1. Impact of Low Energy Availability on Endocrine Suppression Leading to Osteopenia/Osteoporosis in Young Athletes 
Michelle Barrack, PhD, RD, CSSD
Assistant Professor, Nutrition & Dietetics
California State University, Long Beach

2. Objectives
After this presentation, participants will be better able to:
Define energy availability (EA) and identify effects of low energy availability (LEA,≤30 kcal/kgFFM/day) on growth, gonadal, and metabolic hormone function
Outline athlete populations with an increased risk of developing LEA, amenorrhea, low bone mass, and bone stress injury
Discuss protocols for screening, prevention, and treatment for LEA and related health outcomes.

3. Adolescent Sports Participation
Approximately 8 million adolescents participate in high school sports
Many beneficial effects to health, wellbeing
National Federation of State HS Associations, HS Athletics Participation Survey Nattiv et al. Med Sci Sports Exerc. 2007

4. Adolescent Sports Participation
National Federation of State HS Associations, HS Athletics Participation Survey Nattiv et al. Med Sci Sports Exerc. 2007

5. Adolescent Sports Participation
National Federation of State HS Associations, HS Athletics Participation Survey Nattiv et al. Med Sci Sports Exerc. 2007

6. Lifetime BMD Accumulation
1.0
1.4
1.2
0.8
0.6
0.4
0.2
BMD (g/cm2)
Maximal accumulation
between yr
Age (y)
Heaney et al., (2000) Peak bone mass, 11(12):

7. Factors Affecting Bone Mass
Female Athlete Triad, ACSM Position Stand Slideshow

8. Adolescent Athlete: Nutrient Needs
Adolescent athletes represent a population with specialized nutrient needs
Satisfy requirements for growth & development AND the demands of competitive athletics
Optimal diet for a young developing athlete should provide nutrients to:
optimize sports performance, recovery
reduce injury risk
support health, growth, maturation
Bone Health

9. Nutrition for Bone Health
A variety of nutrients support bone development
Micronutrients
Calcium & Vitamin D
Magnesium, Vitamin C, Vitamin K, Iron, Zinc, Vitamin A
Macronutrient: Protein
Energy (Calories)

10. Nutrition for Bone Health
Energy (Calories)
Adequate energy availability needed to promote optimal hormone status and bone formation
Energy Availability = [Energy Intake - Exercise Energy Expenditure]
[Fat Free Mass]
Energy Intake
Exercise Energy Expenditure
Energy Availability
+/or =
Ihle and Loucks. J Bone Miner Res 2004;19:

11. Nutrition for Bone Health
Energy (Calories)
Adequate energy availability needed to promote optimal hormone status and bone formation
Energy Availability = [Energy Intake - Exercise Energy Expenditure]
[Fat Free Mass]
Balanced EA* = 45 kcals/kg FFM/day
Low EA* = < 30 kcals/kg FFM/day
*Needs may vary for adolescents and/or male athletes
Ihle and Loucks. J Bone Miner Res 2004;19:

12. Low Energy Availability
Occurs with or without an eating disorder when:
- intentional or inadvertent restriction of dietary intake
- energy expenditure is high and intake does not match expenditure
May be due to inadequate education regarding energy
requirements
Regardless of the cause, a cascade
of physiologic & neuroendocrine adaptations occur
Nattiv et al. Med Sci Sports Exerc. 2007 12

13. The Female Athlete Triad
Low Energy Availability
Functional Hypothalamic Amenorrhea
Low Bone Mass
Nattiv et al. Med Sci Sports Exerc. 2007 13

14. Leanness Sports & Female Triad
An elevated prevalence in athletes participating in “Leanness” sports
Characteristics of Leanness Sport:
Endurance sports emphasizing a low body weight
Sports requiring revealing uniforms
Sports that use weight categories
Sport emphasizing pre-pubertal body for performance
(Nattiv et al. Med Sci Sports Exerc. 2007; Cobb et al., 2003; Beals & Hill, 2006; Torstveit & Sundgot Borgen, 2005)

15. Low EA, Hormone Levels, and Bone
blood glucose insulin leptin secretion
Inadequate energy
Effects Circulating Leptin: Hypothalamus
Leptin crosses the BBB, binds to Ob-Rb receptors in the arcuate nucleus
Activates POMC, Inhibits NPY/AgRP neurons
Appetite Suppression
Hypothalamic Pituitary Signaling Cascades
Gonadotropin releasing hormone (RH)
Growth hormone axis
Thyrotropin RH
Corticotropin RH
Estradiol
IGF-1
T3/T4
Cortisol
Chan JL, Mantzoros CS. Lancet 2005;366:74-85.

