Endometriosis and the risks of systemic lupus erythematosus and rheumatoid arthritis in the Nurses' Health Study II
Open accessAbstract
Objectives The aetiologies of endometriosis, systemic lupus erythematosus (SLE) and rheumatoid arthritis (RA) are all characterised by immune dysfunction. SLE and RA occur more often in women, and reproductive and hormonal factors have been shown to be related to increased risk. However, only one previous study has evaluated the temporal association between endometriosis and SLE or RA. We sought to investigate the association between laparoscopically confirmed endometriosis and subsequently diagnosed SLE and RA.Methods We analysed data from the Nurses' Health Study II (n=114 453 women) over a 22-year follow-up period. Multivariable, time-varying Cox proportional hazards models were used to calculate HRs and 95% CIs for the association between laparoscopically confirmed endometriosis and confirmed incident SLE or RA.Results From 1989 to 2011, 103 incident cases of SLE and 390 cases of RA were confirmed. Laparoscopically confirmed endometriosis was significantly associated with subsequent SLE diagnosis (HR=2.03; CI 1.17 to 3.51) and RA diagnosis (HR=1.41; CI 1.05 to 1.89). These associations were robust to adjustment for SLE or RA risk factors and for potential confounders; however, adjustment for hysterectomy and oophorectomy attenuated both relations such that they were no longer significant. No significant differences by infertility status or age (<45 years) were observed.Conclusions Our findings suggest an association between endometriosis and risk of SLE and RA. It remains to be understood whether and how endometriosis itself, or hysterectomy or other factors associated with endometriosis, is related to risk of SLE or RA.
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Women with endometriosis are more likely to be diagnosed with inflammatory bowel diseases, allergic manifestations, and autoimmune diseases.
“An increased risk of inflammatory bowel diseases (Chron’s disease, ulcerative colitis) [146] allergic manifestations [sinus allergic rhinitis, and food allergy) [147], autoimmune diseases (systemic lupus erythematosus, rheumatoid arthritis, Sjogren’s syndrome, multiple sclerosis, fibromyalgia) are more likely to be diagnosed in women with endometriosis”
From Hormonal treatments for endometriosis: The endocrine background (2022) · cites this paper as [149]
The Results report that women with laparoscopically confirmed endometriosis had increased subsequent diagnoses of systemic lupus erythematosus and rheumatoid arthritis, although adjustment for hysterectomy or oophorectomy made the associations nonsignificant. The Introduction mentions multiple sclerosis only as suggested comorbidity in case reports; the paper does not establish increased diagnoses of Sjögren’s syndrome or fibromyalgia. Inflammatory bowel diseases and allergic manifestations have separate citations in the citing sentence, so they are not attributed to this source here. (LLM, conf=0.88)
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Arnett, F. C., Edworthy, S. M., Bloch, D. A., McShane, D. J., Fries, J. F., Cooper, N. S., Healey, L. A., Kaplan, S. R., Liang, M. H., Luthra, H. S., et al. (1988) · Arthritis & Rheumatism · doi:10.1002/art.1780310302 · Cited by 19,753 · see citing works
The 1982 revised criteria for the classification of systemic lupus erythematosus
Tan, E. M., Cohen, A. S., Fries, J. F., Masi, A. T., Mcshane, D. J., Rothfield, N. F., Schaller, J. G., Talal, N., & Winchester, R. J. (1982) · Arthritis & Rheumatism · doi:10.1002/art.1780251101 · Cited by 14,519 · see citing works
Hochberg, M. C. (1997) · Arthritis & Rheumatism · doi:10.1002/art.1780400928 · Cited by 11,409 · see citing works
