Evaluation of Neutrophil Extracellular Trap Formation on Smokers and Non-Smokers with Periodontitis

Year 2024, Volume: 25 Issue: 2, 195 - 208, 31.08.2024

Gizem Yücesoy , Ebru Olgun , Kader Yıldız , Merve Başol Göksuluk

https://doi.org/10.69601/meandrosmdj.1536096

Abstract

Objevtive: In this study, we aimed to evaluate neutrophil extracellular trap (NET) in smoker and non-smoker periodontitis patients.
Materials and Methods: 21 subjects [non-smokers and periodontally healthy (S-P-) 7 people, non-smokers with periodontitis (S-P+) 7 people, smokers with periodontitis (S+P+) 7 people] were included in this study. Plaque index (PI), gingival index (GI), probing depth (PD) and clinical attachment level (CAL) parameters were recorded. The peripheral neutrophils isolated from the subjects were activated by phorbol 12-myristate 13-acetate (PMA) to induce NET formation. NET formed after the activation was measured with the fluorometer.
Results: In the S-P- group PI, GI, PD and CAL values were found statistically significantly low (P=0,001; P=<0,001; P=0,003; P=<0,001, respectively). When compared to S+P+ group PMN counts were found low, but this difference was statistically at the border (P=0,05). When compared NET count values, it was the highest in the S+P+ group. When S-P- group and S+P+ group were compared, this difference was statistically significant (P=0,003); but between S-P+ and S+P+ groups, the difference was not statistically significant (P>0.05). NET count with PI, GI, PD, there was mild positive; with CAL strong positive relation has been found.
Conclusion: As a result, even the S+P+ group NET count was found higher, the difference of S-P+ and S+P+ groups was not statistically significant. There is need more researches about smoking effect on NET formation in patients with periodontitis.

Keywords

Periodontitis, Smoking, Neutrophil Extracullular Trap

Ethical Statement

It has been decided that our study is in compliance with the ethical principles specified in Kırıkkale University Clinical Research Ethics Committee Directive (24.10.2017; 19/02).

