Effect of Exercise on Ovulation: A Systematic Review

Abstract

Background

Infertility has been described as a devastating life crisis for couples, and has a particularly severe effect on women, in terms of anxiety and depression. Anovulation accounts for around 30% of female infertility, and while lifestyle factors such as physical activity are known to be important, the relationship between exercise and ovulation is multi-factorial and complex, and to date there are no clear recommendations concerning exercise regimes.

Objectives

The objective of this review was to systematically assess the effect of physical activity on ovulation and to discuss the possible mechanisms by which exercise acts to modulate ovulation in reproductive-age women. This was done with a view to improve existing guidelines for women wishing to conceive, as well as women suffering from anovulatory infertility.

Search Methods

The published literature was searched up to April 2016 using the search terms ovulation, anovulatory, fertility, sport, physical activity and exercise. Both observational and interventional studies were considered, as well as studies that combined exercise with diet. Case studies and articles that did not report anovulation/ovulation or ovarian morphology as outcomes were excluded. Studies involving administered drugs in addition to exercise were excluded.

Results

In total, ten interventions and four observational cohort studies were deemed relevant. Cohort studies showed that there is an increased risk of anovulation in extremely heavy exercisers (>60 min/day), but vigorous exercise of 30–60 min/day was associated with reduced risk of anovulatory infertility. Ten interventions were identified, and of these three have studied the effect of vigorous exercise on ovulation in healthy, ovulating women, but only one showed a significant disruption of ovulation as a result. Seven studies have investigated the effect of exercise on overweight/obese women suffering from polycystic ovary syndrome (PCOS) or anovulatory infertility, showing that exercise, with or without diet, can lead to resumption of ovulation. The mechanism by which exercise affects ovulation is most probably via modulation of the hypothalamic-pituitary-gonadal (HPG) axis due to increased activity of the hypothalamic–pituitary–adrenal (HPA) axis. In heavy exercisers and/or underweight women, an energy drain, low leptin and fluctuating opioids caused by excess exercise have been implicated in HPA dysfunction. In overweight and obese women (with or without PCOS), exercise contributed to lower insulin and free androgen levels, leading to the restoration of HPA regulation of ovulation.

Conclusions

Several clear gaps have been identified in the existing literature. Short-term studies of over-training have not always produced the disturbance to ovulation identified in the observational studies, bringing up the question of the roles of longer term training and chronic energy deficit. We believe this merits further investigation in specific cohorts, such as professional athletes. Another gap is the complete absence of exercise-based interventions in anovulatory women with a normal body mass index (BMI). The possibly unjustified focus on weight loss rather than the exercise programme means there is also a lack of studies comparing types of physical activity, intensity and settings. We believe that these gaps are delaying an efficient and effective use of exercise as a therapeutic modality to treat anovulatory infertility.

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References

  1. 1.

    Hull MG, Glazener CM, Kelly NJ, et al. Population study of causes, treatment, and outcome of infertility. Br Med J (Clin Res Ed). 1985;291:1693–7. doi:10.1093/gerona/glt257.

    CAS  Article  Google Scholar 

  2. 2.

    Greil AL. Infertility and psychological distress: a critical review of the literature. Soc Sci Med. 1997;45:1679–704. doi:10.1016/S0277-9536(97)00102-0.

    CAS  Article  PubMed  Google Scholar 

  3. 3.

    Wright J, Bissonnette F, Duchesne C, et al. Psychosocial distress and infertility—men and women respond differently. Fertil Steril. 1991;55:100–8. <Go to ISI>://WOS:A1991ER18600020

  4. 4.

    Goodarzi MO, Dumesic DA, Chazenbalk G, et al. Polycystic ovary syndrome: etiology, pathogenesis and diagnosis. Nat Rev Endocrinol. 2011;7:219–31. doi:10.1038/nrendo.2010.217.

    CAS  Article  PubMed  Google Scholar 

  5. 5.

    Kessler LM, Craig BM, Plosker SM, et al. Infertility evaluation and treatment among women in the United States. Fertil Steril. 2013;100(1025–1032):e2. doi:10.1016/j.fertnstert.2013.05.040.

