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Relative Energy Deficiency In Sport

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Other Names

  • Female Athletic Triad
  • Low Energy Availability in Athletes (LEA)
  • RED-S or REDS
  • Athletic Triad
  • Female Athlete Triad
  • Male Athlete Triad

Background

  • This page refers to relative energy deficiency in sport (REDS), Female Athlete Triad, and Male Athlete Triad

Definition

  • Female Athelete Triad:
    • Low energy availability
    • Ammenorrhea or Oligomenorrhea
    • Decreased Bone Mineral Density
  • REDS is defined by the presence of:
    • Low energy availability
    • Multiple organ system dysfunction not limited solely to menstrual function and bone health
  • Note that there is some controversy over the distinctions and overlap between REDS and the female athlete triad[1]
    • It can be reasonably stated that REDS is an expansion but not a replacement of the female athlete triad

History

  • The term REDS was first introduced in 2014 by the International Olympic Committee[2]

Epidemiology

  • Disordered Eating
    • Prevalence differs significantly among sports[3]
    • Female athletes: adults (20%), adolescent (13%)[4]
    • Male athletes: adults (8%), adolescent (3%)
  • Secondary amenorrhea
    • Estimated to affect anywhere from 2-5% of all collegiate athletes
    • Up to 69% in ballet dancers[5]
    • Up to 65% in long distance runners[6]
  • Primary amenorrhea
    • 7% of all college athletes[7]
    • Highest in cheerleading, diving and gymnastics (22%)

Pathophysiology

  • Centered around relative energy deficiency
    • The female athlete triad remains defined by low energy availability with subsequent menstrual dysfunction, poor bone health
    • REDS includes additional organ systems such as endocrine, immunology, psychiatry, cardiovascular, gastrointestinal, metabolic and hematological
    • Significant implications to athletes performance and long term overall health
  • Defined by imbalance between energy intake and energy expenditure
    • Energy intake: total daily caloric intake
    • Energy expenditure: defined as energy required to support homeostasis, health, activities of daily living, growth and sporting activities
    • Thought to be primary etiologic factor for other components of REDS
  • Energy availability (EA)
    • EA = energy intake (EI) - energy expenditure (EE)
    • Can also divide above calculate by fat free mass (FFM)
    • Measured in kilo cals (kcals)
    • Average EA in a healthy adult is 45 kcal/kg fat-free mass (FFM) per day
  • Low EA can occur due to
    • Decreased EI
    • Increased exercise load
  • Most cases of REDS are due to disordered eating
    • However, may occur due to mismanaged athlete training program or inadequate increase in EI with new program

Disordered Eating

  • Should be considered as a spectrum
    • On one end, starts with appropriate eating behaviors and ocassional short term restrictive diets
    • On the other end, clinical DE with abnormal behaviors, distorted body image, weight fluctuations, medical complications, impaired athletic performance
  • Many features in common with DSM-5 eating eating disorders including Anorexia Nervosa, Bulimia Nervosa, Binge Eating Disorder[8]
  • Pathogenesis is considered multifacorial including[9]
    • Cultural
    • Familial
    • Individual
    • Genetic/ biochemical
  • Sport-related factors have also been implicated including[10]
    • Dieting to enhance performance
    • Personality factors
    • Pressure to lose weight
    • Frequent weight cytcling
    • Early start to sport specific training
    • Overtraining
    • Recurrent and non-healing injuries
    • Inappropriate coaching behaviors
    • Regulations from certain sports
  • Physiologic appetite regulation
    • Leptin: inhibits hunger, adipokine (secreted by fat cells)
    • Adiponectin: adipokine
    • Ghrelin: promotes hunger, released from stomach in low energy states
    • Peptide YY (PYY): appetite suppressant, released by intestinal cells following caloric intake

