Early-life factors, in-utero exposures and endometriosis risk: a meta-analysis
Open accessAbstract
This meta-analysis aimed to offer a general picture of the available data on the effects of early-life factors on the risk of developing endometriosis in adult life. An advanced, systematic search of the online medical databases PubMed, EMBASE and CINAHL was limited to full-length manuscripts published in English in peer-reviewed journals up to February 2019. Log of relative risk (RR) was employed to calculate the pooled effect sizes using both fixed and random effects modelling and I-squared tests to assess heterogeneity. Funnel plots were used to investigation publication bias. The meta-analysis was registered in PROSPERO (ID CRD42019138668). Six studies that included a total of 2360 women affected by endometriosis were analysed. The pooled results showed that the risk of developing endometriosis in adult life was significantly increased by being born prematurely (logRR 0.21, 95% CI -0.03 to 0.40), having a low birthweight (logRR 0.35, 95% CI -0.15 to 0.54), being formula-fed (logRR 0.65, 95% CI -0.35 to 0.95) and having been exposed to diethylstilbestrol (DES) in utero (logRR 0.65, 95% CI 0.26 to 1.04. Among intrauterine and early neonatal exposures, prematurity, birthweight, formula feeding and DES were risk factors for the development of endometriosis in adult life.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Prenatal exposure to diethylstilbestrol (DES) notably increases endometriosis risk in offspring.
“For example, prenatal exposure to the potent synthetic estrogen diethylstilbestrol (DES) notably increases endometriosis risk in offspring.45”
From Prenatal Origins of Endometriosis Pathology and Pain: Reviewing the Evidence of a Role for Low Testosterone (2023) · cites this paper as [45]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Bias in meta-analysis detected by a simple, graphical test
Egger, M., Smith, G. D., Schneider, M., & Minder, C. (1997) · BMJ · doi:10.1136/bmj.315.7109.629 · Cited by 56,722 · see citing works
Preferred reporting items for systematic reviews and meta-analyses: the PRISMA Statement.
(2009) · PubMed Central · Cited by 44,859 · see citing works
Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & the PRISMA Group* (2009) · Annals of Internal Medicine · doi:10.7326/0003-4819-151-4-200908180-00135 · Cited by 37,554 · see citing works
Funnel plots for detecting bias in meta-analysis
Sterne, J. A. C., & Egger, M. (2001) · Journal of Clinical Epidemiology · doi:10.1016/s0895-4356(01)00377-8 · Cited by 3,779 · see citing works
INFANT MORTALITY, CHILDHOOD NUTRITION, AND ISCHAEMIC HEART DISEASE IN ENGLAND AND WALES
BARKER, D. (1986) · The Lancet · doi:10.1016/s0140-6736(86)91340-1 · Cited by 2,892 · see citing works
Improved tests for a random effects meta‐regression with a single covariate
Knapp, G., & Hartung, J. (2003) · Statistics in Medicine · doi:10.1002/sim.1482 · Cited by 2,075 · see citing works
Peters, J. L., Sutton, A. J., Jones, D. R., Abrams, K. R., & Rushton, L. (2008) · Journal of Clinical Epidemiology · doi:10.1016/j.jclinepi.2007.11.010 · Cited by 2,053 · see citing works
Endometriosis: pathogenesis and treatment
Vercellini, P., Viganò, P., Somigliana, E., & Fedele, L. (2014) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2013.255 · Cited by 1,940 · see citing works
Self-citationEskenazi, B., & Warner, M. L. (1997) · Obstetrics and Gynecology Clinics of North America · doi:10.1016/s0889-8545(05)70302-8 · Cited by 1,617 · see citing works
Fetal and infant origins of adult disease
Barker, D. J. P. (2001) · Monatsschrift Kinderheilkunde · doi:10.1007/s001120170002 · Cited by 1,042 · see citing works
