The Association Between Smoking and Gut Microbiome in Bangladesh

Nicotine and Tobacco Research - Tập 22 Số 8 - Trang 1339-1346 - 2020
Rachel Nolan-Kenney1,2, Fen Wu1,2, Jiyuan Hu1,2, Liying Yang3,4,5, Dervla Kelly6, Huilin Li1,2, Farzana Jasmine7, Muhammad G. Kibriya7, Faruque Parvez8, Ishrat Shaheen9, Golam Sarwar9, Alauddin Ahmed9, Mahbubul Eunus9, Tariqul Islam10, Zhiheng Pei3,4,5, Habibul Ahsan7, Yu Chen1,2
1Department of Environmental Medicine, New York University School of Medicine, New York, NY
2Department of Population Health, New York University School of Medicine, New York, NY
3Department of Medicine, New York University School of Medicine, New York, NY;
4Department of Pathology, New York University School of Medicine, New York, NY
5The Department of Veterans Affairs New York Harbor Healthcare System, New York, NY
6Health Research Institute, Graduate Entry Medical School, University of Limerick, Limerick, Ireland
7Department of Public Health Sciences, Institute for Population and Precision Health, The University of Chicago, Chicago, IL
8Department of Environmental Health Sciences, Mailman School of Public Health, Columbia University, New York, NY
9Department of Informatics, U-Chicago Research Bangladesh, Ltd., Dhaka, Bangladesh
10Department of Health, Research & Training, U-Chicago Research Bangladesh, Ltd., Dhaka, Bangladesh

Tóm tắt

AbstractIntroductionEpidemiological studies that investigate alterations in the gut microbial composition associated with smoking are lacking. This study examined the composition of the gut microbiome in smokers compared with nonsmokers.Aims and MethodsStool samples were collected in a cross-sectional study of 249 participants selected from the Health Effects of Arsenic Longitudinal Study in Bangladesh. Microbial DNA was extracted from the fecal samples and sequenced by 16S rRNA gene sequencing. The associations of smoking status and intensity of smoking with the relative abundance or the absence and presence of individual bacterial taxon from phylum to genus levels were examined.ResultsThe relative abundance of bacterial taxa along the Erysipelotrichi-to-Catenibacterium lineage was significantly higher in current smokers compared to never-smokers. The odds ratio comparing the mean relative abundance in current smokers with that in never-smokers was 1.91 (95% confidence interval = 1.36–2.69) for the genus Catenibacterium and 1.89 (95% confidence interval = 1.39–2.56) for the family Erysipelotrichaceae, the order Erysipelotrichale, and the class Erysipelotrichi (false discovery rate-adjusted p values = .0008–.01). A dose–response association was observed for each of these bacterial taxa. The presence of Alphaproteobacteria was significantly greater comparing current with never-smokers (odds ratio = 4.85, false discovery rate-adjusted p values = .04).ConclusionsOur data in a Bangladeshi population are consistent with evidence of an association between smoking status and dosage with change in the gut bacterial composition.ImplicationsThis study for the first time examined the relationship between smoking and the gut microbiome composition. The data suggest that smoking status may play an important role in the composition of the gut microbiome, especially among individuals with higher levels of tobacco exposure.

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Tài liệu tham khảo

Mathers, 2006, Projections of global mortality and burden of disease from 2002 to 2030, PLoS Med., 3, e442, 10.1371/journal.pmed.0030442

Cohen, 1981, Smoking, health, and survival: prospects in Bangladesh, Lancet., 1, 1090, 10.1016/S0140-6736(81)92251-0

World-Health-Organization

Wu, 2013, A prospective study of tobacco smoking and mortality in Bangladesh, PLoS One., 8, e58516, 10.1371/journal.pone.0058516

Gill, 2006, Metagenomic analysis of the human distal gut microbiome, Science., 312, 1355, 10.1126/science.1124234

Clavel, 2014, Intestinal microbiota in metabolic diseases: from bacterial community structure and functions to species of pathophysiological relevance, Gut Microbes., 5, 544, 10.4161/gmic.29331

Kobayashi, 2013, Identification of heavy smokers through their intestinal microbiota by data mining analysis, Biosci Microbiota Food Health., 32, 77, 10.12938/bmfh.32.77

