Scratching the surface – tobacco-induced bacterial biofilms
More details
Hide details
Departments of Microbiology and Immunology, University of Louisville, Louisville, USA
Oral Immunology and Infectious Diseases, University of Louisville, Louisville, USA
Pediatrics, Washington University School of Medicine, Saint Louis, USA
Submission date: 2014-07-15
Acceptance date: 2014-12-08
Publication date: 2015-02-10
Corresponding author
David A. Scott   

Oral Immunology and Infectious Diseases, University of Louisville, 501 South Preston Street, Louisville, KY 40292, USA
Tobacco Induced Diseases 2015;13(February):1
Individual environmental factors, such as iron, temperature and oxygen, are known to have a profound effect on bacterial phenotype. Therefore, it is surprising so little known is about the influence of chemically complex cigarette smoke on bacterial physiology. Recent evidence has demonstrated that tobacco smoke and components alter the bacterial surface and promote biofilm formation in several important human pathogens, including Staphylococcus aureus, Streptococcus mutans, Klebsiella pneumonia, Porphyromonas gingivalis and Pseudomonas aeruginosa. The mechanisms underlying this phenomenon and the relevance to increased susceptibility to infectious disease in smokers and to treatment are reviewed.
Bagaitkar J, Demuth DR, Scott DA. Tobacco use increases susceptibility to bacterial infection. Tob Induc Dis. 2008;4:12.
Rom O, Avezov K, Aizenbud D, Reznick AZ. Cigarette smoking and inflammation revisited. Respir Physiol Neurobiol. 2013;187(1):5–10.
Stampfli MR, Anderson GP. How cigarette smoke skews immune responses to promote infection, lung disease and cancer. Nat Rev Immunol. 2009;9(5):377–84.
Cogo K, Calvi BM, Mariano FS, Franco GC, Gonçalves RB, Groppo FC. The effects of nicotine and cotinine on Porphyromonas gingivalis colonisation of epithelial cells. Arch Oral Biol. 2009;54(11):1061–7.
Cogo K, Montan MF, Bergamaschi Cde C, D Andrade E, Rosalen PL, Groppo FC. In vitro evaluation of the effect of nicotine, cotinine, and caffeine on oral microorganisms. Can J Microbiol. 2008;54(6):501–8.
Bagaitkar J, Williams LR, Renaud DE, Bemakanakere MR, Martin M, Scott DA, et al. Tobacco-induced alterations to Porphyromonas gingivalis-host interactions. Environ Microbiol. 2009;11(5):1242–53.
Huang J, Carney BF, Denny TP, Weissinger AK, Schell MA. A complex network regulates expression of eps and other virulence genes of Pseudomonas solanacearum. J Bacteriol. 1995;177(5):1259–67.
Li M, Huang R, Zhou X, Zhang K, Zheng X, Gregory RL. Effect of nicotine on dual-species biofilms of Streptococcus mutans and Streptococcus sanguinis. FEMS Microbiol Lett. 2014;350(2):125–32.
Li MY, Huang RJ, Zhou XD, Gregory RL. Role of sortase in Streptococcus mutans under the effect of nicotine. Int J Oral Sci. 2013;5(4):206–11.
Roberts D, Cole P. Effect of tobacco and nicotine on growth of Haemophilus influenzae in vitro. J Clin Pathol. 1979;32(7):728–31.
Petrova OE, Sauer K. Sticky situations: key components that control bacterial surface attachment. J Bacteriol. 2012;194(10):2413–25.
O’Toole G, Kaplan HB, Kolter R. Biofilm formation as microbial development. Annu Rev Microbiol. 2000;54:49–79.
Martinez LC, Vadyvaloo V. Mechanisms of post-transcriptional gene regulation in bacterial biofilms. Front Cell Infect Microbiol. 2014;4:38.
Johnson LR. Microcolony and biofilm formation as a survival strategy for bacteria. J Theor Biol. 2008;251(1):24–34.
de la Fuente-Núñez C, Reffuveille F, Fernández L, Hancock RE. Bacterial biofilm development as a multicellular adaptation: antibiotic resistance and new therapeutic strategies. Curr Opin Microbiol. 2013;16(5):580–9.
Marks LR, RM Reddinger, and AP Hakansson. High levels of genetic recombination during nasopharyngeal carriage and biofilm formation in Streptococcus pneumoniae. MBio. 2012;3(5).
