Endometriosis and inflammatory bowel disease: A systematic review of the literature

  • Francesca Chiaffarino
    Correspondence
    Corresponding author.
    Affiliations
    Department of Woman, Newborn and Child, Fondazione Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Ca’ Granda Ospedale Maggiore Policlinico, Via Commenda 12, 20122, Milan, Italy
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  • Sonia Cipriani
    Affiliations
    Department of Woman, Newborn and Child, Fondazione Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Ca’ Granda Ospedale Maggiore Policlinico, Via Commenda 12, 20122, Milan, Italy
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  • Elena Ricci
    Affiliations
    Department of Woman, Newborn and Child, Fondazione Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Ca’ Granda Ospedale Maggiore Policlinico, Via Commenda 12, 20122, Milan, Italy
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  • Elena Roncella
    Affiliations
    Department of Clinical Sciences and Community Health, Università degli studi di Milano, Fondazione IRCCS Ca’ Granda Ospedale Maggiore Policlinico, Via Commenda 12, 20122, Milan, Italy
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  • Paola Agnese Mauri
    Affiliations
    Department of Clinical Sciences and Community Health, Università degli studi di Milano, Fondazione IRCCS Ca’ Granda Ospedale Maggiore Policlinico, Via Commenda 12, 20122, Milan, Italy
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  • Fabio Parazzini
    Affiliations
    Department of Woman, Newborn and Child, Fondazione Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Ca’ Granda Ospedale Maggiore Policlinico, Via Commenda 12, 20122, Milan, Italy

    Department of Clinical Sciences and Community Health, Università degli studi di Milano, Fondazione IRCCS Ca’ Granda Ospedale Maggiore Policlinico, Via Commenda 12, 20122, Milan, Italy
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  • Paolo Vercellini
    Affiliations
    Department of Woman, Newborn and Child, Fondazione Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Ca’ Granda Ospedale Maggiore Policlinico, Via Commenda 12, 20122, Milan, Italy

    Department of Clinical Sciences and Community Health, Università degli studi di Milano, Fondazione IRCCS Ca’ Granda Ospedale Maggiore Policlinico, Via Commenda 12, 20122, Milan, Italy
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      Abstract

      The potential link between endometriosis and Inflammatory Bowel Disease (IBD) has been investigated over the last twenty years.
      Endometriosis shares with IBD features and symptoms so to become a significant diagnostic challenge, resulting in a delayed or indeterminate diagnosis. We conducted a systematic review to summarize the available data in literature on the co-diagnosis of IBD and endometriosis.
      A systematic literature search was performed using the electronic databases MEDLINE and EMBASE from 1990 to November 2019, using the search terms: inflammatory bowel disease OR ulcerative colitis OR Crohn’s disease AND endometriosis. We selected 23 articles: 15 case-report, 3 clinical series, 3 case-control studies, 1 cross-sectional study and 1 cohort study.
      All the epidemiological studies included in this review reported a positive association between endometriosis and IBD. Meta-analysis was not possible because, due to study design and type of patients included, there were no comparable groups to analyze. In epidemiological studies with a control group, the proportion of IBD in patients with endometriosis varied from 2 to 3.4 %, compared to 0–1 % of the control group. A large nationwide Danish cohort study reported a 50 % increase in the risk of IBD in women with endometriosis in comparison with women in the general population. In a large Danish cohort study women with endometriosis had an increased risk of CD and UC with a standardized incidence ratio of 1.5 (95 % CI 1.3−1.7) and 1.6 (95 % CI 1.3−2.0) respectively.
      Several studies do not provide information on the temporal sequence of endometriosis and IBD and therefore a clear analysis of a cause-effect association between these two pathologies is lacking.
      The high number of case-reports in the literature highlights how the diagnosis can be challenged, as endometriosis can be masquerading as IBD or vice versa or be present within the same patient. Further research is needed to better understand the temporal association between endometriosis and IBD, which could be useful to correct evaluation and improve the management of these patients.