The Epidemiology of Endometriosis
CRAMER, D. W., & MISSMER, S. A. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb02761.x · Cited by 539 · see citing works
Activation of the hypothalamic-pituitary-gonadal axis in infancy: minipuberty
Kuiri-Hänninen, T., Sankilampi, U., & Dunkel, L. (2014) · Hormone Research in Paediatrics · doi:10.1159/000362414 · Cited by 470 · see citing works
Deeply infiltrating endometriosis: pathogenetic implications of the anatomical distribution
Chapron, C., Chopin, N., Borghese, B., Foulot, H., Dousset, B., Vacher-Lavenu, M. C., Vieira, M., Hasan, W., & Bricou, A. (2006) · Human Reproduction · doi:10.1093/humrep/del079 · Cited by 459 · see citing works
Newbold, R. R., Padilla‐Banks, E., & Jefferson, W. N. (2006) · Endocrinology · doi:10.1210/en.2005-1164 · Cited by 432 · see citing works
Role of nuclear progesterone receptor isoforms in uterine pathophysiology
Patel, B., Elguero, S., Thakore, S., Dahoud, W., Bedaiwy, M., & Mesiano, S. (2015) · Human Reproduction Update · doi:10.1093/humupd/dmu056 · Cited by 353 · see citing works
Sapkota, Y., Steinthorsdottir, V., Morris, A. P., Fassbender, A., Rahmioglu, N., De Vivo, I., Buring, J. E., Zhang, F., Edwards, T. L., Jones, S., et al. (2017) · Nature Communications · doi:10.1038/ncomms15539 · Cited by 344 · see citing works
Strom, B. L. (2001) · JAMA · doi:10.1001/jama.286.7.807 · Cited by 313 · see citing works
Statistical methods for dealing with publication bias in meta‐analysis
Jin, Z., Zhou, X., & He, J. (2014) · Statistics in Medicine · doi:10.1002/sim.6342 · Cited by 252 · see citing works
Rahmioglu, N., Nyholt, D. R., Morris, A. P., Missmer, S. A., Montgomery, G. W., & Zondervan, K. T. (2014) · Human Reproduction Update · doi:10.1093/humupd/dmu015 · Cited by 238 · see citing works
Reproductive History and Endometriosis Among Premenopausal Women
Missmer, S. A., Hankinson, S. E., Spiegelman, D., Barbieri, R. L., Malspeis, S., Willett, W. C., & Hunter, D. J. (2004) · Obstetrics & Gynecology · doi:10.1097/01.aog.0000142714.54857.f8 · Cited by 237 · see citing works
Newbold, R. R. (1995) · Environmental Health Perspectives · doi:10.1289/ehp.95103s783 · Cited by 233 · see citing works
The principles and methods behind EFSA's Guidance on Uncertainty Analysis in Scientific Assessment
Benford, D., Halldorsson, T., Jeger, M., Knutsen, H., More, S., Naegeli, H., Noteborn, H., Ockleford, C., Ricci, A., Rychen, G., et al. (2018) · EFSA journal. European Food Safety Authority · doi:10.2903/j.efsa.2018.5122 · Cited by 230 · see citing works
Developmental Origins of Health and Disease: Environmental Exposures
Swanson, J. M., Entringer, S., Buß, C., & Wadhwa, P. D. (2009) · Seminars in Reproductive Medicine · doi:10.1055/s-0029-1237427 · Cited by 214 · see citing works
Perinatal environment and its influences on metabolic programming of offspring
Tamashiro, K. L., & Moran, T. H. (2010) · Physiology & Behavior · doi:10.1016/j.physbeh.2010.04.008 · Cited by 195 · see citing works
Reproductive effects in male and female rats of neonatal exposure to genistein
Nagao, T., Yoshimura, S., Saito, Y., Nakagomi, M., Usumi, K., & Ono, H. (2001) · Reproductive Toxicology · doi:10.1016/s0890-6238(01)00141-1 · Cited by 195 · see citing works
Postnatal Developmental Changes in the Pituitary-Ovarian Axis in Preterm and Term Infant Girls
Kuiri‐Hänninen, T., Kallio, S., Seuri, R. M., Tyrväinen, E., Liakka, A., Tapanainen, J. S., Sankilampi, U., & Dunkel, L. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-1502 · Cited by 194 · see citing works
In utero exposures and the incidence of endometriosis
