Childhood and adolescent exposures and the risk of endometriosis
Abstract
BACKGROUND: Because endometriosis is diagnosed predominantly in young women, exposures occurring during childhood or adolescence may have a major impact on the disease. However, potential risk factors during this time period have received little attention. Our objective was to investigate relationships between childhood and adolescent exposures and the risk of endometriosis. METHODS: E3N is a prospective cohort of 98,995 French women aged 40-65 at enrollment in 1990. Follow-up questionnaires were sent every 2-3 years. Using a nested case-control design, we computed odds ratios (ORs) and 95% confidence intervals using unconditional logistic regression models. RESULTS: A total of 2684 endometriosis cases were reported as surgically ascertained among the 75,918 included women. There were inverse relationships of endometriosis risk with menarcheal age (test for trend, P < 0.0001) and with menstrual cycle length before 17 years of age (test for trend, P = 0.06), whereas menstrual cycle regularity before 17 years of age was not associated with risk. There were modest associations of endometriosis risk with exposure to pet animals (OR = 1.12 [95% confidence interval =1.02-1.22]) or living in a farm for 3 or more consecutive months during childhood (1.12 [1.02-1.24]), although with no link to any specific type of farm animal. In addition, there were positive linear associations between endometriosis risk and level of indoor exposure to passive smoking during childhood (up to 1.34 [1.09-1.64] with several hours exposure a day), experiencing food deprivation during World War II (1.34 [0.94-1.91]), and walking activity at 8-15 years of age (1.17 [1.05-1.31] for 5+ hours a week). CONCLUSIONS: This large study suggests that some exposures during childhood or adolescence may influence the risk of endometriosis. Further research is needed to confirm and better understand these relationships.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Age at menarche and menstrual cycle characteristics have been robustly associated with endometriosis.
“as they [1] have been robustly associated with endometriosis (34–38)”
Cites
Giudice, L. C., & Kao, L. C. (2004) · The Lancet · doi:10.1016/s0140-6736(04)17403-5 · Cited by 3,166 · see citing works
Sinaii, N. (2002) · Human Reproduction · doi:10.1093/humrep/17.10.2715 · Cited by 620 · see citing works
Missmer, S. A. (2004) · American Journal of Epidemiology · doi:10.1093/aje/kwh275 · Cited by 616 · see citing works
The antiestrogenic effect of cigarette smoking in women
Baron, J. A., Vecchia, C. L., & Levi, F. (1990) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(90)90420-c · Cited by 590 · see citing works
Li, Y., He, Y., Qi, L., Jaddoe, V. W., Feskens, E. J. M., Yang, X., Ma, G., & Hu, F. B. (2010) · Diabetes · doi:10.2337/db10-0385 · Cited by 384 · see citing works
The Relation of Endometriosis to Menstrual Characteristics, Smoking, and Exercise
Cramer, D. W. (1986) · JAMA: The Journal of the American Medical Association · doi:10.1001/jama.1986.03370140102032 · Cited by 367 · see citing works
Laufer, M. R., Goitein, L., Bush, M., Cramer, D. W., & Emans, S. J. (1997) · Journal of Pediatric and Adolescent Gynecology · doi:10.1016/s1083-3188(97)70085-8 · Cited by 305 · see citing works
High plasma concentrations of di-(2-ethylhexyl)-phthalate in women with endometriosis
Cobellis, L. (2003) · Human Reproduction · doi:10.1093/humrep/deg254 · Cited by 296 · see citing works
