{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,12]],"date-time":"2025-10-12T02:28:26Z","timestamp":1760236106187,"version":"build-2065373602"},"reference-count":49,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2021,10,27]],"date-time":"2021-10-27T00:00:00Z","timestamp":1635292800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Life"],"abstract":"<jats:p>Background: Systemic scleroderma (SSc) has multiple orofacial effects. The aim of this study was to analyze the expression of inflammatory mediators in biofilm samples. It was hypothesized that different expression levels and clinical associations might be drawn. Methods: A total of 39 biofilm samples from group 1 = SSc and group 2 = healthy control were examined for the expression levels of interleukin (IL)-2,-6, and -10; matrix metalloprotease (MMP)-9; and surface antigens CD90 and CD34 by quantitative real-time PCR and clinical parameters. Relative quantitative (RQ) gene expression was determined using the \u2206\u2206CT method. Results: The mean bleeding on probing values (p = 0.006), clinical attachment loss (CAL) (p = 0.009), gingival recession (p = 0.020), limited mouth opening (p = 0.001) and cervical tooth defects (p = 0.011) were significantly higher in group 1. RQ expressions of IL-2 and CD34 were significantly lower, IL-6, MMP-9, and CD90 were significantly higher. There was a significant positive correlation of IL-6\/MMP-9 and negative correlation of mouth opening\/CAL and IL-6\/CAL. Conclusion: Different expression levels of IL-2, IL-6, MMP-9, CD34 and CD90 were detected in biofilm samples from patients with SSc compared to control. An immunological correlation to the clinical parameters of mouth opening and CAL was shown; thus, we conclude that SSc might have an impact on periodontal tissues.<\/jats:p>","DOI":"10.3390\/life11111145","type":"journal-article","created":{"date-parts":[[2021,10,27]],"date-time":"2021-10-27T23:24:42Z","timestamp":1635377082000},"page":"1145","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Investigation of the Expression of Inflammatory Markers in Oral Biofilm Samples in Patients with Systemic Scleroderma and the Association with Clinical Periodontal Parameters\u2014A Preliminary Study"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8295-9714","authenticated-orcid":false,"given":"Mayte","family":"Buchbender","sequence":"first","affiliation":[{"name":"Department of Oral and Maxillofacial Surgery, University of Erlangen-Nuremberg, 91054 Erlangen, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Amelie","family":"Lugenb\u00fchl","sequence":"additional","affiliation":[{"name":"Department of Oral and Maxillofacial Surgery, University of Erlangen-Nuremberg, 91054 Erlangen, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jakob","family":"Fehlhofer","sequence":"additional","affiliation":[{"name":"Department of Oral and Maxillofacial Surgery, University of Erlangen-Nuremberg, 91054 Erlangen, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9473-8724","authenticated-orcid":false,"given":"Christian","family":"Kirschneck","sequence":"additional","affiliation":[{"name":"Department of Orthodontics, University of Regensburg, 93053 Regensburg, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5778-2742","authenticated-orcid":false,"given":"Jutta","family":"Ries","sequence":"additional","affiliation":[{"name":"Department of Oral and Maxillofacial Surgery, University of Erlangen-Nuremberg, 91054 Erlangen, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0199-9437","authenticated-orcid":false,"given":"Rainer","family":"Lutz","sequence":"additional","affiliation":[{"name":"Department of Oral and Maxillofacial Surgery, University of Erlangen-Nuremberg, 91054 Erlangen, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Michael","family":"Sticherling","sequence":"additional","affiliation":[{"name":"Department of Dermatology, University of Erlangen-Nuremberg, 91054 Erlangen, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Marco Rainer","family":"Kesting","sequence":"additional","affiliation":[{"name":"Department of Oral and Maxillofacial Surgery, University of Erlangen-Nuremberg, 91054 Erlangen, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2021,10,27]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"418","DOI":"10.1111\/scd.12492","article-title":"Systemic Sclerosis: Update for Oral Health Care Providers","volume":"40","author":"Alhendi","year":"2020","journal-title":"Spec. Care Dentist."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1007\/s00281-015-0499-z","article-title":"Genetics of Systemic Sclerosis","volume":"37","author":"Mayes","year":"2015","journal-title":"Semin. Immunopathol."