journal article·2024-06-03Open access

Does Exposure to Burning and Heated Tobacco Affect the Abundance of Perio-Pathogenic Species in the Subgingival Biofilm?

Ivana Mišković, Davor Kuiš, Stjepan Špalj, Aleksandar Pupovac, Bojana Mohar-Vitezić, Jelena Prpić

Applied Sciences· Volume 14· Issue 11

Abstract

This study investigated the impact of tobacco exposure, specifically through heating and burning, on periodontopathogens in the subgingival microbiome among clinically healthy individuals and those diagnosed with periodontitis. The sample comprised 66 subjects (26–56 years, median 38 yrs; 64% females) classified as non-smokers, classic cigarette smokers, and tobacco heating system (THS) smokers (each N = 22). Full-mouth periodontal examination was performed, and 330 paper-point samples from periodontal pockets were collected. Next-generation sequencing of 16S rRNA genes was conducted to identify the composition of subgingival microbiome. Periodontitis prevalence among the groups was ranked as THS (41%) < non-smokers (44%) < cigarette smokers (68%), without statistically significant differences between the groups. The number of perio-pathogenic species was higher in subjects with periodontitis compared to those without (median 7 vs. 6 species; p = 0.005) but without significant differences between exposure groups: non-smokers (6) = smokers (6) < THS (6.5). When combining exposure and periodontal status, each smoker group had more perio-pathogenic species than non-smokers: non-smokers without periodontitis (5) < smokers without periodontitis (5.5) < THS without periodontitis (6); non-smokers with periodontitis (6.5) < THS with periodontitis (7) = smokers with periodontitis (7). Multiple linear regression indicated periodontitis as the sole predictor of perio-pathogenic species quantity, irrespective of the type of tobacco consumption, sex, age, or oral hygiene (R2 = 0.163; p = 0.005). In conclusion, the quantity of perio-pathogenic species in the subgingival microbiome was more influenced by periodontitis than by exposure to tobacco smoke, regardless of whether it was heated or burned.
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Research context

OpenAlex topics: Oral microbiology and periodontitis research · Oral Health Pathology and Treatment · Periodontal Regeneration and Treatments

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Clinical Hospital Centre Rijeka, Krešimirova 40, 51000 Rijeka, Croatia

Department of Periodontology, University of Rijeka, Faculty of Dental Medicine, Krešimirova 40/42, 51000 Rijeka, Croatia

Department of Dental Medicine, Josip Juraj Strossmayer University of Osijek, Faculty of Dental Medicine and Health, Crkvena 21, 31000 Osijek, Croatia

Department of Orthodontics, University of Rijeka, Faculty of Dental Medicine, Krešimirova 40/42, 51000 Rijeka, Croatia

Department of Microbiology and Parasitology, University of Rijeka, Faculty of Medicine, Braće Branchetta 20, 51000 Rijeka, Croatia

Funding

Croatian Science Foundation

References (59)

