Oral Microbiome and Subsequent Risk of Head and Neck Squamous Cell Cancer
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Study information
-
Quality control
- Retracted paper
- Contamination issues suspected
- Batch effect issues suspected
- Uncontrolled confounding suspected
- Results are suspect (various reasons)
- Tags applied
study design
Citation
PMID PubMed identifier for scientific articles.
DOI Digital object identifier for electronic documents.
URI
Authors
Kwak S, Wang C, Usyk M, Wu F, Freedman ND, Huang WY, McCullough ML, Um CY, Shrubsole MJ, Cai Q, Li H, Ahn J, Hayes RB
Journal
JAMA oncology
Year
2024
IMPORTANCE: The oral microbiota may be involved in development of head and neck squamous cell cancer (HNSCC), yet current evidence is largely limited to bacterial 16S amplicon sequencing or small retrospective case-control studies. OBJECTIVE: To test whether oral bacterial and fungal microbiomes are associated with subsequent risk of HNSCC development. DESIGN, SETTING, AND PARTICIPANTS: Prospective nested case-control study among participants providing oral samples in 3 epidemiological cohorts, the American Cancer Society Cancer Prevention Study II Nutrition Cohort, the Prostate, Lung, Colorectal, and Ovarian Cancer Screening Trial, and the Southern Community Cohort Study. Two hundred thirty-six patients who prospectively developed HNSCC were identified during a mean (SD) of 5.1 (3.6) years of follow-up. Control participants who remained HNSCC free were selected by 2:1 frequency matching on cohort, age, sex, race and ethnicity, and time since oral sample collection. Data analysis was conducted in 2023. EXPOSURES: Characterization of the oral bacterial microbiome using whole-genome shotgun sequencing and the oral fungal microbiome using internal transcribed spacer sequencing. Association of bacterial and fungal taxa with HNSCC was assessed by analysis of compositions of microbiomes with bias correction. Association with red and orange oral pathogen complexes was tested by logistic regression. A microbial risk score for HNSCC risk was calculated from risk-associated microbiota. MAIN OUTCOMES AND MEASURES: The primary outcome was HNSCC incidence. RESULTS: The study included 236 HNSCC case participants with a mean (SD) age of 60.9 (9.5) years and 24.6% women during a mean of 5.1 (3.6) years of follow-up, and 485 matched control participants. Overall microbiome diversity at baseline was not related to subsequent HNSCC risk; however 13 oral bacterial species were found to be differentially associated with development of HNSCC. The species included the newly identified Prevotella salivae, Streptococcus sanguinis, and Leptotrichia species, as well as several species belonging to beta and gamma Proteobacteria. The red/orange periodontal pathogen complex was moderately associated with HNSCC risk (odds ratio, 1.06 per 1 SD; 95% CI, 1.00-1.12). A 1-SD increase in microbial risk score (created based on 22 bacteria) was associated with a 50% increase in HNSCC risk (multivariate odds ratio, 1.50; 95% CI, 1.21-1.85). No fungal taxa associated with HNSCC risk were identified. CONCLUSIONS AND RELEVANCE: This case-control study yielded compelling evidence that oral bacteria are a risk factor for HNSCC development. The identified bacteria and bacterial complexes hold promise, along with other risk factors, to identify high-risk individuals for personalized prevention of HNSCC.
Experiment 1
Subjects
- Location of subjects
- United States of America
- Host species Species from which microbiome was sampled. Contact us to have more species added.
- Homo sapiens
- Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology
- Head , Neck Adult head,Cephalic area,Head (volume),Head,head,Collum,Neck (volume),Neck,neck
- Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
- Head and neck squamous cell carcinoma carcinoma of the head and neck,craniocervical region squamous cell carcinoma,head and neck squamous cell carcinoma,HNSCC,SCCHN,squamous cell carcinoma of head and neck,squamous cell carcinoma of the head and neck,squamous cell carcinoma, head and neck,squamous cell carcinomas of head and neck,Head and neck squamous cell carcinoma
- Group 0 name Corresponds to the control (unexposed) group for case-control studies
- Healthy Controls
- Group 1 name Corresponds to the case (exposed) group for case-control studies
- Head and neck squamous cell cancer (HNSCC) participants
- Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
- Case participants with Head and neck squamous cell cancer (HNSCC)
- Group 0 sample size Number of subjects in the control (unexposed) group
- 458
- Group 1 sample size Number of subjects in the case (exposed) group
- 236
Lab analysis
- Sequencing type
- WMS
- 16S variable region One or more hypervariable region(s) of the bacterial 16S gene
- Not specified
- Sequencing platform Manufacturer and experimental platform used for quantifying microbial abundance
- Illumina
Statistical Analysis
- Data transformation Data transformation applied to microbial abundance measurements prior to differential abundance testing (if any).
