Skip to main content

Advertisement

SpringerLink
Log in

Effects of Nicotine on Oral Microorganisms, Human Tissues, and the Interactions between Them

  • Microbiology (M Klein, Section Editor)
  • Published:
Current Oral Health Reports Aims and scope Submit manuscript

Abstract

Purpose

Recent findings on the effects of smoking and nicotine on oral microorganisms and on microbial interactions with human cells were reviewed. A PubMed search identified recent publications in English that addressed the effects of smoking and nicotine on oral microorganisms: growth, biofilm formation, plaque composition, enzyme regulation, and cross-species interactions. Interactions of tobacco-exposed microbes with human tissues are also discussed.

Recent Findings

Smoking alters the oral microbiome. Nicotine increases the pathogenicity of oral microorganisms, either by increasing expression of virulence factors or by increasing the amount of biofilm formed. Nicotine affects human cells via nicotine acetylcholine receptors (nAChRs), and the prokaryote homolog may explain how nicotine affects microbial cells. Interactions of nicotine exposed microbial and human tissues likely contribute to cardiovascular disease.

Summary

The evidence supports the destructive oral and systemic effects of smoking and nicotine exposure, leading to development or exacerbation of dental caries, periodontitis, stomatitis, and heart diseases.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. National Center for Chronic Disease P, Health Promotion Office on S, Health. Reports of the surgeon general. The health consequences of smoking-50 years of progress: a report of the surgeon general. Atlanta (GA): Centers for Disease Control and Prevention (US); 2014.

    Google Scholar 

  2. Shafagoj YA, Mohammed FI, Hadidi KA. Hubble-bubble (water pipe) smoking: levels of nicotine and cotinine in plasma, saliva and urine. Int J Clin Pharmacol Ther. 2002;40(6):249–55. https://doi.org/10.5414/CPP40249.

    Article  CAS  PubMed  Google Scholar 

  3. Jacob N, Golmard JL, Berlin I. Relationships between nicotine and cotinine concentrations in maternal milk and saliva. Acta Paediatr (Oslo, Norway : 1992). 2015;104(8):e360–6. https://doi.org/10.1111/apa.13031.

    Article  CAS  Google Scholar 

  4. Papaseit E, Farre M, Graziano S, Pacifici R, Perez-Mana C, Garcia-Algar O, et al. Monitoring nicotine intake from e-cigarettes: measurement of parent drug and metabolites in oral fluid and plasma. Clin Chem Lab Med. 2017;55(3):415–23. https://doi.org/10.1515/cclm-2016-0405.

    Article  CAS  PubMed  Google Scholar 

  5. Fagan P, Pokhrel P, Herzog TA, Pagano IS, Franke AA, Clanton MS, et al. Nicotine metabolism in young adult daily menthol and nonmenthol smokers. Nicotine Tob Res. 2016;18(4):437–46. https://doi.org/10.1093/ntr/ntv109.

    Article  PubMed  Google Scholar 

  6. Marshall JR, Lotfipour S, Chakravarthy B. Growing trend of alternative tobacco use among the nation’s youth: a new generation of addicts. West J Emerg Med. 2016;17(2):139–42. https://doi.org/10.5811/westjem.2016.1.29383.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Friedewald VE, Kornman KS, Beck JD, Genco R, Goldfine A, Libby P, et al. The American Journal of Cardiology and Journal of Periodontology editors’ consensus: periodontitis and atherosclerotic cardiovascular disease. J Periodontol. 2009;80(7):1021–32. https://doi.org/10.1902/jop.2009.097001.

    Article  PubMed  Google Scholar 

  8. How KY, Song KP, Chan KG. Porphyromonas gingivalis: an overview of periodontopathic pathogen below the gum line. Front Microbiol. 2016;7:53.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Bostanci N, Belibasakis GN. Porphyromonas gingivalis: an invasive and evasive opportunistic oral pathogen. FEMS Microbiol Lett. 2012;333(1):1–9. https://doi.org/10.1111/j.1574-6968.2012.02579.x.

