Endometriosis: a high-risk population for major chronic diseases?

BACKGROUND Despite an estimated prevalence of 10% in women, the etiology of endometriosis remains poorly understood. Over recent decades, endometriosis has been associated with risk of several chronic diseases, such as cancer, autoimmune diseases, asthma/atopic diseases and cardiovascular diseases. A deeper understanding of these associations is needed as they may provide new leads into the causes or consequences of endometriosis. This review summarizes the available epidemiological findings on the associations between endometriosis and other chronic diseases and discusses hypotheses for underlying mechanisms, potential sources of bias and methodological complexities. METHODS We performed a comprehensive search of the PubMed/Medline and ISI Web of Knowledge databases for all studies reporting on the associations between endometriosis and other diseases published in English through to May 2014, using numerous search terms. We additionally examined the reference lists of all identified papers to capture any additional articles that were not identified through computer searches. RESULTS We identified 21 studies on the associations between endometriosis and ovarian cancer, 14 for breast cancer, 8 for endometrial cancer, 4 for cervical cancer, 12 for cutaneous melanoma and 3 for non-Hodgkin's lymphoma, as well as 9 on the links between endometriosis and autoimmune diseases, 6 on the links with asthma and atopic diseases, and 4 on the links with cardiovascular diseases. Endometriosis patients were reported to be at higher risk of ovarian and breast cancers, cutaneous melanoma, asthma, and some autoimmune, cardiovascular and atopic diseases, and at decreased risk of cervical cancer. CONCLUSIONS Increasing evidence suggests that endometriosis patients are at higher risk of several chronic diseases. Although the underlying mechanisms are not yet understood, the available data to date suggest that endometriosis is not harmless with respects to women's long-term health. If these relationships are confirmed, these findings may have important implications in screening practices and in the management and care of endometriosis patients.

[1]  Manuel J. Amador-Patarroyo,et al.  Autoimmune disease and gender: plausible mechanisms for the female predominance of autoimmunity. , 2012, Journal of autoimmunity.

[2]  D. Cramer,et al.  The Epidemiology of Endometriosis , 2002, Obstetrics and gynecology clinics of North America.

[3]  F. M. Salmeri,et al.  Behaviour of Cytokine Levels in Serum and Peritoneal Fluid of Women with Endometriosis , 2003, Gynecologic and Obstetric Investigation.

[4]  K. Osteen,et al.  Immune interactions in endometriosis , 2011, Expert review of clinical immunology.

[5]  D. Macut,et al.  Cardiovascular risk factors and events in women with androgen excess , 2015, Journal of Endocrinological Investigation.

[6]  Stephen H Kennedy,et al.  Impact of endometriosis on quality of life and work productivity: a multicenter study across ten countries. , 2011, Fertility and sterility.

[7]  M. Pike,et al.  Association between endometriosis and risk of histological subtypes of ovarian cancer: a pooled analysis of case–control studies , 2012, The Lancet. Oncology.

[8]  K. Arisawa,et al.  Risk of developing ovarian cancer among women with ovarian endometrioma: a cohort study in Shizuoka, Japan , 2006, International Journal of Gynecologic Cancer.

[9]  S. Kjaer,et al.  Risk of cancer among women with polycystic ovary syndrome: a Danish cohort study. , 2015, Gynecologic oncology.

[10]  M. Goodman,et al.  Endometriosis and its treatment with danazol or lupron in relation to ovarian cancer. , 2003, Clinical cancer research : an official journal of the American Association for Cancer Research.

[11]  B. V. Pedersen,et al.  Increased risk of inflammatory bowel disease in women with endometriosis: a nationwide Danish cohort study , 2011, Gut.

[12]  S. Cleary,et al.  Cancers, infections, and endocrine diseases in women with endometriosis. , 2008, Fertility and Sterility.

[13]  D. Purdie,et al.  A study of infertility treatment and melanoma , 2001, Melanoma research.

[14]  J. Olsen,et al.  Risk for breast cancer among women with endometriosis , 2007, International journal of cancer.

[15]  B. Eskenazi,et al.  Epidemiology of endometriosis. , 1997, Obstetrics and gynecology clinics of North America.

[16]  J. Ludvigsson,et al.  Risk of endometriosis in 11,000 women with celiac disease. , 2011, Human reproduction.

[17]  N. Ragni,et al.  Asthma in women with endometriosis. , 2005, Human reproduction.

