The effect of smoking on inflammatory cell infiltrate subtypes in gingival tissue of patients with chronic periodontitis
Keywords:
Chronic periodontitis, cigarette smoking, immune markersAbstract
Background: Examinations on blood samples and gingival crevicular fluid of subjects with chronic periodontitis showed that smoking increased production of cytokines.
Objective: To evaluate the expression of immune markers on mononuclear inflammatory cell infiltrate at periodontitis and healthy tissue among smoking and non-smoking subjects.
Methods: This case-control study was performed on 41 patients who referred to a clinic of periodontology at a Mashhad dental school in Iran in 2016. The participants were all of Iranian Khorasanian ethnicity with age range of 35-65 years. Gingival biopsies were obtained during routine periodontal flap procedure. Immunohistochemistry using markers of CD20, CD3, CD68, and CD45RO was carried out. Data was analyzed by SPSS version 15, using one-way ANOVA and Tukey HSD test.
Results: Nonsmoker subjects showed significantly greater numbers of CD20+, CD68+, CD3+ cells compared to smoker subjects, both at healthy and periodontitis tissue biopsies (p<0.00), whereas there was no significant difference in terms of CD45RO (p=0.120).
Conclusion: Cigarette smoking, results in infiltrative mononuclear chronic inflammatory cells reduction in connective periodontium.
References
Dahiya, P, Kamal R, Gupta R, Bhardwaj R, Chaudhary K, Kaur S. Reactive oxygen species in
periodontitis. J Indian Soc Periodontol. 2013; 17(4): 411-6. doi: 10.4103/0972-124x.118306. PMID:
, PMCID: PMC3800399.
Matthews JB, Chen FM, Milward MR, Wright HJ, Carter K, McDonagh A, et al. Effect of nicotine,
cotinine and cigarette smoke extract on the neutrophil respiratory burst. J Clin Periodontol. 2011; 38(3):
-18. doi: 10.1111/j.1600-051X.2010.01676.x. PMID: 21214612.
Darveau RP. Periodontitis: a polymicrobial disruption of host homeostasis. Nat Rev Microbiol. 2010; 8(7):
-90. doi: 10.1038/nrmicro2337. PMID: 20514045.
Munz M, Chen H, Jockel-Schneider Y, Adam K, Hoffman P, Berger KA ,et all. A haplotype block
downstream of plasminogen is associated with chronic and aggressive periodontitis. J Clin Periodontol.
doi: 10.1111/jcpe.12749. PMID: 28548211.
Bascones-Martinez A, Matesanz-Perez P, Escribano-Bermejo M, González-Moles MÁ, Bascones-Ilundain
J, Meurman JH. Periodontal disease and diabetes-Review of the literature. Med Oral Patol Oral Cir Bucal.
; 16(6): e722-9. doi: 10.4317/medoral.17032. PMID: 21196866.
Hernandez M, Dutzan N, Garcia-Sesnich J, Abusleme L, Dezerega A, Silva N, et al. Host-pathogen
interactions in progressive chronic periodontitis. J Dent Res. 2011; 90(10): 1164-70. doi:
1177/0022034511401405. PMID: 21471325.
Katuri KK, Alluri JK, Chintagunta C, Tadiboina N, Borugadda R, Loya M, et all. Assessment of
Periodontal Health Status in Smokers and Smokeless Tobacco Users: A Cross-Sectional Study. J Clin
Diagn Res. 2016; 10(10): ZC143-ZC146. doi: 10.7860/JCDR/2016/22160.8700. PMID: 27891477,
PMCID: PMC5121795.
Díaz-Faes L, Guerrero A, Magán-Fernández A, Bravo M, Mesa F. Tooth loss and alveolar bone crest loss
during supportive periodontal therapy in patients with generalized aggressive periodontitis: retrospective
study with follow-up of 8 to 15 years. J Clin Periodontol. 2016; 43(12): 1109-15. doi: 10.1111/jcpe.12596.
