{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,25]],"date-time":"2026-08-25T17:20:38Z","timestamp":1787678438324,"version":"build-2784847793"},"reference-count":50,"publisher":"MDPI AG","issue":"10","license":[{"start":{"date-parts":[[2024,9,24]],"date-time":"2024-09-24T00:00:00Z","timestamp":1727136000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Periodontitis is associated with systemic chronic inflammatory diseases. There is limited evidence on the influence of anti-cytokine therapies on the periodontal condition and microbiome in the tooth pocket of such patients, so the aim of this study was to elucidate this issue. In this observational trial, the periodontal status and the gingival crevicular fluid of 13 patients with different chronic inflammatory diseases were obtained before the initiation of anti-cytokine treatment and 14 weeks after. Gingival crevicular fluid was collected for 16S rRNA gene sequencing from a clinically healthy tooth and the deepest measured pocket. The Shannon Diversity Index significantly increased in the deepest pockets of patients (p = 0.039). The data showed alterations in the diversity of the subgingival microbiome over the course of the study, implying a shift towards a healthier condition after starting anti-cytokine therapy. Additional investigations are needed to analyze whether the administration of selective biologicals can improve periodontal conditions in patients with or without chronic inflammatory diseases.<\/jats:p>","DOI":"10.3390\/microorganisms12101934","type":"journal-article","created":{"date-parts":[[2024,9,24]],"date-time":"2024-09-24T08:54:17Z","timestamp":1727168057000},"page":"1934","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Changes in Periodontal Parameters and Microbiome Composition of Periodontal Pocket in Patients with Chronic Inflammatory Diseases Receiving Targeted Anti-Cytokine Therapy"],"prefix":"10.3390","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-4737-5953","authenticated-orcid":false,"given":"Juliane","family":"Wagner","sequence":"first","affiliation":[{"name":"Department of Oral and Maxillofacial Surgery, University-Hospital Schleswig-Holstein, Campus Kiel, 24105 Kiel, Germany"},{"name":"Cluster of Excellence, Precision Medicine in Inflammation, Christian-Albrechts-University of Kiel, 24105 Kiel, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Luisa","family":"Haker","sequence":"additional","affiliation":[{"name":"Department of Oral and Maxillofacial Surgery, University-Hospital Schleswig-Holstein, Campus Kiel, 24105 Kiel, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4180-6548","authenticated-orcid":false,"given":"Louisa","family":"Mewes","sequence":"additional","affiliation":[{"name":"Department of Prosthodontics, Geriatric Dentistry and Craniomandibular Disorders, Charit\u00e9-Universit\u00e4tsmedizin Berlin, Corporate Member of Freie Universit\u00e4t Berlin, Berlin Institute of Health, Humboldt-Universit\u00e4t zu Berlin, 14197 Berlin, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Corinna","family":"Bang","sequence":"additional","affiliation":[{"name":"Cluster of Excellence, Precision Medicine in Inflammation, Christian-Albrechts-University of Kiel, 24105 Kiel, Germany"},{"name":"Institute of Clinical Molecular Biology, Christian-Albrechts-University of Kiel, 24105 Kiel, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Malte","family":"R\u00fchlemann","sequence":"additional","affiliation":[{"name":"Cluster of Excellence, Precision Medicine in Inflammation, Christian-Albrechts-University of Kiel, 24105 Kiel, Germany"},{"name":"Institute of Clinical Molecular Biology, Christian-Albrechts-University of Kiel, 24105 Kiel, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hendrik","family":"Naujokat","sequence":"additional","affiliation":[{"name":"Department of Oral and Maxillofacial Surgery, University-Hospital Schleswig-Holstein, Campus Kiel, 24105 Kiel, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Johannes Heinrich","family":"Spille","sequence":"additional","affiliation":[{"name":"Department of Oral and Maxillofacial Surgery, University-Hospital Schleswig-Holstein, Campus Kiel, 24105 