Marks LR, Parameswaran GI, Hakansson AP. Pneumococcal interactions with epithelial cells are crucial for optimal biofilm formation and colonization in vitro and in vivo. Infect Immun. 2012;80(8):2744–60.
Hall-Stoodley L, Stoodley P. Evolving concepts in biofilm infections. Cell Microbiol. 2009;11(7):1034–43.
Parsek MR, Singh PK. Bacterial biofilms: an emerging link to disease pathogenesis. Annu Rev Microbiol. 2003;57:677–701.
Zhao G, Usui ML, Lippman SI, James GA, Stewart PS, Fleckman P, et al. Biofilms and Inflammation in Chronic Wounds. Adv Wound Care (New Rochelle). 2013;2(7):389–99.
Belas R. Biofilms, flagella, and mechanosensing of surfaces by bacteria. Trends Microbiol. 2014.
Bjarnsholt T, Alhede M, Alhede M, Eickhardt-Sørensen SR, Moser C, Kühl M, et al. The in vivo biofilm. Trends Microbiol. 2013;21(9):466–74.
Sun F, Qu F, Ling Y, Mao P, Xia P, Chen H, et al. Biofilm-associated infections: antibiotic resistance and novel therapeutic strategies. Future Microbiol. 2013;8(7):877–86.
Van Acker H, Van Dijck P, Coenye T. Molecular mechanisms of antimicrobial tolerance and resistance in bacterial and fungal biofilms. Trends Microbiol. 2014;22(6):326–33.
Banin E, Vasil ML, Greenberg EP. Iron and Pseudomonas aeruginosa biofilm formation. Proc Natl Acad Sci U S A. 2005;102(31):11076–81.
Hostacka A, Ciznar I, Stefkovicova M. Temperature and pH affect the production of bacterial biofilm. Folia Microbiol (Praha). 2010;55(1):75–8.
Ramli NS, Eng Guan C, Nathan S, Vadivelu J. The effect of environmental conditions on biofilm formation of Burkholderia pseudomallei clinical isolates. PLoS One. 2012;7(9):e44104.
Wakabayashi H, Yamauchi K, Kobayashi T, Yaeshima T, Iwatsuki K, Yoshie H. Inhibitory effects of lactoferrin on growth and biofilm formation of Porphyromonas gingivalis and Prevotella intermedia. Antimicrob Agents Chemother. 2009;53(8):3308–16.
Goldstein-Daruech N, Cope EK, Zhao KQ, Vukovic K, Kofonow JM, Doghramji L, et al. Tobacco smoke mediated induction of sinonasal microbial biofilms. PLoS One. 2011;6(1):e15700.
Antunes MB, Chi JJ, Liu Z, Goldstein-Daruech N, Palmer JN, Zhu J, et al. Molecular basis of tobacco-induced bacterial biofilms: an in vitro study. Otolaryngol Head Neck Surg. 2012;147(5):876–84.
Bagaitkar J, Daep CA, Patel CK, Renaud DE, Demuth DR, Scott DA. Tobacco smoke augments Porphyromonas gingivalis - Streptococcus gordonii biofilm formation. PLoS One. 2011;6(11):e27386.
Kulkarni R, Antala S, Wang A, Amaral FE, Rampersaud R, Larussa SJ, et al. Cigarette smoke increases Staphylococcus aureus biofilm formation via oxidative stress. Infect Immun. 2012;80(11):3804–11.
Cockeran R, Herbert JA, Mitchell TJ, Dix-Peek T, Dickens C, Anderson R, et al. Exposure of a 23 F serotype strain of Streptococcus pneumoniae to cigarette smoke condensate is associated with selective upregulation of genes encoding the two-component regulatory system 11 (TCS11). Biomed Res Int. 2014;2014:976347.
Mutepe ND, Cockeran R, Steel HC, Theron AJ, Mitchell TJ, Feldman C, et al. Effects of cigarette smoke condensate on pneumococcal biofilm formation and pneumolysin. Eur Respir J. 2013;41(2):392–5.
Huang R, Li M, Gregory RL. Effect of nicotine on growth and metabolism of Streptococcus mutans. Eur J Oral Sci. 2012;120(4):319–25.
Baboni FB, Guariza Filho O, Moreno AN, Rosa EA. Influence of cigarette smoke condensate on cariogenic and candidal biofilm formation on orthodontic materials. Am J Orthod Dentofacial Orthop. 2010;138(4):427–34.