    Google Scholar 

  6. 6.

    Panidis D, Tziomalos K, Papadakis E, et al. Lifestyle intervention and anti-obesity therapies in the polycystic ovary syndrome: impact on metabolism and fertility. Endocrine. 2013;44:583–90. doi:10.1007/s12020-013-9971-5.

    CAS  Article  PubMed  Google Scholar 

  7. 7.

    Sharma R, Biedenharn KR, Fedor JM, et al. Lifestyle factors and reproductive health: taking control of your fertility. Reprod Biol Endocrinol. 2013;11:66. doi:10.1186/1477-7827-11-66.

    Article  PubMed  PubMed Central  Google Scholar 

  8. 8.

    Haqq L, McFarlane J, Dieberg G, et al. Effect of lifestyle intervention on the reproductive endocrine profile in women with polycystic ovarian syndrome: a systematic review and meta-analysis. Endocr Connect. 2014;3:36–46. doi:10.1530/EC-14-0010.

    Article  PubMed  PubMed Central  Google Scholar 

  9. 9.

    Stener-Victorin E. Hypothetical physiological and molecular basis for the effect of acupuncture in the treatment of polycystic ovary syndrome. Mol Cell Endocrinol. 2013;373:83–90. doi:10.1016/j.mce.2013.01.006.

    CAS  Article  PubMed  Google Scholar 

  10. 10.

    Moran LJ, Hutchison SK, Norman RJ, et al. Lifestyle changes in women with polycystic ovary syndrome. Cochrane database Syst Rev. 2011;7:CD007506. doi:10.1002/14651858.CD007506.pub3.

    Google Scholar 

  11. 11.

    Olive DL. Exercise and fertility: an update. Curr Opin Obstet Gynecol. 2010;22:259–63. doi:10.1097/GCO.0b013e32833c7227.

    Article  PubMed  Google Scholar 

  12. 12.

    Orio F, Muscogiuri G, Ascione A, et al. Effects of physical exercise on the female reproductive system. Minerva Endocrinol. 2013;38:305–19.

    CAS  PubMed  Google Scholar 

  13. 13.

    Warren MP, Perlroth NE. The effects of intense exercise on the female reproductive system. J Endocrinol. 2001;170:3–11. doi:10.1677/joe.0.1700003.

    CAS  Article  PubMed  Google Scholar 

  14. 14.

    Loucks AB. Effects of exercise training on the menstrual cycle: existence and mechanisms. Med Sci Sport Exerc. 1990;22:275–80.

    CAS  Article  Google Scholar 

  15. 15.

    Loucks AB. Energy availability and infertility. Curr Opin Endocrinol Diabetes Obes. 2007;14:470–4. doi:10.1097/MED.0b013e3282f1cb6a.

    Article  PubMed  Google Scholar 

  16. 16.

    Rooney KL, Domar AD. The impact of lifestyle behaviors on infertility treatment outcome. Curr Opin Obstet Gynecol. 2014;26:181–5. doi:10.1097/GCO.0000000000000069.

    Article  PubMed  Google Scholar 

  17. 17.

    Bermon S, Garnier PY, Hirschberg AL, et al. Serum androgen levels in elite female athletes. J Clin Endocrinol Metab. 2014;99:4328–35. doi:10.1210/jc.2014-1391.

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    Frisch RE. Fatness, menarche, and female fertility. Perspect Biol Med. 1985;28:611–33.

    CAS  Article  PubMed  Google Scholar 

  19. 19.

    Chavarro JE, Rich-Edwards JW, Rosner BA, et al. Diet and lifestyle in the prevention of ovulatory disorder infertility. Obstet Gynecol. 2007;110:1050–8. doi:10.1097/01.AOG.0000287293.25465.e1.

    Article  PubMed  Google Scholar 

  20. 20.

    Rich-Edwards JW, Spiegelman D, Garland M, et al. Physical activity, body mass index, and ovulatory disorder infertility. Epidemiology. 2002;13:184–90. doi:10.1097/00001648-200203000-00013.