PMID: 27396322.
Yadalam PK, Rajapandian K, Ravishankar PL, Vartharajan K, Subramaniam S, Dinakar M. Evaluation of
anticardiolipin antibodies in tobacco users and non-tobacco users with severe chronic periodontal disease. J
Int Soc Prev Community Dent. 2016; 6(3): 256-60. doi: 10.4103/2231-0762.183115. PMID: 27382544.
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. doi:
1371/journal.pone.0027386. PMID: 22110637, PMCID: PMC3215692.
He CY, Gao XQ, Jiang LP. The impact of smoking on levels of chronic periodontitis-associated
biomarkers. Exp Mol Pathol. 2016; 101(1): 110-5. doi: 10.1016/j.yexmp.2016.07.004. PMID: 27450647.
Kinane DF, Chestnutt IG. Smoking and periodontal disease. Crit Rev Oral Biol Med. 2000; 11(3): 356-65.
doi: 10.1177/10454411000110030501. PMID: 11021635.
Moon JH, Lee JH, Lee JY. Subgingival microbiome in smokers and non-smokers in Korean chronic
periodontitis patients. Mol Oral Microbiol. 2015; 30(3): 227-41. doi: 10.1111/omi.12086. doi:
1111/omi.12086. PMID: 25283067.
Takeuchi H, Kubota S, Murakashi E, Zhou Y, Endo K, Ng PS, et al. Nicotine-induced CCN2: from
smoking to periodontal fibrosis. J Dent Res. 2010; (89): 34-9. doi: 10.1177/0022034509353403. PMID:
Carinci F, Palmieri A, Girardi A, Cura F, Scapoli L, Lauritano D. Genetic risk assessment of periodontal
disease in healthy patients. Journal of Forensic Research. 2015; 6, no 260. doi: 10.4172/2157- 7145.1000260.
Navarrete M, García J, Dutzan N, Henríquez L, Puente J, Carvajal P, et al. Interferon-γ, interleukins-6 and - 4, and factor XIII-A as indirect markers of the classical and alternative macrophage activation pathways in
chronic periodontitis. J Periodontol. 2014; 85(5): 751-60. doi: 10.1902/jop.2013.130078. PMID: 24070400.
Ribeiro FV, Pino DS, Franck FC, Benatti BB, Tenenbaum H, Perio D, et al. Resveratrol Inhibits
Periodontitis-Related Bone Loss in Rats Submitted to Cigarette Smoke Inhalation. J Periodontol. 2017: 1- 16. doi: 10.1902/jop.2017.170025. PMID: 28492360.
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. doi:
1111/jcpe.12300. PMID: 25139209.
Toker H, Akpinar A, Aydin H, Poyraz O. Influence of smoking on interleukin-1beta level, oxidant status
and antioxidant status in gingival crevicular fluid from chronic periodontitis patients before and after
periodontal treatment. J Periodontal Res. 2012; 47(5): 572-7. doi: 10.1111/j.1600-0765.2012.01468.x.
PMID: 22364664.
Souto GR, Segundo TK, Costa FO, Aguiar MCF, Mesquita RA. Effect of smoking on Langerhans and
dendritic cells in patients with chronic gingivitis. J Periodontol. 2011; 82(4): 619-25. doi:
1902/jop.2010.100488. PMID: 21054228.
Kotsakis GA, Javed F, Hinrichs JE, Karoussis IK, Romanos GE. Impact of cigarette smoking on clinical
outcomes of periodontal flap surgical procedures: a systematic review and meta-analysis. Periodontol.
; 86(2): 254-63. doi: 10.1902/jop.2014.140452. PMID: 25299388.