    Article  CAS  PubMed  Google Scholar 

  10. 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. https://doi.org/10.1902/jop.1996.67.10s.1050.

    Article  CAS  PubMed  Google Scholar 

  11. 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. https://doi.org/10.1902/jop.2000.72.9.1210.

    Article  CAS  PubMed  Google Scholar 

  12. Haffajee AD, Socransky SS. Relationship of cigarette smoking to the subgingival microbiota. J Clin Periodontol. 2001;28(5):377–88. https://doi.org/10.1034/j.1600-051x.2001.028005377.x.

    Article  CAS  PubMed  Google Scholar 

  13. Kamma JJ, Nakou M, Baehni PC. Clinical and microbiological characteristics of smokers with early onset periodontitis. J Periodontal Res. 1999;34(1):25–33. https://doi.org/10.1111/j.1600-0765.1999.tb02218.x.

    Article  CAS  PubMed  Google Scholar 

  14. Weinberg ED. Microbial pathogens with impaired ability to acquire host iron. Biometals. 2000;13(1):85–9. https://doi.org/10.1023/A:1009293500209.

    Article  CAS  PubMed  Google Scholar 

  15. Weinberg ED. Iron availability and infection. Biochim Biophys Acta. 2009;1790(7):600–5. https://doi.org/10.1016/j.bbagen.2008.07.002.

    Article  CAS  PubMed  Google Scholar 

  16. • Kumar PS. Smoking and the subgingival ecosystem: a pathogen-enriched community. Future Microbiol. 2012;7(8):917–9. https://doi.org/10.2217/fmb.12.71. This manuscript represents a brief summary of the effects of smoking on the composition of subgingival bacteria.

    Article  CAS  PubMed  Google Scholar 

  17. •• Bagaitkar J, Demuth DR, Scott DA. Tobacco use increases susceptibility to bacterial infection. Tob Induc Dis. 2008;4(1):12. https://doi.org/10.1186/1617-9625-4-12. This manuscript discusses the effects of tobacco on oral and systemic bacterial infections and discusses the mechanisms by which tobacco may increase susceptibility to infection.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Umeda M, Chen C, Bakker I, Contreras A, Morrison JL, Slots J. Risk indicators for harboring periodontal pathogens. J Periodontol. 1998;69(10):1111–8. https://doi.org/10.1902/jop.1998.69.10.1111.

    Article  CAS  PubMed  Google Scholar 

  19. Socransky SS, Haffajee AD. Periodontal microbial ecology. Periodontol. 2005;38(1):135–87. https://doi.org/10.1111/j.1600-0757.2005.00107.x.

    Article  Google Scholar 

  20. van Winkelhoff AJ, Bosch-Tijhof CJ, Winkel EG, van der Reijden WA. Smoking affects the subgingival microflora in periodontitis. J Periodontol. 2001;72(5):666–71. https://doi.org/10.1902/jop.2001.72.5.666.

    Article  PubMed  Google Scholar 

  21. Mason MR, Preshaw PM, Nagaraja HN, Dabdoub SM, Rahman A, Kumar PS. The subgingival microbiome of clinically healthy current and never smokers. ISME J. 2015;9(1):268–72. https://doi.org/10.1038/ismej.2014.114.

    Article  PubMed  Google Scholar 

  22. Joshi V, Matthews C, Aspiras M, de Jager M, Ward M, Kumar P. Smoking decreases structural and functional resilience in the subgingival ecosystem. J Clin Periodontol. 2014;41(11):1037–47. https://doi.org/10.1111/jcpe.12300.

    Article  PubMed  Google Scholar 

  23. Tsigarida AA, Dabdoub SM, Nagaraja HN, Kumar PS. The influence of smoking on the peri-implant microbiome. J Dent Res. 2015;94(9):1202–17. https://doi.org/10.1177/0022034515590581.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. 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. https://doi.org/10.1111/j.1600-051X.2005.00786.x.