},{"key":"ref_3","first-page":"705","article-title":"Systemic Sclerosis-Dermatological Aspects. Part 1: Pathogenesis, Epidemiology, Clinical Findings","volume":"10","author":"Sticherling","year":"2012","journal-title":"J. Dtsch. Dermatol. Ges."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"A311","DOI":"10.1016\/j.autrev.2009.11.003","article-title":"Geoepidemiology of Systemic Sclerosis","volume":"9","author":"Ranque","year":"2010","journal-title":"Autoimmun. Rev."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1093\/qjmed\/hcp174","article-title":"Improved Survival in Systemic Sclerosis Is Associated with Better Ascertainment of Internal Organ Disease: A Retrospective Cohort Study","volume":"103","author":"Nihtyanova","year":"2010","journal-title":"QJM Int. J. Med."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1087","DOI":"10.1016\/j.autrev.2015.07.012","article-title":"Quality of Life in Systemic Sclerosis","volume":"14","author":"Almeida","year":"2015","journal-title":"Autoimmun. Rev."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1454","DOI":"10.1093\/rheumatology\/keu530","article-title":"Performance of the New Acr\/Eular Classification Criteria for Systemic Sclerosis in Clinical Practice","volume":"54","author":"Jordan","year":"2015","journal-title":"Rheumatology"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"502","DOI":"10.3892\/ijmm.2012.1024","article-title":"Immunohistochemical Analysis of Tgf-Beta1 and Vegf in Gingival and Periodontal Tissues: A Role of These Biomarkers in the Pathogenesis of Scleroderma and Periodontal Disease","volume":"30","author":"Matarese","year":"2012","journal-title":"Int. J. Mol. Med."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/j.berh.2012.01.011","article-title":"Scleroderma-New Aspects in Pathogenesis and Treatment","volume":"26","year":"2012","journal-title":"Best Pract. Res. Clin. Rheumatol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1016\/j.imlet.2018.03.011","article-title":"Different Profile of Cytokine Production in Patients with Systemic Sclerosis and Association with Clinical Manifestations","volume":"198","author":"Dantas","year":"2018","journal-title":"Immunol. Lett."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"R157","DOI":"10.1186\/ar4672","article-title":"Targeting Il-6 by Both Passive or Active Immunization Strategies Prevents Bleomycin-Induced Skin Fibrosis","volume":"16","author":"Desallais","year":"2014","journal-title":"Arthritis Res. Ther."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1235","DOI":"10.1136\/annrheumdis-2011-200955","article-title":"Clinical and Pathological Significance of Interleukin 6 Overexpression in Systemic Sclerosis","volume":"71","author":"Khan","year":"2012","journal-title":"Ann. Rheum. Dis."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1097\/RHU.0000000000001112","article-title":"Vitamin D and Cytokine Profiles in Patients with Systemic Sclerosis","volume":"26","author":"Hax","year":"2020","journal-title":"J. Clin. Rheumatol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1038\/nri3785","article-title":"Periodontitis: From Microbial Immune Subversion to Systemic Inflammation","volume":"15","author":"Hajishengallis","year":"2015","journal-title":"Nat. Rev. Immunol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"208","DOI":"10.1016\/j.semarthrit.2014.05.010","article-title":"Mortality and Survival in Systemic Sclerosis: Systematic Review and Meta-Analysis","volume":"44","author":"Royo","year":"2014","journal-title":"Semin. Arthritis Rheum."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"808","DOI":"10.1111\/jop.12739","article-title":"Impact of Systemic Sclerosis Oral Manifestations on Patients\u2019 Health-Related Quality of Life: A Systematic Review","volume":"47","author":"Smirani","year":"2018","journal-title":"J. Oral Pathol. Med."},{"key":"ref_17","first-page":"549","article-title":"Periodontal Conditions and Tumor Necrosis Factor-Alpha Level in Gingival Crevicular Fluid of Scleroderma Patients","volume":"17","author":"Elimelech","year":"2015","journal-title":"Isr. Med. Assoc. J."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1034\/j.1600-0757.2003.03107.x","article-title":"Proteolytic and Hydrolytic Enzymes from Putative Periodontal Pathogens: Characterization, Molecular Genetics, Effects on Host Defenses and Tissues and Detection in Gingival Crevice Fluid","volume":"31","author":"Eley","year":"2003","journal-title":"Periodontology"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"S135","DOI":"10.4103\/JPBS.JPBS_56_19","article-title":"Gingival Crevicular Fluid: An Overview","volume":"11","author":"Subbarao","year":"2019","journal-title":"J. Pharm. Bioallied Sci."