Missmer, S. A., Hankinson, S. E., Spiegelman, D., Barbieri, R. L., Michels, K. B., & Hunter, D. J. (2004) · Fertility and Sterility · doi:10.1016/j.fertnstert.2004.04.065 · Cited by 184 · see citing works
Jefferson, W. N., Padilla‐Banks, E., & Newbold, R. R. (2005) · Biology of Reproduction · doi:10.1095/biolreprod.105.041277 · Cited by 183 · see citing works
Borghese, B., Mondon, F., Noël, J., Fayt, I., Mignot, T.-M., Vaiman, D., & Chapron, C. (2008) · Molecular Endocrinology · doi:10.1210/me.2008-0322 · Cited by 150 · see citing works
Differentially expressed genes in eutopic and ectopic endometrium of women with endometriosis
Meola, J., Silva, J. C. R. E., Dentillo, D. B., Silva, W. A., Veiga-Castelli, L. C., Bernardes, L. Â. D. S., Ferriani, R. A., de Paz, C. C. P., Giuliatti, S., & Martelli, L. R. (2009) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.12.058 · Cited by 120 · see citing works
Faber, K. A., & Hughes, C. L. (1993) · Reproductive Toxicology · doi:10.1016/0890-6238(93)90007-t · Cited by 119 · see citing works
Postnatal Ovarian Activation Has Effects in Estrogen Target Tissues in Infant Girls
Kuiri‐Hänninen, T., Haanpää, M., Turpeinen, U., Hämäläinen, E. K., Seuri, R. M., Tyrväinen, E., Sankilampi, U., & Dunkel, L. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2013-1677 · Cited by 107 · see citing works
Increased occurrence of autoimmune disease among women exposed in utero to diethylstilbestrol
Noller, K. L., Blair, P. B., O’Brien, P. C., Melton, L. J., Offord, J. R., Kaufman, R. H., & Colton, T. (1988) · Fertility and Sterility · doi:10.1016/s0015-0282(16)59965-8 · Cited by 102 · see citing works
Early‐life soy exposure and age at menarche
Adgent, M. A., Daniels, J. L., Rogan, W. J., Adair, L. S., Edwards, L. J., Westreich, D. J., Maisonet, M., & Marcus, M. (2011) · Paediatric and Perinatal Epidemiology · doi:10.1111/j.1365-3016.2011.01244.x · Cited by 100 · see citing works
Prenatal and Infant Exposures and Age at Menarche
D’Aloisio, A. A., DeRoo, L. A., Baird, D. D., Weinberg, C. R., & Sandler, D. P. (2013) · Epidemiology · doi:10.1097/ede.0b013e31828062b7 · Cited by 100 · see citing works
Mazzuca, M. Q., Wlodek, M. E., Dragomir, N. M., Parkington, H. C., & Tare, M. (2010) · The Journal of Physiology · doi:10.1113/jphysiol.2010.187849 · Cited by 92 · see citing works
Sato, T., Wang, G., Hardy, M. P., Kurita, T., Cunha, G. R., & Cooke, P. S. (2002) · Endocrinology · doi:10.1210/endo.143.7.8878 · Cited by 92 · see citing works
Barbieri, R. L. (1998) · Fertility and Sterility · doi:10.1016/s0015-0282(98)00189-7 · Cited by 92 · see citing works
Enhanced Activity of the Pituitary-Gonadal Axis in Premature Human Infants*
Tapanainen, J. S., KOIVISTO, M., Vihko, R., & Huhtaniemi, I. T. (1981) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-52-2-235 · Cited by 85 · see citing works
Early-life factors and endometriosis risk
Upson, K., Sathyanarayana, S., Scholes, D., & Holt, V. L. (2015) · Fertility and Sterility · doi:10.1016/j.fertnstert.2015.06.040 · Cited by 84 · see citing works
Is, F., McCarron, G., Markham, R., Resta, T., & Watts, A. (1986) · PubMed · Cited by 82 · see citing works
IRVINE, C. H. G., Shand, N., Fitzpatrick, M. G., & Alexander, S. L. (1998) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/68.6.1462s · Cited by 81 · see citing works
Ostrander, P. L., Mills, K. T., & Bern, H. A. (1985) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/74.1.121 · Cited by 75 · see citing works
Newbold, R. R. (2011) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.110.001057 · Cited by 73 · see citing works
Intrauterine exposures and risk of endometriosis
Louis, G. M. B., Hediger, M. L., & Pena, J. B. (2007) · Human Reproduction · doi:10.1093/humrep/dem338 · Cited by 71 · see citing works