    Article  CAS  PubMed  Google Scholar 

  25. Fullmer SC, Preshaw PM, Heasman PA, Kumar PS. Smoking cessation alters subgingival microbial recolonization. J Dent Res. 2009;88(6):524–8. https://doi.org/10.1177/0022034509338676.

    Article  CAS  PubMed  Google Scholar 

  26. Mahanonda R, Seymour GJ, Powell LW, Good MF, Halliday JW. Effect of initial treatment of chronic inflammatory periodontal disease on the frequency of peripheral blood T-lymphocytes specific to periodontopathic bacteria. Oral Microbiol Immunol. 1991;6(4):221–7. https://doi.org/10.1111/j.1399-302X.1991.tb00481.x.

    Article  CAS  PubMed  Google Scholar 

  27. 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. https://doi.org/10.1371/journal.pone.0009323.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Cogo K, Calvi BM, Mariano FS, Franco GC, Goncalves RB, Groppo FC. The effects of nicotine and cotinine on Porphyromonas gingivalis colonisation of epithelial cells. Arch Oral Biol. 2009;54(11):1061–7. https://doi.org/10.1016/j.archoralbio.2009.08.001.

    Article  CAS  PubMed  Google Scholar 

  29. 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. https://doi.org/10.1371/journal.pone.0027386.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. 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(6):837–44. https://doi.org/10.1902/jop.2013.130336.

    Article  PubMed  Google Scholar 

  31. Sayers NM, Gomes BP, Drucker DB, Blinkhorn AS. Possible lethal enhancement of toxins from putative periodontopathogens by nicotine: implications for periodontal disease. J Clin Pathol. 1997;50(3):245–9. https://doi.org/10.1136/jcp.50.3.245.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Preber H, Bergstrom J, Linder LE. Occurrence of periopathogens in smoker and non-smoker patients. J Clin Periodontol. 1992;19(9 Pt 1):667–71. https://doi.org/10.1111/j.1600-051X.1992.tb01716.x.

    Article  CAS  PubMed  Google Scholar 

  33. Van der Velden U, Varoufaki A, Hutter JW, Xu L, Timmerman MF, Van Winkelhoff AJ, et al. Effect of smoking and periodontal treatment on the subgingival microflora. J Clin Periodontol. 2003;30(7):603–10. https://doi.org/10.1034/j.1600-051X.2003.00080.x.

    Article  PubMed  Google Scholar 

  34. Fisher S, Kells L, Picard JP, Gelskey SC, Singer DL, Lix L, et al. Progression of periodontal disease in a maintenance population of smokers and non-smokers: a 3-year longitudinal study. J Periodontol. 2008;79(3):461–8. https://doi.org/10.1902/jop.2008.070296.

    Article  PubMed  Google Scholar 

  35. Esfahrood ZR, Zamanian A, Torshabi M, Abrishami M. The effect of nicotine and cotinine on human gingival fibroblasts attachment to root surfaces. J Basic Clin Physiol Pharmacol. 2015;26(5):517–22. https://doi.org/10.1515/jbcpp-2014-0120.

    Article  CAS  PubMed  Google Scholar 

  36. Kang SW, Park HJ, Ban JY, Chung JH, Chun GS, Cho JO. Effects of nicotine on apoptosis in human gingival fibroblasts. Arch Oral Biol. 2011;56(10):1091–7. https://doi.org/10.1016/j.archoralbio.2011.03.016.

    Article  CAS  PubMed  Google Scholar 

  37. Lee SI, Kang KL, Shin SI, Herr Y, Lee YM, Kim EC. Endoplasmic reticulum stress modulates nicotine-induced extracellular matrix degradation in human periodontal ligament cells. J Periodontal Res. 2012;47(3):299–308. https://doi.org/10.1111/j.1600-0765.2011.01432.x.