Amenorrhea

  • Definitions
    • Eumenorrhea: regular cycles between 21-35 days, may be up to 45 days in adolescents
    • Primary amenorrhea: no menarche by age 15[11]
    • Secondary amenorrhea: absence of 3 consecutive cycles following menarche
    • Oligomenorrhea: cycle length greater than 45 days
  • More subtle findings of menstrual dysfunction likely underestimated
    • Light bleeding
    • Mildly extended menstrual interval
    • Pre- and post-menstrual spotting
  • Functional Hypothalamic Amenorrhea (FHA)
    • Defined by persistent anovulation with no identifiable organic cause[12]
    • Marked reduction in EA, leading to decreased gonadotropic releasing hormone (GnRH), luteinizing hormone (LH), follicle-stimulating hormone (FSH)
    • Results in decreased release of estrogen, progesterone and alterations in menstrual cycle
  • Estimating risk of dysmenorrhea is difficult
    • The probability of developing menstrual dysfunction is greater than 50% when athletes absolute EA drops below 30 kcal/kg of FFM/day[13]
    • There is a dose response relationship between ED/DE and frequency of menstrual dysfunction
    • Severity of menstrual dysfunction does not necessarily correlate with magnitude of ED/DE[14]
  • Rapid fat loss in a period as short as a month may disrupt normal menstrual function

Decreased Bone Mineral Density

  • Normal bone physiology
    • Peak bone mass occurs at around 19 years (women) to 20.5 years (men)[15]
    • Estrogen: increases serum calcium uptake, bone deposition
    • Progesterone: facilitates the activity of estrogen
    • Testosterone: anabolic effects on bone (stimulates osteoclasts)[16]
  • Effects of REDS
    • Estrogen/progrestrone imbalance can lead to negative effects on bone
    • Low testosterone associated with low BMD in male athletes[17]
    • Diminished benefit from osteogenic effects of exercise
  • Implications of low BMD
    • Increased risk of stress fractures[18]
    • Increased risk of injuries
    • Impaired athletic performance
    • Reduced responsiveness to training and performance

Race

  • In REDS, Caucasian women are the most well studied
    • Whether race places a role or not is unclear
  • African American athletes
    • Lower risk of ED[19]
    • Undergo menarche at an earlier age
    • Have greater baseline BMD with lower risk of osteoporosis, fracture[20]
  • Preliminary study[21]
    • Caucasian athletes have greatisk risk of ED, menstrual dysfunction
    • No advantage for BMD in African black athletes
    • (need to get updated citation)

Other

  • Metabolic dsysregulation also occurs with the following[22][23]
    • Insulin
    • Cortisol
    • Growth hormone
    • Insulin-like growth factor-I (IGF-I)
    • 3,3,5-triiodothyronine
    • Grehlin
    • Leptin
    • Peptide tyrosine–tyrosine
    • Glucose
    • Fatty acids
    • Ketones
    • Oxytocin
    • Thyroid function
    • Muscle protein synthesis[24]

Risk Factors

  • Intrinsic
    • Female Gender
  • Race
    • Caucasian, most commonly seen and studied
  • High Risk Sports
    • Gymnastics
    • Figure skating
    • Ballet
    • Diving
    • Swimming
    • Long distance running
  • Risk in male athletes
    • Cyclists[25]
    • Ski Jumpers

Differential Diagnosis

Clinical Features

  • Important to inquire about
    • Eating habits, caloric intake
    • Body image
    • Recent changes in training (duration, intensity, freqwuency)
    • History of stress injuries
    • Medication and supplement use
    • Menstrual history in women (menarche, frequency, etc)
    • Sleep patterns and hygiene
    • Athlete knowledge on energy balance
  • Patients may endorse
    • Disordered eating
    • Fatigue
    • Hair loss
    • Cold hands and feet
    • Dry skin
    • Significant weight loss
    • Increased recovery time from injuries
    • Increased incidence of fractures
    • Cessation of menses
    • Low self-esteem
    • Depression
  • Physical Exam
    • Orthostatic hypotension
    • Hair: Lanugo (fine, thin, soft hair)
    • ENT: parotid gland enlargement, dry mucous membranes
    • Pelvic: Vaginal atrophy, pregnancy
    • Skin: hypercarotenaemia, acne, hirsuitism
    • CV: Bradycardia, arrhythmia, increased resting heart rate
    • Developmental: Tanner staging
  • Special Tests
    • Russells Sign: calluses on knuckles, back of hand due to repeated self-induced vomiting

Evaluation

Screening

  • Screening is challenging as symptoms can be subtle and may not all present simultaneously
    • Requires high index of suspicion
    • Early detection is critical to prevent long term consequences
  • Annual Periodic Health Examination
    • Part of the screening process for REDS
    • Look for presence of ED, weight loss, lack of normal growth, menstrual dysfunction, recurrent injuries or illness, decline in performance, mood changes
  • Screening Tools
    • Multiple exist, needs to be updated

