Research Article
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Clinical and Biochemical Effects of Smoking on Non-Surgical Periodontal Treatment in Grade III Stage C Periodontitis Patients

Year 2023, Volume: 13 Issue: 1, 218 - 227, 28.03.2023
https://doi.org/10.33808/clinexphealthsci.1128101

Abstract

Objective: The purpose of this study was to evaluate the effect of smoking on clinical parameters and the serum and saliva levels of RANKL, OPG, and IL-34 in periodontitis stage III grade C (III-C) patients after non-surgical periodontal treatment (NSPT).
Methods: A total of 60 subjects, 40 periodontitis-III-C patients (20 smokers and 20 non-smokers) and 20 non-smoker periodontally healthy individuals, were included. All clinical periodontal parameters were recorded, and unstimulated saliva and serum samples were collected from all patients at baseline, but at 1 and 3 months only from periodontitis patients (N=40). Saliva and serum levels of RANKL, OPG, and IL-34 were analyzed by ELISA.
Results: At baseline only whole mouth probing depth (PD) and percent of sites with PD>5mm were higher in smokers than non-smoker periodontitis patients (p<.05). All periodontal measurements significantly improved in both periodontitis groups after NSPT (p<.001). After NSPT, the reduction in gingival index (GI), bleeding on probing (BOP), and mean PD in sites initially PD≥5mm were lower in smokers than nonsmoker periodontitis patients (p>.05). Only saliva IL-34 levels were higher in all-periodontitis patients than healthy individuals (p=.001) and decreased in both periodontitis groups after NSPT (p<.05). Moreover, elevated serum RANKL level was detected in smokers compared to nonsmoker periodontitis or healthy ones at baseline (p<.05). Serum RANKL levels exhibited no change after NSPT in either periodontitis groups.
Conclusions: The smokers are less responsive to NSPT, and saliva IL-34 can be a potential inflammatory marker of periodontitis-III-C. Moreover, high serum RANKL levels are associated with smoking.

Supporting Institution

Marmara Üniversitesi Bilimsel Araştırma Projeleri Komisyonu Başkanlığı

Project Number

SAG-C-DRP-241018-0569

Thanks

The authors thank the biochemist S. Çolpan from Farmasina Research Laboratory for technical assistance in the biochemical analysis.

