726
Views
0
CrossRef citations to date
0
Altmetric
Review Article

Exploring the role of oral microbiome dysbiosis in cardiometabolic syndrome and smoking

, , &
Pages 65-84 | Received 31 Oct 2023, Accepted 11 Mar 2024, Published online: 27 Mar 2024

References

  • Ursell LK, Metcalf JL, Parfrey LW, Knight R. Defining the human microbiome. Nutr Rev. 2012;70 Suppl 1(Suppl 1):S38–S44. doi:10.1111/j.1753-4887.2012.00493.x.
  • A review of 10 years of human microbiome research activities at the US National Institutes of Health, Fiscal Years 2007-2016. Microbiome. 2019;7(1):31. doi:10.1186/s40168-019-0620-y.
  • Ezzati M, Lopez AD. Regional, disease specific patterns of smoking-attributable mortality in 2000. Tob Control. 2004;13(4):388–395. doi:10.1136/tc.2003.005215.
  • Sultan S, Lesloom F. A prospective analysis of the association of smoking with cardiometabolic risk. 2023.
  • Wu J, Peters BA, Dominianni C, 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.
  • Wirth R, Maróti G, Mihók R, et al. A case study of salivary microbiome in smokers and non-smokers in Hungary: analysis by shotgun metagenome sequencing. J Oral Microbiol. 2020;12(1):1773067. doi:10.1080/20002297.2020.1773067.
  • Jia YJ, Liao Y, He YQ, et al. Association between oral microbiota and cigarette smoking in the Chinese population. Front Cell Infect Microbiol. 2021;11:658203. doi:10.3389/fcimb.2021.658203.
  • Bui FQ, Almeida-da-Silva CLC, Huynh B, et al. Association between periodontal pathogens and systemic disease. Biomed J. 2019;42(1):27–35. doi:10.1016/j.bj.2018.12.001.
  • Huang Q, Wu X, Zhou X, et al. Association of cigarette smoking with oral bacterial microbiota and cardiometabolic health in Chinese adults. BMC Microbiol. 2023;23(1):346. doi:10.1186/s12866-023-03061-y.
  • Dewhirst FE, Chen T, Izard J, et al. The human oral microbiome. J Bacteriol. 2010;192(19):5002–5017. doi:10.1128/JB.00542-10.
  • Lamont RJ, Koo H, Hajishengallis G. The oral microbiota: dynamic communities and host interactions. Nat Rev Microbiol. 2018;16(12):745–759. doi:10.1038/s41579-018-0089-x.
  • Structure, function and diversity of the healthy human microbiome. Nature. 2012;486(7402):207–214. doi:10.1038/nature11234.
  • Deo P, Deshmukh R. Oral microbiome: unveiling the fundamentals. J Oral Maxillofac Pathol. 2019;23(1):122–128. doi:10.4103/jomfp.JOMFP_304_18.
  • Lim Y, Totsika M, Morrison M, Punyadeera C. Oral microbiome: a new biomarker reservoir for oral and oropharyngeal cancers. Theranostics. 2017;7(17):4313–4321. doi:10.7150/thno.21804.
  • Bacali C, Vulturar R, Buduru S, et al. Oral microbiome: getting to know and befriend neighbors, a biological approach. Biomedicines. 2022;10(3):671. doi:10.3390/biomedicines10030671.
  • Kilian M, Chapple ILC, Hannig M, et al. The oral microbiome – an update for oral healthcare professionals. Br Dent J. 2016;221(10):657–666. doi:10.1038/sj.bdj.2016.865.
  • Marsh PD. Role of the oral microflora in health. Microb Ecol Health Dis. 2009;12(3):130–137. doi:10.1080/089106000750051800.
  • Marsh PD, Takahashi N, Nyvad B. Dental Caries the Disease and Its Clinical Management. 3rd ed. (Fejerskov O, Nyvad B, Kidd E, eds.). John Wiley & Sons; Hoboken, New Jersey, USA; 2016.
  • Willey JM, Sherwood L, Woolverton CJ, Prescott LM. Prescott, Harley, and Klein’s Microbiology. 7th ed. McGraw-Hill Higher Education; New York, NY, USA; 2008.
  • Gao L, Xu T, Huang G, Jiang S, Gu Y, Chen F. Oral microbiomes: more and more importance in oral cavity and whole body. Protein Cell. 2018;9(5):488–500. doi:10.1007/s13238-018-0548-1.