Supporting Institution

BAPK

Project Number

BAPK 2018/065

References

• 1. Papapanou PN, Sanz M, Buduneli N, Dietrich T, Feres M, Fine DH, Flemmig TF, Garcia R, Giannobile WV, Graziani F, Greenwell H, Herrera D, Kao RT, Kebschull M, Kinane DF, Kirkwood KL, Kocher T, Kornman KS, Kumar PS, Loos BG, Machtei E, Meng H, Mombelli A, Needleman I, Offenbacher S, Seymour GJ, Teles R, Tonetti MS. Periodontitis: Consensus report of workgroup 2 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions. J Clin Periodontol. 2018 Jun;45 Suppl 20:S162-S170. doi: 10.1111/jcpe.12946. PMID: 29926490.
• 2. Hinrics JE, Kotsakis G. Classification of diseases and conditions affecting the periodontium. In: Newman M, Takei H, Klokkevold P, Carranza F, eds. Carranza’ s Clinical Periodontology, Chapter 3, 12th Edition, Elsevier Saunders, Missouri. 2015:45-67.
• 3. Buduneli N, Larsson L, Biyikoglu B, Renaud DE, Bagaitkar J, Scott DA. Fatty acid profiles in smokers with chronic periodontitis. J Dent Res. 2011 Jan;90(1):47-52. doi: 10.1177/0022034510380695. Epub 2010 Nov 1. PMID: 21041552; PMCID: PMC3144094.
• 4. Preshaw PM, Chambrone L, Novak KF. Smoking and periodonal disease. In: Newman M, Takei H, Klokkevold P, Carranza F, eds. Carranza’s Clinical Periodontology, Chapter 3, 12th Edition, Elseviers Saunders, Missouri. 2015:178-85.
• 5. Loos BG. Systemic markers of inflammation in periodontitis. J Periodontol. 2005 Nov;76(11 Suppl):2106-15. doi: 10.1902/jop.2005.76.11-S.2106. PMID: 16277583.
• 6. Kantarci A, Oyaizu K, Van Dyke TE. Neutrophil-mediated tissue injury in periodontal disease pathogenesis: findings from localized aggressive periodontitis. J Periodontol. 2003 Jan;74(1):66-75. doi: 10.1902/jop.2003.74.1.66. PMID: 12593599.
• 7. Landzberg M, Doering H, Aboodi GM, Tenenbaum HC, Glogauer M. Quantifying oral inflammatory load: oral neutrophil counts in periodontal health and disease. J Periodontal Res. 2015 Jun;50(3):330-6. doi: 10.1111/jre.12211. Epub 2014 Jul 14. PMID: 25040400.
• 8. Deas DE, Mackey SA, McDonnell HT. Systemic disease and periodontitis: manifestations of neutrophil dysfunction. Periodontol 2000. 2003;32:82-104. doi: 10.1046/j.0906-6713.2003.03207.x. PMID: 12756035.
• 9. Matthews JB, Wright HJ, Roberts A, Cooper PR, Chapple IL. Hyperactivity and reactivity of peripheral blood neutrophils in chronic periodontitis. Clin Exp Immunol. 2007 Feb;147(2):255-64. doi: 10.1111/j.1365-2249.2006.03276.x. PMID: 17223966; PMCID: PMC1810478.
• 10. Chapple IL, Matthews JB. The role of reactive oxygen and antioxidant species in periodontal tissue destruction. Periodontol 2000. 2007;43:160-232. doi: 10.1111/j.1600-0757.2006.00178.x. PMID: 17214840.
• 11. Scott DA, Krauss J. Neutrophils in periodontal inflammation. Front Oral Biol. 2012;15:56-83. doi: 10.1159/000329672. Epub 2011 Nov 11. PMID: 22142957; PMCID: PMC3335266.
• 12. Palmer RM, Wilson RF, Hasan AS, Scott DA. Mechanisms of action of environmental factors--tobacco smoking. J Clin Periodontol. 2005;32 Suppl 6:180-95. doi: 10.1111/j.1600-051X.2005.00786.x. PMID: 16128837.
• 13. Tsai CC, Chen HS, Chen SL, Ho YP, Ho KY, Wu YM, Hung CC. Lipid peroxidation: a possible role in the induction and progression of chronic periodontitis. J Periodontal Res. 2005 Oct;40(5):378-84. doi: 10.1111/j.1600-0765.2005.00818.x. PMID: 16105090.
• 14. Guentsch A, Preshaw PM, Bremer-Streck S, Klinger G, Glockmann E, Sigusch BW. Lipid peroxidation and antioxidant activity in saliva of periodontitis patients: effect of smoking and periodontal treatment. Clin Oral Investig. 2008 Dec;12(4):345-52. doi: 10.1007/s00784-008-0202-z. Epub 2008 May 29. PMID: 18509684.
• 15. Aziz AS, Kalekar MG, Suryakar AN, Benjamin T, Prakashan MJ, Ahmed BM, Sayyad M. Assessment of some biochemical oxidative stress markers in male smokers with chronic periodontitis. Indian J Clin Biochem. 2013 Oct;28(4):374-80. doi: 10.1007/s12291-012-0283-y. Epub 2013 Jan 10. PMID: 24426240; PMCID: PMC3783916.
• 16. Gustafsson A, Asman B, Bergström K. Cigarette smoking as an aggravating factor in inflammatory tissue-destructive diseases. Increase in tumor necrosis Factor-alpha priming of peripheral neutrophils measured as generation of oxygen radicals. Int J Clin Lab Res. 2000;30(4):187-90. doi: 10.1007/s005990070005. PMID: 11289709.