MacKinnon, D. P., Fairchild, A. J., & Fritz, M. S. (2007) · Annual Review of Psychology · doi:10.1146/annurev.psych.58.110405.085542 · Cited by 5,688 · see citing works
Bulun, S. E. (2009) · New England Journal of Medicine · doi:10.1056/nejmra0804690 · Cited by 1,772 · see citing works
Nnoaham, K. E., Hummelshoj, L., Webster, P., d’Hooghe, T., de Cicco Nardone, F., de Cicco Nardone, C., Jenkinson, C., Kennedy, S. H., & Zondervan, K. T. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2011.05.090 · Cited by 1,584 · see citing works
Immunobiology of endometriosis
Lebovic, D. I., Mueller, M. D., & Taylor, R. N. (2001) · Fertility and Sterility · doi:10.1016/s0015-0282(00)01630-7 · Cited by 857 · see citing works
Is the incidence of rheumatoid arthritis rising?: Results from Olmsted County, Minnesota, 1955–2007
Myasoedova, E., Crowson, C. S., Kremers, H. M., Therneau, T. M., & Gabriel, S. E. (2010) · Arthritis & Rheumatism · doi:10.1002/art.27425 · Cited by 804 · see citing works
THE EPIDEMIOLOGY OF RHEUMATOID ARTHRITIS
Gabriel, S. E. (2001) · Rheumatic Disease Clinics of North America · doi:10.1016/s0889-857x(05)70201-5 · Cited by 783 · see citing works
A Prospective Study of Pregravid Determinants of Gestational Diabetes Mellitus
Solomon, C. G. (1997) · JAMA · doi:10.1001/jama.1997.03550130052036 · Cited by 781 · 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
Self-citationFrom T to B and back again: positive feedback in systemic autoimmune disease
Shlomchik, M. J., Craft, J. E., & Mamula, M. J. (2001) · Nature reviews. Immunology · doi:10.1038/35100573 · Cited by 572 · see citing works
Consensus on current management of endometriosis
Johnson, N. P., Hummelshoj, L., for the World Endometriosis Society Montpellier Consortium, Abrao, M. S., Adamson, G. D., Allaire, C., Amelung, V., Andersson, E., Becker, C., Birna Árdal, K. B., et al. (2013) · Human Reproduction · doi:10.1093/humrep/det050 · Cited by 558 · see citing works
Prediction of endometriosis with serum and peritoneal fluid markers: a prospective controlled trial
Bedaiwy, M. A. (2002) · Human Reproduction · doi:10.1093/humrep/17.2.426 · Cited by 485 · see citing works
Causal Mediation Analysis With Survival Data
VanderWeele, T. J. (2011) · Epidemiology · doi:10.1097/ede.0b013e31821db37e · Cited by 481 · see citing works
Karlson, E. W., Mandl, L. A., Hankinson, S. E., & Grodstein, F. (2004) · Arthritis & Rheumatism · doi:10.1002/art.20621 · Cited by 400 · see citing works
Self-citationReproductive and menopausal factors and risk of systemic lupus erythematosus in women
Costenbader, K. H., Feskanich, D., Stampfer, M. J., & Karlson, E. W. (2007) · Arthritis & Rheumatism · doi:10.1002/art.22510 · Cited by 349 · see citing works
Self-citationBehaviour of Cytokine Levels in Serum and Peritoneal Fluid of Women with Endometriosis
Pizzo, A., Salmeri, F. M., Ardita, F. V., Sofo, V., Tripepi, M., & Marsico, S. (2002) · Gynecologic and Obstetric Investigation · doi:10.1159/000067717 · Cited by 285 · see citing works
Treating endometriosis as an autoimmune disease
Nothnick, W. B. (2001) · Fertility and Sterility · doi:10.1016/s0015-0282(01)01878-7 · Cited by 270 · see citing works
Anti–citrullinated peptide antibody assays and their role in the diagnosis of rheumatoid arthritis
Aggarwal, R., Liao, K. P., Nair, R., et al. (2009) · Arthritis Care & Research · doi:10.1002/art.24827 · Cited by 253 · see citing works
Is endometriosis an autoimmune disease?
Gleicher, N., El-Roeiy, A., Confino, E., & Friberg, J. (1988) · International Journal of Gynecology & Obstetrics · doi:10.1016/0020-7292(88)90292-5 · Cited by 251 · see citing works
Is Endometriosis Associated with Systemic Subclinical Inflammation?