16. Low EA, Hormone Levels, and Bone
blood glucose insulin leptin secretion
Inadequate energy
Effects Circulating Leptin: Hypothalamus
Leptin crosses the BBB, binds to Ob-Rb receptors in the arcuate nucleus
Activates POMC, Inhibits NPY/AgRP neurons
Low Energy Availability & Leptin
Low Energy Availability & Leptin
Appetite Suppression
Hypothalamic Pituitary Signaling Cascades
Gonadotropin releasing hormone (RH)
Growth hormone axis
Thyrotropin RH
Corticotropin RH
Estradiol
IGF-1
T3/T4
Cortisol
Chan JL, Mantzoros CS. Lancet 2005;366:74-85.

17. blood glucose insulin leptin secretion
Inadequate energy intake
blood glucose insulin leptin secretion
BRAIN / HYPOTHALAMUS
Estrogen,
LH/FSH
Menstrual
Dysfunctions
Reduced Bone
Formation
IGF-1
Lean Muscle Loss
Reduced Bone
Formation
- Bone Loss
Thyroid
Hormone
Suppressed
Metabolism
Stress
Hormone Levels
Lean Muscle Loss
Bone Loss
Menstrual
Dysfunction
Leptin
Low Food Intake (LEA)
Chan JL, Mantzoros CS. Lancet 2005;366:74-85.

18. Low EA, Hormone Levels, and Bone
Leptin (bone-building effects)
Osteoblast formation
Osteblast apoptosis
Osteoclast maturation
Estradiol (bone-building effects)
Gut Ca2+ absorption
Renal calcium excretion
IGF-1 (bone-building effects)
Collagen deterioration
Synthesis of bone matrix proteins

19. Effect of Low Energy Availability
Athletes need adequate energy during periods of high-volume, intense training to maintain body weight and optimize the effects of training.
Chronic low energy intakes can result in :
Loss of lean muscle mass
Suppressed metabolic rate
Menstrual dysfunction, hypothalamic hypogonadism
Loss or failure to gain bone density
Increased fatigue
Injury and illness
Prolonged recovery
ADA, ACSM Joint Position Stand: Nutrition and Athletic Performance, JADA, 2009
Nattiv et al. Med Sci Sports Exerc. 2007

20. Low EA & Performance Adequate nutrition linked to performance
Undernourishment associated with lower VO2max & running speed
Inadequate carbohydrate intake leads to early glycogen depletion and fatigue
Low protein intake contributes to muscle weakness, muscle wasting
Low blood glucose causes mental fatigue, lack of focus & concentration
Thompson RA and Trattner Sherman R. Routledge, New York, NY, 2010

21. Male Athletes and the Triad
Triad-related research in men
Overtraining in endurance trained men leading to reductions in testosterone & sperm count (Roberts AC et al., 1993)
Lower resting & free testosterone in endurance trained compared to sedentary men (Hackney AC et al., 1988)
Two studies reported lower lumbar spine bone mass in male endurance runners (Bilanin et al., 1989; Fredericson et al., 2007)
One study found a moderate negative association between running training volume & lumbar spine BMD (Hind et al, 2006)

23. Project SPIRIT: Sports Injury Research in Teens
740 high school athletes Six schools in Southern California
(Spring 2003-Spring 2004)
N = 170
(8 sports)
Track & Field (N= 60)
Cross-country (N=33)
Soccer (N= 21) Softball (N= 16) Volleyball (N= 11) Tennis (N= 10)
Swimming (N=13)
Lacrosse (N= 6)
Eating Attitudes/Behaviors (EDE-Q) & Menstrual Questionnaire (N= 589)
Stratified by menstrual status; randomized; DXA BMD Scan (N= 170)
Arch Pediatr Adolesc Med Feb;160(2):

