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

Volumn 22, Issue 2, 2012, Pages 98-108

  Arends, Julie C ^a   Cheung, Min Yuen C ^b   Barrack, Michelle T ^b   Nattiv, Aurelia ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Disordered eating; Female athlete triad; Functional hypothalamic amenorrhea; Increased energy availability; Menstrual disturbances in athletes

Indexed keywords

AMENORRHEA AND OLIGOMENORRHEA; ARTICLE; ATHLETE; BODY MASS; DIET THERAPY; DIETARY INTAKE; ERGOMETRY; FEMALE; HUMAN; MENSTRUAL CYCLE; MENSTRUAL IRREGULARITY; MORPHOMETRICS; RESTORATION OF MENSES; RETROSPECTIVE STUDY; WEIGHT GAIN;

EID: 84858601580     PISSN: 1526484X     EISSN: 15432742     Source Type: Journal    
DOI: 10.1123/ijsnem.22.2.98     Document Type: Article

References (59)

1. Ainsworth, B.E., Haskell, W.L., Herrmann, S.D., Meckes, N., Bassett, D.R., Jr., Tudor-Locke, C., . . . Leon, A.S. (2011). 2011 Compendium of physical activities: A second update of codes and MET values. Medicine and Science in Sports and Exercise, 43, 1575-1581. PubMed doi:10.1249/ MSS.0b013e31821ece12
2. American Psychiatric Association Task Force on DSM-IV. (2000). Diagnostic and statistical manual of mental disorders: DSM IV-TR (4th ed., text rev.). Washington, DC: American Psychiatric Association.
3. Baker, F.C., & Driver, H.S. (2007). Circadian rhythms, sleep and the menstrual cycle. Sleep Medicine, 8, 613-622. PubMed doi:10.1016/j.sleep.2006.09. 011
4. Barrack, M.T., Rauh, M.J., & Nichols, J.F. (2010). Cross-sectional evidence of suppressed bone mineral accrual among female adolescent runners. Journal of Bone and Mineral Research, 25, 1850-1857. PubMed doi:10.1002/jbmr.63
5. Berga, S.L., Marcus, M.D., Loucks, T.L., Hlastala, S., Ringham, R., & Krohn, M.A. (2003). Recovery of ovarian activity in women with functional hypothalamic amenorrhea who were treated with cognitive behavioral therapy. Fertility and Sterility, 80, 976-981. PubMed doi:10.1016/S0015-0282(03)01124-5
6. Bronson, F.H., & Manning, J.M. (1991). The energetic regulation of ovulation: A realistic role for body fat. Biology of Reproduction, 44, 945-950. PubMed doi:10.1095/ biolreprod44.6.945
7. Caronia, L.M., Martin, C., Welt, C.K., Sykiotis, G.P., Quinton, R., Thambundit, A., . . . Pitteloud, N.. (2011). A genetic basis for functional hypothalamic amenorrhea. The New England Journal of Medicine, 364, 215-225. PubMed doi:10.1056/NEJMoa0911064
8. Cobb, K.L., Bachrach, L.K., Greendale, G., Marcus, R., Neer, R.M., Nieves, J., . . . Kelsey, J.L. (2003). Disordered eating, menstrual irregularity, and bone mineral density in female runners. Medicine and Science in Sports and Exercise, 35, 711-719. PubMed doi:10.1249/01.MSS.0000064935.68277. E7
9. Couzinet, B., Young, J., Brailly, S., Le Bouc, Y., Chanson, P., & Schaison, G. (1999). Functional hypothalamic amenorrhoea: A partial and reversible gonadotropin deficiency of nutritional origin. Clinical Endocrinology, 50, 229-235. PubMed doi:10.1046/j.1365-2265.1999.00649.x
10. 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 and Metabolism, 89, 3536-3542. PubMed doi:10.1210/jc.2003-032007
11. De Souza, M.J., Miller, B.E., Loucks, A.B., Luciano, A.A., Pescatello, L.S., Campbell, C.G., & Lasley, B.L. (1998). High frequency of luteal phase deficiency and anovulation in recreational women runners: Blunted elevation in follicle-stimulating hormone observed during lutealfollicular transition. The Journal of Clinical Endocrinology and Metabolism, 83, 4220-4232. PubMed doi:10.1210/ jc.83.12.4220
12. De Souza, M.J., Toombs, R.J., Scheid, J.L., O'Donnell, E., West, S.L., & Williams, N.I. (2010). High prevalence of subtle and severe menstrual disturbances in exercising women: Confirmation using daily hormone measures. Human Reproduction (Oxford, England), 25, 491-503. PubMed doi:10.1093/humrep/ dep411