Angaji M, Gelskey S, Nogueira-Filho G, Brothwell D. A systematic review of clinical efficacy of
adjunctive antibiotics in the treatment of smokers with periodontitis. J Periodontol. 2010; 81(11): 1518-28.
doi: 10.1902/jop.2010.100192. PMID: 20583918.
de Heens GL, Kikkert R, Aarden LA, van der Velden U, Loos BG. Effects of smoking on the ex vivo
cytokine production in periodontitis. J Periodontal Res. 2009; 44(1): 28-34. doi: 10.1111/j.1600- 0765.2007.01047.x. PMID: 18973517.
Goutoudi P, Diza E, Arvanitidou M. Effect of periodontal therapy on crevicular fluid interleukin-6 and
interleukin-8 levels in chronic periodontitis. Int J Dent. 2012; 2012: 362905. doi: 10.1155/2012/362905.
PMID: 22114600, PMCID: PMC3205686.
Fatemi K, Radvar M, Rezaee A, Rafatpanah H, Azangoo khiavi H, Dadpour Y, et al. Comparison of
relative TLR-2 and TLR-4 expression level of disease and healthy gingival tissue of smoking and non-
smoking patients and periodontally healthy control patients. Aust Dent J. 2013; 58(3): 315-20. doi:
1111/adj.12089. PMID: 23981212.
Ardais R, Mário Tde G, Boligon J, Kantorski KZ, Moreira CH. The effect of smoking on bleeding on
probing after nonsurgical periodontal therapy: a quasi-experimental study. Braz Oral Res. 2014; 28: 1-7.
doi: 10.1590/1807-3107BOR-2014.vol28.0058. PMID: 25337935.
Javed F, Al-Kheraif AA, Al Amri MD, Alshehri M, Vohra F, Al-Askar M, et al. Periodontal Status and
Whole Salivary Cytokine Profile Among Smokers and Never-Smokers With and Without Prediabetes. J
Periodontol. 2015; 86(7): 890-8. doi: 10.1902/jop.2015.140593. PMID: 25672658.
Mavropoulos A, Brodin P, Rösing CK, Aass AM, Aars H. Gingival blood flow in periodontitis patients
before and after periodontal surgery assessed in smokers and non-smokers. J Periodontol. 2007; 78(9):
-82. doi: 10.1902/jop.2007.060472. PMID: 17760548.
Bunaes DF, Mustafa M, Mohamed HG, Lie SA, Leknes KN. The effect of smoking on inflammatory and
bone remodeling markers in gingival crevicular fluid and subgingival microbiota following periodontal
therapy. J Periodontal Res. 2017. doi: 10.1111/jre.12438. PMID: 28306142.
Nociti FH Jr, Casati MZ, Duarte PM. Current perspective of the impact of smoking on the progression and
treatment of periodontitis. Periodontology 2000. 2015; 67(1): 187-210. doi: 10.1111/prd.12063. PMID:
Duarte PM, Santos VR, Dos Santos FA, de Lima Pereira SA, Rodrigues DB, Napimoga MH. Role of
smoking and type 2 diabetes in the immunobalance of advanced chronic periodontitis. J Periodontol. 2011;
(3): 429-38. doi: 10.1902/jop.2010.100215. PMID: 20731586.
Park KS, Lee Y. Lymphocyte Apoptosis in Smokers and Non-Smokers Following Different Intensity of
Exercises and Relation with Lactate. Int J Exerc Sci. 2011; 4(3): 204-16. PMID: 27182363, PMCID:
PMC4738908.
Haytural O, Yaman D, Ural EC, Kantarci A, Demirel K. Impact of periodontitis on chemokines in
smokers. Clin Oral Investig. 2015; 19(5): 979-86. doi: 10.1007/s00784-014-1314-2. PMID: 25193410.
Al-Bayaty FH, Baharuddin N, Abdulla MA, Ali HM, Arkilla MB, ALBayaty MF. The influence of
cigarette smoking on gingival bleeding and serum concentrations of haptoglobin and alpha 1-antitrypsin.
Biomed Res Int. 2013; 2013: 684154. doi: 10.1155/2013/684154. PMID: 24286083, PMCID:
PMC3830826.
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