts to conserve energy including a decrease in resting energy expenditure (decrease in TT3 to downgrade metabolism), resulting in weight stability and a reduced ability to lose weight. Your body essentially is adapting to the energy deficiency, and all possible energy is conserved. This is why you can be in a constant calorie deficit, but not be losing weight.

Functional hypothalamic amenorrhea occurs due to the low energy availability. Alterations in the appetite hormones, ghrelin and leptin, are thought to be involved. The ‘hunger hormone’ ghrelin is chronically elevated indicating an energy deficit, and leptin, ‘the satiety hormone’ is reduced. The chronically high ghrelin concentrations in turn disrupt the pulsatility of gonadotropin releasing hormone, which then disrupts luteinizing hormone (LH) secretion, causing disrupted ovarian function. LH pulsatility can be acutely affected by low energy availability. Women on five days below the threshold of energy availability (20 -30kcal/kg ffm) show disrupted LH pulsatility. The ovarian dysfunction that follows disrupted LH secretion includes amenorrhea and oligomenorrhrea, but also luteal deficiency (lack of progesterone in the luteal phase), and anovulation (no ovulation).  One study found that of female athletes who were eumenorrhreic, 78% actually had sub-clinical menstrual disorders 1/3 of the time.


When you are in a constant energy deficit, cortisol is released in order to mobilize fuel sources (increasing energy availability through gluconeogenesis, amino acid mobilization, protein catabolism, mobilization of free fatty acids from adipose tissue, while decreased insulin sensitivity). Stress (any form of stress, from lack of energy to training) also causes an increase in cortisol in order to mobilize fuel (ie. energy to run away from a threat) and decrease inflammation through suppression of the immune system. Chronic cortisol elevation has a catabolic effect on body tissues inhibiting growth, reproductive function and immune function. Considering the perpetual catabolic rather than anabolic state, a high level of injury in general is to be expected. The body can also become cortisol resistant (just like insulin resistance) which will lead to chronic inflammation.

The “Pregnenolone steal” is a recent scientific discovery which shows the hormone pathway of pregnenolone which gets shifted towards the creation of cortisol during times of stress rather than to the production of sex hormones such as testosterone and estradiol (causing the Athlete Triad). The low sex hormones are determining factors in the building of weak bones, DHEA is associated with ‘burnout syndromes’ and hypoestrogenism is also associated with endothelial dysfunction, which results in cardiovascular disease.

Using this information, we can see that the Athlete Triad could actually be considered a sextet, where decreases in exercise performance, decreases in bone mineral density, decreases in sex hormones/ reproductive factors, increases in cardiovascular risk factors, decreases in cognitive ability and decreases in immune function are all a part of the “Triad”. When the ‘classic features’ become obvious, you’ve already done a fair amount of damage. Symptoms that indicate you are headed down this path include impaired exercise performance, immune function, cognitive impairment (brain fog), and of course (for women) disrupted menses.


Energy Availability Hypothesis

The energy availability hypothesis is the most supported hypothesis towards the cause of the Athlete Triad. It was found that when energy availability is reduced below 30 kcal · kg FFM−1 · day−1 ,(FFM= fat free mass), the body suppresses reproductive function (Loucks & Thuma, 2003) and bone formation (Ihle & Loucks, 2004). Studies on monkeys and army rangers found that increasing exercise but maintaining diet (ie. hypocaloric) resulted in hormonal imbalances/ammenorhea, but when caloric intake was increased to > 35 kcal/kg ffm/day menses returned despite maintaining high exercise levels. The healthy zone is considered to be above 45 kcal/kg fat free mass/day.

Stress Hypothesis

In the recent athlete triad literature, there is a lot of bashing of the stress hypothesis. This is because studies have shown that luteinizing hormone pulsatility is affected by calorie restriction and intense exercise, but not intense exercise alone in human and in rat studies. They are suggesting that you can train as hard as you want so long as you eat enough, and you won’t suffer ill effects. However the main study on this had healthy sedentary (rested?) women perform 4 days of intense exercise only. This is not what I call chronic stress.