Agic, A., Xu, H., Finas, D., Banz, C., Diedrich, K., & Hornung, D. (2006) · Gynecologic and Obstetric Investigation · doi:10.1159/000093121 · Cited by 231 · see citing works
Is endornetriosis an autoimmune disease
Gleicher, N., El-Roeiy, A., Confino, E., & Friberg, J. (1987) · Obstetrics and Gynecology · Cited by 223 · see citing works
A connective tissue disease screening questionnaire for population studies
Karlson, E. W., Sánchez‐Guerrero, J., Wright, E. A., Lew, R., Daltroy, L. H., Katz, J. N., & Liang, M. H. (1995) · Annals of Epidemiology · doi:10.1016/1047-2797(94)00096-c · Cited by 221 · see citing works
Self-citationHeinlen, L. D., McClain, M. T., Merrill, J. T., Akbarali, Y., Edgerton, C. C., Harley, J. B., & James, J. A. (2007) · Arthritis & Rheumatism · doi:10.1002/art.22665 · Cited by 202 · see citing works
Environmental and Gene-Environment Interactions and Risk of Rheumatoid Arthritis
Karlson, E. W., & Deane, K. D. (2012) · Rheumatic Disease Clinics of North America · doi:10.1016/j.rdc.2012.04.002 · Cited by 175 · see citing works
Self-citationOnset of symptoms of rheumatoid arthritis in relation to age, sex and menopausal transition.
Goemaere, S., Ackerman, C. T., Goethals, K., et al. (1990) · PubMed · Cited by 171 · see citing works
Sexual disparities in the incidence and course of SLE and RA
Tedeschi, S. K., Bermas, B. L., & Costenbader, K. H. (2013) · Clinical Immunology · doi:10.1016/j.clim.2013.03.003 · Cited by 169 · see citing works
Self-citationIs there an association between autoimmunity and endometriosis?
Eisenberg, V. H., Zolti, M., & Soriano, D. (2012) · Autoimmunity Reviews · doi:10.1016/j.autrev.2012.01.005 · Cited by 164 · see citing works
Sex effects in systemic lupus erythematosus. a clue to pathogenesis
Masi, A. T., & Kaslow, R. A. (1978) · Arthritis & Rheumatism · doi:10.1002/art.1780210413 · Cited by 162 · see citing works
Onset of symptoms of rheumatoid arthritis in relation to age, sex and menopausal transition
Goemaere, S., Ackerman, C. M., Goethals, K., et al. (1991) · Maturitas · doi:10.1016/0378-5122(91)90251-k · Cited by 144 · see citing works
Karlson, E. W., Chibnik, L. B., Tworoger, S. S., Lee, I.-M. M., Buring, J. E., Shadick, N. A., Manson, J. E., & Costenbader, K. H. (2009) · Arthritis & Rheumatism · doi:10.1002/art.24350 · Cited by 125 · see citing works
Self-citationMori, H., Sawairi, M., NAKAGAWA, M., Itoh, N., Wada, K., & Tamaya, T. (1991) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.1991.tb00972.x · Cited by 117 · see citing works
Nielsen, N. M., Jorgensen, K. T., Pedersen, B. V., Rostgaard, K., & Frisch, M. (2011) · Human Reproduction · doi:10.1093/humrep/der105 · Cited by 106 · see citing works
Modifiable risk factors for RA: prevention, better than cure?