24. Female High School Athlete Study (2003-2005)
N= 184 female athletes from 12 schools in Southern California
Aims
Assess the pattern of bone mineral accumulation among female
high school athletes
Identify factors associated with low BMD
Assessments :
- Eating attitudes/behaviors (EDE-Q)
- Menstrual history questionnaire
- BMD by DXA (spine, hip, total body)
Comparison Groups:
Endurance runners (N= 93)
Non-endurance-runner athletes (N= 91) 24

25. Menstrual Irregularity
Prevalence Estimates: Runners vs. Non-Runner Athletes
Runners (N= 93) Non-Runner Athletes (N= 91) * %
Low BMD Z < -2
Menstrual Irregularity
Low BMD Z < -1
Barrack et al. J Bone Miner Res. 2010;25:

26. Number of Menstrual Cycles in the Past Year
Association between Menstrual Function & BMD Z-score in High School Runners (N= 93) b a
BMD Z-score c b
Total body
Lumbar spine
Total Body
Lumbar Spine
a,c
Number of Menstrual Cycles in the Past Year
Barrack et al. Med Sci Sports Exerc., 2008 Dec;40(12):

27. Lumbar Spine BMD Z-scores among EDE-Q groups in Runners
1.0
0.5
-0.5
-1.0
-1.5
-2.0 b
BMD Z-score a
a, b
Normal EDE-Q (N=75)
Elevated Weight and/or Shape Score (N=13)
Elevated Dietary Restraint Score (N=5)
Barrack et al. Am J Clin Nutr. 2000; 87:36-43.

28. Running Participation and BMD in High School Runners
0.9
0.6
0.3
-0.3
-0.6
-0.9
-1.2
-1.5
Total Body
Lumbar Spine b
BMD Z-score b a a 5+
(N= 24)
< 3
(N= 26)
3 - 4
(N= 37)
Lifetime Seasons of Endurance Running
Barrack et al. Med Sci Sports Exerc., 2008 Dec;40(12):

29. Stress Fracture
A bone stress injury (BSI) resulting from repetitive overuse, ranging in severity
Stress reaction    Grade IV Fracture
In retrospective studies, prevalence estimates among female runners & track and field athletes range
from 8.3% to 52.0%
Prospective studies among female runners and military recruits reported an incidence of bone stress injuries of 3.3% to 28.9%
Barrack et al., (2014) AJSM, 42(4),

30. Goolbsy MA, Barrack MT, Nattiv A, Sports Health. 2012 Jul;4(4):352-6

31. Stress Fracture: Risk Factors
Higher Incidence of Bone Stress Injuries with Increasing Female Athlete Triad–Related Risk Factors: A Prospective Multisite Study of Exercising Girls and Women (N= 259)
Highest Risk (46%): h/wk of purposeful exercise - BMD Z score < – additional factors including
BMI <21.0 kg/m2
Oligo-/amenorrhea
Elevated dietary restraint
Participation in a leanness sport
Barrack et al., (2014) AJSM, 42(4),

32. Stress Fracture: Risk Factors
Identifying Sex-Specific Risk Factors for Stress Fractures in Adolescent Runners (N= 748, 442 girls & 306 boys)
Female-Specific Risk Factors - Fracture History
History of dance/gymnastics
BMI < 19 kg/m2
Late age at menarche (>15y)
Male-Specific Risk Factors - Fracture History
Lack of participation in basketball
More seasons of endurance running
Tenforde et al., (2013) Med Sci Sports Exerc, 45(10), p

33. Adolescent Athlete: Nutrient Intake
Limited research on dietary & nutrient intake in adolescent athletes
Prior reports suggest adolescent athletes may consume below-recommended levels of calcium (females), iron (females), vitamin D
Leanness/Endurance Runner
Below recommended intakes of Energy (i.e. calories), Carbohydrate

34. Adolescent Athlete: Recommendations
Current evidence-based nutrition recommendations and position papers specific to adult competitors
Recommend sports dietitians adapt recommendations for adolescent athletes to meet individualized needs (i.e. growth)
Nutrition and Athletic Performance, J Adad Nutr Diet, 2016