Inside the Endometrial Cell Signaling Subway: Mind the Gap(s)
Makieva, S., Giacomini, E., Ottolina, J., Sanchez, A. M., Papaleo, E., & Viganò, P. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19092477 · Cited by 64 · see citing works
Self-citationFetal Origins of Perinatal Morbidity and/or Adult Disease
Rinaudo, P. F., & LAMB, J. A. (2008) · Seminars in Reproductive Medicine · doi:10.1055/s-0028-1087109 · Cited by 63 · see citing works
Genetics of endometriosis: current status and prospects
Vigano, P. (2007) · Frontiers in Bioscience · doi:10.2741/2308 · Cited by 62 · see citing works
Self-citationShinkawa, O., Furuhashi, N., Fukaya, T., Suzuki, M., Kono, H., & Tachibana, Y. (1983) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-56-6-1327 · Cited by 60 · see citing works
Newbold, R. R. (1995) · Environmental Health Perspectives · doi:10.2307/3432514 · Cited by 58 · see citing works
ACOG practice bulletin number 38, September 2002: perinatal care at the threshold of viability
ACOG Committee on Practice Bulletins—Obstetrics (2002) · Obstetrics and Gynecology · doi:10.1016/s0029-7844(02)02260-3 · Cited by 57 · see citing works
Borghese, B., Sibiude, J., Santulli, P., Lafay Pillet, M.-C., Marcellin, L., Brosens, I., & Chapron, C. (2015) · PLoS ONE · doi:10.1371/journal.pone.0117387 · Cited by 55 · see citing works
Wolff, E. F., Sun, L., Hediger, M. L., Sundaram, R., Peterson, C. M., Chen, Z., & Louis, G. M. B. (2012) · Fertility and Sterility · doi:10.1016/j.fertnstert.2012.11.013 · Cited by 55 · see citing works
Vannuccini, S., Lazzeri, L., Orlandini, C., Tosti, C., Clifton, V. L., & Petraglia, F. (2016) · Fertility and Sterility · doi:10.1016/j.fertnstert.2015.12.127 · Cited by 53 · see citing works
The Relationship between Umbilical Cord Estrogens and Perinatal Characteristics
Hickey, M., Hart, R. J., & Keelan, J. A. (2014) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-13-1321 · Cited by 48 · see citing works
Diethylstilbestrol exposure in utero and endometriosis in infertile females
Stillman, R. J., & Miller, L.-R. C. (1984) · Fertility and Sterility · doi:10.1016/s0015-0282(16)47713-7 · Cited by 44 · see citing works
Conditions in utero and cancer risk
Grotmol, T., Weiderpass, E., & Tretli, S. (2006) · European Journal of Epidemiology · doi:10.1007/s10654-006-9036-7 · Cited by 35 · see citing works
Perinatal Environment and Endometriosis
Somigliana, E., Viganò, P., Abbiati, A., Paffoni, A., Benaglia, L., Vercellini, P., & Fedele, L. (2011) · Gynecologic and Obstetric Investigation · doi:10.1159/000323531 · Cited by 32 · see citing works
Self-citationBack to the Original Question in Endometriosis: Implantation or Metaplasia?
Viganò, P., Somigliana, E., Gentilini, D., Benaglia, L., & Vercellini, P. (2009) · Journal of Endometriosis and Pelvic Pain Disorders · doi:10.1177/228402650900100102 · Cited by 31 · see citing works
Self-citationIntractable primary infertility in women exposed to diethylstilbestrol in utero.
Mj, B., & Mm, A. (1986) · PubMed · Cited by 28 · see citing works
Gondret, F., Pére, M.-C., Tacher, S., Daré, S., Tréfeu, C., Huërou‐Luron, I. L., & Louveau, I. (2013) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2013.09.018 · Cited by 23 · see citing works
In utero exposure and endometriosis
Benagiano, G., & Brosens, I. A. (2013) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.3109/14767058.2013.814630 · Cited by 22 · see citing works
Cooke, P. S., Borsdorf, D. C., Ekman, G. C., Doty, K., Clark, S. G., Dziuk, P. J., & Bartol, F. F. (2012) · Theriogenology · doi:10.1016/j.theriogenology.2012.05.028 · Cited by 22 · see citing works
Early Infant Nutrition and Metabolic Programming: What Are the Potential Molecular Mechanisms?
