Oropharyngeal microbiome profiled at admission is predictive of the need for respiratory support among COVID-19 patients
The oropharyngeal microbiome, the collective genomes of the community of microorganisms that colonizes the upper respiratory tract, is thought to influence the clinical course of infection by respiratory viruses, including Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2), the causative a...
Main Authors: | , , , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Frontiers Media S.A.
2022-09-01
|
Series: | Frontiers in Microbiology |
Subjects: | |
Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2022.1009440/full |
_version_ | 1828223345103994880 |
---|---|
author | Evan S. Bradley Evan S. Bradley Abigail L. Zeamer Abigail L. Zeamer Vanni Bucci Vanni Bucci Lindsey Cincotta Marie-Claire Salive Protiva Dutta Shafik Mutaawe Otuwe Anya Christopher Tocci Ann Moormann Doyle V. Ward Doyle V. Ward Beth A. McCormick Beth A. McCormick John P. Haran John P. Haran John P. Haran |
author_facet | Evan S. Bradley Evan S. Bradley Abigail L. Zeamer Abigail L. Zeamer Vanni Bucci Vanni Bucci Lindsey Cincotta Marie-Claire Salive Protiva Dutta Shafik Mutaawe Otuwe Anya Christopher Tocci Ann Moormann Doyle V. Ward Doyle V. Ward Beth A. McCormick Beth A. McCormick John P. Haran John P. Haran John P. Haran |
author_sort | Evan S. Bradley |
collection | DOAJ |
description | The oropharyngeal microbiome, the collective genomes of the community of microorganisms that colonizes the upper respiratory tract, is thought to influence the clinical course of infection by respiratory viruses, including Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2), the causative agent of Coronavirus Infectious Disease 2019 (COVID-19). In this study, we examined the oropharyngeal microbiome of suspected COVID-19 patients presenting to the Emergency Department and an inpatient COVID-19 unit with symptoms of acute COVID-19. Of 115 initially enrolled patients, 50 had positive molecular testing for COVID-19+ and had symptom duration of 14 days or less. These patients were analyzed further as progression of disease could most likely be attributed to acute COVID-19 and less likely a secondary process. Of these, 38 (76%) went on to require some form of supplemental oxygen support. To identify functional patterns associated with respiratory illness requiring respiratory support, we applied an interpretable random forest classification machine learning pipeline to shotgun metagenomic sequencing data and select clinical covariates. When combined with clinical factors, both species and metabolic pathways abundance-based models were found to be highly predictive of the need for respiratory support (F1-score 0.857 for microbes and 0.821 for functional pathways). To determine biologically meaningful and highly predictive signals in the microbiome, we applied the Stable and Interpretable RUle Set to the output of the models. This analysis revealed that low abundance of two commensal organisms, Prevotella salivae or Veillonella infantium (< 4.2 and 1.7% respectively), and a low abundance of a pathway associated with LPS biosynthesis (< 0.1%) were highly predictive of developing the need for acute respiratory support (82 and 91.4% respectively). These findings suggest that the composition of the oropharyngeal microbiome in COVID-19 patients may play a role in determining who will suffer from severe disease manifestations. |
first_indexed | 2024-04-12T17:06:12Z |
format | Article |
id | doaj.art-8c7ffc98f7c34464bed0fbf1b0da6e51 |
institution | Directory Open Access Journal |
issn | 1664-302X |
language | English |
last_indexed | 2024-04-12T17:06:12Z |
publishDate | 2022-09-01 |
publisher | Frontiers Media S.A. |
record_format | Article |
series | Frontiers in Microbiology |