      Keywords

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      References

        • Parazzini F.
        • Luchini L.
        • Vezzoli F.
        • Mezzanotte C.
        • Vercellini P.
        Gruppo italiano perlo studio dell’endometriosi. Prevalence and anatomical distribution of endometriosisin women with selected gynaecological conditions: results from amulticentric Italian study.
        Hum Reprod. 1994; 9: 1158-1162
        • Bulun S.E.
        Endometriosis.
        N Engl J Med. 2009; 360: 268-279
        • Weed J.C.
        • Ray J.E.
        Endometriosis of the bowel.
        Obstet Gynecol. 1987; 69: 727-730
        • Fedele L.
        • Berlanda N.
        • Corsi C.
        • Gazzano G.
        • Morini M.
        • Vercellini P.
        • et al.
        Ileocecal endometriosis: clinical and pathogenetic implications of an underdiagnosed condition.
        Fertil Steril. 2014; 101: 750-753
        • Vercellini P.
        • Buggio L.
        • Berlanda N.
        • Barbara G.
        • Somigliana E.
        • Bosari S.
        Estrogen-progestins and progestins for the management of endometriosis.
        Fertil Steril. 2016; 106: 1552-1571
        • Kvaskoff M.
        • Mu F.
        • Terry K.L.
        • Harris H.R.
        • Poole E.M.
        • Farland L.
        • et al.
        Endometriosis: a high-risk population for major chronic diseases?.
        Hum Reprod Update. 2015; 21: 500-516
        • Molodecky N.A.
        • Soon I.S.
        • Rabi D.M.
        • Ghali W.A.
        • Ferris M.
        • Chernoff G.
        Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review.
        Gastroenterology. 2012; 142: 46-54
        • Nielsen N.M.
        • Jorgensen K.T.
        • Pedersen B.V.
        • Rostgaard K.
        • Frisch M.
        The co-occurrence of endometriosis with multiple sclerosis, systemic lupus erythematosus and Sjogren syndrome.
        Hum Reprod. 2011; 26: 1555-1559
        • Brouwer J.
        • Fleurbaaij R.
        • Hazes J.M.
        • Dolhain R.J.
        • Laven J.S.
        Subfertilityin women with rheumatoid arthritis and the outcome of fertilityassessments.
        Arthritis Care Res (Hoboken). 2017; 69: 1142-1149
        • Aguiar F.M.
        • Castanheira Melo S.B.
        • Carvalho Galvao L.
        • Rosa e Silva J.C.
        • dos Reis R.M.
        • Ferriani R.A.
        Serological testing for celiac disease in women with endometriosis. A pilot study.
        Clin Exp Obstet Gynecol. 2009; 36: 23-25
        • Santoro L.
        • Campo S.
        • D’Onofrio F.
        • Gallo A.
        • Covino M.
        • Campo V.
        • et al.
        Looking for celiac disease in Italian women with endometriosis: a case control study.
        Biomed Res Int. 2014; (ID: 236821)https://doi.org/10.1155/2014/236821
        • Stephansson O.
        • Falconer H.
        • Ludvigsson J.F.
        Risk of endometriosis in 11,000 women with celiac disease.
        Hum Reprod. 2011; 26: 2896-2901
        • Shigesi N.
        • Kvaskoff M.
        • Kirtley S.
        • Feng Q.
        • Fang H.
        • Knight J.C.
        • et al.
        The association between endometriosis and autoimmune disease: a systematic review and meta-analysis.
        Hum Reprod Update. 2019; 25: 486-503
        • Slim K.
        • Nini E.
        • Forestier D.
        • Kwiatkowski F.
        • Panis Y.
        • Chipponi J.
        Methodological index for non-randomized studies (MINORS): development and validation of a new instrument.
