{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,16]],"date-time":"2026-09-16T07:24:06Z","timestamp":1789543446847,"version":"build-2803163510"},"reference-count":39,"publisher":"MDPI AG","issue":"23","license":[{"start":{"date-parts":[[2020,12,6]],"date-time":"2020-12-06T00:00:00Z","timestamp":1607212800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100002322","name":"Coordena\u00e7\u00e3o de Aperfei\u00e7oamento de Pessoal de N\u00edvel Superior","doi-asserted-by":"publisher","award":["PROEX program (grant number 0475\/2019, process number 23038.005614\/2019-74)."],"award-info":[{"award-number":["PROEX program (grant number 0475\/2019, process number 23038.005614\/2019-74)."]}],"id":[{"id":"10.13039\/501100002322","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJERPH"],"abstract":"<jats:p>This study compared the gene expression of the immunoinflammatory markers interleukin (IL)-6, IL-1\u00df, and tumor necrosis factor alpha (TNF-\u03b1), the matrix metalloproteinases (MMP)-1, -2, -8, and -9, and the tissue inhibitors of matrix metalloproteases (TIMP)-1 and -2 in the gingival tissue of individuals with periodontal and peri-implant disease. The study population included individuals with four periodontal statuses: periodontal health (PH group, n = 20); periodontitis (P group, n = 20); peri-implant health (PIH group, n = 20), and peri-implantitis (PI group, n = 20). Gingival biopsies were collected from one tooth per patient according to the inclusion criteria of each group. The mRNA levels of IL-6, IL-1\u00df, TNF-\u03b1, MMP-1, MMP-2, MMP-8, MMP-9, TIMP-1, and TIMP-2 were evaluated by qPCR. The levels of IL-1\u00df were significantly higher in the PI group when compared to the other groups (p &lt; 0.05), while the levels of IL-6 were significantly higher in the groups with periodontal and peri-implant disease when compared with the healthy groups (p &lt; 0.05); however, the levels of IL-6 did not differ between the PI and P groups (p &gt; 0.05). For all other studied biomarkers, no significant differences were observed between groups (p &gt; 0.05). IL-6 and IL-1\u00df presented higher levels of mRNA in diseased periodontal and peri-implant tissues. However, the expression of metalloproteinases and their inhibitors did not differ between the different periodontal statuses.<\/jats:p>","DOI":"10.3390\/ijerph17239100","type":"journal-article","created":{"date-parts":[[2020,12,7]],"date-time":"2020-12-07T12:24:39Z","timestamp":1607343879000},"page":"9100","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":24,"title":["Levels of Gene Expression of Immunological Biomarkers in Peri-Implant and Periodontal Tissues"],"prefix":"10.3390","volume":"17","author":[{"given":"Luciene Cristina","family":"Figueiredo","sequence":"first","affiliation":[{"name":"Dental Research Division, Guarulhos University, S\u00e3o Paulo 07023-070, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3275-5910","authenticated-orcid":false,"given":"Bruno","family":"Bueno-Silva","sequence":"additional","affiliation":[{"name":"Dental Research Division, Guarulhos University, S\u00e3o Paulo 07023-070, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5057-1694","authenticated-orcid":false,"given":"Cristiana Fernandes Plutarco","family":"Nogueira","sequence":"additional","affiliation":[{"name":"Dental Research Division, Guarulhos University, S\u00e3o Paulo 07023-070, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Leonardo Carneiro","family":"Valadares","sequence":"additional","affiliation":[{"name":"Dental Research Division, Guarulhos University, S\u00e3o Paulo 07023-070, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Katia Marina Morilla","family":"Garcia","sequence":"additional","affiliation":[{"name":"Dental Research Division, Guarulhos University, S\u00e3o Paulo 07023-070, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Givelton Coimbra da Luz","family":"Filho","sequence":"additional","affiliation":[{"name":"Dental Research Division, Guarulhos University, S\u00e3o Paulo 07023-070, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Luciano","family":"Milanello","sequence":"additional","affiliation":[{"name":"Dental Research Division, Guarulhos