• 17. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y, Zychlinsky A. Neutrophil extracellular traps kill bacteria. Science. 2004 Mar 5;303(5663):1532-5. doi: 10.1126/science.1092385. PMID: 15001782.
• 18. White P, Sakellari D, Roberts H, Risafi I, Ling M, Cooper P, Milward M, Chapple I. Peripheral blood neutrophil extracellular trap production and degradation in chronic periodontitis. J Clin Periodontol. 2016 Dec;43(12):1041-1049. doi: 10.1111/jcpe.12628. Epub 2016 Oct 27. PMID: 27678376.
• 19. Delgado-Rizo V, Martínez-Guzmán MA, Iñiguez-Gutierrez L, García-Orozco A, Alvarado-Navarro A, Fafutis-Morris M. Neutrophil Extracellular Traps and Its Implications in Inflammation: An Overview. Front Immunol. 2017 Feb 6;8:81. doi: 10.3389/fimmu.2017.00081. PMID: 28220120; PMCID: PMC5292617.
• 20. Fuchs TA, Abed U, Goosmann C, Hurwitz R, Schulze I, Wahn V, Weinrauch Y, Brinkmann V, Zychlinsky A. Novel cell death program leads to neutrophil extracellular traps. J Cell Biol. 2007 Jan 15;176(2):231-41. doi: 10.1083/jcb.200606027. Epub 2007 Jan 8. PMID: 17210947; PMCID: PMC2063942.
• 21. Wang Y, Li M, Stadler S, Correll S, Li P, Wang D, Hayama R, Leonelli L, Han H, Grigoryev SA, Allis CD, Coonrod SA. Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation. J Cell Biol. 2009 Jan 26;184(2):205-13. doi: 10.1083/jcb.200806072. Epub 2009 Jan 19. PMID: 19153223; PMCID: PMC2654299.
• 22. White PC, Chicca IJ, Cooper PR, Milward MR, Chapple IL. Neutrophil Extracellular Traps in Periodontitis: A Web of Intrigue. J Dent Res. 2016 Jan;95(1):26-34. doi: 10.1177/0022034515609097. Epub 2015 Oct 6. PMID: 26442948.
• 23. Remijsen Q, Kuijpers TW, Wirawan E, Lippens S, Vandenabeele P, Vanden Berghe T. Dying for a cause: NETosis, mechanisms behind an antimicrobial cell death modality. Cell Death Differ. 2011 Apr;18(4):581-8. doi: 10.1038/cdd.2011.1. Epub 2011 Feb 4. PMID: 21293492; PMCID: PMC3131909.
• 24. Cooper PR, Palmer LJ, Chapple IL. Neutrophil extracellular traps as a new paradigm in innate immunity: friend or foe? Periodontol 2000. 2013 Oct;63(1):165-97. doi: 10.1111/prd.12025. PMID: 23931060.
• 25. Feldman C, Anderson R. Cigarette smoking and mechanisms of susceptibility to infections of the respiratory tract and other organ systems. J Infect. 2013 Sep;67(3):169-84. doi: 10.1016/j.jinf.2013.05.004. Epub 2013 May 21. PMID: 23707875.
• 26. Hosseinzadeh A, Thompson PR, Segal BH, Urban CF. Nicotine induces neutrophil extracellular traps. J Leukoc Biol. 2016 Nov;100(5):1105-1112. doi: 10.1189/jlb.3AB0815-379RR. Epub 2016 Jun 16. PMID: 27312847; PMCID: PMC5069087.
• 27. Vitkov L, Klappacher M, Hannig M, Krautgartner WD. Extracellular neutrophil traps in periodontitis. J Periodontal Res. 2009 Oct;44(5):664-72. doi: 10.1111/j.1600-0765.2008.01175.x. Epub 2009 May 18. PMID: 19453857.
• 28. Kolaparthy LK, Sanivarapu S, Swarna C, Devulapalli NS. Neutrophil extracellular traps: Their role in periodontal disease. J Indian Soc Periodontol. 2014 Nov-Dec;18(6):693-7. doi: 10.4103/0972-124X.147399. Retraction in: J Indian Soc Periodontol. 2015 Mar-Apr;19(2):128. doi: 10.4103/0972-124X.154336. PMID: 25624623; PMCID: PMC4296451.
• 29. Hirschfeld J, Dommisch H, Skora P, Horvath G, Latz E, Hoerauf A, Waller T, Kawai T, Jepsen S, Deschner J, Bekeredjian-Ding I. Neutrophil extracellular trap formation in supragingival biofilms. Int J Med Microbiol. 2015 Jun-Aug;305(4-5):453-63. doi: 10.1016/j.ijmm.2015.04.002. Epub 2015 Apr 20. PMID: 25959370.
• 30. Sursal N, Yildiz K. NETosis in different aspects (in Turkish). Turk Hij Den Biyol Derg. 2018;74:351-60.
• 31. Baelum V, Luan WM, Chen X, Fejerskov O. A 10-year study of the progression of destructive periodontal disease in adult and elderly Chinese. J Periodontol. 1997 Nov;68(11):1033-42. doi: 10.1902/jop.1997.68.11.1033. PMID: 9407395.
• 32. Baelum V, Luan WM, Chen X, Fejerskov O. Predictors of destructive periodontal disease incidence and progression in adult and elderly Chinese. Community Dent Oral Epidemiol. 1997 Aug;25(4):265-72. doi: 10.1111/j.1600-0528.1997.tb00938.x. PMID: 9332802.
• 33. Beck JD, Sharp T, Koch GG, Offenbacher S. A 5-year study of attachment loss and tooth loss in community-dwelling older adults. J Periodontal Res. 1997 Aug;32(6):516-23. doi: 10.1111/j.1600-0765.1997.tb00567.x. PMID: 9379319.