A prospective study of dietary fat consumption and endometriosis risk
Missmer, S. A., Chavarro, J. E., Malspeis, S., Bertone-Johnson, E. R., Hornstein, M. D., Spiegelman, D., Barbieri, R. L., Willett, W. C., & Hankinson, S. E. (2010) · Human Reproduction · doi:10.1093/humrep/deq044 · Cited by 251 · see citing works
Immune interactions in endometriosis
Herington, J. L., Bruner‐Tran, K. L., Lucas, J. A., & Osteen, K. G. (2011) · Expert Review of Clinical Immunology · doi:10.1586/eci.11.53 · Cited by 226 · see citing works
Epidemiological characteristics in women with and without endometriosis in the Yale series
Matalliotakis, I., Cakmak, H., Fragouli, Y., Goumenou, A., Mahutte, N., & Arıcı, A. (2008) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-007-0479-1 · Cited by 176 · see citing works
Anthropometric Measurements and Body Silhouette of Women
Téhard, B., van Liere, M. J., Com-Nougué, C., & Clavel‐Chapelon, F. (2002) · Journal of the American Dietetic Association · doi:10.1016/s0002-8223(02)90381-0 · Cited by 173 · see citing works
Self-citationExposure to the Chinese Famine in Early Life and the Risk of Metabolic Syndrome in Adulthood
Li, Y., Jaddoe, V. W. V., Qi, L., He, Y., Wang, D., Lai, J., Zhang, J., Fu, P. P., Yang, X., & Hu, F. B. (2011) · Diabetes Care · doi:10.2337/dc10-2039 · Cited by 170 · see citing works
Menstrual Cycle Characteristics and the Risk of Endometriosis
Darrow, S. L., Vena, J., Batt, R., Zielezny, M., Michalek, A., & Selman, S. (1993) · Epidemiology · doi:10.1097/00001648-199303000-00009 · Cited by 169 · see citing works
Epidemiologic determinants of endometriosis: A hospital-based case-control study
Signorello, L. B., Harlow, B. L., Cramer, D. W., Spiegelman, D. L., & Hill, J. A. (1997) · Annals of Epidemiology · doi:10.1016/s1047-2797(97)00017-3 · Cited by 163 · see citing works
Endometriosis in an Adolescent Population: The Emory Experience
Reese, K. A., Reddy, S., & Rock, J. A. (1996) · Journal of Pediatric and Adolescent Gynecology · doi:10.1016/s1083-3188(96)70021-9 · Cited by 160 · see citing works
Epidemiology of endometriosis in a Norwegian county
Moen, M. H., & Schei, B. (1997) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.3109/00016349709024584 · Cited by 154 · see citing works
The accuracy of reports of weight: children's recall of their parents' weights 15 years earlier.
Sørensen, T. I. A., Stunkard, A. J., Teasdale, T. W., et al. (1983) · PubMed · Cited by 129 · see citing works
Reddy, B. S., Rozati, R., Reddy, S., Kodampur, S., Reddy, P. P., & Reddy, R. (2006) · Fertility and Sterility · doi:10.1016/j.fertnstert.2005.08.037 · Cited by 128 · see citing works
Heilier, J.-F., Nackers, F., Verougstraete, V., Tonglet, R., Lison, D., & Donnez, J. (2005) · Fertility and Sterility · doi:10.1016/j.fertnstert.2005.04.001 · Cited by 126 · see citing works
Sadeu, J. C., Hughes, C. L., Agarwal, S. K., & Foster, W. G. (2010) · Critical Reviews in Toxicology · doi:10.3109/10408444.2010.493552 · Cited by 116 · see citing works
Evolutionary origins of insulin resistance: a behavioral switch hypothesis
Watve, M. G., & Yajnik, C. S. (2007) · BMC Evolutionary Biology · doi:10.1186/1471-2148-7-61 · Cited by 114 · see citing works
Portrait, F. R. M., Teeuwiszen, E., & Deeg, D. J. H. (2011) · Social Science & Medicine · doi:10.1016/j.socscimed.2011.04.005 · Cited by 113 · see citing works
Epidemiology of endometriosis in infertile women