    Article  PubMed  Google Scholar 

  21. 21.

    Wojtys EM, Huston LJ, Lindenfeld TN, et al. Association between the menstrual cycle and anterior cruciate ligament injuries in female athletes. Am J Sports Med. 1998;26:614–9.

    CAS  PubMed  Google Scholar 

  22. 22.

    De Souza MJ, Miller BE, Loucks AB, et al. High frequency of luteal phase deficiency and anovulation in recreational women runners: blunted elevation in follicle-stimulating hormone observed during luteal-follicular transition. J Clin Endocrinol Metab. 1998;83:4220–32. doi:10.1210/jcem.83.12.5334.

    PubMed  Google Scholar 

  23. 23.

    Green BB, Daling JR, Weiss NS, et al. Exercise as a risk factor for infertility with ovulatory dysfunction. Am J Public Health. 1986;76:1432–6. doi:10.2105/AJPH.76.12.1432.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. 24.

    Bullen BA, Skrinar GS, Beitins IZ, et al. Induction of menstrual disorders by strenuous exercise in untrained women. N Engl J Med. 1985;312:1349–53. doi:10.1056/NEJM198505233122103.

    CAS  Article  PubMed  Google Scholar 

  25. 25.

    Williams NI, Bullen BA, McArthur JW, et al. Effects of short-term strenuous endurance exercise upon corpus luteum function. Med Sci Sport Exerc. 1999;31:949–58. doi:10.1097/00005768-199907000-00006.

    CAS  Article  Google Scholar 

  26. 26.

    Williams NI, Leidy HJ, Hill BR, et al. Magnitude of daily energy deficit predicts frequency but not severity of menstrual disturbances associated with exercise and caloric restriction. Am J Physiol Endocrinol Metab. 2015;308:E29–39. doi:10.1152/ajpendo.00386.2013.

    CAS  Article  PubMed  Google Scholar 

  27. 27.

    Huber-Buchholz MM, Carey DG, Norman RJ. Restoration of reproductive potential by lifestyle modification in obese polycystic ovary syndrome: role of insulin sensitivity and luteinizing hormone. J Clin Endocrinol Metab. 1999;84:1470–4. doi:10.1210/jcem.84.4.5596.

    CAS  PubMed  Google Scholar 

  28. 28.

    Palomba S, Giallauria F, Falbo A, et al. Structured exercise training programme versus hypocaloric hyperproteic diet in obese polycystic ovary syndrome patients with anovulatory infertility: a 24-week pilot study. Hum Reprod Update. 2008;23:642–50. doi:10.1093/humrep/dem391.

    CAS  Article  Google Scholar 

  29. 29.

    Thomson RL, Buckley JD, Noakes M, et al. The effect of a hypocaloric diet with and without exercise training on body composition, cardiometabolic risk profile, and reproductive function in overweight and obese women with polycystic ovary syndrome. J Clin Endocrinol Metab. 2008;93:3373–80. doi:10.1210/jc.2008-0751.

    CAS  Article  PubMed  Google Scholar 

  30. 30.

    Kuchenbecker WKH, Groen H, van Asselt SJ, et al. In women with polycystic ovary syndrome and obesity, loss of intra-abdominal fat is associated with resumption of ovulation. Hum Reprod. 2011;26:2505–12. doi:10.1093/humrep/der229.

    Article  PubMed  Google Scholar 

  31. 31.

    Nybacka Å, Carlström K, Ståhle A, et al. Randomized comparison of the influence of dietary management and/or physical exercise on ovarian function and metabolic parameters in overweight women with polycystic ovary syndrome. Fertil Steril. 2011;96:1508–13. doi:10.1016/j.fertnstert.2011.09.006.

    Article  PubMed  Google Scholar 

  32. 32.

    Clark A, Ledger W, Galletly C, et al. Weight loss results in significant improvement in pregnancy and ovulation rates in anovulatory obese women. Hum Reprod. 1995;10:2705–12.

