Skip to main content
Top
Published in: Respiratory Research 1/2018

Open Access 01-12-2018 | Research

Effects of smoking on the lower respiratory tract microbiome in mice

Authors: Rui Zhang, Ling Chen, Lei Cao, Kang-jie Li, Yao Huang, Xiao-qian Luan, Ge Li

Published in: Respiratory Research | Issue 1/2018

Login to get access

Abstract

Background

Recent studies break with traditional opinion that the lower respiratory tract is sterile, and increasingly focus on the lung microbiome and disease. Smoking, as an important etiology of inflammatory lung disease, was considered as a factor influencing lung microbiome variations in our study, and we aimed to study the effect of smoking on inflammation and microbial diversity and community.

Methods

Forty male mice were selected and randomly divided into a smoking and a non-smoking group. Mice in the smoking group were exposed to smoke smog for 2 h/day for 90 days. Blood and lung tissues were obtained after the experiment, and ELISA was used to measure interleukin-6 and C reactive protein concentrations. 16S rRNA gene quantification and sequencing technology were used to compare microbial diversity and community between the two groups. SAS 9.1 and R software were used to analyze the data.

Results

Thirty-six mice survived, and the weight of the smoking group increased more slowly than that of the non-smoking group. Denser inflammation and congestion were observed in the lungs of the smoking mice compared with the non-smoking group Higher microbial diversity was observed in the smoking group, and Enterobacter, Acidimicrobiales_norank, and Caulobacteraceae_Unclassified genus were significantly more abundant in the non-smoking group (P < 0.001).