Kiel, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2544-4460","authenticated-orcid":false,"given":"Wolfgang","family":"Lieb","sequence":"additional","affiliation":[{"name":"Institute of Epidemiology, Christian-Albrechts-University of Kiel, 24105 Kiel, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andre","family":"Franke","sequence":"additional","affiliation":[{"name":"Cluster of Excellence, Precision Medicine in Inflammation, Christian-Albrechts-University of Kiel, 24105 Kiel, Germany"},{"name":"Institute of Clinical Molecular Biology, Christian-Albrechts-University of Kiel, 24105 Kiel, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stefan","family":"Schreiber","sequence":"additional","affiliation":[{"name":"Cluster of Excellence, Precision Medicine in Inflammation, Christian-Albrechts-University of Kiel, 24105 Kiel, Germany"},{"name":"Institute of Clinical Molecular Biology, Christian-Albrechts-University of Kiel, 24105 Kiel, Germany"},{"name":"Department of Internal Medicine I, University-Hospital Schleswig-Holstein, Campus Kiel, 24105 Kiel, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Matthias","family":"Laudes","sequence":"additional","affiliation":[{"name":"Cluster of Excellence, Precision Medicine in Inflammation, Christian-Albrechts-University of Kiel, 24105 Kiel, Germany"},{"name":"Department of Internal Medicine I, University-Hospital Schleswig-Holstein, Campus Kiel, 24105 Kiel, Germany"},{"name":"Institute of Diabetes and Clinical Metabolic Research, University-Hospital Schleswig-Holstein, Campus Kiel, 24105 Kiel, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christof","family":"D\u00f6rfer","sequence":"additional","affiliation":[{"name":"Clinic of Conservative Dentistry and Periodontology, University-Hospital Schleswig-Holstein, Campus Kiel, 24105 Kiel, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"J\u00f6rg","family":"Wiltfang","sequence":"additional","affiliation":[{"name":"Department of Oral and Maxillofacial Surgery, University-Hospital Schleswig-Holstein, Campus Kiel, 24105 Kiel, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8316-0565","authenticated-orcid":false,"given":"Christian","family":"Graetz","sequence":"additional","affiliation":[{"name":"Clinic of Conservative Dentistry and Periodontology, University-Hospital Schleswig-Holstein, Campus Kiel, 24105 Kiel, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4622-6051","authenticated-orcid":false,"given":"Dominik Maria","family":"Schulte","sequence":"additional","affiliation":[{"name":"Cluster of Excellence, Precision Medicine in Inflammation, Christian-Albrechts-University of Kiel, 24105 Kiel, Germany"},{"name":"Department of Internal Medicine I, University-Hospital Schleswig-Holstein, Campus Kiel, 24105 Kiel, Germany"},{"name":"Institute of Diabetes and Clinical Metabolic Research, University-Hospital Schleswig-Holstein, Campus Kiel, 24105 Kiel, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,9,24]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"25","DOI":"10.4110\/in.2017.17.1.25","article-title":"Pathogenesis of Inflammatory Bowel Disease and Recent Advances in Biologic Therapies","volume":"17","author":"Kim","year":"2017","journal-title":"Immune Netw."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"91","DOI":"10.3748\/wjg.v20.i1.91","article-title":"Inflammatory Bowel Disease: Pathogenesis","volume":"20","author":"Zhang","year":"2014","journal-title":"World J. Gastroenterol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1094","DOI":"10.1016\/S0140-6736(10)60826-4","article-title":"Rheumatoid Arthritis","volume":"376","author":"Scott","year":"2010","journal-title":"Lancet"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1016\/j.semarthrit.2016.05.012","article-title":"Psoriasis, Psoriatic Arthritis, and Rheumatoid Arthritis: Is All Inflammation the Same?","volume":"46","author":"Coates","year":"2016","journal-title":"Semin. Arthritis Rheum."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1056\/NEJM199901143400207","article-title":"Atherosclerosis\u2014An Inflammatory Disease","volume":"340","author":"Ross","year":"1999","journal-title":"N. Engl. J. Med."