REVIEW PAPER
The effect of smoking on caries-related microorganisms
Jiayi Wu 1
,  
Mingyun Li# 2  
,  
Ruijie Huang# 2, 3  
 
 
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1
Department of Endodontic Dentistry, State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, China
2
State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, China
3
Department of Pediatric Dentistry, West China Hospital of Stomatology, Sichuan University, Chengdu, China
CORRESPONDING AUTHOR
Mingyun Li#   

State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, China
Ruijie Huang#   

Department of Pediatric Dentistry, State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, China
Publish date: 2019-04-18
 
Tob. Induc. Dis. 2019;17(April):32
KEYWORDS
TOPICS
# Contributed equally, co-correspondence authors
ABSTRACT
Introduction:
Epidemiological studies have shown a close relationship between smoking and dental caries. Bacteria are one of the essential factors of caries formation. The imbalance of cariogenic bacteria and commensal bacteria in dental plaque results in higher production of acid that can corrode dental hard tissue. The aim of our review is to summarize the effect of smoking on caries-related bacteria.

Methods:
English articles available in Pubmed and ScienceDirect databases and published before December 2018 were searched. A variety of evidence was collected including not only the influence of cigarette products on bacteria strains in vitro but also their effect on bacterial composition in saliva and dental plaque in vivo. We particularly emphasize the mechanisms by which nicotine acts on oral bacteria.

Results:
The components of cigarettes promote the growth of cariogenic microorganisms. The mechanisms of how nicotine enhances Streptococcus mutans, Lactobacilli, Streptococcus gordonii, Actinomyces and Candida albicans are described separately in detail. The commensal bacteria, Streptococcus sanguinis, show less competitive capability in the presence of nicotine. Smoking influences saliva by lowering the buffer capability, altering its chemical agent and bacterial components, and therefore promotes the formation of a caries-susceptible environment.

Conclusions:
Cigarette smoking and nicotine exposure promote the cariogenic activity of oral microorganisms and the formation of a caries-susceptible environment. This suggests that smokers should quit smoking, amongst other health reasons, also for their oral health.

ACKNOWLEDGEMENTS
We thank Xiaoge Jiang for her kind language editing.
CONFLICTS OF INTEREST
Authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest and none was reported.
FUNDING
This work was partially supported by the National Natural Science Foundation of China (81400501 to ML and 31800114 to RH).
PROVENANCE AND PEER REVIEW
Not commissioned; externally peer reviewed.
 
REFERENCES (73)
1.
Campus G, Cagetti MG, Senna A, Blasi G, Mascolo A, Demarchi P, Strohmenger L. Does smoking increase risk for caries? a cross-sectional study in an Italian military academy. Caries Res. 2011;45(1):40-46. doi:10.1159/000322852
 
2.
Bernabé E, Delgado-Angulo EK, Vehkalahti MM, Aromaa A, Suominen AL. Daily smoking and 4-year caries increment in Finnish adults. Community Dentistry & Oral Epidemiology. 2015;42(5):428-434. doi:10.1111/cdoe.12101
 
3.
Bernabé E, Macritchie H, Longbottom C, Pitts NB, Sabbah W. Birth Weight, Breastfeeding, Maternal Smoking and Caries Trajectories. J Dent Res. 2017;96(2):171-178. doi:10.1177/0022034516678181
 
4.
Nobre MA, Malã P. Prevalence of periodontitis, dental caries, and peri-implant pathology and their relation with systemic status and smoking habits: Results of an open-cohort study with 22009 patients in a private rehabilitation center. J Dent. 2017;67:36-42. doi:10.1016/j.jdent.2017.07.013
 
5.
Benedetti G, Campus G, Strohmenger L, Lingström P. Tobacco and dental caries: a systematic review. Acta Odontol Scand. 2013;71(3-4):363-371. doi:10.3109/00016357.2012.734409
 
6.
Beaglehole R, Myriad Editions, International Dental Federation. The oral health atlas : mapping a neglected global health issue. Cointrin, Switzerland: FDI World Dental Federation; 2009.
 