References

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  • Johnson GK, Guthmiller JM. The impact of cigarette smoking on periodontal disease and treatment. Periodontol 2000. 2007;44(1):178-194. DOI: 10.1111/j.1600-0757.2007.00212.x
  • Helal O, Göstemeyer G, Krois J, Fawzy El Sayed K, Graetz C, Schwendicke F. Predictors for tooth loss in periodontitis patients: Systematic review and meta‐analysis. J Clin Periodontol. 2019;46(7):699-712. DOI: 10.1111/jcpe.13118
  • Guru S, Sam SE, Rajan S, Padmanabhan S. Comparative evaluation of salivary hepatocyte growth factor in smokers and non‐smokers with chronic periodontitis. J Investig Clin Dent. 2018;9(2):e12306. DOI: 10.1111/jicd.12306
  • Preshaw PM, Lauffart B, Zak E, Jeffcoat MK, Barton I, Heasman PA. Progression and treatment of chronic adult periodontitis. J Periodontol. 1999;70(10):1209-1220. DOI: 10.1902/jop.1999.70.10.1209
  • Preshaw P, Holliday R, Law H, Heasman P. Outcomes of non‐surgical periodontal treatment by dental hygienists in training: impact of site‐and patient‐level factors. Int J Dent Hyg. 2013;11(4):273-279. DOI: 10.1111/idh.12032
  • 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
  • Buduneli N, Kardeşler L, Işık H, Willis III CS, Hawkins SI, Kinane DF, Scott DA. Effects of smoking and gingival inflammation on salivary antioxidant capacity. J Clin Periodontol. 2006;33(3):159-164. DOI: 10.1111/j.1600-051X.2006.00892.x
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  • 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. J Clin Periodontol. 2009;80(8):1274-1280. DOI: 10.1902/jop.2009.090106
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  • Yuce HB, Gokturk O, Turkal HA, Inanir A, Benli I, Demir O. Assessment of local and systemic 25-hydroxy-vitamin D, RANKL, OPG, and TNF levels in patients with rheumatoid arthritis and periodontitis. J Oral Sci. 2017;59(3):397-404. DOI: 10.2334/josnusd.16-0677
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  • Shetty B, Divakar DD, Al-Kheraif AA, Alharbi AO, Almutairi MST, Alanazi MM. Role of PDT as an adjunct to SRP on whole salivary RANKL and OPG ratio in type-2 diabetic and normoglycemic individuals with chronic periodontitis. Cytokine. 2021;34:102220. DOI: 10.1016/j.pdpdt.2021.102220
  • Lin H, Lee E, Hestir K, Leo C, Huang M, Bosch E, Halenbeck R, Wu G, Zhou A, Behrens D. Discovery of a cytokine and its receptor by functional screening of the extracellular proteome. Science. 2008;320(5877):807-811. DOI: 10.1126/science.1154370
  • Guruprasad C, Pradeep A. Influence of smoking on interleukin-34 levels in gingival crevicular fluid and plasma in periodontal health and disease: A clinico-biochemical study. Bull Tokyo Dent Coll. 2018;59(4):247-255. DOI: 10.2209/tdcpublication.2017-0051
  • Tonetti MS, Greenwell H, Kornman KS. Staging and grading of periodontitis: Framework and proposal of a new classification and case definition. J Periodontol. 2018;89(Suppl 1):S159-S172. DOI: 10.1002/jper.18-0006
  • Lang NP, Bartold PM. Periodontal health. J Periodontol. 2018;89 Suppl 1:S9-s16. DOI: 10.1002/jper.16-0517
  • Türkoğlu O, Eren G, Emingil G, Azarsız E, Kutukculer N, Atilla G. Does smoking affect gingival crevicular fluid LL-37 levels following non-surgical periodontal treatment in chronic periodontitis? Arch Oral Biol. 2016;61:98-105. DOI: 10.1016/j.archoralbio.2015.10.018
  • Silness J, Löe H. Periodontal disease in pregnancy II. Correlation between oral hygiene and periodontal condition. Acta Odontol Scand. 1964;22(1):121-135. DOI: 10.3109/00016356408993968.
  • Löe H, Silness J. Periodontal disease in pregnancy I. Prevalence and severity. Acta Odontol Scand. 1963;21(6):533-551. DOI: 10.3109/00016356309011240