Lahiri, M., Morgan, C., Symmons, D. P. M., & Bruce, I. N. (2011) · Rheumatology · doi:10.1093/rheumatology/ker299 · Cited by 106 · see citing works
Hormone replacement and contraceptive therapy in autoimmune diseases
Lateef, A., & Petri, M. (2012) · Journal of Autoimmunity · doi:10.1016/j.jaut.2011.11.002 · Cited by 80 · see citing works
Clinical manifestations and survival among adults with (SLE) according to age at diagnosis
Merola, J. F., Bermas, B. L., Lü, B., Karlson, E. W., Massarotti, E. M., Schur, P. H., & Costenbader, K. H. (2014) · Lupus · doi:10.1177/0961203314526291 · Cited by 79 · see citing works
Self-citationAkoum, A., Al-Akoum, M., Lemay, A., Maheux, R., & Leboeuf, M. (2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.06.019 · Cited by 78 · see citing works
Baptist, A. P., & Baldwin, J. L. (2004) · Clinical and Molecular Allergy · doi:10.1186/1476-7961-2-10 · Cited by 73 · see citing works
Arkema, E. V., Goldstein, B. L., Robinson, W. H., et al. (2013) · Arthritis Research & Therapy · doi:10.1186/ar4342 · Cited by 70 · see citing works
The expression of soluble intercellular adhesion molecule-1 in endometriosis
Wu, M., Yang, B., Hsu, C., Lee, Y.-C., & Huang, K. (1998) · Fertility and Sterility · doi:10.1016/s0015-0282(98)00384-7 · Cited by 67 · see citing works
Koumantakis, E., Matalliotakis, I., Neonaki, M., Froudarakis, G., & Georgoulias, V. (1994) · Archives of Gynecology and Obstetrics · doi:10.1007/bf02390936 · Cited by 65 · see citing works
What can epidemiology tell us about systemic lupus erythematosus?
Simard, J. F., & Costenbader, K. H. (2007) · International Journal of Clinical Practice · doi:10.1111/j.1742-1241.2007.01434.x · Cited by 64 · see citing works
Self-citationSex-specific environmental influences on the development of autoimmune diseases
Tiniakou, E., Costenbader, K. H., & Kriegel, M. A. (2013) · Clinical Immunology · doi:10.1016/j.clim.2013.02.011 · Cited by 56 · see citing works
Self-citationPasoto, S. G., Abrão, M. S., Viana, V. S. T., Bueno, C., Leon, E. P., & Bonfá, E. (2005) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.2005.00252.x · Cited by 53 · see citing works
Prevalence of endometriosis in women with systemic lupus erythematosus and Sjögren's syndrome
Matorras, R., Ocerin, I., Unamuno, M., Nieto, A., Peiró, E., Burgos, J., & Expósito, A. (2007) · Lupus · doi:10.1177/0961203307081339 · Cited by 45 · see citing works
Alviggi, C., Carrieri, P. B., Pivonello, R., Scarano, V., Pezzella, M., Placido, G. D., Colao, A., & Matarese, G. (2006) · Journal of Endocrinological Investigation · doi:10.1007/bf03344095 · Cited by 33 · see citing works
Cytokines in relation to autoantibodies before onset of symptoms for systemic lupus erythematosus
Eriksson, C., & Rantapää‐Dahlqvist, S. (2014) · Lupus · doi:10.1177/0961203314523869 · Cited by 25 · see citing works
Hollingsworth, P., Pummer, S. C., & Dawkins, R. L. (1996) · Elsevier eBooks · doi:10.1016/b978-044482383-0/50013-3 · Cited by 13 · see citing works
Mitochondrial hyperpolarization and ATP depletion in patients with systemic lupus erythematosus
Gergely, P., Grossman, C., Niland, B., Puskas, F., Neupane, H., Allam, F., Banki, K., Phillips, P. E., & Perl, A. (2002) · Arthritis & Rheumatism · doi:10.1002/1529-0131(200201)46:1 · Cited by 5 · see citing works
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Sorted by citations
Zondervan, K. T., Becker, C. M., Koga, K., Missmer, S. A., Taylor, R. N., & Viganò, P. (2018) · Nature Reviews Disease Primers · doi:10.1038/s41572-018-0008-5 · Cited by 1,257 · see citing works
Self-citationRisk 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-citationPathophysiology, diagnosis, and management of endometriosis
Horne, A. W., & Missmer, S. A. (2022) · BMJ · doi:10.1136/bmj-2022-070750 · Cited by 661 · see citing works