        ANZ J Surg. 2003; 73: 712-716
        • Asanza-Llorente J.A.
        • Serrano-Egea A.
        • López-López A.
        • García-Aparicio M.
        • Calderón-Duque T.
        • Timón-Peralta J.
        Enterovesical fistula and intestinal obstruction by ileal endometriosis.
        Rev Esp Enferm Dig. 2013; 105: 504-506
        • Boulton R.
        • Chawla M.H.
        • Poole S.
        • Hodgson H.J.
        • Barrison I.G.
        Ileal endometriosis masquerading as Crohn’s ileitis.
        J Clin Gastroenterol. 1997; 25: 338-342
        • Dong C.1
        • Ngu Ws2
        • Wakefield Se.
        Endometriosis masquerading as Crohn’s disease in a patient with acute small bowel obstruction.
        BMJ Case Rep. 2015; : 22https://doi.org/10.1136/bcr-2014-207229
        • Karaman K.1
        • Pala E.E.
        • Bayol U.
        • Akman O.
        • Olmez M.
        • Unluoglu S.
        • et al.
        Endometriosis of the terminal ileum: a diagnostic dilemma.
        Case Rep Pathol. 2012; 2012 (Epub 2012 Sep 11): 742035
        • Minocha A.
        • Davis M.S.
        • Wright R.A.
        Small bowel endometriosis masquerading as regional enteritis.
        Dig Dis Sci. 1994; 39: 1126-1133
        • Tong Y.L.
        • Chen Y.
        • Zhu S.Y.
        Ileocecal endometriosis and a diagnosis dilemma: a case report and literature review.
        World J Gastroenterol. 2013; 19: 3707-3710
        • Correia-Varela-Almeida A.
        • Vázquez-Morón J.M.
        • Ortiz-López E.
        Ileum endometriosis and Crohn’s disease.
        Med Clin (Barc). 2018; 14: e65-e66
        • Evangeliou H.
        • MacDonald S.
        • Blumenkrantz M.
        • Laberge J.M.
        • Morinville V.
        Endometriosis mimicking symptoms of microperforation in a teenage girl with inflammatory bowel disease.
        J Pediatr Gastroenterol Nutr. 2014; 59: e27-29
        • Kaemmerer E.
        • Westerkamp M.
        • Kasperk R.
        • Niepmann G.
        • Scherer A.
        • Gassler N.
        Coincidence of active Crohn’s disease and florid endometriosis in the terminal ileum: a case report.
        World J Gastroenterol. 2013; 19: 4413-4417
        • Oldani A.
        • Monni M.
        • Gentilli S.
        Ileal endometriosis and Crohn’s disease: an unusual association causing acute bowel obstruction.
        Ann Ital Chir. 2016; 87
        • Klein L.J.
        • Pendse A.A.
        • Mittenzwei R.
        Defying Occam’s razor: colonic luminal endometriosis in an adolescent with Crohn’s disease.
        J Adolesc Health. 2019; (pii: S1054-139X(19)30476-30478): 23
        • Ong S.Y.
        • Johnston M.
        • Crowley P.
        Gastrointestinal: refractory ulcerative colitis complicated by colonic stricturing endometriosis.
        J Gastroenterol Hepatol. 2012; 27: 181
        • Terracciano F.
        • Scalisi G.
        • Attino V.
        • Biscaglia G.
        A rare case of sigmoid colon obstruction in patient with ulcerative colitis: role of transabdominal ultrasound-guided biopsy.
        J Ultrasound. 2015; 18: 411-414
        • Nakao A.
        • Iwagaki H.
        • Kanagawa T.
        • Jikuhara A.
        • Matsubara N.
        • Takakura N.
        • et al.
        Crohn’s disease mimicking as bowel endometriosis. Are the symptoms reduced by nafarelin acetate?.
        Arch Gynecol Obstet. 2000; 263: 131-133
        • Teke Z.1
        • Aytekin F.O.
        • Atalay A.O.
        • Demirkan N.C.