Energy Availability

  • Energy Availability (EA)
    • EA (kcal/kg FFM/day) = Energy Intake (kcal/day) - Exercise Energy Expenditure (kcal/day )
    • Measurements require dietician or nutritionist expertise
  • Energy Intake (EI)
    • Retrospective: based on recall
    • Prospective: use of food diary
  • Exercise Energy Expenditure (EEE)
    • Assessed by exercise log
    • May be supplemented or replaced by digital devices
  • Fat Free Mass (FFM)
    • Quantified by DEXA scan or anthropometry[26]
  • Screening tools for ED
    • Eating Disorder Examination interview (EDE-16)
    • Brief Eating Disorder in Athletes Questionnaire (BEDA-Q)

Menstrual Dysfunction

  • Functional Hypothalamic Amenorrhea (FHA)
    • Diagnosis of exclusion and must consider other causes of dysmenorrhea
  • Careful review of gynecological history and reproductive health
    • Includes age of menarche, regularity, medication, family history, other health issues
  • Physical exam
    • Often normal
    • May reveal pregnancy, vaginal atrophy
  • Labs to check
    • Hemoglobin (including iron studies, B12, folate, etc if abnormal)
    • Reproductive: Luteinising Hormone (LH), Follicle Stimulating Hormone (FSH), Prolactin, Estradiol
    • Thyroid: T4, Thyroid Stimulating Hormone (TSH)
    • HCG (pregnancy)
    • Androgen studies

Bone Health

  • Dual-energy X-ray Absorptiometry (DXA)
    • Used to measure bone mineral density
    • Athletes in weight bearing sports should have 5-15% higher BMD than non-athletes[27]
    • Output is given in Z-score
  • Z-score interpretation
    • < -1.0: investigate further
    • -1.0 to -2.0: considered low BMD in athletes
    • < -2.0: considered osteoporosis

Other Evaluation

  • Cardiac screening
    • Electrocardiogram should be considered, especially if abnormal vital signs
    • Assess for arrhythmias, prolonged QTc
  • Additional labs to consider
    • Serum carotene
    • Metabolic panel
    • Prolactin
    • Vitamin D and other vitamin levels

Diagnostic Challenges

  • Complex dose-response relationship between EA and dysfunction of normal metabolic physiology
    • Reduction in EA and subsequent disruption of hormones, bone health vary significantly in degree and thresholds
  • Resting metabolic rate in athletes of small stature is typically underestimated
    • Linear scaling of EA relative to low body mass (LBM)/ FFM inadequate in smaller framed athletes[28]
  • Laboratory abnormalities may not clinically correlate to the athlete
    • At this time, there is a lack of consensus on clear thresholds or associations between low EA and laboratory evaluation of metabolic hormones, menstrual dysfunction[29][30]

Classification

  • N/A

Management

Prognosis

  • Needs to be updated

Prevention

  • The following prevention strategies are based on the IOC consensus group[31]
    • Educational program: healthy eating, nutrition, EA, the risks of dieting and how these affect health and performance.
    • Reduction of emphasis on weigh,
    • Increase emphasis on nutrition, health as a means to enhance performance.
    • Develop realistic and health-promoting goals related to weight and body composition.
    • Avoid: critical comments about an athlete's body shape/weight.
    • Resources: use of reputable sources of information.
    • Promotion of awareness that good performance does not always mean the athlete is healthy.
    • Encouragement and support of appropriate, timely and effective treatment.
  • Healthcare Professional Recommendations
    • Multidisciplinary support team should include sports physician, nutritionist, psychologist, physiotherapist and physiologist.
    • Education of the medical team in the detection and treatment of the REDS
    • Implementation of the REDS Risk Assessment Model in the PHE and the RED-S RTP Model.
  • Sport Organization Recommendations
    • Preventative educational program(s)
    • Rule modifications/changes to address weight-sensitive issues in sport
    • Policies for coaches on the healthy practice of managing athlete eating behavior, weight and body composition.