The type of stress I am talking about is YEARS of intense exercise, or allostatic load. Allostatic Load is defined as “the physiological consequences of chronic exposure to fluctuating or heightened neural or neuroendocrine response that results from repeated or chronic stress.”

Hans Seyle is the father of Stress, and found that the body has only one way of reacting to any type of stress (homework, training, emotional…). His three stages of stress are: alarm, resistance, and exhaustion. Short periods of stress followed by periods of rest cause adaptations to the stressor. Brain senses the stressor (exercise?), epinephrine is released from adrenal medulla, and pituitary releases adrenocorticotropic hormone (ACTH). Epinephrine acts on sympathetic muscle tissues making them more active (fight/flight), and acts on pituitary to release more ACTH. ACTH reaches the adrenal cortex and induces release of anti-inflammatory gluco-corticoids (Piotrowsky, 2010).

The stress hypothesis is linked to overtraining  (OTS is a maladapted response to exercise when excessive and not matched with appropriate rest) and it’s many effects. There are many different theories on the direct causes of overtraining syndrome, including low energy availability. One theory for the cause of OT is disruption to HPA or HPG axes as cortisol, adrenocorticotropic hormone, testosterone, estrogen and progesterone have all been shown to be disrupted in OT athletes.

Chronic stress produces maladaptive changes in the HPA system, which can cause a decrease in the testosterone/cortisol balance (Duke, 2008). Sustained elevations in HPA axis cause sustained elevations of catabolic glucocorticoids which promote immune suppression, visceral fat accumulation, insulin resistance, neuronal destruction, and reductions in growth + reproductive function (Peckett,Timmons, & Riddell, 2012).

So basically the stress hypothesis is that over time, an athlete who is perhaps overtraining or under-recovering, cannot cope or adapt to the stressors. This leads to overtraining or athlete triad syndrome. So yes this is a contentious issue, but I believe that based on the General Adaptation Syndrome model, and looking at overtraining models, the stress hypothesis is a valid cause for FAT or AT.

Challenges to getting healthy

There are many challenges to getting healthy for an athlete with the Athlete Triad. These can include distorted body image and a pressure (external or internal) to remain lean. There is also a theory about  “hunger-high” in which athletes are addicted to the energy derived from stress hormones during fasted/low energy states. This would make an athlete feel as though they had less energy when they are eating more, which would make a return to health more difficult. The slowed thyroid metabolism (caloric set-point) would likely initially cause an increase in calories to be stored as fat, until metabolism returns to normal and the body can begin to properly use the given nutrients. Finally, with an increase in fat free mass that would come from increase energy intake, the diet would have to remain at a higher calorie intake in order to meet the needs of the increased body mass.

Treatment/What to do?

The first step in Athlete triad is prevention. Recognizing that most elite endurance athletes, and athletes in sports that emphasize leanness, are at risk is very important. It is not just a syndrome experienced by women, but by men as well.  Prevention involves making sure that the athlete is meeting the energy (ie. Caloric) demands of the sport (over 45 kcal/kg ffm/day is generally recommended), is not being chronically over-trained, is managing their stress, is taking action to build bone mineral density (Calcium and vitamin D supplementation is the only supplement method that I found in the literature to have a significant effect), and is following a weights protocol (with actual weights!) to build bone mineral density. Knowledge and awareness are key.

Multi-dimensional approach:

Dieticians/Sports Nutritionists can work with athletes to raise their caloric set-points. Compliance to the program is very important, so the athlete needs to be fully aware and on-board with what is being asked of them. A strict daily energy intake vs. energy expenditure log should be used on a regular basis with all athletes.

Coaches can ensure that the athlete isn’t overtraining, and has proper recovery built into the program. Taking the athlete’s total life stress into account when designing training and recovery is important. Since training is the breakdown, and recovery is the build-up, not being able to recover properly (for many reasons: nutrition, sleep, stress…) leads to decreased performance and athlete triad symptoms. Resistance training should be an integral component to all programs. Heart rate variability or resting heart rate as well as other monitoring tools (mood scales etc.) can be used to assess training adaptation and recovery.