    CAS  Article  PubMed  Google Scholar 

  33. 33.

    Clark AM, Thornley B, Tomlinson L, et al. Weight loss in obese infertile women results in improvement in reproductive outcome for all forms of fertility treatment. Hum Reprod. 1998;13:1502–5.

    CAS  Article  PubMed  Google Scholar 

  34. 34.

    Pollock M, Gaesser G, Butcher J, et al. American College of Sports Medicine position stand. Med Sci Sports Exerc. 1998;30:975–91.

    Google Scholar 

  35. 35.

    Gudmundsdottir SL, Flanders WD, Augestad LB. Physical activity and fertility in women: the North-Trøndelag Health Study. Hum Reprod. 2009;24:3196–204. doi:10.1093/humrep/dep337.

    CAS  Article  PubMed  Google Scholar 

  36. 36.

    Wise LA, Rothman KJ, Mikkelsen EM, et al. A prospective cohort study of physical activity and time to pregnancy. Fertil Steril. 2012;97(1136–1142):e4. doi:10.1016/j.fertnstert.2012.02.025.

    Google Scholar 

  37. 37.

    Loucks AB, Callister R. Induction and prevention of low-T3 syndrome in exercising women. Am J Physiol Regul Integr Comp Physiol. 1993;264:R924–30.

    CAS  Google Scholar 

  38. 38.

    Chan JL, Mantzoros CS. Role of leptin in energy-deprivation states: normal human physiology and clinical implications for hypothalamic amenorrhoea and anorexia nervosa. Lancet. 2005;366:74–85. doi:10.1016/S0140-6736(05)66830-4.

    CAS  Article  PubMed  Google Scholar 

  39. 39.

    Laughlin GA, Yen SSC. Hypoleptinemia in women athletes: absence of a diurnal rhythm with amenorrhea. J Clin Endocrinol Metab. 1997;82:318–21. doi:10.1210/jc.82.1.318.

    CAS  Article  PubMed  Google Scholar 

  40. 40.

    Unuane D, Tournaye H, Velkeniers B, et al. Endocrine disorders and female infertility. Best Pract Res Clin Endocrinol Metab. 2011;25:861–73. doi:10.1016/j.beem.2011.08.001.

    CAS  Article  PubMed  Google Scholar 

  41. 41.

    Power ML, Schulkin J. Sex differences in fat storage, fat metabolism, and the health risks from obesity: possible evolutionary origins. Br J Nutr. 2008;99:931–40. doi:10.1017/S0007114507853347.

    CAS  Article  PubMed  Google Scholar 

  42. 42.

    Howlett T, Tomlin S, Ngahfoong L, et al. Release of beta endorphin and met-enkephalin during exercise in normal women: response to training. Br Med J (Clin Res Ed). 1984;288:1950–2. doi:10.1136/bmj.288.6435.1950.

    CAS  Article  Google Scholar 

  43. 43.

    Blake MJ, Stein EA, Vomachka AJ. Effects of exercise training on brain opioid peptides and serum LH in female rats. Peptides. 1984;5:953–8. doi:10.1016/0196-9781(84)90122-0.

    CAS  Article  PubMed  Google Scholar 

  44. 44.

    Heitkamp HC, Schulz H, Röcker K, et al. Endurance training in females: changes in beta-endorphin and ACTH. Int J Sports Med. 1998;19:260–4. doi:10.1055/s-2007-971915.

    CAS  Article  PubMed  Google Scholar 

  45. 45.

    Botticelli G, Modena AB, Bresciani D, et al. Effect of naltrexone treatment on the treadmill exercise-induced hormone release in amenorrheic women. J Endocrinol Investig. 1992;15:839–47. doi:10.1007/BF03348817.

    CAS  Article  Google Scholar 

  46. 46.

    Roa J, Herbison AE. Direct regulation of GnRH neuron excitability by arcuate nucleus POMC and NPY neuron neuropeptides in female mice. Endocrinology. 2012;153:5587–99. doi:10.1210/en.2012-1470.