  • Görgülü NG, Doğan B. Effect of non‐surgical periodontal treatment on salivary and serum biomarkers in stage III grade B and C periodontitis. J Periodontol. 2022. DOI: 10.1002/JPER.21-0536
  • Yamamoto Y, Nishida N, Tanaka M, Hayashi N, Matsuse R, Nakayama K, Morimoto K, Shizukuishi S. Association between passive and active smoking evaluated by salivary cotinine and periodontitis. J Clin Periodontol. 2005;32(10):1041-1046. DOI: 10.1111/j.1600-051X.2005.00819.x
  • Chen Z, Buki K, Vääräniemi J, Gu G, Väänänen HK. The critical role of IL-34 in osteoclastogenesis. PloS one. 2011;6(4):e18689. DOI: 10.1371/journal.pone.0018689
  • Yasuda H. Discovery of the RANKL/RANK/OPG system. J Bone Miner Metab. 2021;39(1):2-11. DOI: 10.1007/s00774-020-01175-1
  • Chang J, Meng HW, Lalla E, Lee CT. The impact of smoking on non-surgical periodontal therapy: A systematic review and meta-analysis. J Clin Periodontol. 2021;48(1):60-75. DOI: 10.1111/jcpe.13384
  • Tsukasaki M. RANKL and osteoimmunology in periodontitis. J Bone Miner Metab. 2021;39(1):82-90. DOI: 10.1007/s00774-020-01165-3
  • Frodge BD, Ebersole JL, Kryscio RJ, Thomas MV, Miller CS. Bone remodeling biomarkers of periodontal disease in saliva. J Periodontol. 2008;79(10):1913-1919. DOI: 10.1902/jop.2008.080070
  • Buduneli N, Bıyıkoğlu B, Sherrabeh S, Lappin DF. Saliva concentrations of RANKL and osteoprotegerin in smoker versus non‐smoker chronic periodontitis patients. J Clin Periodontol. 2008;35(10):846-852. DOI: 10.1111/j.1600-051X.2008.01310.x
  • Al-Sabbagh M, Alladah A, Lin Y, Kryscio RJ, Thomas MV, Ebersole JL, Miller CS. Bone remodeling-associated salivary biomarker MIP-1α distinguishes periodontal disease from health. J Periodontal Res. 2012;47(3):389-395. DOI: 10.1111/j.1600-0765.2011.01445.x
  • Caldeira FID, Hidalgo MAR, Dias MLDC, Scarel-Caminaga RM, Pigossi SC. Systematic review of ratios between disease/health periodontitis modulators and meta-analysis of their levels in gingival tissue and biological fluids. Arch Oral Biol. 2021;127:105147. DOI: 10.1016/j.archoralbio.2021.105147
  • Tabari ZA, Azadmehr A, Tabrizi MAA, Hamissi J, Ghaedi FB. Salivary soluble receptor activator of nuclear factor kappa B ligand/osteoprotegerin ratio in periodontal disease and health. J Periodontal Implant Sci. 2013;43(5):227. DOI: 10.5051/jpis.2013.43.5.227
  • Hikita A, Yana I, Wakeyama H, Nakamura M, Kadono Y, Oshima Y, Nakamura K, Seiki M, Tanaka S. Negative regulation of osteoclastogenesis by ectodomain shedding of receptor activator of NF-kappaB ligand. J Biol Chem. 2006;281(48):36846-36855. DOI: 10.1074/jbc.M606656200
  • Tsukasaki M, Komatsu N, Nagashima K, Nitta T, Pluemsakunthai W, Shukunami C, Iwakura Y, Nakashima T, Okamoto K, Takayanagi H. Host defense against oral microbiota by bone-damaging T cells. Nat Commun. 2018;9(1):701. DOI: 10.1038/s41467-018-03147-6
  • Perlstein TS, Lee RT. Smoking, metalloproteinases, and vascular disease. Arterioscler Thromb Vasc Biol. 2006;26(2):250-256. DOI: 10.1161/01.ATV.0000199268.27395.4f
  • Lum L, Wong BR, Josien R, Becherer JD, Erdjument-Bromage H, Schlöndorff J, Tempst P, Choi Y, Blobel CP. Evidence for a role of a tumor necrosis factor-alpha (TNF-alpha)-converting enzyme-like protease in shedding of TRANCE, a TNF family member involved in osteoclastogenesis and dendritic cell survival. J Biol Chem. 1999;274(19):13613-13618. DOI: 10.1074/jbc.274.19.13613
  • Ozçaka O, Biçakci N, Pussinen P, Sorsa T, Köse T, Buduneli N. Smoking and matrix metalloproteinases, neutrophil elastase and myeloperoxidase in chronic periodontitis. Oral Dis. 2011;17(1):68-76. DOI: 10.1111/j.1601-0825.2010.01705.x
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Year 2023, Volume: 13 Issue: 1, 218 - 227, 28.03.2023
https://doi.org/10.33808/clinexphealthsci.1128101