Physiotherapists can work with athletes on their biomechanics and functional strength to decrease occurrence of stress fractures due to imbalances. The physiotherapist is often the first to work with athletes suffering from stress fractures, and so knowledge of the athlete triad is very important so they can either help the athlete themselves, or refer the athlete to other specialists.

In the end, the athlete needs to be made aware of this very common problem that can have lasting negative effects, and needs to be able to take their health into their own hands. Proper information is the first step, followed by a plan that puts health as a priority. An unhealthy athlete will not succeed in the long run, so they may as well start trying to maintain health early, rather than wait until too late.

References

Anderson, D. D. (2008). Assessment and natraceutical management of  stress-induced adrenal dysfunction. Integrative Medecine, 7(5), 18-25.

Braam, L. A. J. L. M., Knapen, M. H. J., Guesens, P., Brouns, F., & Vermeer, C. (2003). Factors affecting bone loss in female endurance athletes: A two year follow up study. American Journal of Sports Medicine, 31(6), 889-895.

Cosh, S., Crabb, S., LeCouteur, A., & Kettler, L. (2012). Accountability, monitoring and surveillance: Body regulation in elite sport. J Health Psychology, 17(4), 610-622.

Dawson-Hughes, B., Dallal, G. E., Krall, E. A., Sadowski, L., Sahyoun, N., & Tannebaum, S. (1990). A controlled trial of the effect of calcium supplementation on bone density in postmenopausal women. The New England Journal of Medicine, 323,878-883.

De Souza, M. J., Hontscharuk, R., Olmsted, M., Kerr, G., Williams, N. (2007). Drive for thinness score is a proxy indicator of energy deficiency in exercising women. Appetite 48(3). 369-367.

De Souza, M. J., Leidy, H. J., O’Donnell, E., Lasley, B., & Williams, N. I. (2004). Fasting ghrelin levels in physically active women: relationship with menstrual disturbances and metabolic hormones. The Journal of Clinical Endocrinology & Metabolism 89(7), 3536-3542.
Di Carlo C., Palomba S., De Fazio M., Gianturco M., Armellino M., Nappi C. (1999). Hypogonadotropic hypogonadism in obese women after biliopancreatic diversion. Fertil Steril, 72(5),905-9.

Duke, J. W., Jr. (2008). Influence of exercise training on the free testosterone to cortisol ratio. The University of North Carolina at Chapel Hill). ProQuest Dissertations and Theses, , 91. Retrieved from http://search.proquest.com.ezproxy.library.uvic.ca/docview/89218524?accountid=14846. (89218524).

Female Athlete Triad Coalition. (2013). Female Athlete Triad Coalition: An International Consortium. Retrieved December 20, 2012 from http://www.femaleathletetriad.org

Fleck, S. J. (1983). Body composition of elite American athletes. The American Journal of Sports Medicine, 11(6), 398-403.

Golden, N. H., Lanzkowsky, L., Schenbendach, J., Palestro, C. J., Jacobson, M. S., & Shenker, I. R. (2002). The effect of estrogen-progestin treatment on bone mineral density in anorexia nervosa. Journal of Pediatric and Adolescent Gynecology, 15(3), 135-143.

Heyward, V. H. (2010). Advanced fitness assessment and exercise prescription (6thed). Burgess Publishing Company.

Hind, K. (2008). Recovery of bone mineral density and fertility in a former amenorrheic athlete. Journal of Sports Science and Medicine, 7, 415-419.

Hobart, J. A., & Smucker, D. R. (2000).  The female athlete triad. American Family Physician, 61(11), 3357-3364.

Je, S. H., Joo, N., Choi, B., Kim, K., Kim, B., Park, S., Cho, D., Kim, K., & Lee, D. (2011). Vitamin K supplement along with vitamin D and calcium reduced serum concentration of undercarboxylated osteocalcin while increasing bone mineral density in korean postmenopausal women over sixty-years old. Journal of Korean Medical Science, 26(8), 1093,1098.

