Obesity is associated with decreased risk of microscopic colitis in women

Robert S Sandler, Temitope O Keku, John T Woosley, Dale P Sandler, Joseph A Galanko, Anne F Peery, Robert S Sandler, Temitope O Keku, John T Woosley, Dale P Sandler, Joseph A Galanko, Anne F Peery

Abstract

Background: Microscopic colitis is a leading cause of diarrhea in the older adults. There is limited information about risk factors. We hypothesized that obesity would be associated with microscopic colitis.

Aim: To examine the association between obesity and microscopic colitis in men and women undergoing colonoscopy.

Methods: We conducted a case-control study at the University of North Carolina Hospitals. We identified and enrolled men and women referred for elective, outpatient colonoscopy for chronic diarrhea. We excluded patients with a past diagnosis of Crohn's disease or ulcerative colitis. A research pathologist reviewed biopsies on every patient and classified them as microscopic colitis cases or non-microscopic colitis controls. Patients provided information on body weight, height and exposure to medications via structured interviews or Internet based forms. The analysis included 110 patients with microscopic colitis (cases) and 252 non-microscopic colitis controls. Multivariable analyses were performed using logistic regression to estimate odds ratios and 95% confidence intervals.

Results: Cases were older and more likely than controls to be white race. Study subjects were well educated, but cases were better educated than controls. Cases with microscopic colitis had lower body mass index than controls and reported more weight loss after the onset of diarrhea. Compared to patients who were normal or under-weight, obese (BMI > 30 kg/m2) patients were substantially less likely to have microscopic colitis after adjusting for age and education, adjusted OR (aOR) 0.35, 95% confidence interval (CI) 0.18-0.66). When stratified by sex, the association was limited to obese women, aOR 0.21, 95%CI: 0.10-0.45. Patients with microscopic colitis were more likely to report weight loss after the onset of diarrhea. After stratifying by weight loss, there remained a strong inverse association between obesity and microscopic colitis, aOR 0.33, 95%CI: 0.10 - 1.11 among the patients who did not lose weight. Ever use of birth control pills was associated with lower risk of microscopic colitis after adjusting for age, education and BMI, aOR 0.38, 95%CI: 0.17-0.84.

Conclusion: Compared to controls also seen for diarrhea, microscopic colitis cases were less likely to be obese. Mechanisms are unknown but could involve hormonal effects of obesity or the gut microbiome.

Keywords: Colitis; Diarrhea/epidemiology; Humans; Microscopic/epidemiology; Obesity.

Conflict of interest statement

Conflict-of-interest statement: Disclosures: None of the authors have financial, professional or personal conflicts of interest.

©The Author(s) 2022. Published by Baishideng Publishing Group Inc. All rights reserved.

