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Abstract

Decades after its discovery in East Africa, Zika virus (ZIKV) emerged in Brazil in 2013 and infected millions of people during intense urban transmission. Whether vertebrates other than humans are involved in ZIKV transmission cycles remained unclear. Here, we investigate the role of different animals as ZIKV reservoirs by testing 1723 sera of pets, peri-domestic animals and African non-human primates (NHP) sampled during 2013–2018 in Brazil and 2006–2016 in Côte d'Ivoire. Exhaustive neutralization testing substantiated co-circulation of multiple flaviviruses and failed to confirm ZIKV infection in pets or peri-domestic animals in Côte d'Ivoire (=259) and Brazil (=1416). In contrast, ZIKV seroprevalence was 22.2% (2/9, 95% CI, 2.8–60.1) in West African chimpanzees () and 11.1% (1/9, 95% CI, 0.3–48.3) in king colobus (). Our results indicate that while NHP may represent ZIKV reservoirs in Africa, pets or peri-domestic animals likely do not play a role in ZIKV transmission cycles.

Funding
This study was supported by the:
  • Horizon 2020 (Award 734548)
    • Principle Award Recipient: JanFelix Drexler
  • Deutsche Forschungsgemeinschaft (Award FOR2136; CA 1108/3-1)
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2022-01-25
2024-04-20
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References

  1. Petersen LR, Jamieson DJ, Honein MA. Zika Virus. N Engl J Med 2016; 375:294–295 [View Article] [PubMed]
    [Google Scholar]
  2. Mayer SV, Tesh RB, Vasilakis N. The emergence of arthropod-borne viral diseases: A global prospective on dengue, chikungunya and zika fevers. Acta Trop 2017; 166:155–163 [View Article] [PubMed]
    [Google Scholar]
  3. Faye O, Freire CCM, Iamarino A, Faye O, de Oliveira JVC et al. Molecular evolution of Zika virus during its emergence in the 20(th) century. PLoS Negl Trop Dis 2014; 8:e2636 [View Article] [PubMed]
    [Google Scholar]
  4. Valentine MJ, Murdock CC, Kelly PJ. Sylvatic cycles of arboviruses in non-human primates. Parasit Vectors 2019; 12:463 [View Article] [PubMed]
    [Google Scholar]
  5. Faria NR, Azevedo R do S da S, Kraemer MUG, Souza R, Cunha MS et al. Zika virus in the Americas: Early epidemiological and genetic findings. Science 2016; 352:345–349 [View Article] [PubMed]
    [Google Scholar]
  6. Brady OJ, Osgood-Zimmerman A, Kassebaum NJ, Ray SE, de Araújo VEM et al. The association between Zika virus infection and microcephaly in Brazil 2015-2017: An observational analysis of over 4 million births. PLoS Med 2019; 16:e1002755 [View Article] [PubMed]
    [Google Scholar]
  7. Netto EM, Moreira-Soto A, Pedroso C, Höser C, Funk S et al. High Zika Virus Seroprevalence in Salvador, Northeastern Brazil Limits the Potential for Further Outbreaks. mBio 2017; 8:e01390-17 [View Article] [PubMed]
    [Google Scholar]
  8. Berry N, Ferguson D, Ham C, Hall J, Jenkins A et al. High susceptibility, viral dynamics and persistence of South American Zika virus in New World monkey species. Sci Rep 2019; 9:14495 [View Article] [PubMed]
    [Google Scholar]
  9. de Oliveira-Filho EF, Oliveira RAS, Ferreira DRA, Laroque PO, Pena LJ et al. Seroprevalence of selected flaviviruses in free-living and captive capuchin monkeys in the state of Pernambuco, Brazil. Transbound Emerg Dis 2018; 65:1094–1097 [View Article] [PubMed]
    [Google Scholar]
  10. Moreira-Soto A, Carneiro I de O, Fischer C, Feldmann M, Kümmerer BM et al. Limited evidence for infection of urban and peri-urban nonhuman primates with zika and chikungunya viruses in Brazil. mSphere 2018; 3: [View Article]