  • Zhang Y, Wang X, Li H, Ni C, Du Z, Yan F. Human oral microbiota and its modulation for oral health. Biomed Pharmacother. 2018;99:883–893. doi:10.1016/j.biopha.2018.01.146.
  • Verma D, Garg PK, Dubey AK. Insights into the human oral microbiome. Arch Microbiol. 2018;200(4):525–540. doi:10.1007/s00203-018-1505-3.
  • Seymour GJ, Ford PJ, Cullinan MP, Leishman S, Yamazaki K. Relationship between periodontal infections and systemic disease. Clin Microbiol Infect. 2007;13 Suppl 4:3–10. doi:10.1111/j.1469-0691.2007.01798.x.
  • Offenbacher S, Jared HL, O’Reilly PG, et al. Potential pathogenic mechanisms of periodontitis-associated pregnancy complications. Ann Periodontol. 1998;3(1):233–250. doi:10.1902/annals.1998.3.1.233.
  • Joshipura KJ, Rimm EB, Douglass CW, Trichopoulos D, Ascherio A, Willett WC. Poor oral health and coronary heart disease. J Dent Res. 1996;75(9):1631–1636. doi:10.1177/00220345960750090301.
  • Joshipura KJ, Hung HC, Rimm EB, Willett WC, Ascherio A. Periodontal disease, tooth loss, and incidence of ischemic stroke. Stroke. 2003;34(1):47–52. doi:10.1161/01.STR.0000052974.79428.0C.
  • Genco RJ, Grossi SG, Ho A, Nishimura F, Murayama Y. A proposed model linking inflammation to obesity, diabetes, and periodontal infections. J Periodontol. 2005;76(11 Suppl):2075–2084. doi:10.1902/jop.2005.76.11-S.2075.
  • Beck JD, Offenbacher S. Systemic effects of periodontitis: epidemiology of periodontal disease and cardiovascular disease. J Periodontol. 2005;76(11 Suppl):2089–2100. doi:10.1902/jop.2005.76.11-S.2089.
  • Meyle J, Chapple I. Molecular aspects of the pathogenesis of periodontitis. Periodontol 2000. 2015;69(1):7–17. doi:10.1111/prd.12104.
  • Ramseier CA, Anerud A, Dulac M, et al. Natural history of periodontitis: disease progression and tooth loss over 40 years. J Clin Periodontol. 2017;44(12):1182–1191. doi:10.1111/jcpe.12782.
  • King S, Chow CK, Eberhard J. Oral health and cardiometabolic disease: understanding the relationship. Intern Med J. 2022;52(2):198–205. doi:10.1111/imj.15685.
  • Loesche WJ, Grossman NS. Periodontal disease as a specific, albeit chronic, infection: diagnosis and treatment. Clin Microbiol Rev. 2001;14(4):727–752. doi:10.1128/CMR.14.4.727-752.2001.
  • Holmstrup P, Damgaard C, Olsen I, et al. Comorbidity of periodontal disease: two sides of the same coin? An introduction for the clinician. J Oral Microbiol. 2017;9(1):1332710. doi:10.1080/20002297.2017.1332710.
  • Contaldo M, Itro A, Lajolo C, Gioco G, Inchingolo F, Serpico R. Overview on osteoporosis, periodontitis and oral dysbiosis: the emerging role of oral microbiota. Appl Sci. 2020;10(17):6000. doi:10.3390/app10176000.
  • Polak D, Shapira L. An update on the evidence for pathogenic mechanisms that may link periodontitis and diabetes. J Clin Periodontol. 2018;45(2):150–166. doi:10.1111/jcpe.12803.
  • Sanz M, Marco del Castillo A, Jepsen S, et al. Periodontitis and cardiovascular diseases: consensus report. J Clin Periodontol. 2020;47(3):268–288. doi:10.1111/jcpe.13189.
  • Parvaneh M, Witting PK, Ku J, et al. Periodontitis induces endothelial dysfunction in mice. Sci Rep. 2021;11(1):14993. doi:10.1038/s41598-021-94418-8.
  • Hasturk H, Kantarci A. Activation and resolution of periodontal inflammation and its systemic impact. Periodontol 2000. 2015;69(1):255–273. doi:10.1111/prd.12105.
  • Rosier BT, Marsh PD, Mira A. Resilience of the oral microbiota in health: mechanisms that prevent dysbiosis. J Dent Res. 2018;97(4):371–380. doi:10.1177/0022034517742139.
