{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,8]],"date-time":"2026-07-08T15:18:37Z","timestamp":1783523917336,"version":"3.55.0"},"reference-count":42,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2022,10,20]],"date-time":"2022-10-20T00:00:00Z","timestamp":1666224000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2022,10,20]],"date-time":"2022-10-20T00:00:00Z","timestamp":1666224000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>\n                    Oral mucositis (OM) is a complex acute cytotoxicity of antineoplastic treatment that affects 40\u201385% of patients undergoing hematopoietic stem-cell transplantation. OM is associated with prolonged hospitalization, increased extensive pharmacotherapy, need for parenteral nutrition, and elevated treatment costs. As OM onset relates to the mucosal microenvironment status, with a particular role for microbiota-driven inflammation, we aimed to investigate whether the oral mucosa microbiota was associated with the clinical course of OM in patients undergoing allogeneic hematopoietic stem-cell transplantation. We collected oral mucosa samples from 30 patients and analyzed the oral mucosa microbiota by 16S rRNA sequencing. A total of 13 patients (43%) developed ulcerative OM. We observed that specific taxa were associated with oral mucositis grade and time to oral mucositis healing.\n                    <jats:italic>Porphyromonas<\/jats:italic>\n                    relative abundance at preconditioning was positively correlated with ulcerative OM grade (Spearman \u03c1\u2009=\u20090.61, P\u2009=\u20090.028) and higher\n                    <jats:italic>Lactobacillus<\/jats:italic>\n                    relative abundance at ulcerative OM onset was associated with shortened ulcerative OM duration (P\u2009=\u20090.032). Additionally, we generated a machine-learning-based bacterial signature that uses pre-treatment microbial profiles to predict whether a patient will develop OM during treatment. Our findings suggest that further research should focus on host-microbiome interactions to better prevent and treat OM.\n                  <\/jats:p>","DOI":"10.1038\/s41598-022-21775-3","type":"journal-article","created":{"date-parts":[[2022,10,20]],"date-time":"2022-10-20T07:07:06Z","timestamp":1666249626000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":24,"title":["Commensal oral microbiota impacts ulcerative oral mucositis clinical course in allogeneic stem cell transplant recipients"],"prefix":"10.1038","volume":"12","author":[{"given":"Julia S.","family":"Bruno","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vitor","family":"Heidrich","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Franciele H.","family":"Knebel","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vin\u00edcius Campos","family":"de Molla","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Claudia Joffily","family":"Parahyba","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wanessa","family":"Miranda-Silva","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paula F.","family":"Asprino","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Luciana","family":"Tucunduva","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vanderson","family":"Rocha","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yana","family":"Novis","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Celso","family":"Arrais-Rodrigues","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anamaria A.","family":"Camargo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eduardo R.","family":"Fregnani","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2022,10,20]]},"reference":[{"key":"21775_CR1","doi-asserted-by":"publisher","first-page":"4423","DOI":"10.1002\/cncr.33100","volume":"126","author":"S Elad","year":"2020","unstructured":"Elad, S. et al. MASCC\/ISOO clinical practice guidelines for the management of mucositis secondary to cancer therapy. Cancer 126, 4423\u20134431 (2020).","journal-title":"Cancer"},{"key":"21775_CR2","doi-asserted-by":"publisher","first-page":"354","DOI":"10.3389\/fphar.2017.00354","volume":"8","author":"M Cinausero","year":"2017","unstructured":"Cinausero, M. et al. New frontiers in the pathobiology and treatment of cancer regimen-related mucosal injury. Front. Pharmacol. 