Risk factors for endometriosis

DOI

https://dx.doi.org/10.18565/aig.2020.2.68-75

Tumanova U.N., Shchegolev A.I., Pavlovich S.V., Serov V.N.
1) Academician V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology, and Perinatology, Ministry of Health of Russia, Moscow, Russia; 2) I.M. Sechenov First Moscow State Medical University, Ministry of Health of Russia, Moscow, Russia

The increased incidence of endometriosis is due both to improved diagnosis, a larger number of surgical interventions and the increasing influence of various risk factors. The paper analyzes the data available in the literature on risk factors for endometriosis. It is indicated that the risk factors for endometriosis depend on a female patient’s age from the antenatal period to adulthood, as well as have certain differences in various countries and regions. The modifiable factors include diet, environmental influences, parity, breastfeeding duration, and physical activity. Other factors, such as genetic factors, early menarche, and the length of the menstrual cycle, are considered unmodifiable. It is emphasized that the presence of several risk factors can serve as the basis for classifying these women as a separate risk group, as well as for making a special more thorough examination to identify the foci of endometriosis.

lactation

menarche

parity

risk factor

endometriosis

Full text (in Russian)

Moen M.H., Schei B. Epidemiology of endometriosis in a Norwegian county. Acta Obstet Gynecol Scand. 1997; 76: 559–62. doi: 10.3109/00016349709024584
Meuleman C., Vandenabeele B., Fieuws S., Spiessens C, Timmerman D, D’Hooghe T. High prevalence of endometriosis in infertile women with normal ovulation and normospermic partners. Fertil Steril. 2009; 92: 68–74.doi: 10.1016/j.fertnstert.2008.04.056
Liston W.A., Bradford W.P., Downie J., Kerr M.G. Laparoscopy in a general gynecologic unit. Am J Obstet Gynecol. 1972; 113: 672–7. doi: 0002-9378(72)90636-9
Buck Louis G.M., Hediger M.L., Peterson C.M., Croughan M., Sundaram R., Stanford J., et al. Incidence of endometriosis by study population and diagnostic method: the ENDO study. Fertil Steril. 2011; 96: 360–5. doi: 10.1016/j.fertnstert.2011.05.087
Giudice L.C., Kao L.C. Endometriosis. Lancet. 2004; 364 (9447): 1789–99. doi: 10.1016/S0140-6736(04)17403-5
Yamamoto A., Johnstone E.B., Bloom M.S., Huddleston H.G., Fujimoto V.Y. A higher prevalence of endometriosis among Asian women does not contribute to poorer IVF outcomes. J Assist Reprod Genet. 2017; 34: 765–74. doi: 10.1007/s10815-017-0919-1
Hudelist G., Fritzer N., Thomas A., Niehues C., Oppelt P., Haas D., et al. Diagnostic delay for endometriosis in Austria and Germany: causes and possible consequences. Hum Reprod. 2012; 27: 3412–6. doi: 10.1093/humrep/des316
Щеголев А.И., Быков А.Г., Туманова У.Н., Павлович С.В. Эндометриоз и развитие опухолей. Акушерство и гинекология. 2016; 11: 49-56. [Shchegolev A.I., Bykov A.G., Tumanova U.N., Pavlovich S.V. Endometriosis and the development of tumors. Akusherstvo i ginekologiya / Obstetrics and gynecology. 2016; 11: 49–56. (in Russian)].
Harada T., ed. Endometriosis. Pathogenesis and treatment. Springer, 2014. 477 p. doi: 10.1007/978-4-431-54421-0
Vannuccini S., Lazzeri L., Orlandini C., Tosti C., Clifton V.L., Petraglia F. Potential influence of in utero and early neonatal exposures on the later development of endometriosis. Fertil Steril. 2016; 105(4): 997–1002. doi: 10.1016/j.fertnstert.2015.12.127
Kashima K., Ishimaru T., Okamura H., Suginami H., Ikuma K., Murakami T. et al. Familial risk among Japanese patients with endometriosis. Int J Gynaecol Obstet. 2004; 84: 61–4. doi: 10.1016/s0020-7292(03)00340-0
Vigano P., Somigliana E., Vignali M., Busacca M., Blasio A.M. Genetics of endometriosis: current status and prospects. Front Biosci. 2007; 1: 3247–55. doi: 10.2741/2308
Пономаренко И.В., Полоников А.В., Чурносов М.И. Молекулярные механизмы и факторы риска развития эндометриоза. Акушерство и гинекология. 2019; 3: 26-31. [Ponomarenko I.V., Polonikov A.V., Churnosov M.I. Molecular mechanisms of and risk factors for endometriosis. Akusherstvo i ginekologiya/Obstetrics and gynecology. 2019; 3: 26–31. (in Russian)]. doi: 10.18565/aig.2019.3.26-31
Rahmioglu N., Nyholt D.R., Morris A.P., Missmer S.A., Montgomery G.W., Zondervan K.T. Genetic variants underlying risk of endometriosis: insights from meta-analysis of eight genome-wide association and replication datasets. Hum Reprod Update. 2014; 20: 702–16. doi: 10.1093/humupd/dmu015
