Risk factors for diminished ovarian reserve in women: Current state of the problem
https://doi.org/10.29413/ABS.2024-9.3.6
Abstract
Ovarian reserve is the basis of female fertility. The main markers of ovarian reserve are the level of anti-Mullerian hormone and the number of antral follicles. In addition to the natural age-related loss of follicles, many women experience a premature diminished ovarian reserve associated with a number of factors. This can be caused by both various diseases and environmental factors, lifestyle, and social aspects.
The aim of this review was to examine the influence of external factors on the ovarian reserve and women fertility. A systematic analysis of data from modern scientific literature, domestic and foreign sources was carried out. The search involved such resources as PubMed, MEDLINE, Science Direct, eLibrary, Scopus, Cyberleninka. A detailed analysis of the influence of environmental pollution, lifestyle (sleep, nutrition, physical activity), previous surgeries, bad habits, obesity, psychological and social factors on the ovarian reserve and reproductive function of women was carried out. Significantly diminished ovarian reserve was noted with low sleep quality, excessive physical activity, and an unbalanced diet poor with animal proteins. Regular consumption of alcohol, smoking and exposure to certain chemical environmental pollutants cause premature follicle apoptosis and the onset of menopause. Circadian dysrhythmia, chronic stress and obesity can lead to the ovarian menstrual cycle disorders and the development of infertility in women. Previous parovarium surgeries are a significant risk factor for diminished ovarian reserve. Further population-based studies are needed to determine the precise mechanisms of influence of various factors on female fertility.
Keywords
About the Authors
S. V. ZotovRussian Federation
Semen V. Zotov – Dr. Sc. (Med.), Head Physician, Obstetrician-Gynecologist, Reproductologist
Uritskogo str. 20, Novosibirsk 630099
V. V. Likhacheva
Russian Federation
Victoria V. Likhacheva – Dr. Sc. (Med.), Docent, Professor a the Department of Obstetrics and Gynecology
Stroiteley ave, 5, Novokuznetsk 654005
P. Yu. Motyreva
Russian Federation
Polina Yu. Motyreva – Senior Biologist
Kommunisticheskaya str. 17/1, Novosibirsk 630099
O. V. Azarova
Russian Federation
Olga V. Azarova – Dr. Sc. (Med.), Reproductologist, Head of the ART Department
Kutuzova str. 17A, Novokuznetsk 654041
B. I. Ayzikovich
Russian Federation
Boris I. Ayzikovich – Dr. Sc. (Med.), Professor at the Department of Fundamental Medicine
Pirogova str. 1, Novosibirsk 630090
References
1. Delbaere I, Verbiest S, Tydén T. Knowledge about the impact of age on fertility: A brief review. Ups J Med Sci. 2020; 125(2): 167-174. doi: 10.1080/03009734.2019.1707913
2. Wang Y, Yuan Y, Meng D, Liu X, Gao Y, Wang F, et al. Effects of environmental, social and surgical factors on ovarian reserve: Implications for age-relative female fertility. Int J Gynaecol Obstet. 2021; 154(3): 451-458. doi: 10.1002/ijgo.13567
3. Ge W, Li L, Dyce PW, De Felici M, Shen W. Establishment and depletion of the ovarian reserve: Physiology and impact of environmental chemicals. Cell Mol Life Sci. 2019; 76(9): 1729-1746. doi: 10.1007/s00018-019-03028-1
4. Sutton P, Woodruff TJ, Perron J, Stotland N, Conry JA, Miller MD, et al. Toxic environmental chemicals: The role of reproductive health professionals in preventing harmful exposures. Am J Obstet Gynecol. 2012; 207(3): 164-173. doi: 10.1016/j.ajog.2012.01.034
5. Vabre P, Gatimel N, Moreau J, Gayrard V, Picard-Hagen N, Parinaud J, et al. Environmental pollutants, a possible etiology for premature ovarian insufficiency: A narrative review of animal and human data. Environ Health. 2017; 16(1): 37. doi: 10.1186/s12940-017-0242-4
6. Sharara F, Seifer D, Flaws J. Environmental toxicants and female reproduction. Fertil Steril. 1998; 70(4): 613-622. doi: 10.1016/S0015-0282(98)00253-2
7. Luderer U. Ovarian toxicity from reactive oxygen species. Vitam Horm. 2014; 94: 99-127. doi: 10.1016/B978-0-12-800095-3.00004-3
8. Tokmak A, Yildirim G, Sarikaya E, Cinar M, Bogdaycioglu N, Yilmaz FM. Increased oxidative stress markers may be a promising indicator of risk for primary ovarian insufficiency: A cross-sectional case control study. Rev Bras Ginecol Obstet. 2015; 37: 411-416. doi: 10.1590/SO100-720320150005397
9. Richardson MC, Guo M, Fauser BC, Macklon NS. Environmental and developmental origins of ovarian reserve. Hum Reprod Update. 2014; 20(3): 353-369. doi: 10.1093/humupd/dmt057
10. Gore AC, Chappell VA, Fenton SE, Flaws JA, Nadal A, Prins GS, et al. EDC-2: The Endocrine Society’s second scientific statement on endocrine-disrupting chemicals. Endocr Rev. 2015; 36: E1-E150. doi: 10.1210/er.2015-1093
11. Bergman A, Heindel J, Jobling S, Kidd K, Zoeller RT. State of the science of endocrine disrupting chemicals, 2012. Toxicol Lett. 2013; 211(Suppl): S3. doi: 10.1016/j.toxlet.2012.03.020
12. di Renzo GC, Conry JA, Blake J, Defrancesco MS, Denicola N, Martin JN, et al. International Federation of Gynecology and Obstetrics (FIGO) opinion on reproductive health impacts of exposure to toxic environmental chemicals. Int J Gynecol Obstet. 2015; 131: 219-225. doi: 10.1016/j.ijgo.2015.09.002
13. Zhurabekova GA, Balmagambetova AD, Zhumagulova SS, Kuschanova AM, Abdelazim IA. Markers of the ovarian reserve of women living in the Aral Sea zone. West Kazakhstan Medical Journal. 2015; 4(48): 33-37. (In Russ.).