    Article  CAS  PubMed  Google Scholar 

  38. Takeuchi-Igarashi H, Kubota S, Tachibana T, Murakashi E, Takigawa M, Okabe M, et al. Matrix remodeling response of human periodontal tissue cells toward fibrosis upon nicotine exposure. Odontology. 2016;104(1):35–43. https://doi.org/10.1007/s10266-014-0177-y.

    Article  CAS  PubMed  Google Scholar 

  39. 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. https://doi.org/10.1111/j.1462-2920.2008.01852.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Wu L, Zhou Y, Zhou Z, Liu Y, Bai Y, Xing X, et al. Nicotine induces the production of IL-1beta and IL-8 via the alpha7 nAChR/NF-kappaB pathway in human periodontal ligament cells: an in vitro study. Cell Physiol Biochem. 2014;34(2):423–31. https://doi.org/10.1159/000363011.

    Article  PubMed  Google Scholar 

  41. Hayes MJ, Cheng B, Musolino R, Rogers AA. Dietary analysis and nutritional counselling for caries prevention in dental practise: a pilot study. Aust Dent J. 2017;62(4):485–92. https://doi.org/10.1111/adj.12524.

    Article  CAS  PubMed  Google Scholar 

  42. Dye B, Thornton-Evans G, Li X, Iafolla T. Dental caries and tooth loss in adults in the United States, 2011-2012. NCHS data brief. 2015;197:197.

    Google Scholar 

  43. Peterson SN, Snesrud E, Liu J, Ong AC, Kilian M, Schork NJ, et al. The dental plaque microbiome in health and disease. PLoS One. 2013;8(3):e58487. https://doi.org/10.1371/journal.pone.0058487.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Moynihan P, Petersen PE. Diet, nutrition and the prevention of dental diseases. Public Health Nutr. 2004;7(1A):201–26.

    Article  PubMed  Google Scholar 

  45. Wen ZT, Yates D, Ahn SJ, Burne RA. Biofilm formation and virulence expression by Streptococcus mutans are altered when grown in dual-species model. BMC Microbiol. 2010;10(1):111. https://doi.org/10.1186/1471-2180-10-111.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Ahn SJ, Burne RA. Effects of oxygen on biofilm formation and the AtlA autolysin of Streptococcus mutans. J Bacteriol. 2007;189(17):6293–302. https://doi.org/10.1128/JB.00546-07.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Zijnge V, van Leeuwen MB, Degener JE, Abbas F, Thurnheer T, Gmur R, et al. Oral biofilm architecture on natural teeth. PLoS One. 2010;5(2):e9321. https://doi.org/10.1371/journal.pone.0009321.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Aguilar-Zinser V, Irigoyen ME, Rivera G, Maupome G, Sanchez-Perez L, Velazquez C. Cigarette smoking and dental caries among professional truck drivers in Mexico. Caries Res. 2008;42(4):255–62. https://doi.org/10.1159/000135670.

    Article  CAS  PubMed  Google Scholar 

  49. Avsar A, Darka O, Topaloglu B, Bek Y. Association of passive smoking with caries and related salivary biomarkers in young children. Arch Oral Biol. 2008;53(10):969–74. https://doi.org/10.1016/j.archoralbio.2008.05.007.

    Article  CAS  PubMed  Google Scholar 

  50. Campus G, Cagetti MG, Senna A, Blasi G, Mascolo A, Demarchi P, et al. Does smoking increase risk for caries? A cross-sectional study in an Italian military academy. Caries Res. 2011;45(1):40–6. https://doi.org/10.1159/000322852.

    Article  CAS  PubMed  Google Scholar 

  51. • 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. https://doi.org/10.1111/j.1600-0722.2012.00971.x. This manuscript is the first to state the effect of nicotine on S. mutans.

