Skip to content
1887

Abstract

To date, data on animal enteroviruses (EVs) are scarce, especially in Central Africa. The aim of this study was to characterize EVs among pigs and goats in Cameroon and the Central African Republic (CAR). A total of 226 pig and goat faecal samples collected in two previous studies carried out in Cameroon and CAR were pooled and screened with molecular assays targeting EV-Es, EV-Fs and EV-Gs. EV genomes were amplified by RT-PCR and their sequences were obtained by Illumina sequencing and assembly. Based on the capsid sequences, 27 EV-G sequences were identified and assigned to 11 virus types, while no EV-E or EV-F was observed. Phylogenetic analysis revealed that the EV-Gs detected in Central Africa do not form specific clusters compared to EV-Gs previously reported in other continents. This suggests a worldwide circulation of EV-Gs, which is likely due to the massive international trade of live animals. One human EV, EV-C99, which belongs to the species , was detected in pigs. This is the third detection of such an event in a similar context, reinforcing the hypothesis that some EV-Cs could be infecting pigs. Our work provides new data on the genetic diversity of EVs circulating among domestic animals in Central Africa.

Funding
This study was supported by the:
  • Institut Pasteur (Award ACIP-162)
    • Principle Award Recipient: MaelBessaud
  • Institut Pasteur, Paris (Award Calmette & Yersin internship grant)
    • Principle Award Recipient: AbdouFatawou MODIYINJI
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/acmi/10.1099/acmi.0.000886.v3
2025-01-08
2025-01-17
Loading full text...

Full text loading...

/deliver/fulltext/acmi/7/1/acmi000886.v3.html?itemId=/content/journal/acmi/10.1099/acmi.0.000886.v3&mimeType=html&fmt=ahah