8, 354 (2017).","journal-title":"Front. Pharmacol."},{"key":"21775_CR3","doi-asserted-by":"publisher","first-page":"2079","DOI":"10.1007\/s00277-021-04568-y","volume":"100","author":"A Wysocka-S\u0142owik","year":"2021","unstructured":"Wysocka-S\u0142owik, A., Gil, L., \u015alebioda, Z., Kr\u0119gielczak, A. & Dorocka-Bobkowska, B. Oral mucositis in patients with acute myeloid leukemia treated with allogeneic hematopoietic stem cell transplantation in relation to the conditioning used prior to transplantation. Ann. Hematol. 100, 2079\u20132086 (2021).","journal-title":"Ann. Hematol."},{"key":"21775_CR4","doi-asserted-by":"publisher","first-page":"159","DOI":"10.1097\/CCO.0000000000000180","volume":"27","author":"A Villa","year":"2015","unstructured":"Villa, A. & Sonis, S. T. Mucositis: Pathobiology and management. Curr. Opin. Oncol. 27, 159\u2013164 (2015).","journal-title":"Curr. Opin. Oncol."},{"key":"21775_CR5","doi-asserted-by":"publisher","first-page":"5059","DOI":"10.1007\/s00520-020-05579-7","volume":"28","author":"HR Wardill","year":"2020","unstructured":"Wardill, H. R. et al. Prediction of mucositis risk secondary to cancer therapy: A systematic review of current evidence and call to action. Support Care Cancer 28, 5059\u20135073 (2020).","journal-title":"Support Care Cancer"},{"key":"21775_CR6","doi-asserted-by":"publisher","first-page":"618150","DOI":"10.3389\/fimmu.2021.618150","volume":"12","author":"C Xia","year":"2021","unstructured":"Xia, C. et al. A phase II randomized clinical trial and mechanistic studies using improved probiotics to prevent oral mucositis induced by concurrent radiotherapy and chemotherapy in nasopharyngeal carcinoma. Front. Immunol. 12, 618150 (2021).","journal-title":"Front. Immunol."},{"key":"21775_CR7","doi-asserted-by":"publisher","first-page":"1935","DOI":"10.21873\/anticanres.13303","volume":"39","author":"V de Sanctis","year":"2019","unstructured":"de Sanctis, V. et al. Lactobacillus brevis CD2 for prevention of oral mucositis in patients with head and neck tumors: A multicentric randomized study. Anticancer Res. 39, 1935\u20131942 (2019).","journal-title":"Anticancer Res."},{"key":"21775_CR8","doi-asserted-by":"publisher","first-page":"1081","DOI":"10.1002\/cncr.31907","volume":"125","author":"C Jiang","year":"2019","unstructured":"Jiang, C. et al. A randomized, double-blind, placebo-controlled trial of probiotics to reduce the severity of oral mucositis induced by chemoradiotherapy for patients with nasopharyngeal carcinoma. Cancer 125, 1081\u20131090 (2019).","journal-title":"Cancer"},{"key":"21775_CR9","doi-asserted-by":"publisher","first-page":"1015","DOI":"10.1016\/j.oraloncology.2009.08.006","volume":"45","author":"ST Sonis","year":"2009","unstructured":"Sonis, S. T. Mucositis: The impact, biology and therapeutic opportunities of oral mucositis. Oral Oncol. 45, 1015\u20131020 (2009).","journal-title":"Oral Oncol."},{"key":"21775_CR10","doi-asserted-by":"publisher","first-page":"3231","DOI":"10.1007\/s00520-012-1463-2","volume":"20","author":"AMGA Laheij","year":"2012","unstructured":"Laheij, A. M. G. A. et al. Oral bacteria and yeasts in relationship to oral ulcerations in hematopoietic stem cell transplant recipients. Support Care Cancer 20, 3231\u20133240 (2012).","journal-title":"Support Care Cancer"},{"key":"21775_CR11","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41598-021-96939-8","volume":"11","author":"VC de Molla","year":"2021","unstructured":"de Molla, V. C. et al. Disruption of the oral microbiota is associated with a higher risk of relapse after allogeneic hematopoietic stem cell transplantation. Sci. Rep. 11, 1\u201311 (2021).","journal-title":"Sci. Rep."