Naturally Acquired Picornavirus Infections in Primates at the Dhaka Zoo

Enteroviruses (EVs) are a genetically and antigenically diverse group of viruses infecting humans. A mostly distinct set of EV variants have additionally been documented to infect wild apes and several, primarily captive, Old World monkey (OWM) species. To investigate the prevalence and genetic characteristics of EVs infecting OWMs in the wild, fecal samples from mandrills (Mandrillus sphinx) and other species collected in remote regions of southern Cameroon were screened for EV RNA. Remarkably high rates of EV positivity were detected in M. sphinx (100 of 102 screened), Cercocebus torquatus (7/7), and Cercopithecus cephus (2/4), with high viral loads indicative of active infection. Genetic characterization in VP4/VP2 and VP1 regions allowed EV variants to be assigned to simian species H (EV-H) and EV-J (including one or more new types), while seven matched simian EV-B variants, SA5 and EV110 (chimpanzee). Sequences from the remaining 70 formed a new genetic group distinct in VP4/2 and VP1 region from all currently recognized human or simian EV species. Complete genome sequences were obtained from three to determine their species assignment. In common with EV-J and the EV-A A13 isolate, new group sequences were chimeric, being most closely related to EV-A in capsid genes and to EV-B in the nonstructural gene region. Further recombination events created different groupings in 5= and 3= untranslated regions. While clearly a distinct EV group, the hybrid nature of new variants prevented their unambiguous classification as either members of a new species or as divergent members of EV-A using current International Committee on Taxonomy of Viruses (ICTV) assignment criteria. IMPORTANCEThis study is the first large-scale investigation of the frequency of infection and diversity of enteroviruses (EVs) infecting monkeys (primarily mandrills) in the wild. Our findings demonstrate extremely high frequencies of active infection (95%) among mandrills and other Old World monkey species inhabiting remote regions of Cameroon without human contact. EV variants detected were distinct from those infecting human populations, comprising members of enterovirus species B, J, and H and a large novel group of viruses most closely related to species A in the P1 region. The viral sequences obtained contribute substantially to our growing understanding of the genetic diversity of EVs and the existence of interspecies chimerism that characterizes the novel variants in the current study, as well as in previously characterized species A and J viruses infecting monkeys. The latter findings will contribute to future development of consensus criteria for species assignments in enteroviruses and other picornavirus genera.

Section: Ev-a Ev-b Ev-c Ev-j Simian Ev-bsupporting

confidence: 79%

“…(mostly rhesus macaques [83%]) in the Yerkes National Primate Center in the United States and at the Dhaka Zoo in Bangladesh identified four further simian EV types (EV92 in species A; EV103, EV112, and EV115 in species J) (13,15), whereas no simian EVs were detected in synanthropic (e.g., pet) monkeys (12).…”

mentioning

confidence: 99%

High Rates of Infection with Novel Enterovirus Variants in Wild Populations of Mandrills and Other Old World Monkey Species

Nguyen

Harvala

Ngole

et al. 2014

“…9), this difference did not reach statistical significance after adjustment for multiple comparisons. SV19 was reported by RT-PCR in 41% of tested rhesus macaque fecal specimens collected from a zoo in Dhaka, Bangladesh (39). Using a panenterovirus real-time PCR, we also showed significantly lower C T values in the acute-and chronic-diarrhea groups of animals, supporting generally higher picornavirus RNA loads in diarrheic cases than in the healthy group.…”

Section: Discussionmentioning

confidence: 54%

Case-Control Comparison of Enteric Viromes in Captive Rhesus Macaques with Acute or Idiopathic Chronic Diarrhea