    [Google Scholar]
  11. Terzian ACB, Zini N, Sacchetto L, Rocha RF, Parra MCP et al. Evidence of natural Zika virus infection in neotropical non-human primates in Brazil. Sci Rep 2018; 8:16034 [View Article] [PubMed]
    [Google Scholar]
  12. Austgen LE, Bowen RA, Bunning ML, Davis BS, Mitchell CJ et al. Experimental infection of cats and dogs with West Nile virus. Emerg Infect Dis 2004; 10:82–86 [View Article] [PubMed]
    [Google Scholar]
  13. Shimoda H, Tamaru S, Morimoto M, Hayashi T, Shimojima M et al. Experimental infection of Japanese encephalitis virus in dogs. J Vet Med Sci 2011; 73:1241–1242 [View Article] [PubMed]
    [Google Scholar]
  14. Davoust B, Leparc-Goffart I, Demoncheaux JP, Tine R, Diarra M et al. Serologic surveillance for West Nile virus in dogs, Africa. Emerg Infect Dis 2014; 20:1415–1417 [View Article] [PubMed]
    [Google Scholar]
  15. Kumar K, Arshad SS, Selvarajah GT, Abu J, Toung OP et al. Prevalence and risk factors of Japanese encephalitis virus (JEV) in livestock and companion animal in high-risk areas in Malaysia. Trop Anim Health Prod 2018; 50:741–752 [View Article] [PubMed]
    [Google Scholar]
  16. Durand B, Haskouri H, Lowenski S, Vachiery N, Beck C et al. Seroprevalence of West Nile and Usutu viruses in military working horses and dogs, Morocco, 2012: dog as an alternative WNV sentinel species?. Epidemiol Infect 2016; 144:1857–1864 [View Article] [PubMed]
    [Google Scholar]
  17. Coetzer JA, Theodoridis A. Clinical and pathological studies in adult sheep and goats experimentally infected with Wesselsbron disease virus. Onderstepoort J Vet Res 1982; 49:19–22 [PubMed]
    [Google Scholar]
  18. Coetzer JA, Barnard BJ. Hydrops amnii in sheep associated with hydranencephaly and arthrogryposis with wesselsbron disease and rift valley fever viruses as aetiological agents. Onderstepoort J Vet Res 1977; 44:119–126 [PubMed]
    [Google Scholar]
  19. Vilibic-Cavlek T, Petrovic T, Savic V, Barbic L, Tabain I et al. Epidemiology of usutu virus: The European Scenario. Pathogens 2020; 9:E699. [View Article] [PubMed]
    [Google Scholar]
  20. Ladreyt H, Auerswald H, Tum S, Ken S, Heng L et al. Comparison of Japanese encephalitis force of infection in pigs, poultry and dogs in cambodian villages. Pathogens 2020; 9:E719 [View Article] [PubMed]
    [Google Scholar]
  21. García-Bocanegra I, Jurado-Tarifa E, Cano-Terriza D, Martínez R, Pérez-Marín JE et al. Exposure to West Nile virus and tick-borne encephalitis virus in dogs in Spain. Transbound Emerg Dis 2018; 65:765–772 [View Article] [PubMed]
    [Google Scholar]
  22. Lecollinet S, Pronost S, Coulpier M, Beck C, Gonzalez G et al. Viral equine encephalitis, a growing threat to the horse population in Europe?. Viruses 2019; 12:E23 [View Article]
    [Google Scholar]
  23. de Oliveira-Filho EF, Fischer C, Berneck BS, Carneiro IO, Kühne A et al. Ecologic determinants of west nile virus seroprevalence among equids, Brazil. Emerg Infect Dis 2021; 27:2466–2470 [View Article] [PubMed]
    [Google Scholar]
  24. Schwarz ER, Pozor MA, Pu R, Barr KL, Beachboard SE et al. Experimental infection of pregnant female sheep with zika virus during early gestation. Viruses 2019; 11:E795 [View Article] [PubMed]
    [Google Scholar]
  25. Ragan IK, Blizzard EL, Gordy P, Bowen RA. Investigating the potential role of North American Animals as hosts for zika virus. Vector Borne Zoonotic Dis 2017; 17:161–164 [View Article] [PubMed]