},{"key":"21775_CR12","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1111\/j.1574-6968.2012.02579.x","volume":"333","author":"N Bostanci","year":"2012","unstructured":"Bostanci, N. & Belibasakis, G. N. Porphyromonas gingivalis: An invasive and evasive opportunistic oral pathogen. FEMS Microbiol. Lett. 333, 1\u20139 (2012).","journal-title":"FEMS Microbiol. Lett."},{"key":"21775_CR13","doi-asserted-by":"publisher","first-page":"731","DOI":"10.1038\/s41575-021-00488-4","volume":"18","author":"E Read","year":"2021","unstructured":"Read, E., Curtis, M. A. & Neves, J. F. The role of oral bacteria in inflammatory bowel disease. Nat. Rev. Gastroenterol. Hepatol. 18, 731\u2013742 (2021).","journal-title":"Nat. Rev. Gastroenterol. Hepatol."},{"key":"21775_CR14","doi-asserted-by":"publisher","first-page":"3333","DOI":"10.1126\/sciadv.aau3333","volume":"5","author":"SS Dominy","year":"2019","unstructured":"Dominy, S. S. et al. Porphyromonas gingivalis in Alzheimer\u2019s disease brains: Evidence for disease causation and treatment with small-molecule inhibitors. Sci. Adv. 5, 3333 (2019).","journal-title":"Sci. Adv."},{"key":"21775_CR15","doi-asserted-by":"publisher","first-page":"81","DOI":"10.1111\/jop.12152","volume":"44","author":"AM Stringer","year":"2015","unstructured":"Stringer, A. M. & Logan, R. M. The role of oral flora in the development of chemotherapy-induced oral mucositis. J. Oral Pathol. Med. 44, 81\u201387 (2015).","journal-title":"J. Oral Pathol. Med."},{"key":"21775_CR16","doi-asserted-by":"publisher","first-page":"262","DOI":"10.3389\/fcimb.2019.00262","volume":"9","author":"L Jia","year":"2019","unstructured":"Jia, L. et al. Pathogenesis of important virulence factors of Porphyromonas gingivalis via toll-like receptors. Front. Cell Infect. Microbiol. 9, 262 (2019).","journal-title":"Front. Cell Infect. Microbiol."},{"key":"21775_CR17","doi-asserted-by":"publisher","first-page":"e000138","DOI":"10.1136\/esmoopen-2016-000138","volume":"1","author":"A Sharma","year":"2016","unstructured":"Sharma, A. et al. Lactobacillus brevis CD2 lozenges prevent oral mucositis in patients undergoing high dose chemotherapy followed by haematopoietic stem cell transplantation. ESMO Open 1, e000138 (2016).","journal-title":"ESMO Open"},{"key":"21775_CR18","doi-asserted-by":"publisher","first-page":"16929","DOI":"10.1038\/s41598-019-53073-w","volume":"9","author":"AMGA Laheij","year":"2019","unstructured":"Laheij, A. M. G. A. et al. Microbial changes in relation to oral mucositis in autologous hematopoietic stem cell transplantation recipients. Sci. Rep. 9, 16929 (2019).","journal-title":"Sci. Rep."},{"key":"21775_CR19","doi-asserted-by":"publisher","first-page":"2912","DOI":"10.1182\/bloodadvances.2020001827","volume":"4","author":"R Shouval","year":"2020","unstructured":"Shouval, R. et al. Patterns of salivary microbiota injury and oral mucositis in recipients of allogeneic hematopoietic stem cell transplantation. Blood Adv. 4, 2912\u20132917 (2020).","journal-title":"Blood Adv."},{"key":"21775_CR20","doi-asserted-by":"publisher","first-page":"1090","DOI":"10.3390\/jcm9041090","volume":"9","author":"A Lee","year":"2020","unstructured":"Lee, A. et al. Association of HSV-1 and reduced oral bacteriota diversity with chemotherapy-induced oral mucositis in patients undergoing autologous hematopoietic stem cell transplantation. J. Clin. Med. 9, 1090 (2020).","journal-title":"J. Clin. Med."},{"key":"21775_CR21","doi-asserted-by":"publisher","first-page":"690","DOI":"10.1007\/s12185-020-02958-y","volume":"112","author":"M Takahashi","year":"2020","unstructured":"Takahashi, M. et al. An analysis of oral microbial flora by T-RFLP in patients undergoing hematopoietic stem cell transplantation. Int. J. Hematol. 112, 690\u2013696 (2020).","journal-title":"Int. J. Hematol."