Abstract

Project Number

SAG-C-DRP-241018-0569

References

  • Apatzidou D, Riggio M, Kinane D. Impact of smoking on the clinical, microbiological and immunological parameters of adult patients with periodontitis. J Clin Periodontol. 2005;32(9):973-983. DOI: 10.1111/j.1600-051X.2005.00788.x
  • Johnson GK, Guthmiller JM. The impact of cigarette smoking on periodontal disease and treatment. Periodontol 2000. 2007;44(1):178-194. DOI: 10.1111/j.1600-0757.2007.00212.x
  • Helal O, Göstemeyer G, Krois J, Fawzy El Sayed K, Graetz C, Schwendicke F. Predictors for tooth loss in periodontitis patients: Systematic review and meta‐analysis. J Clin Periodontol. 2019;46(7):699-712. DOI: 10.1111/jcpe.13118
  • Guru S, Sam SE, Rajan S, Padmanabhan S. Comparative evaluation of salivary hepatocyte growth factor in smokers and non‐smokers with chronic periodontitis. J Investig Clin Dent. 2018;9(2):e12306. DOI: 10.1111/jicd.12306
  • Preshaw PM, Lauffart B, Zak E, Jeffcoat MK, Barton I, Heasman PA. Progression and treatment of chronic adult periodontitis. J Periodontol. 1999;70(10):1209-1220. DOI: 10.1902/jop.1999.70.10.1209
  • Preshaw P, Holliday R, Law H, Heasman P. Outcomes of non‐surgical periodontal treatment by dental hygienists in training: impact of site‐and patient‐level factors. Int J Dent Hyg. 2013;11(4):273-279. DOI: 10.1111/idh.12032
  • 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
  • Buduneli N, Kardeşler L, Işık H, Willis III CS, Hawkins SI, Kinane DF, Scott DA. Effects of smoking and gingival inflammation on salivary antioxidant capacity. J Clin Periodontol. 2006;33(3):159-164. DOI: 10.1111/j.1600-051X.2006.00892.x
  • Ojima M, Hanioka T. Destructive effects of smoking on molecular and genetic factors of periodontal disease. Tob Induc Dis. 2010;8(1):1-8. DOI: 10.1186/1617-9625-8-4
  • Tanaka H, Tanabe N, Shoji M, Suzuki N, Katono T, Sato S, Motohashi M, Maeno M. Nicotine and lipopolysaccharide stimulate the formation of osteoclast-like cells by increasing macrophage colony-stimulating factor and prostaglandin E2 production by osteoblasts. Life Sci. 2006;78(15):1733-1740. DOI: 10.1016/j.lfs.2005.08.017
  • Linden GJ, Lyons A, Scannapieco FA. Periodontal systemic associations: Review of the evidence. J Periodontol. 2013;84 (Suppl 4):8-19. DOI: 10.1902/jop.2013.1340010.
  • Kong Y-Y, Yoshida H, Sarosi I, Tan H-L, Timms E, Capparelli C, Morony S, Oliveira-dos-Santos AJ, Van G, Itie A. OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature. 1999;397(6717):315-323. DOI: 10.1038/16852
  • Lacey D, Timms E, Tan H-L, Kelley M, Dunstan C, Burgess T, Elliott R, Colombero A, Elliott G, Scully S. Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell. 1998;93(2):165-176. DOI: 10.1016/S0092-8674(00)81569-X
  • Simonet W, Lacey D, Dunstan C, Kelley M, Chang M-S, Lüthy R, Nguyen H, Wooden S, Bennett L, Boone T. Osteoprotegerin: a novel secreted protein involved in the regulation of bone density. Cell. 1997;89(2):309-319. DOI: 10.1016/S0092-8674(00)80209-3
  • Özçaka Ö, Nalbantsoy A, Köse T, Buduneli N. Plasma osteoprotegerin levels are decreased in smoker chronic periodontitis patients. Aust Dent J. 2010;55(4):405-410. DOI: 10.1111/j.1834-7819.2010.01261.x
  • Lappin DF, Sherrabeh S, Jenkins WM, Macpherson LM. Effect of smoking on serum RANKL and OPG in sex, age and clinically matched supportive‐therapy periodontitis patients. J Clin Periodontol. 2007;34(4):271-277. DOI: 10.1111/j.1600-051X.2007.01048.x