    [Google Scholar]
  26. Pauvolid-Corrêa A, Gonçalves Dias H, Marina Siqueira Maia L, Porfírio G, Oliveira Morgado T et al. Zika Virus Surveillance at the Human-Animal Interface in West-Central Brazil, 2017-2018. Viruses 2019; 11:E1164 [View Article] [PubMed]
    [Google Scholar]
  27. Beck C, Leparc-Goffart I, Desoutter D, Debergé E, Bichet H et al. Serological evidence of infection with dengue and Zika viruses in horses on French Pacific Islands. PLoS Negl Trop Dis 2019; 13:e0007162 [View Article] [PubMed]
    [Google Scholar]
  28. Vasilakis N, Weaver SC. Flavivirus transmission focusing on Zika. Curr Opin Virol 2017; 22:30–35 [View Article] [PubMed]
    [Google Scholar]
  29. Pereira Dos Santos T, Roiz D, Santos de Abreu FV, Luz SLB, Santalucia M et al. Potential of Aedes albopictus as a bridge vector for enzootic pathogens at the urban-forest interface in Brazil. Emerg Microbes Infect 2018; 7:191 [View Article] [PubMed]
    [Google Scholar]
  30. Delatte H, Desvars A, Bouétard A, Bord S, Gimonneau G et al. Blood-feeding behavior of Aedes albopictus, a vector of Chikungunya on La Réunion. Vector Borne Zoonotic Dis 2010; 10:249–258 [View Article] [PubMed]
    [Google Scholar]
  31. Ponlawat A, Harrington LC. Blood feeding patterns of Aedes aegypti and Aedes albopictus in Thailand. J Med Entomol 2005; 42:844–849 [View Article] [PubMed]
    [Google Scholar]
  32. Kamgang B, Nchoutpouen E, Simard F, Paupy C. Notes on the blood-feeding behavior of Aedes albopictus (Diptera: Culicidae) in Cameroon. Parasit Vectors 2012; 5:57 [View Article] [PubMed]
    [Google Scholar]
  33. Omondi D, Masiga DK, Ajamma YU, Fielding BC, Njoroge L et al. Unraveling host-vector-arbovirus interactions by two-gene high resolution melting mosquito bloodmeal analysis in a kenyan wildlife-livestock interface. PLoS One 2015; 10:e0134375 [View Article] [PubMed]
    [Google Scholar]
  34. Fitzpatrick DM, Hattaway LM, Hsueh AN, Ramos-Niño ME, Cheetham SM. PCR-Based Bloodmeal Analysis of Aedes aegypti and Culex quinquefasciatus (Diptera: Culicidae) in St. George Parish, Grenada. J Med Entomol 2019; 56:1170–1175 [View Article] [PubMed]
    [Google Scholar]
  35. Akoua-Koffi C, Diarrassouba S, Bénié VB, Ngbichi JM, Bozoua T et al. Investigation surrounding a fatal case of yellow fever in Côte d’Ivoire in 1999. Bull Soc Pathol Exot 2001; 94:227–230 [PubMed]
    [Google Scholar]
  36. Sales K da S, de Oliveira Miranda DE, Costa PL, da Silva FJ, Figueredo LA et al. Home sweet home: sand flies find a refuge in remote indigenous villages in north-eastern Brazil, where leishmaniasis is endemic. Parasit Vectors 2019; 12:118 [View Article] [PubMed]
    [Google Scholar]
  37. Zimmermann F, Köhler SM, Nowak K, Dupke S, Barduhn A et al. Low antibody prevalence against Bacillus cereus biovar anthracis in Taï National Park, Côte d’Ivoire, indicates high rate of lethal infections in wildlife. PLoS Negl Trop Dis 2017; 11:e0005960 [View Article] [PubMed]
    [Google Scholar]
  38. Gogarten JF, Davies TJ, Benjamino J, Gogarten JP, Graf J et al. Factors influencing bacterial microbiome composition in a wild non-human primate community in Taï National Park, Côte d’Ivoire. ISME J 2018; 12:2559–2574 [View Article] [PubMed]
    [Google Scholar]
  39. Gogarten JF, Akoua-Koffi C, Calvignac-Spencer S, Leendertz SAJ, Weiss S et al. The ecology of primate retroviruses - an assessment of 12 years of retroviral studies in the Taï national park area, Côte d׳Ivoire. Virology 2014; 460–461:147–153 [View Article] [PubMed]