• 34. Haber J. Smoking is a major risk factor for periodontitis. Curr Opin Periodontol. 1994:12-8. PMID: 8032453.
• 35. Mullally BH. The influence of tobacco smoking on the onset of periodontitis in young persons. Tob Induc Dis. 2004 Jun 15;2(2):53-65. doi: 10.1186/1617-9625-2-2-53. PMID: 19570272; PMCID: PMC2671536.
• 36. Albandar JM, Streckfus CF, Adesanya MR, Winn DM. Cigar, pipe, and cigarette smoking as risk factors for periodontal disease and tooth loss. J Periodontol. 2000 Dec;71(12):1874-81. doi: 10.1902/jop.2000.71.12.1874. PMID: 11156044.
• 37. Luzzi LI, Greghi SL, Passanezi E, Sant'ana AC, Lauris JR, Cestari TM. Evaluation of clinical periodontal conditions in smokers and non-smokers. J Appl Oral Sci. 2007 Dec;15(6):512-7. doi: 10.1590/s1678-77572007000600011. PMID: 19089190; PMCID: PMC4327501.
• 38. Kweider M, Lowe GD, Murray GD, Kinane DF, McGowan DA. Dental disease, fibrinogen and white cell count; links with myocardial infarction? Scott Med J. 1993 Jun;38(3):73-4. doi: 10.1177/003693309303800304. PMID: 8356427.
• 39. Smith MR, Kinmonth AL, Luben RN, Bingham S, Day NE, Wareham NJ, Welch A, Khaw KT. Smoking status and differential white cell count in men and women in the EPIC-Norfolk population. Atherosclerosis. 2003 Aug;169(2):331-7. doi: 10.1016/s0021-9150(03)00200-4. PMID: 12921986.
• 40. Higuchi T, Omata F, Tsuchihashi K, Higashioka K, Koyamada R, Okada S. Current cigarette smoking is a reversible cause of elevated white blood cell count: Cross-sectional and longitudinal studies. Prev Med Rep. 2016 Aug 9;4:417-22. doi: 10.1016/j.pmedr.2016.08.009. PMID: 27583199; PMCID: PMC4995538.
• 41. Karlsson A, Nixon JB, McPhail LC. Phorbol myristate acetate induces neutrophil NADPH-oxidase activity by two separate signal transduction pathways: dependent or independent of phosphatidylinositol 3-kinase. J Leukoc Biol. 2000 Mar;67(3):396-404. doi: 10.1002/jlb.67.3.396. PMID: 10733101.
• 42. Rheu GB, Ji S, Ryu JJ, Lee JB, Shin C, Lee JY, Huh JB, Shin SW. Risk assessment for clinical attachment loss of periodontal tissue in Korean adults. J Adv Prosthodont. 2011 Mar;3(1):25-32. doi: 10.4047/jap.2011.3.1.25. Epub 2011 Mar 31. PMID: 21503190; PMCID: PMC3076570.
• 43. Palmer LJ, Chapple IL, Wright HJ, Roberts A, Cooper PR. Extracellular deoxyribonuclease production by periodontal bacteria. J Periodontal Res. 2012 Aug;47(4):439-45. doi: 10.1111/j.1600-0765.2011.01451.x. Epub 2011 Dec 12. PMID: 22150619.
• 44. Gillespie MN, Owasoyo JO, Kojima S, Jay M. Enhanced chemotaxis and superoxide anion production by polymorphonuclear leukocytes from nicotine-treated and smoke-exposed rats. Toxicology. 1987 Jul;45(1):45-52. doi: 10.1016/0300-483x(87)90113-2. PMID: 3037731.
• 45. Qiu SL, Zhang H, Tang QY, Bai J, He ZY, Zhang JQ, Li MH, Deng JM, Liu GN, Zhong XN. Neutrophil extracellular traps induced by cigarette smoke activate plasmacytoid dendritic cells. Thorax. 2017 Dec;72(12):1084-1093. doi: 10.1136/thoraxjnl-2016-209887. Epub 2017 Jul 18. PMID: 28720648.
• 46. Nguyen H, Finkelstein E, Reznick A, Cross C, van der Vliet A. Cigarette smoke impairs neutrophil respiratory burst activation by aldehyde-induced thiol modifications. Toxicology. 2001 Mar 7;160(1-3):207-17. doi: 10.1016/s0300-483x(00)00450-9. PMID: 11246141.
• 47. Zappacosta B, Persichilli S, Minucci A, Stasio ED, Carlino P, Pagliari G, Giardina B, Sole PD. Effect of aqueous cigarette smoke extract on the chemiluminescence kinetics of polymorphonuclear leukocytes and on their glycolytic and phagocytic activity. Luminescence. 2001 Sep-Oct;16(5):315-9. doi: 10.1002/bio.661. PMID: 11590703.
• 48. White PC, Hirschfeld J, Milward MR, Cooper PR, Wright HJ, Matthews JB, Chapple ILC. Cigarette smoke modifies neutrophil chemotaxis, neutrophil extracellular trap formation and inflammatory response-related gene expression. J Periodontal Res. 2018 Aug;53(4):525-535. doi: 10.1111/jre.12542. Epub 2018 Mar 25. PMID: 29574730.
• 49. Rajendran V, Uppoor A. A perspective on NETosis in diabetes and periodontal diseases. J Indian Soc Periodontol. 2018 Jul-Aug;22(4):290-293. doi: 10.4103/jisp.jisp_230_18. PMID: 30131618; PMCID: PMC6077958.