The eukaryotic gut virome in hematopoietic stem cell transplantation: new clues in enteric graft-versus-host disease

Nat Med. 2017 Sep;23(9):1080-1085. doi: 10.1038/nm.4380. Epub 2017 Jul 31.

Abstract

Much attention has been focused on the role of the bacterial microbiome in human health, but the virome is understudied. Although previously investigated in individuals with inflammatory bowel diseases or solid-organ transplants, virome dynamics in allogeneic hematopoietic stem cell transplantation (HSCT) and enteric graft-versus-host disease (GVHD) remain unexplored. Here we characterize the longitudinal gut virome in 44 recipients of HSCT using metagenomics. A viral 'bloom' was identified, and significant increases were demonstrated in the overall proportion of vertebrate viral sequences following transplantation (P = 0.02). Increases in both the rates of detection (P < 0.0001) and number of sequences (P = 0.047) of persistent DNA viruses (anelloviruses, herpesviruses, papillomaviruses and polyomaviruses) over time were observed in individuals with enteric GVHD relative to those without, a finding accompanied by a reduced phage richness (P = 0.01). Picobirnaviruses were detected in 18 individuals (40.9%), more frequently before or within a week after transplant than at later time points (P = 0.008). In a time-dependent Cox proportional-hazards model, picobirnaviruses were predictive of the occurrence of severe enteric GVHD (hazard ratio, 2.66; 95% confidence interval (CI) = 1.46-4.86; P = 0.001), and correlated with higher fecal levels of two GVHD severity markers, calprotectin and α1-antitrypsin. These results reveal a progressive expansion of vertebrate viral infections over time following HSCT, and they suggest an unexpected association of picobirnaviruses with early post-transplant GVHD.

MeSH terms

  • Adolescent
  • Adult
  • Aged
  • Anelloviridae / genetics
  • Anelloviridae / immunology
  • DNA, Viral / analysis*
  • Feces / chemistry
  • Female
  • Gastrointestinal Microbiome / genetics
  • Gastrointestinal Microbiome / immunology*
  • Graft vs Host Disease / immunology*
  • Hematopoietic Stem Cell Transplantation*
  • Herpesviridae / genetics
  • Herpesviridae / immunology
  • Humans
  • Intestinal Diseases / immunology*
  • Intestines / virology*
  • Leukocyte L1 Antigen Complex / metabolism
  • Male
  • Metagenomics
  • Middle Aged
  • Papillomaviridae / genetics
  • Papillomaviridae / immunology
  • Picobirnavirus / genetics
  • Picobirnavirus / immunology
  • Polyomaviridae / genetics
  • Polyomaviridae / immunology
  • Proportional Hazards Models
  • Risk Factors
  • Severity of Illness Index
  • Transplantation, Homologous
  • Young Adult
  • alpha 1-Antitrypsin / metabolism

Substances

  • DNA, Viral
  • Leukocyte L1 Antigen Complex
  • alpha 1-Antitrypsin