    CAS  PubMed  Google Scholar 

  52. Huang R, Li M, Gregory RL. Nicotine promotes Streptococcus mutans extracellular polysaccharide synthesis, cell aggregation and overall lactate dehydrogenase activity. Arch Oral Biol. 2015;60(8):1083–90. https://doi.org/10.1016/j.archoralbio.2015.04.011.

    Article  CAS  PubMed  Google Scholar 

  53. 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. https://doi.org/10.1111/1574-6968.12317.

    Article  CAS  PubMed  Google Scholar 

  54. 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. https://doi.org/10.1038/ijos.2013.86.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Li M, Huang R, Zhou X, Qiu W, Xu X, Gregory RL. Effect of nicotine on cariogenic virulence of Streptococcus mutans. Folia Microbiol (Praha). 2016;61(6):505–12. https://doi.org/10.1007/s12223-016-0465-8.

    Article  CAS  Google Scholar 

  56. • Dubois AE, Bennett ZC, Khalid U, Khalid A, Meece RA, Difiore GJ, et al. Nicotine: its stimulating and inhibitory effects on oral microorganisms. Fine Focus 2014: 63. This manusript demonstrates the effect of nicotine on several important oral microorganisms.

  57. Huang R, Li M, Ye M, Yang K, Xu X, Gregory RL. Effects of nicotine on Streptococcus gordonii growth, biofilm formation, and cell aggregation. Appl Environ Microbiol. 2014;80(23):7212–8. https://doi.org/10.1128/AEM.02395-14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Tanner AC, Mathney JM, Kent RL, Chalmers NI, Hughes CV, Loo CY, et al. Cultivable anaerobic microbiota of severe early childhood caries. J Clin Microbiol. 2011;49(4):1464–74. https://doi.org/10.1128/JCM.02427-10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Webb BC, Thomas CJ, Willcox MD, Harty DW, Knox KW. Candida-associated denture stomatitis. Aetiology and management: a review. Part 1. Factors influencing distribution of Candida species in the oral cavity. Aust Dent J. 1998;43(1):45–50. https://doi.org/10.1111/j.1834-7819.1998.tb00152.x.

    Article  CAS  PubMed  Google Scholar 

  60. Webb BC, Thomas CJ, Willcox MD, Harty DW, Knox KW. Candida-associated denture stomatitis. Aetiology and management: a review. Part 2. Oral diseases caused by Candida species. Aust Dent J. 1998;43(3):160–6. https://doi.org/10.1111/j.1834-7819.1998.tb00157.x.

    Article  CAS  PubMed  Google Scholar 

  61. Arendorf TM, Walker DM. Denture stomatitis: a review. J Oral Rehabil. 1987;14(3):217–27. https://doi.org/10.1111/j.1365-2842.1987.tb00713.x.

    Article  CAS  PubMed  Google Scholar 

  62. Ashkanane A, Gomez GF, Levon J, Windsor LJ, Eckert GJ, Gregory RL. Nicotine upregulates coaggregation of Candida albicans and Streptococcus mutans. J Prosthodont. 2017; https://doi.org/10.1111/jopr.12643.

  63. Friedewald VE, Kornman KS, Beck JD, Genco R, Goldfine A, Libby P, et al. The American Journal of Cardiology and Journal of Periodontology Editors’ consensus: periodontitis and atherosclerotic cardiovascular disease. Am J Cardiol. 2009;104(1):59–68. https://doi.org/10.1016/j.amjcard.2009.05.002.

    Article  PubMed  Google Scholar 

  64. Frostegard J. Immunity, atherosclerosis and cardiovascular disease. BMC Med. 2013;11(1):117. https://doi.org/10.1186/1741-7015-11-117.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Libby P. Inflammation in atherosclerosis. Arterioscler Thromb Vasc Biol. 2012;32(9):2045–51. https://doi.org/10.1161/ATVBAHA.108.179705.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Spagnoli LG, Bonanno E, Sangiorgi G, Mauriello A. Role of inflammation in atherosclerosis. J Nucl Med. 2007;48(11):1800–15. https://doi.org/10.2967/jnumed.107.038661.