Conclusions

Smoking altered microbial diversities and communities in the lower respiratory tract of mice. Microbial variation should be considered in future studies focusing on smoking-induced inflammatory disease.
Literature
1.
go back to reference Laurenzi GA, Potter RT, Kass EH. Bacteriologic flora of the lower respiratory tract. N Engl J Med. 1961;265:1273–8.CrossRef Laurenzi GA, Potter RT, Kass EH. Bacteriologic flora of the lower respiratory tract. N Engl J Med. 1961;265:1273–8.CrossRef
2.
go back to reference Niederman MS, Sarois GA. Respiratory tract infections. Philadelphia: Lippincott Williams & Wilkins; 2005. Niederman MS, Sarois GA. Respiratory tract infections. Philadelphia: Lippincott Williams & Wilkins; 2005.
3.
go back to reference Pecora DV. A comparison of transtracheal aspiration with other methods of determining the bacterial flora of the lower respiratory tract. N Engl J Med. 1963;269:664–6.CrossRef Pecora DV. A comparison of transtracheal aspiration with other methods of determining the bacterial flora of the lower respiratory tract. N Engl J Med. 1963;269:664–6.CrossRef
4.
go back to reference Murphy TF, Brauer AL, Schiffmacher AT, Sethi S. Persistent colonization by Haemophilus influenza in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2004;170:266–72.CrossRef Murphy TF, Brauer AL, Schiffmacher AT, Sethi S. Persistent colonization by Haemophilus influenza in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2004;170:266–72.CrossRef
5.
go back to reference Dickson RP, Erb Downward JR, Freeman CM, Walker N, Scales BS, Beck JM, et al. Changes in the lung microbiome following lung transplantation include the emergence of two distinct pseudomonas species with distinct clinical associations. PLoS One. 2014;9(5):e97214.CrossRef Dickson RP, Erb Downward JR, Freeman CM, Walker N, Scales BS, Beck JM, et al. Changes in the lung microbiome following lung transplantation include the emergence of two distinct pseudomonas species with distinct clinical associations. PLoS One. 2014;9(5):e97214.CrossRef
6.
go back to reference Maciej D, Maria S, Mariusz B, Joanna Ś, Janusz K. Bronchial bacterial colonization in patients with lung cancer. Advances in Respiratory Medicine. 2009;77(3):242–7. Maciej D, Maria S, Mariusz B, Joanna Ś, Janusz K. Bronchial bacterial colonization in patients with lung cancer. Advances in Respiratory Medicine. 2009;77(3):242–7.
7.
go back to reference Hilty M, Burke C, Pedro H, Cardenas P, Bush A, Bossley C, et al. Disordered microbial communities in asthmatic airways. PLoS One. 2010;5(1):1–9.CrossRef Hilty M, Burke C, Pedro H, Cardenas P, Bush A, Bossley C, et al. Disordered microbial communities in asthmatic airways. PLoS One. 2010;5(1):1–9.CrossRef
8.
go back to reference Gleeson K, Eggli DF, Maxwell SL. Quantitative aspiration during sleep in normal subjects. Chest. 1997;111(5):1266–72.CrossRef Gleeson K, Eggli DF, Maxwell SL. Quantitative aspiration during sleep in normal subjects. Chest. 1997;111(5):1266–72.CrossRef
9.
go back to reference Huxley EJ, Viroslav J, Gray WR, Pierce AK. Pharyngeal aspiration in normal adults and patients with depressed consciousness. Am J Med. 1978;64(4):564–8.CrossRef Huxley EJ, Viroslav J, Gray WR, Pierce AK. Pharyngeal aspiration in normal adults and patients with depressed consciousness. Am J Med. 1978;64(4):564–8.CrossRef
10.
go back to reference Morris A, Beck JM, Schloss PD, Campbell TB, Crothers K, Curtis JL, et al. Comparison of the respiratory microbiome in healthy non-smokers and smokers. Am J Respir Crit Care Med. 2013;187(10):1067–75.CrossRef Morris A, Beck JM, Schloss PD, Campbell TB, Crothers K, Curtis JL, et al. Comparison of the respiratory microbiome in healthy non-smokers and smokers. Am J Respir Crit Care Med. 2013;187(10):1067–75.CrossRef
11.
go back to reference Bowers RM, Sullivan AP, Costello EK, Collett JL Jr, Knight R, Fierer N. Sources of bacteria in outdoor air across cities in the midwestern United States. Appl Environ Microbiol. 2011;77(18):6350–6.CrossRef Bowers RM, Sullivan AP, Costello EK, Collett JL Jr, Knight R, Fierer N. Sources of bacteria in outdoor air across cities in the midwestern United States. Appl Environ Microbiol. 2011;77(18):6350–6.CrossRef
