Temporal variation in oral microbiome composition of patients undergoing autologous hematopoietic cell transplantation with keratinocyte growth factor

. 2023 Sep 13 ; 23 (1) : 258. [epub] 20230913

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid37704974
Odkazy

PubMed 37704974
PubMed Central PMC10500729
DOI 10.1186/s12866-023-03000-x
PII: 10.1186/s12866-023-03000-x
Knihovny.cz E-zdroje

INTRODUCTION: Autologous hematopoietic cell transplantation (AHCT) is a well-established treatment for lymphoma. Unintended effects of this therapy include oral mucositis (OM) and gastrointestinal toxicities, resulting in poor clinical outcomes. The gut microbiome has been previously linked to transplant toxicities among allogeneic recipients, but little is known about the effects of AHCT on the oral microbiome. METHODS: Seven patients with non-Hodgkin or Hodgkin lymphoma undergoing AHCT with palifermin (keratinocyte growth factor) were included. Buccal swab samples were collected at baseline and 14- and 28-days post-treatment. Oral microbial communities were characterized with 16 S rRNA amplicon sequencing. Temporal trends in community composition, alpha diversity, and beta diversity were investigated. RESULTS: A significant reduction in the relative abundance of the genera Gemella and Actinomyces were observed from baseline. No significant temporal differences in alpha diversity were observed. Significant changes in beta diversity were recorded. CONCLUSION: Results of this pilot study suggest treatment with AHCT and palifermin affects the oral microbiome, resulting in temporal shifts in oral microbial community composition. Future studies are warranted to confirm these trends and further investigate the effects of AHCT on the oral microbiome and how these shifts may affect health outcomes.

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El Jurdi N, Filali-Mouhim A, Salem I, Retuerto M, Dambrosio NM, Baer L et al. Gastrointestinal Microbiome and Mycobiome Changes during Autologous Transplantation for Multiple Myeloma: Results of a Prospective Pilot Study. Biol Blood Marrow Transplant [Internet]. 2019 Aug 1 [cited 2020 Apr 25];25(8):1511–9. Available from: http://www.ncbi.nlm.nih.gov/pubmed/30959164. PubMed

Sonis ST, Oster G, Fuchs H, Bellm L, Bradford WZ, Edelsberg J et al. Oral mucositis and the clinical and economic outcomes of hematopoietic stem-cell transplantation. J Clin Oncol [Internet]. 2001 Apr 15 [cited 2020 Apr 24];19(8):2201–5. Available from: http://www.ncbi.nlm.nih.gov/pubmed/11304772. PubMed

Bellm LA, Epstein JB, Rose-Ped A, Martin P, Fuchs HJ. Patient reports of complications of bone marrow transplantation. Support Care Cancer. 2000;8(1):33–9. doi: 10.1007/s005209900095. PubMed DOI

McGuire DB, Altomonte V, Peterson DE, Wingard JR, Jones RJ, Grochow LB. Patterns of mucositis and pain in patients receiving preparative chemotherapy and bone marrow transplantation. Oncol Nurs Forum. 1993;20(10):1493–502. PubMed

Woo S-B, Sonis ST, Monopoli MM, Sonis AL. A longitudinal study of oral ulcerative mucositis in bone marrow transplant recipients. Cancer. 1993;72(5):1612–7. doi: 10.1002/1097-0142(19930901)72:5<1612::AID-CNCR2820720520>3.0.CO;2-Q. PubMed DOI

Shouval R, Eshel A, Dubovski B, Kuperman AA, Danylesko I, Fein JA, et al. Patterns of salivary microbiota injury and oral mucositis in recipients of allogeneic hematopoietic stem cell transplantation. Blood Adv. 2020;4(13):2912–7. doi: 10.1182/bloodadvances.2020001827. PubMed DOI PMC

Ohbayashi Y, Imataki O, Uemura M, Takeuchi A, Aoki S, Tanaka M, et al. Oral microorganisms and bloodstream infection in allogeneic hematopoietic stem cell transplantation. Clin Oral Investig. 2021;25(7):4359–67. doi: 10.1007/s00784-020-03749-9. PubMed DOI

Lee A, Hong J, Shin D-Y, Koh Y, Yoon S-S, Kim P-J 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. 2020;9(4). PubMed PMC

