GCF Levels of Osteoclastogenesis-Related Cytokines in Periodontitis in Relation to Smoking During Non-Surgical Periodontal Therapy

Nilüfer Erenler; Emine Pirim Görgün

doi:10.19127/mbsjohs.1239668

Research Article

GCF Levels of Osteoclastogenesis-Related Cytokines in Periodontitis in Relation to Smoking During Non-Surgical Periodontal Therapy

Year 2023, Volume: 9 Issue: 1, 154 - 168, 28.02.2023

Nilüfer Erenler Emine Pirim Görgün

https://doi.org/10.19127/mbsjohs.1239668

Abstract

Objective: Interleukins (IL) -1β, -34, receptor activator of nuclear factor-kB ligand (RANKL), and osteoprotegerin (OPG) play a crucial role in osteoclastogenesis and bone resorption through modulating inflammatory processes and osteoclastogenesis. Smoking is the major risk factor in the initiation and progression of the periodontitis, and adversely affects the outcomes of non-surgical periodontal therapy. To date, there is no study investigating both gingival crevicular fluid (GCF) IL-1β, IL-34, RANKL, and OPG levels before and after non-surgical periodontal therapy in smoking and non-smoking patients with periodontitis stage 3, grade B and C. The aim of current research was to examine the GCF levels of some osteoclastogenesis-related cytokines in periodontitis in relation to smoking before and after periodontal therapy.

Methods: At baseline, full-mouth periodontal status together with GCF samples were collected from 116 individuals, including 60 periodontitis patients (30 smokers and 30 nonsmokers) and 56 periodontally healthy controls (28 smokers and 28 nonsmokers). Non-surgical periodontal therapy, consisting of instruction for daily plaque control and scaling and root planing (SRP), was performed. GCF sampling and full-mouth periodontal measurements were repeated 6 weeks after completion of SRP. The GCF levels of biomarkers were measured by enzyme-linked immunosorbent assay.

Results: The periodontitis groups exhibited significant improvement in clinical parameters. At baseline, the GCF IL-1β levels in periodontitis groups were significantly higher than periodontally healthy controls (p<0.05) and it was significantly decreased in periodontitis groups after non-surgical periodontal therapy. At baseline, the GCF IL-34 levels in periodontitis groups were significantly higher than periodontal healthy controls(p<0.05) and the GCF IL-34 level was significantly decreased in non-smoking periodontitis patients. At baseline and after periodontal therapy, the GCF RANKL levels were similar in all groups. The GCF OPG level was significantly lowest in non-smoking periodontitis patients at baseline and the GCF OPG level was significantly increased in smoking and non-smoking periodontitis patients after non-surgical periodontal therapy.

Conclusion: In the periodontal inflammation process, GCF IL-34 level followed a similar pathway to GCF IL-1β, suggesting that IL-34 may be a marker in the pathogenesis of periodontal disease. The significant decrease in GCF IL-34 and a significant increase in GCF OPG level in the non-smoker periodontitis group after periodontal therapy suggest the negative effect of smoking on the response to periodontal therapy. More comprehensive studies are needed by increasing the number of samples included in the study groups in order to better understand the pathogenesis of periodontitis.