12.
go back to reference Bertolini V, Gandolfi I, Ambrosini R, Bestetti G, Innocente E, Rampazzo G, et al. Temporal variability and effect of environmental variables on airborne bacterial communities in an urban area of northern Italy. Appl Microbiol Biotechnol. 2013;97(14):6561–70.CrossRef Bertolini V, Gandolfi I, Ambrosini R, Bestetti G, Innocente E, Rampazzo G, et al. Temporal variability and effect of environmental variables on airborne bacterial communities in an urban area of northern Italy. Appl Microbiol Biotechnol. 2013;97(14):6561–70.CrossRef
13.
go back to reference Lighthart B. Mini-review of the concentration variations found in the alfresco atmospheric bacterial populations. Aerobiologia. 2000;16(1):7–16.CrossRef Lighthart B. Mini-review of the concentration variations found in the alfresco atmospheric bacterial populations. Aerobiologia. 2000;16(1):7–16.CrossRef
14.
go back to reference Erb-Downward JR, Thompson DL, Han MK, Freeman CM, McCloskey L, Schmidt LA, et al. Analysis of the Lung Microbiome in the “Healthy” Smoker and in COPD. PLoS ONE. 2011;6(2):1–12 15.CrossRef Erb-Downward JR, Thompson DL, Han MK, Freeman CM, McCloskey L, Schmidt LA, et al. Analysis of the Lung Microbiome in the “Healthy” Smoker and in COPD. PLoS ONE. 2011;6(2):1–12 15.CrossRef
15.
go back to reference Charlson ES, Bittinger K, Haas AR, Fitzgerald AS, Frank I, Yadav A, et al. topographical continuity of bacterial populations in the healthy human respiratory tract. Am J Respir Crit Care Med. 2011;184:957–96.CrossRef Charlson ES, Bittinger K, Haas AR, Fitzgerald AS, Frank I, Yadav A, et al. topographical continuity of bacterial populations in the healthy human respiratory tract. Am J Respir Crit Care Med. 2011;184:957–96.CrossRef
16.
go back to reference Oţelea M, Cappon IȘ, Neicu MG, Rașcu A. Smoking and work overload level. Pneumologia. 2016;65(4):225–30.PubMed Oţelea M, Cappon IȘ, Neicu MG, Rașcu A. Smoking and work overload level. Pneumologia. 2016;65(4):225–30.PubMed
17.
go back to reference American Cancer Society. Cancer facts and figures 2016. Atlanta: American Cancer Society; 2016. American Cancer Society. Cancer facts and figures 2016. Atlanta: American Cancer Society; 2016.
18.
go back to reference Brant LJ, Gordon-Salant S, Pearson JD, Klein LL, Morrell CH, Metter EJ, et al. Risk factors related to age-associated hearing loss in the speech frequencies. J Am Acad Audiol. 1996;7(3):152–60.PubMed Brant LJ, Gordon-Salant S, Pearson JD, Klein LL, Morrell CH, Metter EJ, et al. Risk factors related to age-associated hearing loss in the speech frequencies. J Am Acad Audiol. 1996;7(3):152–60.PubMed
19.
go back to reference Cosio MG, Saetta M, Agusti A. Immunologic aspects of chronic obstructive pulmonary disease. N Engl J Med. 2009;360:2445–54.CrossRef Cosio MG, Saetta M, Agusti A. Immunologic aspects of chronic obstructive pulmonary disease. N Engl J Med. 2009;360:2445–54.CrossRef
20.
go back to reference Billings J, Zeitel L, Lukomnick J, et al. Impact of socioeconomic status on hospital use in new York City. Health Aff. 1993;12:162–73.CrossRef Billings J, Zeitel L, Lukomnick J, et al. Impact of socioeconomic status on hospital use in new York City. Health Aff. 1993;12:162–73.CrossRef
21.
go back to reference Haines HM, Cynthia O, Pierce D, Bourke L. Notwithstanding high prevalence of overweight and obesity, smoking remains the Most important factor in poor self-rated health and hospital use in an Australian regional community. AIMS Public Health. 2017;4(4):402–17.CrossRef Haines HM, Cynthia O, Pierce D, Bourke L. Notwithstanding high prevalence of overweight and obesity, smoking remains the Most important factor in poor self-rated health and hospital use in an Australian regional community. AIMS Public Health. 2017;4(4):402–17.CrossRef
22.
go back to reference Fleischer NL, Lozano P, Arillo Santillán E, Reynales Shigematsu LM, Thrasher JF. The impact of neighborhood violence and social cohesion on smoking behaviors among a cohort of smokers in Mexico. J Epidemiol Community Health. 2015;69(11):1083–90.CrossRef Fleischer NL, Lozano P, Arillo Santillán E, Reynales Shigematsu LM, Thrasher JF. The impact of neighborhood violence and social cohesion on smoking behaviors among a cohort of smokers in Mexico. J Epidemiol Community Health. 2015;69(11):1083–90.CrossRef