7.
Mucci LA, Brooks DR. Lower use of dental services among long term cigarette smokers. J Epidemiol Community Health. 2001;55(6):389-393. doi:10.1136/jech.55.6.389
 
8.
Sherwood NE, Hennrikus DJ, Jeffery RW, Lando HA, Murray DM. Smokers with multiple behavioral risk factors: how are they different? Prev Med. 2000;31(4):299-307. doi:10.1006/pmed.2000.0710
 
9.
Axelsson P, Paulander J, Lindhe J. Relationship between smoking and dental status in 35-, 50-, 65-, and 75-year-old individuals. J Clin Periodontol. 1998;25(4):297-305. doi:10.1111/j.1600-051x.1998.tb02444.x
 
10.
Takahashi N, Nyvad B. Ecological Hypothesis of Dentin and Root Caries. Caries Res. 2016;50(4):422-431. doi:10.1159/000447309
 
11.
Ertel A, Eng R, Smith SM. The differential effect of cigarette smoke on the growth of bacteria found in humans. Chest. 1991;100(3):628-630. doi:10.1378/chest.100.3.628
 
12.
Baboni FB, Guariza FO, Moreno AN, Rosa E. Influence of cigarette smoke condensate on cariogenic and candidal biofilm formation on orthodontic materials. Am J Orthod Dentofacial Orthop. 2010;138(4):427-434. doi:10.1016/j.ajodo.2009.05.023
 
13.
Zonuz AT, Rahmati A, Mortazavi H, Khashabi E, Farahani RM. Effect of cigarette smoke exposure on the growth of Streptococcus mutans and Streptococcus sanguis: an in vitro study. Nicotine Tob Res. 2008;10(1):63-67. doi:10.1080/14622200701705035
 
14.
Courtney R. The Health Consequences of Smoking-50 Years of Progress: A Report of the Surgeon General, 2014Us Department of Health and Human Services Atlanta, GA: Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for. Drug Alcohol Rev. 2015;34(6):694-695. doi:10.1111/dar.12309
 
15.
Lindemeyer RG, Baum RH, Hsu SC, Going RE. In vitro effect of tobacco on the growth of oral cariogenic streptococci. J Am Dent Assoc. 1981;103(5):719-722. doi:10.14219/jada.archive.1981.0372
 
16.
Takahashi N, Nyvad B. The role of bacteria in the caries process: ecological perspectives. J Dent Res. 2011;90(3):294-303. doi:10.1177/0022034510379602
 
17.
Van HJ, Sansone C, Joshipura K, Kent R. Mutans streptococci and non-mutans streptococci acidogenic at low pH, and in vitro acidogenic potential of dental plaque in two different areas of the human dentition. J Dent Res. 1991;70(12):1503-1507. doi:10.1177/00220345910700120601
 
18.
Huang R, Li M, Gregory RL. Effect of nicotine on growth and metabolism of Streptococcus mutans. Eur J Oral Sci. 2012;120(4):319-325. doi:10.1111/j.1600-0722.2012.00971.x
 
19.
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):1083-1090. doi:10.1016/j.archoralbio.2015.04.011
 
20.
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):125-132. doi:10.1111/1574-6968.12317
 
21.
Sommer P, Klein JP, Sch Ller M, Frank RM. Lactate dehydrogenase from Streptococcus mutans: purification, characterization, and crossed antigenicity with lactate dehydrogenases from Lactobacillus casei, Actinomyces viscosus, and Streptococcus sanguis. Infect Immun. 1985;47(2):489-495. https://www.ncbi.nlm.nih.gov/p.... Accessed December 17, 2018.
 
22.
Sutherland IW. The biofilm matrix – an immobilized but dynamic microbial environment. Trends Microbiol. 2001;9(5):222-227. doi:10.1016/s0966-842x(01)02012-1
 
23.
Bowen WH, Koo H. Biology ofStreptococcus mutans-Derived Glucosyltransferases: Role in Extracellular Matrix Formation of Cariogenic Biofilms. Caries Res. 2011;45(1):69-86. doi:10.1159/000324598
 
24.
Aoki H, Shiroza T, Hayakawa M, Sato S, Kuramitsu HK. Cloning of a Streptococcus mutans glucosyltransferase gene coding for insoluble glucan synthesis. Infect Immun. 1986;53(3):587-594. PMID: 3017865.
 