Grigg J, Walters H, Sohal SS, Wood-Baker R, Reid DW, Xu CB, et al. Cigarette smoke and platelet-activating factor receptor dependent adhesion of Streptococcus pneumoniae to lower airway cells. Thorax. 2012;67(10):908–13.
Teughels W, Van Eldere J, van Steenberghe D, Cassiman JJ, Fives-Taylor P, Quirynen M. Influence of nicotine and cotinine on epithelial colonization by periodontopathogens. J Periodontol. 2005;76(8):1315–22.
Benedetti G, Campus G, Strohmenger L, Lingström P. Tobacco and dental caries: a systematic review. Acta Odontol Scand. 2013;71(3–4):363–71.
Diaz PI. Microbial diversity and interactions in subgingival biofilm communities. Front Oral Biol. 2012;15:17–40.
Palmer RM, Wilson RF, Hasan AS, Scott DA. Mechanisms of action of environmental factors–tobacco smoking. J Clin Periodontol. 2005;32 Suppl 6:180–95.
Kumar PS, Matthews CR, Joshi V, de Jager M, Aspiras M. Tobacco smoking affects bacterial acquisition and colonization in oral biofilms. Infect Immun. 2011;79(11):4730–8.
Zeller I, Hutcherson JA, Lamont RJ, Demuth DR, Gumus P, Nizam N, et al. Altered Antigenic Profiling and Infectivity of Porphyromonas Gingivalis in Smokers and Non-Smokers With Periodontitis. J Periodontol. 2014;85:837–44.
Shchipkova AY, Nagaraja HN, Kumar PS. Subgingival microbial profiles of smokers with periodontitis. J Dent Res. 2010;89(11):1247–53.
Morris A, Beck JM, Schloss PD, Campbell TB, Crothers K, Curtis JL, et al. Comparison of the respiratory microbiome in healthy nonsmokers and smokers. Am J Respir Crit Care Med. 2013;187(10):1067–75.
Fullmer SC, Preshaw PM, Heasman PA, Kumar PS. Smoking cessation alters subgingival microbial recolonization. J Dent Res. 2009;88(6):524–8.
Zambon JJ, Grossi SG, Machtei EE, Ho AW, Dunford R, Genco RJ. Cigarette smoking increases the risk for subgingival infection with periodontal pathogens. J Periodontol. 1996;67(10 Suppl):1050–4.
Haffajee AD, Socransky SS. Relationship of cigarette smoking to the subgingival microbiota. J Clin Periodontol. 2001;28(5):377–88.
Eggert FM, McLeod MH, Flowerdew G. Effects of smoking and treatment status on periodontal bacteria: evidence that smoking influences control of periodontal bacteria at the mucosal surface of the gingival crevice. J Periodontol. 2001;72(9):1210–20.
Kamma JJ, Nakou M, Baehni PC. Clinical and microbiological characteristics of smokers with early onset periodontitis. J Periodontal Res. 1999;34(1):25–33.
Grossi SG, Goodson JM, Gunsolley JC, Otomo-Corgel J, Bland PS, Doherty F, et al. Mechanical therapy with adjunctive minocycline microspheres reduces red-complex bacteria in smokers. J Periodontol. 2007;78(9):1741–50.
Bagaitkar J, Demuth DR, Daep CA, Renaud DE, Pierce DL, Scott DA. Tobacco upregulates P. gingivalis fimbrial proteins which induce TLR2 hyposensitivity. PLoS One. 2010;5(5):e9323.
Kuboniwa M, Amano A, Hashino E, Yamamoto Y, Inaba H, Hamada N, et al. Distinct roles of long/short fimbriae and gingipains in homotypic biofilm development by Porphyromonas gingivalis. BMC Microbiol. 2009;9:105.
Darveau RP, Arbabi S, Garcia I, Bainbridge B, Maier RV. Porphyromonas gingivalis lipopolysaccharide is both agonist and antagonist for p38 mitogen-activated protein kinase activation. Infect Immun. 2002;70:1867–73.
Buduneli N, Larsson L, Biyikoglu B, Renaud DE, Bagaitkar J, Scott DA. Fatty acid profiles in smokers with chronic periodontitis. J Dent Res. 2011;90:47–52.