Oku S, Takeshita T, Futatsuki T, Kageyama S, Asakawa M, Mori Y, et al. Disrupted tongue microbiota and detection of nonindigenous bacteria on the day of allogeneic hematopoietic stem cell transplantation. PLoS Pathog. 2020;16(3):e1008348. doi: 10.1371/journal.ppat.1008348. PubMed DOI PMC

de Molla VC, Heidrich V, Bruno JS, Knebel FH, Miranda-Silva W, Asprino PF, et al. Disruption of the oral microbiota is associated with a higher risk of relapse after allogeneic hematopoietic stem cell transplantation. Sci Rep. 2021;11(1):17552. doi: 10.1038/s41598-021-96939-8. PubMed DOI PMC

Ames NJ, Sulima P, Ngo T, Barb J, Munson PJ, Paster BJ, et al. A characterization of the oral microbiome in allogeneic stem cell transplant patients. PLoS ONE. 2012;7(10):e47628. doi: 10.1371/journal.pone.0047628. PubMed DOI PMC

Laheij AMGA, Raber-Durlacher JE, Koppelmans RGA, Huysmans MCDNJM, Potting C, van Leeuwen SJM et al. Microbial changes in relation to oral mucositis in autologous hematopoietic stem cell transplantation recipients. Sci Rep. 2019;9(1). PubMed PMC

Laheij AMGA, de Soet JJ, von dem Borne PA, Kuijper EJ, Kraneveld EA, van Loveren C, et al. Oral bacteria and yeasts in relationship to oral ulcerations in hematopoietic stem cell transplant recipients. Support Care Cancer. 2012;20(12):3231–40. doi: 10.1007/s00520-012-1463-2. PubMed DOI PMC

Weber D, Frauenschläger K, Ghimire S, Peter K, Panzer I, Hiergeist A et al. The association between acute graft-versus-host disease and antimicrobial peptide expression in the gastrointestinal tract after allogeneic stem cell transplantation. Palaniyandi S, editor. PLoS One [Internet]. 2017 Sep 21 [cited 2021 Jan 13];12(9):e0185265. 10.1371/journal.pone.0185265. PubMed PMC

Sen T, Thummer RP. The impact of human microbiotas in hematopoietic stem cell and organ transplantation. Front Immunol. 2022;13:932228. doi: 10.3389/fimmu.2022.932228. PubMed DOI PMC

Badia P, Andersen H, Haslam D, Nelson AS, Pate AR, Golkari S, et al. Improving oral health and modulating the oral Microbiome to reduce bloodstream infections from oral organisms in Pediatric and Young Adult hematopoietic stem cell transplantation recipients: a Randomized Controlled Trial. Biol Blood Marrow Transplant. 2020;26(9):1704–10. doi: 10.1016/j.bbmt.2020.05.019. PubMed DOI PMC

Herbers AHE, van der Velden WJFM, de Haan AFJ, Donnelly JP, Blijlevens NMA. Impact of palifermin on intestinal mucositis of HSCT recipients after BEAM. Bone Marrow Transplant [Internet]. 2014 Jan [cited 2020 Apr 9];49(1):8–10. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23955637. PubMed

Stiff PJ, Emmanouilides C, Bensinger WI, Gentile T, Blazar B, Shea TC et al. Palifermin reduces patient-reported mouth and throat soreness and improves patient functioning in the hematopoietic stem-cell transplantation setting. J Clin Oncol [Internet]. 2006 Nov 20 [cited 2020 Apr 9];24(33):5186–93. Available from: http://www.ncbi.nlm.nih.gov/pubmed/16391299. PubMed

Spielberger R, Stiff P, Bensinger W, Gentile T, Weisdorf D, Kewalramani T, et al. Palifermin for oral mucositis after intensive therapy for hematologic cancers. N Engl J Med. 2004;351(25):2590–8. doi: 10.1056/NEJMoa040125. PubMed DOI

Vadhan-Raj S, Goldberg JD, Perales MA, Berger DP, van den Brink MRM. Clinical applications of palifermin: amelioration of oral mucositis and other potential indications. J Cell Mol Med. 2013;17(11):1371–84. doi: 10.1111/jcmm.12169. PubMed DOI PMC

El Jurdi N, Fair C, Rogosheske J, Shanley R, Arora M, Bachanova V, et al. Effect of keratinocyte growth factor on Hospital Readmission and Regimen-Related toxicities after autologous hematopoietic cell transplantation for Lymphoma. Transpl Cell Ther. 2021;27(2):179e1–4. doi: 10.1016/j.jtct.2020.11.005. PubMed DOI

Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 2012;6(8):1621–4. doi: 10.1038/ismej.2012.8. PubMed DOI PMC

Gohl DM, Vangay P, Garbe J, MacLean A, Hauge A, Becker A, et al. Systematic improvement of amplicon marker gene methods for increased accuracy in microbiome studies. Nat Biotechnol. 2016;34(9):942–9. doi: 10.1038/nbt.3601. PubMed DOI

Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009;75(23):7537–41. doi: 10.1128/AEM.01541-09. PubMed DOI PMC

Aronesty E. Comparison of sequencing Utility Programs. Open Bioinforma J. 2013;7(1):1–8. doi: 10.2174/1875036201307010001. DOI

Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, et al. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 2007;35(21):7188–96. doi: 10.1093/nar/gkm864. PubMed DOI PMC

Schloss PD, Westcott SL. Assessing and improving methods used in operational taxonomic unit-based approaches for 16S rRNA gene sequence analysis. Appl Environ Microbiol. 2011;77(10):3219–26. doi: 10.1128/AEM.02810-10. PubMed DOI PMC

Huse SM, Welch DM, Morrison HG, Sogin ML. Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ Microbiol. 2010;12(7):1889–98. doi: 10.1111/j.1462-2920.2010.02193.x. PubMed DOI PMC

Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011;27(16):2194–200. doi: 10.1093/bioinformatics/btr381. PubMed DOI PMC

Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, et al. The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 2009;37(Database issue):D141–5. doi: 10.1093/nar/gkn879. PubMed DOI PMC

CLARKE KR Non-parametric multivariate analyses of changes in community structure. Austral Ecol. 1993;18(1):117–43. doi: 10.1111/j.1442-9993.1993.tb00438.x. DOI

Napeñas JJ, Brennan MT, Coleman S, Kent ML, Noll J, Frenette G, et al. Molecular methodology to assess the impact of cancer chemotherapy on the oral bacterial flora: a pilot study. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2010;109(4):554–60. doi: 10.1016/j.tripleo.2009.11.015. PubMed DOI

Rashidi A, Kaiser T, Graiziger C, Holtan SG, Tauseef •, Rehman U et al. Specific gut microbiota changes heralding bloodstream infection and neutropenic fever during intensive chemotherapy. Leukemia [Internet]. 2019 [cited 2022 Jun 20]; 10.1038/s41375-019-0547-0. PubMed

Hong B-Y, Sobue T, Choquette L, Dupuy AK, Thompson A, Burleson JA, et al. Chemotherapy-induced oral mucositis is associated with detrimental bacterial dysbiosis. Microbiome. 2019;7(1):66. doi: 10.1186/s40168-019-0679-5. PubMed DOI PMC

Maier L, Pruteanu M, Kuhn M, Zeller G, Telzerow A, Anderson EE, et al. Extensive impact of non-antibiotic drugs on human gut bacteria. Nature. 2018;555(7698):623–8. doi: 10.1038/nature25979. PubMed DOI PMC

Jensen SB, Mouridsen HT, Reibel J, Brünner N, Nauntofte B. Adjuvant chemotherapy in breast cancer patients induces temporary salivary gland hypofunction. Oral Oncol. 2008;44(2):162–73. doi: 10.1016/j.oraloncology.2007.01.015. PubMed DOI

Marsh PD, Do T, Beighton D, Devine DA. Influence of saliva on the oral microbiota. Periodontol 2000. 2016;70(1):80–92. doi: 10.1111/prd.12098. PubMed DOI

Verma D, Garg PK, Dubey AK. Insights into the human oral microbiome. Arch Microbiol. 2018;200(4):525–40. doi: 10.1007/s00203-018-1505-3. PubMed DOI

Wade WG. The oral microbiome in health and disease. Pharmacol Res. 2013;69(1):137–43. doi: 10.1016/j.phrs.2012.11.006. PubMed DOI

Krishnan K, Chen T, Paster BJ. A practical guide to the oral microbiome and its relation to health and disease. Oral Dis. 2017;23(3):276–86. doi: 10.1111/odi.12509. PubMed DOI PMC

Irfan M, Delgado RZR, Frias-Lopez J. The oral Microbiome and Cancer. Front Immunol. 2020;11:591088. doi: 10.3389/fimmu.2020.591088. PubMed DOI PMC

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