  • Tang TH, Fitzsimmons TR, Bartold PM. Effect of smoking on concentrations of receptor activator of nuclear factor κ B ligand and osteoprotegerin in human gingival crevicular fluid. J Clin Periodontol. 2009;36(9):713-718. DOI: 10.1111/j.1600-051X.2009.01444.x
  • 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. J Clin Periodontol. 2009;80(8):1274-1280. DOI: 10.1902/jop.2009.090106
  • Behfarnia P, Saied-Moallemi Z, Javanmard SH, Naseri R. Serum, saliva, and GCF concentration of RANKL and osteoprotegerin in smokers versus nonsmokers with chronic periodontitis. Adv Biomed Res. 2016;5:80. DOI: 10.4103/2277-9175.180992.
  • Yuce HB, Gokturk O, Turkal HA, Inanir A, Benli I, Demir O. Assessment of local and systemic 25-hydroxy-vitamin D, RANKL, OPG, and TNF levels in patients with rheumatoid arthritis and periodontitis. J Oral Sci. 2017;59(3):397-404. DOI: 10.2334/josnusd.16-0677
  • Doğan SB, Dede FÖ, Balli U, Sertoglu E. Emerging roles of Interleukin-34 together with receptor activator of nuclear factor-kB ligand and osteoprotegerin levels in periodontal disease. Cytokine. 2021;144:155584. DOI: 10.1016/j.cyto.2021.155584
  • Shetty B, Divakar DD, Al-Kheraif AA, Alharbi AO, Almutairi MST, Alanazi MM. Role of PDT as an adjunct to SRP on whole salivary RANKL and OPG ratio in type-2 diabetic and normoglycemic individuals with chronic periodontitis. Cytokine. 2021;34:102220. DOI: 10.1016/j.pdpdt.2021.102220
  • Lin H, Lee E, Hestir K, Leo C, Huang M, Bosch E, Halenbeck R, Wu G, Zhou A, Behrens D. Discovery of a cytokine and its receptor by functional screening of the extracellular proteome. Science. 2008;320(5877):807-811. DOI: 10.1126/science.1154370
  • Guruprasad C, Pradeep A. Influence of smoking on interleukin-34 levels in gingival crevicular fluid and plasma in periodontal health and disease: A clinico-biochemical study. Bull Tokyo Dent Coll. 2018;59(4):247-255. DOI: 10.2209/tdcpublication.2017-0051
  • Tonetti MS, Greenwell H, Kornman KS. Staging and grading of periodontitis: Framework and proposal of a new classification and case definition. J Periodontol. 2018;89(Suppl 1):S159-S172. DOI: 10.1002/jper.18-0006
  • Lang NP, Bartold PM. Periodontal health. J Periodontol. 2018;89 Suppl 1:S9-s16. DOI: 10.1002/jper.16-0517
  • Türkoğlu O, Eren G, Emingil G, Azarsız E, Kutukculer N, Atilla G. Does smoking affect gingival crevicular fluid LL-37 levels following non-surgical periodontal treatment in chronic periodontitis? Arch Oral Biol. 2016;61:98-105. DOI: 10.1016/j.archoralbio.2015.10.018
  • Silness J, Löe H. Periodontal disease in pregnancy II. Correlation between oral hygiene and periodontal condition. Acta Odontol Scand. 1964;22(1):121-135. DOI: 10.3109/00016356408993968.
  • Löe H, Silness J. Periodontal disease in pregnancy I. Prevalence and severity. Acta Odontol Scand. 1963;21(6):533-551. DOI: 10.3109/00016356309011240
  • Görgülü NG, Doğan B. Effect of non‐surgical periodontal treatment on salivary and serum biomarkers in stage III grade B and C periodontitis. J Periodontol. 2022. DOI: 10.1002/JPER.21-0536
  • Yamamoto Y, Nishida N, Tanaka M, Hayashi N, Matsuse R, Nakayama K, Morimoto K, Shizukuishi S. Association between passive and active smoking evaluated by salivary cotinine and periodontitis. J Clin Periodontol. 2005;32(10):1041-1046. DOI: 10.1111/j.1600-051X.2005.00819.x
