Association between Cigarette Smoking Status and Composition of Gut Microbiota: Population-Based Cross-Sectional Study
Tóm tắt
There have been few large-scale studies on the relationship between smoking and gut microbiota. We investigated the relationship between smoking status and the composition of gut microbiota. This was a population-based cross-sectional study using Healthcare Screening Center cohort data. A total of 758 men were selected and divided into three groups: never (n = 288), former (n = 267), and current smokers (n = 203). Among the three groups, there was no difference in alpha diversity, however, Jaccard-based beta diversity showed significant difference (p = 0.015). Pairwise permutational multivariate analysis of variance (PERMANOVA) tests between never and former smokers did not show a difference; however, there was significant difference between never and current smokers (p = 0.017) and between former and current smokers (p = 0.011). Weighted UniFrac-based beta diversity also showed significant difference among the three groups (p = 0.038), and pairwise PERMANOVA analysis of never and current smokers showed significant difference (p = 0.01). In the analysis of bacterial composition, current smokers had an increased proportion of the phylum Bacteroidetes with decreased Firmicutes and Proteobacteria compared with never smokers, whereas there were no differences between former and never smokers. In conclusion, gut microbiota composition of current smokers was significantly different from that of never smokers. Additionally, there was no difference in gut microbiota composition between never and former smokers.
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Tài liệu tham khảo
Alberg, 2014, The 2014 surgeon general’s report: Commemorating the 50th anniversary of the 1964 report of the advisory committee to the us surgeon general and updating the evidence on the health consequences of cigarette smoking, Am. J. Epidemiol., 179, 403, 10.1093/aje/kwt335
Centers for Disease Control and Prevention (US), National Center for Chronic Disease Prevention and Health Promotion (US), and Office on Smoking and Health (US) (2010). Publications and Reports of the Surgeon General. How Tobacco Smoke Causes Disease: The Biology and Behavioral Basis for Smoking-Attributable Disease: A Report of the Surgeon General.
Bilano, 2015, Global trends and projections for tobacco use, 1990–2025: An analysis of smoking indicators from the who comprehensive information systems for tobacco control, Lancet, 385, 966, 10.1016/S0140-6736(15)60264-1
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
Biedermann, 2014, Smoking cessation alters intestinal microbiota: Insights from quantitative investigations on human fecal samples using fish, Inflamm. Bowel Dis., 20, 1496, 10.1097/MIB.0000000000000129
Biedermann, L., Zeitz, J., Mwinyi, J., Sutter-Minder, E., Rehman, A., Ott, S.J., Steurer-Stey, C., Frei, A., Frei, P., and Scharl, M. (2013). Smoking cessation induces profound changes in the composition of the intestinal microbiota in humans. PLoS ONE, 8.
Browne, 2017, Transmission of the gut microbiota: Spreading of health, Nat. Rev. Microbiol., 15, 531, 10.1038/nrmicro.2017.50
Thomas, 2017, The host microbiome regulates and maintains human health: A primer and perspective for non-microbiologists, Cancer Res., 77, 1783, 10.1158/0008-5472.CAN-16-2929
Claus, 2016, The gut microbiota: A major player in the toxicity of environmental pollutants?, NPJ Biofilms Microbiomes, 2, 16003, 10.1038/npjbiofilms.2016.3
Faith, 2013, The long-term stability of the human gut microbiota, Science, 341, 1237439, 10.1126/science.1237439
Zhang, H., Diao, H., Jia, L., Yuan, Y., Thamm, D.H., Wang, H., Jin, Y., Pei, S., Zhou, B., and Yu, F. (2017). Proteus mirabilis inhibits cancer growth and pulmonary metastasis in a mouse breast cancer model. PLoS ONE, 12.
Gilbert, 2016, Microbiome-wide association studies link dynamic microbial consortia to disease, Nature, 535, 94, 10.1038/nature18850
Ley, 2010, Obesity and the human microbiome, Curr. Opin. Gastroenterol., 26, 5, 10.1097/MOG.0b013e328333d751
Capurso, 2017, The interaction between smoking, alcohol and the gut microbiome, Best Pract. Res. Clin. Gastroenterol., 31, 579, 10.1016/j.bpg.2017.10.006
Rogers, M.A., Greene, M.T., Saint, S., Chenoweth, C.E., Malani, P.N., Trivedi, I., and Aronoff, D.M. (2012). Higher rates of clostridium difficile infection among smokers. PLoS ONE, 7.