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1038\/nature21363","article-title":"Inflammation, Metaflammation and Immunometabolic Disorders","volume":"542","author":"Hotamisligil","year":"2017","journal-title":"Nature"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"860","DOI":"10.1038\/nature05485","article-title":"Inflammation and Metabolic Disorders","volume":"444","author":"Hotamisligil","year":"2006","journal-title":"Nature"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1007\/s00125-011-2342-y","article-title":"Periodontitis and Diabetes: A Two-Way Relationship","volume":"55","author":"Preshaw","year":"2012","journal-title":"Diabetologia"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"259074","DOI":"10.1155\/2015\/259074","article-title":"Relationship between Periodontitis and Rheumatoid Arthritis: Review of the Literature","volume":"2015","author":"Melo","year":"2015","journal-title":"Mediat. Inflamm."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"757","DOI":"10.1111\/jdv.14249","article-title":"Periodontitis and Risk of Psoriasis: Another Comorbidity","volume":"31","author":"Christophers","year":"2017","journal-title":"J. Eur. Acad. Dermatol. Venereol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"382","DOI":"10.1111\/jcpe.12698","article-title":"Inflammatory Bowel Disease and Oral Health: Systematic Review and a Meta-Analysis","volume":"44","author":"Papageorgiou","year":"2017","journal-title":"J. Clin. Periodontol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"606","DOI":"10.1038\/nrrheum.2017.132","article-title":"The Case for Periodontitis in the Pathogenesis of Rheumatoid Arthritis","volume":"13","author":"Potempa","year":"2017","journal-title":"Nat. Rev. Rheumatol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1111\/prd.12221","article-title":"Periodontitis: Facts, Fallacies and the Future","volume":"75","author":"Slots","year":"2017","journal-title":"Periodontol. 2000"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"857","DOI":"10.1111\/jdv.14051","article-title":"Periodontitis and Risk of Psoriasis: A Systematic Review and Meta-Analysis","volume":"31","author":"Ungprasert","year":"2017","journal-title":"J. Eur. Acad. Dermatol. Venereol."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Holmstrup, P., Damgaard, C., Olsen, I., Klinge, B., Flyvbjerg, A., Nielsen, C.H., and Hansen, P.R. (2017). Comorbidity of Periodontal Disease: Two Sides of the Same Coin? An Introduction for the Clinician. J. Oral. Microbiol., 9.","DOI":"10.1080\/20002297.2017.1332710"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1111\/prd.12147","article-title":"Microbial Colonization of the Periodontal Pocket and Its Significance for Periodontal Therapy","volume":"76","author":"Mombelli","year":"2018","journal-title":"Periodontol. 2000"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1111\/j.1600-0765.1991.tb02067.x","article-title":"Black-Pigmenting Gram-Negative Bacteria in Periodontal Disease. I. Topographic Distribution in the Human Dentition","volume":"26","author":"Mombelli","year":"1991","journal-title":"J. Periodontal Res."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"S173","DOI":"10.1002\/JPER.17-0721","article-title":"Periodontitis: Consensus Report of Workgroup 2 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions","volume":"89","author":"Papapanou","year":"2018","journal-title":"J. Periodontol."},{"key":"ref_19","first-page":"177","article-title":"Experimental Gingivitis in Man","volume":"36","author":"Loe","year":"1965","journal-title":"J. Periodontol. 1930"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"176","DOI":"10.1177\/08959374970110010901","article-title":"Physiological approaches to the control of oral biofilms","volume":"11","author":"Marsh","year":"1997","journal-title":"Adv. Dent. Res."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"134","DOI":"10.1111\/j.1600-051X.1998.tb02419.x","article-title":"Microbial Complexes in Subgingival Plaque","volume":"25","author":"Socransky","year":"1998","journal-title":"J. Clin. Periodontol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1111\/prd.12010","article-title":"Lessons Learned and Unlearned in Periodontal Microbiology","volume":"62","author":"Teles","year":"2013","journal-title":"Periodontol. 