University, S\u00e3o Paulo 07023-070, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Felipe Machado","family":"Esteves","sequence":"additional","affiliation":[{"name":"Dental Research Division, Guarulhos University, S\u00e3o Paulo 07023-070, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1971-0195","authenticated-orcid":false,"given":"Jamil Awad","family":"Shibli","sequence":"additional","affiliation":[{"name":"Dental Research Division, Guarulhos University, S\u00e3o Paulo 07023-070, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tamires Szeremeske","family":"Miranda","sequence":"additional","affiliation":[{"name":"Dental Research Division, Guarulhos University, S\u00e3o Paulo 07023-070, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,12,6]]},"reference":[{"key":"ref_1","first-page":"S286","article-title":"Peri-implant diseases and conditions: Consensus report of workgroup 4 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions","volume":"45","author":"Blanco","year":"2018","journal-title":"J. Clin. Periodontol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"975","DOI":"10.1111\/j.1600-0501.2008.01566.x","article-title":"Composition of supra- and subgingival biofilm of subjects with healthy and diseased implants","volume":"19","author":"Shibli","year":"2008","journal-title":"Clin. Oral Implant. Res."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"e10","DOI":"10.1111\/clr.12846","article-title":"Transforming growth factor-b, interleukin-17, and IL-23 gene expression profiles associated with human peri-implantitis","volume":"28","author":"Mardegan","year":"2017","journal-title":"Clin. Oral Implant. Res."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"689","DOI":"10.1111\/jre.12354","article-title":"Could cytokine levels in the peri-implant crevicular fluid be used to distinguish between healthy implants and implants with peri-implantitis? A systematic review","volume":"51","author":"Duarte","year":"2016","journal-title":"J. Periodontal. Res."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1017\/erm.2013.8","article-title":"Inflammatory mediators in the pathogenesis of periodontitis","volume":"15","author":"Bage","year":"2013","journal-title":"Expert Rev. Mol. Med."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Teixeira, M.K.S., Lira-Junior, R., Louren\u00e7o, E.J.V., Telles, D.M., Bostr\u00f6m, E.A., Figueredo, C.M., and Bostanci, N. (2019). The modulation of the TREM-1\/PGLYRP1\/MMP-8 axis in peri-implant diseases. Clin. Oral Investig.","DOI":"10.1007\/s00784-019-03047-z"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3402\/jom.v3i0.5304","article-title":"Review of osteoimmunology and the host response in endodontic and periodontal lesions","volume":"3","author":"Graves","year":"2011","journal-title":"J. Oral Microbiol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"2067","DOI":"10.1111\/jcmm.12613","article-title":"Do oral bacteria alter the regenerative potential of stem cells? A concise review","volume":"19","author":"Chatzivasileiou","year":"2015","journal-title":"J. Cell. Mol. Med."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Ramenzoni, L., Russo, R., Moccia, M.D., Attin, T., and Schmidlin, P.R. (2019). Periodontal bacterial supernatants modify differentiation, migration and inflammatory cytokine expression in human periodontal. PLoS ONE, 14.","DOI":"10.1371\/journal.pone.0219181"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1283","DOI":"10.1002\/jbm.b.32693","article-title":"Dental implants stimulate expression of Interleukin-8 and its receptor in human blood-An in vitro approach","volume":"100","author":"Quabius","year":"2012","journal-title":"J. Biomed. Mater. Res. B Appl. Biomater."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1111\/j.1600-0757.1998.tb00124.x","article-title":"The diagnosis and treatment of periimplantitis","volume":"17","author":"Mombelli","year":"1998","journal-title":"Periodontol. 2000"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1832","DOI":"10.3892\/etm.2017.4176","article-title":"Identification of key genes and pathways for peri-implantitisthrough the analysis of gene expression data","volume":"13","author":"Zhang","year":"2017","journal-title":"Exp. Ther. Med."