The effect of smoking on clinical and biochemical early healing outcomes of coronally advanced flap with connective tissue graft: Prospective cohort study.
8-hydroxy-deoxyguanosine
angiogenin
gingival recession
hypoxia inducible factor-1𝛼
smoking
vascular endothelial growth factor
Journal
Journal of periodontology
ISSN: 1943-3670
Titre abrégé: J Periodontol
Pays: United States
ID NLM: 8000345
Informations de publication
Date de publication:
12 Jul 2023
12 Jul 2023
Historique:
revised:
09
06
2023
received:
28
03
2023
accepted:
10
06
2023
pubmed:
12
7
2023
medline:
12
7
2023
entrez:
12
7
2023
Statut:
aheadofprint
Résumé
This study aimed to determine the effects of smoking on early (≤3 months) clinical outcomes and relevant molecular biomarkers following root coverage surgery. Eighteen smokers and 18 nonsmokers, status biochemically verified, with RT1 gingival recession defects were recruited and completed study procedures. All patients received coronally advanced flap plus connective tissue graft. Baseline and 3 month recession depth (RD), recession width (RW), keratinized tissue width (KTW), clinical attachment level (CAL), and gingival phenotype (GP) were recorded. Root coverage (RC) percentage and complete root coverage (CRC) were calculated. Recipient (gingival crevicular fluid) and donor (wound fluid) site VEGF-A, HIF-1α, 8-OHdG, and ANG levels were determined. There were no significant intergroup differences for any baseline or postoperative clinical parameters (P > 0.05), except for whole mouth gingival index (increased in nonsmokers at 3 months; P < 0.05). Compared to baseline, RD, RW, CAL, KTW, and GP significantly improved postoperatively, without significant intergroup differences. There were no significant intergroup differences for RC (smokers = 83%, nonsmokers = 91%, P = 0.069), CRC (smokers = 50%, nonsmokers = 72%, P = 0.177), and CAL gain (P = 0.193). The four biomarker levels significantly increased postoperatively (day 7; P ≤ 0.042) in both groups and returned to baseline (day 28) without significant intergroup differences (P > 0.05). Similarly, donor site parameters were not different between groups. Strong correlations, consistent over time, were found between biomarkers implicated in angiogenesis (VEGF-A, HIF-1α, and ANG). The early (3 month) clinical and molecular changes after root coverage surgery utilizing a coronally advanced flap plus connective tissue graft are similar between smokers and nonsmokers.
Sections du résumé
BACKGROUND
BACKGROUND
This study aimed to determine the effects of smoking on early (≤3 months) clinical outcomes and relevant molecular biomarkers following root coverage surgery.
METHODS
METHODS
Eighteen smokers and 18 nonsmokers, status biochemically verified, with RT1 gingival recession defects were recruited and completed study procedures. All patients received coronally advanced flap plus connective tissue graft. Baseline and 3 month recession depth (RD), recession width (RW), keratinized tissue width (KTW), clinical attachment level (CAL), and gingival phenotype (GP) were recorded. Root coverage (RC) percentage and complete root coverage (CRC) were calculated. Recipient (gingival crevicular fluid) and donor (wound fluid) site VEGF-A, HIF-1α, 8-OHdG, and ANG levels were determined.
RESULTS
RESULTS
There were no significant intergroup differences for any baseline or postoperative clinical parameters (P > 0.05), except for whole mouth gingival index (increased in nonsmokers at 3 months; P < 0.05). Compared to baseline, RD, RW, CAL, KTW, and GP significantly improved postoperatively, without significant intergroup differences. There were no significant intergroup differences for RC (smokers = 83%, nonsmokers = 91%, P = 0.069), CRC (smokers = 50%, nonsmokers = 72%, P = 0.177), and CAL gain (P = 0.193). The four biomarker levels significantly increased postoperatively (day 7; P ≤ 0.042) in both groups and returned to baseline (day 28) without significant intergroup differences (P > 0.05). Similarly, donor site parameters were not different between groups. Strong correlations, consistent over time, were found between biomarkers implicated in angiogenesis (VEGF-A, HIF-1α, and ANG).