Wu, 2016, Cigarette smoking and the oral microbiome in a large study of American adults, ISME J., 10, 2435, 10.1038/ismej.2016.37

Lim, 2016, Analysis of the association between host genetics, smoking, and sputum microbiota in healthy humans, Sci Rep., 6, 23745, 10.1038/srep23745

Mason, 2015, The subgingival microbiome of clinically healthy current and never smokers, ISME J., 9, 268, 10.1038/ismej.2014.114

Vogtmann, 2015, Association between tobacco use and the upper gastrointestinal microbiome among Chinese men, Cancer Causes Control., 26, 581, 10.1007/s10552-015-0535-2

Cox, 2011, The upper airway microbiome of smokers, ex-smokers and never-smokers in busselton, Western Australia, 183

Ramakrishnan, 2015, Impact of cigarette smoking on the middle meatus microbiome in health and chronic rhinosinusitis, Int Forum Allergy Rhinol., 5, 981, 10.1002/alr.21626

Einarsson, 2016, Community dynamics and the lower airway microbiota in stable chronic obstructive pulmonary disease, smokers and healthy non-smokers, Thorax., 71, 795, 10.1136/thoraxjnl-2015-207235

Allais, 2016, Chronic cigarette smoke exposure induces microbial and inflammatory shifts and mucin changes in the murine gut, Environ Microbiol., 18, 1352, 10.1111/1462-2920.12934

Benjamin, 2012, Smokers with active Crohn’s disease have a clinically relevant dysbiosis of the gastrointestinal microbiota, Inflamm Bowel Dis., 18, 1092, 10.1002/ibd.21864

Opstelten, 2016, Gut microbial diversity is reduced in smokers with Crohn’s disease, Inflamm Bowel Dis., 22, 2070, 10.1097/MIB.0000000000000875

Biedermann, 2013, Smoking cessation induces profound changes in the composition of the intestinal microbiota in humans, PLoS One., 8, e59260, 10.1371/journal.pone.0059260

Ahsan, 2006, Health Effects of Arsenic Longitudinal Study (HEALS): description of a multidisciplinary epidemiologic investigation, J Expo Sci Environ Epidemiol., 16, 191, 10.1038/sj.jea.7500449

Yang, 2009, Inflammation and intestinal metaplasia of the distal esophagus are associated with alterations in the microbiome, Gastroenterology., 137, 588, 10.1053/j.gastro.2009.04.046

Caporaso, 2010, QIIME allows analysis of high-throughput community sequencing data, Nat Methods., 7, 335, 10.1038/nmeth.f.303

Haas, 2011, Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons, Genome Res., 21, 494, 10.1101/gr.112730.110

Edgar, 2010, Search and clustering orders of magnitude faster than BLAST, Bioinformatics., 26, 2460, 10.1093/bioinformatics/btq461

Wang, 2007, Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy, Appl Environ Microbiol., 73, 5261, 10.1128/AEM.00062-07

McMurdie, 2013, phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data, PLoS One., 8, e61217, 10.1371/journal.pone.0061217

Lozupone, 2008, Species divergence and the measurement of microbial diversity, FEMS Microbiol Rev., 32, 557, 10.1111/j.1574-6976.2008.00111.x

Lozupone, 2005, UniFrac: a new phylogenetic method for comparing microbial communities, Appl Environ Microbiol., 71, 8228, 10.1128/AEM.71.12.8228-8235.2005

Lozupone, 2007, Quantitative and qualitative beta diversity measures lead to different insights into factors that structure microbial communities, Appl Environ Microbiol., 73, 1576, 10.1128/AEM.01996-06

Bray, 1957, An ordination of upland forest communities of southern Wisconsin, Ecol Monogr., 27, 249, 10.2307/1942268

Zhao, 2015, Testing in microbiome-profiling studies with MiRKAT, the Microbiome Regression-Based Kernel Association Test, Am J Hum Genet., 96, 797, 10.1016/j.ajhg.2015.04.003

Peng, 2016, Zero-inflated beta regression for differential abundance analysis with metagenomics data, J Comput Biol., 23, 102, 10.1089/cmb.2015.0157