Yen C.F., Kim M.R., Lee C.L. Epidemiologic Factors Associated with Endometriosis in East Asia. Gynecol Minim Invasive Ther. 2019; 8(1): 4–11. doi: 10.4103/GMIT.GMIT_83_18
Cho Y.J., Kim N.H., Jeong K.A., Lee J.Y., Moon H.S., Kim H.L., et al. Association between MMP‑2 and TIMP‑2 gene polymorphisms and advanced‑stage endometriosis in Korean women. Am J Reprod Immunol. 2013; 69: 73–84. doi: 10.1111/aji.12020
Shan K., Xiao‑Wei M., Na W., Xiu‑Feng Z., Deng‑Gui W., Wei G., et al. Association of three single nucleotide polymorphisms of the E‑cadherin gene with endometriosis in a Chinese population. Reproduction. 2007; 134: 373–8. doi: 10.1530/REP-07-0104
Birt J.A., Taylor K.H., Davis J.W., Sharpe-Timms K.L. Developmental exposure of fetal ovaries and fetal germ cells to endometriosis in an endometriosis model causes differential gene expression in the preimplantation embryos of the first-generation and second-generation embryos. Fertil Steril. 2013; 100: 1436–43. doi: 10.1016/j.fertnstert.2013.07.007
Stilley J.A., Woods-Marshall R., Sutovsky M., Sutovsky P., Sharpe-Timms K.L. Reduced fecundity in female rats with surgically induced endometriosis and in their daughters: a potential role for tissue inhibitors of metalloproteinase 1. Biol Reprod. 2009; 80: 649–56. doi: 10.1095/biolreprod.108.073411
Patel B., Elguero S., Thakore S., , Dahoud W, Bedaiwy M, Mesiano S. Role of nuclear progesterone receptor isoforms in uterine pathophysiology. Hum Reprod Update. 2015; 21: 155–73. doi: 10.1093/humupd/dmu056
Maclaran K., Agarwal N., Odejinmi F. Co-existence of uterine myomas and endometriosis in women undergoing laparoscopic myomectomy: risk factors and surgical implications. J Minim Invasive Gynecol. 2014; 21: 1086–90. doi: 10.1016/j.jmig.2014.05.013
Missmer S.A., Hankinson S.E., Spiegelman D., Barbieri R.L., Michels K.B., Hunter D.J. In utero exposures and the incidence of endometriosis. Fertil Steril. 2004; 82: 1501–8. doi: 10.1016/j.fertnstert.2004.04.065
Mazzuca M.Q., Wlodek M.E., Dragomir N.M., Parkington HC, Tare M. Uteroplacental insufficiency programs regional vascular dysfunction and alters arterial stiffness in female offspring. J Physiol. 2010; 588: 1997–2010.doi: 10.1113/jphysiol.2010.187849
Gondret F., Pere M.C., Tacher S., Dare S., Trefeu C., le Huberou–Luron I., et al. Spontaneous intrauterine growth restriction modulates the endocrine status and the developmental expression of genes in porcine fetal and neonatal adipose tissue. Gen Comp Endocrinol. 2013; 1: 208–16. doi: 10.1016/j.ygcen.2013.09.018
Farland L.V., Missmer S.A., Bijon A., Gusto G., Gelot A., Clavel-Chapelon F., et al. Associations among body size across the life course, adult height and endometriosis. Hum Reprod. 2017; 32: 1732–42. doi: 10.1093/humrep/dex207
Yi K.W., Shin J.H., Park M.S., Kim T., Kim S.H., Hur J.Y. Association of body mass index with severity of endometriosis in Korean women. Int J Gynaecol Obstet. 2009; 105: 39–42. doi: 10.1016/j.ijgo.2008.11.001
Raimondo D., Mabrouk M., Zannoni L., Arena A., Zanello M., Benfenati A., et al. Severe ureteral endometriosis: frequency and risk factors. J Obstet Gynaecol. 2018; 38: 257–60. doi: 10.1080/01443615.2017.1349083
Shah D.K., Correia K.F., Vitonis A.F., Missmer S.A. Body size and endometriosis: results from 20 years of follow-up within the Nurses’ Health Study II prospective cohort. Hum Reprod. 2013; 28: 1783–92. doi: 10.1093/humrep/det120
McCann S.E., Freudenheim J.L., Darrow S.L., Batt R.E., Zielezny M.A. Endometriosis and body fat distribution. Obstet Gynecol. 1993; 82: 545–9. PMID: 8377980
Cramer D.W., Wilson E., Stillman R.J., Berger M.J., Belisle S., Schiff I., et al. The relation of endometriosis to menstrual characteristics, smoking, and exercise. JAMA. 1986; 255: 1904–8. PMID: 3951117
Saha R., Kuja-Halkola R., Tornvall P., Marions L. Reproductive and lifestyle factors associated with endometriosis in a large cross-sectional population sample. J Womens Health (Larchmt). 2017; 26: 152–8. doi: 10.1089/jwh.2016.5795
Missmer S.A., Hankinson S.E., Spiegelman D., Barbieri R.L., Malspeis S., Willett W.C., et al. Reproductive history and endometriosis among premenopausal women. Obstet Gynecol. 2004; 104: 965–74. doi: 10.1097/01.AOG.0000142714.54857.f8
Vercellini P., Eskenazi B., Consonni D., Somigliana E., Parazzini F., Abbiati A., et al. Oral contraceptives and risk of endometriosis: a systematic review and meta-analysis. Hum Reprod Update. 2011; 17: 159–70. doi: 10.1093/humupd/dmq042