Ruchat, S.-M., Bouchard, L., & Hivert, M. (2014) · Current Nutrition Reports · doi:10.1007/s13668-014-0088-0 · Cited by 18 · see citing works
Liede, A., PAL, T., MITCHELL, M., & NAROD, S. A. (2000) · Journal of Medical Genetics · doi:10.1136/jmg.37.10.794 · Cited by 11 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The adverse role of endocrine disrupting chemicals in the reproductive system
Pan, J., Liu, P., Yu, X., Zhang, Z., & Liu, J. (2024) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1324993 · Cited by 197 · see citing works
“The risk of developing EMs in adult life was signi fi cantly increased by exposure to DES in utero (76).”
BackgroundThe evolutionary biology of endometriosis
Dinsdale, N., Nepomnaschy, P., & Crespi, B. (2021) · Evolution, Medicine, and Public Health · doi:10.1093/emph/eoab008 · Cited by 53 · see citing works
“First, prenatal exposure to the potent synthetic estrogen diethylstilbestrol (DES) is significantly associated with higher endometriosis risk in offspring [88].”
BackgroundVercellini, P., Bandini, V., Viganò, P., Stefano, G. D., Merli, C. E. M., & Somigliana, E. (2023) · Human Reproduction · doi:10.1093/humrep/dead229 · Cited by 49 · see citing works
“…2020; Salliss et al., 2021; Muraoka et al. , 2023; Yang et al. , 2023), or other features of modern life that may influence the risk of these diseases (Missmer and Cramer, 2003; Vigan � o et al. , 2004; Ottolina et al. , 2020; Sasamoto et al. , 2020; Shafrir et al. , 2018; Koninckx et al. , 2021a).”
BackgroundSelf-citationZhang, Y., & Ma, N. (2021) · Frontiers in Medicine · doi:10.3389/fmed.2021.680833 · Cited by 45 · see citing works
“We also found that breastfeeding was positively associated with the risk of endometriosis although this may be affected by a certain amount of bias (37).”
BackgroundEndometriosis and environmental factors: A critical review
Coiplet, E., Courbière, B., Agostini, A., Boubli, L., Bretelle, F., & Netter, A. (2022) · Journal of Gynecology Obstetrics and Human Reproduction · doi:10.1016/j.jogoh.2022.102418 · Cited by 38 · see citing works
Developmental exposure to phytoestrogens found in soy: New findings and clinical implications
Suen, A. A., Kenan, A. C., & Williams, C. J. (2021) · Biochemical Pharmacology · doi:10.1016/j.bcp.2021.114848 · Cited by 38 · see citing works
Szukiewicz, D. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241512195 · Cited by 36 · see citing works
An update for endometriosis management: a position statement
Petraglia, F., Vannuccini, S., Santulli, P., Marcellin, L., & Chapron, C. (2024) · Journal of Endometriosis and Uterine Disorders · doi:10.1016/j.jeud.2024.100062 · Cited by 25 · see citing works
Multigenerational endometriosis : consequence of fetal exposure to diethylstilbestrol ?