13. Ding, J.H, Sheckter, C.B., Drinkwater, B.L., Soules, M.R., & Bremner, W.J. (1988). High serum cortisol levels in exercise-associated amenorrhea. Annals of Internal Medicine, 108, 530-534. PubMed
14. Drinkwater, B.L., Bruemner, B., & Chesnut, C.H., III. (1990). Menstrual history as a determinant of current bone density in young athletes. Journal of the American Medical Association, 263, 545-548. PubMed doi:10.1001/ jama.1990.03440040084033
15. Drinkwater, B.L., Nilson, K., Chesnut, C.H., III, Bremner, W.J., Shainholtz, S., & Southworth, M.B. (1984). Bone mineral content of amenorrheic and eumenorrheic athletes. The New England Journal of Medicine, 311, 277-281. PubMed doi:10.1056/NEJM198408023110501
16. Drinkwater, B.L., Nilson, K., Ott, S., & Chesnut, C.H., III. (1986). Bone mineral content after resumption of menses in amenorrheic athletes. Journal of the American Medical Association, 256, 380-382. PubMed doi:10.1001/jama. 1986.03380030082032
17. Ducher, G., Eser, P., Hill, B., & Bass, S. (2009). History of amenorrhoea compromises some of the exercise-induced benefits in cortical and trabecular bone in the peripheral and axial skeleton: A study in retired elite gymnasts. Bone, 45, 760-767. PubMed doi:10.1016/j.bone.2009.06.021
18. Dueck, C.A., Matt, K.S., Manore, M.M., & Skinner, J.S. (1996). Treatment of athletic amenorrhea with a diet and training intervention program. International Journal of Sport Nutrition, 6, 24-40. PubMed
19. Food and Agriculture Organization of the United Nations, World Health Organization, & United Nations University. (2001). Joint FAO/WHO/UNU expert consultation on human energy requirements October 2001. Rome, Italy: FAO Headquarters.
20. Fredericson, M., & Kent, K. (2005). Normalization of bone density in a previously amenorrheic runner with osteoporosis. Medicine and Science in Sports and Exercise, 37, 1481-1486. PubMed doi:10.1249/01. mss.0000177561.95201. 8f
21. Golden, N.H., Jacobson, M.S., Schebendach, J., Solanto, M.V., Hertz, S.M., & Shenker, I.R. (1997). Resumption of menses in anorexia nervosa. Archives of Pediatrics & Adolescent Medicine, 151, 16-21. PubMed doi:10.1001/archpedi.1997.02170380020003
22. Keen, A.D., & Drinkwater, B.L. (1997). Irreversible bone loss in former amenorrheic athletes. Osteoporosis International, 7, 311-315. PubMed doi:10.1007/BF01623770
23. Key, A., Mason, H., Allan, R., & Lask, B. (2002). Restoration of ovarian and uterine maturity in adolescents with anorexia nervosa. The International Journal of Eating Disorders, 32, 319-325. PubMed doi:10.1002/eat.10087
24. Kopp-Woodroffe, S.A., Manore, M.M., Dueck, C.A., Skinner, J.S., & Matt, K.S. (1999). Energy and nutrient status of amenorrheic athletes participating in a diet and exercise training intervention program. International Journal of Sport Nutrition, 9, 70-88. PubMed (Pubitemid 29122763)
25. Laughlin, G.A., Dominguez, C.E., & Yen, S.S. (1998). Nutritional and endocrine-metabolic aberrations in women with functional hypothalamic amenorrhea. The Journal of Clinical Endocrinology and Metabolism, 83, 25-32. PubMed doi:10.1210/jc.83.1.25
26. Liu, S.L., & Lebrun, C.M. (2006). Effect of oral contraceptives and hormone replacement therapy on bone mineral density in premenopausal and perimenopausal women: A systematic review. British Journal of Sports Medicine, 40, 11-25. PubMed doi:10.1136/bjsm.2005.020065
27. Livingstone, M.B., Strain, J.J., Prentice, A.M., Coward, W.A., Nevin, G.B., Barker, M.E., . . . Whitehead, R.G. (1991). Potential contribution of leisure activity to the energy expenditure patterns of sedentary populations. The British Journal of Nutrition, 65, 145-155. PubMed doi:10.1079/ BJN19910076
28. Lloyd, T., Myers, C., Buchanan, J.R., & Demers, L.M. (1988). Collegiate women athletes with irregular menses during adolescence have decreased bone density. Obstetrics and Gynecology, 72, 639-642. PubMed
