We hypothesized that tobacco smoke induces alterations to the 3-OH fatty acids present in lipid A in a manner consistent with a microflora of reduced inflammatory potential. Whole saliva samples and full-mouth clinical periodontal recordings were obtained from persons with (22 smokers; 15 non-smokers) and without (14 smokers; 15 non-smokers) chronic periodontitis. Clear differences in the contributions of multiple saturated 3-OH fatty acid species were noted in the group with disease compared with healthy individuals. Increases in the long-chain fatty acids associated with anaerobic bacterial periodontopathogens, particularly 3-OH-Ci17.0 (146.7%, relative to controls), were apparent. Significant reductions in the 3-OH fatty acids associated with the consensus (high potency) enteric LPS structure (3-OH-C12.0 and 3-OH-C14.0; 33.3% and 15.8% reduction, respectively) were noted in smokers compared with non-smokers with chronic periodontitis. Thus, smoking is associated with specific structural alterations to the lipid-A-derived 3-OH fatty acid profile in saliva that are consistent with an oral microflora of reduced inflammatory potential. These findings provide much-needed mechanistic insight into the established clinical conundrum of increased infection with periodontal pathogens but reduced clinical inflammation in smokers.
AhMKJohnsonGKKaldahlWBPatilKDKalkwarfKL (1994). The effect of smoking on the response to periodontal therapy. J Clin Periodontol21:91-97.
2.
Al-QutubMNBrahamPHKarimi-NaserLMLiuXGencoCADarveauRP (2006). Hemin-dependent modulation of the lipid A structure of Porphyromonas gingivalis lipopolysaccharide. Infect Immun74:4474-4485.
3.
ArmitageGC (1999). Development of a classification system for periodontal diseases and conditions. Ann Periodontol4:1-6.
4.
BagyiKHaczkuAMartonISzaboJGasparAAndrasiM. (2009). Role of pathogenic oral flora in postoperative pneumonia following brain surgery. BMC Infect Dis9:104.
5.
BainbridgeBWCoatsSRPhamTTReifeRADarveauRP (2006). Expression of a Porphyromonas gingivalis lipid A palmitylacyltransferase in Escherichia coli yields a chimeric lipid A with altered ability to stimulate interleukin-8 secretion. Cell Microbiol8:120-129.
6.
BaljoonM (2005). Tobacco smoking and vertical periodontal bone loss. Swed Dent J Suppl174:1-62.
7.
BarbourSENakashimaKZhangJBTangadaSHahnCLSchenkeinHA. (1997). Tobacco and smoking: environmental factors that modify the host response (immune system) and have an impact on periodontal health. Crit Rev Oral Biol Med8:437-460.
8.
BerezowABErnstRKCoatsSRBrahamPHKarimi-NaserLMDarveauRP (2009). The structurally similar, penta-acylated lipopolysaccharides of Porphyromonas gingivalis and Bacteroides elicit strikingly different innate immune responses. Microb Pathog47:68-77.
9.
BergströmJ (2004). Influence of tobacco smoking on periodontal bone height. Long-term observations and a hypothesis. J Clin Periodontol31:260-266.
10.
BoströmLBergströmJDahlénGLinderLE (2001). Smoking and subgingival microflora in periodontal disease. J Clin Periodontol28:212-219.
11.
BrondzIOlsenI (1991). Multivariate analyses of cellular fatty acids in Bacteroides, Prevotella, Porphyromonas, Wolinella, and Campylobacter spp. J Clin Microbiol29:183-189.
12.
CalsinaGRamonJMEcheverriaJJ (2002). Effects of smoking on periodontal tissues. J Clin Periodontol29:771-776.
13.
DahleURTronstadLOlsenI (1996). 3-Hydroxy fatty acids in a lipopolysaccharide-like material from Treponema denticola strain FM. Endod Dent Traumatol12:202-205.
14.
DixonDRDarveauRP (2005). Lipopolysaccharide heterogeneity: innate host responses to bacterial modification of lipid A structure. J Dent Res84:584-595.
15.
FerrandoRSzponarBSanchezALarssonLValero-GuillenPL (2005). 3-Hydroxy fatty acids in saliva as diagnostic markers in chronic periodontitis. J Microbiol Methods62:285-291.
16.
FisherSKellsLPicardJ-PGelskeySCSingerDLLixL. (2008). Progression of periodontal disease in a maintenance population of smokers and non-smokers: a three-year longitudinal study. J Periodontol79:461-468.
17.
GomesSCNonnenmacherCSusinCOppermannRVMuttersRMarcantonioRA (2008). The effect of a supragingival plaque-control regimen on the subgingival microbiota in smokers and never-smokers: evaluation by real-time polymerase chain reaction. J Periodontol79:2297-2304.
HaberJ (1994). Smoking is a major risk factor for periodontitis. Curr Opin Periodontol1994:12-18.
20.
HaffajeeADSocranskySS (2001). Relationship of cigarette smoking to the subgingival microbiota. J Clin Periodontol28:377-388.
21.
HaffajeeADCuginiMADibartSSmithCKentRLJrSocranskySS (1997). The effect of SRP on the clinical and microbiological parameters of periodontal diseases. J Clin Periodontol24:324-334.
22.
HoltSCEbersoleJL (2005). Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: the “red complex,” a prototype polybacterial pathogenic consortium in periodontitis. Periodontol 200038:72-122.
23.