  • Chen Z, Buki K, Vääräniemi J, Gu G, Väänänen HK. The critical role of IL-34 in osteoclastogenesis. PloS one. 2011;6(4):e18689. DOI: 10.1371/journal.pone.0018689
  • Yasuda H. Discovery of the RANKL/RANK/OPG system. J Bone Miner Metab. 2021;39(1):2-11. DOI: 10.1007/s00774-020-01175-1
  • Chang J, Meng HW, Lalla E, Lee CT. The impact of smoking on non-surgical periodontal therapy: A systematic review and meta-analysis. J Clin Periodontol. 2021;48(1):60-75. DOI: 10.1111/jcpe.13384
  • Tsukasaki M. RANKL and osteoimmunology in periodontitis. J Bone Miner Metab. 2021;39(1):82-90. DOI: 10.1007/s00774-020-01165-3
  • Frodge BD, Ebersole JL, Kryscio RJ, Thomas MV, Miller CS. Bone remodeling biomarkers of periodontal disease in saliva. J Periodontol. 2008;79(10):1913-1919. DOI: 10.1902/jop.2008.080070
  • Buduneli N, Bıyıkoğlu B, Sherrabeh S, Lappin DF. Saliva concentrations of RANKL and osteoprotegerin in smoker versus non‐smoker chronic periodontitis patients. J Clin Periodontol. 2008;35(10):846-852. DOI: 10.1111/j.1600-051X.2008.01310.x
  • Al-Sabbagh M, Alladah A, Lin Y, Kryscio RJ, Thomas MV, Ebersole JL, Miller CS. Bone remodeling-associated salivary biomarker MIP-1α distinguishes periodontal disease from health. J Periodontal Res. 2012;47(3):389-395. DOI: 10.1111/j.1600-0765.2011.01445.x
  • Caldeira FID, Hidalgo MAR, Dias MLDC, Scarel-Caminaga RM, Pigossi SC. Systematic review of ratios between disease/health periodontitis modulators and meta-analysis of their levels in gingival tissue and biological fluids. Arch Oral Biol. 2021;127:105147. DOI: 10.1016/j.archoralbio.2021.105147
  • Tabari ZA, Azadmehr A, Tabrizi MAA, Hamissi J, Ghaedi FB. Salivary soluble receptor activator of nuclear factor kappa B ligand/osteoprotegerin ratio in periodontal disease and health. J Periodontal Implant Sci. 2013;43(5):227. DOI: 10.5051/jpis.2013.43.5.227
  • Hikita A, Yana I, Wakeyama H, Nakamura M, Kadono Y, Oshima Y, Nakamura K, Seiki M, Tanaka S. Negative regulation of osteoclastogenesis by ectodomain shedding of receptor activator of NF-kappaB ligand. J Biol Chem. 2006;281(48):36846-36855. DOI: 10.1074/jbc.M606656200
  • Tsukasaki M, Komatsu N, Nagashima K, Nitta T, Pluemsakunthai W, Shukunami C, Iwakura Y, Nakashima T, Okamoto K, Takayanagi H. Host defense against oral microbiota by bone-damaging T cells. Nat Commun. 2018;9(1):701. DOI: 10.1038/s41467-018-03147-6
  • Perlstein TS, Lee RT. Smoking, metalloproteinases, and vascular disease. Arterioscler Thromb Vasc Biol. 2006;26(2):250-256. DOI: 10.1161/01.ATV.0000199268.27395.4f
  • Lum L, Wong BR, Josien R, Becherer JD, Erdjument-Bromage H, Schlöndorff J, Tempst P, Choi Y, Blobel CP. Evidence for a role of a tumor necrosis factor-alpha (TNF-alpha)-converting enzyme-like protease in shedding of TRANCE, a TNF family member involved in osteoclastogenesis and dendritic cell survival. J Biol Chem. 1999;274(19):13613-13618. DOI: 10.1074/jbc.274.19.13613
  • Ozçaka O, Biçakci N, Pussinen P, Sorsa T, Köse T, Buduneli N. Smoking and matrix metalloproteinases, neutrophil elastase and myeloperoxidase in chronic periodontitis. Oral Dis. 2011;17(1):68-76. DOI: 10.1111/j.1601-0825.2010.01705.x
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There are 50 citations in total.

