{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,28]],"date-time":"2026-10-28T02:46:11Z","timestamp":1793155571336,"version":"4.5.0"},"reference-count":55,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2026,1,5]],"date-time":"2026-01-05T00:00:00Z","timestamp":1767571200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Med."],"abstract":"<jats:sec>\n                    <jats:title>Objective<\/jats:title>\n                    <jats:p>To systematically evaluate the association between smoking and both periodontal inflammation and alveolar bone resorption in patients with chronic periodontitis.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods<\/jats:title>\n                    <jats:p>A computerized search was conducted using databases such as PubMed, Embase, Web of Science, and China National Knowledge Infrastructure to identify studies published between January 2005 and January 2023 that examined the relationship between smoking and both periodontal inflammation and alveolar bone resorption in chronic periodontitis. A total of 1,654 articles were initially retrieved. After applying the inclusion and exclusion criteria, 13 studies were included in the final analysis, comprising a total of 1,653 patients\u2014893 in the study group and 760 in the control group. The study group included smoker chronic periodontitis patients, and the control group included non-smoker chronic periodontitis patients. Two independent researchers screened the literature and extracted relevant data. Meta-analysis was performed using RevMan 5.3 software.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>\n                      Compared with the control group, the study group showed significantly higher levels of intercellular adhesion molecule 1 (mean difference [MD]\u202f=\u202f135.93; 95% confidence interval [CI]: 48.91, 222.95;\n                      <jats:italic>p<\/jats:italic>\n                      \u202f=\u202f0.002), high-mobility group box 1 (MD\u202f=\u202f6.02; 95% CI: 1.30, 10.73;\n                      <jats:italic>p<\/jats:italic>\n                      \u202f=\u202f0.01), interleukin-17 (MD\u202f=\u202f94.62; 95% CI: 23.34, 165.90;\n                      <jats:italic>p<\/jats:italic>\n                      \u202f=\u202f0.009), C-terminal telopeptide of type I collagen (MD\u202f=\u202f14.56; 95% CI: 12.03, 17.09;\n                      <jats:italic>p<\/jats:italic>\n                      \u202f&amp;lt;\u202f0.00001), receptor activator of nuclear factor kappa-B ligand (MD\u202f=\u202f1.49; 95% CI: 0.85, 2.14;\n                      <jats:italic>p<\/jats:italic>\n                      \u202f&amp;lt;\u202f0.00001) and matrix metalloproteinase 9 (MD\u202f=\u202f27.15; 95% CI: 5.94, 48.37;\n                      <jats:italic>p<\/jats:italic>\n                      \u202f=\u202f0.01), as well as lower levels of osteoprotegerin (MD\u202f=\u202f\u22121.52; 95% CI: \u22122.98, \u22120.06;\n                      <jats:italic>p<\/jats:italic>\n                      \u202f=\u202f0.04). There were no significant differences in chitinase-3-like protein 1 levels (MD\u202f=\u202f16.40; 95% CI: \u22123.84, 36.64;\n                      <jats:italic>p<\/jats:italic>\n                      \u202f=\u202f0.11), procollagen type I N-terminal propeptide levels (MD\u202f=\u202f\u22124.35; 95% CI: \u221210.71, 2.02;\n                      <jats:italic>p<\/jats:italic>\n                      \u202f=\u202f0.18) and N-terminal telopeptide of type I collagen levels (MD\u202f=\u202f9.03; 95% CI: \u22126.75, 24.80;\n                      <jats:italic>p<\/jats:italic>\n                      \u202f=\u202f0.26) in the gingival crevicular fluid between the two groups.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusion<\/jats:title>\n                    <jats:p>Smoking exacerbates periodontal inflammation and promotes alveolar bone resorption in patients with chronic periodontitis.