HIV-induced immunosuppression is associated with colonization of the proximal gut by environmental bacteria

Liying Yang, Michael A. Poles, Gene S. Fisch, Yingfei Ma, Carlos Nossa, Joan A. Phelan, Zhiheng Pei

Research output: Contribution to journalArticle

Abstract

Objectives: To evaluate the impact of HIV infection on colonization resistance in the proximal gut. Design: It was a case-control study. Methods: We contrasted microbiota composition between eight HIV-1-infected patients and eight HIV-negative controls to characterize community alteration and detect exogenous bacteria in the esophagus, stomach, and duodenum, as well as the mouth using a universal 16s ribosomal RNA gene survey and correlated the findings with HIV serostatus and peripheral blood T-cell counts. Results: HIV infection was associated with an enrichment of Proteobacteria (P=0.020) and depletion of Firmicutes (P = 0.005) in the proximal gut. In particular, environmental species Burkholderia fungorum and Bradyrhizobium pachyrhizi colonized the duodenum of HIV patients who had abnormal blood CD4 + T-cell counts but were absent in HIV-negative controls or HIV patients whose CD4 + cell counts were normal. The two species coexisted and exhibited a decreasing trend proximally toward the stomach and esophagus and were virtually absent in the mouth. B. fungorum always outnumbered B. pachyrhizi in a ratio of approximately 15 to 1 regardless of the body sites (P <0.0001, r 2 = 0.965). Their abundance was inversely correlated with CD4 + cell counts (P = 0.004) but not viral load. Overgrowth of potential opportunistic pathogens for example, Prevotella, Fusobacterium, and Ralstonia and depletion of beneficial bacteria, for example, Lactobacillus was also observed in HIV patients. Conclusions: The colonization of the duodenum by environmental bacteria reflects loss of colonization resistance in HIV infection. Their correlation with CD4 + cell counts suggests that compromised immunity could be responsible for the observed invasion by exogenous microbes.

Original languageEnglish (US)
Pages (from-to)19-29
Number of pages11
JournalAIDS
Volume30
Issue number1
DOIs
StatePublished - Jan 2 2016

Fingerprint

Immunosuppression
HIV
CD4 Lymphocyte Count
Bacteria
Duodenum
HIV Infections
Esophagus
Mouth
Stomach
Ralstonia
Fusobacterium
Prevotella
16S Ribosomal RNA
Burkholderia
Bradyrhizobium
T-Lymphocytes
Proteobacteria
Blood Cell Count
Microbiota
Lactobacillus

Keywords

  • Bradyrhizobium pachyrhizi
  • Burkholderia fungorum
  • CD4 +
  • colonization resistance
  • duodenum
  • dysbiosis
  • environmental bacteria
  • HIV-1
  • Lactobacillus
  • microbiome
  • microbiota
  • proximal gut

ASJC Scopus subject areas

  • Immunology and Allergy
  • Immunology
  • Infectious Diseases

Cite this

Yang, L., Poles, M. A., Fisch, G. S., Ma, Y., Nossa, C., Phelan, J. A., & Pei, Z. (2016). HIV-induced immunosuppression is associated with colonization of the proximal gut by environmental bacteria. AIDS, 30(1), 19-29. https://doi.org/10.1097/QAD.0000000000000935

HIV-induced immunosuppression is associated with colonization of the proximal gut by environmental bacteria. / Yang, Liying; Poles, Michael A.; Fisch, Gene S.; Ma, Yingfei; Nossa, Carlos; Phelan, Joan A.; Pei, Zhiheng.

In: AIDS, Vol. 30, No. 1, 02.01.2016, p. 19-29.

Research output: Contribution to journalArticle

Yang, L, Poles, MA, Fisch, GS, Ma, Y, Nossa, C, Phelan, JA & Pei, Z 2016, 'HIV-induced immunosuppression is associated with colonization of the proximal gut by environmental bacteria', AIDS, vol. 30, no. 1, pp. 19-29. https://doi.org/10.1097/QAD.0000000000000935
Yang, Liying ; Poles, Michael A. ; Fisch, Gene S. ; Ma, Yingfei ; Nossa, Carlos ; Phelan, Joan A. ; Pei, Zhiheng. / HIV-induced immunosuppression is associated with colonization of the proximal gut by environmental bacteria. In: AIDS. 2016 ; Vol. 30, No. 1. pp. 19-29.
@article{012381648dcf42d887dbc384327aa2a1,
title = "HIV-induced immunosuppression is associated with colonization of the proximal gut by environmental bacteria",
abstract = "Objectives: To evaluate the impact of HIV infection on colonization resistance in the proximal gut. Design: It was a case-control study. Methods: We contrasted microbiota composition between eight HIV-1-infected patients and eight HIV-negative controls to characterize community alteration and detect exogenous bacteria in the esophagus, stomach, and duodenum, as well as the mouth using a universal 16s ribosomal RNA gene survey and correlated the findings with HIV serostatus and peripheral blood T-cell counts. Results: HIV infection was associated with an enrichment of Proteobacteria (P=0.020) and depletion of Firmicutes (P = 0.005) in the proximal gut. In particular, environmental species Burkholderia fungorum and Bradyrhizobium pachyrhizi colonized the duodenum of HIV patients who had abnormal blood CD4 + T-cell counts but were absent in HIV-negative controls or HIV patients whose CD4 + cell counts were normal. The two species coexisted and exhibited a decreasing trend proximally toward the stomach and esophagus and were virtually absent in the mouth. B. fungorum always outnumbered B. pachyrhizi in a ratio of approximately 15 to 1 regardless of the body sites (P <0.0001, r 2 = 0.965). Their abundance was inversely correlated with CD4 + cell counts (P = 0.004) but not viral load. Overgrowth of potential opportunistic pathogens for example, Prevotella, Fusobacterium, and Ralstonia and depletion of beneficial bacteria, for example, Lactobacillus was also observed in HIV patients. Conclusions: The colonization of the duodenum by environmental bacteria reflects loss of colonization resistance in HIV infection. Their correlation with CD4 + cell counts suggests that compromised immunity could be responsible for the observed invasion by exogenous microbes.",
keywords = "Bradyrhizobium pachyrhizi, Burkholderia fungorum, CD4 +, colonization resistance, duodenum, dysbiosis, environmental bacteria, HIV-1, Lactobacillus, microbiome, microbiota, proximal gut",
author = "Liying Yang and Poles, {Michael A.} and Fisch, {Gene S.} and Yingfei Ma and Carlos Nossa and Phelan, {Joan A.} and Zhiheng Pei",
year = "2016",
month = "1",
day = "2",
doi = "10.1097/QAD.0000000000000935",
language = "English (US)",
volume = "30",
pages = "19--29",
journal = "AIDS",
issn = "0269-9370",
publisher = "Lippincott Williams and Wilkins",
number = "1",