Gaspari, L., Soyer‐Gobillard, M., Paris, F., Kalfa, N., Hamamah, S., & Sultan, C. (2021) · Environmental Health · doi:10.1186/s12940-021-00780-5 · Cited by 18 · see citing works
Crespi, B. J., & Evans, S. F. (2023) · Journal of Pain Research · doi:10.2147/jpr.s389166 · Cited by 17 · see citing works
“For example, prenatal exposure to the potent synthetic estrogen diethylstilbestrol (DES) notably increases endometriosis risk in offspring.(45) Prenatal exposure to the anti-androgenic chemical bisphenol A (BPA), results in shorter AGDs among female rats,(46) and, in mice, it has been linked with earlier first estrus…”
BackgroundEndometriosis and comorbidities: molecular mechanisms and clinical implications
Petraglia, F., Vannuccini, S., Donati, C., Jeljeli, M. M., Bourdon, M., & Chapron, C. (2025) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2025.09.002 · Cited by 22 · see citing works
Piani, L. L., Chiaffarino, F., Cipriani, S., Viganò, P., Somigliana, E., & Parazzini, F. (2022) · Scientific Reports · doi:10.1038/s41598-022-21173-9 · Cited by 15 · see citing works
Self-citationRecent insights explaining susceptibility to endometriosis—From genetics to environment
Pais, A. S., & Almeida‐Santos, T. (2023) · WIREs Mechanisms of Disease · doi:10.1002/wsbm.1624 · Cited by 14 · see citing works
Rossi, M., Seidita, I., Vannuccini, S., Prisinzano, M., Donati, C., & Petraglia, F. (2023) · Vitamins and hormones · doi:10.1016/bs.vh.2023.01.007 · Cited by 16 · see citing works
Berndt, S., Ribeiro, L. P., Rowlands, I. J., Doust, J. A., & Mishra, G. D. (2024) · Fertility and Sterility · doi:10.1016/j.fertnstert.2024.10.048 · Cited by 9 · see citing works
Liu, X., Ding, D., Shen, M., Yan, D., & Guo, S. (2023) · Biomedicines · doi:10.3390/biomedicines11102618 · Cited by 9 · see citing works
“…with the report that prenatal exposure to diethylstilbestrol (DES), a synthetic non-steroid estrogen, resulted in an increased risk of developing endometriosis in adult life [56] and with the report of a possible multigenerational and likely transgenerational effect of fetal exposition to DES [57].”
BackgroundCardio‐Metabolic Risk Profile of Women With Endometriosis: A Population‐Based Study
Naz, M. S. G., Noroozzadeh, M., Ardebili, S. N., Mousavi, M. A., Azizi, F., & Tehrani, F. R. (2024) · Endocrinology Diabetes & Metabolism · doi:10.1002/edm2.70008 · Cited by 11 · see citing works
Youseflu, S., Savabi-Esfahani, M., Jafarabadi, M. A., & Maleki, A. (2022) · Breastfeeding Medicine · doi:10.1089/bfm.2022.0126 · Cited by 7 · see citing works
“34 Also, in 2016, Olsˇarova´ and Mishra conducted a systematic review of 11 observational studies to evaluate effect of early-life factors such as preterm birth, maternal smoking, passive smoking, in utero exposure to diethylstilbestrol, and breastfeeding on the risk of endometriosis.”
Brønd, M., Breintoft, K., Forman, A., Henriksen, T. B., Ramlau‐Hansen, C. H., Rytter, D., & Arendt, L. H. (2023) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1111/aogs.14594 · Cited by 7 · see citing works
Salmeri, N., Casalechi, M., Reschini, M., Orsi, M., Iurlaro, E., Fustinoni, S., Polledri, E., Vercellini, P., Viganò, P., Benaglia, L., et al. (2025) · Reproductive Biology and Endocrinology · doi:10.1186/s12958-025-01467-z · Cited by 3 · see citing works
“However, only indirect indicators of such hyper-estrogenic intrauterine milieu, such as the ano-genital distance, have been evaluated up to now [7–9].”
Self-citationBuggio, L., Reschini, M., Viganò, P., Dridi, D., Galati, G., Chinè, A., Giola, F., Somigliana, E., & Benaglia, L. (2023) · Journal of Clinical Medicine · doi:10.3390/jcm12052040 · Cited by 2 · see citing works
“However, recently, the potential intrauterine origin of endometriosis has been gaining consensus [3,4].”