  • Hajishengallis G. The inflammophilic character of the periodontitis-associated microbiota. Mol Oral Microbiol. 2014;29(6):248–257. doi:10.1111/omi.12065.
  • Maekawa T, Krauss JL, Abe T, et al. Porphyromonas gingivalis manipulates complement and TLR signaling to uncouple bacterial clearance from inflammation and promote dysbiosis. Cell Host Microbe. 2014;15(6):768–778. doi:10.1016/j.chom.2014.05.012.
  • Duran-Pinedo AE, Chen T, Teles R, et al. Community-wide transcriptome of the oral microbiome in subjects with and without periodontitis. ISME J. 2014;8(8):1659–1672. doi:10.1038/ismej.2014.23.
  • Humphrey LL, Fu R, Buckley DI, Freeman M, Helfand M. Periodontal disease and coronary heart disease incidence: a systematic review and meta-analysis. J Gen Intern Med. 2008;23(12):2079–2086. doi:10.1007/s11606-008-0787-6.
  • Larvin H, Kang J, Aggarwal VR, Pavitt S, Wu J. Risk of incident cardiovascular disease in people with periodontal disease: a systematic review and meta‐analysis. Clin Exp Dent Res. 2021;7(1):109–122. doi:10.1002/cre2.336.
  • Leng WD, Zeng XT, Kwong JSW, Hua XP. Periodontal disease and risk of coronary heart disease: an updated meta-analysis of prospective cohort studies. Int J Cardiol. 2015;201:469–472. doi:10.1016/j.ijcard.2015.07.087.
  • Leira Y, Seoane J, Blanco M, et al. Association between periodontitis and ischemic stroke: a systematic review and meta-analysis. Eur J Epidemiol. 2017;32(1):43–53. doi:10.1007/s10654-016-0170-6.
  • Muñoz Aguilera E, Suvan J, Buti J, et al. Periodontitis is associated with hypertension: a systematic review and meta-analysis. Cardiovasc Res. 2020;116(1):28–39. doi:10.1093/cvr/cvz201.
  • Garde S, Akhter R, Nguyen MA, Chow CK, Eberhard J. Periodontal therapy for improving lipid profiles in patients with type 2 diabetes mellitus: a systematic review and meta-analysis. Int J Mol Sci. 2019;20(15):3826. doi:10.3390/ijms20153826.
  • Stöhr J, Barbaresko J, Neuenschwander M, Schlesinger S. Bidirectional association between periodontal disease and diabetes mellitus: a systematic review and meta-analysis of cohort studies. Sci Rep. 2021;11(1):13686. doi:10.1038/s41598-021-93062-6.
  • Fontana CR, Grecco C, Bagnato VS, de Freitas LM, Boussios CI, Soukos NS. Molecular analyses of two bacterial sampling methods in ligature-induced periodontitis in rats. Clin Exp Dent Res. 2018;4(1):19–24. doi:10.1002/cre2.98.
  • Marotz C, Molinsky R, Martino C, et al. Early microbial markers of periodontal and cardiometabolic diseases in ORIGINS. NPJ Biofilms Microbiomes. 2022;8(1):30. doi:10.1038/s41522-022-00289-w.
  • Moon JH, Lee JH, Lee JY. Subgingival microbiome in smokers and non-smokers in Korean chronic periodontitis patients. Mol Oral Microbiol. 2015;30(3):227–241. doi:10.1111/omi.12086.
  • Schenkein HA, Loos BG. Inflammatory mechanisms linking periodontal diseases to cardiovascular diseases. J Clin Periodontol. 2013;40 Suppl 14 (0 14):S51–S69. doi:10.1111/jcpe.12060.
  • Grundy SM, Cleeman JI, Daniels SR, et al. Diagnosis and management of the metabolic syndrome: An American Heart Association/National Heart, Lung, and Blood Institute scientific statement. Circulation. 2005;112(17):2735–2752. doi:10.1161/CIRCULATIONAHA.105.169404.
  • Hossain P, Kawar B, El Nahas M. Obesity and diabetes in the developing world—a growing challenge. N Engl J Med. 2007;356(3):213–215. doi:10.1056/NEJMp068177.