        Crohn’s disease complicated by multiple stenoses and internal fistulas clinically mimicking small bowel endometriosis.
        World J Gastroenterol. 2008; 14: 146-151
        • Jess T.
        • Frisch M.
        • Jørgensen K.T.
        • Pedersen B.V.
        • Nielsen N.M.
        Increased risk of inflammatory bowel disease in women with endometriosis: a nationwide Danish cohort study.
        Gut. 2012; 61: 1279-1283
        • Greenbaum H.
        • Weil C.
        • Chodick G.
        • Shalev V.
        • Eisenberg V.H.
        Evidence for an association between endometriosis, fibromyalgia, and autoimmune diseases.
        Am J Reprod Immunol. 2019; 81
        • Porpora M.G.
        • Scaramuzzino S.
        • Sangiuliano C.
        • Piacenti I.
        • Bonanni V.
        • Piccioni M.G.
        • et al.
        High prevalence of autoimmune diseases in women with endometriosis: a case-control study.
        Gynecol Endocrinol. 2019; https://doi.org/10.1080/09513590.2019.1655727
        • de Silva P.S.
        • Hansen H.H.
        • Wehberg S.
        • Friedman S.
        Nørgård BM.RIsk of ectopic pregnancy in women with inflammatory bowel disease: a 22-year nationwide cohort study.
        Clin Gastroenterol Hepatol. 2018; 16: 83-89
        • Yantiss R.K.
        • Clement P.B.
        • Young R.H.
        Endometriosis of the intestinal tract: a study of 44 cases of a disease that may cause diverse challenges in clinical and pathologic evaluation.
        Am J Surg Pathol. 2001; 25: 445-454
        • Craninx M.
        • D’Haens G.
        • Cokelaere K.
        • Baert F.
        • Penninckx F.
        • D’Hoore A.
        • et al.
        Crohn’s disease and intestinal endometriosis: an intriguing co-existence.
        Eur J Gastroenterol Hepatol. 2000; 12: 217-221
        • Guadagno A.
        • Grillo F.
        • Vellone V.G.
        • Ferrero S.
        • Fasoli A.
        • Fiocca R.
        • et al.
        Intestinal endometriosis: mimicker of inflammatory bowel disease?.
        Digestion. 2015; 92: 14-21
        • Lee K.K.
        • Jharap B.
        • Maser E.A.
        • Colombel J.-F.
        Impact of concomitant endometriosis on phenotype and natural history of inflammatory bowel disease.
        Inflamm Bowel Dis. 2016; 22: 159-163
        • Nnoaham K.E.
        • Hummelshoj L.
        • Webster P.
        • d’Hooghe T.
        • de Cicco Nardone F.
        • de CiccoNardone C.
        Impact of endometriosis on quality of life and work productivity: a multicenter study across ten countries.
        Fertil Steril. 2011; 96: 366-373
        • Cornish J.A.
        • Tan E.
        • Simillis C.
        • Clark S.K.
        • Teare J.
        • Tekkis P.P.
        The risk of oral contraceptives in the etiology of inflammatory bowel disease: a meta-analysis.
        Am J Gastroenterol. 2008; 103: 2394-2400
        • Felder J.B.
        • Korelitz B.I.
        • Rajapakse R.
        • Schwarz S.
        • Horatagis A.P.
        • Gleim G.
        Effects of nonsteroidal anti-inflammatory drugs on inflammatory bowel disease: a case-control study.
        Am J Gastroenterol. 2000; 95: 1949-1954
        • Borghini R.
        • Porpora M.G.
        • Casale R.
        • Marina M.
        • Palmieri E.
        • Greco N.
        • et al.
        Irritable bowel syndrome-like disorders in endometriosis: prevalence of nickel sensitivity and effects of a low-nickel diet. An Open-Label Pilot Study.
        Nutrients. 2020; 12: E341