Benjamini, 1995, Controlling the false discovery rate—a practical and powerful approach to multiple testing, J Roy Stat Soc B Met., 57, 289, 10.1111/j.2517-6161.1995.tb02031.x

Asnicar, 2015, Compact graphical representation of phylogenetic data and metadata with GraPhlAn, PeerJ., 3, e1029, 10.7717/peerj.1029

Sapkota, 2010, Human pathogens abundant in the bacterial metagenome of cigarettes, Environ Health Perspect., 118, 351, 10.1289/ehp.0901201

Wang, 2012, Side-stream smoking reduces intestinal inflammation and increases expression of tight junction proteins, World J Gastroenterol., 18, 2180, 10.3748/wjg.v18.i18.2180

Talukder, 2011, Chronic cigarette smoking causes hypertension, increased oxidative stress, impaired NO bioavailability, endothelial dysfunction, and cardiac remodeling in mice, Am J Physiol Heart Circ Physiol., 300, H388, 10.1152/ajpheart.00868.2010

Tharappel, 2010, Effects of cigarette smoke on the activation of oxidative stress-related transcription factors in female A/J mouse lung, J Toxicol Environ Health A., 73, 1288, 10.1080/15287394.2010.484708

Vallès, 2018, Types of tobacco consumption and the oral microbiome in the United Arab Emirates Healthy Future (UAEHFS) pilot study, Sci Rep., 8, 11327, 10.1038/s41598-018-29730-x

Gautam, 2011, Effect of cigarette smoking on the periodontal health status: a comparative, cross sectional study, J Indian Soc Periodontol., 15, 383, 10.4103/0972-124X.92575

Rad, 2010, Effect of long-term smoking on whole-mouth salivary flow rate and oral health, J Dent Res Dent Clin Dent Prospects., 4, 110

Zhang, 2013, Human gut microbiota changes reveal the progression of glucose intolerance, PLoS One., 8, e71108, 10.1371/journal.pone.0071108

Lambeth, 2015, Composition, diversity and abundance of gut microbiome in prediabetes and type 2 diabetes, J Diabetes Obes., 2, 1

Karlsson, 2012, Symptomatic atherosclerosis is associated with an altered gut metagenome, Nat Commun., 3, 1245, 10.1038/ncomms2266

Shin, 2016, Lifestyle and geographic insights into the distinct gut microbiota in elderly women from two different geographic locations, J Physiol Anthropol., 35, 31, 10.1186/s40101-016-0121-7

Greiner, 2011, Effects of the gut microbiota on obesity and glucose homeostasis, Trends Endocrinol Metab., 22, 117, 10.1016/j.tem.2011.01.002

Dinh, 2015, Intestinal microbiota, microbial translocation, and systemic inflammation in chronic HIV infection, J Infect Dis., 211, 19, 10.1093/infdis/jiu409

Kaakoush, 2015, Insights into the role of erysipelotrichaceae in the human host, Front Cell Infect Microbiol., 5, 84, 10.3389/fcimb.2015.00084

Cho, 2016, Quantification of Slackia and Eggerthella spp. in human feces and adhesion of representatives strains to Caco-2 cells, Front Microbiol., 7, 658, 10.3389/fmicb.2016.00658

Boyle, 2010, Effects of cigarette smoke on the human oral mucosal transcriptome, Cancer Prev Res (Phila)., 3, 266, 10.1158/1940-6207.CAPR-09-0192

Ugai, 2019, Association of BMI, smoking and alcohol with multiple myeloma mortality in Asians: a pooled analysis of more than 800,000 participants in the Asia Cohort Consortium, Cancer Epidemiol Biomarkers Prev., 10.1158/1055-9965.EPI-19-0389

Fowke, 2015, Associations of body mass index, smoking, and alcohol consumption with prostate cancer mortality in the Asia Cohort Consortium, Am J Epidemiol., 182, 381, 10.1093/aje/kwv089

Yang, 2019, Tobacco smoking and mortality in Asia: a pooled meta-analysis, JAMA Netw Open., 2, e191474, 10.1001/jamanetworkopen.2019.1474