  • Wilson PWF, D’Agostino RB, Parise H, Sullivan L, Meigs JB. Metabolic syndrome as a precursor of cardiovascular disease and type 2 diabetes mellitus. Circulation. 2005;112(20):3066–3072. doi:10.1161/CIRCULATIONAHA.105.539528.
  • Kelli HM, Kassas I. Cardio metabolic syndrome: a global epidemic. J Diabetes Metab. 2016;6:513. doi:10.4172/2155-6156.1000513.
  • Arnlöv J, Ingelsson E, Sundström J, Lind L. Impact of Body Mass Index and the metabolic syndrome on the risk of cardiovascular disease and death in middle-aged men. Circulation. 2010;121(2):230–236. doi:10.1161/CIRCULATIONAHA.109.887521.
  • Irace C, Cortese C, Fiaschi E, et al. Components of the metabolic syndrome and carotid atherosclerosis. Hypertension. 2005;45(4):597–601. doi:10.1161/01.HYP.0000158945.52283.c2.
  • Misra A, Khurana L. Obesity and the metabolic syndrome in developing countries. J Clin Endocrinol Metab. 2008;93(11 SUPPL. 1):S9–S30. doi:10.1210/jc.2008-1595.
  • Grundy SM. Metabolic syndrome pandemic. Arterioscler Thromb Vasc Biol. 2008;28(4):629–636. doi:10.1161/ATVBAHA.107.151092.
  • Eyth E, Naik R. Hemoglobin A1C. StatPearls Publishing; St. Petersburg, Florida, United States; 2023.
  • Saeedi P, Petersohn I, Salpea P, et al. Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: Results from the International Diabetes Federation Diabetes Atlas, 9th edition. Diabetes Res Clin Pract. 2019; November; 157:107843. doi:10.1016/j.diabres.2019.107843.
  • Lockhart PB, Bolger AF, Papapanou PN, et al. Periodontal disease and atherosclerotic vascular disease: does the evidence support an independent association? Circulation. 2012;125(20):2520–2544. doi:10.1161/CIR.0b013e31825719f3.
  • Lalla E, Papapanou PN. Diabetes mellitus and periodontitis: a tale of two common interrelated diseases. Nat Rev Endocrinol. 2011;7(12):738–748. doi:10.1038/nrendo.2011.106.
  • Kebschull M, Demmer RT, Papapanou PN. Gum bug, leave my heart alone !”—Epidemiologic and mechanistic evidence linking periodontal infections and atherosclerosis. J Dent Res. 2010;89(9):879–902. doi:10.1177/0022034510375281.
  • Ebersole JL, Holt SC, Hansard R, Novak MJ. Microbiologic and immunologic characteristics of periodontal disease in Hispanic Americans with type 2 diabetes. J Periodontol. 2008;79(4):637–646. doi:10.1902/jop.2008.070455.
  • Miranda TS, Feres M, Retamal-Valdés B, Perez-Chaparro PJ, Maciel SS, Duarte PM. Influence of glycemic control on the levels of subgingival periodontal pathogens in patients with generalized chronic periodontitis and type 2 diabetes. J Appl Oral Sci. 2017;25(1):82–89. doi:10.1590/1678-77572016-0302.
  • Shaalan A, Lee S, Feart C, et al. Alterations in the oral microbiome associated with diabetes, overweight, and dietary components. Front Nutr. 2022;9:914715. doi:10.3389/fnut.2022.914715.
  • Pandian DS, Victor DJ, Cholan P, Prakash P, Subramanian S, Shankar SP. Comparative analysis of the red-complex organisms and recently identified periodontal pathogens in the subgingival plaque of diabetic and nondiabetic patients with severe chronic periodontitis. J Indian Soc Periodontol. 2023;27(1):51–56. doi:10.4103/jisp.jisp_136_21.
  • Sohail MU, Hedin L, Al-Asmakh M. Dysbiosis of the salivary microbiome is associated with hypertension and correlated with metabolic syndrome biomarkers. Diabetes Metab Syndr Obes. 2021;14:4641–4653. doi:10.2147/DMSO.S325073.
  • Lim SS, Vos T, Flaxman AD, et al. A comparative risk assessment of burden of disease and injury attributable to 67 risk factors and risk factor clusters in 21 regions, 1990–2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet. 2012;380(9859):2224–2260. doi:10.1016/S0140-6736(12)61766-8.
  • Iqbal AM, Jamal SF. Essential Hypertension. StatPearls Publishing; St. Petersburg, Florida, United States; 2022.