Details

Primary Language English
Subjects Health Care Administration
Journal Section Articles
Authors

Volkan Arıkan This is me 0000-0003-2293-0578

Nimet Gül Görgülü 0000-0002-0890-9695

Başak Doğan 0000-0002-3602-4886

Project Number SAG-C-DRP-241018-0569
Publication Date March 28, 2023
Submission Date June 8, 2022
Published in Issue Year 2023 Volume: 13 Issue: 1

Cite

APA Arıkan, V., Görgülü, N. G., & Doğan, B. (2023). Clinical and Biochemical Effects of Smoking on Non-Surgical Periodontal Treatment in Grade III Stage C Periodontitis Patients. Clinical and Experimental Health Sciences, 13(1), 218-227. https://doi.org/10.33808/clinexphealthsci.1128101
AMA Arıkan V, Görgülü NG, Doğan B. Clinical and Biochemical Effects of Smoking on Non-Surgical Periodontal Treatment in Grade III Stage C Periodontitis Patients. Clinical and Experimental Health Sciences. March 2023;13(1):218-227. doi:10.33808/clinexphealthsci.1128101
Chicago Arıkan, Volkan, Nimet Gül Görgülü, and Başak Doğan. “Clinical and Biochemical Effects of Smoking on Non-Surgical Periodontal Treatment in Grade III Stage C Periodontitis Patients”. Clinical and Experimental Health Sciences 13, no. 1 (March 2023): 218-27. https://doi.org/10.33808/clinexphealthsci.1128101.
EndNote Arıkan V, Görgülü NG, Doğan B (March 1, 2023) Clinical and Biochemical Effects of Smoking on Non-Surgical Periodontal Treatment in Grade III Stage C Periodontitis Patients. Clinical and Experimental Health Sciences 13 1 218–227.
IEEE V. Arıkan, N. G. Görgülü, and B. Doğan, “Clinical and Biochemical Effects of Smoking on Non-Surgical Periodontal Treatment in Grade III Stage C Periodontitis Patients”, Clinical and Experimental Health Sciences, vol. 13, no. 1, pp. 218–227, 2023, doi: 10.33808/clinexphealthsci.1128101.
ISNAD Arıkan, Volkan et al. “Clinical and Biochemical Effects of Smoking on Non-Surgical Periodontal Treatment in Grade III Stage C Periodontitis Patients”. Clinical and Experimental Health Sciences 13/1 (March 2023), 218-227. https://doi.org/10.33808/clinexphealthsci.1128101.
JAMA Arıkan V, Görgülü NG, Doğan B. Clinical and Biochemical Effects of Smoking on Non-Surgical Periodontal Treatment in Grade III Stage C Periodontitis Patients. Clinical and Experimental Health Sciences. 2023;13:218–227.
MLA Arıkan, Volkan et al. “Clinical and Biochemical Effects of Smoking on Non-Surgical Periodontal Treatment in Grade III Stage C Periodontitis Patients”. Clinical and Experimental Health Sciences, vol. 13, no. 1, 2023, pp. 218-27, doi:10.33808/clinexphealthsci.1128101.
Vancouver Arıkan V, Görgülü NG, Doğan B. Clinical and Biochemical Effects of Smoking on Non-Surgical Periodontal Treatment in Grade III Stage C Periodontitis Patients. Clinical and Experimental Health Sciences. 2023;13(1):218-27.

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