References

    1. Miehlke S, Guagnozzi D, Zabana Y, Tontini GE, Kanstrup Fiehn AM, Wildt S, Bohr J, Bonderup O, Bouma G, D'Amato M, Heiberg Engel PJ, Fernandez-Banares F, Macaigne G, Hjortswang H, Hultgren-Hornquist E, Koulaouzidis A, Kupcinskas J, Landolfi S, Latella G, Lucendo A, Lyutakov I, Madisch A, Magro F, Marlicz W, Mihaly E, Munck LK, Ostvik AE, Patai AV, Penchev P, Skonieczna-Zydecka K, Verhaegh B, Munch A. European guidelines on microscopic colitis: United European Gastroenterology and European Microscopic Colitis Group statements and recommendations. United European Gastroenterol J . 2021
    1. Lindstrom CG. Collagenous colitis' with watery diarrhoea--a new entity? Pathol Eur. 1976;11:87–89.
    1. Read NW, Krejs GJ, Read MG, Santa Ana CA, Morawski SG, Fordtran JS. Chronic diarrhea of unknown origin. Gastroenterology. 1980;78:264–271.
    1. Weimers P, Ankersen DV, Lophaven S, Bonderup OK, Münch A, Løkkegaard ECL, Burisch J, Munkholm P. Incidence and prevalence of microscopic colitis between 2001 and 2016: A Danish nationwide cohort study. J Crohns Colitis. 2020
    1. Bergman D, Clements MS, Khalili H, Agréus L, Hultcrantz R, Ludvigsson JF. A nationwide cohort study of the incidence of microscopic colitis in Sweden. Aliment Pharmacol Ther. 2019;49:1395–1400.
    1. Davidson S, Sjöberg K, Engel PJH, Lo Rinc E, Fiehn AK, Vigren L, Munck LK. Microscopic colitis in Denmark and Sweden: incidence, putative risk factors, histological assessment and endoscopic activity. Scand J Gastroenterol. 2018;53:818–824.
    1. Gentile NM, Yen EF. The Incidence of Microscopic Colitis: Microscopic No More. Dig Dis Sci. 2017;62:1394–1395.
    1. Park T, Cave D, Marshall C. Microscopic colitis: A review of etiology, treatment and refractory disease. World J Gastroenterol. 2015;21:8804–8810.
    1. Jaruvongvanich V, Poonsombudlert K, Ungprasert P. Smoking and Risk of Microscopic Colitis: A Systematic Review and Meta-analysis. Inflamm Bowel Dis. 2019;25:672–678.
    1. Burke KE, Ananthakrishnan AN, Lochhead P, Olen O, Ludvigsson JF, Richter JM, Chan AT, Khalili H. Smoking is Associated with an Increased Risk of Microscopic Colitis: Results From Two Large Prospective Cohort Studies of US Women. J Crohns Colitis. 2018;12:559–567.
    1. Vigren L, Tysk C, Ström M, Kilander AF, Hjortswang H, Bohr J, Benoni C, Larson L, Sjöberg K. Celiac disease and other autoimmune diseases in patients with collagenous colitis. Scand J Gastroenterol. 2013;48:944–950.
    1. Liu PH, Burke KE, Ananthakrishnan AN, Lochhead P, Olen O, Ludvigsson JF, Richter JM, Chan AT, Khalili H. Obesity and Weight Gain Since Early Adulthood Are Associated With a Lower Risk of Microscopic Colitis. Clin Gastroenterol Hepatol. 2019;17:2523–2532.e1.
    1. Cotter TG, Binder M, Harper EP, Smyrk TC, Pardi DS. Optimization of a Scoring System to Predict Microscopic Colitis in a Cohort of Patients With Chronic Diarrhea. J Clin Gastroenterol. 2017;51:228–234.
    1. Lewis SJ, Heaton KW. Stool form scale as a useful guide to intestinal transit time. Scand J Gastroenterol. 1997;32:920–924.
    1. Sandler RS, Keku TO, Woosley JT, Galanko JA, Peery AF. Medication use and microscopic colitis. Aliment Pharmacol Ther. 2021;54:1193–1201.
    1. Greenland S, Pearl J, Robins JM. Causal diagrams for epidemiologic research. Epidemiology. 1999;10:37–48.
    1. Larsson JK, Sonestedt E, Ohlsson B, Manjer J, Sjöberg K. The association between the intake of specific dietary components and lifestyle factors and microscopic colitis. Eur J Clin Nutr. 2016;70:1309–1317.
    1. Pascua MF, Kedia P, Weiner MG, Holmes J, Ellenberg J, Lewis JD. Microscopic colitis and Medication Use. Clin Med Insights Gastroenterol. 2010;2010:11–19.
    1. Morgan DM, Cao Y, Miller K, McGoldrick J, Bellavance D, Chin SM, Halvorsen S, Maxner B, Richter JM, Sassi S, Burke KE, Yarze JC, Ludvigsson JF, Staller K, Chung DC, Khalili H. Microscopic Colitis Is Characterized by Intestinal Dysbiosis. Clin Gastroenterol Hepatol. 2020;18:984–986.
    1. Roth B, Manjer J, Ohlsson B. Microscopic colitis and reproductive factors related to exposure to estrogens and progesterone. Drug Target Insights. 2013;7:53–62.
    1. Kane JS, Rotimi O, Everett SM, Samji S, Michelotti F, Ford AC. Development and validation of a scoring system to identify patients with microscopic colitis. Clin Gastroenterol Hepatol. 2015;13:1125–1131.
    1. Kane JS, Sood R, Law GR, Gracie DJ, To N, Gold MJ, Ford AC. Validation and modification of a diagnostic scoring system to predict microscopic colitis. Scand J Gastroenterol. 2016;51:1206–1212.