Self-citationThe association between endometriosis and autoimmune diseases: a systematic review and meta-analysis
Shigesi, N., Kvaskoff, M., Kirtley, S., Feng, Q., Fang, H., Knight, J. C., Missmer, S. A., Rahmioglu, N., Zondervan, K. T., & Becker, C. M. (2019) · Human Reproduction Update · doi:10.1093/humupd/dmz014 · Cited by 382 · see citing works
Self-citationHormonal treatments for endometriosis: The endocrine background
Vannuccini, S., Clemenza, S., Rossi, M., & Petraglia, F. (2022) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-021-09666-w · Cited by 336 · see citing works
The link between immunity, autoimmunity and endometriosis: a literature update
Zhang, T., De Carolis, C., Man, G. C. W., & Wang, C. C. (2018) · Autoimmunity Reviews · doi:10.1016/j.autrev.2018.03.017 · Cited by 196 · see citing works
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Tashiro, T., & Sawada, Y. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23084457 · Cited by 104 · see citing works
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Porpora, M. G., Scaramuzzino, S., Sangiuliano, C., Piacenti, I., Bonanni, V., Piccioni, M. G., Ostuni, R., Masciullo, L., & Benedetti Panici, P. L. (2020) · Gynecological Endocrinology · doi:10.1080/09513590.2019.1655727 · Cited by 61 · see citing works
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Koninckx, P. R., Ussia, A., Keckstein, J., Wattiez, A., & Adamyan, L. (2016) · Gynecological Surgery · doi:10.1007/s10397-016-0970-4 · Cited by 30 · see citing works
Garitazelaia, A., Rueda-Martínez, A., Arauzo, R., de Miguel, J., Cilleros-Portet, A., Marí, S., Bilbao, J. R., Fernandez-Jimenez, N., & García-Santisteban, I. (2021) · Life · doi:10.3390/life11010024 · Cited by 22 · see citing works
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Di Maida, F., Lambertini, L., Grosso, A. A., Mari, A., Vannuccini, S., Capezzuoli, T., Fambrini, M., Petraglia, F., & Minervini, A. (2022) · Journal of Minimally Invasive Gynecology · doi:10.1016/j.jmig.2022.07.004 · Cited by 5 · see citing works
- Authors
- Harris, H. R., Costenbader, K. H., Mu, F., Kvaskoff, M., Malspeis, S., Karlson, E. W., & Missmer, S. A.
- Affiliations
- Brigham and Women's Hospital (US)
- Harvard University (US)
- Université Paris-Sud (FR)
- Corresponding author
- Harris, Holly R
- ORCID
- Venue
- Annals of the Rheumatic Diseases
- Publisher
- Elsevier BV
- Published
- 2016-07
- Volume
- 75
- Issue
- 7
- Pages
- 1279-1284
- ISSN
- 0003-4967 (ISSN-L)
- PMC
- PMC4740245
- OpenAlex
- W1937039726
- Cited by
- 112
- References
- 51
- Citations by year
- 2026: 6 · 2025: 15 · 2024: 17 · 2023: 6 · 2022: 15 · 2021: 10 · 2020: 12 · 2019: 8 · 2018: 8 · 2017: 6 · 2016: 9
- FWCI
- 13.73
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- Annals of the Rheumatic Diseases (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- HighWire Press Open Archive (submittedVersion)
- Funders
- National Cancer Institute (UM1CA176726)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (R01AR049880, P30AR070253)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD057210, R01HD052473)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Health Sciences › Medicine › Rheumatology › Systemic Lupus Erythematosus Research
- Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
- Keywords
- endometriosis, systemic lupus erythematosus, rheumatoid arthritis, autoimmune disease susceptibility, hysterectomy, oophorectomy, immune dysfunction, temporal association, women's health
- MeSH terms
- Adult, Arthritis, Rheumatoid, Endometriosis, Female, Follow-Up Studies, Humans, Lupus Erythematosus, Systemic, Nurses, Prospective Studies, Risk Factors, Proportional Hazards Models
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