1. The Female Athlete Triad
Britt Marcussen, MD, CAQ Sports Medicine
Fellowship Director Primary Care Sports Medicine

2. Disclosers
none

3. Thank You
To Elizabeth Joy, MD Intermountain Health

4. Goals
Define and describe the Female Athlete Triad-Relative Energy Deficiency in Sports.
Go over the data for why it’s bad for you.
Describe screening, evaluation and treatment for athletes affected by the Triad
Review current recommendations for restriction and return to sports

5. Let’s Keep our Eye on the Ball

6. Activity Level of American Girls
■ All     ■ Boys     ■ Girls
Troiano RP. MSSE 2008
Only 42 % of elementary school age children in the US achieve 60 min of PA a day and that number drops by a factor of 5 as children enter middle school and high school. This fall off is even more substantial amongst females. With only % % meeting recommended levels of activity at age 16

7. Disordered eating Amenorrhea Osteoporosis Definition Defined 1992
3 inter-related entities
Disordered eating
Amenorrhea
Osteoporosis
Greatest risk in young female athletes in lean physique and endurance sports
45% of female swimmers view revealing suits as a stressor (Sundgot-Borgen and Torstviet, 2005)

8. But…there is a lot more to it!
2007 update (MSSE 2007)
Spectrum of symptoms & conditions between health & disease
Identifies low energy availability
Can and often does occur unintentionally
Can include disordered eating/eating disorders

9. Low Energy Availability
The Continuum
Optimal Energy
Availability
Optimal
Bone Health
Eumenorrhea
Functional
Hypothalamic
Amenorrhea
Osteoporosis
Low Energy Availability
with or without an
Eating Disorder

10. Prevalence in College Athletes
425 female college athletes, 7 Universities
3.3 % reported a diagnosis of anorexia nervosa
2.3 % reported a diagnosis of bulimia nervosa
15.2 – 32.4 % scored “at-risk” for EDO
31 % reported menstrual irregularity
34.3 % reported bone injuries during collegiate career
(Beals and Manore Int Sp Nutr, 2002)

11. Prevalence in HS (Arch Pediatr Adolesc Med. 2006 Feb;160(2):137-42)
18.2, 23.5 and 21.8% met criteria for DE, menstrual irregularity and low bone mass (dxa)
20% met one triad component, 5.9 % had two of the components of the triad and 1.2% had all three.
There are about 3.2 million girls in HS sports…so that’s a lot of girls!
170 Calf HS athletes across 8 sports

12. More HS Data Rauh et al. Abstract ACSM 2011 38 HS CC runners
35 had EDE-Q scores < 3 (normal eating behavior)
Food Diary and looked at leptin/estradiol/IGF-1/T3/BAP/CTX/Ht/Weight/DXA for bone and body mass data
Of the 35 with normal eating behavior
48% had evidence of menstrual dysfunction
25% had low BMD
37% had abnormal bone turnover makers

13. 2013 meta-analysis in Medicine & Science in Sports & Exercise
Analyzed rates of Triad components
65 studies from 12 countries (39 from U.S.)
60 studies on competitive athletes (vs. recreational)
3 components: 0-16%
2 components: %
1 component: 16-60%
LS athletes had higher prevalence than NLS

14. In the Recreational Females
De Souza et al. Human Reprod 2010
50% of a group of 67 exercising women were found to have evidence of subclinical menstrual dysfunction such and anovulation and luteal phase disorders.
33% had frank amenorrhea.
Mean age of 26, BMI 22, Exercise hours=7.6

15. Non Sanctioned Sports are also at risk!
Lifetime prevalence of any eating disorder (ED) was 50% in professional dancers
Point prevalence of ED ranged 13.6% % in young student dancers.
Prevalence of menstrual disturbance varied
10.2% for secondary amenorrhea
70% for lifetime history of menstrual disturbance
32% of university-level dancers developed a menstrual disturbance during their freshman year.
Prevalence of low bone mineral density
10% % for low bone mineral density/osteopenia
8.9% % for osteoporosis
Hincapie. Arch Phys Med Rehab 2010

16. Negative Energy Balance
-Overtraining
-Restricting
-Poor Nutrition
-Reduced injury Risk
-Peak Performance
Healthy Balance
Intake=Output
Unhealthy Balance
-Poor Performance
Intake>Output