General

  • Requires multi-modal approach
    • Correct energy imbalance: increase energy intake, decrease energy expenditure
    • Address menstrual dysfunction
    • Improve bone health
    • Psychological interventions
    • Improve performance
  • RED-S Clinical Assessment Tool
    • Tool developed by IOC to aid in evaluation, management of at risk athletes
    • Provides guide to activity recommendations

Energy Availability

  • Correct energy imbalance
    • Primary treatment for REDS
    • Increased energy intake
    • Decreased energy expenditure
  • Increase Energy Intake
    • Addition of energy rich supplement was helpful[32]
    • Measuring EA is challenging
    • Practical approach is to increase EI by 300-600 kcal/day
  • Decrease Energy expenditure
    • Insert rest day into training program
    • Decrease training volume
  • Education is critical
    • Many athletes believe their symptoms to be normal
    • Important to gain trust of athletes, family, teammates, coaches
    • Promote concept of 'eat to perform'

Menstrual Dysfunction

  • General
    • Weight gain is strong predictor of recovery of normal menstrual function[33]
    • Time frame of recovery varies based on severity and duration of symptoms
  • Oral Contraception
    • Should be considered in amenorrheic athlete
    • Does not correct etiology of REDS

Bone Health

  • General
    • Healthy weight gain is the most effective method of restoring bone formation, resorption and normal BMD[34]
    • Full recovery may not be possible in some cases due to impaired bone microarchitecture[35]
  • Training
    • Mechanical loading and impact sports can improve BMD[36]
    • Programming with high-impact loading, resistance training should be prescribed
  • Calcium
    • Athlete should be consuming 1500 mg/day through diet and/or supplements
  • Vitamin D
    • Deficiency more common in north climates during winter months
    • Recommend maintaining vitamin D [25(OH)D] blood levels above 32–50 ng/mL[37]
    • Can supplement with 1500-200 IU/day
  • Estradiol
    • Transdermal application has shown some benefit for BMD[38]
    • Oral contraceptives have show benefit in amenorrheic athletes[39], but appear to have detrimental effects on BMD in athletes with FHA[40]
  • Bisphosphonates
    • Not recommended in women of reproductive age
    • Known to be teratogenic
  • Other medications
  • In men

Psychiatric Considerations

  • General
    • Psychiatric component often present, especially if athlete unable to follow treatment plan
    • Eating disorder correlates to resistance to treatment plan[41]
  • Treatment
    • Should be provided by professional knowledgeable about eating disorders in athletes
    • Type, frequency, intensity and duration will vary from athlete to athlete
    • Can generally be performed on an outpatient basis
    • Inpatient management should be considered if suicidal behavior, lack of progress as outpatient
  • Modalities
    • Cognitive behavioral therapy
    • Dialectical behavior therapy
    • Family-based therapy
  • Pharmacotherapy
    • Anti-depressants most often prescribed
    • Particularly useful if co-morbid conditions present

Rehab and Return to Play

Rehabilitation

Return to Play

  • Risk stratification
    • Based on guidelines from IOC Consensus group, Norwegian Olympic Training Center[31]
    • Useful to determine who can return to or participate in sports
  • High risk/ red light
    • Should not be cleared to participate
    • Due to severity of symptoms, sports may post jeopary to their health, distract athlete from seeking appropriate care
  • Moderate risk/ yellow light
    • Cleared for sports only with close supervision and medical treatment plan
    • Re-evaluation at regular intervals (1-3 months)
  • Low risk/ green light
    • Unrestricted with monitoring

Complications

Long term implications

  • Anemia
  • Chronic fatigue
  • Weakened Immune system and increased risk of infection
  • Cardiovascular dysfunction[42]
    • Endothelial dysfunction, abnormal lipid profiles
  • Endocrine dysfunction
    • Slowing of glucose utilization, mobilization of fat stores, slowing metabolic rate[43]
  • Gastrointestinal dysfunction
  • Reproductive dysfunction
  • Skeletal dysfunction
  • Renal dysfunction
  • Central Nervous System dysfunction
  • Psychological stress
    • Depression
    • Anxiety
    • Altered perception of normalcy