2000"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"172","DOI":"10.1016\/j.molmed.2014.11.004","article-title":"Polymicrobial Synergy and Dysbiosis in Inflammatory Disease","volume":"21","author":"Lamont","year":"2015","journal-title":"Trends Mol. Med."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1111\/prd.12002","article-title":"Inflammatory and Immune Pathways in the Pathogenesis of Periodontal Disease","volume":"64","author":"Cekici","year":"2014","journal-title":"Periodontol. 2000"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1111\/j.1600-051X.2005.00684.x","article-title":"Levels of Interleukin-17 in Gingival Crevicular Fluid and in Supernatants of Cellular Cultures of Gingival Tissue from Patients with Chronic Periodontitis","volume":"32","author":"Vernal","year":"2005","journal-title":"J. Clin. Periodontol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"633","DOI":"10.1177\/0022034509339889","article-title":"The Involvement of IL-23 and the Th17 Pathway in Periodontitis","volume":"88","author":"Ohyama","year":"2009","journal-title":"J. Dent. Res."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1111\/j.1600-0722.2011.00842.x","article-title":"Effect of Interleukin-17 on the Expression of Chemokines in Gingival Epithelial Cells","volume":"119","author":"Takahashi","year":"2011","journal-title":"Eur. J. Oral. Sci."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/j.it.2013.09.001","article-title":"Immunomicrobial Pathogenesis of Periodontitis: Keystones, Pathobionts, and Host Response","volume":"35","author":"Hajishengallis","year":"2014","journal-title":"Trends Immunol."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Bunte, K., and Beikler, T. (2019). Th17 Cells and the IL-23\/IL-17 Axis in the Pathogenesis of Periodontitis and Immune-Mediated Inflammatory Diseases. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20143394"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1111\/jcpe.12837","article-title":"A Systematic Review and Meta-Analysis of Epidemiologic Observational Evidence on the Effect of Periodontitis on Diabetes an Update of the EFP-AAP Review","volume":"45","author":"Graziani","year":"2018","journal-title":"J. Clin. Periodontol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"S24","DOI":"10.1902\/jop.2013.1340019","article-title":"Periodontitis and Atherosclerotic Cardiovascular Disease: Consensus Report of the Joint Efp\/Aapworkshop on Periodontitis and Systemic Diseases","volume":"84","author":"Tonetti","year":"2013","journal-title":"J. Periodontol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"S74","DOI":"10.1002\/JPER.17-0719","article-title":"Periodontal Health and Gingival Diseases and Conditions on an Intact and a Reduced Periodontium: Consensus Report of Workgroup 1 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions","volume":"89","author":"Chapple","year":"2018","journal-title":"J. Periodontol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"S159","DOI":"10.1002\/JPER.18-0006","article-title":"Staging and Grading of Periodontitis: Framework and Proposal of a New Classification and Case Definition","volume":"89","author":"Tonetti","year":"2018","journal-title":"J. Periodontol."},{"key":"ref_34","first-page":"11","article-title":"The Role of Occlusion in Periodontal Disease and the Biological Rationale for Splinting in Treatment of Periodontitis","volume":"10","author":"Lindhe","year":"1977","journal-title":"Oral. Sci. Rev."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"D633","DOI":"10.1093\/nar\/gkt1244","article-title":"Ribosomal Database Project: Data and Tools for High Throughput Rrna Analysis","volume":"42","author":"Cole","year":"2014","journal-title":"Nucleic Acids Res."