spelling | doaj.art-8c7ffc98f7c34464bed0fbf1b0da6e512022-12-22T03:23:56ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-09-011310.3389/fmicb.2022.10094401009440Oropharyngeal microbiome profiled at admission is predictive of the need for respiratory support among COVID-19 patientsEvan S. Bradley0Evan S. Bradley1Abigail L. Zeamer2Abigail L. Zeamer3Vanni Bucci4Vanni Bucci5Lindsey Cincotta6Marie-Claire Salive7Protiva Dutta8Shafik Mutaawe9Otuwe Anya10Christopher Tocci11Ann Moormann12Doyle V. Ward13Doyle V. Ward14Beth A. McCormick15Beth A. McCormick16John P. Haran17John P. Haran18John P. Haran19Department of Emergency Medicine, UMass Memorial Medical Center, Worcester, MA, United StatesProgram in Microbiome Dynamics, University of Massachusetts Medical School, Worcester, MA, United StatesProgram in Microbiome Dynamics, University of Massachusetts Medical School, Worcester, MA, United StatesDepartment of Microbiology and Physiologic Systems, University of Massachusetts Medical School, Worcester, MA, United StatesProgram in Microbiome Dynamics, University of Massachusetts Medical School, Worcester, MA, United StatesDepartment of Microbiology and Physiologic Systems, University of Massachusetts Medical School, Worcester, MA, United StatesDepartment of Emergency Medicine, UMass Memorial Medical Center, Worcester, MA, United StatesDepartment of Emergency Medicine, UMass Memorial Medical Center, Worcester, MA, United StatesDepartment of Emergency Medicine, UMass Memorial Medical Center, Worcester, MA, United StatesDepartment of Emergency Medicine, UMass Memorial Medical Center, Worcester, MA, United StatesDepartment of Emergency Medicine, UMass Memorial Medical Center, Worcester, MA, United StatesDepartment of Biology and Biotechnology, Worcester Polytechnique Institute, Worcester, MA, United StatesDepartment of Medicine, University of Massachusetts Medical School, Worcester, MA, United StatesProgram in Microbiome Dynamics, University of Massachusetts Medical School, Worcester, MA, United StatesDepartment of Microbiology and Physiologic Systems, University of Massachusetts Medical School, Worcester, MA, United StatesProgram in Microbiome Dynamics, University of Massachusetts Medical School, Worcester, MA, United StatesDepartment of Microbiology and Physiologic Systems, University of Massachusetts Medical School, Worcester, MA, United StatesDepartment of Emergency Medicine, UMass Memorial Medical Center, Worcester, MA, United StatesProgram in Microbiome Dynamics, University of Massachusetts Medical School, Worcester, MA, United StatesDepartment of Microbiology and Physiologic Systems, University of Massachusetts Medical School, Worcester, MA, United StatesThe oropharyngeal microbiome, the collective genomes of the community of microorganisms that colonizes the upper respiratory tract, is thought to influence the clinical course of infection by respiratory viruses, including Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2), the causative agent of Coronavirus Infectious Disease 2019 (COVID-19). In this study, we examined the oropharyngeal microbiome of suspected COVID-19 patients presenting to the Emergency Department and an inpatient COVID-19 unit with symptoms of acute COVID-19. Of 115 initially enrolled patients, 50 had positive molecular testing for COVID-19+ and had symptom duration of 14 days or less. These patients were analyzed further as progression of disease could most likely be attributed to acute COVID-19 and less likely a secondary process. Of these, 38 (76%) went on to require some form of supplemental oxygen support. To identify functional patterns associated with respiratory illness requiring respiratory support, we applied an interpretable random forest classification machine learning pipeline to shotgun metagenomic sequencing data and select clinical covariates. When combined with clinical factors, both species and metabolic pathways abundance-based models were found to be highly predictive of the need for respiratory support (F1-score 0.857 for microbes and 0.821 for functional pathways). To determine biologically meaningful and highly predictive signals in the microbiome, we applied the Stable and Interpretable RUle Set to the output of the models. This analysis revealed that low abundance of two commensal organisms, Prevotella salivae or Veillonella infantium (< 4.2 and 1.7% respectively), and a low abundance of a pathway associated with LPS biosynthesis (< 0.1%) were highly predictive of developing the need for acute respiratory support (82 and 91.4% respectively). These findings suggest that the composition of the oropharyngeal microbiome in COVID-19 patients may play a role in determining who will suffer from severe disease manifestations.https://www.frontiersin.org/articles/10.3389/fmicb.2022.1009440/fulloropharyngeal microbiomeCOVID-19SARS-CoV-2random forest classificationcommensal organismsPrevotella |