Paris K., Aris A. Endometriosis-associated infertility: A decade’s trend study of women from the Estrie Region of Quebec, Canada. Gynecol Endocrinol. 2010; 26: 838–42. doi: 10.3109/09513590.2010.487590
Prescott J., Farland L.V., Tobias D.K., Gaskins A.J., Spiegelman D., Chavarro J.E., et al. A prospective cohort study of endometriosis and subsequent risk of infertility. Hum Reprod. 2016; 31: 1475–82. doi: 10.1093/humrep/dew085
Upson K., Sathyanarayana S., Scholes D., Holt V.L. Early-life factors and endometriosis risk. Fertil Steril. 2015; 104: 964–71. doi: 10.1016/j.fertnstert.2015.06.040
Dubova E.A., Pavlov K.A., Lyapin V.M., Shchyogolev A.I., Sukhikh G.T. Vascular endothelial growth factor and its receptors in the placental villi of pregnant patients with pre-eclampsia. Bull. Exp. Biol. Med. 2013; 154(6): 792–5. doi: 10.1007/s10517-013-2058-8
Воднева Д.Н., Романова В.В., Дубова Е.А., Павлов К.А., Шмаков Р.Г., Щеголев А.И. Клинико-морфологические особенности ранней и поздней преэклампсии. Акушерство и гинекология. 2014; 2: 35–40. [Vodneva D.N., Romanova V.V., Dubova E.A., Pavlov K.A., Shmakov R.G., Shchegolev A.I. The clinical and morphological features of early and late-onset preeclampsia. Akusherstvo i ginekologiya/Obstetrics and gynecology. 2014; 2: 35–40.(in Russian)]/
Jefferson W.N., Patisaul H.B., Williams C.J. Reproductive consequences of developmental phytoestrogen exposure. Reproduction 2012; 143: 247–60. doi: 10.1530/REP-11-0369
McCarver G., Bhatia J., Chambers C., Clarke R., Etzel R., Foster W., et al. NTP-CERHR expert panel report on the developmental toxicity of soy infant formula. Birth Defects Res. B. Dev. Reprod. Toxicol. 2011; 92: 421–68. doi: 10.1002/bdrb.20314
Mvondo M.A., Ekenfack J.D., Essono S.M., Namekong H.S., Awounfack S.F., Laschke M.W., et al. Soy intake since the prepubertal age may contribute to the pathogenesis of endometriosis in adulthood. J Med Food. 2019; 22(6): 631–8. doi: 10.1089/jmf.2018.0160
Hoffman C.S., Small C.M., Blanck H.M., Tolbert P., Rubin C., Marcus M. Endometriosis among women exposed to polybrominated biphenyls. Ann Epidemiol. 2007; 17: 503–10. doi: 10.1016/j.annepidem.2006.11.005
Eskenazi B., Mocarelli P., Warner M., Samuels S., Vercellini P., Olive D., et al. Serum dioxin concentrations and endometriosis: a cohort study in Seveso, Italy. Environ Health Perspect. 2002; 110: 629–34. doi: 10.1289/ehp.02110629
Yasui T., Hayashi K., Nagai K., Mizunuma H., Kubota T., Lee J.S., et al. Risk profiles for endometriosis in Japanese women: Results from a repeated survey of self-reports. J Epidemiol. 2015; 25: 194–203. doi: 10.2188/jea.JE20140124
Kvaskoff M., Bijon A., Clavel-Chapelon F., Mesrine S., Boutron-Ruault M.C. Childhood and adolescent exposures and the risk of endometriosis. Epidemiology. 2013; 24: 261–9. doi: 10.1097/EDE.0b013e3182806445
Missmer S.A., Chavarro J.E., Malspeis S., Bertone-Johnson E.R., Hornstein M.D., Spiegelman D., et al. A prospective study of dietary fat consumption and endometriosis risk. Hum Reprod. 2010; 25: 1528–35. doi: 10.1093/humrep/deq044
Savaris A.L., do Amaral V.F. Nutrient intake, anthropometric data and correlations with the systemic antioxidant capacity of women with pelvic endometriosis. Eur J Obstet Gynecol Reprod Biol. 2011; 158: 314–8. doi: 10.1016/j.ejogrb.2011.05.014
Shafrir A.L., Farland L.V., Shah D.K., Harris H.R, Kvaskoff M., Zondervan K. et al. Risk for and consequences of endometriosis: A critical epidemiologic review. Best Pract Res Clin Obstet Gynaecol. 2018; 51: 1–15. doi: 10.1016/j.bpobgyn.2018.06.001
Chiaffarino F., Bravi F., Cipriani S., Parazzini F., Ricci E., Vigano P., et al. Coffee and caffeine intake and risk of endometriosis: a meta-analysis. Eur J Nutr. 2014; 53: 1573–9. doi: 10.1007/s00394-014-0662-7
Heilier J.F., Donnez J., Nackers F., Parazzini F., Ricci E., Vigano P., et al. Environmental and host-associated risk factors in endometriosis and deep endometriotic nodules: a matched case-control study. Environ Res. 2007; 103: 121–9. doi: 10.1016/j.envres.2006.04.004
Vitonis A.F., Hankinson S.E., Hornstein M.D., Missmer S.A. Adult physical activity and endometriosis risk. Epidemiology. 2010; 21: 16–23. doi: 10.1097/EDE.0b013e3181c15d40
Schernhammer E.S., Vitonis A.F., Rich-Edwards J., Missmer S.A. Rotating nightshift work and the risk of endometriosis in premenopausal women. Am J Obstet Gynecol. 2011; 205: 476 e1-8. doi: 10.1016/j.ajog.2011.06.002