  • Bondonno CP, Liu AH, Croft KD, et al. Antibacterial mouthwash blunts oral nitrate reduction and increases blood pressure in treated hypertensive men and women. Am J Hypertens. 2015;28(5):572–575. doi:10.1093/ajh/hpu192.
  • Murugesan S, Al Khodor S. Salivary microbiome and hypertension in the Qatari population. J Transl Med. 2023;21(1):454. doi:10.1186/s12967-023-04247-8.
  • Barbadoro P, Ponzio E, Coccia E, et al. Association between hypertension, oral microbiome and salivary nitric oxide: A case-control study. Nitric Oxide. 2021;106:66–71. doi:10.1016/j.niox.2020.11.002.
  • Gordon JH, LaMonte MJ, Genco RJ, et al. Is the oral microbiome associated with blood pressure in older women? High Blood Press Cardiovasc Prev. 2019;26(3):217–225. doi:10.1007/s40292-019-00322-8.
  • Perry SE, Huckabee M, Tompkins G, Milne T. The association between oral bacteria, the cough reflex and pneumonia in patients with acute stroke and suspected dysphagia. J Oral Rehabil. 2020;47(3):386–394. doi:10.1111/joor.12903.
  • Boaden E, Lyons M, Singhrao SK, et al. Oral flora in acute stroke patients: a prospective exploratory observational study. Gerodontology. 2017;34(3):343–356. doi:10.1111/ger.12271.
  • Kobayashi R, Ogawa Y, Hashizume-Takizawa T, Kurita-Ochiai T. Oral bacteria affect the gut microbiome and intestinal immunity. Pathog Dis. 2020;78(3) doi:10.1093/femspd/ftaa024.
  • Pasini E, Aquilani R, Testa C, et al. Pathogenic gut flora in patients with chronic heart failure. JACC Heart Fail. 2016;4(3):220–227. doi:10.1016/j.jchf.2015.10.009.
  • Leskelä J, Pietiäinen M, Safer A, et al. Serum lipopolysaccharide neutralizing capacity in ischemic stroke. PLoS One. 2020;15(2):e0228806. doi:10.1371/journal.pone.0228806.
  • Maki KA, Ganesan SM, Meeks B, et al. The role of the oral microbiome in smoking-related cardiovascular risk: a review of the literature exploring mechanisms and pathways. J Transl Med. 2022;20(1):584. doi:10.1186/s12967-022-03785-x.
  • Liljestrand JM, Paju S, Pietiäinen M, et al. Immunologic burden links periodontitis to acute coronary syndrome. Atherosclerosis. 2018;268:177–184. doi:10.1016/j.atherosclerosis.2017.12.007.
  • Ziebolz D, Rost C, Schmidt J, et al. Periodontal bacterial DNA and their link to human cardiac tissue: findings of a pilot study. Thorac Cardiovasc Surg. 2018;66(1):83–90. doi:10.1055/s-0035-1564689.
  • Ziebolz D, Jahn C, Pegel J, et al. Periodontal bacteria DNA findings in human cardiac tissue – is there a link of periodontitis to heart valve disease? Int J Cardiol. 2018;251:74–79. doi:10.1016/j.ijcard.2017.09.001.
  • Neves AL, Coelho J, Couto L, Leite-Moreira A, Roncon-Albuquerque R. Metabolic endotoxemia: a molecular link between obesity and cardiovascular risk. J Mol Endocrinol. 2013;51(2):R51–R64. doi:10.1530/JME-13-0079.
  • Lund Håheim L, Schwarze PE, Thelle DS, Nafstad P, Rønningen KS, Olsen I. Low levels of antibodies for the oral bacterium Tannerella forsythia predict cardiovascular disease mortality in men with myocardial infarction: a prospective cohort study. Med Hypotheses. 2020;138:109575. doi:10.1016/j.mehy.2020.109575.
  • Serra e Silva Filho W, Casarin RCV, Nicolela EL, Passos HM, Sallum AW, Gonçalves RB. Microbial diversity similarities in periodontal pockets and atheromatous plaques of cardiovascular disease patients. PLoS One. 2014;9(10):e109761. doi:10.1371/journal.pone.0109761.
  • Mahalakshmi K, Krishnan P, Arumugam SB. Association of periodontopathic anaerobic bacterial co-occurrence to atherosclerosis” – a cross-sectional study. Anaerobe. 2017;44:66–72. doi:10.1016/j.anaerobe.2017.02.003.
