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      The Influence of Second-Hand Cigarette Smoke Exposure during Childhood and Active Cigarette Smoking on Crohn’s Disease Phenotype Defined by the Montreal Classification Scheme in a Western Cape Population, South Africa

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          Abstract

          Background

          Smoking may worsen the disease outcomes in patients with Crohn’s disease (CD), however the effect of exposure to second-hand cigarette smoke during childhood is unclear. In South Africa, no such literature exists. The aim of this study was to investigate whether disease phenotype, at time of diagnosis of CD, was associated with exposure to second-hand cigarette during childhood and active cigarette smoking habits.

          Methods

          A cross sectional examination of all consecutive CD patients seen during the period September 2011-January 2013 at 2 large inflammatory bowel disease centers in the Western Cape, South Africa was performed. Data were collected via review of patient case notes, interviewer-administered questionnaire and clinical examination by the attending gastroenterologist. Disease phenotype (behavior and location) was evaluated at time of diagnosis, according to the Montreal Classification scheme. In addition, disease behavior was stratified as ‘complicated’ or ‘uncomplicated’, using predefined definitions. Passive cigarette smoke exposure was evaluated during 3 age intervals: 0–5, 6–10, and 11–18 years.

          Results

          One hundred and ninety four CD patients were identified. Cigarette smoking during the 6 months prior to, or at time of diagnosis was significantly associated with ileo-colonic (L3) disease (RRR = 3.63; 95%CI, 1.32–9.98, p = 0.012) and ileal (L1) disease (RRR = 3.54; 95%CI, 1.06–11.83, p = 0.040) compared with colonic disease. In smokers, childhood passive cigarette smoke exposure during the 0–5 years age interval was significantly associated with ileo-colonic CD location (RRR = 21.3; 95%CI, 1.16–391.55, p = 0.040). No significant association between smoking habits and disease behavior at diagnosis, whether defined by the Montreal scheme, or stratified as ‘complicated’ vs ‘uncomplicated’, was observed.

          Conclusion

          Smoking habits were associated with ileo-colonic (L3) and ileal (L1) disease at time of diagnosis in a South African cohort.

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          Most cited references36

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          Spatial organization and composition of the mucosal flora in patients with inflammatory bowel disease.

          The composition and spatial organization of the mucosal flora in biopsy specimens from patients with inflammatory bowel disease (IBD; either Crohn's disease or ulcerative colitis), self-limiting colitis, irritable-bowel syndrome (IBS), and healthy controls were investigated by using a broad range of fluorescent bacterial group-specific rRNA-targeted oligonucleotide probes. Each group included 20 subjects. Ten patients who had IBD and who were being treated with antibiotics were also studied. Use of nonaqueous Carnoy fixative to preserve the mucus layer was crucial for detection of bacteria adherent to the mucosal surface (mucosal bacteria). No biofilm was detectable in formalin-fixed biopsy specimens. Mucosal bacteria were found at concentrations greater than 10(9)/ml in 90 to 95% of IBD patients, 95% of patients with self-limiting colitis, 65% of IBS patients, and 35% of healthy controls. The mean density of the mucosal biofilm was 2 powers higher in IBD patients than in patients with IBS or controls, and bacteria were mostly adherent. Bacteroides fragilis was responsible for >60% of the biofilm mass in patients with IBD but for only 30% of the biofilm mass in patients with self-limiting colitis and 40% of the biofilm in IBS patients but for <15% of the biofilm in IBD patients. In patients treated with (5-ASA) or antibiotics, the biofilm could be detected with 4,6-diamidino-2-phenylindole but did not hybridize with fluorescence in situ hybridization probes. A Bacteroides fragilis biofilm is the main feature of IBD. This was not previously recognized due to a lack of appropriate tissue fixation. Both 5-ASA and antibiotics suppress but do not eliminate the adherent biofilm.
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            Inflammatory bowel disease in Asia: a systematic review.