CONCLUSIONS
CONCLUSIONS
The early (3 month) clinical and molecular changes after root coverage surgery utilizing a coronally advanced flap plus connective tissue graft are similar between smokers and nonsmokers.
Identifiants
pubmed: 37436705
doi: 10.1002/JPER.23-0214
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : TUBITAK 1002 project program
ID : 219S117
Informations de copyright
© 2023 The Authors. Journal of Periodontology published by Wiley Periodicals LLC on behalf of American Academy of Periodontology.
Références
Periodontology A. Glossary of periodontal terms. The American Academy of Periodontology; 2001.
Zucchelli G, Mounssif I. Periodontal plastic surgery. Periodontol 2000. 2015;68(1):333-368.
Chambrone L, Tatakis DN. Periodontal soft tissue root coverage procedures: a systematic review from the AAP Regeneration Workshop. J Periodontol. 2015;86:S8-S51.
Tatakis DN, Chambrone L, Allen EP, et al. Periodontal soft tissue root coverage procedures: a consensus report from the AAP Regeneration Workshop. J Periodontol. 2015;86:S52-S55.
Erley KJ, Swiec GD, Herold R, Bisch FC, Peacock ME. Gingival recession treatment with connective tissue grafts in smokers and non-smokers. J Periodontol. 2006;77(7):1148-1155.
Nguyen T, Lee KJ, Chen JL, et al. Therapeutic prognosis system for root coverage procedures. Int J Periodontics Restorative Dent. 2021;41(3):383-389.
Agnihotri R, Pandurang P, Kamath SU, et al. Association of cigarette smoking with superoxide dismutase enzyme levels in subjects with chronic periodontitis. J Periodontol. 2009;80(4):657-662.
Hao CP, Cao NJ, Zhu YH, Wang W. The impact of smoking on periodontitis patients' GCF/serum cytokine profile both before and after periodontal therapy: a meta-analysis. BMC Oral Health. 2023;23(1):60.
Wang Y, Anderson EP, Tatakis DN. Whole transcriptome analysis of smoker palatal mucosa identifies multiple downregulated innate immunity genes. J Periodontol. 2020;91(6):756-766.
Johnson GK, Guthmiller JM. The impact of cigarette smoking on periodontal disease and treatment. Periodontol 2000. 2007;44:178-194.
Bucknall T. Factors affecting wound-healing. Probl Gen Surg. 1989;6(2):194-219.
Wang Y, Tatakis DN. Integrative mRNA/miRNA expression analysis in healing human gingiva. J Periodontol. 2020;92(6):863-874.
Johnson KE, Wilgus TA. Vascular endothelial growth factor and angiogenesis in the regulation of cutaneous wound repair. Adv Wound Care (New Rochelle). 2014;3(10):647-661.
Hong WX, Hu MS, Esquivel M, et al. The role of hypoxia-inducible factor in wound healing. Adv Wound Care (New Rochelle). 2014;3(5):390-399.
Park JM, Han YM, Jeong M, et al. Synthetic 8-hydroxydeoxyguanosine inhibited metastasis of pancreatic cancer through concerted inhibitions of ERM and Rho-GTPase. Free Radic Biol Med. 2017;110:151-161.
Cucci LM, Satriano C, Marzo T, La Mendola D. Angiogenin and copper crossing in wound healing. Int J Mol Sci. 2021;22(19):10704.
Kumar V, Abbas AK, Aster JC. Robbins Basic Pathology. 9th ed. Elsevier - Health Sciences Division; 2015:106.
Albina JE, Mastrofrancesco B, Vessella JA, Louis CA, Henry WL Jr, Reichner JS. HIF-1 expression in healing wounds: HIF-1alpha induction in primary inflammatory cells by TNF-alpha. Am J Physiol Cell Physiol. 2001;281(6):C1971-C1977.