14. Bedrick BS, Broughton DE, Schulte M, Boots CE, Eskew AM, Jungheim ES. Physical activity is negatively associated with antral follicle count. Fertil Steril. 2017; 107: E32-E33. doi: 10.1016/j.fertnstert.2017.02.061
15. Hart RJ. Physiological aspects of female fertility: Role of the environment, modern lifestyle, and genetics. Physiol Rev. 2016; 96(3): 873-909. doi: 10.1152/physrev.00023.2015
16. Grisotto G, Langton CR, Li Y, Bertone-Johnson ER, Baden MY, Franco OH, et al. Association of plant-based diet and early onset of natural menopause. Menopause. 2022; 29(7): 861-867. doi: 10.1097/GME.0000000000001985
17. Morris DH, Jones ME, Schoemaker MJ, McFadden E, Ashworth A, Swerdlow AJ. Body mass index, exercise, and other lifestyle factors in relation to age at natural menopause: Analyses from the breakthrough generations study. Am J Epidemiol. 2012; 175(10): 998-1005. doi: 10.1093/aje/kwr447
18. Purdue-Smithe AC, Whitcomb BW, Manson JE, Hankinson SE, Rosner BA, Troy LM, et al. A prospective study of dairy-food intake and early menopause. Am J Epidemiol. 2019; 188(1): 188-196. doi: 10.1093/aje/kwy212
19. Romijn JA, Adriaanse R, Brabant G, Prank K, Endert E, Wiersinga WM. Pulsatile secretion of thyrotropin during fasting: A decrease of thyrotropin pulse amplitude. J Clin Endocrinol Metab. 1990; 70: 1631-1636. doi: 10.1210/jcem-70-6-1631
20. Vengrzhinovskaya OI, Fadeeva MI. Association of circadian dysrhythmia with the genesis of metabolic disorders. Modern Science: Actual Problems of Theory and Practice. Series: Natural and Technical Sciences. 2021; 4(2): 75-80. (In Russ.). doi: 10.37882/2223-2966.2021.04-2.02
21. Lee A, Ader M, Bray GA, Bergman RN. Diurnal variation in glucose tolerance. Cyclic suppression of insulin action and insulin secretion in normal-weight, but not obese, subjects. Diabetes. 1992; 41(6): 750-759. doi: 10.2337/diab.41.6.750
22. Anothaisintawee T, Lertrattananon D, Thamakaison S. Later chronotype is associated with higher hemoglobin A1c in prediabetes patients. Chronobiol Int. 2017; 34: 393-402. doi: 10. 1080/07420528.2017.1279624
23. Kim W, Lee J, Ha J, Jo K, Lim DJ, Lee JM, et al. Association between sleep duration and subclinical thyroid dysfunction based on nationally representative data. J Clin Med. 2019; 8(11): 2010. doi: 10.3390/jcm8112010
24. Smetnik AA, Sazonova AI. The impact of the thyroid and its disease on female reproductive function. Obstetrics and Gynegology. 2019; 3: 46-52. (In Russ.). doi: 10.18565/aig.2019.3.46-52
25. Koyyada A, Orsu P. Role of hypothyroidism and associated pathways in pregnancy and infertility: Clinical insights. Tzu Chi Med J. 2020; 32(4): 312-317. doi: 10.4103/tcmj.tcmj_255_19
26. Kloss JD, Perlis ML, Zamzow JA, Culnan EJ, Gracia CR. Sleep, sleep disturbance, and fertility in women. Sleep Med Rev. 2015; 22: 78-87. doi: 10.1016/j.smrv.2014.10.005
27. Penzias A, Bendikson K, Butts S. Smoking and infertility: A committee opinion. Fertil Steril. 2018; 110(4): 611-618. doi: 10.1016/j.fertnstert.2018.06.016
28. Schuh-Huerta SM, Johnson NA, Rosen MP, Sternfeld B, Cedars MI, Reijo Pera RA. Genetic variants and environmental factors associated with hormonal markers of ovarian reserve in Caucasian and African American women. Hum Reprod. 2012; 27(2): 594-608. doi: 10.1093/humrep/der391
29. Soldin OP, Makambi KH, Soldin SJ, O’Mara DM. Steroid hormone levels associated with passive and active smoking. Steroids. 2011; 76: 653-659. doi: 10.1016/j.steroids.2011.02.042
30. Kee K, Flores M, Cedars MI, Reijo Pera RA. Human primordial germ cell formation is diminished by exposure to environmental toxicants acting through the AHR signaling pathway. Toxicol Sci. 2010; 117: 218-224. doi: 10.1093/toxsci/kfq179
31. Aizikovich BI, Aizikovich IV, Verba OYu, Zotov SV, Medvedeva IV. Outcomes of ART in women suffering from tobacco addiction. International Journal of Applied and Fundamental Research. 2012; (2): 69. (In Russ.).