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1149","DOI":"10.3758\/BRM.41.4.1149","article-title":"Statistical Power Analyses Using G*Power 3.1: Tests for Correlation and Regression Analyses","volume":"41","author":"Faul","year":"2009","journal-title":"Behav. Res. Methods"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"175","DOI":"10.3758\/BF03193146","article-title":"G*Power 3: A Flexible Statistical Power Analysis Program for the Social, Behavioral, and Biomedical Sciences","volume":"39","author":"Faul","year":"2007","journal-title":"Behav. Res. Methods"},{"key":"ref_38","first-page":"32","article-title":"A New Method for Non-Parametric Multivariate Analysis of Variance","volume":"26","author":"Anderson","year":"2001","journal-title":"Austral Ecol."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"McMurdie, P.J., and Holmes, S. (2013). Phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0061217"},{"key":"ref_40","first-page":"732","article-title":"Vegan: Community Ecology Package. R Package Version 2.5-6. 2019","volume":"8","author":"Oksanen","year":"2020","journal-title":"Community Ecol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"122","DOI":"10.1111\/adj.12684","article-title":"Interaction of Biologic Therapy with Apical Periodontitis and Periodontitis: A Systematic Review","volume":"64","author":"Peddis","year":"2019","journal-title":"Aust. Dent. J."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Shi, M., Wei, Y., Hu, W., Nie, Y., Wu, X., and Lu, R. (2018). The Subgingival Microbiome of Periodontal Pockets with Different Probing Depths in Chronic and Aggressive Periodontitis: A Pilot Study. Front. Cell Infect. Microbiol., 8.","DOI":"10.3389\/fcimb.2018.00124"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"500","DOI":"10.1093\/rheumatology\/keu356","article-title":"A Possible Link between Ankylosing Spondylitis and Periodontitis: A Systematic Review and Meta-Analysis","volume":"54","author":"Ratz","year":"2015","journal-title":"Rheumatology"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1237","DOI":"10.1016\/j.jid.2018.12.014","article-title":"Oral Health in Patients with Psoriasis\u2014A Prospective Study","volume":"139","author":"Woeste","year":"2019","journal-title":"J. Investig. Dermatol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.cyto.2017.01.016","article-title":"Activity of Inflammatory Bowel Disease Influences the Expression of Cytokines in Gingival Tissue","volume":"95","author":"Figueredo","year":"2017","journal-title":"Cytokine"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"7963","DOI":"10.3748\/wjg.v22.i35.7963","article-title":"Periodontal and Inflammatory Bowel Diseases: Is There Evidence of Complex Pathogenic Interactions?","volume":"22","author":"Figueredo","year":"2016","journal-title":"World J. Gastroenterol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1126\/science.aan4526","article-title":"Ectopic Colonization of Oral Bacteria in the Intestine Drives T(H)1 Cell Induction and Inflammation","volume":"358","author":"Atarashi","year":"2017","journal-title":"Science"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"2907062","DOI":"10.1155\/2019\/2907062","article-title":"Are There Any Common Genetic Risk Markers for Rheumatoid Arthritis and Periodontal Diseases? A Case-Control Study","volume":"2019","author":"Schulz","year":"2019","journal-title":"Mediat. Inflamm."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"522","DOI":"10.1111\/jcpe.13087","article-title":"Secreted Frizzled-Related Protein 5 Serum Levels in Human Periodontitis\u2014A Nested Case-Control Study","volume":"46","author":"Schulz","year":"2019","journal-title":"J. Clin. Periodontol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1902","DOI":"10.1016\/j.joen.2014.08.013","article-title":"An Overview on Biologic Medications and Their Possible Role in Apical Periodontitis","volume":"40","author":"Cotti","year":"2014","journal-title":"J. Endod."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/12\/10\/1934\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T16:01:30Z","timestamp":1760112090000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/12\/10\/1934"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,9,24]]},"references-count":50,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2024,10]]}},"alternative-id":["microorganisms12101934"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms12101934","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,9,24]]}}}