spellingShingle | Evan S. Bradley Evan S. Bradley Abigail L. Zeamer Abigail L. Zeamer Vanni Bucci Vanni Bucci Lindsey Cincotta Marie-Claire Salive Protiva Dutta Shafik Mutaawe Otuwe Anya Christopher Tocci Ann Moormann Doyle V. Ward Doyle V. Ward Beth A. McCormick Beth A. McCormick John P. Haran John P. Haran John P. Haran Oropharyngeal microbiome profiled at admission is predictive of the need for respiratory support among COVID-19 patients Frontiers in Microbiology oropharyngeal microbiome COVID-19 SARS-CoV-2 random forest classification commensal organisms Prevotella |
title | Oropharyngeal microbiome profiled at admission is predictive of the need for respiratory support among COVID-19 patients |
title_full | Oropharyngeal microbiome profiled at admission is predictive of the need for respiratory support among COVID-19 patients |
title_fullStr | Oropharyngeal microbiome profiled at admission is predictive of the need for respiratory support among COVID-19 patients |
title_full_unstemmed | Oropharyngeal microbiome profiled at admission is predictive of the need for respiratory support among COVID-19 patients |
title_short | Oropharyngeal microbiome profiled at admission is predictive of the need for respiratory support among COVID-19 patients |
title_sort | oropharyngeal microbiome profiled at admission is predictive of the need for respiratory support among covid 19 patients |
topic | oropharyngeal microbiome COVID-19 SARS-CoV-2 random forest classification commensal organisms Prevotella |
url | https://www.frontiersin.org/articles/10.3389/fmicb.2022.1009440/full |
work_keys_str_mv | AT evansbradley oropharyngealmicrobiomeprofiledatadmissionispredictiveoftheneedforrespiratorysupportamongcovid19patients AT evansbradley oropharyngealmicrobiomeprofiledatadmissionispredictiveoftheneedforrespiratorysupportamongcovid19patients AT abigaillzeamer oropharyngealmicrobiomeprofiledatadmissionispredictiveoftheneedforrespiratorysupportamongcovid19patients AT abigaillzeamer oropharyngealmicrobiomeprofiledatadmissionispredictiveoftheneedforrespiratorysupportamongcovid19patients AT vannibucci oropharyngealmicrobiomeprofiledatadmissionispredictiveoftheneedforrespiratorysupportamongcovid19patients AT vannibucci oropharyngealmicrobiomeprofiledatadmissionispredictiveoftheneedforrespiratorysupportamongcovid19patients AT lindseycincotta oropharyngealmicrobiomeprofiledatadmissionispredictiveoftheneedforrespiratorysupportamongcovid19patients AT marieclairesalive oropharyngealmicrobiomeprofiledatadmissionispredictiveoftheneedforrespiratorysupportamongcovid19patients AT protivadutta oropharyngealmicrobiomeprofiledatadmissionispredictiveoftheneedforrespiratorysupportamongcovid19patients AT shafikmutaawe oropharyngealmicrobiomeprofiledatadmissionispredictiveoftheneedforrespiratorysupportamongcovid19patients AT otuweanya oropharyngealmicrobiomeprofiledatadmissionispredictiveoftheneedforrespiratorysupportamongcovid19patients AT christophertocci oropharyngealmicrobiomeprofiledatadmissionispredictiveoftheneedforrespiratorysupportamongcovid19patients AT annmoormann oropharyngealmicrobiomeprofiledatadmissionispredictiveoftheneedforrespiratorysupportamongcovid19patients AT doylevward oropharyngealmicrobiomeprofiledatadmissionispredictiveoftheneedforrespiratorysupportamongcovid19patients AT doylevward oropharyngealmicrobiomeprofiledatadmissionispredictiveoftheneedforrespiratorysupportamongcovid19patients AT bethamccormick oropharyngealmicrobiomeprofiledatadmissionispredictiveoftheneedforrespiratorysupportamongcovid19patients AT bethamccormick oropharyngealmicrobiomeprofiledatadmissionispredictiveoftheneedforrespiratorysupportamongcovid19patients AT johnpharan oropharyngealmicrobiomeprofiledatadmissionispredictiveoftheneedforrespiratorysupportamongcovid19patients AT johnpharan oropharyngealmicrobiomeprofiledatadmissionispredictiveoftheneedforrespiratorysupportamongcovid19patients AT johnpharan oropharyngealmicrobiomeprofiledatadmissionispredictiveoftheneedforrespiratorysupportamongcovid19patients |