[18]  N. Weiss,et al.  Risk of epithelial ovarian cancer in relation to benign ovarian conditions and ovarian surgery , 2008, Cancer Causes & Control.

[19]  L. Cardon,et al.  What makes a good case-control study? Design issues for complex traits such as endometriosis. , 2002, Human reproduction.

[20]  E. Holly,et al.  Cutaneous melanoma in women. III. Reproductive factors and oral contraceptive use. , 1995, American journal of epidemiology.

[21]  Y. Aksoy,et al.  Carotid intima-media thickness: a new marker of patients with uterine leiomyoma. , 2014, European journal of obstetrics, gynecology, and reproductive biology.

[22]  D. Soriano,et al.  Is there an association between autoimmunity and endometriosis? , 2012, Autoimmunity reviews.

[23]  R. Frisch,et al.  Reproductive Factors and Melanoma of the Skin Among Women , 1989, International journal of dermatology.

[24]  H. Chung,et al.  Risk and prognosis of ovarian cancer in women with endometriosis: a meta-analysis , 2014, British Journal of Cancer.

[25]  M. Stampfer,et al.  Metabolic disorders and breast cancer risk (United States) , 2001, Cancer Causes & Control.

[26]  J. Sampson Endometrial carcinoma of the ovary arising in endometrial tissue in that organ , 1925 .

[27]  L. Nieman,et al.  High rates of autoimmune and endocrine disorders, fibromyalgia, chronic fatigue syndrome and atopic diseases among women with endometriosis: a survey analysis. , 2002, Human reproduction.

[28]  R. Ferriani,et al.  Serological testing for celiac disease in women with endometriosis. A pilot study. , 2009, Clinical and experimental obstetrics & gynecology.

[29]  Aguiar Fm,et al.  Serological testing for celiac disease in women with endometriosis. A pilot study. , 2009 .

[30]  A. Venn,et al.  Risk of cancer after use of fertility drugs with in-vitro fertilisation , 1999, The Lancet.

[31]  S. Missmer Commentary: Endometriosis--epidemiologic considerations for a potentially 'high-risk' population. , 2009, International journal of epidemiology.

[32]  L. Brinton,et al.  Ovarian cancer risk associated with varying causes of infertility. , 2004, Fertility and sterility.

[33]  R. Frisch,et al.  Red hair color, melanoma, and endometriosis: suggestive associations , 2000, International journal of dermatology.

[34]  P. Sparén,et al.  Endometriosis and the risk of cancer with special emphasis on ovarian cancer. , 2006, Human reproduction.

[35]  John A. Barry,et al.  Risk of endometrial, ovarian and breast cancer in women with polycystic ovary syndrome: a systematic review and meta-analysis , 2014, Human reproduction update.

[36]  L. Brinton,et al.  Causes of Infertility as Predictors of Subsequent Cancer Risk , 2005, Epidemiology.

[37]  J. Donnez,et al.  Oxidative stress and peritoneal endometriosis. , 2002, Fertility and sterility.

[38]  J. Arkins,et al.  The association of atopic diseases with endometriosis. , 1987, Annals of allergy.

[39]  Dan-Feng Du,et al.  The relationship between thyroiditis and polycystic ovary syndrome: a meta-analysis. , 2013, International journal of clinical and experimental medicine.

[40]  K. Costenbader,et al.  Sex-specific environmental influences on the development of autoimmune diseases. , 2013, Clinical immunology.

[41]  M. Goodman,et al.  Oral contraceptive use, reproductive history, and risk of epithelial ovarian cancer in women with and without endometriosis. , 2004, American journal of obstetrics and gynecology.

[42]  C. Borgfeldt,et al.  Cancer risk after hospital discharge diagnosis of benign ovarian cysts and endometriosis. , 2004, Acta obstetricia et gynecologica Scandinavica.

[43]  Z. Zhao,et al.  The search for genes contributing to endometriosis risk. , 2008, Human reproduction update.

[44]  C. Petta,et al.  Thyroid autoimmunity and thyroid dysfunction in women with endometriosis. , 2007, Human reproduction.

[45]  M. Morgan,et al.  Factors related to inflammation of the ovarian epithelium and risk of ovarian cancer. , 2000, Epidemiology.

[46]  L. Brinton,et al.  Citations from the literature , 2003 .

[47]  L. Brinton,et al.  Breast cancer risk associated with gynecologic surgery and indications for such surgery , 1997, International journal of cancer.