Show source-provided references
1. Periodontal diseases10.1016/S0140-6736(05)67728-8 ↗
2. The oral microbiome diversity and its relation to human diseases10.1007/s12223-014-0342-2 ↗
3. Sedghi, L.M., Bacino, M., and Kapila, Y.L. (2021). Periodontal disease: The good, the bad, and the unknown. Front. Cell. Infect. Microbiol., 11.10.3389/fcimb.2021.766944 ↗
4. The breadth of bacterial diversity in the human periodontal pocket and other oral sites10.1111/j.1600-0757.2006.00174.x ↗
5. The oral microbiome in health and disease10.1016/j.phrs.2012.11.006 ↗
6. Di Stefano, M., Polizzi, A., Santonocito, S., Romano, A., Lombardi, T., and Isola, G. (2022). Impact of oral microbiome in periodontal health and periodontitis: A critical review on prevention and treatment. Int. J. Mol. Sci., 23.10.3390/ijms23095142 ↗
7. Lindhe, J.A., Lang, N.P.B., and Karring, T.C. (2008). Textbook of Clinical Periodontology and Implant Dentistry, Wiley Blackwell. [5th ed.].
8. Beyond the red complex and into more complexity: The polymicrobial synergy and dysbiosis (PSD) model of periodontal disease etiology10.1111/j.2041-1014.2012.00663.x ↗
9. Microbial complexes in subgingival plaque10.1111/j.1600-051X.1998.tb02419.x ↗
10. Lindhe, J.A., Lang, N.P.B., and Karring, T.C. (2008). Textbook of Clinical Periodontology and Implant Dentistry, Wiley Blackwell. [5th ed.].
11. A new classification scheme for periodontal and peri-implant diseases and conditions—Introduction and key changes from the 1999 classification10.1111/jcpe.12935 ↗
12. An overview of iQOS® as a new heat-not-burn tobacco product and its potential effects on human health and the environment10.4274/tjps.galenos.2018.79095 ↗
13. World Health Organization (2020). Heated Tobacco Products (HTPs) Information Sheet, World Health Organization. Available online: https://www.who.int/publications/i/item/WHO-HEP-HPR-2020.2.
14. European Respiratory Society (2018). ERS Position Paper on Heated Tobacco Products, European Respiratory Society. Available online: https://www.ersnet.org/news-and-features/news/ers-position-paper-on-heated-tobacco-products/.
15. Adverse effects of electronic cigarettes on the disease-naive oral microbiome10.1126/sciadv.aaz0108 ↗
16. Chemical analysis and simulated pyrolysis of tobacco heating system 2.2 compared to conventional cigarettes10.1093/ntr/nty005 ↗
17. Heated tobacco products: The example of IQOS10.1136/tobaccocontrol-2018-054601 ↗
18. Assessment of tobacco heating product THP1.0. Part 8: Study to determine puffing topography, mouth level exposure and consumption among Japanese users10.1016/j.yrtph.2017.08.005 ↗
19. (2023, December 24). Phillip Morris Int., Stamford, Connecticut. About Us, Our Products. Available online: https://www.pmi.com/markets/croatia/hr/about-us/our-products.
20. Influence of smoking heating up tobacco products and e-cigarettes on the microbiota of dental plaque
21. Karasneh, J.A., Al Habashneh, R.A., Marzouka, N.A., and Thornhill, M.H. (2017). Effect of cigarette smoking on subgingival bacteria in healthy subjects and patients with chronic periodontitis. BMC Oral Health, 17.10.1186/s12903-017-0359-4 ↗
22. Subgingival microbial profiles of smokers with periodontitis10.1177/0022034510377203 ↗
23. Yu, G., Phillips, S., Gail, M.H., Goedert, J.J., Humphrys, M.S., Ravel, J., Ren, Y., and Caporaso, N.E. (2017). The effect of cigarette smoking on the oral and nasal microbiota. Microbiome, 5.10.1186/s40168-016-0226-6 ↗
24. The prevalence of pathogenic periodontal microflora in healthy young adult smokers10.1902/jop.2000.71.4.562 ↗
25. Kozak, M., and Pawlik, A. (2023). The role of the oral microbiome in the development of diseases. Int. J. Mol. Sci., 24.10.3390/ijms24065231 ↗
26. Periodontal disease and periodontal bacteria as triggers for rheumatoid arthritis10.1016/j.berh.2017.08.001 ↗
27. Visentin, D., Gobin, I., and Maglica, Ž. (2023). Periodontal pathogens and their links to neuroinflammation and neurodegeneration. Microorganisms, 11.10.3390/microorganisms11071832 ↗
28. Association of periodontal red complex bacteria with the incidence of gastrointestinal cancers: A systematic review and meta-Analysis
29. Pardo, A., Signoriello, A., Signoretto, C., Messina, E., Carelli, M., Tessari, M., De Manna, N.D., Rossetti, C., Albanese, M., and Lombardo, G. (2021). Detection of periodontal pathogens in oral samples and cardiac specimens in patients undergoing aortic valve replacement: A pilot study. J. Clin. Med., 10.10.3390/jcm10173874 ↗