See Also

References

  1. ↑ Williams, N. I., Koltun, K. J., Strock, N. C. A., & De Souza, M. J. (2019). Perspectives for Progress - Female Athlete Triad and Relative Energy Deficiency in Sport. Exercise and Sport Sciences Reviews, 1. doi:10.1249/jes.0000000000000200 
  2. ↑ Sundgot-Borgen, Jorunn, et al. "How to minimise the health risks to athletes who compete in weight-sensitive sports review and position statement on behalf of the Ad Hoc Research Working Group on Body Composition, Health and Performance, under the auspices of the IOC Medical Commission." British journal of sports medicine 47.16 (2013): 1012-1022.
  3. ↑ Sundgot-Borgen J, Torstveit MK. Aspects of disordered eating continuum in elite high-intensity sports. Scand J Med Sci Sports 2010;20(Suppl 2):112–21.
  4. ↑ Martinsen M, Sundgot-Borgen J. Higher prevalence of eating disorders among adolescent elite athletes than controls. Med Sci Sports Exerc 2013;45:1188–97.
  5. ↑ Abraham SF, Beumont PJ, Fraser IS, et al. Body weight, exercise and menstrual status among ballet dancers in training. Br J Obstet Gynaecol 1982;89:507–10.
  6. ↑ Dusek T. Influence of high intensity training on menstrual cycle disorders in athletes. Croat Med J 2001;42:79–82.
  7. ↑ Beals KA, Manore MM. Disorders of the female athlete triad among collegiate athletes. Int J Sport Nutr Exerc Metab 2002;12:281–93
  8. ↑ American Psychiatric Association. Diagnostic and statistical manual of mental disorders, 5th edn. Washington, DC: American Psychiatric Association, 2013
  9. ↑ Stice E, South K, Shaw H. Future directions in etiologic, prevention, and treatment research for eating disorders. J Clin Child Adolesc Psychol 2012;41:845–55.
  10. ↑ Sundgot-Borgen J, Meyer NL, Lohman TG, et al. How to minimise the health risks to athletes who compete in weight-sensitive sports review and position statement on behalf of the Ad Hoc Research Working Group on Body Composition, Health and Performance, under the auspices of the IOC Medical Commission. Br J Sports Med 2013;47:1012–22.
  11. ↑ American Society of Reproductive Medicine Practice Committee. Current evaluation of amenorrhea—has an update (reviewed June 2008). Fert Steril 2008;90:S219–25
  12. ↑ Gordon, C.M. (2010). Clinical practice. Functional hypothalamic amenorrhea. The New England Journal of Medicine, 363(4), 365–371.
  13. ↑ Lieberman, J.L., De Souza, M.J., Wagstaff, D.A., & Williams, N.I. (2018). Menstrual disruption with exercise is not linked to an energy availability threshold. Medicine & Science in Sports and Exercise, 50(3), 551–561.
  14. ↑ Williams, N.I., Leidy, H.J., Hill, B.R., Lieberman, J.L., Legro, R.S., & De Souza, M.J. (2015). Magnitude of daily energy deficit predicts frequency but not severity of menstrual disturbances associated with exercise and caloric restriction. American Journal of Physiology. Endocrinology and Metabolism, 308(1), E29–E39.
  15. ↑ Baxter-Jones AD, Faulkner RA, Forwood MR, et al. Bone mineral accrual from 8 to 30 years of age: an estimation of peak bone mass. J Bone Miner Res 2011;26:1729–39.
  16. ↑ Abu EO, Horner A, Kusec V, et al. The localization of androgen receptors in human bone. J Clin Endocrinol Metab 1997;82:3493–7
  17. ↑ Hind K, Truscott JG, Evans JA. Low lumbar spine bone mineral density in both male and female endurance runners. Bone 2006;39:880–5
  18. ↑ Chen YT, Tenforde AS, Fredericson M. Update on stress fractures in female athletes: epidemiology, treatment, and prevention. Curr Rev Musculoskelet Med 2013;6:173–81.
  19. ↑ Pernick Y, Nichols JF, Rauh MJ, et al. Disordered eating among a multi-racial/ethnic sample of female high-school athletes. J Adolesc Health 2006;38:689–95.
  20. ↑ Fang J, Freeman R, Jeganathan R, et al. Variations in hip fracture hospitalization rates among different race/ethnicity groups in New York City. Ethn Dis 2004;14:280–4.
  21. ↑ Kark S, Ochoa EA, Harris MM, et al. The Female Athlete Triad: Preliminary data from a multi-site study on triad and race. Med Sci Sports Exerc 2012; (in press)