Keywords

periodontitis, cytokine, non-surgical periodontal therapy, smoking

Supporting Institution

sivas cumhuriyet university

Project Number

diş 224

Thanks

we thank very much to Ömer Poyraz for elisa analysis

References

1. Chapple I, Brock G, Milward M, Ling N, Matthews J. Compromised GCF total antioxidant capacity in periodontitis: cause or effect? Journal of clinical periodontology. 2007;34(2):103-10.
2. Vettore MV, Leao AT, Monteiro Da Silva AM, Quintanilha RS, Lamarca GA. The relationship of stress and anxiety with chronic periodontitis. Journal of clinical periodontology. 2003 May;30(5):394-402.
3. Amarasena N, Ekanayaka AN, Herath L, Miyazaki H. Tobacco use and oral hygiene as risk indicators for periodontitis. Community dentistry and oral epidemiology. 2002 Apr;30(2):115-23. PubMed
4. Amarasekara DS, Yun H, Kim S, Lee N, Kim H, Rho J. Regulation of osteoclast differentiation by cytokine networks. Immune network. 2018;18(1).
5. C NG, A RP. Influence of Smoking on Interleukin-34 Levels in Gingival Crevicular Fluid and Plasma in Periodontal Health and Disease: A Clinico-biochemical Study. The Bulletin of Tokyo Dental College. 2018 Nov 30;59(4):247-55.
6. Guruprasad CN, Pradeep AR. Effect of nonsurgical periodontal therapy on interleukin-34 levels in periodontal health and disease. Indian journal of dental research: official publication of Indian Society for Dental Research. 2018 May-Jun;29(3):280-5.
7. Belibasakis GN, Bostanci N. The RANKL-OPG system in clinical periodontology. Journal of clinical periodontology. 2012 Mar;39(3):239-48. PubMed
8. Bostanci N, İlgenli T, Emingil G, Afacan B, Han B, Töz H, et al. Gingival crevicular fluid levels of RANKL and OPG in periodontal diseases: implications of their relative ratio. Journal of clinical periodontology. 2007;34(5):370-6.
9. Buduneli N, Bıyıkoğlu B, Sherrabeh S, Lappin DF. Saliva concentrations of RANKL and osteoprotegerin in smoker versus non‐smoker chronic periodontitis patients. Journal of clinical periodontology. 2008;35(10):846-52.
10. Loe H. The Gingival Index, the Plaque Index, and the Retention Index Systems. J Periodontol. 1967 Nov-Dec;38(6):Suppl:610-6.
11. Newman MG, Takei H, Klokkevold PR, Carranza FA. Carranza's clinical periodontology: Elsevier health sciences; 2011.
12. Salvi GE, Lawrence HP, Offenbacher S, Beck JD. Influence of risk factors on the pathogenesis of periodontitis. Periodontology 2000. 1997;14(1):173-201.
13. Moreira P, Lima P, Sathler K, Imanishi S, Costa J, Gomez R, et al. Interleukin‐6 expression and gene polymorphism are associated with severity of periodontal disease in a sample of Brazilian individuals. Clinical & Experimental Immunology. 2007;148(1):119-26.
14. Griffiths GS. Formation, collection, and significance of gingival crevice fluid. Periodontology 2000. 2003;31(1):32-42.
15. Gamonal J, Acevedo A, Bascones A, Jorge O, Silva A. Levels of interleukin‐1β,‐8, and‐10 and RANTES in gingival crevicular fluid and cell populations in adult periodontitis patients and the effect of periodontal treatment. Journal of Periodontology. 2000;71(10):1535-45.
16. Tomar SL, Asma S. Smoking‐attributable periodontitis in the United States: findings from NHANES III. Journal of Periodontology. 2000;71(5):743-51.
17. Chatrchaiwiwatana S, Ratanasiri A. Periodontitis associated with tobacco smoking among rural Khon Kaen Thai males: analysis of two data sets. Journal of the Medical Association of Thailand. 2011;92(11):1524.
18. Vouros ID, Kalpidis C, Chadjipantelis T, Konstantinidis AB. Cigarette smoking associated with advanced periodontal destruction in a Greek sample population of patients with periodontal disease. Journal of the International Academy of Periodontology. 2009;11(4):250-7.
19. Apatzidou D, Riggio M, Kinane D. Impact of smoking on the clinical, microbiological and immunological parameters of adult patients with periodontitis. Journal of clinical periodontology. 2005;32(9):973-83.