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.3389\/fmed.2025.1666722","type":"journal-article","created":{"date-parts":[[2026,1,5]],"date-time":"2026-01-05T07:45:20Z","timestamp":1767599120000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":4,"title":["A study on the association between smoking, periodontal inflammation and alveolar bone resorption in patients with chronic periodontitis based on biomarkers: a meta-analysis"],"prefix":"10.3389","volume":"12","author":[{"given":"Bing","family":"Li","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Li","family":"Xia","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cui","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qingqing","family":"Zhu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhe","family":"Chen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2026,1,5]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"98","DOI":"10.1080\/00325481.2018.1396876","article-title":"Chronic periodontitis, inflammatory cytokines, and interrelationship with other chronic diseases","volume":"130","author":"Cardoso","year":"2018","journal-title":"Postgrad Med"},{"key":"ref2","doi-asserted-by":"publisher","first-page":"909","DOI":"10.1016\/j.imbio.2014.08.003","article-title":"Effect of smoking on immunity in human chronic periodontitis","volume":"219","author":"Souto","year":"2014","journal-title":"Immunobiology"},{"key":"ref3","doi-asserted-by":"publisher","first-page":"642","DOI":"10.1111\/jre.12146","article-title":"Smoking-related cotinine levels and host responses in chronic periodontitis","volume":"49","author":"Ebersole","year":"2014","journal-title":"J Periodontal Res"},{"key":"ref4","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1111\/prd.12449","article-title":"The role of cigarette smoking in periodontal disease and treatment outcomes of dental implant therapy","volume":"90","author":"Apatzidou","year":"2022","journal-title":"Periodontol 2000"},{"key":"ref5","doi-asserted-by":"publisher","first-page":"1041","DOI":"10.1111\/jre.13166","article-title":"Does smoking influence tryptophan metabolism in periodontal inflammation? A cross-sectional study","volume":"58","author":"\u00d6nder","year":"2023","journal-title":"J Periodontal Res"},{"key":"ref6","doi-asserted-by":"publisher","first-page":"1274","DOI":"10.1902\/jop.2009.090106","article-title":"Interleukin-17, RANKL, and osteoprotegerin levels in gingival crevicular fluid from smoking and non-smoking patients with chronic periodontitis during initial periodontal treatment","volume":"80","author":"Buduneli","year":"2009","journal-title":"J Periodontol"},{"key":"ref7","doi-asserted-by":"publisher","first-page":"143","DOI":"10.1902\/jop.2011.110130","article-title":"The effect of smoking on periodontal bone regeneration: a systematic review and meta-analysis","volume":"83","author":"Patel","year":"2012","journal-title":"J Periodontol"},{"key":"ref8","doi-asserted-by":"publisher","first-page":"658","DOI":"10.1034\/j.1600-051x.2000.027009658.x","article-title":"The association of cigarette smoking with alveolar bone loss in postmenopausal females","volume":"27","author":"Payne","year":"2000","journal-title":"J Clin Periodontol"},{"key":"ref9","doi-asserted-by":"publisher","first-page":"205","DOI":"10.1111\/prd.12317","article-title":"Understanding resolution of inflammation in periodontal diseases: is chronic inflammatory periodontitis a failure to resolve?","volume":"82","author":"Van Dyke","year":"2020","journal-title":"Periodontol"},{"key":"ref10","doi-asserted-by":"publisher","first-page":"263","DOI":"10.1016\/j.actbio.2020.01.031","article-title":"Reduction of inflammation in a chronic periodontitis model in rats by TNF-\u03b1 gene silencing with a topically applied siRNA-loaded calcium phosphate paste","volume":"105","author":"Tenkumo","year":"2020","journal-title":"Acta Biomater"},{"key":"ref11","doi-asserted-by":"publisher","first-page":"1885","DOI":"10.1097\/CM9.0000000000003153","article-title":"Lactate aggravates inflammation through the upregulation of ICAM-1 via GPR81-HSPA12B-mediated signaling in acute lung