23.
go back to reference Lee J, Taneja V, Vassallo R. Cigarette smoking and inflammation: cellular and molecular mechanisms. J Dent Res. 2012;91(2):142–9.CrossRef Lee J, Taneja V, Vassallo R. Cigarette smoking and inflammation: cellular and molecular mechanisms. J Dent Res. 2012;91(2):142–9.CrossRef
24.
go back to reference Churg A, Dai J, Tai H, Xie C, Wright JL. Tumor necrosis factor-alpha is central to acute cigarette smoke-induced inflammation and connective tissue breakdown. Am J Respir Crit Care Med. 2002;166:849–54.CrossRef Churg A, Dai J, Tai H, Xie C, Wright JL. Tumor necrosis factor-alpha is central to acute cigarette smoke-induced inflammation and connective tissue breakdown. Am J Respir Crit Care Med. 2002;166:849–54.CrossRef
25.
go back to reference Gualano RC, Hansen MJ, Vlahos R, Jones JE, Park-Jones RA, Deliyannis G, et al. Cigarette smoke worsens lung inflammation and impairs resolution of influenza infection in mice. Respir Res. 2008;9:53–69.CrossRef Gualano RC, Hansen MJ, Vlahos R, Jones JE, Park-Jones RA, Deliyannis G, et al. Cigarette smoke worsens lung inflammation and impairs resolution of influenza infection in mice. Respir Res. 2008;9:53–69.CrossRef
26.
go back to reference Vlahos R, Bozinovski S, Jones JE, Powell J, Gras J, Lilja A, et al. Differential protease, innate immunity, and NF-kappaB induction profiles during lung inflammation induced by subchronic cigarette smoke exposure in mice. American journal of physiology. Lung cellular and molecular physiology. 2006;290(5):L931–45.CrossRef Vlahos R, Bozinovski S, Jones JE, Powell J, Gras J, Lilja A, et al. Differential protease, innate immunity, and NF-kappaB induction profiles during lung inflammation induced by subchronic cigarette smoke exposure in mice. American journal of physiology. Lung cellular and molecular physiology. 2006;290(5):L931–45.CrossRef
27.
go back to reference Guerassimov A, Hoshino Y, Takubo Y, Turcotte A, Yamamoto M, Ghezzo H, et al. The development of emphysema in cigarette smoke exposed mice is strain dependent. Am J Respir Crit Care Med. 2004;170(9):974–80.CrossRef Guerassimov A, Hoshino Y, Takubo Y, Turcotte A, Yamamoto M, Ghezzo H, et al. The development of emphysema in cigarette smoke exposed mice is strain dependent. Am J Respir Crit Care Med. 2004;170(9):974–80.CrossRef
28.
go back to reference Matsuoka K, Kanai T. The gut microbiota and inflammatory bowel disease. Semin Immunopathol. 2015;37(1):47–55.CrossRef Matsuoka K, Kanai T. The gut microbiota and inflammatory bowel disease. Semin Immunopathol. 2015;37(1):47–55.CrossRef
29.
go back to reference Gotts JE, Chun LF, Abbott J, Fang X, Takasaki N, Nishimura SL, et al. Cigarette smoke exposure worsens acute lung injury in antibiotic-treated bacterial pneumonia in mice. American journal of physiology. Lung cellular and molecular physiology. 2018;3:1–11. Gotts JE, Chun LF, Abbott J, Fang X, Takasaki N, Nishimura SL, et al. Cigarette smoke exposure worsens acute lung injury in antibiotic-treated bacterial pneumonia in mice. American journal of physiology. Lung cellular and molecular physiology. 2018;3:1–11.
30.
go back to reference Abusleme L, Hong BY, Hoare A, Konkel JE, Diaz PI, Niki M. Moutsopoulos. Oral microbiome characterization in murine models. Bio-protocol. 2017;7(24):1–17.CrossRef Abusleme L, Hong BY, Hoare A, Konkel JE, Diaz PI, Niki M. Moutsopoulos. Oral microbiome characterization in murine models. Bio-protocol. 2017;7(24):1–17.CrossRef
31.
go back to reference Dang RY, Zhao CY, Fan X, Zhao ZL, Jiang XG, Li G. Effect of cigarette smoke on bacteria distribution of lower respiratory tract in mice. Shandong Medical Journal. 2018;58(20):9–12. Dang RY, Zhao CY, Fan X, Zhao ZL, Jiang XG, Li G. Effect of cigarette smoke on bacteria distribution of lower respiratory tract in mice. Shandong Medical Journal. 2018;58(20):9–12.
32.