32. Ajzikovitch IV, Ajzikovitch BI, Zotov SV, Medvedeva IV. The influence of women smoking on the quality of oocytes and results of IVF methods. Vestnik of Novosibirsk State University. Series: Biology, Clinical Medicine. 2012; 10(2): 165-168. (In Russ.).
33. Perez MF, Mead EL, Atuegwu NC, Mortensen EM, Goniewicz M, Oncken C. Biomarkers of toxicant exposure and inflammation among women of reproductive age who use electronic or conventional cigarettes. J Womens Health (Larchmt). 2021; 30(4): 539-550. doi: 10.1089/jwh.2019.8075
34. Dai H, Benowitz NL, Achutan C, Farazi PA, Degarege A, Khan AS. Exposure to toxicants associated with use and transitions between cigarettes, e-cigarettes, and no tobacco. JAMA Netw Open. 2022; 5(2): e2147891. doi: 10.1001/jamanetworkopen.2021.47891
35. Mikkelsen EM, Riis AH, Wise LA, Hatch EE, Rothman KJ, Cueto HT, et al. Alcohol consumption and fecundability: Prospective Danish cohort study. BMJ. 2016; 354: i4262. doi: 10.1136/bmj.i4262
36. Fan D, Liu LI, Xia Q. Female alcohol consumption and fecundability: A systematic review and dose-response meta-analysis. Sci Rep. 2017; 7(1): 13815. doi: 10.1038/s41598-017-14261-8
37. Ng M, Fleming T, Robinson M. Global, regional, and national prevalence of overweight and obesity in children and adults during 1980–2013: A systematic analysis for the Global Burden of Disease Study 2013. Lancet. 2014; 384(9945): 766-781. doi: 10.1016/S0140-6736(14)60460-8
38. Ramlau-Hansen CH, Thulstrup AM, Nohr EA. Subfecundity in overweight and obese couples. Hum Reprod. 2007; 22(6): 1634-1637. doi: 10.1093/humrep/dem035
39. Grigoryan OR, Mikheev RK, Andreeva EN, Dedov II. Ovarian reserve in women with obesity. Obesity and Metabolism. 2019; 16(3): 69-75. (In Russ.). doi: 10.14341/omet9862
40. Bellver J, Ayllón Y, Ferrando M. Female obesity impairs in vitro fertilization outcome without affecting embryo quality. Fertil Steril. 2010; 93(2): 447-454. doi: 10.1016/j.fertnstert.2008.12.032
41. Durmanova AK, Otarbayev NK, Kaiyrlykyzy A, Zhangazieva KK, Ibrayeva ZN, Donenbayeva GB, et al. Ovarian reserve and adipokine levels in reproductive-aged obese women. Terapevticheskii arkhiv. 2016; 88(10): 46-50. (In Russ.). doi: 10.17116/terarkh2016881046-5
42. Wang Y, Wu L, Yang Z, Xu R, Duan Y, Lin J, et al. Association of body mass index with serum anti-Müllerian hormone and inhibin B levels among 8323 women attending a reproductive medical center: A cross-sectional study. Endocrine. 2022; 75(1): 284-292. doi: 10.1007/s12020-021-02839-2
43. Kriseman M, Mills C, Kovanci E, Sangi-Haghpeykar H, Gibbons W. Antimullerian hormone levels are inversely associated with body mass index (BMI) in women with polycystic ovary syndrome. J Assist Reprod Genet. 2015; 32(9): 1313-1316. doi: 10.1007/s10815-015-0540-0
44. Gaskins AJ, Rich-Edwards JW, Missmer SA, Rosner B, Chavarro JE. Association of fecundity with changes in adult female weight. Obstet Gynecol. 2015; 126: 850-858. doi: 10.1097/AOG.0000000000001030
45. Rosstat. Demographic yearbook of Russia. 2021. (In Russ.). URL: https://rosstat.gov.ru/folder/210/document/13207 дата доступа: 21.08.2022.