  22. ↑ Wade GN, Jones JE. Neuroendocrinology of nutritional infertility. Am J Physiol Regul Integr Comp Physiol 2004;287:R1277–96
  23. ↑ Elliott-Sale, Kirsty J., et al. "Endocrine effects of relative energy deficiency in sport." International Journal of Sport Nutrition and Exercise Metabolism 28.4 (2018): 335-349.
  24. ↑ Areta JL, Burke LM, Ross ML, et al. Timing and distribution of protein ingestion during prolonged recovery from resistance exercise alters myofibrillar protein synthesis. J Physiol 2013;591(Pt 9):2319–31
  25. ↑ Müller W, Groschl W, Müller R, et al. Underweight in ski jumping: the solution of the problem. Int J Sports Med 2006;27:926–34
  26. ↑ Ackland TR, Lohman TG, Sundgot-Borgen J, et al. Current status of body composition assessment in sport: review and position statement on behalf of the ad hoc research working group on body composition health and performance, under the auspices of the I.O.C. Medical Commission. Sports Med 2012;42:227–49
  27. ↑ Duckham RL, Baxter-Jones AD, Johnston JD, et al. Does physical activity in adolescence have site and sex specific benefits on young adult bone size, content and estimated strength? J Bone Miner Res 2014;29:479–86.
  28. ↑ Loucks AB, Kiens B, Wright HH. Energy availability in athletes. J Sports Sci 2011;29(Suppl 1):S7–15.
  29. ↑ Koehler K, Achtzehn S, Braun H, et al. Comparison of self-reported energy availability and metabolic hormones to assess adequacy of dietary energy intake in young elite athletes. Appl Physiol Nutr Metab 2013;38:725–33.
  30. ↑ Reed JL, De Souza MJ, Williams NI. Changes in energy availability across the season in Division I female soccer players. J Sports Sci 2013;31:314–24.
  31. ↑ 31.0 31.1 Mountjoy M, Sundgot-Borgen J, Burke L, et al. The IOC consensus statement: beyond the Female Athlete Triad—Relative Energy Deficiency in Sport (RED-S). British Journal of Sports Medicine 2014;48:491-497.
  32. ↑ Dueck CA, Matt KS, Manore MM, et al. Treatment of athletic amenorrhea with a diet and training intervention program. Int J Sport Nutr 1996;6:24–40.
  33. ↑ Arends JC, Cheung MY, Barrack MT, et al. Restoration of menses with nonpharmacologic therapy in college athletes with menstrual disturbances: a 5-year retrospective study. Int J Sport Nutr Exerc Metab 2012;22:98–108
  34. ↑ Misra M, Prabhakaran R, Miller KK, et al. Weight gain and restoration of menses as predictors of bone mineral density change in adolescent girls with anorexia nervosa-1. J Clin Endocrinol Metab 2008;93:1231–7
  35. ↑ Ackerman KE, Misra M. Bone health and the female athlete triad in adolescent athletes. Phys Sports Med 2011;39:131–41.
  36. ↑ Michalopoulou M, Kambas A, Leontsini D, et al. Physical activity is associated with bone geometry of premenarcheal girls in a dose-dependent manner. Metabolism 2013;62:1811–18
  37. ↑ Holick MF, Binkley NC, Bischoff-Ferrari HA, et al. Evaluation, treatment, and prevention of vitamin D deficiency: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab 2011;96:1911–30
  38. ↑ Misra M, Klibanski A. Bone health in anorexia nervosa. Curr Opin Endocrinol Diabetes Obes 2011;18:376–82
  39. ↑ Cobb KL, Bachrach LK, Sowers M, et al. The effect of oral contraceptives on bone mass and stress fractures in female runners. Med Sci Sports Exerc 2007;39:1464–73
  40. ↑ Scheid JL, Toombs RJ, Ducher G, et al. Estrogen and peptide YY are associated with bone mineral density in premenopausal exercising women. Bone 2011;49:194–201
  41. ↑ Thompson RA, Sherman RT. Eating disorders in sport. New York: Routledge, 2010.
  42. ↑ Rickenlund A, Eriksson MJ, Schenck-Gustafsson K, et al. Amenorrhea in female athletes is associated with endothelial dysfunction and unfavorable lipid profile. J Clin Endocrinol Metab 2005;90:1354–9.
  43. ↑ Loucks AB, Thuma JR. Luteinizing hormone pulsatility is disrupted at a threshold of energy availability in regularly menstruating women. J Clin Endocrinol Metab 2003;88:297–311.
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