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1736","DOI":"10.1902\/jop.2003.74.12.1736","article-title":"Reproducibility of probing depth measurement using a constant-force electronic probe: Analysis of inter- and intraexaminer variability","volume":"74","author":"Araujo","year":"2003","journal-title":"J. Periodontol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"426","DOI":"10.1902\/jop.2011.110324","article-title":"Expression of immune-inflammatory markers in sites of chronic periodontitis in patients with type 2 diabetes","volume":"83","author":"Duarte","year":"2012","journal-title":"J. Periodontol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"292","DOI":"10.1111\/jre.12394","article-title":"Diabetes may affect the expression of matrix metalloproteinases and their inhibitors more than smoking in chronic periodontitis","volume":"52","author":"Bastos","year":"2017","journal-title":"J. Periodontal. Res."},{"key":"ref_16","first-page":"22034520949851","article-title":"Microbial Community-Driven Etiopathogenesis of Peri-Implantitis","volume":"12","author":"Belibasakis","year":"2020","journal-title":"J. Dent. Res."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"e064","DOI":"10.1590\/1807-3107bor-2019.vol33.0064","article-title":"Does subgingival bacterial colonization differ between implants and teeth? A systematic review","volume":"33","author":"Formiga","year":"2019","journal-title":"Braz. Oral Res."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1111\/j.1600-0757.2010.00348.x","article-title":"Comparative biology of chronic and aggressive periodontitis vs. peri-implantitis","volume":"53","author":"Lang","year":"2010","journal-title":"Periodontol. 2000"},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Netea, M.G., Simon, A., van de Veerdonk, F., Kullberg, B.J., Van der Meer, J.W., and Joosten, L.A. (2010). IL-1beta processing in host defense: Beyond the inflammasomes. PLoS Pathog., 6.","DOI":"10.1371\/journal.ppat.1000661"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1055\/s-0040-1712718","article-title":"Cytokines and Chemokines in Periodontitis","volume":"14","author":"Ramadan","year":"2020","journal-title":"Eur. J. Dent."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"190","DOI":"10.1111\/cid.12694","article-title":"Use of IL-1 \u03b2, IL-6, TNF-\u03b1, and MMP-8 biomarkers to distinguish peri-implant diseases: A systematic review and meta-analysis","volume":"21","author":"Ghassib","year":"2019","journal-title":"Clin. Implant. Dent. Relat. Res."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1016\/j.bbamcr.2009.04.003","article-title":"Matrix metalloproteinases: Fold and function of their catalytic domains","volume":"1803","author":"Tallant","year":"2010","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"442","DOI":"10.1046\/j.1524-475X.1999.00442.x","article-title":"Analysis of the acute and chronic wound environments: The role of proteases and their inhibitors","volume":"7","author":"Trengove","year":"1999","journal-title":"Wound Repair Regen."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1334","DOI":"10.1016\/j.biocel.2007.10.024","article-title":"Metalloproteinases and their inhibitors: Regulators of would healing","volume":"40","author":"Gill","year":"2008","journal-title":"Int. J. Biochem. Cell Biol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"955","DOI":"10.1016\/0092-8674(92)90391-O","article-title":"Collagenase expression in the lungs of transgenic mice causes pulmonary emphysema","volume":"71","author":"Dalal","year":"1992","journal-title":"Cell"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1016\/j.ejvs.2004.02.001","article-title":"Elevation in plasma MMP-9 following carotid endarterectomy is associated with particulate cerebral embolisation","volume":"27","author":"Molloy","year":"2004","journal-title":"Eur. J. Vasc. Endovasc. Surg."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"523","DOI":"10.2174\/157340606778250261","article-title":"Matrix metalloproteinase (MMP)-7 activates MMP-8 but not MMP-13","volume":"2","author":"Dozier","year":"2006","journal-title":"Med. Chem."