Matorras, R., Rodíquez, F., Pijoan, J. I., Ramón, O., de Terán, G. G., & Rodríguez-Escudero, F. (1995) · Fertility and Sterility · doi:10.1016/s0015-0282(16)57293-8 · Cited by 109 · see citing works
Heilier, J.-F., Donnez, J., Nackers, F., Rousseau, R., Verougstraete, V., Rosenkranz, K., Donnez, O., Grandjean, F., Lison, D., & Tonglet, R. (2006) · Environmental Research · doi:10.1016/j.envres.2006.04.004 · Cited by 108 · see citing works
Characteristics Related to the Prevalence of Minimal or Mild Endometriosis in Infertile Women
Bérubé, S., Marcoux, S., & Maheux, R. (1998) · Epidemiology · doi:10.1097/00001648-199809000-00006 · Cited by 104 · see citing works
Vitonis, A. F., Baer, H. J., Hankinson, S. E., Laufer, M. R., & Missmer, S. A. (2010) · Human Reproduction · doi:10.1093/humrep/deq039 · Cited by 98 · see citing works
Cromi, A., Ghezzi, F., Raffaelli, R., Bergamini, V., Siesto, G., & Bolis, P. F. (2009) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.6320 · Cited by 95 · see citing works
van Noord, P. A. H., & Kaaks, R. (1991) · Annals of Human Biology · doi:10.1080/03014469100001402 · Cited by 85 · see citing works
Dioxin-like PCBs and Endometriosis
Bruner‐Tran, K. L., & Osteen, K. G. (2010) · Systems Biology in Reproductive Medicine · doi:10.3109/19396360903381023 · Cited by 77 · 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
The link between environmental toxicant exposure and endometriosis
Dana, L. A. (2007) · Frontiers in bioscience · doi:10.2741/2782 · Cited by 64 · see citing works
A validation study on status and age of natural menopause reported in the E3N cohort
Clavel‐Chapelon, F., & Dormoy-Mortier, N. (1998) · Maturitas · doi:10.1016/s0378-5122(98)00020-6 · Cited by 64 · see citing works
Self-citationFarming environment and prevalence of atopy at age 31: prospective birth cohort study in Finland
Lampi, J., Canoy, D., Jarvis, D., Hartikainen, A., Keski‐Nisula, L., Järvelin, M., & Pekkanen, J. (2011) · Clinical & Experimental Allergy · doi:10.1111/j.1365-2222.2011.03777.x · Cited by 61 · see citing works
Childhood exposure to the 1944–1945 Dutch famine and subsequent female reproductive function
Elias, S. G., van Noord, P. A. H., Peeters, P. H. M., et al. (2005) · Human Reproduction · doi:10.1093/humrep/dei090 · Cited by 60 · see citing works
Current Approaches to Optimizing the Treatment of Endometriosis in Adolescents
Laufer, M. R. (2008) · Gynecologic and Obstetric Investigation · doi:10.1159/000148027 · Cited by 59 · see citing works
Zhong, Y., Carmella, S. G., Upadhyaya, P., Hochalter, J. B., Rauch, D., Oliver, A., Jensen, J. A., Hatsukami, D. K., Wang, J., Zimmerman, C. L., et al. (2010) · Chemical Research in Toxicology · doi:10.1021/tx100345x · Cited by 55 · see citing works
Kvaskoff, M., Mesrine, S., Clavel-Chapelon, F., & Boutron-Ruault, M.-C. (2009) · International Journal of Epidemiology · doi:10.1093/ije/dyp175 · Cited by 53 · see citing works
Self-citationOrganochlorine pesticides and endometriosis
Cooney, M., Louis, G. M. B., Hediger, M. L., et al. (2010) · Reproductive Toxicology · doi:10.1016/j.reprotox.2010.05.011 · Cited by 46 · see citing works
Adult Physical Activity and Endometriosis Risk
Vitonis, A. F., Hankinson, S. E., Hornstein, M. D., & Missmer, S. A. (2009) · Epidemiology · doi:10.1097/ede.0b013e3181c15d40 · Cited by 40 · see citing works
Recreational Physical Activity and Endometrioma Risk
Dhillon, P. K. (2003) · American Journal of Epidemiology · doi:10.1093/aje/kwg122 · Cited by 32 · see citing works
The association of atopic diseases with endometriosis.