    Article  PubMed  Google Scholar 

  67. Campbell LA, Rosenfeld ME. Infection and atherosclerosis development. Arch Med Res. 2015;46(5):339–50. https://doi.org/10.1016/j.arcmed.2015.05.006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Rosenfeld ME, Campbell LA. Pathogens and atherosclerosis: update on the potential contribution of multiple infectious organisms to the pathogenesis of atherosclerosis. Thromb Haemost. 2011;106(5):858–67. https://doi.org/10.1160/TH11-06-0392.

    Article  CAS  PubMed  Google Scholar 

  69. Lanter BB, Sauer K, Davies DG. Bacteria present in carotid arterial plaques are found as biofilm deposits which may contribute to enhanced risk of plaque rupture. MBio. 2014;5(3):e01206–14. https://doi.org/10.1128/mBio.01206-14.

    Article  PubMed  PubMed Central  Google Scholar 

  70. Nakano K, Nemoto H, Nomura R, Homma H, Yoshioka H, Shudo Y, et al. Serotype distribution of Streptococcus mutans a pathogen of dental caries in cardiovascular specimens from Japanese patients. J Med Microbiol. 2007;56(Pt 4):551–6. https://doi.org/10.1099/jmm.0.47051-0.

    Article  CAS  PubMed  Google Scholar 

  71. Nakano K, Nemoto H, Nomura R, Inaba H, Yoshioka H, Taniguchi K, et al. Detection of oral bacteria in cardiovascular specimens. Oral Microbiol Immunol. 2009;24(1):64–8. https://doi.org/10.1111/j.1399-302X.2008.00479.x.

    Article  CAS  PubMed  Google Scholar 

  72. Reyes L, Herrera D, Kozarov E, Rolda S, Progulske-Fox A. Periodontal bacterial invasion and infection: contribution to atherosclerotic pathology. J Periodontol. 2013;84(4 Suppl):S30–50. https://doi.org/10.1902/jop.2013.1340012.

    PubMed  Google Scholar 

  73. Nakano K, Wada K, Nomura R, Nemoto H, Inaba H, Kojima A, et al. Characterization of aortic aneurysms in cardiovascular disease patients harboring Porphyromonas gingivalis. Oral Dis. 2011;17(4):370–8. https://doi.org/10.1111/j.1601-0825.2010.01759.x.

    Article  CAS  PubMed  Google Scholar 

  74. Kozarov E. Bacterial invasion of vascular cell types: vascular infectology and atherogenesis. Futur Cardiol. 2012;8(1):123–38. https://doi.org/10.2217/fca.11.75.

    Article  CAS  Google Scholar 

  75. Nakano K, Inaba H, Nomura R, Nemoto H, Takeda M, Yoshioka H, et al. Detection of cariogenic Streptococcus mutans in extirpated heart valve and atheromatous plaque specimens. J Clin Microbiol. 2006;44(9):3313–7. https://doi.org/10.1128/JCM.00377-06.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Nomura R, Nakano K, Nemoto H, Fujita K, Inagaki S, Takahashi T, et al. Isolation and characterization of Streptococcus mutans in heart valve and dental plaque specimens from a patient with infective endocarditis. J Med Microbiol. 2006;55(Pt 8):1135–40. https://doi.org/10.1099/jmm.0.46609-0.

    Article  CAS  PubMed  Google Scholar 

  77. Sakki T, Knuuttila M. Controlled study of the association of smoking with lactobacilli, mutans streptococci and yeasts in saliva. Eur J Oral Sci. 1996;104(5–6):619–22. https://doi.org/10.1111/j.1600-0722.1996.tb00151.x.