Jeukendrup, A., & Gleeson, M. (2010). Sport nutrition: an introduction to energy production and performance (2nd ed.). Windsor: Human Kinetics.

Kahn, K. M., Liu-Ambrose, T., Sran, M. M., Ashe, M. C., Donaldson, M. G., & Wark, J. D. (2002). New criteria for female athlete triad syndrome? British Journal of Sports Medicine, 36, 10-13.

Knechtle, B., Wirth, A., & Rosemann, T. (2011). Is body fat a predictor variable for race performance in recreational female ironman triathletes? Medicina Sportiva, 15(1), 6-12.
Kreher, J. B., & Schwartz, J. B. (2012). Overtraining syndrome: A practical guide. Sports Health: A Multidisciplinary Approach, 4(2), 128-138.

Loucks, A. B., Verdun, M., & Heath, E. M. (1997). Low energy availability, not stress of exercise, alters LH pulsatility in exercising women. Journal of Applied Physiology, 84(1), 37-46.

Lloyd, T., Andon, M. B., Rollings, N., Martel, J. K., Landis, J. R., Demers, L. M., Eggli, D. F., Kieselhorst, K., & Kulin, H. E. (1993). Calcium supplementation and bone mineral density in adolescent girls. Journal of American Medical Association, 270(7), 841-844.

Manore, M. M.,  Kam, L. C., & Loucks, A. B. (2007). The female athlete triad: components, nutrition issues, and health consequences. Journal of Sports Sciences, 25(1), 61-71.

Miller, S. M., Kukuljan, S., Turner, A. I., van der Pligt, P., & Ducher, G. (2012). Energy deficiency, menstrual disturbances, and low bone mass: What do exercising Australian women know about the female athlete triad?. Int J Sport Nutr Exerc Metab, 22(2), 131-138.

Nazem, T.G., & Ackerman, K.E. (2012).  The female athlete triad. Sports  Health: A Multidisciplinary Approach, 4(4), 302-311. 


Oleson, C. V., Busconi, B.D., & Baran, D. T. (2002). Bone density in competitive figure skaters. Arch Phys Med Rehabil, 83, 122-128.


Pallett, G. K. (1994). Anaerobic threshold, maximal oxygen uptake and percent body fat as predictors of olympic distance triathlon performance. The University of Manitoba (Canada). ProQuest Dissertations and Theses, 109-109. Retrieved from http://search.proquest.com.ezproxy.library.uvic.ca/docview/304138379?accountid=14846. (304138379).

Pantano, K. J. (2009). Strategies used by physical therapists in the U.S. for treatment and prevention of the female athlete triad. Physical Therapy in Sport, 10, 3-11.

Peckett, A., Timmons, B. W., & Riddell, M. C. (2012). Interaction of exercise, stress, and inflammation on growth. Handbook of Growth and Growth Monitoring in Health and Disease, DOI 10.1007/978-1-4419-1795-9_145,

Peer, K. S. (2004). Bone health in athletes: Factors and future considerations. Orthopaedic Nursing, 23(3), 174-183.

Piotrowsky, N. A. (2010). General adaptation syndrome. Salem Health: Psychology and Mental Health, 2, 830-834.
Russell, M., Stark, J., Nayak, S., Miller, K. K., Herzog, D. B., Klibanski, A., Misra, M. (2009). Peptide YY in adolescent athletes with amenorrhea, eumenorrheic athletes and non-athletic controls. Bone 45(1), 104-109.

Scott, J. M. (2012). Male endurance athlete tetrad. The Ohio State University). ProQuest Dissertations and Theses, , 118. Retrieved from http://search.proquest.com.ezproxy.library.uvic.ca/docview/1114895475?accountid=14846. (1114895475

Sherman, R.T., and Thompson, R.A. (2006).  Practical use of the international Olympic committee medical commission position stand on the female athlete triad: A case example.  Int J of Eating Disorders, 39: 193-201.

Teegarden, D., & Weaver, C. M. (1994). Calcium supplementation increases bone density in adolescent girls. Nutrition Reviews, 52(5), 171-173.





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