Nichols, T. R., Lamb, K., & Arkins, J. A. (1987) · PubMed · Cited by 27 · see citing works
Farming in childhood, diet in adulthood and asthma history
Varraso, R., Oryszczyn, M., Mathieu, N., Moual, N. L., Boutron‐Ruault, M., Clavel‐Chapelon, F., Romieu, I., & Kauffmann, F. (2011) · European Respiratory Journal · doi:10.1183/09031936.00115010 · Cited by 25 · see citing works
Self-citationA case-control epidemiologic study of endometriosis.
Han, M., Pan, L., Wu, B.-Z., & Bian, X. (1994) · PubMed · Cited by 20 · see citing works
Martin, L. B., Weil, Z. M., Bowers, S., et al. (2008) · Journal of Comparative Physiology B · doi:10.1007/s00360-008-0253-0 · Cited by 19 · see citing works
N’Gom, P. T., Solon, J. A., Moore, S. E., Morgan, G., Prentice, A. M., & Aspinall, R. (2011) · Journal of Biomedical Science · doi:10.1186/1423-0127-18-41 · Cited by 18 · see citing works
Changes in reproductive indices in Chuvashian women whose maturation was during World War II
Kalichman, L., Malkin, I., & Kobyliansky, E. (2006) · Maturitas · doi:10.1016/j.maturitas.2006.08.005 · Cited by 15 · see citing works
Adolescent Physical Activity and Endometriosis Risk
Vitonis, A. F., Maruti, S. S., Hankinson, S. E., Hornstein, M. D., & Missmer, S. A. (2009) · Journal of Endometriosis and Pelvic Pain Disorders · doi:10.1177/2284026509001003-406 · Cited by 13 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Risk for and consequences of endometriosis: A critical epidemiologic review
Shafrir, A. L., Farland, L. V., Shah, D. K., Harris, H. R., Kvaskoff, M., Zondervan, K., & Missmer, S. A. (2018) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2018.06.001 · Cited by 823 · see citing works
Self-citationVitonis, A. F., Vincent, K., Rahmioglu, N., Fassbender, A., Buck Louis, G. M., Hummelshoj, L., Giudice, L. C., Stratton, P., Adamson, G. D., Becker, C. M., et al. (2014) · Fertility and Sterility · doi:10.1016/j.fertnstert.2014.07.1244 · Cited by 236 · see citing works
Dawson, A., Llauradó Fernandez, M., Anglesio, M., Yong, P. J., & Carey, M. S. (2018) · ecancermedicalscience · doi:10.3332/ecancer.2018.803 · Cited by 106 · see citing works
- Authors
- Kvaskoff, M., Bijon, A., Clavel-Chapelon, F., Mesrine, S., & Boutron-Ruault, M.-C.
- Affiliations
- Brigham and Women's Hospital (US)
- Venue
- Epidemiology
- Published
- 2013-03
- Volume
- 24
- Issue
- 2
- Pages
- 261-269
- ISSN
- 1044-3983 (ISSN-L)
- OpenAlex
- W2033054579
- Cited by
- 47
- References
- 48
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 1 · 2023: 4 · 2022: 3 · 2021: 3 · 2020: 7 · 2019: 2 · 2018: 4 · 2017: 7 · 2016: 3 · 2014: 6 · 2013: 1
- FWCI
- 4.02
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Epidemiology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Menstrual Health and Disorders
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Ectopic Pregnancy Diagnosis and Management
- Keywords
- endometriosis, children's exposure, adolescent exposure, age at menarche, menstrual cycle length, menstrual cycle regularity, farm exposure, passive smoking, food deprivation, World War II, physical activity, risk factors
- MeSH terms
- Adult, Allergens, Animals, Animals, Domestic, Contraceptives, Oral, Endometriosis, Environmental Exposure, Female, France, Humans, Menarche, Menstrual Cycle, Middle Aged, Progestins, Prospective Studies, Surveys and Questionnaires, Risk Factors, Cohort Studies, Logistic Models, Case-Control Studies
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