20. Gomes SC, Piccinin FB, Oppermann RV, Susin C, Marcantonio R. The effect of smoking on gingival crevicular fluid volume during the treatment of gingivitis. Acta odontologica latinoamericana: AOL. 2009;22(3):201-6.
21. Javed F, Abduljabbar T, Vohra F, Malmstrom H, Rahman I, Romanos GE. Comparison of periodontal parameters and self‐perceived oral symptoms among cigarette smokers, individuals vaping electronic cigarettes, and never‐smokers. Journal of periodontology. 2017;88(10):1059-65.
22. Oh H, Hirano J, Takai H, Ogata Y. Effects of initial periodontal therapy on interleukin-1β level in gingival crevicular fluid and clinical periodontal parameters. J Oral Sci. 2015 Jun;57(2):67-71.
23. Orozco A, Gemmell E, Bickel M, Seymour GJ. Interleukin-1beta, interleukin-12 and interleukin-18 levels in gingival fluid and serum of patients with gingivitis and periodontitis. Oral microbiology and immunology. 2006 Aug;21(4):256-60.
24. Rawlinson A, Grummitt JM, Walsh TF, Ian Douglas C. Interleukin 1 and receptor antagonist levels in gingival crevicular fluid in heavy smokers versus non‐smokers. Journal of clinical periodontology. 2003;30(1):42-8.
25. Tymkiw KD, Thunell DH, Johnson GK, Joly S, Burnell KK, Cavanaugh JE, et al. Influence of smoking on gingival crevicular fluid cytokines in severe chronic periodontitis. Journal of clinical periodontology. 2011;38(3):219-28.
26. Stashenko P, Dewhirst FE, Rooney ML, Desjardins LA, Heeley JD. Interleukin‐1β is a potent inhibitor of bone formation in vitro. Journal of Bone and Mineral Research. 1987;2(6):559-65.
27. Toker H, Poyraz O, Eren K. Effect of periodontal treatment on IL‐1β, IL‐1ra, and IL‐10 levels in gingival crevicular fluid in patients with aggressive periodontitis. Journal of clinical periodontology. 2008;35(6):507-13.
28. Boström EA, Lundberg P. The newly discovered cytokine IL-34 is expressed in gingival fibroblasts, shows enhanced expression by pro-inflammatory cytokines, and stimulates osteoclast differentiation. PloS one. 2013;8(12):e81665.
29. Guruprasad C, Pradeep A. Interleukin‐34 levels in gingival crevicular fluid and plasma in periodontal health and disease with and without type‐2 diabetes mellitus. Journal of investigative and clinical dentistry. 2018;9(2):e12317.
30. Clavel G, Thiolat A, Boissier MC. Interleukin newcomers creating new numbers in rheumatology: IL-34 to IL-38. Joint bone spine. 2013 Oct;80(5):449-53.
31. Gorgun EP, Toker H. Value of Gingival Crevicular Fluid Levels of Biomarkers IL-1 β, IL-22 and IL-34 for the Prediction of Severity of Periodontal Diseases and Outcome of Non-Surgical Periodontal Treatment. Int J Acad Med Pharm. 2022;4(1):24-30.
32. Luo Q, Gu X-H. [Expression of cytokines Il-6, IL-34 and M-CSFR in chronic periodontitis and its clinical significance]. Shanghai Kou Qiang Yi Xue. 2018 2018/12//;27(6):652-6.
33. Guruprasad CN, Pradeep AR. Interleukin-34 Levels in Gingival Crevicular Fluid and Plasma in Healthy and Diseased Periodontal Tissue in Presence or Absence of Obesity: A Clinico-biochemical Study. The Bulletin of Tokyo Dental College. 2018;59(2):79-86.
34. Kong YY, Yoshida H, Sarosi I, Tan HL, Timms E, Capparelli C, et al. OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature. 1999 Jan 28;397(6717):315-23.
35. Crotti T, Smith MD, Hirsch R, Soukoulis S, Weedon H, Capone M, et al. Receptor activator NF κB ligand (RANKL) and osteoprotegerin (OPG) protein expression in periodontitis. Journal of periodontal research. 2003;38(4):380-7.
36. Mogi M, Otogoto J, Ota N, Togari A. Differential expression of RANKL and osteoprotegerin in gingival crevicular fluid of patients with periodontitis. Journal of dental research. 2004;83(2):166-9.
37. Wara‐aswapati N, Surarit R, Chayasadom A, Boch JA, Pitiphat W. RANKL upregulation associated with periodontitis and Porphyromonas gingivalis. Journal of periodontology. 2007;78(6):1062-9.
38. Buduneli N, Buduneli E, Kütükçüler N. Interleukin-17, RANKL, and osteoprotegerin levels in gingival crevicular fluid from smoking and non-smoking patients with chronic periodontitis during initial periodontal treatment. Journal of periodontology. 2009 Aug;80(8):1274-80.