Kaval B, Renaud DE, Scott DA, Buduneli N. The role of smoking and gingival crevicular fluid markers on coronally advanced flap outcomes. J Periodontol. 2014;85(3):395-405.
Dias AT, de Menezes CC, Kahn S, Fischer RG, da Silva Figueredo CM, Fernandes GVO. Gingival recession treatment with enamel matrix derivative associated with coronally advanced flap and subepithelial connective tissue graft: a split-mouth randomized controlled clinical trial with molecular evaluation. Clin Oral Investig. 2022;26(2):1453-1463.
Silva CO, Sallum AW, de Lima AF, Tatakis DN. Coronally positioned flap for root coverage: poorer outcomes in smokers. J Periodontol. 2006;77(1):81-87.
Silva CO, de Lima AF, Sallum AW, Tatakis DN. Coronally positioned flap for root coverage in smokers and non-smokers: stability of outcomes between 6 months and 2 years. J Periodontol. 2007;78(9):1702-1707.
Martins AG, Andia DC, Sallum AW, Sallum EA, Casati MZ, Nociti Jr FH. Smoking may affect root coverage outcome: a prospective clinical study in humans. J Periodontol. 2004;75(4):586-591.
Andia DC, Martins AG, Casati MZ, Sallum EA, Nociti FH. Root coverage outcome may be affected by heavy smoking: a 2-year follow-up study. J Periodontol. 2008;79(4):647-653.
Souza SL, Macedo GO, Tunes RS, et al. Subepithelial connective tissue graft for root coverage in smokers and non-smokers: a clinical and histologic controlled study in humans. J Periodontol. 2008;79(6):1014-1021.
Jain RB. Analysis of self-reported versus biomarker based smoking prevalence: methodology to compute corrected smoking prevalence rates. Biomarkers. 2017;22(5):476-487.
Cairo F, Nieri M, Cincinelli S, Mervelt J, Pagliaro U. The interproximal clinical attachment level to classify gingival recessions and predict root coverage outcomes: an explorative and reliability study. J Clin Periodontol. 2011;38(7):661-666.
Silness J, Loe H. Periodontal disease in pregnancy II. Correlation between oral hygiene and periodontal condition. Acta Odontol Scand. 1964;22:121-135.
Löe H, Silness P. Periodontal disease in pregnancy I. Acta Odontol Scand. 1963;21:533-551.
Ainamo J, Bay I. Problems and proposals for recording gingivitis and plaque. Int Dent J. 1975;25(4):229-235.
Cairo F, Cortellini P, Tonetti M, et al. Coronally advanced flap with and without connective tissue graft for the treatment of single maxillary gingival recession with loss of inter-dental attachment. A randomized controlled clinical trial. J Clin Periodontol. 2012;39(8):760-768.
da Silva Neves FL, Silveira CA, Dias SB, et al. Comparison of two power densities on the healing of palatal wounds after connective tissue graft removal: randomized clinical trial. Lasers Med Sci. 2016;31(7):1371-1378.
BinShabaib MS, Mehmood A, Akram Z, ALHarthi SS. Peri-implant clinical and radiographic status and whole salivary cotinine levels among cigarette and waterpipe smokers and never-smokers. J Oral Sci. 2018;60(2):247-252.
Önder C, Kurgan Ş, Altıngöz SM, et al. Impact of non-surgical periodontal therapy on saliva and serum levels of markers of oxidative stress. Clin Oral Investig. 2017;21(6):1961-1969.
Bernert JT Jr, McGuffey JE, Morrison MA, Pirkle JL. Comparison of serum and salivary cotinine measurements by a sensitive high-performance liquid chromatography-tandem mass spectrometry method as an indicator of exposure to tobacco smoke among smokers and nonsmokers. J Anal Toxicol. 2000;24(5):333-339.
Loe H, Holm-Pedersen P. Absence and presence of fluid from normal and inflamed gingivae. Periodontics. 1965;3:171-177.