Frank, 2007, Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases, Proc. Natl. Acad. Sci. USA, 104, 13780, 10.1073/pnas.0706625104
Quigley, 2017, Gut microbiome as a clinical tool in gastrointestinal disease management: Are we there yet?, Nat. Rev. Gastroenterol. Hepatol., 14, 315, 10.1038/nrgastro.2017.29
Parkes, 2014, Smoking in inflammatory bowel disease: Impact on disease course and insights into the aetiology of its effect, J. Crohns Colitis, 8, 717, 10.1016/j.crohns.2014.02.002
Kim, 2018, Correlation between gut microbiota and personality in adults: A cross-sectional study, Brain Behav. Immun., 69, 374, 10.1016/j.bbi.2017.12.012
Fadrosh, 2014, An improved dual-indexing approach for multiplexed 16s rrna gene sequencing on the illumina miseq platform, Microbiome, 2, 6, 10.1186/2049-2618-2-6
Kozich, 2013, Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the miseq illumina sequencing platform, Appl. Environ. Microbiol., 79, 5112, 10.1128/AEM.01043-13
Edgar, 2013, Uparse: Highly accurate otu sequences from microbial amplicon reads, Nat. Methods, 10, 996, 10.1038/nmeth.2604
Gonzalez, 2013, Advancing our understanding of the human microbiome using QIIME, Methods Enzymol., 531, 371, 10.1016/B978-0-12-407863-5.00019-8
Chao, 2003, Nonparametric estimation of shannon’s index of diversity when there are unseen species in sample, Environ. Ecol. Stat., 10, 429, 10.1023/A:1026096204727
Lozupone, 2011, Unifrac: An effective distance metric for microbial community comparison, ISME J., 5, 169, 10.1038/ismej.2010.133
Mandal, 2015, Analysis of composition of microbiomes: A novel method for studying microbial composition, Microb. Ecol. Health Dis., 26, 27663
Wu, 2016, Cigarette smoking and the oral microbiome in a large study of american adults, ISME J., 10, 2435, 10.1038/ismej.2016.37
Opstelten, 2016, Gut microbial diversity is reduced in smokers with Crohn’s disease, Inflamm. Bowel Dis., 22, 2070, 10.1097/MIB.0000000000000875
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
Ley, 2006, Microbial ecology: Human gut microbes associated with obesity, Nature, 444, 1022, 10.1038/4441022a
Koliada, A., Syzenko, G., Moseiko, V., Budovska, L., Puchkov, K., Perederiy, V., Gavalko, Y., Dorofeyev, A., Romanenko, M., and Tkach, S. (2017). Association between body mass index and firmicutes/bacteroidetes ratio in an adult ukrainian population. BMC Microbiol., 17.
Jha, 2014, Global effects of smoking, of quitting, and of taxing tobacco, N. Engl. J. Med., 370, 60, 10.1056/NEJMra1308383
Tomoda, 2011, Cigarette smoke decreases organic acids levels and population of bifidobacterium in the caecum of rats, J. Toxicol. Sci., 36, 261, 10.2131/jts.36.261
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
Zijlstra, 1994, Effect of nicotine on rectal mucus and mucosal eicosanoids, Gut, 35, 247, 10.1136/gut.35.2.247
Verschuere, 2011, Cigarette smoking alters epithelial apoptosis and immune composition in murine galt, Lab. Investig., 91, 1056, 10.1038/labinvest.2011.74
Eliakim, 2002, Chronic nicotine administration differentially alters jejunal and colonic inflammation in interleukin-10 deficient mice, Eur. J. Gastroenterol. Hepatol., 14, 607, 10.1097/00042737-200206000-00005
Chi, 2017, Nicotine alters the gut microbiome and metabolites of gut-brain interactions in a sex-specific manner, Chem. Res. Toxicol., 30, 2110, 10.1021/acs.chemrestox.7b00162
Jandhyala, 2015, Role of the normal gut microbiota, World J. Gastroenterol., 21, 8787, 10.3748/wjg.v21.i29.8787
Sopori, 2002, Effects of cigarette smoke on the immune system, Nat. Rev. Immunol., 2, 372, 10.1038/nri803
Fachi, 2016, Regulation of immune cell function by short-chain fatty acids, Clin. Transl. Immunol., 5, e73, 10.1038/cti.2016.17
Johnson, 2017, Microbiome and metabolic disease: Revisiting the bacterial phylum bacteroidetes, J. Mol. Med., 95, 1, 10.1007/s00109-016-1492-2
Morrison, 2016, Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism, Gut Microbes, 7, 189, 10.1080/19490976.2015.1134082
Mariat, D., Firmesse, O., Levenez, F., Guimaraes, V., Sokol, H., Dore, J., Corthier, G., and Furet, J.P. (2009). The firmicutes/bacteroidetes ratio of the human microbiota changes with age. BMC Microbiol., 9.
Choi, 2014, Trends in cigarette smoking among adolescents and adults in South Korea, Epidemiol. Health, 36, e2014023, 10.4178/epih/e2014023