Regulation of Nicotine Tolerance by Quorum Sensing and High Efficiency of Quorum Quenching Under Nicotine Stress in Pseudomonas aeruginosa PAO1
Huiming Tang, Yunyun Zhang, Yifan Ma, Mengmeng Tang, Dongsheng Shen, Meizhen Wang
Frontiers in Cellular and Infection Microbiology
Who Opted Out of an Opt-Out Smoking-Cessation Programme for Hospitalised Patients?
Georges J. Nahhas, K. Michael Cummings, Vince Talbot, Matthew J. Carpenter, Benjamin A. Toll, Graham W. Warren
Journal of Smoking Cessation
Prevalence of Cigarette Smoking and Associated Factors among Male Citizens in Tehran, Iran
Aziz Kassani, Abdolvahab Baghbanian, Rostam Menati, Jafar Hassanzadeh, Mohsen Asadi-Lari, Walieh Menati
Asian Pacific Journal of Cancer Prevention
Inflammatory Mechanisms in Hidradenitis Suppurativa
G. Kelly, Errol P. Prens
Dermatologic Clinics
The association of active and secondhand smoking with oral health in adults: Japan public health center-based study
Masayuki Ueno, Satoko Ohara, Norie Sawada, Manami Inoue, Shoichiro Tsugane, Yoko Kawaguchi
Tobacco Induced Diseases
Ecophysiological consequences of alcoholism on human gut microbiota: implications for ethanol-related pathogenesis of colon cancer
Atsuki Tsuruya, Akika Kuwahara, Yuta Saito, Haruhiko Yamaguchi, Takahisa Tsubo, Shogo Suga, Makoto Inai, Yuichi Aoki, Seiji Takahashi, Eri Tsutsumi, Yoshihide Suwa, Hidetoshi Morita, Kenji Kinoshita, Yukari Totsuka, Wataru Suda, Kenshiro Oshima, Masahira Hattori, Takeshi Mizukami, Akira Yokoyama, Takefumi Shimoyama, Toru Nakayama
Scientific Reports
Pathophysiology of hidradenitis suppurativa: An update
Errol Prens, Inge Deckers
Journal of the American Academy of Dermatology
Cultural variation in antismoking video ads between the United States, Taiwan, and China
Tzu-Jung Wong, Jessica L. King, Jamie L. Pomeranz
Health Education Research
Site-specific treatment outcome in smokers following non-surgical and surgical periodontal therapy
Dagmar F. Bunaes, Stein Atle Lie, Morten Enersen, Anne Nordrehaug Aastrøm, Kamal Mustafa, Knut N. Leknes
Journal of Clinical Periodontology
Nicotine Enhances Staphylococcus epidermidis Biofilm Formation by Altering the Bacterial Autolysis, Extracellular DNA Releasing, and Polysaccharide Intercellular Adhesin Production
Yang Wu, Yue Ma, Tao Xu, Qing-zhao Zhang, Jinna Bai, Jiaxue Wang, Tao Zhu, Qiang Lou, Friedrich Götz, Di Qu, Chun-quan Zheng, Ke-qing Zhao
Frontiers in Microbiology
Nicotine enhances the thickness of biofilm and adherence of Candida albicans ATCC 14053 and Candida parapsilosis ATCC 22019
Shan Gunasegar, Wan Himratul-Aznita
FEMS Yeast Research
Effect of tobacco on periodontal disease and oral cancer
Yixin Zhang, Jinxiu He, Bing He, Ruijie Huang, Mingyun Li
Tobacco Induced Diseases
Cigarette smoke exposure redirects Staphylococcus aureus to a virulence profile associated with persistent infection
Alicia Lacoma, Andrew Edwards, Bernadette Young, José Domínguez, Cristina Prat, Maisem Laabei
Scientific Reports
Lyn regulates epithelial–mesenchymal transition in CS-exposed model through Smad2/3 signaling
Xiaobo Liang, Xiang He, Yin Li, Junyi Wang, Dehong Wu, Xiefang Yuan, Xiaoyun Wang, Guoping Li
Respiratory Research
Porphyromonas gingivalis genes conferring fitness in a tobacco‐rich environment
Justin Hutcherson, Himabindu Gogenini, Gwyneth Lamont, Daniel Miller, Zuzanna Nowakowska, Anna Lasica, Chengcheng Liu, Jan Potempa, Richard Lamont, Deborah Yoder‐Himes, David Scott