25.
Hanada N, Kuramitsu HK. Isolation and characterization of the Streptococcus mutans gtfC gene, coding for synthesis of both soluble and insoluble glucans. Infect Immun. 1988;56(8):1999-2005. PMID: 2969375.
 
26.
Hanada N, Kuramitsu HK. Isolation and characterization of the Streptococcus mutans gtfD gene, coding for primer-dependent soluble glucan synthesis. Infect Immun. 1989;57(7):2079-2085. PMID: 2543630.
 
27.
Banas JA, Russell RR, Ferretti JJ. Sequence analysis of the gene for the glucan-binding protein of Streptococcus mutans Ingbritt. Infect Immun. 1990;58(3):667-673. PMID: 2307516.
 
28.
Smith DJ, Akita H, King WF, Taubman MA. Purification and antigenicity of a novel glucan-binding protein of Streptococcus mutans. Infect Immun. 1994;62(6):2545-2552. PMID: 8188378.
 
29.
Sato Y, Yamamoto Y, Kizaki H. Cloning and sequence analysis of the gbpC gene encoding a novel glucan-binding protein of Streptococcus mutans. Infect Immun. 1997;65(2):668-675. PMID: 9009329.
 
30.
Shah DS, Russell RR. A novel glucan-binding protein with lipase activity from the oral pathogen Streptococcus mutans. Microbiology. 2004;150(6):1947-1956. doi:10.1099/mic.0.26955-0
 
31.
Lynch DJ, Fountain TL, Mazurkiewicz JE, Banas JA. Glucan-binding proteins are essential for shaping Streptococcus mutans biofilm architecture. Fems Microbiol Lett. 2010;268(2):158-165. doi:10.1111/j.1574-6968.2006.00576.x
 
32.
van Ruyven FO, Lingstrã MP, Van HJ, Kent R. Relationship among mutans streptococci, "low-pH" bacteria, and lodophilic polysaccharide-producing bacteria in dental plaque and early enamel caries in humans. J Dent Res. 2000;79(2):778-784. doi:10.1177/00220345000790021201
 
33.
Hujanen M, Linko S, Linko YY, Leisola M. Optimisation of media and cultivation conditions for L(+)(S)-lactic acid production by Lactobacillus casei NRRL B-441. Appl Microbiol Biotechnol. 2001;56(1-2):126-130. doi:10.1007/s002530000501
 
34.
DuBois AE, Bennett ZC, Khalid U, Khalid A, Meece RA, Difiore GJ, Gregory RL. Nicotine: Its Stimulating and Inhibitory Effects on Oral Microorganisms. Fine Focus. 2014;1:63-75. http://cardinalscholar.bsu.edu.... Accessed December 17, 2018.
 
35.
Valdebenito B, Tullume-Vergara PO, González W, Kreth J, Giacaman RA. In silico analysis of the competition between Streptococcus sanguinis and Streptococcus mutans in the dental biofilm. Mol Oral Microbiol. 2017;33(2):168-180. doi:10.1111/omi.12209
 
36.
Kreth J, Merritt J, Shi W, Qi F. Co-ordinated bacteriocin production and competence development: a possible mechanism for taking up DNA from neighbouring species. Mol Microbiol. 2010;57(2):392-404. doi:10.1111/j.1365-2958.2005.04695.x
 
37.
Kreth J, Zhang Y, Herzberg MC. Streptococcal antagonism in oral biofilms: Streptococcus sanguinis and Streptococcus gordonii interference with Streptococcus mutans. J Bacteriol. 2008;190(13):4632-4640. doi:10.1128/jb.00276-08
 
38.
Tong H, Chen W, Shi W, Fengxia QI, Dong X. SO-LAAO, a Novel L-Amino Acid Oxidase That Enables Streptococcus oligofermentans To Outcompete Streptococcus mutans by Generating H2O2 from Peptone. J Bacteriol. 2008;190(13):4716-4721. doi:10.1128/jb.00363-08
 
39.
Kolenbrander PE, Palmer RJ, Rickard AH, Jakubovics NS, Chalmers NI, Diaz PI. Bacterial interactions and successions during plaque development. Periodontol 2000. 2006;42(1):47-79. doi:10.1111/j.1600-0757.2006.00187.x
 