    Article  CAS  PubMed  Google Scholar 

  78. Wu J, Peters BA, Dominianni C, Zhang Y, Pei Z, Yang L, et al. Cigarette smoking and the oral microbiome in a large study of American adults. ISME J. 2016;10(10):2435–46. https://doi.org/10.1038/ismej.2016.37.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. • Abranches J, Miller JH, Martinez AR, Simpson-Haidaris PJ, Burne RA, Lemos JA. The collagen-binding protein Cnm is required for Streptococcus mutans adherence to and intracellular invasion of human coronary artery endothelial cells. Infect Immun. 2011;79(6):2277–84. https://doi.org/10.1128/IAI.00767-10. This paper demonstrated that Cnm is critical for S. mutans invasion of endothelial cells.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Lapirattanakul J, Nomura R, Nemoto H, Naka S, Ooshima T, Nakano K. Multilocus sequence typing of Streptococcus mutans strains with the cbm gene encoding a novel collagen-binding protein. Arch Oral Biol. 2013;58(8):989–96. https://doi.org/10.1016/j.archoralbio.2013.02.007.

    Article  CAS  PubMed  Google Scholar 

  81. • Nomura R, Nakano K, Naka S, Nemoto H, Masuda K, Lapirattanakul J, et al. Identification and characterization of a collagen-binding protein, Cbm, in Streptococcus mutans. Mol Oral Microbiol. 2012;27(4):308–23. https://doi.org/10.1111/j.2041-1014.2012.00649.x. This is the first paper to describe S. mutans collagen binding protein Cbm.

    Article  CAS  PubMed  Google Scholar 

  82. Aviles-Reyes A, Miller JH, Lemos JA, Abranches J. The collagen binding proteins of Streptococcus mutans and related streptococci. Mol Oral Microbiol. 2016;32(2):89–106.

    Article  PubMed  Google Scholar 

  83. Nomura R, Naka S, Nemoto H, Inagaki S, Taniguchi K, Ooshima T, et al. Potential involvement of collagen-binding proteins of Streptococcus mutans in infective endocarditis. Oral Dis. 2013;19(4):387–93. https://doi.org/10.1111/odi.12016.

    Article  CAS  PubMed  Google Scholar 

  84. Kojima A, Nakano K, Wada K, Takahashi H, Katayama K, Yoneda M, et al. Infection of specific strains of Streptococcus mutans, oral bacteria, confers a risk of ulcerative colitis. Sci Rep. 2012;2(1):332. https://doi.org/10.1038/srep00332.

    Article  PubMed  PubMed Central  Google Scholar 

  85. Miyatani F, Kuriyama N, Watanabe I, Nomura R, Nakano K, Matsui D, et al. Relationship between Cnm-positive Streptococcus mutans and cerebral microbleeds in humans. Oral Dis. 2015;21(7):886–93. https://doi.org/10.1111/odi.12360.

    Article  CAS  PubMed  Google Scholar 

  86. Nakano K, Hokamura K, Taniguchi N, Wada K, Kudo C, Nomura R, et al. The collagen-binding protein of Streptococcus mutans is involved in haemorrhagic stroke. Nat Commun. 2011;2:485. https://doi.org/10.1038/ncomms1491.

    Article  PubMed  PubMed Central  Google Scholar 

  87. Heeschen C, Weis M, Aicher A, Dimmeler S, Cooke JP. A novel angiogenic pathway mediated by non-neuronal nicotinic acetylcholine receptors. J Clin Invest. 2002;110(4):527–36. https://doi.org/10.1172/JCI0214676.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Lee J, Cooke JP. The role of nicotine in the pathogenesis of atherosclerosis. Atherosclerosis. 2011;215(2):281–3. https://doi.org/10.1016/j.atherosclerosis.2011.01.003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Lee J, Cooke JP. Nicotine and pathological angiogenesis. Life Sci. 2012;91(21–22):1058–64. https://doi.org/10.1016/j.lfs.2012.06.032.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Cooke JP. New insights into tobacco-induced vascular disease: clinical ramifications. Methodist DeBakey cardiovasc J. 2015;11(3):156–9. https://doi.org/10.14797/mdcj-11-3-156.