JohnsonGKGuthmillerJM (2007). The impact of cigarette smoking on periodontal disease and treatment. Periodontol 200044:178-194.
24.
JohnsonGKHillM (2004). Cigarette smoking and the periodontal patient. J Periodontol75:196-209.
25.
KammaJJNakouMBaehniPC (1999). Clinical and microbiological characteristics of smokers with early onset periodontitis. J Periodontal Res34:25-33.
26.
KhairaNPalmerRMWilsonRFScottDAWadeWG (2000). Production of volatile sulphur compounds in diseased periodontal pockets is significantly increased in smokers. Oral Dis6:371-375.
LarssonLSarafA (1997). Use of gas chromatography-ion trap tandem mass spectrometry for the detection and characterization of microorganisms in complex samples. Mol Biotechnol7:279-287.
29.
LoescheWGrossmanNS (2001). Periodontal disease as a specific, albeit chronic, infection: diagnosis and disease. Clin Microbiol Rev14:727-752.
30.
Martinez-PabonMCRestrepo-OspinaDPIsaza-GuzmanDMOrozco-RojasLMTobon-ArroyaveSI (2008). Detection of Treponema denticola in saliva obtained from patients with various periodontal conditions. Clin Oral Investig12:73-81.
31.
McMurrayCMMooreGEVincentR (1969). Gingival bleeding after cessation of smoking. J Oral Med24:131.
32.
MullallyBH (2004). The influence of tobacco smoking on the onset of periodontitis in young persons. Tob Induc Dis2:53-65.
33.
NairPSutherlandGPalmerRMWilsonRFScottDA (2003). Gingival bleeding on probing increases after quitting smoking. J Clin Periodontol30:435-437.
34.
OgawaTNakazawaMMasuiK (1996). Immunopharmacological activities of the nontoxic monophosphoryl lipid A of Porphyromonas gingivalis. Vaccine14:70-76.
35.
OgawaTAsaiYMakimuraYTamaiR (2007). Chemical structure and immunobiological activity of Porphyromonas gingivalis lipid A. Front Biosci12:3795-3812.
36.
PalmerRMWilsonRFHasanASScottDA (2005). Mechanisms of action of environmental factors—tobacco smoking. J Clin Periodontol32(Suppl 6):180-195.
37.
PindborgJJ (1947). Tobacco and gingivitis. J Dent Res26:261 (passim).
38.
RebeilRErnstRKGowenBBMillerSIHinnebuschBJ (2004). Variation in lipid A structure in the pathogenic yersiniae. Mol Microbiol52:1363-1373.
39.
SakamotoMSuzukiMUmedaMIshikawaIBennoY (2002). Reclassification of Bacteroides forsythus (Tanner et al., 1986) as Tannerella forsythensis corrig., gen. nov., comb. nov. Int J Syst Evol Microbiol52(Pt 3):841-849.
40.
SchrommABBrandenburgKLoppnowHMoranAPKochMHRietschelET. (2000). Biological activities of lipopolysaccharides are determined by the shape of their lipid A portion. Eur J Biochem267:2008-2013.
41.
SchultzCPWolfVLangeRMertensEWeckeJNaumannD. (1998). Evidence for a new type of outer membrane lipid in oral spirochete Treponema denticola. Functioning permeation barrier without lipopolysaccharides. J Biol Chem273:15661-15666.
42.
ScottDASingerDL (2004). Suppression of overt gingival inflammation in tobacco smokers—clinical and mechanistic considerations. Int J Dent Hyg2:104-110.
43.
ScottDAPalmerRMStapletonJA (2001). Validation of smoking status in clinical research into inflammatory periodontal disease. J Clin Periodontol28:715-722.
44.
SebastianALarssonL (2003). Characterization of the microbial community in indoor environments: a chemical-analytical approach. Appl Environ Microbiol69:3103-3109.
45.
ShiloahJPattersMRWaringMB (2000). The prevalence of pathogenic periodontal microflora in healthy young adult smokers. J Periodontol71:562-567.
46.
SingARostDTvardovskaiaNRoggenkampAWiedemannAKirschningCJ. (2002). Yersinia V-antigen exploits Toll-like receptor 2 and CD14 for interleukin 10-mediated immunosuppression. J Exp Med196:1017-1024.
47.
SzponarBNorinEMidtvedtTLarssonL (2002). Limitations in the use of 3-hydroxy fatty acid analysis to determine endotoxin in mammalian samples. J Microbiol Methods50:283-289.
48.
UmedaMChenCBakkerIContrerasAMorrisonJLSlotsJ (1998). Risk indicators for harboring periodontal pathogens. J Periodontol69:1111-1118.
49.
Van AsscheNVan EsscheMPauwelsMTeughelsWQuirynenM (2009). Do periodontopathogens disappear after full-mouth tooth extraction?J Clin Periodontol36:1043-1047.
50.
van WinkelhoffAJBosch-TijhofCJWinkelEGvan der ReijdenWA (2001). Smoking affects the subgingival microflora in periodontitis. J Periodontol72:666-671.
51.
WyssC (2007). Fatty acids synthesized by oral treponemes in chemically defined media. FEMS Microbiol Lett269:70-76.
52.
ZambonJJGrossiSGMachteiEEHoAWDunfordRGencoRJ (1996). Cigarette smoking increases the risk for subgingival infection with periodontal pathogens. J Periodontol67(10 Suppl):1050S-1054S.