    [Google Scholar]
  40. Laengin T, Augenstein S, Stadlbauer E, Girgnhuber H, Gloeck M et al. Performance of an Automated Zika IgG Immunoassay in the Detection of Zika IgG Specific Antibodies-A Validation Approach in Samples from Prevalence Areas and Non-Endemic Countries. Trop Med Infect Dis 2020; 5:E97 [View Article] [PubMed]
    [Google Scholar]
  41. Fischer C, de Oliveira-Filho EF, Drexler JF. Viral emergence and immune interplay in flavivirus vaccines. Lancet Infect Dis 2020; 20:15–17 [View Article] [PubMed]
    [Google Scholar]
  42. Fischer C, Jo WK, Haage V, Moreira-Soto A, de Oliveira Filho EF et al. Challenges towards serologic diagnostics of emerging arboviruses. Clin Microbiol Infect 2021; 27:1221–1229 [View Article] [PubMed]
    [Google Scholar]
  43. Katzelnick LC, Fonville JM, Gromowski GD, Bustos Arriaga J, Green A et al. Dengue viruses cluster antigenically but not as discrete serotypes. Science 2015; 349:1338–1343 [View Article] [PubMed]
    [Google Scholar]
  44. White SK, Lednicky JA, Okech BA, Dunford JC. Spondweni Virus in Field-Caught Culex quinquefasciatus Mosquitoes, Haiti, 2016. Emerg Infect Dis 2018; 24:1765–1767 [View Article] [PubMed]
    [Google Scholar]
  45. Inouye S, Matsuno S, Tsurukubo Y. “Original antigenic sin” phenomenon in experimental flavivirus infections of guinea pigs: studies by enzyme-linked immunosorbent assay. Microbiol Immunol 1984; 28:569–574 [View Article] [PubMed]
    [Google Scholar]
  46. Lindsey NP, Staples JE, Powell K, Rabe IB, Fischer M et al. Ability To Serologically Confirm Recent Zika Virus Infection in Areas with Varying Past Incidence of Dengue Virus Infection in the United States and U.S. Territories in 2016. J Clin Microbiol 2018; 56:e01115-17 [View Article] [PubMed]
    [Google Scholar]
  47. Diallo D, Sall AA, Diagne CT, Faye O, Hanley KA et al. Patterns of a sylvatic yellow fever virus amplification in southeastern Senegal, 2010. Am J Trop Med Hyg 2014; 90:1003–1013 [View Article] [PubMed]
    [Google Scholar]
  48. Dick GWA, Kitchen SF, Haddow AJ. Zika virus. I. Isolations and serological specificity. Trans R Soc Trop Med Hyg 1952; 46:509–520 [View Article] [PubMed]
    [Google Scholar]
  49. Althouse BM, Hanley KA, Diallo M, Sall AA, Ba Y et al. Impact of climate and mosquito vector abundance on sylvatic arbovirus circulation dynamics in Senegal. Am J Trop Med Hyg 2015; 92:88–97 [View Article] [PubMed]
    [Google Scholar]
  50. McCrae AW, Kirya BG. Yellow fever and Zika virus epizootics and enzootics in Uganda. Trans R Soc Trop Med Hyg 1982; 76:552–562 [View Article] [PubMed]
    [Google Scholar]
  51. Monath TP, Kemp GE. Importance of nonhuman primates in yellow fever epidemiology in Nigeria. Trop Geogr Med 1973; 25:28–38 [PubMed]
    [Google Scholar]
  52. Althouse BM, Guerbois M, Cummings DAT, Diop OM, Faye O et al. Role of monkeys in the sylvatic cycle of chikungunya virus in Senegal. Nat Commun 2018; 9:1046 [View Article] [PubMed]
    [Google Scholar]
  53. Stephenson EB, Peel AJ, Reid SA, Jansen CC, McCallum H. The non-human reservoirs of Ross River virus: a systematic review of the evidence. Parasit Vectors 2018; 11:188 [View Article] [PubMed]
    [Google Scholar]
  54. Bueno MG, Martinez N, Abdalla L, Duarte Dos Santos CN, Chame M. Animals in the Zika Virus Life Cycle: What to Expect from Megadiverse Latin American Countries. PLoS Negl Trop Dis 2016; 10:12 [View Article] [PubMed]
    [Google Scholar]
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