- centered log-ratio
- Statistical test
- ANCOM
- Significance threshold p-value or FDR threshold used for differential abundance testing (if any)
- 0.05
- MHT correction Have statistical tests be corrected for multiple hypothesis testing (MHT)?
- Yes
- Matched on Factors on which subjects have been matched on in a case-control study
- age, ethnic group, time, race, sex, Matched on: "cohort" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.cohort
- Confounders controlled for Confounding factors that have been accounted for by stratification or model adjustment
- age, ethnic group, race, sex, smoking status, Confounders controlled for: "number of cigarettes consumption per day" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.number of cigarettes consumption per day, Confounders controlled for: "alcohol consumption status" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.alcohol consumption status, Confounders controlled for: "grams of ethanol consumption per day" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.grams of ethanol consumption per day, Confounders controlled for: "oral HPV-16 status" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.oral HPV-16 status
Alpha Diversity
- Pielou Quantifies how equal the community is numerically
- unchanged
- Shannon Estimator of species richness and species evenness: more weight on species richness
- unchanged
- Richness Number of species
- decreased
Signature 1
Source: Figure 1, eTable 4
Description: Associations between bacteria species and risk of overall and site-specific Head and Neck squamous cell cancer (HNSCC)
Abundance in Group 1: increased abundance in Head and neck squamous cell cancer (HNSCC) participants
| NCBI | Quality Control | Links |
|---|---|---|
| Pyramidobacter piscolens | ||
| Porphyromonas cangingivalis | ||
| Prevotella sp. HUN102 | ||
| Secundilactobacillus paracollinoides | ||
| Streptococcus gallolyticus | ||
| Streptococcus plurextorum |
Signature 2
Source: Figure 1a, eTable 4
Description: Associations between bacteria species and risk of overall and site-specific Head and Neck squamous cell cancer (HNSCC)
Abundance in Group 1: decreased abundance in Head and neck squamous cell cancer (HNSCC) participants
| NCBI | Quality Control | Links |
|---|---|---|
| Segatella salivae | ||
| Streptococcus sanguinis | ||
| Leptotrichia sp. oral taxon 212 | ||
| Eikenella corrodens | ||
| Rodentibacter pneumotropicus | ||
| Pasteurella multocida | ||
| Simonsiella muelleri |
Revision editor(s): Tosin
Experiment 2
Differences from previous experiment shown
Subjects
- Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology
- Oral cavity Bucca,Buccal cavity,Cavity of mouth,Oral cavity,oral cavity
- Group 1 sample size Number of subjects in the case (exposed) group
- 62
Lab analysis
Statistical Analysis
- Confounders controlled for Confounding factors that have been accounted for by stratification or model adjustment
- age, ethnic group, race, sex, smoking status, Confounders controlled for: "number of cigarettes consumption per day" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.number of cigarettes consumption per day, Confounders controlled for: "grams of ethanol consumption per day" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.grams of ethanol consumption per day, Confounders controlled for: "alcohol consumption status" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.alcohol consumption status, Confounders controlled for: "oral HPV-16 status" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.oral HPV-16 status
Alpha Diversity
- Pielou Quantifies how equal the community is numerically
- unchanged
- Shannon Estimator of species richness and species evenness: more weight on species richness
- unchanged
- Richness Number of species
- decreased
Signature 1
Source: eTable 4
Description: Associations between bacteria species and risk of overall and site-specific Head and Neck squamous cell cancer (HNSCC)
Abundance in Group 1: increased abundance in Head and neck squamous cell cancer (HNSCC) participants
| NCBI | Quality Control | Links |
|---|---|---|
| Campylobacter curvus | ||
| Schleiferilactobacillus harbinensis | ||
| Streptobacillus moniliformis | ||
| Treponema medium | ||
| Capnocytophaga sp. oral taxon 338 |
Revision editor(s): Tosin
Signature 2
Source: eTable 4
Description: Associations between bacteria species and risk of overall and site-specific Head and Neck squamous cell cancer (HNSCC)
Abundance in Group 1: decreased abundance in Head and neck squamous cell cancer (HNSCC) participants
Revision editor(s): Tosin
Experiment 3
Differences from previous experiment shown