BackgroundSelf-citationTata Laksana Terkini untuk Endometriosis
Halim, B., & Adiwinata, T. (2021) · MEDICINUS · doi:10.56951/medicinus.v34i3.77 · Cited by 1 · see citing works
Pathogenesis of Endometriosis: Theories of the Cells of Origin and Methods of Dissemination
Martin, D. C. (2022) · Springer eBooks · doi:10.1007/978-3-030-97236-3_3
Estudo epidemiológico da endometriose no Estado do Maranhão
Santos, K. F. A., Cunha, E. R., Mendes, L. E. B., Ribeiro, A. A., Araújo, S. R. M., Pereira, T. V., Pereira, E. F. C., Pereira, S. J., Fróes, J. M. L., & de Souza, M. T. P. (2022) · Research Society and Development · doi:10.33448/rsd-v11i15.37163
FATORES DE RISCO AO DESENVOLVIMENTO DA ENDOMETRIOSE
Silva, A. L. F. E., Loss, A. M. R., dos Santos, M. A., de Oliveira, V. E., Álvares, V. G., & de Aquino, É. C. (2023) · doi:10.56161/sci.ed.20230917c11
A IMPORTÂNCIA DA HIGIENE MENSTRUAL NA PROMOÇÃO DA SAÚDE, UMA REVISÃO DE LITERATURA
Mendonça, C. C. C., da Silva, G. G. B., Pinto, J. M. P., Santos, J. S., Daniel, M. H. B., & de Aquino, É. C. (2023) · doi:10.56161/sci.ed.20230917c2
SILVA, S. R. D., Paier, C. R. K., Júnior, E. M. L., de Moraes, M. O., & Rodrigues, F. A. R. (2023) · doi:10.56161/sci.ed.20230917c4
CANDIDÍASE VULVOVAGINAL DE REPETIÇÃO: POSSÍVEIS CAUSAS E PROFILAXIA
Brito, M. O., Ccapa, R. J. Q., Medeiros, J. L. B., Guimarães, L. H. M., de Morais, G. H. D., & de Aquino, É. C. (2023) · doi:10.56161/sci.ed.20230917c8
ATUAÇÃO DA FISIOTERAPIA NO PUERPÉRIO: UMA REVISÃO INTEGRATIVA
Paiva, E. D. S., Bastos, D. L., Carvalho, R. E. O., de Sousa, L. M., Nascimento, A., de Sousa, I. B. M., de Sousa, F. V. G., de Sousa, M. M., de Vasconcelos, N. F., & Cunha, F. M. A. M. (2023) · doi:10.56161/sci.ed.20230917c6
de Sousa, F. V. G., de Sousa, I. B. M., de Sousa, M. M., Rodrigues, F. A. M., de Souza, E. F., Sousa, J. F., Gomes, D. B., Bezerra, A. M., & Cunha, F. M. A. M. (2023) · doi:10.56161/sci.ed.20230917c1
ANÁLISE DE FORMAS DE TRATAMENTO PARA O TRANSTORNO DISFÓRICO PRÉ-MENSTRUAL: UMA REVISÃO INTEGRATIVA
Laporte, K. F., Oliveira, D. C., da Silva, A. C. S. A., Rodrigues, D. F. D. C., dos Anjos, D. A., de Oliveira, G. A., & da Silva, A. P. (2023) · doi:10.56161/sci.ed.20230917c5
A PRÁTICA DA FISIOTERAPIA NO PROLÁPSO DE ORGÃOS PÉLVICOS: UMA REVISÃO INTEGRATIVA
Paiva, E. D. S., Filho, J. V. D., de Albuquerque, B. J., Mariano, A. L., Sousa, V. K. D. M., de Souza, D. M. L., Nogueira, M. B. R., Barreto, M. D. S., Gonçalves, F. F. L., & Cunha, F. M. A. M. (2023) · doi:10.56161/sci.ed.20230917c3
MÉTODOS CONTRACEPTIVOS: UMA REVISÃO ABRANGENTE DA LITERATURA
dos Santos, M. N., da Cunha, L. G. M., Silva, L. V. D. L., Flores, G. C., Jaime, H. M., Evangelista, I. C., Moraes, A. L. A., & Barbosa, A. F. (2023) · doi:10.56161/sci.ed.20230917c12
CÂNCER DE MAMA E ESTRATÉGIAS PARA UM DIAGNÓSTICO PRECOCE: UMA REVISÃO INTEGRATIVA
Costa, T. E. M. D. L., de Oliveira, C. B., de Lima, C. C. M., da Silva, I. A., Silva, L. A. P., Nascimento, G. K. D. S., Ferreira, C. D. D. S., Pereira, J. V. D. S., CRUZ, L. A. D. M., & Barros, M. B. S. C. (2023) · doi:10.56161/sci.ed.20230917c7
EXAME CITOPATOLÓGICO COMO FORMA DE RASTREAMENTO DO CÂNCER DO COLO DE ÚTERO
