Oral Microbiome in HIV-Infected Women: Shifts in the Abundance of Pathogenic and Beneficial Bacteria Are Associated with Aging, HIV Load, CD4 Count, and Antiretroviral Therapy

From BugSigDB
Reviewed Marked as Reviewed by Folakunmi on 2024-2-25
Citation
PMID PubMed identifier for scientific articles.
DOI Digital object identifier for electronic documents.
URI
Authors
Lewy T, Hong BY, Weiser B, Burger H, Tremain A, Weinstock G, Anastos K, George MD
Journal
AIDS research and human retroviruses
Year
2019
Keywords:
HIV, aging, disease progression, opportunistic infection, oral microbiome, saliva
Human immunodeficiency virus (HIV)-associated nonacquired immunodeficiency syndrome (AIDS) conditions, such as cardiovascular disease, diabetes, osteoporosis, and dementia are more prevalent in older than in young adult HIV-infected subjects. Although the oral microbiome has been studied as a window into pathogenesis in aging populations, its relationship to HIV disease progression, opportunistic infections, and HIV-associated non-AIDS conditions is not well understood. We utilized 16S rDNA-based pyrosequencing to compare the salivary microbiome in three groups: (1) Chronically HIV-infected women >50 years of age (aging); (2) HIV-infected women <35 years of age (young adult); and (3) HIV-uninfected age-matched women. We also examined correlations between salivary dysbiosis, plasma HIV RNA, CD4+ T cell depletion, and opportunistic oral infections. In both aging and young adult women, HIV infection was associated with salivary dysbiosis characterized by increased abundance of Prevotella melaninogenica and Rothia mucilaginosa. Aging was associated with increased bacterial diversity in both uninfected and HIV-infected women. In HIV-infected women with oral coinfections, aging was also associated with reduced abundance of the common commensal Veillonella parvula. Patients taking antiretroviral therapy showed increased numbers of Neisseria and Haemophilus. High plasma HIV RNA levels correlated positively with the presence of Prevotella and Veillonella, and negatively with the abundance of potentially beneficial Streptococcus and Lactobacillus. Circulating CD4+ T cell numbers correlated positively with the abundance of Streptococcus and Lactobacillus. Our findings extend previous studies of the role of the microbiome in HIV pathogenesis, providing new evidence that HIV infection is associated with a shift toward an increased pathogenic footprint of the salivary microbiome. Taken together, the data suggest a complex relationship, worthy of additional study, between chronic dysbiosis in the oral cavity, aging, viral burden, CD4+ T cell depletion, and long-term antiretroviral therapy.

Experiment 1


Reviewed Marked as Reviewed by Folakunmi on 2024-2-25

Curated date: 2021/01/10

Curator: WikiWorks

Revision editor(s): Lwaldron, WikiWorks, Atrayees

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
Saliva Sailva normalis,Saliva atomaris,Saliva molecularis,Salivary gland secretion,Saliva,saliva
Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
HIV infection [X]Human immunodeficiency virus disease,[X]Human immunodeficiency virus disease (disorder),[X]Unspecified human immunodeficiency virus [HIV] disease,[X]Unspecified human immunodeficiency virus [HIV] disease (disorder),HIV - Human immunodeficiency virus infection,HIV INFECT,HIV Infection,HIV infection,HIV Infections,HIV infectious disease,HTLV III INFECT,HTLV III Infections,HTLV III LAV INFECT,HTLV III LAV Infections,HTLV WIII INFECTIONS,HTLV WIII LAV INFECTIONS,HTLV-III Infection,HTLV-III Infections,HTLV-III-LAV Infection,HTLV-III-LAV Infections,HUMAN IMMUNO VIRUS DIS,human immunodeficiency virus,Human immunodeficiency virus [HIV] disease,HUMAN IMMUNOdeficiency VIRUS [HIV] INFECTION,Human immunodeficiency virus caused disease or disorder,Human immunodeficiency virus disease,Human immunodeficiency virus disease (disorder),Human immunodeficiency virus disease or disorder,Human immunodeficiency virus infection,Human immunodeficiency virus infection (disorder),Human immunodeficiency virus infection, NOS,Human immunodeficiency virus infectious disease,human immunodeficiency virus infectious disease,Infection, HIV,Infection, HTLV-III,Infection, HTLV-III-LAV,Infections, HIV,Infections, HTLV-III,Infections, HTLV-III-LAV,LYMPHOTROPIC VIRUS TYPE III INFECTIONS HUMAN T,T LYMPHOTROPIC VIRUS TYPE III INFECT HUMAN,T Lymphotropic Virus Type III Infections, Human,T-Lymphotropic Virus Type III Infections, Human,Unspecified human immunodeficiency virus [HIV] disease (disorder),hIV infection
Group 0 name Corresponds to the control (unexposed) group for case-control studies
Age-matched HIV-uninfected women
Group 1 name Corresponds to the case (exposed) group for case-control studies
HIV-positive women who have been taking ART for more than 1 year
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
HIV-positive women who have been taking antiretroviral therapy (ART) for more than 1 year
Group 0 sample size Number of subjects in the control (unexposed) group
3
Group 1 sample size Number of subjects in the case (exposed) group
3