40.
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):7212-7218. doi:10.1128/aem.02395-14
 
41.
Li L, Tanzer JM, Scannapieco FA. Identification and analysis of the amylase-binding protein B (AbpB) and gene ( abpB ) from Streptococcus gordonii. FEMS Microbiol Lett. 2002;212(2):151-157. doi:10.1111/j.1574-6968.2002.tb11259.x
 
42.
Rogers JD, Haase EM, Brown AE, Douglas CW, Gwynn JP, Scannapieco FA. Identification and analysis of a gene (abpA) encoding a major amylase-binding protein in Streptococcus gordonii. Microbiology. 1998;144(5):1223-1233. doi:10.1099/00221287-144-5-1223
 
43.
Aguirre A, Levine MJ, Cohen RE, Tabak LA. Immunochemical quantitation of α-amylase and secretory IgA in parotid saliva from people of various ages. Arch Oral Biol. 1987;32(4):297-301. doi:10.1016/0003-9969(87)90024-0
 
44.
Zheng L, Chen Z, Itzek A, Herzberg MC, Kreth J. CcpA regulates biofilm formation and competence in Streptococcus gordonii. Mol Oral Microbiol. 2012;27(2):83-94. doi:10.1111/j.2041-1014.2011.00633.x
 
45.
Vickerman MM, Sulavik MC, Nowak JD, Gardner NM, Jones GW, Clewell DB. Nucleotide sequence analysis of the Streptococcus gordonii glucosyltransferase gene, gtfG. DNA Seq. 1997;7(2):83-95. doi:10.3109/10425179709020155
 
46.
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):206-211. doi:10.1038/ijos.2013.86
 
47.
Paterson GK, Mitchell TJ. The biology of Gram-positive sortase enzymes. Trends Microbiol. 2004;12(2):89-95. doi:10.1016/j.tim.2003.12.007
 
48.
Holmes AR, McNab R, Jenkinson HF. Candida albicans binding to the oral bacterium Streptococcus gordonii involves multiple adhesin-receptor interactions. Infect Immun. 1996;64(11):4680-4685. PMID: 8890225.
 
49.
Jenkinson HF, Terry SD, McNab R, Tannock GW. Inactivation of the gene encoding surface protein SspA in Streptococcus gordonii DL1 affects cell interactions with human salivary agglutinin and oral actinomyces. Infect Immun. 1993;61(8):3199-3208. PMID: 8335350.
 
50.
Takahashi Y, Konishi K, Cisar JO, Yoshikawa M. Identification and characterization of hsa, the gene encoding the sialic acid-binding adhesin of Streptococcus gordonii DL1. Infect Immun. 2002;70(3):1209-1218. doi:10.1128/iai.70.3.1209-1218.2002
 
51.
Kolenbrander PE, Andersen RN, Ganeshkumar N. Nucleotide sequence of the Streptococcus gordonii PK488 coaggregation adhesin gene, scaA, and ATP-binding cassette. Infect Immun. 1994;62(10):4469-4480. PMID: 7927711.
 
52.
Klein RS, Harris CA, Small CB, Moll B, Lesser M, Friedland GH. Oral candidiasis in high-risk patients as the initial manifestation of the acquired immunodeficiency syndrome. N Engl J Med. 1984;311(6):354-358. doi:10.1056/nejm198408093110602
 
53.
Metwalli KH, Khan SA, Krom BP, Jabra-Rizk MA. Streptococcus mutans, Candida albicans, and the human mouth: a sticky situation. Plos Pathog. 2013;9(10):e1003616. doi:10.1371/journal.ppat.1003616
 
54.
Klinke T, Guggenheim B, Klimm W, Thurnheer T. Dental caries in rats associated with Candida albicans. Caries Res. 2011;45(2):100-106. doi:10.1159/000324809
 
55.
Xiao J, Moon Y, Li L, et al. Candida albicans Carriage in Children with Severe Early Childhood Caries (S-ECC) and Maternal Relatedness. Plos One. 2016;11(10):e0164242. doi:10.1371/journal.pone.0164242
 