29. Loucks, A.B. (1989). Alterations in the hypothalamic-pituitaryovarian and the hypothalamic-pituitary-adrenal axes in athletic women. The Journal of Clinical Endocrinology and Metabolism, 68, 402-411. PubMed doi:10.1210/ jcem-68-2-402
30. Loucks, A.B. (1990). Effects of exercise training on the menstrual cycle: Existence and mechanisms. Medicine and Science in Sports and Exercise, 22, 275-280. PubMed
31. Loucks, A.B., & Callister, R. (1993). Induction and prevention of low-T3 syndrome in exercising women. The American Journal of Physiology, 264, R924-R930. PubMed (Pubitemid 23152574)
32. Loucks, A.B., & Heath, E.M. (1994). Induction of low-T3 syndrome in exercising women occurs at a threshold of energy availability. The American Journal of Physiology, 266, R817-R823. PubMed
33. Loucks, A.B., & Horvath, S.M. (1985). Athletic amenorrhea: A review. Medicine and Science in Sports and Exercise, 17, 56-72. PubMed (Pubitemid 15140411)
34. Loucks, A.B., Laughlin, G.A., Mortola, J.F., Girton, L., Nelson, J.C., & Yen, S.S. (1992). Hypothalamic-pituitary-thyroidal function in eumenorrheic and amenorrheic athletes. The Journal of Clinical Endocrinology and Metabolism, 75, 514-518. PubMed doi:10.1210/jc.75.2.514
35. Loucks, A.B., & Thuma, J.R. (2003). Luteinizing hormone pulsatility is disrupted at a threshold of energy availability in regularly menstruating women. The Journal of Clinical Endocrinology and Metabolism, 88, 297-311. PubMed doi:10.1210/jc.2002-020369
36. Loucks, A.B., Verdun, M., & Heath, E.M. (1998). Low energy availability, not stress of exercise, alters LH pulsatility in exercising women. Journal of Applied Physiology, 84, 37-46. PubMed (Pubitemid 28065108)
37. Miller, K.K., Lee, E.E., Lawson, E.A., Madhusmita, M., Minihan, J., Grinspoon, S.K., . . . Klibanski, A. (2006). Determinants of skeletal loss and recovery in anorexia nervosa. The Journal of Clinical Endocrinology and Metabolism, 91, 2931-2937. PubMed doi:10.1210/jc.2005-2818
38. Misra, M., Prabhakaran, R., Miller, K.K., Goldstein, M.A., Mickley, D., Clauss, L., . . . Klibanski, A. (2008). Weight gain and restoration of menses as predictors of bone mineral density change in adolescent girls with anorexia nervosa-I. The Journal of Clinical Endocrinology and Metabolism, 93, 1231-1237. PubMed doi:10.1210/ jc.2007-1434
39. Myerson, M., Gutin, B., Warren, M.P., May, M.T., Contento, I., Lee, M., . . . Brooks-Gunn, J. (1991). Resting metabolic rate and energy balance in amenorrheic and eumenorrheic runners. Medicine and Science in Sports and Exercise, 23, 15-22. PubMed
40. National Academy of Sciences. Institute of Medicine. Food and Nutrition Board (2005). Dietary reference intakes for energy. Carbohydrates, fiber, fat, fatty acids, cholesterol, protein, and amino acids. Washington, DC: The National Academies Press.
41. Nattiv, A., Loucks, A.B., Manore, M.M., Sanborn, C.F., Sundgot- Borgen, J., & Warren, M.P. (2007). American College of Sports Medicine position stand. The female athlete triad. Medicine and Science in Sports and Exercise, 39, 1867-1882. PubMed doi:10.1249/mss.0b013e318149f111
42. Practice Committee of American Society for Reproductive Medicine. (2008). Current evaluation of amenorrhea. Fertility and Sterility, 90(5 Suppl.), S219-S225. PubMed
43. Register, T.C., Jayo, M.J., & Jerome, C.P. (1997). Oral contraceptive treatment inhibits the normal acquisition of bone mineral in skeletally immature young adult female monkeys. Osteoporosis International, 7, 348-353. PubMed doi:10.1007/BF01623776
44. Roza AM, Shizgal HM. (1984). The Harris Benedict equation re-evaluated: Resting energy requirements and the body cell mass. The American Journal of Clinical Nutrition, 40, 168-182. PubMed (Pubitemid 14096658)