Year 2023, Volume: 9 Issue: 1, 154 - 168, 28.02.2023

Nilüfer Erenler Emine Pirim Görgün

https://doi.org/10.19127/mbsjohs.1239668

Abstract

Keywords

periodontitis, cytokine, non-surgical periodontal therapy, smoking

Project Number

diş 224

References

1. Chapple I, Brock G, Milward M, Ling N, Matthews J. Compromised GCF total antioxidant capacity in periodontitis: cause or effect? Journal of clinical periodontology. 2007;34(2):103-10.
2. Vettore MV, Leao AT, Monteiro Da Silva AM, Quintanilha RS, Lamarca GA. The relationship of stress and anxiety with chronic periodontitis. Journal of clinical periodontology. 2003 May;30(5):394-402.
3. Amarasena N, Ekanayaka AN, Herath L, Miyazaki H. Tobacco use and oral hygiene as risk indicators for periodontitis. Community dentistry and oral epidemiology. 2002 Apr;30(2):115-23. PubMed
4. Amarasekara DS, Yun H, Kim S, Lee N, Kim H, Rho J. Regulation of osteoclast differentiation by cytokine networks. Immune network. 2018;18(1).
5. C NG, A RP. Influence of Smoking on Interleukin-34 Levels in Gingival Crevicular Fluid and Plasma in Periodontal Health and Disease: A Clinico-biochemical Study. The Bulletin of Tokyo Dental College. 2018 Nov 30;59(4):247-55.
6. Guruprasad CN, Pradeep AR. Effect of nonsurgical periodontal therapy on interleukin-34 levels in periodontal health and disease. Indian journal of dental research: official publication of Indian Society for Dental Research. 2018 May-Jun;29(3):280-5.
7. Belibasakis GN, Bostanci N. The RANKL-OPG system in clinical periodontology. Journal of clinical periodontology. 2012 Mar;39(3):239-48. PubMed
8. Bostanci N, İlgenli T, Emingil G, Afacan B, Han B, Töz H, et al. Gingival crevicular fluid levels of RANKL and OPG in periodontal diseases: implications of their relative ratio. Journal of clinical periodontology. 2007;34(5):370-6.
9. Buduneli N, Bıyıkoğlu B, Sherrabeh S, Lappin DF. Saliva concentrations of RANKL and osteoprotegerin in smoker versus non‐smoker chronic periodontitis patients. Journal of clinical periodontology. 2008;35(10):846-52.
10. Loe H. The Gingival Index, the Plaque Index, and the Retention Index Systems. J Periodontol. 1967 Nov-Dec;38(6):Suppl:610-6.
11. Newman MG, Takei H, Klokkevold PR, Carranza FA. Carranza's clinical periodontology: Elsevier health sciences; 2011.
12. Salvi GE, Lawrence HP, Offenbacher S, Beck JD. Influence of risk factors on the pathogenesis of periodontitis. Periodontology 2000. 1997;14(1):173-201.
13. Moreira P, Lima P, Sathler K, Imanishi S, Costa J, Gomez R, et al. Interleukin‐6 expression and gene polymorphism are associated with severity of periodontal disease in a sample of Brazilian individuals. Clinical & Experimental Immunology. 2007;148(1):119-26.
14. Griffiths GS. Formation, collection, and significance of gingival crevice fluid. Periodontology 2000. 2003;31(1):32-42.
15. Gamonal J, Acevedo A, Bascones A, Jorge O, Silva A. Levels of interleukin‐1β,‐8, and‐10 and RANTES in gingival crevicular fluid and cell populations in adult periodontitis patients and the effect of periodontal treatment. Journal of Periodontology. 2000;71(10):1535-45.
16. Tomar SL, Asma S. Smoking‐attributable periodontitis in the United States: findings from NHANES III. Journal of Periodontology. 2000;71(5):743-51.
17. Chatrchaiwiwatana S, Ratanasiri A. Periodontitis associated with tobacco smoking among rural Khon Kaen Thai males: analysis of two data sets. Journal of the Medical Association of Thailand. 2011;92(11):1524.
18. Vouros ID, Kalpidis C, Chadjipantelis T, Konstantinidis AB. Cigarette smoking associated with advanced periodontal destruction in a Greek sample population of patients with periodontal disease. Journal of the International Academy of Periodontology. 2009;11(4):250-7.
19. Apatzidou D, Riggio M, Kinane D. Impact of smoking on the clinical, microbiological and immunological parameters of adult patients with periodontitis. Journal of clinical periodontology. 2005;32(9):973-83.
20. Gomes SC, Piccinin FB, Oppermann RV, Susin C, Marcantonio R. The effect of smoking on gingival crevicular fluid volume during the treatment of gingivitis. Acta odontologica latinoamericana: AOL. 2009;22(3):201-6.
21. Javed F, Abduljabbar T, Vohra F, Malmstrom H, Rahman I, Romanos GE. Comparison of periodontal parameters and self‐perceived oral symptoms among cigarette smokers, individuals vaping electronic cigarettes, and never‐smokers. Journal of periodontology. 2017;88(10):1059-65.