[48]  C. Dirksen,et al.  Endometriosis Cost Assessment (the EndoCost Study): A Cost-of-Illness Study Protocol , 2010, Gynecologic and Obstetric Investigation.

[49]  C. la Vecchia,et al.  Hormone-related factors and gynecological conditions in relation to endometrial cancer risk , 2009, European journal of cancer prevention : the official journal of the European Cancer Prevention Organisation.

[50]  F. Clavel-Chapelon,et al.  Personal history of endometriosis and risk of cutaneous melanoma in a large prospective cohort of French women. , 2007, Archives of internal medicine.

[51]  F. Bonomini,et al.  Atherosclerosis and oxidative stress. , 2008, Histology and histopathology.

[52]  R. G. M. Frcog Endometriosis: an invasive disease , 2001 .

[53]  A. Wakatsuki,et al.  Increased asymmetric dimethylarginine and enhanced inflammation are associated with impaired vascular reactivity in women with endometriosis. , 2011, Atherosclerosis.

[54]  L. Brewster,et al.  Hypertension risk in Dutch women with symptomatic uterine fibroids. , 2015, American journal of hypertension.

[55]  A. Aris Endometriosis-associated ovarian cancer: A ten-year cohort study of women living in the Estrie Region of Quebec, Canada , 2010, Journal of ovarian research.

[56]  X. Shu,et al.  Impact of Premature Ovarian Failure on Mortality and Morbidity among Chinese Women , 2014, PloS one.

[57]  W. Willett,et al.  A prospective study of dietary fat consumption and endometriosis risk. , 2010, Human reproduction.

[58]  K. Jochumsen,et al.  The relation between endometriosis and ovarian cancer – a review , 2014, Acta obstetricia et gynecologica Scandinavica.

[59]  M. Montalto,et al.  Looking for Celiac Disease in Italian Women with Endometriosis: A Case Control Study , 2014, BioMed research international.

[60]  Elizabeth W Karlson,et al.  Reproductive and menopausal factors and risk of systemic lupus erythematosus in women. , 2007, Arthritis and rheumatism.

[61]  M. Ballweg Overcoming Endometriosis: New Help from the Endometriosis Association , 1987 .

[62]  Robert N. Taylor,et al.  Relative Expression of 1,25-Dihydroxyvitamin D3 Receptor, Vitamin D 1α-Hydroxylase, Vitamin D 24-Hydroxylase, and Vitamin D 25-Hydroxylase in Endometriosis and Gynecologic Cancers , 2007, Reproductive Sciences.

[63]  F. Gloria-Bottini,et al.  Acid phosphatase locus 1 genetic polymorphism, endometriosis, and allergy. , 2008, Fertility and sterility.

[64]  Luisa Mola Morales,et al.  Women with endometriosis have a higher DNA repair capacity and diminished breast cancer risk. , 2013, Molecular cancer biology.

[65]  E. Mascha,et al.  Genetic Polymorphism in the Fibrinolytic System and Endometriosis , 2006, Obstetrics and gynecology.

[66]  S. Jick,et al.  Use of metformin and the risk of ovarian cancer: a case-control analysis. , 2011, Gynecologic oncology.

[67]  M. Bots,et al.  Cardiovascular disease risk in women with premature ovarian insufficiency: A systematic review and meta-analysis , 2016, European journal of preventive cardiology.

[68]  M. Wrensch,et al.  Family and personal medical history and risk of meningioma. , 2011, Journal of neurosurgery.

[69]  Ildikó Kriszbacher,et al.  Inflammation, atherosclerosis, and coronary artery disease. , 2005, New England Journal of Medicine.

[70]  J. Cerhan,et al.  Postmenopausal cancer risk after self‐reported endometriosis diagnosis in the Iowa Women's Health Study , 2002, Cancer.

[71]  J. Sampson ENDOMETRIAL CARCINOMA OF THE OVARY, ARISING IN ENDOMETRIAL TISSUE IN THAT ORGAN , 1925 .

[72]  P. Vercellini,et al.  Association between endometriosis and cancer: a comprehensive review and a critical analysis of clinical and epidemiological evidence. , 2006, Gynecologic oncology.

[73]  B. V. Pedersen,et al.  The co-occurrence of endometriosis with multiple sclerosis, systemic lupus erythematosus and Sjogren syndrome. , 2011, Human reproduction.