References

  1. Simmonds P, Gorbalenya AE, Harvala H, Hovi T, Knowles NJ et al. Recommendations for the nomenclature of enteroviruses and rhinoviruses. Arch Virol 2020; 165:793–797 [View Article] [PubMed]
    [Google Scholar]
  2. Oberste MS, Maher K, Kilpatrick DR, Pallansch MA. Molecular evolution of the human enteroviruses: correlation of serotype with VP1 sequence and application to picornavirus classification. J Virol 1999; 73:1941–1948 [View Article] [PubMed]
    [Google Scholar]
  3. Oberste MS, Maher K, Flemister MR, Marchetti G, Kilpatrick DR et al. Comparison of classic and molecular approaches for the identification of untypeable enteroviruses. J Clin Microbiol 2000; 38:1170–1174 [View Article] [PubMed]
    [Google Scholar]
  4. Zell R, Krumbholz A, Dauber M, Hoey E, Wutzler P. Molecular-based reclassification of the bovine enteroviruses. J Gen Virol 2006; 87:375–385 [View Article] [PubMed]
    [Google Scholar]
  5. Sadeuh-Mba S, Doté J, Joffret M-L, Chesnais M, Filhol T et al. Animal enteroviruses: a glimpse of a wide evolutionary landscape. Virologie 2023; 27:159–172 [View Article] [PubMed]
    [Google Scholar]
  6. Oberste MS, Feeroz MM, Maher K, Nix WA, Engel GA et al. Characterizing the picornavirus landscape among synanthropic nonhuman primates in Bangladesh, 2007 to 2008. J Virol 2013; 87:558–571 [View Article]
    [Google Scholar]
  7. Nollens HH, Rivera R, Palacios G, Wellehan JFX, Saliki JT et al. New recognition of Enterovirus infections in bottlenose dolphins (Tursiops truncatus). Vet Microbiol 2009; 139:170–175 [View Article] [PubMed]
    [Google Scholar]
  8. He H, Tang C, Chen X, Yue H, Ren Y et al. Isolation and characterization of a new enterovirus F in yak feces in the Qinghai-Tibetan Plateau. Arch Virol 2017; 162:523–527 [View Article] [PubMed]
    [Google Scholar]
  9. McClenahan SD, Scherba G, Borst L, Fredrickson RL, Krause PR et al. Discovery of a bovine enterovirus in alpaca. PLoS One 2013; 8:e68777 [View Article] [PubMed]
    [Google Scholar]
  10. Chang X, Lin Q, Hu J, Wang X, Li X et al. Discovery of a virus of the species Enterovirus F in goats. Arch Virol 2019; 164:2551–2558 [View Article] [PubMed]
    [Google Scholar]
  11. Zheng T. Characterisation of two enteroviruses isolated from Australian brushtail possums (Trichosurus vulpecula) in New Zealand. Arch Virol 2007; 152:191–198 [View Article] [PubMed]
    [Google Scholar]
  12. Doté J, Joffret M-L, Beta BN, Ait-Ahmed M, Banga-Mingo V et al. Characterization of enteroviruses circulating among farm animals and children in Central African Republic. Emerg Microbes Infect 2024; 13:2368212 [View Article] [PubMed]
    [Google Scholar]
  13. Faleye TOC, Adewumi OM, Olayinka OA, Donbraye E, Oluremi B et al. Draft genome sequence of a bovine enterovirus isolate recovered from Sewage in Nigeria. Microbiol Resour Announc 2018; 7:e01466-18 [View Article] [PubMed]
    [Google Scholar]
  14. Sobhy NM, Mor SK, Mohammed MEM, Bastawecy IM, Fakhry HM et al. Isolation and molecular characterization of bovine enteroviruses in Egypt. Vet J 2015; 206:317–321 [View Article] [PubMed]
    [Google Scholar]
  15. Bohou Kombila L, N’dilimabaka N, Garcia D, Rieu O, Engone Ondo JD et al. Molecular identification of enteric viruses in domestic animals in Northeastern Gabon, Central Africa. Animals 2023; 13:2512 [View Article] [PubMed]
    [Google Scholar]
  16. Bessaud M, Pillet S, Ibrahim W, Joffret M-L, Pozzetto B et al. Molecular characterization of human enteroviruses in the Central African Republic: uncovering wide diversity and identification of a new human enterovirus A71 genogroup. J Clin Microbiol 2012; 50:1650–1658 [View Article] [PubMed]
    [Google Scholar]
  17. Sadeuh-Mba SA, Kavunga-Membo H, Joffret M-L, Yogolelo R, Endegue-Zanga MC et al. Genetic landscape and macro-evolution of co-circulating Coxsackieviruses A and Vaccine-derived Polioviruses in the Democratic Republic of Congo, 2008-2013. PLoS Negl Trop Dis 2019; 13:e0007335 [View Article] [PubMed]
    [Google Scholar]
  18. Ndiaye AK, Diop PAM, Diop OM. Environmental surveillance of poliovirus and non-polio enterovirus in urban sewage in Dakar, Senegal (2007-2013). Pan Afr Med J 2014; 19:243 [View Article] [PubMed]
    [Google Scholar]
  19. Osundare FA, Opaleye OO, Akindele AA, Adedokun SA, Akanbi OA et al. Detection and characterization of human enteroviruses, human cosaviruses, and a new human parechovirus type in healthy individuals in Osun State, Nigeria, 2016/2017. Viruses 2019; 11:1037 [View Article] [PubMed]
    [Google Scholar]
  20. Modiyinji AF, Sanding GMAM, Atsama MA, Monamele CG, Nola M et al. Serological and molecular investigation of hepatitis E virus in pigs reservoirs from Cameroon reveals elevated seroprevalence and presence of genotype 3. PLoS ONE 2020; 15:e0229073 [View Article]
    [Google Scholar]
  21. Nombot-Yazenguet MP de M, Modiyinji AF, Tricou V, Manirakiza A, Njouom R et al. Investigating animal reservoirs for hepatitis E virus in Bangui, Central African Republic. PLoS One 2024; 19:e0300608 [View Article] [PubMed]
    [Google Scholar]