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1007\/s00109-008-0420-5","article-title":"A new redox-dependent mechanism of MMP-1 activity control comprising reduced low-molecular-weight thiols and oxidizing radicals","volume":"87","author":"Koch","year":"2009","journal-title":"J. Mol. Med."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Checchi, V., Maravic, T., Bellini, P., Generali, L., Consolo, U., Breschi, L., and Mazzoni, A. (2020). The Role of Matrix Metalloproteinases in Periodontal Disease. Int. J. Environ. Res. Public Health, 17.","DOI":"10.3390\/ijerph17144923"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1016\/j.cca.2009.09.012","article-title":"Circulating matrix metalloproteinase-8 (MMP-8) and MMP-9 are increased in chronic periodontal disease and decrease after non-surgical periodontal therapy","volume":"409","author":"Marcaccini","year":"2009","journal-title":"Clin. Chim. Acta"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"180","DOI":"10.1111\/j.1600-051X.2009.01512.x","article-title":"Gingival crevicular fluid levels of MMP-8, MMP-9, TIMP-2, and MPO decrease after periodontal therapy","volume":"37","author":"Marcaccini","year":"2010","journal-title":"J. Clin. Periodontol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"487","DOI":"10.1111\/j.1600-051X.2010.01563.x","article-title":"Salivary MMP-8, TIMP-1, and ICTP as markers of advanced periodontitis","volume":"37","author":"Gursoy","year":"2010","journal-title":"J. Clin. Periodontol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1111\/j.1601-0825.2009.01603.x","article-title":"Detection of gingival crevicular fluid MMP-8 levels with different laboratory and chair-side methods","volume":"16","author":"Sorsa","year":"2010","journal-title":"Oral Dis."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1111\/clr.12566","article-title":"Host-derived biomarkers at teeth and implants in partially edentulous patients. A 10-year retrospective study","volume":"27","author":"Ramseier","year":"2016","journal-title":"Clin. Oral Implant. Res."},{"key":"ref_35","first-page":"1306396","article-title":"The Ability of Quantitative, Specific, and Sensitive Point-of-Care\/Chair-Side Oral Fluid Immunotests for aMMP-8 to Detect Periodontal and Peri-Implant Diseases","volume":"5","author":"Alassiri","year":"2018","journal-title":"Dis. Markers"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"430","DOI":"10.1034\/j.1600-0501.2000.011005430.x","article-title":"Tissue inhibitor of metalloproteinases-1, matrix metalloproteinases-1 and -8, and collagenase activity levels in peri-implant crevicular fluid after implantation","volume":"11","author":"Nomura","year":"2000","journal-title":"Clin. Oral Implant. Res."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1016\/j.jpor.2012.07.002","article-title":"Matrix metalloproteinase-8 is the major potential collagenase in active peri-implantitis","volume":"56","author":"Arakawa","year":"2012","journal-title":"J. Prosthodont. Res."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1007\/s00784-015-1501-9","article-title":"Correlation between peri-implantar sulcular fluid rate and expression of collagenase2 (MMP8)","volume":"20","author":"Janska","year":"2016","journal-title":"Clin. Oral Investig."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Kensara, A., Hefni, E., Williams, M.A., Saito, H., Mongodin, E., and Masri, R. (2020). Microbiological Profile and Human Immune Response Associated with Peri-Implantitis: A Systematic Review. J. Prosthodont., 5.","DOI":"10.1111\/jopr.13270"}],"container-title":["International Journal of Environmental Research and Public Health"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1660-4601\/17\/23\/9100\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T10:41:33Z","timestamp":1760179293000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1660-4601\/17\/23\/9100"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,12,6]]},"references-count":39,"journal-issue":{"issue":"23","published-online":{"date-parts":[[2020,12]]}},"alternative-id":["ijerph17239100"],"URL":"https:\/\/doi.org\/10.3390\/ijerph17239100","relation":{},"ISSN":["1660-4601"],"issn-type":[{"value":"1660-4601","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,12,6]]}}}