22. Oh H, Hirano J, Takai H, Ogata Y. Effects of initial periodontal therapy on interleukin-1β level in gingival crevicular fluid and clinical periodontal parameters. J Oral Sci. 2015 Jun;57(2):67-71.
23. Orozco A, Gemmell E, Bickel M, Seymour GJ. Interleukin-1beta, interleukin-12 and interleukin-18 levels in gingival fluid and serum of patients with gingivitis and periodontitis. Oral microbiology and immunology. 2006 Aug;21(4):256-60.
24. Rawlinson A, Grummitt JM, Walsh TF, Ian Douglas C. Interleukin 1 and receptor antagonist levels in gingival crevicular fluid in heavy smokers versus non‐smokers. Journal of clinical periodontology. 2003;30(1):42-8.
25. Tymkiw KD, Thunell DH, Johnson GK, Joly S, Burnell KK, Cavanaugh JE, et al. Influence of smoking on gingival crevicular fluid cytokines in severe chronic periodontitis. Journal of clinical periodontology. 2011;38(3):219-28.
26. Stashenko P, Dewhirst FE, Rooney ML, Desjardins LA, Heeley JD. Interleukin‐1β is a potent inhibitor of bone formation in vitro. Journal of Bone and Mineral Research. 1987;2(6):559-65.
27. Toker H, Poyraz O, Eren K. Effect of periodontal treatment on IL‐1β, IL‐1ra, and IL‐10 levels in gingival crevicular fluid in patients with aggressive periodontitis. Journal of clinical periodontology. 2008;35(6):507-13.
28. Boström EA, Lundberg P. The newly discovered cytokine IL-34 is expressed in gingival fibroblasts, shows enhanced expression by pro-inflammatory cytokines, and stimulates osteoclast differentiation. PloS one. 2013;8(12):e81665.
29. Guruprasad C, Pradeep A. Interleukin‐34 levels in gingival crevicular fluid and plasma in periodontal health and disease with and without type‐2 diabetes mellitus. Journal of investigative and clinical dentistry. 2018;9(2):e12317.
30. Clavel G, Thiolat A, Boissier MC. Interleukin newcomers creating new numbers in rheumatology: IL-34 to IL-38. Joint bone spine. 2013 Oct;80(5):449-53.
31. Gorgun EP, Toker H. Value of Gingival Crevicular Fluid Levels of Biomarkers IL-1 β, IL-22 and IL-34 for the Prediction of Severity of Periodontal Diseases and Outcome of Non-Surgical Periodontal Treatment. Int J Acad Med Pharm. 2022;4(1):24-30.
32. Luo Q, Gu X-H. [Expression of cytokines Il-6, IL-34 and M-CSFR in chronic periodontitis and its clinical significance]. Shanghai Kou Qiang Yi Xue. 2018 2018/12//;27(6):652-6.
33. Guruprasad CN, Pradeep AR. Interleukin-34 Levels in Gingival Crevicular Fluid and Plasma in Healthy and Diseased Periodontal Tissue in Presence or Absence of Obesity: A Clinico-biochemical Study. The Bulletin of Tokyo Dental College. 2018;59(2):79-86.
34. Kong YY, Yoshida H, Sarosi I, Tan HL, Timms E, Capparelli C, et al. OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature. 1999 Jan 28;397(6717):315-23.
35. Crotti T, Smith MD, Hirsch R, Soukoulis S, Weedon H, Capone M, et al. Receptor activator NF κB ligand (RANKL) and osteoprotegerin (OPG) protein expression in periodontitis. Journal of periodontal research. 2003;38(4):380-7.
36. Mogi M, Otogoto J, Ota N, Togari A. Differential expression of RANKL and osteoprotegerin in gingival crevicular fluid of patients with periodontitis. Journal of dental research. 2004;83(2):166-9.
37. Wara‐aswapati N, Surarit R, Chayasadom A, Boch JA, Pitiphat W. RANKL upregulation associated with periodontitis and Porphyromonas gingivalis. Journal of periodontology. 2007;78(6):1062-9.
38. Buduneli N, Buduneli E, Kütükçüler N. Interleukin-17, RANKL, and osteoprotegerin levels in gingival crevicular fluid from smoking and non-smoking patients with chronic periodontitis during initial periodontal treatment. Journal of periodontology. 2009 Aug;80(8):1274-80.

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Details

Primary Language	English
Subjects	Health Care Administration
Journal Section	Research articles
Authors	Nilüfer Erenler 0000-0002-6098-2144 Emine Pirim Görgün 0000-0002-8867-1663
Project Number	diş 224
Publication Date	February 28, 2023
Published in Issue	Year 2023 Volume: 9 Issue: 1

Cite

Vancouver	Erenler N, Pirim Görgün E. GCF Levels of Osteoclastogenesis-Related Cytokines in Periodontitis in Relation to Smoking During Non-Surgical Periodontal Therapy. Mid Blac Sea J Health Sci. 2023;9(1):154-68.

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