Subjects
- Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology
- Pharynx Anterior part of foregut,Pharyngeal tube,Pharynx,pharynx
- Group 1 sample size Number of subjects in the case (exposed) group
- 63
Lab analysis
Statistical Analysis
- Confounders controlled for Confounding factors that have been accounted for by stratification or model adjustment
- age, ethnic group, race, sex, smoking status, Confounders controlled for: "alcohol consumption status" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.alcohol consumption status, Confounders controlled for: "oral HPV-16 status" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.oral HPV-16 status, Confounders controlled for: "grams of ethanol consumption per day" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.grams of ethanol consumption per day, Confounders controlled for: "number of cigarettes consumption per day" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.number of cigarettes consumption per day
Alpha Diversity
- Pielou Quantifies how equal the community is numerically
- unchanged
- Shannon Estimator of species richness and species evenness: more weight on species richness
- unchanged
- Richness Number of species
- decreased
Signature 1
Source: eTable 4
Description: Associations between bacteria species and risk of overall and site-specific Head and Neck squamous cell cancer (HNSCC)
Abundance in Group 1: increased abundance in Head and neck squamous cell cancer (HNSCC) participants
Revision editor(s): Tosin
Signature 2
Source: eTable 4
Description: Associations between bacteria species and risk of overall and site-specific Head and Neck squamous cell cancer (HNSCC)
Abundance in Group 1: decreased abundance in Head and neck squamous cell cancer (HNSCC) participants
Revision editor(s): Tosin
Experiment 4
Differences from previous experiment shown
Subjects
- Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology
- Larynx Kehlkopf@de,Larynx,larynx
- Group 1 sample size Number of subjects in the case (exposed) group
- 111
Lab analysis
Statistical Analysis
- Confounders controlled for Confounding factors that have been accounted for by stratification or model adjustment
- age, ethnic group, race, sex, smoking status, Confounders controlled for: "oral HPV-16 status" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.oral HPV-16 status, Confounders controlled for: "grams of ethanol consumption per day" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.grams of ethanol consumption per day, Confounders controlled for: "alcohol consumption status" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.alcohol consumption status, Confounders controlled for: "nunber of cigarettes consumption per day" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.nunber of cigarettes consumption per day
Alpha Diversity
- Pielou Quantifies how equal the community is numerically
- unchanged
- Shannon Estimator of species richness and species evenness: more weight on species richness
- unchanged
- Richness Number of species
- decreased
Signature 1
Source: eTable 4
Description: Associations between bacteria species and risk of overall and site-specific Head and Neck squamous cell cancer (HNSCC)
Abundance in Group 1: increased abundance in Head and neck squamous cell cancer (HNSCC) participants
Revision editor(s): Tosin
Signature 2
Source: eTable 4
Description: Associations between bacteria species and risk of overall and site-specific Head and Neck squamous cell cancer (HNSCC)
Abundance in Group 1: decreased abundance in Head and neck squamous cell cancer (HNSCC) participants
Revision editor(s): Tosin
Experiment 5
Differences from previous experiment shown
Subjects
- Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology
- Oral cavity Bucca,Buccal cavity,Cavity of mouth,Oral cavity,oral cavity
- Group 1 sample size Number of subjects in the case (exposed) group
- 62
Lab analysis
Statistical Analysis
- Confounders controlled for Confounding factors that have been accounted for by stratification or model adjustment
- age, ethnic group, race, sex, smoking status, Confounders controlled for: "number of cigarettes consumption per day" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.number of cigarettes consumption per day, Confounders controlled for: "grams of ethanol consumption per day" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.grams of ethanol consumption per day, Confounders controlled for: "oral HPV-16 status" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.oral HPV-16 status, Confounders controlled for: "alcohol consumption status" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.alcohol consumption status