Lab analysis

Sequencing type
16S
16S variable region One or more hypervariable region(s) of the bacterial 16S gene
V3-V4
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).
relative abundances
Statistical test
Mann-Whitney (Wilcoxon)
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)?
No
Matched on Factors on which subjects have been matched on in a case-control study
age

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
increased

Signature 1

Reviewed Marked as Reviewed by Folakunmi on 2024-2-24

Curated date: 2021/01/10

Curator: Michael Lutete

Revision editor(s): WikiWorks, Atrayees

Source: Supplementary Figure S3

Description: Differences in abundance of salivary bacteria between HIV uninfected women and HIV-positive women on ART

Abundance in Group 1: increased abundance in HIV-positive women who have been taking ART for more than 1 year

NCBI Quality ControlLinks
Oribacterium
Moryella

Revision editor(s): WikiWorks, Atrayees

Experiment 2


Reviewed Marked as Reviewed by Folakunmi on 2024-2-25

Curated date: 2021/01/10

Curator: WikiWorks

Revision editor(s): Lwaldron, WikiWorks, Atrayees

Differences from previous experiment shown

Subjects

Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
HIV infection , Oral candidiasis [X]Human immunodeficiency virus disease,[X]Human immunodeficiency virus disease (disorder),[X]Unspecified human immunodeficiency virus [HIV] disease,[X]Unspecified human immunodeficiency virus [HIV] disease (disorder),HIV - Human immunodeficiency virus infection,HIV INFECT,HIV Infection,HIV infection,HIV Infections,HIV infectious disease,HTLV III INFECT,HTLV III Infections,HTLV III LAV INFECT,HTLV III LAV Infections,HTLV WIII INFECTIONS,HTLV WIII LAV INFECTIONS,HTLV-III Infection,HTLV-III Infections,HTLV-III-LAV Infection,HTLV-III-LAV Infections,HUMAN IMMUNO VIRUS DIS,human immunodeficiency virus,Human immunodeficiency virus [HIV] disease,HUMAN IMMUNOdeficiency VIRUS [HIV] INFECTION,Human immunodeficiency virus caused disease or disorder,Human immunodeficiency virus disease,Human immunodeficiency virus disease (disorder),Human immunodeficiency virus disease or disorder,Human immunodeficiency virus infection,Human immunodeficiency virus infection (disorder),Human immunodeficiency virus infection, NOS,Human immunodeficiency virus infectious disease,human immunodeficiency virus infectious disease,Infection, HIV,Infection, HTLV-III,Infection, HTLV-III-LAV,Infections, HIV,Infections, HTLV-III,Infections, HTLV-III-LAV,LYMPHOTROPIC VIRUS TYPE III INFECTIONS HUMAN T,T LYMPHOTROPIC VIRUS TYPE III INFECT HUMAN,T Lymphotropic Virus Type III Infections, Human,T-Lymphotropic Virus Type III Infections, Human,Unspecified human immunodeficiency virus [HIV] disease (disorder),hIV infection,Candidiasis of mouth,candidiasis of mouth,Candidiasis of mouth (disorder),Candidiasis, Oral,mouth candidiasis,oral candidiasis,Oral moniliasis,oral moniliasis,thrush,thrush (disorder),Thrush, oral,thrush, oral,Oral candidiasis
Group 0 name Corresponds to the control (unexposed) group for case-control studies
Age-matched HIV-uninfected womenn
Group 1 name Corresponds to the case (exposed) group for case-control studies
HIV-positive women with oral candidiasis
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
HIV-positive women with oral candidiasis