go back to reference Murakami K, McGuire R, Cox RA, Jodoin JM, Bjertnaes LJ, Katahira J, et al. Heparin nebulization attenuates acute lung injury in Sepsis following smoke inhalation in sheep. Shock. 2002;18(3):236–41.CrossRef Murakami K, McGuire R, Cox RA, Jodoin JM, Bjertnaes LJ, Katahira J, et al. Heparin nebulization attenuates acute lung injury in Sepsis following smoke inhalation in sheep. Shock. 2002;18(3):236–41.CrossRef
33.
go back to reference Mason KL, Erb Downward JR, Mason KD, Falkowski NR, Eaton KA, Kao JY, et al. Candida albicans and bacterial microbiota interactions in the cecum during recolonization following broad-spectrum antibiotic therapy. Infect Immun. 2012;80:3371–80.CrossRef Mason KL, Erb Downward JR, Mason KD, Falkowski NR, Eaton KA, Kao JY, et al. Candida albicans and bacterial microbiota interactions in the cecum during recolonization following broad-spectrum antibiotic therapy. Infect Immun. 2012;80:3371–80.CrossRef
34.
go back to reference Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A. 2011;108(Suppl 1):4516–22.CrossRef Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A. 2011;108(Suppl 1):4516–22.CrossRef
35.
go back to reference Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol. 2013;79:5112–20.CrossRef Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol. 2013;79:5112–20.CrossRef
36.
go back to reference Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009;75:7537–41.CrossRef Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009;75:7537–41.CrossRef
38.
go back to reference Amato KR, Yeoman CJ, Kent A, Righini N, Carbonero F, Estrada A, et al. Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes. The ISME Journal. 2013;7:1344–53.CrossRef Amato KR, Yeoman CJ, Kent A, Righini N, Carbonero F, Estrada A, et al. Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes. The ISME Journal. 2013;7:1344–53.CrossRef
39.
go back to reference Lozupone C, Lladser ME, Knights D, Stombaugh J, Knight R. UniFrac: an effective distance metric for microbial community comparison. The ISME Journal. 2011;5:169–72.CrossRef Lozupone C, Lladser ME, Knights D, Stombaugh J, Knight R. UniFrac: an effective distance metric for microbial community comparison. The ISME Journal. 2011;5:169–72.CrossRef
40.
go back to reference Dickson RP, Erb-Downward JR, Freeman CM, McCloskey L, Falkowski NR, Huffnagle GB, et al. Bacterial topography of the healthy human lower respiratory tract. MBio. 2017;8:1–12.CrossRef Dickson RP, Erb-Downward JR, Freeman CM, McCloskey L, Falkowski NR, Huffnagle GB, et al. Bacterial topography of the healthy human lower respiratory tract. MBio. 2017;8:1–12.CrossRef
41.
go back to reference Dickson RP, Erb-Downward JR, Martinez FJ, Huffnagle GB. The Microbiome and the Respiratory Tract. Annu Rev Physiol. 2016;78:481–504. Dickson RP, Erb-Downward JR, Martinez FJ, Huffnagle GB. The Microbiome and the Respiratory Tract. Annu Rev Physiol. 2016;78:481–504.
42.
go back to reference Cox MJ, Allgaier M, Taylor B, Baek MS, Huang YJ, Daly RA, Lynch SV, et al. Airway microbiota and pathogen abundance in age-stratified cystic fibrosis patients. PLoS One. 2010;5:e11044.CrossRef Cox MJ, Allgaier M, Taylor B, Baek MS, Huang YJ, Daly RA, Lynch SV, et al. Airway microbiota and pathogen abundance in age-stratified cystic fibrosis patients. PLoS One. 2010;5:e11044.CrossRef
43.
go back to reference Iwai S, Huang D, Fong S, Jarlsberg LG, Worodria W, Yoo S, et al. The lung microbiome of Ugandan HIV-infected pneumonia patients is compositionally and functionally distinct from that of san Franciscan patients. PLoS One. 2014;9:e95726.CrossRef Iwai S, Huang D, Fong S, Jarlsberg LG, Worodria W, Yoo S, et al. The lung microbiome of Ugandan HIV-infected pneumonia patients is compositionally and functionally distinct from that of san Franciscan patients. PLoS One. 2014;9:e95726.CrossRef
44.
go back to reference Garcia-Nunez M, Millares L, Pomares X, Ferrari R, Perez-Brocal V, Gallego M, et al. Severity-related changes of bronchial microbiome in chronic obstructive pulmonary disease. J Clin Microbiol. 2014;52:4217–23.CrossRef Garcia-Nunez M, Millares L, Pomares X, Ferrari R, Perez-Brocal V, Gallego M, et al. Severity-related changes of bronchial microbiome in chronic obstructive pulmonary disease. J Clin Microbiol. 2014;52:4217–23.CrossRef
45.