Alpha Diversity
- Pielou Quantifies how equal the community is numerically
- unchanged
- Shannon Estimator of species richness and species evenness: more weight on species richness
- unchanged
- Richness Number of species
- decreased
Signature 1
Source: eTable 5
Description: Associations between fungal species and risk of overall and site-specific Head and Neck squamous cell cancer (HNSCC)
Abundance in Group 1: increased abundance in Head and neck squamous cell cancer (HNSCC) participants
| NCBI | Quality Control | Links |
|---|---|---|
| Penicillium neocrassum |
Revision editor(s): Tosin
Experiment 6
Differences from previous experiment shown
Subjects
- Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology
- Pharynx Anterior part of foregut,Pharyngeal tube,Pharynx,pharynx
- Group 1 sample size Number of subjects in the case (exposed) group
- 63
Lab analysis
Statistical Analysis
- Confounders controlled for Confounding factors that have been accounted for by stratification or model adjustment
- age, ethnic group, race, sex, smoking status, Confounders controlled for: "oral HPV-16 status" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.oral HPV-16 status, Confounders controlled for: "alcohol consumption status" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.alcohol consumption status, Confounders controlled for: "grams of ethanol consumption per day" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.grams of ethanol consumption per day, Confounders controlled for: "number of cigarettes consumption per day" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.number of cigarettes consumption per day
Alpha Diversity
- Pielou Quantifies how equal the community is numerically
- unchanged
- Shannon Estimator of species richness and species evenness: more weight on species richness
- unchanged
- Richness Number of species
- decreased
Signature 1
Source: eTable 5
Description: Associations between fungal species and risk of overall and site-specific Head and Neck squamous cell cancer (HNSCC)
Abundance in Group 1: increased abundance in Head and neck squamous cell cancer (HNSCC) participants
| NCBI | Quality Control | Links |
|---|---|---|
| Malassezia sympodialis |
Revision editor(s): Tosin
Signature 2
Source: eTable 5
Description: Associations between fungal species and risk of overall and site-specific Head and Neck squamous cell cancer (HNSCC)
Abundance in Group 1: decreased abundance in Head and neck squamous cell cancer (HNSCC) participants
| NCBI | Quality Control | Links |
|---|---|---|
| Orbilia sp. |
Revision editor(s): Tosin
Experiment 7
Differences from previous experiment shown
Subjects
- Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology
- Larynx Kehlkopf@de,Larynx,larynx
- Group 1 sample size Number of subjects in the case (exposed) group
- 111
Lab analysis
Statistical Analysis
- Confounders controlled for Confounding factors that have been accounted for by stratification or model adjustment
- age, ethnic group, race, sex, smoking status, Confounders controlled for: "number of cigarettes consumption per day" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.number of cigarettes consumption per day, Confounders controlled for: "alcohol consumption status" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.alcohol consumption status, Confounders controlled for: "grams of ethanol consumption per day" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.grams of ethanol consumption per day, Confounders controlled for: "oral HPV-16 status" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.oral HPV-16 status
Alpha Diversity
- Pielou Quantifies how equal the community is numerically
- unchanged
- Shannon Estimator of species richness and species evenness: more weight on species richness
- unchanged
- Richness Number of species
- decreased
Signature 1
Source: eTable 5
Description: Associations between fungal species and risk of overall and site-specific Head and Neck squamous cell cancer (HNSCC)
Abundance in Group 1: increased abundance in Head and neck squamous cell cancer (HNSCC) participants
| NCBI | Quality Control | Links |
|---|---|---|
| unclassified Pleosporales |
Revision editor(s): Tosin
Signature 2
Source: eTable 5
Description: Associations between fungal species and risk of overall and site-specific Head and Neck squamous cell cancer (HNSCC)
Abundance in Group 1: decreased abundance in Head and neck squamous cell cancer (HNSCC) participants
| NCBI | Quality Control | Links |
|---|---|---|
| Vishniacozyma victoriae | ||
| Parengyodontium album |
Revision editor(s): Tosin
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