injury","volume":"137","author":"Chang","year":"2024","journal-title":"Chin Med J"},{"key":"ref12","doi-asserted-by":"publisher","first-page":"500","DOI":"10.1016\/j.joen.2019.01.018","article-title":"Endothelial dysfunction marker variation in Young adults with chronic apical periodontitis before and after endodontic treatment","volume":"45","author":"Bergandi","year":"2019","journal-title":"J Endodont"},{"key":"ref13","doi-asserted-by":"publisher","first-page":"824","DOI":"10.1038\/s41577-023-00894-6","article-title":"The multifunctional protein HMGB1: 50 years of discovery","volume":"23","author":"Tang","year":"2023","journal-title":"Nat Rev Immunol"},{"key":"ref14","doi-asserted-by":"publisher","first-page":"4059","DOI":"10.7150\/thno.84935","article-title":"Soluble CD93 lectin-like domain sequesters HMGB1 to ameliorate inflammatory diseases","volume":"13","author":"Huang","year":"2023","journal-title":"Theranostics"},{"key":"ref15","doi-asserted-by":"publisher","first-page":"1447597","DOI":"10.3389\/fimmu.2024.1447597","article-title":"An early HMGB1 rise 12 hours before creatinine predicts acute kidney injury and multiple organ failure in a smoke inhalation and burn swine model","volume":"15","author":"Yang","year":"2024","journal-title":"Front Immunol"},{"key":"ref16","doi-asserted-by":"publisher","first-page":"402","DOI":"10.1038\/s41392-023-01620-3","article-title":"The IL-17 family in diseases: from bench to bedside","volume":"8","author":"Huangfu","year":"2023","journal-title":"Signal Transduct Target Ther"},{"key":"ref17","doi-asserted-by":"publisher","first-page":"552","DOI":"10.4103\/jisp.jisp_47_21","article-title":"Interleukin-17 levels in gingival crevicular fluid of aggressive periodontitis and chronic periodontitis patients","volume":"26","author":"Wankhede","year":"2022","journal-title":"J Indian Soc Periodontol"},{"key":"ref18","doi-asserted-by":"publisher","first-page":"616","DOI":"10.1007\/s10266-023-00843-8","article-title":"Effects of smoking on the salivary and GCF levels of IL-17 and IL-35 in periodontitis","volume":"112","author":"Taskaldiran","year":"2024","journal-title":"Odontology"},{"key":"ref19","doi-asserted-by":"publisher","first-page":"eaax3519","DOI":"10.1126\/scitranslmed.aax3519","article-title":"Chi3l1\/YKL-40 is controlled by the astrocyte circadian clock and regulates neuroinflammation and Alzheimer's disease pathogenesis","volume":"12","author":"Lananna","year":"2020","journal-title":"Sci Transl Med"},{"key":"ref20","doi-asserted-by":"publisher","first-page":"1240","DOI":"10.1902\/jop.2014.130631","article-title":"Analysis of YKL-40 acute-phase protein and interleukin-6 levels in periodontal disease","volume":"85","author":"Keles","year":"2014","journal-title":"J Periodontol"},{"key":"ref21","doi-asserted-by":"publisher","first-page":"2781","DOI":"10.3390\/cimb45040182","article-title":"Do elevated YKL-40 levels drive the immunosuppressive tumor microenvironment in colorectal Cancer? Assessment of the Association of the Expression of YKL-40, MMP-8, IL17A, and PD-L1 with coexisting type 2 diabetes, obesity, and active smoking","volume":"45","author":"Ochman","year":"2023","journal-title":"Curr Issues Mol Biol"},{"key":"ref22","doi-asserted-by":"publisher","first-page":"2364","DOI":"10.3390\/nu16142364","article-title":"S-Equol ameliorates menopausal osteoarthritis in rats through reducing oxidative stress and cartilage degradation","volume":"16","author":"Hu","year":"2024","journal-title":"Nutrients"},{"key":"ref23","doi-asserted-by":"publisher","first-page":"e2544","DOI":"10.1210\/clinem\/dgae842","article-title":"Estimating net bone formation relative to resorption using reference bone turnover markers","volume":"110","author":"Shieh","year":"2025","journal-title":"J Clin Endocrinol Metab"},{"key":"ref24","doi-asserted-by":"publisher","first-page":"100","DOI":"10.1186\/s11658-024-00614-5","article-title":"New mechanistic understanding of osteoclast differentiation and bone resorption mediated by P2X7 receptors and PI3K-Akt-GSK3\u03b2 