[74]  D. Whiteman,et al.  Endometrioid and clear cell ovarian cancers: a comparative analysis of risk factors. , 2008, European journal of cancer.

[75]  M. Goodman,et al.  Infertility, fertility drugs, and ovarian cancer: a pooled analysis of case-control studies. , 2002, American journal of epidemiology.

[76]  A. Sober,et al.  DYSPLASTIC NEVI, CUTANEOUS MELANOMA, AND GYNECOLOGIC DISORDERS , 1992, International journal of dermatology.

[77]  R. Ferriani,et al.  Unfavorable lipid profile in women with endometriosis. , 2010, Fertility and sterility.

[78]  A. Arıcı,et al.  High rate of allergies among women with endometriosis , 2012, Journal of Obstetrics and Gynaecology Research.

[79]  F. Grodstein,et al.  Do breast-feeding and other reproductive factors influence future risk of rheumatoid arthritis? Results from the Nurses' Health Study. , 2004, Arthritis and rheumatism.

[80]  K. Lamb,et al.  Endometriosis: a comparison of associated disease histories. , 1986, American journal of preventive medicine.

[81]  S. Simoens,et al.  Non-health-care costs associated with endometriosis. , 2011, Human reproduction.

[82]  Sajal Gupta,et al.  Role of oxidative stress in endometriosis. , 2006, Reproductive biomedicine online.

[83]  D. Brogan,et al.  Breast cancer risk in young women and history of selected medical conditions. , 1999, International journal of epidemiology.

[84]  A. Green,et al.  Talcum powder, chronic pelvic inflammation and NSAIDs in relation to risk of epithelial ovarian cancer , 2008, International journal of cancer.

[85]  C. C. Hsu,et al.  The expression of soluble intercellular adhesion molecule-1 in endometriosis. , 1998, Fertility and sterility.

[86]  V. Georgoulias,et al.  Soluble serum interleukin-2 receptor, interleukin-6 and interleukin-1a in patients with endometriosis and in controls , 1994, Archives of Gynecology and Obstetrics.

[87]  B. Pasternack,et al.  The influence of medical conditions associated with hormones on the risk of breast cancer. , 1993, International journal of epidemiology.

[88]  A. Gasbarrini,et al.  M057 ENDOTHELIAL DYSFUNCTION BUT NOT INCREASED CAROTID INTIMA‐MEDIA THICKNESS IN YOUNG EUROPEAN WOMEN WITH ENDOMETRIOSIS , 2012, Human reproduction.

[89]  L. Giudice,et al.  Bisphenol A and phthalates and endometriosis: the Endometriosis: Natural History, Diagnosis and Outcomes Study. , 2013, Fertility and sterility.

[90]  E. Fish,et al.  Sex affects immunity. , 2012, Journal of autoimmunity.

[91]  P. Vercellini,et al.  Principles of phenomics in endometriosis. , 2012, Human reproduction update.

[92]  R. Seemann,et al.  Overt hypothyroidism is associated with the presence of uterine leiomyoma: a retrospective analysis. , 2014, European journal of obstetrics, gynecology, and reproductive biology.

[93]  P. Sparén,et al.  The risk of cancer and the role of parity among women with endometriosis. , 2007, Human reproduction.

[94]  M. Mikołajczyk,et al.  Oxidative stress may be a piece in the endometriosis puzzle. , 2003, Fertility and sterility.

[95]  L. Manganaro,et al.  Role of environmental organochlorinated pollutants in the development of endometriosis. , 2013, Clinical and experimental obstetrics & gynecology.

[96]  W. Nothnick Treating endometriosis as an autoimmune disease. , 2001, Fertility and sterility.

[97]  A. Morris,et al.  Genetic variants underlying risk of endometriosis: insights from meta-analysis of eight genome-wide association and replication datasets , 2014, Human reproduction update.

[98]  F. V. van Leeuwen,et al.  Increased risk for ovarian cancer and borderline ovarian tumours in subfertile women with endometriosis. , 2013, Human reproduction.

[99]  C. Vestergaard,et al.  Endometriosis and type 1 allergies/immediate type hypersensitivity: a systematic review. , 2014, European journal of obstetrics, gynecology, and reproductive biology.

[100]  R. Matorras,et al.  Prevalence of endometriosis in women with systemic lupus erythematosus and Sjögren's syndrome , 2007, Lupus.