Adenovirus Infections in African Humans and Wild Non-Human Primates: Great Diversity and Cross-Species Transmission

Abstract

Non-human primates (NHPs) are known hosts for adenoviruses (AdVs), so there is the possibility of the zoonotic or cross-species transmission of AdVs. As with humans, AdV infections in animals can cause diseases that range from asymptomatic to fatal. The aim of this study was to investigate the occurrence and diversity of AdVs in: (i) fecal samples of apes and monkeys from different African countries (Republic of Congo, Senegal, Djibouti and Algeria), (ii) stool of humans living near gorillas in the Republic of Congo, in order to explore the potential zoonotic risks. Samples were screened by real-time and standard PCRs, followed by the sequencing of the partial DNA polymerase gene in order to identify the AdV species. The prevalence was 3.3 folds higher in NHPs than in humans. More than 1/3 (35.8%) of the NHPs and 1/10 (10.5%) of the humans excreted AdVs in their feces. The positive rate was high in great apes (46%), with a maximum of 54.2% in chimpanzees (Pan troglodytes) and 35.9% in gorillas (Gorilla gorilla), followed by monkeys (25.6%), with 27.5% in Barbary macaques (Macaca sylvanus) and 23.1% in baboons (seven Papio papio and six Papio hamadryas). No green monkeys (Chlorocebus sabaeus) were found to be positive for AdVs. The AdVs detected in NHPs were members of Human mastadenovirus E (HAdV-E), HAdV-C or HAdV-B, and those in the humans belonged to HAdV-C or HAdV-D. HAdV-C members were detected in both gorillas and humans, with evidence of zoonotic transmission since phylogenetic analysis revealed that gorilla AdVs belonging to HAdV-C were genetically identical to strains detected in humans who had been living around gorillas, and, inversely, a HAdV-C member HAdV type was detected in gorillas. This confirms the gorilla-to-human transmission of adenovirus. which has been reported previously. In addition, HAdV-E members, the most often detected here, are widely distributed among NHP species regardless of their origin, i.e., HAdV-E members seem to lack host specificity. Virus isolation was successful from a human sample and the strain of the Mbo024 genome, of 35 kb, that was identified as belonging to HAdV-D, exhibited close identity to HAdV-D members for all genes. This study provides information on the AdVs that infect African NHPs and the human populations living nearby, with an evident zoonotic transmission. It is likely that AdVs crossed the species barrier between different NHP species (especially HAdV-E members), between NHPs and humans (especially HAdV-C), but also between humans, NHPs and other animal species.

Potential zoonotic pathogens hosted by endangered bonobos

“…In our recent study on AdV circulation in African humans and NHPs, HAdV-B, HAdV-C, HAdV-D and HAdV-E were found in both humans and/or NHPs from the Congo. We demonstrated a possible jump of a human strain of HAdV-C to gorillas, and, vice versa, a gorilla strain of HAdV-C to humans sharing the same living area in the Congo 33 . HAdV-B members were detected in Lola and HAdV-E in Ekolo, and they were previously reported in captive bonobos from the Jacksonville Zoo, USA 23 .…”

“…Indeed, pure DNA/RNA extracts from stool samples may contain a considerable amount of polymerase inhibitors 32 . The choice to use the dilution at 1:10 is therefore explained by the fact that we have sought to limit the polymerase inhibitors while having a sufficient DNA/RNA quantity 33 . Dilution at 1:100 would have allowed us to further limit the amount of inhibitor but with less DNA/RNA available.…”

Detection of zoonotic pathogens in animals performed at the University Hospital Institute Méditerranée Infection (Marseille – France)

“…A synthesis of studies conducted at the IHU, using mainly faeces from great apes, has been published recently [ 13 ]. Thus, human adenovirus genotypes were discovered in gorillas from Congo-Brazzaville and, conversely, simian genotypes have been found in human beings sharing the same living area as the gorillas [ 14 ]. Again, a recombinant coxsackie/poliovirus has been found in wild gorillas and in the guardians of the reserve.…”

Understanding Post Entry Sorting of Adenovirus Capsids; A Chance to Change Vaccine Vector Properties

“…Furthermore, Ads can also spontaneously recombine, thereby generating new species [ 12 ], as it was the case for AdE4, which is the only human species E virus and is likely to have resulted from the recombination between human species B and a simian Ad [ 13 ]. Although infections in humans with non-human Ads are naturally rare, they are not impossible [ 14 , 15 ]. The capacity of a variety of non-human Ads to infect (or transduce) human cells makes them attractive (vaccine) vector platforms.…”