Longitudinal analysis at three oral sites links oral microbiota to clinical outcomes in allogeneic hematopoietic stem-cell transplant
ABSTRACT Allogeneic hematopoietic stem-cell transplant (allo-HSCT) is potentially curative for several hematological disorders. Before stem-cell infusion, recipients undergo a conditioning regimen with chemo/radiotherapy and immunosuppressants, requiring the use of antibiotics to treat and prevent i...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-12-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.02910-23 |
| _version_ | 1797393674010624000 |
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| author | Vitor Heidrich Franciele H. Knebel Julia S. Bruno Vinícius C. de Molla Wanessa Miranda-Silva Paula F. Asprino Luciana Tucunduva Vanderson Rocha Yana Novis Eduardo R. Fregnani Celso Arrais-Rodrigues Anamaria A. Camargo |
| author_facet | Vitor Heidrich Franciele H. Knebel Julia S. Bruno Vinícius C. de Molla Wanessa Miranda-Silva Paula F. Asprino Luciana Tucunduva Vanderson Rocha Yana Novis Eduardo R. Fregnani Celso Arrais-Rodrigues Anamaria A. Camargo |
| author_sort | Vitor Heidrich |
| collection | DOAJ |
| description | ABSTRACT Allogeneic hematopoietic stem-cell transplant (allo-HSCT) is potentially curative for several hematological disorders. Before stem-cell infusion, recipients undergo a conditioning regimen with chemo/radiotherapy and immunosuppressants, requiring the use of antibiotics to treat and prevent infections. This regimen promotes drastic alterations in the recipient’s microbiota, including the oral microbiota, which have been associated with allo-HSCT complications and poor outcomes. However, long-term longitudinal studies on the oral microbiota of allo-HSCT recipients are scarce and disregard the existence of distinct microbiota within the oral cavity. Here, we used 16S rRNA gene sequencing to characterize the longitudinal microbiota dynamics in a prospective cohort of 31 allo-HSCT recipients at three oral sites (gingival crevicular fluid, oral mucosa, and supragingival biofilm). We found declines in bacterial diversity and major shifts in microbiota composition in all oral sites during allo-HSCT, including blooms of potentially pathogenic genera. These blooms in some cases preceded respiratory infections caused by the blooming bacteria. We also noticed that differences in microbiota composition between oral sites were lost during allo-HSCT. Overall, after allo-HSCT, the distinct oral microbiota returned to their preconditioning state, although at variable levels of competence per patient. After stratifying patients based on recovery levels, we found that recoverers of the oral mucosa microbiota composition had earlier reconstitution of normal blood leukocyte counts. Most notably, oral mucosa microbiota recovery was an independent biomarker of better allo-HSCT outcomes. This study highlights the potential clinical impact of the oral microbiota in the allo-HSCT setting and the clinical value of tracking oral microbiota changes during allo-HSCT. IMPORTANCE The oral cavity is the ultimate doorway for microbes entering the human body. We analyzed oral microbiota dynamics in allogeneic hematopoietic stem-cell transplant recipients and showed that microbiota injury and recovery patterns were highly informative on transplant complications and outcomes. Our results highlight the importance of tracking the recipient’s microbiota changes during allogeneic hematopoietic stem-cell transplant to improve our understanding of its biology, safety, and efficacy. |
| first_indexed | 2024-03-09T00:06:16Z |
| format | Article |
| id | doaj.art-70c48db0a68d4a7d9880f5820479517e |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-03-09T00:06:16Z |
| publishDate | 2023-12-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-70c48db0a68d4a7d9880f5820479517e2023-12-12T13:17:18ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-12-0111610.1128/spectrum.02910-23Longitudinal analysis at three oral sites links oral microbiota to clinical outcomes in allogeneic hematopoietic stem-cell transplantVitor Heidrich0Franciele H. Knebel1Julia S. Bruno2Vinícius C. de Molla3Wanessa Miranda-Silva4Paula F. Asprino5Luciana Tucunduva6Vanderson Rocha7Yana Novis8Eduardo R. Fregnani9Celso Arrais-Rodrigues10Anamaria A. Camargo11Centro de Oncologia Molecular, Hospital Sírio-Libanês , São Paulo, BrazilCentro de Oncologia Molecular, Hospital Sírio-Libanês , São Paulo, BrazilCentro de Oncologia Molecular, Hospital Sírio-Libanês , São Paulo, BrazilHospital Nove de Julho, Rede DASA , São Paulo, BrazilCentro de Oncologia Molecular, Hospital Sírio-Libanês , São Paulo, BrazilCentro de Oncologia Molecular, Hospital Sírio-Libanês , São Paulo, BrazilCentro de Oncologia, Hospital Sírio-Libanês , São Paulo, BrazilHospital das Clínicas da Faculdade de Medicina, Universidade de São Paulo , São Paulo, BrazilCentro de Oncologia, Hospital Sírio-Libanês , São Paulo, BrazilCentro de Oncologia Molecular, Hospital Sírio-Libanês , São Paulo, BrazilHospital Nove de Julho, Rede DASA , São Paulo, BrazilCentro de Oncologia Molecular, Hospital Sírio-Libanês , São Paulo, BrazilABSTRACT Allogeneic hematopoietic stem-cell transplant (allo-HSCT) is potentially curative for several hematological disorders. Before stem-cell infusion, recipients undergo a conditioning regimen with chemo/radiotherapy and immunosuppressants, requiring the use of antibiotics to treat and prevent infections. This regimen promotes drastic alterations in the recipient’s microbiota, including the oral microbiota, which have been associated with allo-HSCT complications and poor outcomes. However, long-term longitudinal studies on the oral microbiota of allo-HSCT recipients are scarce and disregard the existence of distinct microbiota within the oral cavity. Here, we used 16S rRNA gene sequencing to characterize the longitudinal microbiota dynamics in a prospective cohort of 31 allo-HSCT recipients at three oral sites (gingival crevicular fluid, oral mucosa, and supragingival biofilm). We found declines in bacterial diversity and major shifts in microbiota composition in all oral sites during allo-HSCT, including blooms of potentially pathogenic genera. These blooms in some cases preceded respiratory infections caused by the blooming bacteria. We also noticed that differences in microbiota composition between oral sites were lost during allo-HSCT. Overall, after allo-HSCT, the distinct oral microbiota returned to their preconditioning state, although at variable levels of competence per patient. After stratifying patients based on recovery levels, we found that recoverers of the oral mucosa microbiota composition had earlier reconstitution of normal blood leukocyte counts. Most notably, oral mucosa microbiota recovery was an independent biomarker of better allo-HSCT outcomes. This study highlights the potential clinical impact of the oral microbiota in the allo-HSCT setting and the clinical value of tracking oral microbiota changes during allo-HSCT. IMPORTANCE The oral cavity is the ultimate doorway for microbes entering the human body. We analyzed oral microbiota dynamics in allogeneic hematopoietic stem-cell transplant recipients and showed that microbiota injury and recovery patterns were highly informative on transplant complications and outcomes. Our results highlight the importance of tracking the recipient’s microbiota changes during allogeneic hematopoietic stem-cell transplant to improve our understanding of its biology, safety, and efficacy.https://journals.asm.org/doi/10.1128/spectrum.02910-23oral microbiome16S rRNA gene sequencingallogeneic hematopoietic cell transplantmicrobiome stabilityblooming of bacteriabiomarkers |
| spellingShingle | Vitor Heidrich Franciele H. Knebel Julia S. Bruno Vinícius C. de Molla Wanessa Miranda-Silva Paula F. Asprino Luciana Tucunduva Vanderson Rocha Yana Novis Eduardo R. Fregnani Celso Arrais-Rodrigues Anamaria A. Camargo Longitudinal analysis at three oral sites links oral microbiota to clinical outcomes in allogeneic hematopoietic stem-cell transplant Microbiology Spectrum oral microbiome 16S rRNA gene sequencing allogeneic hematopoietic cell transplant microbiome stability blooming of bacteria biomarkers |
| title | Longitudinal analysis at three oral sites links oral microbiota to clinical outcomes in allogeneic hematopoietic stem-cell transplant |
| title_full | Longitudinal analysis at three oral sites links oral microbiota to clinical outcomes in allogeneic hematopoietic stem-cell transplant |
| title_fullStr | Longitudinal analysis at three oral sites links oral microbiota to clinical outcomes in allogeneic hematopoietic stem-cell transplant |
| title_full_unstemmed | Longitudinal analysis at three oral sites links oral microbiota to clinical outcomes in allogeneic hematopoietic stem-cell transplant |
| title_short | Longitudinal analysis at three oral sites links oral microbiota to clinical outcomes in allogeneic hematopoietic stem-cell transplant |
| title_sort | longitudinal analysis at three oral sites links oral microbiota to clinical outcomes in allogeneic hematopoietic stem cell transplant |
| topic | oral microbiome 16S rRNA gene sequencing allogeneic hematopoietic cell transplant microbiome stability blooming of bacteria biomarkers |
| url | https://journals.asm.org/doi/10.1128/spectrum.02910-23 |
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