17. Low Energy Availability
Hoch, Papanek et al. Clin J Sports Medicine 2011
22 Professional Ballet Dancers
77% Had a negative energy balance
32% Had DE
3 day food diary with energy expenditure determined by accelerometer

18. Genetics 156 158 153 BMI 18.5 Regular periods
Retired after completed femoral neck stress fracture and AVN of the femoral head
158
BMI 20
3 periods
2 stress fractures, missed most of two seasons
153
BMI 17
No stress fractures

19. Exercise Energy Expenditure
EEE = MET X Wgt (kg) X Duration (hours)
60 kg Female soccer player
2 hours of soccer practice
30 minutes of running at 10 min miles
Running = 10 MET Soccer = 10 MET
10 X 60 X 2 = 1200 kcal
10 X 60 X .5 = 300 kcal
EEE = 1500 kcal

20. Exercise Energy Expenditure
Amount of dietary energy remaining for other body functions after exercise training
Dietary energy intake (EI) – exercise energy expenditure (EEE) normalized to fat-free mass (FFM)
EA = (EI – EEE)/FFM, kcal/kg FFM/day
Example:
Dietary energy intake of 2000 kcal/day
Exercise energy expenditure of 600 kcal/day
Fat-free mass of 51 kg EA = (2000 – 600)/51 = 27.5 kcal/kg FFM/day
Normal EA = > 30 kcal/kg FFM/day
Goal EA = 35 – 45 kcal/kg FFM/day

21. Nutritional and endocrine factors set the stage for low BMD
High Energy Expenditure
Low Energy Intake
FEMALE ATHLETE TRIAD
ANOREXIA NERVOSA
Physiological Adaptations to Conserve Fuel
Hormonal Abnormalities:
↓ Estrogen
Metabolic Abnormalities:
↓ Leptin ↑ Ghrelin
↓ T3 ↑ PYY
↓ Insulin ↑ Cortisol
↓ IGF ↑ GH
↑ Bone Resorption
Uncoupling of Bone Turnover
↓ Bone Formation
Thanks to Mary Jane De Souza for this slide
Thanks to Dr. MaryJane DeSouza at Penn State University for these slides. In the setting of the Female Athlete Triad, and conditions such as anorexia nervosa where these is low energy intake and often times high energy expenditure, physiological adaptations to conserve energy take place. A number of metabolic abnormalities take place including. Of course the ovaries decrease the production of estrogen, and the combination of these phenomena result in the both increased bone resoirption and decreased bone formation, which in turn leads to decreased bone strength and decreased bone mineral density
Nutritional and endocrine factors set the stage for low BMD
↓ Bone Strength

22. Bone Health and the Triad
Weight bearing exercise generally leads to stronger bones less prone to fracture and osteoporosis.
Low energy availability and menstrual dysfunction (low estrogen) can lead to low BMD.

23. Bone Health and the Triad
2 prospective studies (Goolsby et al. CJSM, and Barrow and Saga AJSM 1988) looked at college track and CC athletes. Both these studies and others that followed demonstrated that menstrual irregularly is an independent risk factor for stress fractures.

24. Low Energy Availability and Risk of Injury

25. It’s not just the bones!
2 recent studies of HS athletes demonstrated increased risk of all injuries not just stress fracture
Rauh et al. J Athletic Training 2010
163 female athletes across 8 sports
Low BMD/oligomenorrhea and amenorrhea were associated with an increased injury risk.
Thien-Nissenbaum et al. J Athletic Training 2012
249 female athletes' in multiple sports
50% reported there periods stopped during their training/competitive season
Those with menstrual irregularity had a significantly higher proportion of major injuries (missed more than 22 days) although the number of these types of injuries were small.
Trend: Those with menstrual irregularity were 3x more likely to an injury lasting more than 7 days.

26. The 4th Part of the Triad Endothelial Dysfunction
One of the sentinel/central issues in the pathogenesis of CVD
Multiple studies (Hoch et al MSSE CJSM 2011, Yoshida et al. Arthrosc Thomb Vasc Biol 2006) All showed significantly diminished flow mediated dilatation in amenorrheic athletes.

