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Published in: Sports Medicine 8/2017

01-08-2017 | Systematic Review

Effect of Exercise on Ovulation: A Systematic Review

Authors: Osnat Hakimi, Luiz-Claudio Cameron

Published in: Sports Medicine | Issue 8/2017

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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.
Literature
3.
go back to reference 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 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
8.
12.
go back to reference Orio F, Muscogiuri G, Ascione A, et al. Effects of physical exercise on the female reproductive system. Minerva Endocrinol. 2013;38:305–19.PubMed Orio F, Muscogiuri G, Ascione A, et al. Effects of physical exercise on the female reproductive system. Minerva Endocrinol. 2013;38:305–19.PubMed
14.
go back to reference Loucks AB. Effects of exercise training on the menstrual cycle: existence and mechanisms. Med Sci Sport Exerc. 1990;22:275–80.CrossRef Loucks AB. Effects of exercise training on the menstrual cycle: existence and mechanisms. Med Sci Sport Exerc. 1990;22:275–80.CrossRef
18.
21.
go back to reference 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.PubMed 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.PubMed
22.
go back to reference 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 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
26.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
27.
go back to reference 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.PubMed 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.PubMed
28.
go back to reference 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.CrossRef 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.CrossRef
29.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
30.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
31.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
32.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
33.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
34.
go back to reference Pollock M, Gaesser G, Butcher J, et al. American College of Sports Medicine position stand. Med Sci Sports Exerc. 1998;30:975–91. Pollock M, Gaesser G, Butcher J, et al. American College of Sports Medicine position stand. Med Sci Sports Exerc. 1998;30:975–91.
37.
go back to reference 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. 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.
45.
go back to reference 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.CrossRef 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.CrossRef
47.
go back to reference 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.PubMed 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.PubMed
49.
go back to reference Gambacciani M, Yen SS, Rasmussen DD. GnRH release from the mediobasal hypothalamus: in vitro inhibition by corticotropin-releasing factor. Neuroendocrinology. 1986;43:533–6.CrossRefPubMed Gambacciani M, Yen SS, Rasmussen DD. GnRH release from the mediobasal hypothalamus: in vitro inhibition by corticotropin-releasing factor. Neuroendocrinology. 1986;43:533–6.CrossRefPubMed
53.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
54.
go back to reference 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.PubMed 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.PubMed
56.
go back to reference Norman RJ, Wu R, Stankiewicz MT. 4: Polycystic ovary syndrome. Med J Aust. 2004;180:132–7.PubMed Norman RJ, Wu R, Stankiewicz MT. 4: Polycystic ovary syndrome. Med J Aust. 2004;180:132–7.PubMed
59.
go back to reference Khaskheli MN, Baloch S, Baloch AS. Infertility and weight reduction: influence and outcome. J Coll Physicians Surg Pak. 2013;23:798–801.PubMed Khaskheli MN, Baloch S, Baloch AS. Infertility and weight reduction: influence and outcome. J Coll Physicians Surg Pak. 2013;23:798–801.PubMed
60.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
61.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
62.
go back to reference Guzick DS, Wing R, Smith D, et al. Endocrine consequences of weight loss in obese, hyperandrogenic, anovulatory women. Fertil Steril. 1994;61:598–604.CrossRefPubMed Guzick DS, Wing R, Smith D, et al. Endocrine consequences of weight loss in obese, hyperandrogenic, anovulatory women. Fertil Steril. 1994;61:598–604.CrossRefPubMed
64.
67.
go back to reference 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. 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.
69.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
70.
go back to reference 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.PubMed 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.PubMed
72.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
Metadata
Title
Effect of Exercise on Ovulation: A Systematic Review
Authors
Osnat Hakimi
Luiz-Claudio Cameron
Publication date
01-08-2017
Publisher
Springer International Publishing
Published in
Sports Medicine / Issue 8/2017
Print ISSN: 0112-1642
Electronic ISSN: 1179-2035
DOI
https://doi.org/10.1007/s40279-016-0669-8

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