High Seroprevalence of Enterovirus Infections in Apes and Old World Monkeys

Harvala, Heli; McIntyre, Chloe; Imai, Natsuko; Clasper, Lucy; Djoko, Cyrille F.; LeBreton, Matthew; Vermeulen, Marion; Saville, A Marion; Mutapi, Francisca; Tamoufé, Ubald; Kiyang, John; Biblia, Tafon G.; Midzi, Nicholas; Mduluza, Takafira; Pépin, Jacques; Njoum, Richard; Smura, Teemu; Fair, Joseph N.; Wolfe, Nathan; Roivainen, Merja; Simmonds, Peter

doi:10.3201/eid1802.111363

Cited by 23 publications

(21 citation statements)

References 13 publications

(18 reference statements)

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“…As for EV-A76, the unique HEV-D strain EV-D111 was recently shown to infect both humans and chimpanzees in Central Africa (32)(33)(34). Together with previous reports, this study suggests that cross-species transmission of EVs may play a role in the diversity and evolution of HEVs in certain regions, including sub-Saharan Africa (60,61). Contacts between humans and nonhuman primates have significantly increased in Central Africa during the last decades (62), and this could promote the cross-species transmission of new viral pathogens to humans.…”

Section: Discussionsupporting

confidence: 58%

High Frequency and Diversity of Species C Enteroviruses in Cameroon and Neighboring Countries

et al. 2013

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Section: Discussionsupporting

confidence: 58%

High Frequency and Diversity of Species C Enteroviruses in Cameroon and Neighboring Countries

et al. 2013

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“…We can offer a few possible explanations for this finding. 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).…”

Section: Discussionmentioning

confidence: 99%

“…Experimental infection has shown the capacity of Asian monkey species to sustain infection with human enteroviruses (44)(45)(46), and numerous studies have reported the presence of antibody to human EV in a variety of NHP species in natural settings (21,22).…”

Section: Discussionmentioning

confidence: 99%

“…In humans, EV may cause illness ranging from undifferentiated fever and the common cold to rashes, meningitis, encephalitis, acute flaccid paralysis, and neonatal sepsis (20). There is serological evidence for cross-species transmission of enteroviruses between humans and NHP (21,22), and human enteroviruses have occasionally been isolated from NHP (23)(24)(25), but there are few data on enteroviral disease in NHP. We recently identified an "unusual" group of human EVs (EV76, EV89, EV90, and EV91), isolated from stool specimens of children with acute flaccid paralysis in Bangladesh (26).…”

mentioning

confidence: 99%

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

Oberste

Feeroz

Maher

et al. 2013

J Virol

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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.

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“…It is increasingly clear that relationships between variants infecting humans and nonhuman primates are complex, notwithstanding the growing evidence for zoonotic infections in both directions (12,38) and continuing uncertainty about the timescales for the original divergence of types and species and appearance of interspecies chimeras. Understanding which genome regions ultimately determine host range and disease outcomes are essential in assessment of the risk of simian enteroviruses as potential zoonotic and pathogenic infections in humans.…”

Section: Genome Configurationsmentioning

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

J Virol

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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.

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High Seroprevalence of Enterovirus Infections in Apes and Old World Monkeys

Cited by 23 publications

References 13 publications

High Frequency and Diversity of Species C Enteroviruses in Cameroon and Neighboring Countries

High Frequency and Diversity of Species C Enteroviruses in Cameroon and Neighboring Countries

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

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

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