27. Screening for the Female Athlete Triad (www.femaleathletriad.com)
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 last 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)?
8 items on DE
3 on menstrual df
1 bone health
Reps from AMSSM/AOSM/AAP/Am diet ass/ACSM/IOC/NCAA/NATA

28. Other risk factors… (+) Family history of osteoporosis
(+) Family history of eating disorder
Vegetarianism (gateway to anorexia)
History of low calcium intake (lactose intolerance)
Low vitamin D level
Prior stress fracture(s)
Co-existing personality factors (perfectionism) and/or mental health disorders (e.g., anxiety, obsessive compulsive disorder)

29. Clinical Journal of Sports Med 2012
Review of PPE among 257 Div I universities
Only 9% included at least 9 of the 12 recommended items
44% included fewer than 4 items

30. Screening in Iowa

31. Screen to Diagnosis Almost Always involves a Multidisciplinary Team:
Physician
Track periods-May take a year or more for periods to return
Eval bone health-DXA
Monitor for serious complications and need for hospitalization
In athletes determine clearance for sport
Educate coaches/parents/teammates
Nutritionist/Dietition
Nutritional intake and analysis
Psychiatrist/Psychologist
Address phycology components related to food and body image

32. Limitations of DXA Limitations of DXA It is a 2D image of a 3D object
Smaller bones have lower BMD
Body fat matters-fat=higher BMD
The organic portion of the bone/matrix that contributes elastic properties to the bone is not taken into consideration

33. To Treat of Not Treat Menstrual Dysfunction?
Non-pharmacologic interventions are treatment of choice
Ensuring adequate energy intake
Optimizing stored energy
Goal being restoration of regular menstruation
Calories/Calcium/Vit D
Hormone replacement therapy
Topical estrogen + oral progesterone – preferred
Estradiol 1 mg patch + Medroxyprogesterone 10 mg PO qday X 10 days every 2-3 months
Consider Nuvaring in sexually active females with a desire for contraception
Avoid combined oral contraceptives (suppress IGF-1)

34. Does it Work to increase BMD Misra M. J Bone Miner Res
Does it Work to increase BMD Misra M. J Bone Miner Res Oct 20(10):
110 girls with anorexia nervosa
40 normal weight no ED controls
Physiologic doses of transdermal estrogen and oral progesterone
This study by Dr. Madhu Misra at Harvard, enrolled 110 girls with AN (along with 40 normal weight no ED controls) to examine the effect of physiologic doses of estrogen and progesterone on BMD. Followed fthem or 18 months. She found that physiological doses of estrogen and progesterone increased BMD in adolescent females with AN. In contrast those on placebo continued to lose BMD. She also observed NO DECREASE in IGF-1 in subjects on either transdermal estrogen or those taking low physiologic doses of estrogen.

35. Who should we consider treating?
Pharmacological therapy may be considered in an athlete with:
BMD Z-score < -2.0
Clinically significant fracture history
Lack of response to at least 1 year of non-pharmacological therapy
BMD Z-score between -1.0 and -2.0
> 2 additional Triad risk factors
Lack of response to 1 year of non-pharmacological therapy
Clinically Significant Fracture
1 high risk stress reaction/ fracture (femoral neck, sacrum, pelvis)
2 prior stress reactions/ fractures
1 low energy traumatic fracture

36. Guidelines for Clearance and RTP (2014 Consensus Statement, De Souza et al BJSM 2014)

38. Provisional clearance: Limited clearance
Clearance Defined
Provisional clearance:
Full training/competition based on the athlete’s compliance and follow through with a written contract 
Limited clearance
Limitations are specified with the athlete’s training and competition (specified in a written contract).
Restricted from training and competition
Clearance status can be revised/upgraded if the health care team determines the athlete can reach the stated health goals as outlined in the written contract.

40. Summary
The Female Athlete Triad and Low Energy Availability is common in female athletes.
Sports with high aesthetic aspects (gymnastics/dance/swimming) are particularly high risk.
Screening at the PPE is probably the best time to identify athletes at risk but the screening tools/forms are likely inadequate.
Absence of periods is NOT an adaptation to sports it is a marker of energy deficiency and risk for injury.
Treatment involves a multidisciplinary team of physicians/nutritions and mental health experts.
Non-pharmacologic treatment is the mainstay of any treatment program.
Clearance and RTP decisions are challenging. There are guidelines that can help risk stratify athletes (2014 Consensus Paper).