Molecular Oral Microbiology
A Comparison of Flavorless Electronic Cigarette-Generated Aerosol and Conventional Cigarette Smoke on the Planktonic Growth of Common Oral Commensal Streptococci
John Nelson, Giancarlo Cuadra, Dominic Palazzolo
International Journal of Environmental Research and Public Health
Effect of nicotine on Staphylococcus aureus biofilm formation and virulence factors
Le Shi, Yang Wu, Chen Yang, Yue Ma, Qing-zhao Zhang, Wei Huang, Xiao-yi Zhu, Ying-jie Yan, Jia-xue Wang, Tao Zhu, Di Qu, Chun-quan Zheng, Ke-Qing Zhao
Scientific Reports
The Effects of Self vs. Group Affirmation and Message Framing on College Students’ Vape-Free Campus Policy Support
Jungmi Jun, Taylor Wen, Linwan Wu
Health Communication
Environmental factors and periodontal microbiome
Nurcan Buduneli
Periodontology 2000
Effects of Cigarette Smoke Condensate on Growth and Biofilm Formation by Mycobacterium tuberculosis
Moloko Cholo, Sipho Rasehlo, Eudri Venter, Chantelle Venter, Ronald Anderson
BioMed Research International
Hidradenitis Suppurativa: Host-Microbe and Immune Pathogenesis Underlie Important Future Directions
Simon Jiang, Melodi Whitley, Paula Mariottoni, Tarannum Jaleel, Amanda MacLeod
JID Innovations
Cigarette Smoking and Opium Use in Relation to the Oral Microbiota in Iran
Zeni Wu, Yongli Han, J. Caporaso, Nicholas Bokulich, Ashraf Mohamadkhani, Alireza Moayyedkazemi, Xing Hua, Farin Kamangar, Yunhu Wan, Shalabh Suman, Bin Zhu, Amy Hutchinson, Casey Dagnall, Kristine Jones, Belynda Hicks, Jianxin Shi, Reza Malekzadeh, Christian Abnet, Akram Pourshams, Emily Vogtmann, Jan Claesen
Microbiology Spectrum
Microorganisms: crucial players of smokeless tobacco for several health attributes
Akanksha Vishwakarma, Digvijay Verma
Applied Microbiology and Biotechnology
Pasif Sigara İçiciliğinin Çocuklarda Sistemik ve Ağız-Diş Sağlığına Etkisi
Selcuk Dental Journal
The effect of cigarette smoke condensate ( CSC ) on Pseudomonas aeruginosa virulence and antibiotic sensitivity
Suzanne Abdelmalek, Shaheen Alhadad, Omar Abu‐Omar, Maram Afaneh, Luay Abu‐Qatouseh, Phillip Collier
Journal of Applied Microbiology
Innate immunity and microbial dysbiosis in hidradenitis suppurativa – vicious cycle of chronic inflammation
Divya Chopra, Rachel Arens, Watcharee Amornpairoj, Michelle Lowes, Marjana Tomic-Canic, Natasa Strbo, Hadar Lev-Tov, Irena Pastar
Frontiers in Immunology
Tobacco prevention and control interventions in humanitarian settings: a scoping review protocol
Nachiket Gudi, Ansuman Swain, Muralidhar Kulkarni, Sanjay Pattanshetty, Sanjay Zodpey
BMJ Open
NLRP3 inflammasome activation in cigarette smoke priming for Pseudomonas aeruginosa-induced acute lung injury
Alexis White, Zhengke Wang, Xing Wang, Michelle King, Cynthia Guo, Chris Mantsounga, Alfred Ayala, Alan Morrison, Gaurav Choudhary, Frank Sellke, Eboni Chambers, Lorraine Ware, Sharon Rounds, Qing Lu
Redox Biology
Analysis of Bacterial Biofilm Formation and MUC5AC and MUC5B Expression in Chronic Rhinosinusitis Patients
Georgi Popov, Radoslav Aleksandrov, Veronika Petkova, Radka Kaneva, Raina Gergova, Todor Kundurzhiev, Diana Popova
Journal of Clinical Medicine
Microbiome and the Eye
Mohammed Khan, Mohammed Khan, Ikuko Kato
Influence of Smoking on Periodontal and Implant Therapy: A Narrative Review
Marwa Madi, Steph Smith, Sami Alshehri, Osama Zakaria, Khalid Almas
International Journal of Environmental Research and Public Health