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
increased

Signature 1

Reviewed Marked as Reviewed by Folakunmi on 2024-2-24

Curated date: 2021/01/10

Curator: Michael Lutete

Revision editor(s): WikiWorks, Atrayees

Source: Supplementary Figure S3

Description: Differences in abundance of salivary bacteria between HIV uninfected women and HIV-positive women coinfected with oral candidiasis

Abundance in Group 1: increased abundance in HIV-positive women with oral candidiasis

NCBI Quality ControlLinks
Veillonella
Lachnospiraceae

Revision editor(s): WikiWorks, Atrayees

Experiment 3


Reviewed Marked as Reviewed by Folakunmi on 2024-2-24

Curated date: 2021/01/10

Curator: WikiWorks

Revision editor(s): WikiWorks, Atrayees

Differences from previous experiment shown

Subjects

Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
Age Age,age
Group 0 name Corresponds to the control (unexposed) group for case-control studies
HIV uninfected women who are less than 35 years of age
Group 1 name Corresponds to the case (exposed) group for case-control studies
HIV uninfected women who are 50 years of age or older
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
HIV-negative women who are 50 years of age or older
Group 0 sample size Number of subjects in the control (unexposed) group
4
Group 1 sample size Number of subjects in the case (exposed) group
4

Lab analysis

Statistical Analysis

Matched on Factors on which subjects have been matched on in a case-control study
Not specified

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
increased

Signature 1

Reviewed Marked as Reviewed by Folakunmi on 2024-2-24

Curated date: 2021/01/10

Curator: Michael Lutete

Revision editor(s): WikiWorks, Atrayees

Source: Supplementary Figure S3

Description: Differences in abundance of salivary bacteria between young HIV uninfected women and old HIV uninfected women

Abundance in Group 1: increased abundance in HIV uninfected women who are 50 years of age or older

NCBI Quality ControlLinks
Oribacterium
Moryella

Revision editor(s): WikiWorks, Atrayees

Experiment 4


Reviewed Marked as Reviewed by Folakunmi on 2024-2-25

Curated date: 2023/08/24

Curator: Atrayees

Revision editor(s): Atrayees, Folakunmi

Differences from previous experiment shown

Subjects

Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
Coinfection , Age Coinfection,coinfection,Age,age
Group 0 name Corresponds to the control (unexposed) group for case-control studies
young HIV-infected group without coinfection
Group 1 name Corresponds to the case (exposed) group for case-control studies
aging HIV-infected women with coinfections
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
aging HIV-infected women with coinfections; Hairy leukoplakia, oral candida, kaposi's sarcoma, HPV

Lab analysis

Statistical Analysis

Statistical test
LEfSe
LDA Score above Threshold for the linear discriminant analysis (LDA) score for studies using the popular LEfSe tool
2

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
increased

Signature 1

Reviewed Marked as Reviewed by Folakunmi on 2024-2-24

Curated date: 2023/08/24

Curator: Atrayees

Revision editor(s): Atrayees, Folakunmi

Source: Figure 5

Description: LEfSe was performed to identify statistically different bacterial taxa in their relative abundance between young adult HIV-infected women versus aging HIV-infected women with coinfection.

Abundance in Group 1: increased abundance in aging HIV-infected women with coinfections

NCBI Quality ControlLinks
Desulfovibrio sp.
Lactobacillus sp.
Limosilactobacillus reuteri
Mucispirillum schaedleri
Odoribacter sp.
unclassified Aerococcaceae
unclassified Clostridiaceae
unclassified Streptococcaceae
Lactococcus sp.
Oscillospira
unclassified Bacteria

Revision editor(s): Atrayees, Folakunmi

Signature 2

Reviewed Marked as Reviewed by Folakunmi on 2024-2-24

Curated date: 2023/08/24

Curator: Atrayees

Revision editor(s): Atrayees

Source: Figure 5

Description: LEfSe was performed to identify statistically different bacterial taxa in their relative abundance between young adult HIV-infected women versus aging HIV-infected women with coinfection.

Abundance in Group 1: decreased abundance in aging HIV-infected women with coinfections

NCBI Quality ControlLinks
Solobacterium moorei
Bulleidia sp.
Veillonella parvula
unclassified Mycoplasmatota

Revision editor(s): Atrayees