  22. World Health Organization Polio laboratory manual, 4th edition; 2004 https://iris.who.int/bitstream/handle/10665/68762/WHO_IVB_04.10.pdf?sequence=1&isAllowed=y accessed 24 July 2024
  23. Joffret M-L, Polston PM, Razafindratsimandresy R, Bessaud M, Heraud J-M et al. Whole genome sequencing of enteroviruses species A to D by high-throughput sequencing: application for viral mixtures. Front Microbiol 2018; 9:2339 [View Article] [PubMed]
    [Google Scholar]
  24. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [View Article] [PubMed]
    [Google Scholar]
  25. Brown BA, Maher K, Flemister MR, Naraghi-Arani P, Uddin M et al. Resolving ambiguities in genetic typing of human enterovirus species C clinical isolates and identification of enterovirus 96, 99 and 102. J Gen Virol 2009; 90:1713–1723 [View Article] [PubMed]
    [Google Scholar]
  26. Razafindratsimandresy R, Joffret M-L, Andriamandimby SF, Andriamamonjy S, Rabemanantsoa S et al. Enterovirus detection in different regions of Madagascar reveals a higher abundance of enteroviruses of species C in areas where several outbreaks of vaccine-derived polioviruses occurred. BMC Infect Dis 2022; 22:821 [View Article] [PubMed]
    [Google Scholar]
  27. Sadeuh-Mba SA, Bessaud M, Massenet D, Joffret M-L, Endegue M-C et al. High frequency and diversity of species C enteroviruses in Cameroon and neighboring countries. J Clin Microbiol 2013; 51:759–770 [View Article] [PubMed]
    [Google Scholar]
  28. Bero DM, da Silva EE, Júnior IP de S, Nhassengo SA, Machado RS et al. Enterovirus detection in stool samples from Mozambican children with acute gastroenteritis. Acta Trop 2023; 238:106755 [View Article] [PubMed]
    [Google Scholar]
  29. Mombo IM, Boundenga L, Berthet N, Atencia R, Cox D et al. A second genome sequence of an enterovirus C99 detected in A healthy Chimpanzee. Microbiol Resour Announc 2020; 9:00893–20 [View Article] [PubMed]
    [Google Scholar]
  30. Mombo IM, Berthet N, Lukashev AN, Bleicker T, Brünink S et al. First detection of an enterovirus C99 in a captive Chimpanzee with acute flaccid paralysis, from the Tchimpounga Chimpanzee rehabilitation center, Republic of Congo. PLoS One 2015; 10:e0136700 [View Article] [PubMed]
    [Google Scholar]
  31. Tsuchiaka S, Naoi Y, Imai R, Masuda T, Ito M et al. Genetic diversity and recombination of enterovirus G strains in Japanese pigs: high prevalence of strains carrying a papain-like cysteine protease sequence in the enterovirus G population. PLoS One 2018; 13:e0190819 [View Article] [PubMed]
    [Google Scholar]
  32. Lu L, Van Dung N, Bryant JE, Carrique-Mas J, Van Cuong N et al. Evolution and phylogeographic dissemination of endemic porcine picornaviruses in Vietnam. Virus Evol 2016; 2:vew001 [View Article] [PubMed]
    [Google Scholar]
  33. Sawant PM, Atre N, Kulkarni A, Gopalkrishna V. Detection and molecular characterization of porcine enterovirus G15 and teschovirus from India. Pathog Dis 2020; 78:ftaa039 [View Article] [PubMed]
    [Google Scholar]
  34. Jeon JH, Lee C. Prevalence and molecular characterization of novel recombinant enterovirus G isolates in Jeju Province of South Korea. Korean J Vet Res 2019; 59:89–96 [View Article]
    [Google Scholar]
  35. Janetanakit T, Chaiyawong S, Charoenkul K, Tangwangvivat R, Chamsai E et al. Distribution and genetic diversity of Enterovirus G (EV-G) on pig farms in Thailand. BMC Vet Res 2021; 17:277 [View Article] [PubMed]
    [Google Scholar]
  36. Bunke J, Receveur K, Oeser AC, Fickenscher H, Zell R et al. High genetic diversity of porcine enterovirus G in Schleswig-Holstein, Germany. Arch Virol 2018; 163:489–493 [View Article] [PubMed]
    [Google Scholar]
  37. Boros Á, László Z, Pankovics P, Marosi A, Albert M et al. High prevalence, genetic diversity and a potentially novel genotype of Sapelovirus A (Picornaviridae) in enteric and respiratory samples in Hungarian swine farms. J Gen Virol 2020; 101:609–621 [View Article] [PubMed]
    [Google Scholar]
  38. Shang P, Misra S, Hause B, Fang Y. A naturally occurring recombinant enterovirus expresses a torovirus deubiquitinase. J Virol 2017; 91:e00450-17 [View Article] [PubMed]
    [Google Scholar]
  39. Ramesh A, Bailey ES, Ahyong V, Langelier C, Phelps M et al. Metagenomic characterization of swine slurry in a North American swine farm operation. Sci Rep 2021; 11:16994 [View Article] [PubMed]
    [Google Scholar]
  40. Zhang G, Wilsden G, Knowles NJ, McCauley JW. Complete nucleotide sequence of a coxsackie B5 virus and its relationship to swine vesicular disease virus. J Gen Virol 1993; 74 (Pt 5):845–853 [View Article] [PubMed]
    [Google Scholar]
  41. Lomakina NF, Yu Shustova E, Strizhakova OM, Felix Drexler J, Lukashev AN. Epizootic of vesicular disease in pigs caused by coxsackievirus B4 in the Soviet Union in 1975. J Gen Virol 2016; 97:49–52 [View Article] [PubMed]
    [Google Scholar]
  42. Li Z, Chen W, Qiu Z, Li Y, Fan J et al. African swine fever virus: a review. Life 2022; 12:1255 [View Article] [PubMed]
    [Google Scholar]
/content/journal/acmi/10.1099/acmi.0.000886.v3
Loading
/content/journal/acmi/10.1099/acmi.0.000886.v3
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error