45. Sanborn, C.F., Albrecht, B.H., & Wagner, W.W., Jr. (1987). Athletic amenorrhea: Lack of association with body fat. Medicine and Science in Sports and Exercise, 19, 207-212. PubMed (Pubitemid 17110073)
46. Sobanski, E., Hiltmann, W.D., Blanz, B., Klein, M., & Schmidt, M.H. (1997). Pelvic ultrasound scanning of the ovaries in adolescent anorectic patients at low weight and after weight recovery. European Child & Adolescent Psychiatry, 6(4), 207-211. PubMed (Pubitemid 28027167)
47. Speroff, L., & Fritz, M.A. (2005). Clinical gynecologic endocrinology and infertility (7th ed.). Philadelphia, PA: Lippincott Williams and Wilkins.
48. Sum, M., & Warren, M.P. (2009). Hypothalamic amenorrhea in young women with polycystic ovary syndrome. Fertility and Sterility, 92, 2106-2108. PubMed doi:10.1016/j. fertnstert.2009.05.063
49. Vescovi, J.D., Jamal, S.A., & De Souza, M.J. (2008). Strategies to reverse bone loss in women with functional hypothalamic amenorrhea: A systematic review of the literature. Osteoporosis International, 19, 465-478. PubMed doi:10.1007/s00198-007-0518-6
50. Warren, M.P. (1980). The effects of exercise on pubertal progression and reproductive function in girls. The Journal of Clinical Endocrinology and Metabolism, 51, 1150-1157. PubMed doi:10.1210/jcem-51-5-1150
51. Warren, M.P. (1983). Effects of undernutrition on reproductive function in the human. Endocrine Reviews, 4, 363-377. PubMed doi:10.1210/edrv-4-4-363
52. Warren, M.P., Brooks-Gunn, J., Fox, R.P., Holderness, C.C., Hyle, E.P., & Hamilton, W.G. (2002). Osteopenia in exercise-associated amenorrhea using ballet dancers as a model: A longitudinal study. The Journal of Clinical Endocrinology and Metabolism, 87, 3162-3168. PubMed doi:10.1210/jc.87.7.3162
53. Warren, M.P., Brooks-Gunn, J., Fox, R.P., Holderness, C.C., Hyle, E.P., Hamilton, W.G., & Hamilton, L. (2003). Persistent osteopenia in ballet dancers with amenorrhea and delayed menarche despite hormone therapy: A longitudinal study. Fertility and Sterility, 80, 398-404. PubMed doi:10.1016/S0015-0282(03)00660-5
54. Warren, M.P., & Goodman, L.R. (2003). Exercise-induced endocrine pathologies. Journal of Endocrinological Investigation, 26, 873-878. PubMed (Pubitemid 38049170)
55. Warren, M.P., Miller, K.K., Olson, W.H., Grinspoon, S.K., & Friedman, A.J. (2005). Effects of an oral contraceptive (norgestimate/ethinyl estradiol) on bone mineral density in women with hypothalamic amenorrhea and osteopenia: An open-label extension of a double-blind, placebocontrolled study. Contraception, 72(3), 206-211. PubMed doi:10.1016/j.contraception.2005.03.007
56. Williams, N.I., Berger, S.L., & Cameron, J.L. (2007). Synergism between psychosocial and metabolic stressors: Impact on reproductive function in cynomolgus monkeys. American Journal of Physiology. Endocrinology and Metabolism, 293, E270-E276. PubMed doi:10.1152/ ajpendo.00108.2007
57. Williams, N.I., Caston-Balderrama, A.L., Helmreich, D.L., Parfitt, D.B., Nosbisch, C., & Cameron, J.L. (2001). Longitudinal changes in reproductive hormones and menstrual cyclicity in cynomolgus monkeys during strenuous exercise training: Abrupt transition to exercise-induced amenorrhea. Endocrinology, 142, 2381-2389. PubMed doi:10.1210/en.142.6.2381
58. Williams, N.I., Helmreich, D.L., Parfitt, D.B., Caston-Balderrama, A., & Cameron, J.L. (2001). Evidence for a causal role of low energy availability in the induction of menstrual cycle disturbances during strenuous exercise training. The Journal of Clinical Endocrinology and Metabolism, 86, 5184-5193. PubMed doi:10.1210/jc.86.11.5184
59. Zanker, C.L., Cooke, C.B., Truscott, J.G., Oldroyd, B., & Jacobs, H.S. (2004). Annual changes of bone density over 12 years in an amenorrheic athlete. Medicine and Science in Sports and Exercise, 36, 137-142. PubMed doi:10.1249/01.MSS.0000106186.68674.2C