  • Chalupova M, Skalova A, Hajek T, et al. Bacterial DNA detected on pathologically changed heart valves using 16S rRNA gene amplification. Folia Microbiol (Praha). 2018;63(6):707–711. doi:10.1007/s12223-018-0611-6.
  • Moreno S, Parra B, Botero JE, et al. Periodontal microbiota and microorganisms isolated from heart valves in patients undergoing valve replacement surgery in a clinic in Cali, Colombia. Biomedica. 2017;37(4):516–525. doi:10.7705/biomedica.v37i4.3232.
  • Oliveira FAF, Forte CPF, Silva Pg de B, et al. Molecular analysis of oral bacteria in heart valve of patients with cardiovascular disease by real-time polymerase chain reaction. Medicine (Baltimore). 2015;94(47):e2067. doi:10.1097/MD.0000000000002067.
  • Nakano K, Nemoto H, Nomura R, et al. Detection of oral bacteria in cardiovascular specimens. Oral Microbiol Immunol. 2009;24(1):64–68. doi:10.1111/j.1399-302X.2008.00479.x.
  • Koren O, Spor A, Felin J, et al. Human oral, gut, and plaque microbiota in patients with atherosclerosis. Proc Natl Acad Sci USA. 2011;108 Suppl 1 (Suppl 1):4592–4598. doi:10.1073/pnas.1011383107.
  • Tam J, Hoffmann T, Fischer S, Bornstein S, Gräßler J, Noack B. Obesity alters composition and diversity of the oral microbiota in patients with type 2 diabetes mellitus independently of glycemic control. PLoS One. 2018;13(10):e0204724. doi:10.1371/journal.pone.0204724.
  • de Andrade DR, Silva PA, Colombo AV, Silva‐Boghossian CM. Subgingival microbiota in overweight and obese young adults with no destructive periodontal disease. J Periodontol. 2021;92(10):1410–1419. doi:10.1002/JPER.20-0187.
  • Lu M, Xuan S, Wang Z. Oral microbiota: A new view of body health. Food Sci Hum Wellness. 2019;8(1):8–15. doi:10.1016/j.fshw.2018.12.001.
  • Kamalul Aripin NF, Idayu Zahid N, Abdul Rahim MA, et al. A review of salivary composition changes induced by fasting and its impact on health. Food Sci Human Wellness. 2023;13(1):50–64. doi:10.26599/FSHW.2022.9250004.
  • Sohail MU, Elrayess MA, Al Thani AA, Al-Asmakh M, Yassine HM. Profiling the oral microbiome and plasma biochemistry of obese hyperglycemic subjects in Qatar. Microorganisms. 2019;7(12):645. doi:10.3390/microorganisms7120645.
  • Yang Y, Cai Q, Zheng W, et al. Oral microbiome and obesity in a large study of low-income and African-American populations. J Oral Microbiol. 2019;11(1):1650597. doi:10.1080/20002297.2019.1650597.
  • Coker MO, Lebeaux RM, Hoen AG, et al. Metagenomic analysis reveals associations between salivary microbiota and body composition in early childhood. Sci Rep. 2022;12(1):13075. doi:10.1038/s41598-022-14668-y.
  • Iyer P. Oral cavity is the gateway to the body: role of oral health professionals: a narrative review. J Calif Dent Assoc. 2023;51(1). doi:10.1080/19424396.2023.2193372.
  • Sun K, Liu J, Ning G. Active smoking and risk of metabolic syndrome: a meta-analysis of prospective studies. PLoS One. 2012;7(10):e47791. doi:10.1371/journal.pone.0047791.
  • Kelishadi R, Noori A, Qorbani M, et al. Are active and passive smoking associated with cardiometabolic risk factors in adolescents? The CASPIAN-III study. Paediatr Int Child Health. 2016;36(3):181–188. doi:10.1179/2046905515Y.0000000039.
  • Gastaldelli A, Folli F, Maffei S. Impact of tobacco smoking on lipid metabolism, body weight and cardiometabolic risk. Curr Pharm Des. 2010;16(23):2526–2530. doi:10.2174/138161210792062858.
  • Azevedo PS, Polegato BF, Paiva S, et al. The role of glucose metabolism and insulin resistance in cardiac remodelling induced by cigarette smoke exposure. J Cell Mol Med. 2021;25(2):1314–1318. doi:10.1111/jcmm.16053.