Kapusinszky

Ardeshir

Mulvaney

et al. 2017

Diarrhea is the major cause of non-research-associated morbidity and mortality affecting the supply of rhesus macaques and, potentially, their responses to experimental treatments. Idiopathic chronic diarrhea (ICD) in rhesus macaques also resembles ulcerative colitis, one form of human inflammatory bowel disease. To test for viral etiologies, we characterized and compared the fecal viromes from 32 healthy animals, 31 animals with acute diarrhea, and 29 animals with ICD. The overall fractions of eukaryotic viral reads were 0.063% for the healthy group, 0.131% for the acute-diarrhea group, and 0.297% for the chronic-diarrhea group. Eukaryotic viruses belonging to 6 viral families, as well as numerous circular Rep-encoding singlestranded DNA (CRESS DNA) viral genomes, were identified. The most commonly detected sequences were from picornaviruses, making up 59 to 88% of all viral reads, followed by 9 to 17% for CRESS DNA virus sequences. The remaining 5 virus families, Adenoviridae, Astroviridae, Anelloviridae, Picobirnaviridae, and Parvoviridae, collectively made up 1 to 3% of the viral reads, except for parvoviruses, which made up 23% of the viral reads in the healthy group. Detected members of the families Picornaviridae and Parvoviridae were highly diverse, consisting of multiple genera, species, and genotypes. Coinfections with members of up to six viral families were detected. Complete and partial viral genomes were assembled and used to measure the number of matching short sequence reads in feces from the 92 animals in the two clinical and the healthy control groups. Several enterovirus genotypes and CRESS DNA genomes were associated with ICD relative to healthy animals. Conversely, higher read numbers from different parvoviruses were associated with healthy animals. Our study reveals a high level of enteric coinfections with diverse viruses in a captive rhesus macaque colony and identifies several viruses positively or negatively associated with ICD.KEYWORDS enterovirus, sapelovirus, parvovirus, CRESS-DNA, idiopathic diarrhea, rhesus macaques, enteric disease etiology W e compared the enteric viromes of captive rhesus macaques (Macaca mulatta) with acute and idiopathic chronic diarrhea (ICD) to those of healthy animals using a case-control study. The genomes of several known and new viruses were characterized using metagenomics. We showed that some specific enterovirus genotypes and some small circular DNA genomes are associated with chronic idiopathic diarrhea, providing candidates for further testing of their pathogenicity. Other viruses, including some parvoviruses, were found at significantly higher levels in healthy animals.

“…3), but we have so far been unable to generate additional capsid sequence to confirm this possibility. Strikingly, no known simian EVs were identified in any of the NHP fecal samples screened in this study (but see our accompanying paper for this project, which characterizes EVs among NHP at the Dhaka Zoo that were collected during the same sampling periods [43]). …”

Section: Resultsmentioning

confidence: 99%

“…First, it is possible that efficient transmission of simian picornaviruses requires correspondingly higher NHP population densities, as are found typically in zoos and research colonies (21,37,50,51). Indeed, in our accompanying paper to this article, which analyzed fecal specimens from zoo NHP in Bangladesh, we found that over 90% of EV detected were (43). Multiple-age caging and a high density within cages may create favorable conditions for persistent EV cycling and variation by interspecies transmission.…”

Section: Discussionmentioning

confidence: 99%

Characterizing the Picornavirus Landscape among Synanthropic Nonhuman Primates in Bangladesh, 2007 to 2008

Oberste

Feeroz

Maher

et al. 2013

Self Cite

The term synanthropic describes organisms that thrive in human-altered habitats. Where synanthropic nonhuman primates (NHP) share an ecological niche with humans, cross-species transmission of infectious agents can occur. In Bangladesh, synanthropic NHP are found in villages, densely populated cities, religious sites, and protected forest areas. NHP are also kept as performing monkeys and pets. To investigate possible transmission of enteric picornaviruses between humans and NHP, we collected fecal specimens from five NHP taxa at16 locations in Bangladesh during five field sessions, from January 2007 to June 2008. Specimens were screened using real-time PCR assays for the genera Enterovirus, Parechovirus, and Sapelovirus; PCR-positive samples were typed by VP1 sequencing. To compare picornavirus diversity between humans and NHP, the same assays were applied to 211 human stool specimens collected in Bangladesh in 2007 to 2008 for acute flaccid paralysis surveillance. Picornaviruses were detected in 78 of 677 (11.5%) NHP fecal samples. Twenty distinct human enterovirus (EV) serotypes, two bovine EV types, six human parechovirus serotypes, and one virus related to Ljungan virus were identified. Twenty-five additional enteroviruses and eight parechoviruses could not be typed. Comparison of the picornavirus serotypes detected in NHP specimens with those detected in human specimens revealed considerable overlap. Strikingly, no known simian enteroviruses were detected among these NHP populations. In conclusion, enteroviruses and parechoviruses may be transmitted between humans and synanthropic NHP in Bangladesh, but the directionality of transmission is unknown. These findings may have important implications for the health of both human and NHP populations.