}

TY - JOUR

T1 - HIV-induced immunosuppression is associated with colonization of the proximal gut by environmental bacteria

AU - Yang, Liying

AU - Poles, Michael A.

AU - Fisch, Gene S.

AU - Ma, Yingfei

AU - Nossa, Carlos

AU - Phelan, Joan A.

AU - Pei, Zhiheng

PY - 2016/1/2

Y1 - 2016/1/2

N2 - Objectives: To evaluate the impact of HIV infection on colonization resistance in the proximal gut. Design: It was a case-control study. Methods: We contrasted microbiota composition between eight HIV-1-infected patients and eight HIV-negative controls to characterize community alteration and detect exogenous bacteria in the esophagus, stomach, and duodenum, as well as the mouth using a universal 16s ribosomal RNA gene survey and correlated the findings with HIV serostatus and peripheral blood T-cell counts. Results: HIV infection was associated with an enrichment of Proteobacteria (P=0.020) and depletion of Firmicutes (P = 0.005) in the proximal gut. In particular, environmental species Burkholderia fungorum and Bradyrhizobium pachyrhizi colonized the duodenum of HIV patients who had abnormal blood CD4 + T-cell counts but were absent in HIV-negative controls or HIV patients whose CD4 + cell counts were normal. The two species coexisted and exhibited a decreasing trend proximally toward the stomach and esophagus and were virtually absent in the mouth. B. fungorum always outnumbered B. pachyrhizi in a ratio of approximately 15 to 1 regardless of the body sites (P <0.0001, r 2 = 0.965). Their abundance was inversely correlated with CD4 + cell counts (P = 0.004) but not viral load. Overgrowth of potential opportunistic pathogens for example, Prevotella, Fusobacterium, and Ralstonia and depletion of beneficial bacteria, for example, Lactobacillus was also observed in HIV patients. Conclusions: The colonization of the duodenum by environmental bacteria reflects loss of colonization resistance in HIV infection. Their correlation with CD4 + cell counts suggests that compromised immunity could be responsible for the observed invasion by exogenous microbes.

AB - Objectives: To evaluate the impact of HIV infection on colonization resistance in the proximal gut. Design: It was a case-control study. Methods: We contrasted microbiota composition between eight HIV-1-infected patients and eight HIV-negative controls to characterize community alteration and detect exogenous bacteria in the esophagus, stomach, and duodenum, as well as the mouth using a universal 16s ribosomal RNA gene survey and correlated the findings with HIV serostatus and peripheral blood T-cell counts. Results: HIV infection was associated with an enrichment of Proteobacteria (P=0.020) and depletion of Firmicutes (P = 0.005) in the proximal gut. In particular, environmental species Burkholderia fungorum and Bradyrhizobium pachyrhizi colonized the duodenum of HIV patients who had abnormal blood CD4 + T-cell counts but were absent in HIV-negative controls or HIV patients whose CD4 + cell counts were normal. The two species coexisted and exhibited a decreasing trend proximally toward the stomach and esophagus and were virtually absent in the mouth. B. fungorum always outnumbered B. pachyrhizi in a ratio of approximately 15 to 1 regardless of the body sites (P <0.0001, r 2 = 0.965). Their abundance was inversely correlated with CD4 + cell counts (P = 0.004) but not viral load. Overgrowth of potential opportunistic pathogens for example, Prevotella, Fusobacterium, and Ralstonia and depletion of beneficial bacteria, for example, Lactobacillus was also observed in HIV patients. Conclusions: The colonization of the duodenum by environmental bacteria reflects loss of colonization resistance in HIV infection. Their correlation with CD4 + cell counts suggests that compromised immunity could be responsible for the observed invasion by exogenous microbes.

KW - Bradyrhizobium pachyrhizi

KW - Burkholderia fungorum

KW - CD4 +

KW - colonization resistance

KW - duodenum

KW - dysbiosis

KW - environmental bacteria

KW - HIV-1

KW - Lactobacillus

KW - microbiome

KW - microbiota

KW - proximal gut

UR - http://www.scopus.com/inward/record.url?scp=84957657749&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84957657749&partnerID=8YFLogxK

U2 - 10.1097/QAD.0000000000000935

DO - 10.1097/QAD.0000000000000935

M3 - Article

C2 - 26731752

AN - SCOPUS:84957657749

VL - 30

SP - 19

EP - 29

JO - AIDS

JF - AIDS

SN - 0269-9370

IS - 1

ER -