go back to reference Dickson RP, Singer BH, Newstead MW, Falkowski NR, Erb-Downward JR, Standiford TJ, et al. Enrichment of the lung microbiome with gut bacteria in sepsis and the acute respiratory distress syndrome. Nature microbiology. 2016;1:16113.CrossRef Dickson RP, Singer BH, Newstead MW, Falkowski NR, Erb-Downward JR, Standiford TJ, et al. Enrichment of the lung microbiome with gut bacteria in sepsis and the acute respiratory distress syndrome. Nature microbiology. 2016;1:16113.CrossRef
46.
go back to reference Rogers GB, Zain NM, Bruce KD, Burr LD, Chen AC, Rivett DW, et al. A novel microbiota stratification system predicts future exacerbations in bronchiectasis. Annals of the American Thoracic Society. 2014;11:496–503.CrossRef Rogers GB, Zain NM, Bruce KD, Burr LD, Chen AC, Rivett DW, et al. A novel microbiota stratification system predicts future exacerbations in bronchiectasis. Annals of the American Thoracic Society. 2014;11:496–503.CrossRef
47.
go back to reference Molyneaux PL, Cox MJ, Willis-Owen SA, Mallia P, Russell KE, Russell AM, et al. The role of bacteria in the pathogenesis and progression of idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2014;190:906–13.CrossRef Molyneaux PL, Cox MJ, Willis-Owen SA, Mallia P, Russell KE, Russell AM, et al. The role of bacteria in the pathogenesis and progression of idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2014;190:906–13.CrossRef
48.
go back to reference Han MK, Zhou Y, Murray S, Tayob N, Noth I, Lama VN, et al. Lung microbiome and disease progression in idiopathic pulmonary fibrosis: an analysis of the COMET study. Lancet Respir Med. 2014;2:548–56.CrossRef Han MK, Zhou Y, Murray S, Tayob N, Noth I, Lama VN, et al. Lung microbiome and disease progression in idiopathic pulmonary fibrosis: an analysis of the COMET study. Lancet Respir Med. 2014;2:548–56.CrossRef
49.
go back to reference Nayak SK. Probiotics and immunity: a fish perspective. Fish & shellfish immunology. 2010;29:2–14.CrossRef Nayak SK. Probiotics and immunity: a fish perspective. Fish & shellfish immunology. 2010;29:2–14.CrossRef
51.
go back to reference Little MA, Klesges RC, Bursac Z, Ebbert JO, Halbert JP, Dunkle AN, et al. Why Don't Cancer survivors quit smoking? An evaluation of readiness for smoking cessation in Cancer survivors. Journal of cancer prevention. 2018;23(1):44–50.CrossRef Little MA, Klesges RC, Bursac Z, Ebbert JO, Halbert JP, Dunkle AN, et al. Why Don't Cancer survivors quit smoking? An evaluation of readiness for smoking cessation in Cancer survivors. Journal of cancer prevention. 2018;23(1):44–50.CrossRef
52.
go back to reference Kim G, Song H, Park K, Noh H, Lee E, Lee H, et al. Association of Time to first morning cigarette and chronic obstructive pulmonary disease measured by spirometry in current smokers. Korean journal of family medicine. 2018;39(2):67–73.CrossRef Kim G, Song H, Park K, Noh H, Lee E, Lee H, et al. Association of Time to first morning cigarette and chronic obstructive pulmonary disease measured by spirometry in current smokers. Korean journal of family medicine. 2018;39(2):67–73.CrossRef
53.
go back to reference Margaritopoulos GA, Vasarmidi E, Jacob J, Wells AU, Antoniou KM. Smoking and interstitial lung diseases. Eur Respir Rev: 2015;24(137):428–435. d. Margaritopoulos GA, Vasarmidi E, Jacob J, Wells AU, Antoniou KM. Smoking and interstitial lung diseases. Eur Respir Rev: 2015;24(137):428–435. d.
54.
go back to reference Sopori M. Effects of cigarette smoke on the immune system. Nat Rev Immunol. 2002;2:372–7.CrossRef Sopori M. Effects of cigarette smoke on the immune system. Nat Rev Immunol. 2002;2:372–7.CrossRef
55.
go back to reference Tvedt T, Ersvaer E, Tveita AA, Bruserud O. Interleukin-6 in allogeneic stem cell transplantation: its possible importance for immune regulation and as a therapeutic target. Front Immunology. 2017;8:667.CrossRef Tvedt T, Ersvaer E, Tveita AA, Bruserud O. Interleukin-6 in allogeneic stem cell transplantation: its possible importance for immune regulation and as a therapeutic target. Front Immunology. 2017;8:667.CrossRef
56.