            The incidence and prevalence of inflammatory bowel diseases (IBD), Crohn's disease (CD) and ulcerative colitis (UC), are lower in Asia than in the West. However, across Asia the incidence and prevalence of IBD has increased rapidly over the last two to four decades. These changes may relate to increased contact with the West, westernization of diet, increasing antibiotics use, improved hygiene, vaccinations, or changes in the gut microbiota. Genetic factors also differ between Asians and the Caucasians. In Asia, UC is more prevalent than CD, although CD incidence is rapidly increasing in certain areas. There is a male predominance of CD in Asia, but a trend towards equal sex distribution for UC. IBD is diagnosed at a slightly older age than in the West, and there is rarely a second incidence peak as in the West. A positive family history is much less common than in the West, as are extra-intestinal disease manifestations. There are clear ethnic differences in incidence within countries in Asia, and an increased incidence in IBD in migrants from Asia to the West. Research in Asia, an area of rapidly changing IBD epidemiology, may lead to the discovery of critical etiologic factors that lead to the development of IBD. © 2012 Journal of Gastroenterology and Hepatology Foundation and Blackwell Publishing Asia Pty Ltd.
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              A population-based case control study of potential risk factors for IBD.

              We aimed to pursue potential etiological clues to Crohn's disease (CD) and ulcerative colitis (UC) through a population-based case control survey study. Cases with CD (n = 364) and UC (n = 217), ages 18-50 yr were drawn from the population-based University of Manitoba IBD Research Registry. Potential control subjects were drawn from the population-based Manitoba Health Registry by age, gender, and geographic residence matching to the cases (n = 433). Subjects were administered a multiitem questionnaire. By univariate analysis, some of the variables predictive of CD included lower likelihood of living on a farm, of having drunk unpasteurized milk or having eaten pork, and UC patients were less likely to have drunk unpasteurized milk and to have eaten pork. On multivariate analysis, variables significantly associated with CD were being Jewish (OR = 4.32, 95% CI 1.10-16.9), having a first degree relative with IBD (OR = 3.07, 95% CI 1.73-5.46), ever having smoked (OR = 1.54, 95% CI, 1.06-2.25), living longer with a smoker (OR = 1.03, 95% CI, 1.01-1.04). Being a first generation Canadian (OR = 0.33, 95% CI, 0.17-0.62), having pet cats before age 5 (OR = 0.66, 95% CI, 0.46-0.96) and having larger families (OR = 0.87, 95% CI, 0.79-0.96) were protective against CD. For UC being Jewish (OR = 7.46, 95% CI, 2.33-23.89), having a relative with IBD (OR = 2.23, 95% CI, 1.27-3.9), and ever smoking (OR = 1.62, 95% CI, 1.14-2.32) were predictive. This study reinforced the increased risk associated with family history, being Jewish, and smoking history, however, a number of significant associations with CD and UC on univariate and multivariate analysis may support the "hygiene hypothesis" and warrant further exploration in prospective studies.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                30 September 2015
                2015
                : 10
                : 9
                : e0139597
                Affiliations
                [1 ]Community Health Division, Department of Interdisciplinary Health Sciences, University of Stellenbosch, Cape Town, South Africa
                [2 ]Centre for Evidence-Based Health Care, Department of Interdisciplinary Health Sciences, University of Stellenbosch, Cape Town, South Africa
                [3 ]Department of Dietetics, University of the Western Cape, Cape Town, South Africa
                CWRU/UH Digestive Health Institute, UNITED STATES
                Author notes

                Competing Interests: This research was funded by a Scholarship in Gastroenterology; a grant from the AstraZeneca/South African Gastroenterology Society (SAGES) - recipient ARB. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The authors are not employees or consultants of the funders, in any capacity. This research is not involved in any products in development or any marketed products. The funders do not hold any copyright or patents in this research. The funding from the Scholarship in Gastroenterology; a grant from the AstraZeneca/South African Gastroenterology Society (SAGES) does not alter the authors' adherence to PLOS ONE policies on sharing data and materials.

                Conceived and designed the experiments: TC ARB. Performed the experiments: TC ARB. Analyzed the data: TC TME. Contributed reagents/materials/analysis tools: TC TME ARB. Wrote the paper: TC ARB.

                Article
                PONE-D-15-29877
                10.1371/journal.pone.0139597
                4589355
                26422615
                b262f396-ae84-4141-a893-c69ea809a6f6
                Copyright @ 2015

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 8 July 2015
                : 14 September 2015
                Page count
                Figures: 0, Tables: 4, Pages: 12
                Funding
                This study was supported by Scholarship in Gastroenterology; a grant from the AstraZeneca/South African Gastroenterology Society (SAGES) - recipient ARB. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Custom metadata
                Data has been made publicly available via Figshare at: ( http://dx.doi.org/10.6084/m9.figshare.1159053).

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