  • Rigotti NA, Clair C. Managing tobacco use: The neglected cardiovascular disease risk factor. Eur Heart J. 2013;34(42):3259–3267. doi:10.1093/eurheartj/eht352.
  • Harris KK, Zopey M, Friedman TC. Erratum: metabolic effects of smoking cessation. Nat Rev Endocrinol. 2016;12(11):684–684. doi:10.1038/nrendo.2016.171.
  • Byung JK, Bum SK, Ki CS, Jin HK, Man HL, Jung RP. Association of smoking status, weight change, and incident metabolic syndrome in men: A 3-year follow-up study. Diabetes Care. 2009;32(7):1314–1316. doi:10.2337/dc09-0060.
  • Berkowitz L, Pardo-Roa C, Salazar GA, et al. Mucosal exposure to cigarette components induces intestinal inflammation and alters antimicrobial response in mice. Front Immunol. 2019;10:2289. doi:10.3389/fimmu.2019.02289.
  • Lee SH, Yun Y, Kim SJ, et al. Association between cigarette smoking status and composition of gut microbiota: population-based cross-sectional study. J Clin Med. 2018;7(9):282. doi:10.3390/jcm7090282.
  • Tintinger Gr TA. Harmful interactions of non-essential heavy metals with cells of the innate immune system. J Clin Toxicol. 2011;s3(01). doi:10.4172/2161-0495.S3-005.
  • Centers for Disease Control and Prevention [CDC]. How Tobacco smoke causes disease: the biology and behavioral basis for smoking-attributable disease: a report of the surgeon general. 2010
  • Ghio AJ, Hilborn ED, Stonehuerner JG, et al. Particulate matter in cigarette smoke alters iron homeostasis to produce a biological effect. Am J Respir Crit Care Med. 2008;178(11):1130–1138. doi:10.1164/rccm.200802-334OC.
  • van der Vaart H, Postma DS, Timens W, ten Hacken NHT. Acute effects of cigarette smoke on inflammation and oxidative stress: a review. Thorax. 2004;59(8):713–721. doi:10.1136/thx.2003.012468.
  • Roy J, Pallepati P, Bettaieb A, Averill-Bates DA. Acrolein induces apoptosis through the death receptor pathway in A549 lung cells: role of p53. Can J Physiol Pharmacol. 2010;88(3):353–368. doi:10.1139/Y09-134.
  • Yoshida M, Tomitori H, Machi Y, et al. Acrolein toxicity: comparison with reactive oxygen species. Biochem Biophys Res Commun. 2009;378(2):313–318. doi:10.1016/j.bbrc.2008.11.054.
  • Jamal QMS, Alharbi AH, Dhasmana A, Saxena A, Albejaidi F, Sajid M. Deciphering the influence of cigarette smoke carcinogens on CNS associated biomolecules: a computational synergistic approach. CNS Neurol Disord Drug Targets. 2021;20(6):540–555. doi:10.2174/1871527320666210309142714.
  • McEachern EK, Hwang JH, Sladewski KM, et al. Analysis of the effects of cigarette smoke on staphylococcal virulence phenotypes. Infect Immun. 2015;83(6):2443–2452. doi:10.1128/IAI.00303-15.
  • Chien J, Hwang JH, Nilaad S, et al. Cigarette smoke exposure promotes virulence of pseudomonas aeruginosa and induces resistance to neutrophil killing. Infect Immun. 2020;88(11) doi:10.1128/IAI.00527-20.
  • Brook I. The impact of smoking on oral and nasopharyngeal bacterial flora. J Dent Res. 2011;90(6):704–710. doi:10.1177/0022034510391794.
  • Shaw L, Ribeiro ALR, Levine AP, et al. The human salivary microbiome is shaped by shared environment rather than genetics: evidence from a large family of closely related individuals. mBio. 2017;8(5). doi:10.1128/mBio.01237-17.
  • Rodríguez-Rabassa M, López P, Rodríguez-Santiago R, et al. Cigarette smoking modulation of saliva microbial composition and cytokine levels. Int J Environ Res Public Health. 2018;15(11):2479. doi:10.3390/ijerph15112479.
  • Rizzatti G, Lopetuso LR, Gibiino G, Binda C, Gasbarrini A. Proteobacteria: a common factor in human diseases. Biomed Res Int. 2017;2017:9351507–9351507. doi:10.1155/2017/9351507.