35. Nutrition for Bone Health
Energy (Calories)
Adequate Energy Availability needed to promote optimal hormone status and bone formation
Meeting micronutrient needs (with LEA) is NOT enough
For athletes, energy needs will vary based on body composition and exercise energy expenditure [60 kg female athlete, 20% fat]
Nutrition and Athletic Performance, J Adad Nutr Diet, 2016

36. Nutrition for Bone Health
Energy (Calories)
Adequate Energy Availability needed to promote optimal hormone status and bone formation
Meeting micronutrient needs (with LEA) is NOT enough
For athletes, energy needs will vary based on body composition and exercise energy expenditure [60 kg female athlete, 20% fat]
Energy Intake = (EA * FFM) + EEE
= (45 * 48 kg) + 750
= 2,910 kcal
Nutrition and Athletic Performance, J Adad Nutr Diet, 2016

37. Nutrition for Bone Health
Tips for optimizing Energy intake
Enhance current meals/snacks with high calorie, nutrient-rich foods
Nuts, nut butters, dried fruit, trail mix, hummus, oil-based salad dressings, smoothies, bagels
Add 1-2 snacks per day
Gradual introduction of calories (~ kcal increase)
Small frequent meals

38. Nutrition for Bone Health
Tips for optimizing Energy intake
Replenish post-exercise (1-1.2 g/kg CHO; 0.3 g/kg PRO)
Include calcium & vitamin D rich foods
Whole grain cereal, fruit, 2% milk
Smoothie (banana, yogurt, nut butter)
Bagel sandwich with turkey & cheese
Oatmeal with yogurt & berries

39. Nutrition Interventions
Impact of Increased Caloric Intake on Bone Health and Menstrual Cyclicity in Energy Deficient Exercising Women
Twelve-month randomized control trial to test the effectiveness of increased food intake to improve bone health and restore menstrual cycles in women with 1) menstrual disturbances; 2) who exercise regularly and 3) have a chronic energy deficit.

40. Nutrition Interventions
Case Report of Two Exercising Women
Resumption of menses after 23 days
Subject
Age (y) 24
Weight (kg)
54.0
BMI (kg/m2)
19.7
Body Fat (%)
22.7
Age at Menarche (y) 13
Duration of Amenorrhea (days) 90
Physical Activity (hours/week)
7.3
Subject
BL Post
Energy intake (kcal)
1,482
1,904
Weekly EEE (kcal)
237
REE/pREE
0.87
0.94
* Elevated dietary restraint at baseline
Mallinson et al., J Int Soc Sports Nut, 10(1):34, 2013

41. Nutrition Interventions
Change in anthropometric, hormonal, metabolic, and bone-related indicators after the 12-month intervention
Subject
Weight (kg)
2.8
BMI (kg)
1.0
Fat mass (%)
17.5
Leptin (%)
279.8
Ghrelin (pmol/L)
-12.1
TT3 (nmol/L)
31.5
P1NP (%)
51.6
CTx (%)
-36.1
Mallinson et al., J Int Soc Sports Nut, 10(1):34, 2013

42. Preliminary Results from a Prospective Study Using the Female Athlete Triad Cumulative Risk Assessment (Triad-RA)
155 (76 male, 69 female) middle & long distance runners at two NCAA Division I programs, followed prospectively for four years.
The TRIAD-RA used to identify runners at low, moderate, or high risk for the Triad, followed by individualized nutrition interventions
Among a subset of 12 female athletes w/consecutive DXA scans:
Five had > 2% improvement in L1-L4 spine BMD (two females with >5%)
Number of runners with amenorrhea/oligomenorrhea decreased
Number of runners with BSI’s decreased
Kraus et al., Med Sci Sports Exerc, 49(5S):1098, May 2017

43. Conclusions
Adolescent athletes represent a unique athlete population with specialized needs for optimizing performance, growth, and bone health
A variety of nutrients (vitamins, minerals, macronutrients) and energy availability play key roles during this critical period of bone mineral accrual
Low energy availability affects endocrine function and key hormones involved in bone formation and resorption
Nutrition interventions targeting at-risk athlete young adult populations have show promise
Further research is recommended to identify evidence-based nutrition interventions for adolescent athletes at risk for low BMD