    CAS  Article  PubMed  Google Scholar 

  47. 47.

    Sapolsky RM, Romero LM, Munck AU. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev. 2000;21:55–89. doi:10.1210/er.21.1.55.

    CAS  PubMed  Google Scholar 

  48. 48.

    Dobson H, Smith RF. What is stress, and how does it affect reproduction? Anim Reprod Sci. 2000;60–61:743–52. doi:10.1016/S0378-4320(00)00080-4.

    Article  PubMed  Google Scholar 

  49. 49.

    Gambacciani M, Yen SS, Rasmussen DD. GnRH release from the mediobasal hypothalamus: in vitro inhibition by corticotropin-releasing factor. Neuroendocrinology. 1986;43:533–6.

    CAS  Article  PubMed  Google Scholar 

  50. 50.

    Warren MP, Goodman LR. Exercise-induced endocrine pathologies. J Endocrinol Investig. 2003;26:873–8. doi:10.1007/BF03345238.

    CAS  Article  Google Scholar 

  51. 51.

    Tilbrook A, Turner A, Clarke I. Effects of stress on reproduction in non-rodent mammals: the role of glucocorticoids and sex differences. Rev Reprod. 2000;5:105–13. doi:10.1530/ror.0.0050105.

    CAS  Article  PubMed  Google Scholar 

  52. 52.

    Wade GN, Jones JE. Lessons from experimental disruption of estrous cycles and behaviors. Med Sci Sports Exerc. 2003;35:1573–80. doi:10.1249/01.MSS.0000084526.51285.D6.

    CAS  Article  PubMed  Google Scholar 

  53. 53.

    Loucks AB, Mortola JF, Girton L, et al. Alterations in the hypothalamic-pituitary-ovarian and the hypothalamic-pituitary-adrenal axes in athletic women. J Clin Endocrinol Metab. 1989;68:402–11. doi:10.1210/jcem-68-2-402.

    CAS  Article  PubMed  Google Scholar 

  54. 54.

    Loucks AB, Verdun M, Heath EM. Low energy availability, not stress of exercise, alters LH pulsatility in exercising women. J Appl Physiol. 1998;84:37–46.

    CAS  PubMed  Google Scholar 

  55. 55.

    OpenStax, Anatomy and Physiology. OpenStax CNX. 2016.https://opentextbc.ca/anatomyandphysiology/.

  56. 56.

    Norman RJ, Wu R, Stankiewicz MT. 4: Polycystic ovary syndrome. Med J Aust. 2004;180:132–7.

    PubMed  Google Scholar 

  57. 57.

    Harrison CL, Lombard CB, Moran LJ, et al. Exercise therapy in polycystic ovary syndrome: a systematic review. Hum Reprod Update. 2011;17:171–83. doi:10.1093/humupd/dmq045.

    Article  PubMed  Google Scholar 

  58. 58.

    Kort JD, Winget C, Kim SH, et al. A retrospective cohort study to evaluate the impact of meaningful weight loss on fertility outcomes in an overweight population with infertility. Fertil Steril. 2014;101:1400–3. doi:10.1016/j.fertnstert.2014.01.036.

    Article  PubMed  Google Scholar 

  59. 59.

    Khaskheli MN, Baloch S, Baloch AS. Infertility and weight reduction: influence and outcome. J Coll Physicians Surg Pak. 2013;23:798–801.

    PubMed  Google Scholar 

  60. 60.

    Hutchison SK, Stepto NK, Harrison CL, et al. Effects of exercise on insulin resistance and body composition in overweight and obese women with and without polycystic ovary syndrome. J Clin Endocrinol Metab. 2011;96:E48–56. doi:10.1210/jc.2010-0828.

    CAS  Article  PubMed  Google Scholar 

  61. 61.

    Dolfing JG, Stassen CM, van Haard PMM, et al. Comparison of MRI-assessed body fat content between lean women with polycystic ovary syndrome (PCOS) and matched controls: less visceral fat with PCOS. Hum Reprod. 2011;26:1495–500. doi:10.1093/humrep/der070.