signaling","volume":"29","author":"Lu","year":"2024","journal-title":"Cell Mol Biol Lett"},{"key":"ref25","doi-asserted-by":"publisher","first-page":"187","DOI":"10.1177\/00220345211019689","article-title":"LncRNA Nron inhibits bone resorption in periodontitis","volume":"101","author":"Li","year":"2022","journal-title":"J Dent Res"},{"key":"ref26","doi-asserted-by":"publisher","first-page":"619","DOI":"10.1007\/s00223-019-00610-4","article-title":"Does smoking impair bone regeneration in the dental alveolar socket?","volume":"105","author":"Shah","year":"2019","journal-title":"Calcif Tissue Int"},{"key":"ref27","doi-asserted-by":"publisher","first-page":"62","DOI":"10.1038\/s41413-024-00362-4","article-title":"Mapping RANKL- and OPG-expressing cells in bone tissue: the bone surface cells as activators of osteoclastogenesis and promoters of the denosumab rebound effect","volume":"12","author":"El-Masri","year":"2024","journal-title":"Bone Res"},{"key":"ref28","doi-asserted-by":"publisher","first-page":"6910312","DOI":"10.1155\/2020\/6910312","article-title":"RANKL\/RANK\/OPG pathway: a mechanism involved in exercise-induced bone remodeling","volume":"2020","author":"Tobeiha","year":"2020","journal-title":"Biomed Res Int"},{"key":"ref29","doi-asserted-by":"publisher","first-page":"1521","DOI":"10.1002\/jbmr.4897","article-title":"Osteocyte RANKL drives bone resorption in mouse ligature-induced periodontitis","volume":"38","author":"Kittaka","year":"2023","journal-title":"J Bone Miner Res"},{"key":"ref30","doi-asserted-by":"publisher","first-page":"3548","DOI":"10.1021\/pr2012158","article-title":"Smoke-induced signal molecules in bone marrow cells from altered low-density lipoprotein receptor-related protein 5 mice","volume":"11","author":"Ma","year":"2012","journal-title":"J Proteome Res"},{"key":"ref31","doi-asserted-by":"publisher","first-page":"1806","DOI":"10.3390\/ijms23031806","article-title":"The role of matrix metalloproteinases (MMP-8, MMP-9, MMP-13) in periodontal and Peri-implant pathological processes","volume":"23","author":"Luchian","year":"2022","journal-title":"Int J Mol Sci"},{"key":"ref32","doi-asserted-by":"publisher","first-page":"27(7)","DOI":"10.3390\/molecules27072174","article-title":"Salivary MMP-9 levels in chronic periodontitis patients with type-II diabetes mellitus","volume":"27","author":"Arshad","year":"2022","journal-title":"Molecules"},{"key":"ref33","doi-asserted-by":"publisher","first-page":"297","DOI":"10.1186\/s12931-023-02598-w","article-title":"Keratin 15 protects against cigarette smoke-induced epithelial mesenchymal transformation by MMP-9","volume":"24","author":"Zhu","year":"2023","journal-title":"Respir Res"},{"key":"ref34","doi-asserted-by":"publisher","first-page":"603","DOI":"10.1007\/s10654-010-9491-z","article-title":"Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses","volume":"25","author":"Stang","year":"2010","journal-title":"Eur J Epidemiol"},{"key":"ref35","doi-asserted-by":"publisher","first-page":"105280","DOI":"10.1016\/j.archoralbio.2021.105280","article-title":"Moringa oleifera lam. Leaf extract safely inhibits periodontitis by regulating the expression of p38\u03b1\/MAPK14-OPG\/RANKL","volume":"132","author":"Wang","year":"2021","journal-title":"Arch Oral Biol"},{"key":"ref36","volume-title":"Mechanistic links between periodontitis and diabetes","author":"Nadat","year":"2018"},{"key":"ref37","doi-asserted-by":"publisher","first-page":"e12979","DOI":"10.1111\/cmi.12979","article-title":"MiRNA-218 regulates osteoclast differentiation and inflammation response in periodontitis rats through Mmp9","volume":"21","author":"Guo","year":"2019","journal-title":"Cell Microbiol"},{"key":"ref38","doi-asserted-by":"publisher","first-page":"703","DOI":"10.3892\/mmr.2018.9697","article-title":"IL-18 promotes the secretion of matrix metalloproteinases in human periodontal ligament fibroblasts by activating NF-\u03baB signaling","volume":"19","author":"Wang","year":"2019","journal-title":"Mol Med Rep"},{"key":"ref39","article-title":"Relationship