Keskiner I, Lutfioğlu M, Aydogdu A, Saygun NI, Serdar MA. Effect of photobiomodulation on transforming growth factor-β1, platelet-derived growth factor-bb, and interleukin-8 release in palatal wounds after free gingival graft harvesting: a randomized clinical study. Photomed Laser Surg. 2016;34(6):263-271.
Conway TB, Beck FM, Walters JD. Gingival fluid ciprofloxacin levels at healthy and inflamed human periodontal sites. J Periodontol. 2000;71(9):1448-1452.
Kerner S, Borghetti A, Katsahian S, et al. A retrospective study of root coverage procedures using an image analysis system. J Clin Periodontol. 2008;35(4):346-355.
Chambrone L, Chambrone D, Pustiglioni FE, Chambrone LA, Lima LA. The influence of tobacco smoking on the outcomes achieved by root-coverage procedures: a systematic review. J Am Dent Assoc. 2009;140(3):294-306.
Tonetti MS, Pini-Prato G, Cortellini P. Effect of cigarette smoking on periodontal healing following GTR in infrabony defects. A preliminary retrospective study. J Clin Periodontol. 1995;22(3):229-234.
Silva CO, Ribeiro Edel P, Sallum AW, Tatakis DN. Free gingival grafts: graft shrinkage and donor-site healing in smokers and non-smokers. J Periodontol. 2010;81(5):692-701.
Burkhardt R, Hämmerle CH, Lang NP, Research Group on Oral Soft Tissue Biology & Wound Healing. Self-reported pain perception of patients after mucosal graft harvesting in the palatal area. J Clin Periodontol. 2015;42(3):281-287.
Guiha R, el Khodeiry S, Mota L, Caffesse R. Histological evaluation of healing and revascularization of the subepithelial connective tissue graft. J Periodontol. 2001;72(4):470-478.
Pan SC, Wu LW, Chen CL, Shieh SJ, Chiu HY. Angiogenin expression in burn blister fluid: implications for its role in burn wound neovascularization. Wound Repair Regen. 2012;20(5):731-739.
Kifune T, Ito H, Ishiyama M, et al. Hypoxia-induced upregulation of angiogenic factors in immortalized human periodontal ligament fibroblasts. J Oral Sci. 2018;60(4):519-525.
Meng LB, Zhang YM, Shan MJ, Qiu Y, Zhang TJ, Gong T. Pivotal micro factors associated with endothelial cells. Chin Med J (Engl). 2019;132(16):1965-1973.
Kishimoto K, Liu S, Tsuji T, Olson KA, Hu GF. Endogenous angiogenin in endothelial cells is a general requirement for cell proliferation and angiogenesis. Oncogene. 2005;24(3):445-456.
Oladipupo S, Hu S, Kovalski J, et al. VEGF is essential for hypoxia-inducible factor-mediated neovascularization but dispensable for endothelial sprouting. Proc Natl Acad Sci USA. 2011;108(32):13264-13269.
Morelli T, Neiva R, Nevins ML, et al. Angiogenic biomarkers and healing of living cellular constructs. J Dent Res. 2011;90(4):456-462.
Wang Y, Tatakis DN. Human gingiva transcriptome during wound healing. J Clin Periodontol. 2017;44(4):394-402.
Choi YS, Choi HJ, Min JK, et al. Interleukin-33 induces angiogenesis and vascular permeability through ST2/TRAF6-mediated endothelial nitric oxide production. Blood. 2009;114(14):3117-3126.
Shan S, Li Y, Wang J, et al. Nasal administration of interleukin-33 induces airways angiogenesis and expression of multiple angiogenic factors in a murine asthma surrogate. Immunology. 2016;148(1):83-91.
Liu J, Wang W, Wang L, et al. IL-33 initiates vascular remodelling in hypoxic pulmonary hypertension by up-regulating hif-1α and vegf-expression in vascular endothelial cells. E Bio Medicine. 2018;33:196-210.