    CAS  Article  PubMed  Google Scholar 

  62. 62.

    Guzick DS, Wing R, Smith D, et al. Endocrine consequences of weight loss in obese, hyperandrogenic, anovulatory women. Fertil Steril. 1994;61:598–604.

    CAS  Article  PubMed  Google Scholar 

  63. 63.

    Froment P, Touraine P. Thiazolidinediones and fertility in polycystic ovary syndrome (PCOS). PPAR Res. 2006;2006:1–8. doi:10.1155/PPAR/2006/73986.

    Article  Google Scholar 

  64. 64.

    Bruner B, Chad K, Chizen D. Effects of exercise and nutritional counseling in women with polycystic ovary syndrome. Appl Physiol Nutr Metab. 2006;31:384–91. doi:10.1139/h06-007.

    CAS  Article  PubMed  Google Scholar 

  65. 65.

    Ennour-Idrissi K, Maunsell E, Diorio C. Effect of physical activity on sex hormones in women: a systematic review and meta-analysis of randomized controlled trials. Breast Cancer Res. 2015;17:139. doi:10.1186/s13058-015-0647-3.

    Article  PubMed  PubMed Central  Google Scholar 

  66. 66.

    Tarlatzis BC, Fauser B, Thessaloniki EA-S. Consensus on infertility treatment related to polycystic ovary syndrome. Hum Reprod. 2008;23:462–77. doi:10.1093/humrep/dem426.

    Article  Google Scholar 

  67. 67.

    Fukui H, Toyoshima K. Influence of music on steroid hormones and the relationship between receptor polymorphisms and musical ability: a pilot study. Front Psychol. 2013;4:1–8. doi:10.3389/fpsyg.2013.00910.

    Google Scholar 

  68. 68.

    Quiroga Murcia C, Bongard S, Kreutz G. Emotional and neurohumoral responses to dancing tango Argentino: the effects of music and partner. Music Med. 2009;1:14–21. doi:10.1177/1943862109335064.

    Article  Google Scholar 

  69. 69.

    Galletly C, Clark A, Tomlinson L, et al. A group program for obese, infertile women: weight loss and improved psychological health. J Psychosom Obstet Gynaecol. 1996;17:125–8.

    CAS  Article  PubMed  Google Scholar 

  70. 70.

    Surekha T, Himabindu Y, Sriharibabu M, et al. Impact of physical activity on ovarian reserve markers in normal, overweight and obese reproductive age women. Indian J Physiol Pharmacol. 2014;58:162–5.

    CAS  PubMed  Google Scholar 

  71. 71.

    Garavaglia E, Ricci E, Chiaffarino F, et al. Leisure and occupational physical activity at different ages and risk of endometriosis. Eur J Obstet Gynecol Reprod Biol. 2014;183:104–8. doi:10.1016/j.ejogrb.2014.10.031.

    CAS  Article  PubMed  Google Scholar 

  72. 72.

    Rickenlund A, Carlström K, Ekblom B, et al. Hyperandrogenicity is an alternative mechanism underlying oligomenorrhea or amenorrhea in female athletes and may improve physical performance. Fertil Steril. 2003;79:947–55. doi:10.1016/S0015-0282(02)04850-1.

    Article  PubMed  Google Scholar 

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Correspondence to Osnat Hakimi.

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Osnat Hakimi was supported by “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior” (CAPES), Brazilian Ministry of Education (Instituto de Genética e Bioquímica-Universidade Federal de Uberlândia). No other sources of funding were used to assist in the preparation of this article.

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Osnat Hakimi and Luiz-Claudio Cameron declare that they have no conflicts of interest relevant to the content of this review.

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Hakimi, O., Cameron, L. Effect of Exercise on Ovulation: A Systematic Review. Sports Med 47, 1555–1567 (2017). https://doi.org/10.1007/s40279-016-0669-8

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Keywords

  • Luteinizing Hormone
  • Normal Body Mass Index
  • Female Athlete
  • Intense Exercise
  • Vigorous Exercise