of smoking with periodontal tissue inflammation and alveolar bone resorption in patients with chronic periodontitis","author":"Li","year":"2018","journal-title":"J Hainan Med Univ"},{"key":"ref40","doi-asserted-by":"publisher","first-page":"110","DOI":"10.1016\/j.yexmp.2016.07.004","article-title":"The impact of smoking on levels of chronic periodontitis-associated biomarkers","volume":"101","author":"He","year":"2016","journal-title":"Exp Mol Pathol"},{"key":"ref41","first-page":"7147","article-title":"Assessment of salivary interleukin-17 and vitamin d levels in smokers with severe periodontitis patients and healthy individuals","volume":"13","author":"Hussein","year":"2022","journal-title":"J Pharm Negat Results"},{"key":"ref42","doi-asserted-by":"publisher","first-page":"1117","DOI":"10.1007\/s00784-020-03411-4","article-title":"Salivary and serum markers of angiogenesis in periodontitis in relation to smoking","volume":"25","author":"Y\u0131lmaz \u015ea\u015ft\u0131m","year":"2021","journal-title":"Clin Oral 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Periodontol"},{"key":"ref46","first-page":"339","article-title":"Influence of smoking on matrix metalloproteinase-9 in the gingival crevicular fluid","volume":"11","author":"Hwang","year":"2011","journal-title":"J Dent Hyg Sci"},{"key":"ref47","doi-asserted-by":"publisher","first-page":"179","DOI":"10.1515\/ijamh-2022-0081","article-title":"Unpacking the mysteries of puberty among school going adolescents in district of east Khasi Hills, Meghalaya","volume":"35","author":"Ningombam","year":"2023","journal-title":"Int J Adolesc Med Health"},{"key":"ref48","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1046\/j.0904-2512.2001.joptest.doc.x","article-title":"Expression of ICAM-1 and E-selectin in gingival tissues of smokers and non-smokers with periodontitis","volume":"31","author":"Rezavandi","year":"2002","journal-title":"J Oral Pathol Med"},{"key":"ref49","doi-asserted-by":"publisher","first-page":"5195290","DOI":"10.1155\/2018\/5195290","article-title":"HMBG1 as a driver of inflammatory and immune processes in the pathogenesis of ocular diseases","volume":"2018","author":"Liu","year":"2018","journal-title":"J Ophthalmol"},{"key":"ref50","doi-asserted-by":"publisher","first-page":"943","DOI":"10.1177\/0022034510369297","article-title":"IL-17 in sera from patients with aggressive periodontitis","volume":"89","author":"Schenkein","year":"2010","journal-title":"J Dent Res"},{"key":"ref51","doi-asserted-by":"publisher","first-page":"667","DOI":"10.1111\/odi.12334","article-title":"YKL-40 level in gingival crevicular fluid from patients with periodontitis and type 2 diabetes","volume":"21","author":"Kido","year":"2015","journal-title":"Oral Dis"},{"key":"ref52","doi-asserted-by":"publisher","first-page":"933","DOI":"10.1016\/j.jfma.2017.01.006","article-title":"Levels of high-mobility group box-1 in gingival crevicular fluid in nonsmokers and smokers with chronic periodontitis","volume":"116","author":"Lin","year":"2017","journal-title":"J Formos Med Assoc"},{"key":"ref53","doi-asserted-by":"publisher","first-page":"5559","DOI":"10.3390\/app11125559","article-title":"Association of Self-Rated Pain with clinical Peri-implant parameters and cytokine profile in smokers and never smokers with and without Peri-Implantitis","volume":"11","author":"Alshahrani","year":"2021","journal-title":"Appl Sci"},{"key":"ref54","first-page":"1362","article-title":"Circulation levels of YKL-40 and Hs-CRP in stage 3 molar-incisor pattern of periodontitis","volume":"27","author":"Yucel","year":"2021","journal-title":"Ann Med Res"},{"key":"ref55","doi-asserted-by":"publisher","first-page":"128","DOI":"10.1016\/j.archoralbio.2019.04.008","article-title":"MAEA rs6815464 polymorphism and periodontitis in postmenopausal Japanese females: a cross-sectional study","volume":"102","author":"Che","year":"2019","journal-title":"Arch Oral Biol"}],"container-title":["Frontiers in 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