},{"key":"21775_CR22","doi-asserted-by":"publisher","first-page":"1761135","DOI":"10.1080\/20002297.2020.1761135","volume":"12","author":"J-LC Mougeot","year":"2020","unstructured":"Mougeot, J.-L.C. et al. Lasting Gammaproteobacteria profile changes characterized hematological cancer patients who developed oral mucositis following conditioning therapy. J. Oral Microbiol. 12, 1761135 (2020).","journal-title":"J. Oral Microbiol."},{"key":"21775_CR23","doi-asserted-by":"publisher","first-page":"734","DOI":"10.3390\/microorganisms10040734","volume":"10","author":"AMGA Laheij","year":"2022","unstructured":"Laheij, A. M. G. A. et al. Long-term analysis of resilience of the oral microbiome in allogeneic stem cell transplant recipients. Microorganisms 10, 734 (2022).","journal-title":"Microorganisms"},{"key":"21775_CR24","doi-asserted-by":"publisher","first-page":"1453","DOI":"10.1002\/cncr.28592","volume":"120","author":"RV Lalla","year":"2014","unstructured":"Lalla, R. V. et al. MASCC\/ISOO clinical practice guidelines for the management of mucositis secondary to cancer therapy. Cancer 120, 1453\u20131461 (2014).","journal-title":"Cancer"},{"key":"21775_CR25","doi-asserted-by":"publisher","first-page":"e1","DOI":"10.1093\/nar\/gks808","volume":"41","author":"A Klindworth","year":"2013","unstructured":"Klindworth, A. et al. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 41, e1 (2013).","journal-title":"Nucleic Acids Res."},{"key":"21775_CR26","doi-asserted-by":"publisher","first-page":"88122","DOI":"10.18632\/oncotarget.21490","volume":"8","author":"H Wang","year":"2017","unstructured":"Wang, H. et al. Breast tissue, oral and urinary microbiomes in breast cancer. Oncotarget 8, 88122\u201388138 (2017).","journal-title":"Oncotarget"},{"key":"21775_CR27","doi-asserted-by":"publisher","first-page":"852","DOI":"10.1038\/s41587-019-0209-9","volume":"37","author":"E Bolyen","year":"2019","unstructured":"Bolyen, E. et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 37, 852\u2013857 (2019).","journal-title":"Nat. Biotechnol."},{"key":"21775_CR28","doi-asserted-by":"publisher","first-page":"581","DOI":"10.1038\/nmeth.3869","volume":"13","author":"BJ Callahan","year":"2016","unstructured":"Callahan, B. J. et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581\u2013583 (2016).","journal-title":"Nat. Methods"},{"key":"21775_CR29","doi-asserted-by":"publisher","first-page":"e2584","DOI":"10.7717\/peerj.2584","volume":"4","author":"T Rognes","year":"2016","unstructured":"Rognes, T., Flouri, T., Nichols, B., Quince, C. & Mah\u00e9, F. VSEARCH: A versatile open source tool for metagenomics. PeerJ 4, e2584 (2016).","journal-title":"PeerJ"},{"key":"21775_CR30","doi-asserted-by":"publisher","first-page":"D590","DOI":"10.1093\/nar\/gks1219","volume":"41","author":"C Quast","year":"2013","unstructured":"Quast, C. et al. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 41, D590\u2013D596 (2013).","journal-title":"Nucleic Acids Res."},{"key":"21775_CR31","unstructured":"Team, R. A Language and Environment for Statistical Computing. https:\/\/www.r-project.org\/ (2017)."},{"key":"21775_CR32","doi-asserted-by":"publisher","first-page":"e9593","DOI":"10.7717\/peerj.9593","volume":"8","author":"L Beule","year":"2020","unstructured":"Beule, L. & Karlovsky, P. Improved normalization of species count data in ecology by scaling with ranked subsampling (SRS): Application to microbial communities. PeerJ 8, e9593 (2020).","journal-title":"PeerJ"},{"key":"21775_CR33","doi-asserted-by":"publisher","first-page":"11473","DOI":"10.3390\/app112311473","volume":"11","author":"V Heidrich","year":"2021","unstructured":"Heidrich, V., Karlovsky, P. & Beule, L. \u201cSRS\u201d R Package and \u201cq2-srs\u201d QIIME 2 plugin: Normalization of microbiome data using scaling with ranked subsampling (SRS). Appl. Sci. 11, 11473 (2021).","journal-title":"Appl. Sci."