Received 27.09.2019

Accepted 04.10.2019

Ulyana N Tumanova., PhD, senior researcher at the Department of Morbid Anatomy, National Medical Research Center of Obstetrics, Gynecology, and Perinatology named after Academician V.I. Kulakov, Ministry of Health of Russia. Tel: +74955314444. E-mail: ashegolev@oparina4.ru
117997, Russia, Moscow, Ac. Oparina str. 4.
Aleksandr I. Shchegolev, MD, professor, head of the Department of Morbid Anatomy, National Medical Research Center of Obstetrics, Gynecology, and Perinatology named after Academician V.I. Kulakov, Ministry of Health of Russia. Tel: +74955314444. E-mail: ashegolev@oparina4.ru
117997, Russia, Moscow, Ac. Oparina str. 4.
Stanislav V. Pavlovich, PhD, National Medical Research Center of Obstetrics, Gynecology, and Perinatology named after Academician V.I. Kulakov, Ministry of Health of Russia; head of training, Professor of the Department of Obstetrics, Gynecology and Perinatology, First Moscow State Medical University named after I.M. Sechenov of the Ministry of Health of the Russian Federation (Sechenov University), Тel.: +74954387287. E.mail: @oparina4.ru
117997, Russia, Moscow, Ac. Oparina str. 4.
Vladimir N. Serov, MD, professor, academician of the Russian Academy of Sciences, chief researcher, National Medical Research Center of Obstetrics, Gynecology, and Perinatology named after Academician V.I. Kulakov, Ministry of Health of Russia. Тel.: +74954387287. E.mail: v_serov@oparina4.ru
117997, Russia, Moscow, Ac. Oparina str. 4.

For citation: Tumanova U.N., Shchegolev A.I., Pavlovich S.V.,
Serov V.N. Risk factors for endometriosis.
Akusherstvo i Ginekologiya/ Obstetrics and gynecology. 2020;2: 68-75 (In Russian).
https://dx.doi.org/10.18565/aig.2020.2.68-75

Risk factors for endometriosis

Tumanova U.N., Shchegolev A.I., Pavlovich S.V., Serov V.N.

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