    Article  PubMed  PubMed Central  Google Scholar 

  91. Heeschen C, Jang JJ, Weis M, Pathak A, Kaji S, Hu RS, et al. Nicotine stimulates angiogenesis and promotes tumor growth and atherosclerosis. Nat Med. 2001;7(7):833–9. https://doi.org/10.1038/89961.

    Article  CAS  PubMed  Google Scholar 

  92. Heeschen C, Weis M, Cooke JP. Nicotine promotes arteriogenesis. J Am Coll Cardiol. 2003;41(3):489–96. https://doi.org/10.1016/S0735-1097(02)02818-8.

    Article  CAS  PubMed  Google Scholar 

  93. Wang C, Chen H, Zhu W, Xu Y, Liu M, Zhu L, et al. Nicotine accelerates atherosclerosis in apolipoprotein E-deficient mice by activating alpha7 nicotinic acetylcholine receptor on mast cells. Arterioscler Thromb Vasc Biol. 2017;37(1):53–65. https://doi.org/10.1161/ATVBAHA.116.307264.

    Article  PubMed  Google Scholar 

  94. Bocquet N, Prado de Carvalho L, Cartaud J, Neyton J, Le Poupon C, Taly A, et al. A prokaryotic proton-gated ion channel from the nicotinic acetylcholine receptor family. Nature. 2007;445(7123):116–9. https://doi.org/10.1038/nature05371.

    Article  CAS  PubMed  Google Scholar 

  95. Corringer PJ, Baaden M, Bocquet N, Delarue M, Dufresne V, Nury H, et al. Atomic structure and dynamics of pentameric ligand-gated ion channels: new insight from bacterial homologues. J Physiol. 2010;588(Pt 4):565–72. https://doi.org/10.1113/jphysiol.2009.183160.

    Article  CAS  PubMed  Google Scholar 

  96. Lepore BW, Indic M, Pham H, Hearn EM, Patel DR, van den Berg B. Ligand-gated diffusion across the bacterial outer membrane. Proc Natl Acad Sci U S A. 2011;108(25):10121–6. https://doi.org/10.1073/pnas.1018532108.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. •• Cecchini M, Changeux JP. The nicotinic acetylcholine receptor and its prokaryotic homologues: structure, conformational transitions & allosteric modulation. Neuropharmacology. 2015;96(Pt B):137–49. https://doi.org/10.1016/j.neuropharm.2014.12.006. This paper reviews the most recent advances on signal transduction mechanisms of the nAChR and prokaryotic homologs .

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Taylor Dietl, Nasreen El-ezmerli, Jennifer Foltz, Reed A. McKinney, Nicole Shepherd, Emily Taylor, and Cunge Zheng for experimental data. Support provided by Franciscan Health Indianapolis, Indiana, USA (DRW) and the University of Dammam, Saudi Arabia (AAB).

Author information

Authors and Affiliations

  1. Department of Biomedical and Applied Sciences, Indiana University School of Dentistry, 1121 W. Michigan Street, Indianapolis, IN, 46202, USA

    Dawn R. Wagenknecht, AbdulRahman AbuBaker BalHaddad & Richard L. Gregory

  2. Restorative Dental Sciences Department, College of Dentistry, University of Dammam, Dammam, Saudi Arabia

    AbdulRahman AbuBaker BalHaddad

Authors
  1. Dawn R. Wagenknecht
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. AbdulRahman AbuBaker BalHaddad
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Richard L. Gregory
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Richard L. Gregory.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

Additional information

This article is part of the topical collection on Microbiology

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wagenknecht, D.R., BalHaddad, A.A. & Gregory, R.L. Effects of Nicotine on Oral Microorganisms, Human Tissues, and the Interactions between Them. Curr Oral Health Rep 5, 78–87 (2018). https://doi.org/10.1007/s40496-018-0173-3

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40496-018-0173-3

Keywords

Search

Navigation