},{"key":"21775_CR34","doi-asserted-by":"publisher","first-page":"379","DOI":"10.1002\/j.1538-7305.1948.tb01338.x","volume":"27","author":"CE Shannon","year":"1948","unstructured":"Shannon, C. E. A mathematical theory of communication. Bell Syst. Tech. J. 27, 379\u2013423 (1948).","journal-title":"Bell Syst. Tech. J."},{"key":"21775_CR35","doi-asserted-by":"publisher","first-page":"e61217","DOI":"10.1371\/journal.pone.0061217","volume":"8","author":"PJ McMurdie","year":"2013","unstructured":"McMurdie, P. J. & Holmes, S. phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8, e61217 (2013).","journal-title":"PLoS ONE"},{"key":"21775_CR36","first-page":"325","volume":"27","author":"JTC Roger Bray","year":"1957","unstructured":"Roger Bray, J. T. C. An ordination of the upland forest communities of southern Wisconsin. Ecol. Soc. Am. 27, 325\u2013349 (1957).","journal-title":"Ecol. Soc. Am."},{"key":"21775_CR37","doi-asserted-by":"publisher","unstructured":"Anderson, B. M. J. Permutational Multivariate Analysis of Variance (PERMANOVA), 1\u201315. https:\/\/doi.org\/10.1002\/9781118445112.stat07841.","DOI":"10.1002\/9781118445112.stat07841"},{"key":"21775_CR38","first-page":"1","volume":"35","author":"PM Valero-Mora","year":"2010","unstructured":"Valero-Mora, P. M. ggplot2: Elegant graphics for data analysis. J. Stat. Softw. Book Rev. 35, 1\u20133 (2010).","journal-title":"J. Stat. Softw. Book Rev."},{"key":"21775_CR39","doi-asserted-by":"publisher","first-page":"3514","DOI":"10.1038\/s41467-020-17041-7","volume":"11","author":"H Lin","year":"2020","unstructured":"Lin, H. & Peddada, S. D. Analysis of compositions of microbiomes with bias correction. Nat. Commun. 11, 3514 (2020).","journal-title":"Nat. Commun."},{"key":"21775_CR40","unstructured":"Therneau, T. M. A Package for Survival Analysis in R. https:\/\/cran.r-project.org\/package=survival (2021)."},{"key":"21775_CR41","unstructured":"Kassambara, A., Kosinski, M. & Przemyslaw Biecek, S. F. Survminer: Drawing Survival Curves Using \u201cggplot2\u201d (2021)."},{"key":"21775_CR42","doi-asserted-by":"publisher","first-page":"1","DOI":"10.18637\/jss.v011.i09","volume":"11","author":"A Karatzoglou","year":"2004","unstructured":"Karatzoglou, A., Smola, A., Hornik, K. & Zeileis, A. kernlab\u2014An S4 package for Kernel methods in R. J. Stat. Softw. 11, 1\u201320 (2004).","journal-title":"J. Stat. Softw."}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-022-21775-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-022-21775-3","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-022-21775-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,15]],"date-time":"2022-12-15T05:11:07Z","timestamp":1671081067000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-022-21775-3"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,10,20]]},"references-count":42,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2022,12]]}},"alternative-id":["21775"],"URL":"https:\/\/doi.org\/10.1038\/s41598-022-21775-3","relation":{"has-preprint":[{"id-type":"doi","id":"10.21203\/rs.3.rs-1551598\/v1","asserted-by":"object"}]},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,10,20]]},"assertion":[{"value":"12 April 2022","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"4 October 2022","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"20 October 2022","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"17 December 2022","order":4,"name":"change_date","label":"Change Date","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"Update","order":5,"name":"change_type","label":"Change Type","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The original online version of this Article was revised: In the original version of this Article, the author names Paula F. Asprino, Anamaria A. Camargo and Eduardo R. Fregnani were incorrectly indexed. The original Article has been corrected.","order":6,"name":"change_details","label":"Change Details","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"17527"}}