go back to reference Granet C, Miossec P. Combination of the pro-inflammatory cytokines IL-1,TNF-alpha and IL-17 leads to enhanced expression and additional recruitment of AP-1 family members,Egr-1 and NF-kappaB in osteoblast-like cells. Cytokine. 2004;26(4):169–77.CrossRef Granet C, Miossec P. Combination of the pro-inflammatory cytokines IL-1,TNF-alpha and IL-17 leads to enhanced expression and additional recruitment of AP-1 family members,Egr-1 and NF-kappaB in osteoblast-like cells. Cytokine. 2004;26(4):169–77.CrossRef
57.
go back to reference Davé S, Van Dyke TE. The link between periodontal disease and cardiovascular disease is probably inflammation. Oral Dis. 2008;14:95–101.CrossRef Davé S, Van Dyke TE. The link between periodontal disease and cardiovascular disease is probably inflammation. Oral Dis. 2008;14:95–101.CrossRef
58.
go back to reference Ridker PM. Inflammatory biomarkers and risks of myocardial infarction, stroke, diabetes, and total mortality: implications for longevity. Nutr Rev. 2007;65:S253–9.CrossRef Ridker PM. Inflammatory biomarkers and risks of myocardial infarction, stroke, diabetes, and total mortality: implications for longevity. Nutr Rev. 2007;65:S253–9.CrossRef
59.
go back to reference Mendall MA, Patel P, Asante M, Ballam L, Morris J, Strachan DP, et al. Relation of serum cytokine concentrations to cardiovascular risk factors and coronary heart disease. Heart. 1997;78:273–7.CrossRef Mendall MA, Patel P, Asante M, Ballam L, Morris J, Strachan DP, et al. Relation of serum cytokine concentrations to cardiovascular risk factors and coronary heart disease. Heart. 1997;78:273–7.CrossRef
60.
go back to reference Monsó E. Microbiome in chronic obstructive pulmonary disease. Annals Translation Medicine. 2017;5(12):251.CrossRef Monsó E. Microbiome in chronic obstructive pulmonary disease. Annals Translation Medicine. 2017;5(12):251.CrossRef
61.
go back to reference Molyneaux PL, Maher TM. The role of infection in the pathogenesis of idiopathic pulmonary fibrosis. Eur Respir Rev. 2013;22:376–81.CrossRef Molyneaux PL, Maher TM. The role of infection in the pathogenesis of idiopathic pulmonary fibrosis. Eur Respir Rev. 2013;22:376–81.CrossRef
62.
go back to reference Yu GQ, Phillips S, Gail MH, Goedert JJ, Humphrys MS, Ravel J, et al. The effect of cigarette smoking on the oral and nasal microbiota. Microbiome. 2017;5:1–6.CrossRef Yu GQ, Phillips S, Gail MH, Goedert JJ, Humphrys MS, Ravel J, et al. The effect of cigarette smoking on the oral and nasal microbiota. Microbiome. 2017;5:1–6.CrossRef
63.
go back to reference Russell SL, Gold MJ, Willing BP, Thorson L, McNagny KM, Finlay BB. Perinatal antibiotic treatment affects murine microbiota, immune responses and allergic asthma. Gut Microbes. 2013;4(02):158–64.CrossRef Russell SL, Gold MJ, Willing BP, Thorson L, McNagny KM, Finlay BB. Perinatal antibiotic treatment affects murine microbiota, immune responses and allergic asthma. Gut Microbes. 2013;4(02):158–64.CrossRef
64.
go back to reference Sze MA, Dimitriu PA, Hayashi S, Elliott WM, McDonough JE, Gosselink JV, et al. The lung tissue microbiome in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2012;185(10):1073–80.CrossRef Sze MA, Dimitriu PA, Hayashi S, Elliott WM, McDonough JE, Gosselink JV, et al. The lung tissue microbiome in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2012;185(10):1073–80.CrossRef
65.
go back to reference Huang YJ, Kim E, Cox MJ, Brodie EL, Brown R, Wiener-Kronish JP, et al. A persistent and diverse airway microbiota present during chronic obstructive pulmonary disease exacerbations. OMICS International. 2010;14:9–16.CrossRef Huang YJ, Kim E, Cox MJ, Brodie EL, Brown R, Wiener-Kronish JP, et al. A persistent and diverse airway microbiota present during chronic obstructive pulmonary disease exacerbations. OMICS International. 2010;14:9–16.CrossRef
Metadata
Title
Effects of smoking on the lower respiratory tract microbiome in mice
Authors
Rui Zhang
Ling Chen
Lei Cao
Kang-jie Li
Yao Huang
Xiao-qian Luan
Ge Li
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Respiratory Research / Issue 1/2018
Electronic ISSN: 1465-993X
DOI
https://doi.org/10.1186/s12931-018-0959-9

Other articles of this Issue 1/2018

Respiratory Research 1/2018 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine