Endometriosis risk in relation to naevi, freckles and skin sensitivity to sun exposure: the French E3N cohort
Abstract
BACKGROUND: Endometriosis is an important women's health issue, however its aetiology remains unknown. An association between endometriosis and cutaneous melanoma was described, possibly explained through common genetic features. To further investigate this association, we assessed the link between phenotypic traits predisposing to melanoma and the risk of endometriosis. METHODS: Using a case-control design, we analysed data from 97,215 women of the Etude Epidémiologique auprès de femmes de l'Education Nationale study, a cohort of 98,995 French women insured by a national health scheme mostly covering teachers, and aged 40-65 years at inclusion in 1990. Risk estimates were computed using unconditional logistic regression models. RESULTS: After adjustment for potential confounding factors, there was a positive dose-effect relationship between risk of endometriosis (reported as surgically ascertained, n = 4241) and skin sensitivity to sun exposure [moderate: odds ratio (OR) 1.09, 95% confidence interval (CI) 0.99-1.19; high: OR 1.22; 95% CI 1.10-1.36; compared with none; Ptrend < 0.0001], number of naevi (few: OR 1.19, 95% CI 1.05-1.35; many: OR 1.37, 95% CI 1.21-1.55; very many: OR 1.59, 95% CI 1.37-1.83; compared with none; Ptrend < 0.0001) and number of freckles (few: OR 1.08, 95% CI 1.00-1.17; very many/many: OR 1.11, 95% CI 1.03-1.20; compared with none; Ptrend = 0.005). CONCLUSION: This study is, to our knowledge, the first to report a positive dose-effect relationship between the risk of endometriosis and skin sensitivity to sun exposure, and number of naevi and freckles. These data suggest that endometriosis and melanoma may share some genetic features.
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?
Hair and eye color are associated with endometriosis.
“Two questions on hair and eye color, previously associated with endometriosis (71–75) and possibly useful in marking genetic subpopulations, are also included.”
Cites
The Measurement of Observer Agreement for Categorical Data
Landis, J. R., & Koch, G. G. (1977) · Biometrics · doi:10.2307/2529310 · Cited by 81,148 · see citing works
(1990) · Choice Reviews Online · doi:10.5860/choice.27-3338 · Cited by 35,305 · see citing works
Giudice, L. C., & Kao, L. C. (2004) · The Lancet · doi:10.1016/s0140-6736(04)17403-5 · Cited by 3,166 · see citing works
International Journal of Obesity
(2019) · International Journal of Obesity · doi:10.1038/41366.1476-5497 · Cited by 2,092 · see citing works
Melanin pigmentation in mammalian skin and its hormonal regulation
Slominski, A., Tobin, D. J., Shibahara, S., & Wortsman, J. (2004) · Physiological Reviews · doi:10.1152/physrev.00044.2003 · Cited by 2,015 · see citing works
Meta-analysis of risk factors for cutaneous melanoma: I. Common and atypical naevi
Gandini, S., Sera, F., Cattaruzza, M. S., Pasquini, P., ABENI, D. D., Boyle, P., & Melchi, C. F. (2004) · European Journal of Cancer · doi:10.1016/j.ejca.2004.10.015 · Cited by 838 · see citing works
Gandini, S., Sera, F., Cattaruzza, M. S., Pasquini, P., Zanetti, R., Masini, C., Boyle, P., & Melchi, C. F. (2005) · European Journal of Cancer · doi:10.1016/j.ejca.2005.03.034 · Cited by 786 · see citing works
Bulletti, C., Coccia, M. E., Battistoni, S., & Borini, A. (2010) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-010-9436-1 · Cited by 776 · see citing works
Missmer, S. A. (2004) · American Journal of Epidemiology · doi:10.1093/aje/kwh275 · Cited by 616 · see citing works
PTEN signaling pathways in melanoma
Wu, H., Goel, V., & Haluska, F. G. (2003) · Oncogene · doi:10.1038/sj.onc.1206451 · Cited by 482 · see citing works
Fournier, A., Berrino, F., Ríboli, E., Avenel, V., & Clavel‐Chapelon, F. (2004) · International Journal of Cancer · doi:10.1002/ijc.20710 · Cited by 400 · see citing works
Self-citationEndometriosis: cost estimates and methodological perspective
Simoens, S., Hummelshoj, L., & D'Hooghe, T. (2007) · Human Reproduction Update · doi:10.1093/humupd/dmm010 · Cited by 357 · see citing works
A prospective study of pigmentation, sun exposure, and risk of cutaneous malignant melanoma in women
Veierod, M. B., Weiderpass, E., Thorn, M., Hansson, J., Lund, E., Armstrong, B., & Adami, H.-O. (2003) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djg075 · Cited by 333 · see citing works
Genetics of melanoma predisposition
Hayward, N. K. (2003) · Oncogene · doi:10.1038/sj.onc.1206445 · Cited by 321 · see citing works
Endometriosis and the risk of cancer with special emphasis on ovarian cancer
Melin, A., Sparén, P., Persson, I., & Bergqvist, A. (2006) · Human Reproduction · doi:10.1093/humrep/dei462 · Cited by 306 · see citing works
Somigliana, E., Viganò, P., Parazzini, F., Stoppelli, S., Giambattista, E., & Vercellini, P. (2006) · Gynecologic Oncology · doi:10.1016/j.ygyno.2005.11.033 · Cited by 296 · see citing works
The biological actions of estrogens on skin
Thornton, M. J. (2002) · Experimental Dermatology · doi:10.1034/j.1600-0625.2002.110601.x · Cited by 248 · see citing works
Zhu, G., Duffy, D. L., Eldridge, A., Grace, M., Mayne, C., O'Gorman, L. E., Aitken, J. F., Neale, M. C., Hayward, N. K., Green, A. C., et al. (1999) · The American Journal of Human Genetics · doi:10.1086/302494 · Cited by 237 · see citing works
The melanocortin-1-receptor gene is the major freckle gene
Bastiaens, M. T. (2001) · Human Molecular Genetics · doi:10.1093/hmg/10.16.1701 · Cited by 234 · see citing works
The search for genes contributing to endometriosis risk
Montgomery, G. W., Nyholt, D. R., Zhao, Z. Z., Treloar, S. A., Painter, J. N., Missmer, S. A., Kennedy, S. H., & Zondervan, K. T. (2008) · Human Reproduction Update · doi:10.1093/humupd/dmn016 · Cited by 211 · see citing works
Treloar, S. A., Wicks, J., Nyholt, D. R., Montgomery, G. W., Bahlo, M., Smith, V. E., Dawson, G., Mackay, I., Weeks, D. E., Bennett, S. T., et al. (2005) · The American Journal of Human Genetics · doi:10.1086/432960 · Cited by 195 · 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-citationINCIDENCE OF PELVIC ENDOMETRIOSIS IN ROCHESTER, MINNESOTA, 1970–1979
Houston, D. E., Noller, K. L., Melton, L. J., Selwyn, B. J., & Hardy, R. J. (1987) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a114634 · Cited by 167 · see citing works
The risk of cancer and the role of parity among women with endometriosis
Melin, A., Sparén, P., & Bergqvist, A. (2007) · Human Reproduction · doi:10.1093/humrep/dem209 · Cited by 152 · see citing works
Farquhar, C. M. (2007) · BMJ · doi:10.1136/bmj.39073.736829.be · Cited by 146 · see citing works
Possible involvement of hMLH1, p16INK4a and PTEN in the malignant transformation of endometriosis
Martini, M., Ciccarone, M., Garganese, G., Maggiore, C., Evangelista, A., Rahimi, S., Zannoni, G. F., Vittori, G., & Larocca, L. M. (2002) · International Journal of Cancer · doi:10.1002/ijc.10715 · Cited by 134 · see citing works
Causes of Infertility as Predictors of Subsequent Cancer Risk
Brinton, L. A., Westhoff, C. L., Scoccia, B., Lamb, E. J., Althuis, M. D., Mabie, J. E., & Moghissi, K. S. (2005) · Epidemiology · doi:10.1097/01.ede.0000164812.02181.d5 · Cited by 134 · see citing works
Oestrogen receptor‐β expression in melanocytic lesions
Schmidt, A. N., Nanney, L. B., Boyd, A. S., King, L. E., & Ellis, D. L. (2006) · Experimental Dermatology · doi:10.1111/j.1600-0625.2006.00502.x · Cited by 133 · 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
Estrogen Receptor-α Methylation Predicts Melanoma Progression
Mori, T., Martinez, S. R., O'Day, S. J., Morton, D. L., Umetani, N., Kitago, M., Tanemura, A., Nguyen, S. L., Tran, A. N., Wang, H.-J., et al. (2006) · Cancer Research · doi:10.1158/0008-5472.can-06-0801 · Cited by 114 · see citing works
Development and reliability of a brief skin cancer risk assessment tool
Glanz, K., Schoenfeld, E. R., Weinstock, M. A., Layi, G., Kidd, J. M., & Shigaki, D. M. (2003) · Cancer Detection and Prevention · doi:10.1016/s0361-090x(03)00094-1 · Cited by 114 · see citing works
EPIDEMIOLOGY OF MELANOCYTIC NEVI
Green, A. C., & Swerdlow, A. J. (1989) · Epidemiologic Reviews · doi:10.1093/oxfordjournals.epirev.a036037 · Cited by 110 · see citing works
Reproducibility of a Self-Administered Questionnaire for Assessment of Melanoma Risk
Westerdahl, J., Anderson, H., Olsson, H. L., et al. (1996) · International Journal of Epidemiology · doi:10.1093/ije/25.2.245 · Cited by 76 · see citing works
A genome-wide scan for naevus count: linkage to CDKN2A and to other chromosome regions
Zhu, G., Montgomery, G. W., James, M. R., Trent, J. M., Hayward, N. K., Martin, N. G., & Duffy, D. L. (2006) · European Journal of Human Genetics · doi:10.1038/sj.ejhg.5201729 · Cited by 72 · see citing works
OXHOLM, D., Knudsen, U. B., Kryger‐Baggesen, N., & Ravn, P. (2007) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1080/00016340701619407 · Cited by 72 · see citing works
Goumenou, A. G., Arvanitis, D. A., Matalliotakis, I., Koumantakis, E. E., & Spandidos, D. A. (2001) · Fertility and Sterility · doi:10.1016/s0015-0282(00)01663-0 · Cited by 71 · 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-citationGenetics of endometriosis: heritability and candidate genes
Bischoff, F., & Simpson, J. L. (2004) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2004.01.004 · Cited by 57 · see citing works
Endometriosis: The way forward
Hompes, P. G. A., & Mijatovic, V. (2007) · Gynecological Endocrinology · doi:10.1080/09513590601010474 · Cited by 55 · see citing works
Baxter, A. J., Hughes, M. C. B., Kvaskoff, M., Siskind, V., Shekar, S. N., Aitken, J. F., Green, A. C., Duffy, D. L., Hayward, N. K., Martin, N. G., et al. (2008) · Twin Research and Human Genetics · doi:10.1375/twin.11.2.183 · Cited by 51 · see citing works
Self-citationWoodworth, S. H., Singh, M., Yussman, M. A., Sanfilippo, J. S., Cook, C. L., & Lincoln, S. R. (1995) · Fertility and Sterility · doi:10.1016/s0015-0282(16)57809-1 · Cited by 45 · see citing works
Kvaskoff, M., Mesrine, S., Fournier, A., Boutron‐Ruault, M., & Clavel‐Chapelon, F. (2007) · Archives of Internal Medicine · doi:10.1001/archinte.167.19.2061 · Cited by 42 · see citing works
Self-citationHornstein, M. D., Thomas, P. P., Sober, A. J., Wyshak, G., Albright, N. L., & Frisch, R. E. (1997) · Human Reproduction · doi:10.1093/humrep/12.1.143 · Cited by 41 · see citing works
Natural hair color and the incidence of endometriosis
Missmer, S. A., Spiegelman, D., Hankinson, S. E., Malspeis, S., Barbieri, R. L., & Hunter, D. J. (2006) · Fertility and Sterility · doi:10.1016/j.fertnstert.2005.12.008 · Cited by 38 · see citing works
Reproductive Factors and Melanoma of the Skin Among Women
Wyshak, G., Frisch, R. E., Albright, N. L., et al. (1989) · International Journal of Dermatology · doi:10.1111/j.1365-4362.1989.tb04606.x · Cited by 32 · see citing works
Red hair color, melanoma, and endometriosis: suggestive associations
Wyshak, G., & Frisch, R. E. (2000) · International Journal of Dermatology · doi:10.1046/j.1365-4362.2000.00051-2.x · Cited by 28 · see citing works
DYSPLASTIC NEVI, CUTANEOUS MELANOMA, AND GYNECOLOGIC DISORDERS
Frisch, R. E., Wyshak, G., Albert, L. S., & Sober, A. J. (1992) · International Journal of Dermatology · doi:10.1111/j.1365-4362.1992.tb03948.x · Cited by 23 · see citing works
低い受胎率の6例の患者における、塩化ストロンチウム(SrCl2)による卵母細胞活性化後の3例の妊娠と分娩の成功
Kumagai, S., Tanaka, A., Nishinaka, C., et al. (2006) · Fertility and Sterility · Cited by 13 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
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
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
Childhood and adolescent exposures and the risk of endometriosis
Kvaskoff, M., Bijon, A., Clavel-Chapelon, F., Mesrine, S., & Boutron-Ruault, M.-C. (2013) · Epidemiology · doi:10.1097/ede.0b013e3182806445 · Cited by 47 · see citing works
Self-citation‘Here comes the sun’: pigmentary traits and sun habits in women with endometriosis
Somigliana, E., Vigano, P., Abbiati, A., Gentilini, D., Parazzini, F., Benaglia, L., Vercellini, P., & Fedele, L. (2010) · Human Reproduction · doi:10.1093/humrep/dep453 · Cited by 40 · see citing works
Overall Adiposity, Adipose Tissue Distribution, and Endometriosis: A Systematic Review
Backonja, U., Buck Louis, G. M., & Lauver, D. R. (2016) · Nursing Research · doi:10.1097/nnr.0000000000000146 · Cited by 39 · see citing works
- Authors
- Kvaskoff, M., Mesrine, S., Clavel-Chapelon, F., & Boutron-Ruault, M.-C.
- Affiliations
- Inserm (FR)
- Venue
- International Journal of Epidemiology
- Publisher
- Oxford University Press (OUP)
- Published
- 2009-04-07
- Volume
- 38
- Issue
- 4
- Pages
- 1143-1153
- ISSN
- 0300-5771 (ISSN-L)
- 1464-3685
- OpenAlex
- W2154512225
- Cited by
- 53
- References
- 49
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 2 · 2023: 1 · 2022: 4 · 2021: 3 · 2020: 6 · 2018: 2 · 2017: 5 · 2016: 2 · 2014: 8 · 2013: 3 · 2012: 4
- FWCI
- 5.89
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- International Journal of Epidemiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Ligue Contre le Cancer
- Fondation de France
- Institut Gustave-Roussy
- Cancer Council Queensland
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Health Sciences › Medicine › Oncology › Cutaneous Melanoma Detection and Management
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › melanin and skin pigmentation
- Keywords
- endometriosis, melanoma, freckles, sun exposure, dose-response relationship, genetic susceptibility, shared genetic risk, women's health
- MeSH terms
- Adult, Aged, Endometriosis, Epidemiologic Methods, Female, France, Hair Color, Humans, Melanosis, Middle Aged, Nevus, Pigmented, Phenotype, Photosensitivity Disorders, Skin, Skin Neoplasms, Skin Pigmentation, Sunlight, Age Distribution
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