  • Yang Y, Zheng W, Cai QY, et al. Cigarette smoking and oral microbiota in low-income and African-American populations. J Epidemiol Community Health. 2019;73(12):1108–1115. doi:10.1136/jech-2019-212474.
  • Al-Zyoud W, Hajjo R, Abu-Siniyeh A, Hajjaj S. Salivary microbiome and cigarette smoking: a first of its kind investigation in Jordan. Int J Environ Res Public Health. 2019;17(1):256. doi:10.3390/ijerph17010256.
  • Sato N, Kakuta M, Uchino E, et al. The relationship between cigarette smoking and the tongue microbiome in an East Asian population. J Oral Microbiol. 2020;12(1):1742527. doi:10.1080/20002297.2020.1742527.
  • Sato N, Kakuta M, Hasegawa T, et al. Metagenomic analysis of bacterial species in tongue microbiome of current and never smokers. NPJ Biofilms Microbiomes. 2020;6(1):11. doi:10.1038/s41522-020-0121-6.
  • Suzuki N, Nakano Y, Yoneda M, Hirofuji T, Hanioka T. The effects of cigarette smoking on the salivary and tongue microbiome. Clin Exp Dent Res. 2022;8(1):449–456. doi:10.1002/cre2.489.
  • Al Bataineh MT, Dash NR, Elkhazendar M, et al. Revealing oral microbiota composition and functionality associated with heavy cigarette smoking. J Transl Med. 2020;18(1):421. doi:10.1186/s12967-020-02579-3.
  • Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI. The human microbiome project. Nature. 2007;449(7164):804–810. doi:10.1038/nature06244.
  • Lynge Pedersen AM, Belstrøm D. The role of natural salivary defences in maintaining a healthy oral microbiota. J Dent. 2019;80 Suppl 1:S3–S12. doi:10.1016/j.jdent.2018.08.010.
  • Murugesan S, Al Ahmad SF, Singh P, Saadaoui M, Kumar M, Al Khodor S. Profiling the salivary microbiome of the Qatari population. J Transl Med. 2020;18(1):127. doi:10.1186/s12967-020-02291-2.
  • Nasidze I, Li J, Quinque D, Tang K, Stoneking M. Global diversity in the human salivary microbiome. Genome Res. 2009;19(4):636–643. doi:10.1101/gr.084616.108.
  • Li J, Quinque D, Horz HP, et al. Comparative analysis of the human saliva microbiome from different climate zones: Alaska, Germany, and Africa. BMC Microbiol. 2014;14(1):316. doi:10.1186/s12866-014-0316-1.
  • Clarke T, Brinkac L, Greco C, et al. Sampling from four geographically divergent young female populations demonstrates forensic geolocation potential in microbiomes. Sci Rep. 2022;12(1):18547. doi:10.1038/s41598-022-21779-z.
  • Ogbanga N, Nelson A, Ghignone S, et al. The oral microbiome for geographic origin: an Italian study. Forensic Sci Int Genet. 2023;64:102841. doi:10.1016/j.fsigen.2023.102841.
  • Neculae E, Gosav EM, Valasciuc E, Dima N, Floria M, Tanase DM. The oral microbiota in valvular heart disease: current knowledge and future directions. Life (Basel). 2023;13(1):182. doi:10.3390/life13010182.
  • Premaraj TS, Vella R, Chung J, et al. Ethnic variation of oral microbiota in children. Sci Rep. 2020;10(1):14788. doi:10.1038/s41598-020-71422-y.
  • Altayb HN, Chaieb K, Baothman O, Alzahrani FA, Zamzami MA, Almugadam BS. Study of oral microbiota diversity among groups of families originally from different countries. Saudi J Biol Sci. 2022;29(7):103317. doi:10.1016/j.sjbs.2022.103317.
  • Araújo V, Fehn AM, Phiri A, Wills J, Rocha J, Gayà-Vidal M. Oral microbiome homogeneity across diverse human groups from southern Africa: first results from southwestern Angola and Zimbabwe. BMC Microbiol. 2023;23(1):226. doi:10.1186/s12866-023-02970-2.
  • Ma G, Qiao Y, Shi H, Zhou J, Li Y. Comparison of the oral microbiota structure among people from the same ethnic group living in different environments. Biomed Res Int. 2022;2022:6544497–13. doi:10.1155/2022/6544497.