56.
Liu S, Qiu W, Zhang K, et al. Nicotine Enhances Interspecies Relationship between Streptococcus mutans and Candida albicans. Biomed Res Int. 2017;2017:7953920. doi:10.1155/2017/7953920
 
57.
Falsetta ML, Klein MI, Colonne PM, et al. Symbiotic relationship between Streptococcus mutans and Candida albicans synergizes virulence of plaque biofilms in vivo. Infect Immun. 2014;82(5):1968-1981. doi:10.1128/iai.00087-14
 
58.
Raja M, Hannan A, Ali K. Association of oral candidal carriage with dental caries in children. Caries Res. 2010;44(3):272-276. doi:10.1159/000314675
 
59.
Jarosz LM, Deng DM, van der Mei HC, Crielaard W, Krom BP. Streptococcus mutans competence-stimulating peptide inhibits Candida albicans hypha formation. Eukaryot Cell. 2009;8(11):1658-1664. doi:10.1128/ec.00070-09
 
60.
Heintze U. Secretion rate, buffer effect and number of lactobacilli and Streptococcus mutans of whole saliva of cigarette smokers and nonsmokers. Scand J Dent Res. 1984;92(4):294-301. doi:10.1111/j.1600-0722.1984.tb00894.x
 
61.
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):619-622. doi:10.1111/j.1600-0722.1996.tb00151.x
 
62.
Ravald N, Birkhed D, Hamp SE. Root caries susceptibility in periodontally treated patients. Results after 12 years. J Clin Periodontol. 1993;20(2):124-129. doi:10.1111/j.1600-051x.1993.tb00326.x
 
63.
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):2435-2446. doi:10.1038/ismej.2016.37
 
64.
Seneviratne CJ, Zhang CF, Samaranayake LP. Dental plaque biofilm in oral health and disease. Chin J Dent Res. 2011;14(2):87-94. https://cjdr.quintessenz.de/in.... Accessed December 17, 2018.
 
65.
Krzysciak W, Jurczak A, Koscielniak D, Bystrowska B, Skalniak A. The virulence of Streptococcus mutans and the ability to form biofilms. Eur J Clin Microbiol Infect Dis. 2014;33(4):499-515. doi:10.1007/s10096-013-1993-7
 
66.
Macgregor ID, Edgar WM, Greenwood AR. Effects of cigarette smoking on the rate of plaque formation. J Clin Periodontol. 1985;12(1):35-41. doi:10.1111/j.1600-051x.1985.tb01351.x
 
67.
Huang R, Li M, Gregory RL. Bacterial interactions in dental biofilm. Virulence. 2011;2(5):435-444. doi:10.4161/viru.2.5.16140
 
68.
Vukosavljevic D, Custodio W, Buzalaf MA, Hara AT, Siqueira WL. Acquired pellicle as a modulator for dental erosion. Arch Oral Biol. 2014;59(6):631-638. doi:10.1016/j.archoralbio.2014.02.002
 
69.
Evans P, Der G, Ford G, Hucklebridge F, Hunt K, Lambert S. Social class, sex, and age differences in mucosal immunity in a large community sample. Brain Behav Immun. 2000;14(1):41-48. doi:10.1006/brbi.1999.0571
 
70.
Golpasand HL, Zakavi F, Ansarifar S, Ghasemzadeh O, Solgi G. Association of dental caries and salivary sIgA with tobacco smoking. Aust Dent J. 2013;58(2):219-223. doi:10.1111/adj.12059
 
71.
Avsar A, Darka O, Bodrumlu EH, Bek Y. Evaluation of the relationship between passive smoking and salivary electrolytes, protein, secretory IgA, sialic acid and amylase in young children. Arch Oral Biol. 2009;54(5):457-463. doi:10.1016/j.archoralbio.2009.01.017
 
72.
Struzycka I. The oral microbiome in dental caries. Pol J Microbiol. 2014;63(2):127-135. http://www.pjm.microbiology.pl.... Accessed December 17, 2018.
 
73.
Jette AM, Feldman HA, Tennstedt SL. Tobacco use: a modifiable risk factor for dental disease among the elderly. Am J Public Health. 1993;83(9):1271-1276. doi:10.2105/ajph.83.9.1271
 
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