    1. Audrain-McGovern J, Benowitz NL. Cigarette smoking, nicotine, and body weight. Clin Pharmacol Ther. 2011;90:164–168.
    1. Pickett-Blakely O. Obesity and irritable bowel syndrome: a comprehensive review. Gastroenterol Hepatol . 2014;10:411–416.
    1. Pasquali R. Obesity and androgens: facts and perspectives. Fertil Steril. 2006;85:1319–1340.
    1. Pasquali R, Oriolo C. Obesity and Androgens in Women. Front Horm Res. 2019;53:120–134.
    1. Maruvada P, Leone V, Kaplan LM, Chang EB. The Human Microbiome and Obesity: Moving beyond Associations. Cell Host Microbe. 2017;22:589–599.
    1. Hertz S, Durack J, Kirk KF, Nielsen HL, Lin DL, Fadrosh D, Lynch K, Piceno Y, Thorlacius-Ussing O, Nielsen H, Lynch SV. Microscopic Colitis Patients Possess a Perturbed and Inflammatory Gut Microbiota. Dig Dis Sci . 2021
    1. Rindom Krogsgaard L, Kristian Munck L, Bytzer P, Wildt S. An altered composition of the microbiome in microscopic colitis is driven towards the composition in healthy controls by treatment with budesonide. Scand J Gastroenterol. 2019;54:446–452.
    1. Yoon K, Kim N. Roles of Sex Hormones and Gender in the Gut Microbiota. J Neurogastroenterol Motil. 2021;27:314–325.
    1. Burke KE, Ananthakrishnan AN, Lochhead P, Liu PH, Olen O, Ludvigsson JF, Richter JM, Tworoger SS, Chan AT, Khalili H. Identification of Menopausal and Reproductive Risk Factors for Microscopic Colitis-Results From the Nurses' Health Study. Gastroenterology. 2018;155:1764–1775.e2.
    1. Verhaegh BPM, Pierik MJ, Goudkade D, Cuijpers YSMT, Masclee AAM, Jonkers DMAE. Early Life Exposure, Lifestyle, and Comorbidity as Risk Factors for Microscopic Colitis: A Case-Control Study. Inflamm Bowel Dis. 2017;23:1040–1046.
    1. Braniste V, Leveque M, Buisson-Brenac C, Bueno L, Fioramonti J, Houdeau E. Oestradiol decreases colonic permeability through oestrogen receptor beta-mediated up-regulation of occludin and junctional adhesion molecule-A in epithelial cells. J Physiol. 2009;587:3317–3328.
    1. Angum F, Khan T, Kaler J, Siddiqui L, Hussain A. The Prevalence of Autoimmune Disorders in Women: A Narrative Review. Cureus. 2020;12:e8094.
    1. Williams WV. Hormonal contraception and the development of autoimmunity: A review of the literature. Linacre Q. 2017;84:275–295.
    1. Sonnenberg A, Turner KO, Genta RM. Associations of Microscopic Colitis With Other Lymphocytic Disorders of the Gastrointestinal Tract. Clin Gastroenterol Hepatol. 2018;16:1762–1767.
    1. Green HD, Beaumont RN, Thomas A, Hamilton B, Wood AR, Sharp S, Jones SE, Tyrrell J, Walker G, Goodhand J, Kennedy NA, Ahmad T, Weedon MN. Genome-Wide Association Study of Microscopic Colitis in the UK Biobank Confirms Immune-Related Pathogenesis. J Crohns Colitis. 2019;13:1578–1582.
    1. Masclee GM, Coloma PM, Kuipers EJ, Sturkenboom MC. Increased risk of microscopic colitis with use of proton pump inhibitors and non-steroidal anti-inflammatory drugs. Am J Gastroenterol. 2015;110:749–759.
    1. Gentile NM, Khanna S, Loftus EV, Jr , Smyrk TC, Tremaine WJ, Harmsen WS, Zinsmeister AR, Kammer PP, Pardi DS. The epidemiology of microscopic colitis in Olmsted County from 2002 to 2010: a population-based study. Clin Gastroenterol Hepatol . 2014;12:838–842.
    1. Fernández-Bañares F, de Sousa MR, Salas A, Beltrán B, Piqueras M, Iglesias E, Gisbert JP, Lobo B, Puig-Diví V, García-Planella E, Ordás I, Andreu M, Calvo M, Montoro M, Esteve M, Viver JM RECOMINA Project, GETECCU Grupo Español de Enfermedades de Crohn y Colitis Ulcerosa. Epidemiological risk factors in microscopic colitis: a prospective case-control study. Inflamm Bowel Dis. 2013;19:411–417.
    1. Rasmussen MA, Munck LK. Systematic review: are lymphocytic colitis and collagenous colitis two subtypes of the same disease - microscopic colitis? Aliment Pharmacol Ther. 2012;36:79–90.
    1. Gado AS, Ebeid BA, El Hindawi AA, Akl MM, Axon AT. Prevalence of microscopic colitis in patients with chronic diarrhea in Egypt: a single-center study. Saudi J Gastroenterol. 2011;17:383–386.
    1. Inoue Y, Qin B, Poti J, Sokol R, Gordon-Larsen P. Epidemiology of Obesity in Adults: Latest Trends. Curr Obes Rep. 2018;7:276–288.
    1. Tome J, Sehgal K, Kamboj AK, Harmsen WS, Kammer PP, Loftus EV, Jr , Tremaine WJ, Khanna S, Pardi DS. The Epidemiology of Microscopic Colitis in Olmsted County, Minnesota: Population-Based Study From 2011 to 2019. Clin Gastroenterol Hepatol. 2021

Source: PubMed

3
Suscribir