Gomes, J. P. D. L., Gomes, K. P. D. L., Barros, M. C. D. S., de Araujo, G. M., Coelho, E. L. D. H., Freitas, T. S. D. S., Luiz, L. M. S., Motta, L. S. V., da Silva, Y. V. N., & da Silva, T. D. P. S. (2023) · doi:10.56161/sci.ed.20230917c10
CERCLAGEM UTERINA COMO MÉTODO PREVENTIVO DO PARTO PREMATURO: UMA REVISÃO DA LITERATURA
Ferreira, D. M. G., Araújo, F. B., Freires, M. E. F., Martins, V. M. P., Alves, G. M. M., Arcanjo, C. C. T., TEIXEIRA, C. R., Oliveira, A. D. N., Costa, A. D. O., & Balreira, I. C. T. (2023) · doi:10.56161/sci.ed.20230917c9
ATUAÇÃO MULTIDISCIPLINAR EM MULHERES COM LOMBALGIA DEVIDO AO AUMENTO DO ÚTERO DURANTE A GRAVIDEZ
de Sousa, M. V. A., Muniz, K. L., Muniz, K. L., Sousa, S. G., de Oliveira, V. B., Sales, P. L. P., dos Santos, N. C., Souza, W. R. D. S., Fé, J. A. D. M. M., de Almeida, S. A., et al. (2023) · doi:10.56161/sci.ed.20230917c13
Villegas‐Echeverri, J. D., Paiva, L. R., Rodríguez, L. F. G., López-Isanoa, J. D., Posada, J. F. D. L. R., Orjuela, J. C., Paúl, C. M., Bastidas-Guarín, C., Flórez, Á. J. E., Cuello-Salcedo, A. M., et al. (2026) · Revista Colombiana de Obstetricia y Ginecología · doi:10.18597/rcog.4671
Panigrahi, S. K., Priyadarshini, V., Pradhan, S., & Behera, S. (2026) · F1000Research · doi:10.12688/f1000research.168615.1
Farhadi‐Azar, M., Naz, M. S. G., Mousavi, M. A., Pezhdam, P., Azizi, F., & Tehrani, F. R. (2026) · Journal of Endocrinological Investigation · doi:10.1007/s40618-026-02993-2
Liao, Y., Shi, Y., Pang, X., Yang, Y., Chen, X., Tang, Z., Xie, P., & Cao, X. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1924352
“In addition, early-life developmental exposures such as low birth weight and in-utero diethylstilbestrol (DES) exposure have been associated with long-term susceptibility to EMs (42, 43).”
Nagy, S., Busznyák, C., Dézsi, C., Gulyás-Oldal, V., Paschali, E., Sallai, D., Gálóczi, I., & Szili, K. (2026) · Frontiers in Reproductive Health · doi:10.3389/frph.2026.1943184
- Authors
- Ottolina, J., Schimberni, M., Makieva, S., Bartiromo, L., Fazia, T., Bernardinelli, L., Viganò, P., Candiani, M., & Gentilini, D.
- Affiliations
- IRCCS Ospedale San Raffaele (IT)
- University of Pavia (IT)
- Corresponding author
- Ottolina, Jessica
- ORCID
- Venue
- Reproductive BioMedicine Online
- Publisher
- Elsevier BV
- Published
- 2020-08
- Volume
- 41
- Issue
- 2
- Pages
- 279-289
- ISSN
- 1472-6483 (ISSN-L)
- OpenAlex
- W3024766212
- Cited by
- 42
- References
- 65
- Citations by year
- 2026: 5 · 2025: 2 · 2024: 4 · 2023: 21 · 2022: 5 · 2021: 5
- FWCI
- 1.14
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Reproductive BioMedicine Online (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Effects and risks of endocrine disrupting chemicals
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Ectopic Pregnancy Diagnosis and Management
- Keywords
- endometriosis, early life risk factors, prenatal exposure, preterm birth, low birth weight, bottle feeding, diethylstilbestrol, neonatal exposure, endometriosis risk
- MeSH terms
- Birth Weight, Endometriosis, Female, Humans, Pregnancy, Prenatal Exposure Delayed Effects, Risk Factors
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review