30. Cigarette smoking reduction and health risks: A systematic review and meta-analysis10.1093/ntr/ntaa156 ↗
31. Larsson, S.C., and Burgess, S. (2022). Appraising the causal role of smoking in multiple diseases: A systematic review and meta-analysis of Mendelian randomization studies. EBioMedicine, 82.10.1016/j.ebiom.2022.104154 ↗
32. Smoking and microbiome in oral, airway, gut and some systemic diseases10.1186/s12967-019-1971-7 ↗
33. Aldakheel, F.M., Alduraywish, S.A., Jhugroo, P., Jhugroo, C., and Divakar, D.D. (2020). Quantification of pathogenic bacteria in the subgingival oral biofilm samples collected from cigarette-smokers, individuals using electronic nicotine delivery systems and non-smokers with and without periodontitis. Arch Oral Biol., 117.10.1016/j.archoralbio.2020.104793 ↗
34. Mišković, I., Kuiš, D., Špalj, S., Pupovac, A., and Prpić, J. (2024). Periodontal health status in adults exposed to tobacco heating system aerosol and cigarette smoke vs. non-smokers: A cross-sectional study. Dent. J., 12.10.3390/dj12020026 ↗
35. Ristrl, R. (2023, November 02). Sample Size Calculator Version 1.061. Available online: https://homepage.univie.ac.at/robin.ristl/samplesize.php.
36. Replacing PICO in non-interventional studies10.1136/bmjebm-2021-111889 ↗
37. Lindhe, J.A., Lang, N.P.B., and Karring, T.C. (2008). Textbook of Clinical Periodontology and Implant Dentistry, Wiley Blackwell. [5th ed.].
38. Implementation of the new classification of periodontal diseases: Decision-making algorithms for clinical practice and education10.1111/jcpe.13104 ↗
39. Bašić, K., Peroš, K., Bošnjak, Z., and Šutej, I. (2021). Subgingival microbiota profile in association with cigarette smoking in young adults: A cross-sectional study. Dent. J., 9.10.3390/dj9120150 ↗
40. Coming of age: Ten years of next-generation sequencing technologies10.1038/nrg.2016.49 ↗
41. Next-generation DNA sequencing10.1038/nbt1486 ↗
42. The application of next generation sequencing technology in medical diagnostics: A perspective
43. The road from next-generation sequencing to personalized medicine10.2217/pme.14.34 ↗
44. Proinflammatory cytokine levels and peri-implant parameters among cigarette smokers, individuals vaping electronic cigarettes, and non-smokers10.1002/JPER.18-0045 ↗
45. Subgingival microbiome in smokers and non-smokers in periodontitis: An exploratory study using traditional targeted techniques and a next-generation sequencing10.1111/jcpe.12087 ↗
46. Comparison of curet and paper point sampling of subgingival bacteria as analyzed by real-time polymerase chain reaction10.1902/jop.2007.060218 ↗
47. Evaluation of human and microbial DNA content in subgingival plaque samples collected by paper points or curette10.1016/j.mimet.2015.01.023 ↗
48. Association of red complex bacteria with periodontal disease: A clinico microbiological study
49. Abdulkareem, A.A., Al-Taweel, F.B., Al-Sharqi, A.J.B., Gul, S.S., Sha, A., and Chapple, I.L.C. (2023). Current concepts in the pathogenesis of periodontitis: From symbiosis to dysbiosis. J. Oral Microbiol., 15.10.1080/20002297.2023.2197779 ↗
50. Association between periodontal pathogens and severity of periodontal diseases among adolescents in Kunming City: China10.31584/jhsmr.20241029 ↗
51. Porphyromonas gingivalis, the most influential pathogen in red-complex bacteria: A cross-sectional study on the relationship between bacterial count and clinical periodontal status in Japan10.1002/JPER.21-0011 ↗
52. Persistence of Tannerella forsythia and Fusobacterium nucleatum in dental plaque: A strategic alliance10.1007/s40496-020-00254-6 ↗
53. Jiang, Y., Zhou, X., Cheng, L., and Li, M. (2020). The impact of smoking on subgingival microflora: From periodontal health to disease. Front. Microbiol., 11.10.3389/fmicb.2020.00066 ↗
54. Current understanding of periodontal disease pathogenesis and targets for host-modulation therapy10.1111/prd.12331 ↗
55. Do periodontopathogens disappear after full-mouth tooth extraction?10.1111/j.1600-051X.2009.01477.x ↗
56. Evaluation of red-complex bacteria loads in complete denture patients: A pilot study10.1038/s41405-023-00133-z ↗
57. Microbial dysbiosis in periodontitis10.4103/0972-124X.118334 ↗
58. The impact of smoking on subgingival plaque and the development of periodontitis: A literature review10.3389/froh.2021.751099 ↗
59. Smoking and periodontal microorganisms10.1016/j.jdsr.2019.03.002 ↗