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Zijnge, V., van Leeuwen, M.B., Degener, J.E., Abbas, F., Thurnheer, T., Gmur, R., and Harmsen, H.J. (2010). Oral Biofilm Architecture on Natural Teeth. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0009321"},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Buchbender, M., Fehlhofer, J., Proff, P., Most, T., Ries, J., Hannig, M., Neurath, M.F., Gund, M., Atreya, R., and Kesting, M. (2021). Expression of Inflammatory Mediators in Biofilm Samples and Clinical Association in Inflammatory Bowel Disease Patients-a Preliminary Study. Clin. Oral Investig., open access.","DOI":"10.1007\/s00784-021-04093-2"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"704","DOI":"10.1016\/j.ijom.2011.02.026","article-title":"Temporomandibular Joint Involvement in Rheumatoid Arthritis, Systemic Lupus Erythematosus and Systemic Sclerosis","volume":"40","author":"Aliko","year":"2011","journal-title":"Int. J. Oral Maxillofac. Surg."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"11","DOI":"10.5301\/jsrd.5000231","article-title":"Standardization of the Modified Rodnan Skin Score for Use in Clinical Trials of Systemic Sclerosis","volume":"2","author":"Khanna","year":"2017","journal-title":"J. Scleroderma Relat. Disord."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1551596","DOI":"10.1080\/20022727.2018.1551596","article-title":"Microcosm Biofilms Cultured from Different Oral Niches in Periodontitis Patients","volume":"11","author":"Cieplik","year":"2019","journal-title":"J. Oral Microbiol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1007\/s00393-009-0560-1","article-title":"Pathogenesis of Parodontitis in Rheumatic Diseases","volume":"69","author":"Detert","year":"2010","journal-title":"Z. Fur. Rheumatol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"2733","DOI":"10.1007\/s10067-017-3861-9","article-title":"Risk Association between Scleroderma Disease Characteristics, Periodontitis, and Tooth Loss","volume":"36","author":"Isola","year":"2017","journal-title":"Clin. Rheumatol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"300060520941375","DOI":"10.1177\/0300060520941375","article-title":"Reduced Salivary Flow and Caries Status Are Correlated with Disease Activity and Severity in Patients with Diffuse Cutaneous Systemic Sclerosis","volume":"48","author":"Parat","year":"2020","journal-title":"J. Int. Med. Res."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"763","DOI":"10.1902\/jop.2016.150475","article-title":"Increased Periodontal Attachment Loss in Patients with Systemic Sclerosis","volume":"87","author":"Pischon","year":"2016","journal-title":"J. Periodontol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1097","DOI":"10.1902\/jop.2010.100593","article-title":"Periodontal Status of Adults with Systemic Sclerosis: Case-Control Study","volume":"82","author":"Leung","year":"2011","journal-title":"J. Periodontol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"104957","DOI":"10.1016\/j.archoralbio.2020.104957","article-title":"Cytokine Profiles of Healthy and Diseased Sites in Individuals with Periodontitis","volume":"120","author":"Miranda","year":"2020","journal-title":"Arch. Oral Biol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"641","DOI":"10.1007\/s00784-018-2471-5","article-title":"The Ratios of Pro-Inflammatory to Anti-Inflammatory Cytokines in the Serum of Chronic Periodontitis Patients with and without Type 2 Diabetes and\/or Smoking Habit","volume":"23","author":"Miranda","year":"2019","journal-title":"Clin. Oral Investig."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"713","DOI":"10.1111\/jre.12438","article-title":"The Effect of Smoking on Inflammatory and Bone Remodeling Markers in Gingival Crevicular Fluid and Subgingival Microbiota Following Periodontal Therapy","volume":"52","author":"Bunaes","year":"2017","journal-title":"J. Periodontal. Res."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"155197","DOI":"10.1016\/j.cyto.2020.155197","article-title":"Chemokines and Cytokines Profile in Whole Saliva of Patients with Periodontitis","volume":"135","author":"Kawamoto","year":"2020","journal-title":"Cytokine"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"853","DOI":"10.1111\/jcpe.12286","article-title":"Cytokine Gene Expression Profiles During Initiation, Progression and Resolution of Periodontitis","volume":"41","author":"Ebersole","year":"2014","journal-title":"J. Clin. Periodontol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1362","DOI":"10.1136\/annrheumdis-2018-213031","article-title":"Therapeutic Interleukin-6 Blockade Reverses Transforming Growth Factor-Beta Pathway Activation in Dermal Fibroblasts: Insights from the Fasscinate Clinical Trial in Systemic Sclerosis","volume":"77","author":"Denton","year":"2018","journal-title":"Ann. Rheum. Dis."