46. Martin JA, Hamilton BE, Osterman M, Driscoll AK. Births: Final data for 2019. National vital statistics reports: From the Centers for Disease Control and Prevention, National Center for Health Statistics. Nat Vital Stat Syst. 2021; 70(2): 1-51.
47. Molina-García L, Hidalgo-Ruiz M, Cocera-Ruíz EM, Conde-Puertas E, Delgado-Rodríguez M, Martínez-Galiano JM. The delay of motherhood: Reasons, determinants, time used to achieve pregnancy, and maternal anxiety level. PloS One. 2019; 14(12): e0227063. doi: 10.1371/journal.pone.0227063
48. Panay N, Kalu E. Management of premature ovarian failure. Best Pract Res Clin Obstet Gynaecol. 2009; 23(1): 129-140. doi: 10.1016/j.bpobgyn.2008.10.008
49. Huang H, Zhao J, Jiang L, Xie Y, Xia Y, Lv R, et al. Paeoniflorin improves menopause depression in ovariectomized rats under chronic unpredictable mild stress. Int J Clin Experim Med. 2015; 8(4): 5103-5111.
50. Xi W, Mao H, Cui Z, Yao H, Shi R, Gao Y. Scream soundinduced chronic psychological stress results in diminished ovarian reserve in adult female rat. Endocrinol. 2022; 163(6): bqac042. doi: 10.1210/endocr/bqac04
51. Patel A, Sharma P, Kumar P, Binu VS. Sociocultural determinants of infertility stress in patients undergoing fertility treatments. J Human Reprod Sci. 2018; 11(2): 172-179. doi: 10.4103/jhrs.JHRS_134_17
52. Watson D, Clark LA, Tellegen A. Development and validation of brief measures of positive and negative affect: The PANAS scales. J Pers Soc Psychol. 1988; 54(6): 1063-1070. doi: 10.1037/0022-3514.54.6.1063
53. Bleil ME, Adler NE, Pasch LA, Sternfeld B, Gregorich SE, Rosen MP, et al. Depressive symptomatology, psychological stress and ovarian reserve: A role for psychological factors in ovarian aging? Menopause. 2012; 19(11): 1176-1185. doi: 10.1097/gme.0b013e31825540d8
54. Ayzikovich BI, Zotov SV, Kuleshov VM, Motyreva PYu, Filimonov SN, Likhacheva VV. Treatment of endometrioid ovarian cysts concerning fertility: A review of modern methods. Mother and Baby in Kuzbass. 2021; (2): 32-39. (In Russ.). doi: 10.24411/2686-7338-2021-10020
55. Song T, Kim WY, Lee KW, Kim KH. Effect on ovarian reserve of hemostasis by bipolar coagulation versus suture during laparoendoscopic single-site cystectomy for ovarian endometriomas. J Minim Invasive Gynecol. 2015; 22: 415-420. doi: 10.1016/j.jmig.2014.11.002
56. Muzii L, Achilli C, Lecce F, Bianchi A, Franceschetti S, Marchetti C, et al. Second surgery for recurrent endometriomas is more harmful to healthy ovarian tissue and ovarian reserve than first surgery. Fertil Steril. 2015; 103(3): 738-743. doi: 10.1016/j.fertnstert.2014.12.101
57. Muzii L, Di Tucci C, Galati G, Mattei G, Chinè A, Cascialli G, et al. Endometriosis-associated infertility: Surgery or IVF? Minerva Obstet Gynecol. 2021; 73(2): 226-232. doi: 10.23736/S2724-606X.20.04765-6
58. Zotov SV, Motyreva PYu, Kuleshov VM, Ayzikovich BI, Likhacheva VV, Filimonov SN. Advantages of reducing therapy of endometriod cysts by comparison with laparoscopic excision before IVF programs. Medicine in Kuzbass. 2021; 20(1): 26-31. (In Russ.) doi: 10.24411/2687-0053-2021-10005
Review
For citations:
Zotov S.V., Likhacheva V.V., Motyreva P.Yu., Azarova O.V., Ayzikovich B.I. Risk factors for diminished ovarian reserve in women: Current state of the problem. Acta Biomedica Scientifica. 2024;9(3):69-78. (In Russ.) https://doi.org/10.29413/ABS.2024-9.3.6