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"480","DOI":"10.1007\/s11596-008-0424-y","article-title":"Expression of Mmp-9 and Timp-1 in Lesions of Systemic Sclerosis and Its Implications","volume":"28","author":"Meng","year":"2008","journal-title":"J. Huazhong Univ. Sci. Technolog. Med. Sci."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1185\/030079905X30680","article-title":"The Effect of Bosentan on Matrix Metalloproteinase-9 Levels in Patients with Systemic Sclerosis-Induced Pulmonary Hypertension","volume":"21","author":"Giannelli","year":"2005","journal-title":"Curr. Med. Res. Opin."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1046\/j.1365-2230.2002.01011.x","article-title":"Decreased Mmp-9 Activity in the Serum of Patients with Diffuse Cutaneous Systemic Sclerosis","volume":"27","author":"Kikuchi","year":"2002","journal-title":"Clin. Exp. Dermatol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1191","DOI":"10.1111\/jcpe.13349","article-title":"Diagnostic and Prognostic Ability of Salivary Mmp-9 and S100a8 for Periodontitis","volume":"47","author":"Kim","year":"2020","journal-title":"J. Clin. Periodontol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1398","DOI":"10.1902\/jop.2001.72.10.1398","article-title":"Is Collagen Breakdown During Periodontitis Linked to Inflammatory Cells and Expression of Matrix Metalloproteinases and Tissue Inhibitors of Metalloproteinases in Human Gingival Tissue?","volume":"72","author":"Seguier","year":"2001","journal-title":"J. Periodontol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1016\/j.adaj.2018.08.025","article-title":"Meta-Analysis of the Association between Serum and Gingival Crevicular Fluid Matrix Metalloproteinase-9 and Periodontitis","volume":"150","author":"Yang","year":"2019","journal-title":"J. Am. Dent. Assoc."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1111\/jop.12978","article-title":"Clinicopathological and Immunohistochemical Features of the Oral Lymphoepithelial Cyst: A Multicenter Study","volume":"49","author":"Coelho","year":"2020","journal-title":"J. Oral Pathol. Med."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"2208","DOI":"10.1111\/jdv.15120","article-title":"Cd34 Stromal Expression Is Inversely Proportional to Smooth Muscle Actin Expression and Extent of Morphea","volume":"32","author":"Lee","year":"2018","journal-title":"J. Eur. Acad. Dermatol. Venereol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"2650","DOI":"10.1016\/j.ajpath.2016.06.020","article-title":"Altered Dermal Fibroblasts in Systemic Sclerosis Display Podoplanin and Cd90","volume":"186","author":"Nazari","year":"2016","journal-title":"Am. J. Pathol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"390","DOI":"10.1038\/nrrheum.2014.53","article-title":"Fibrosis--a Lethal Component of Systemic Sclerosis","volume":"10","author":"Ho","year":"2014","journal-title":"Nat. Rev. Rheumatol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1111\/jre.12635","article-title":"Immunohistochemical Study of Cd34 and Podoplanin in Periodontal Disease","volume":"54","author":"Goncalves","year":"2019","journal-title":"J. Periodontal Res."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"140","DOI":"10.1016\/S0923-1811(01)00128-1","article-title":"Serum Levels of Interleukin-6 and Interleukin-10 Correlate with Total Skin Thickness Score in Patients with Systemic Sclerosis","volume":"27","author":"Sato","year":"2001","journal-title":"J. Dermatol. Sci."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1740","DOI":"10.1016\/j.joen.2017.03.040","article-title":"External Cervical Resorption: A New Oral Manifestation of Systemic Sclerosis","volume":"43","author":"Bucchi","year":"2017","journal-title":"J. Endod."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"673","DOI":"10.1002\/acr.22739","article-title":"Relationship between Disease Characteristics and Oral Radiologic Findings in Systemic Sclerosis: Results from a Canadian Oral Health Study","volume":"68","author":"Baron","year":"2016","journal-title":"Arthritis Care Res."}],"container-title":["Life"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2075-1729\/11\/11\/1145\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T07:21:24Z","timestamp":1760167284000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2075-1729\/11\/11\/1145"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,10,27]]},"references-count":49,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2021,11]]}},"alternative-id":["life11111145"],"URL":"https:\/\/doi.org\/10.3390\/life11111145","relation":{},"ISSN":["2075-1729"],"issn-type":[{"type":"electronic","value":"2075-1729"}],"subject":[],"published":{"date-parts":[[2021,10,27]]}}}