Skip to main content

Advertisement

SpringerLink
Log in

Serological evidence of Zika virus infection in non-human primates in Zambia

  • Brief Report
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

Zika virus (ZIKV) circulation occurs between non-human primates (NHPs) in a sylvatic transmission cycle. To investigate evidence of flavivirus infection in NHPs in Zambia, we performed a plaque reduction neutralization test (PRNT) to quantify neutralizing antibodies. PRNT revealed that sera from NHPs (African green monkeys and baboons) exhibited neutralizing activity against ZIKV (34.4%; 33/96), whereas a PRNT for yellow fever virus using NHP sera showed no neutralization activity. ZIKV genomic RNA was not detected in splenic tissues from NHPs, suggesting that the presence of anti-ZIKV neutralizing antibodies represented resolved infections. Our evidence suggests that ZIKV is maintained in NHP reservoirs in Zambia.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

References

  1. Almeida MA, JaC Cardoso, Dos Santos E, da Fonseca DF, Cruz LL, Faraco FJ, Bercini MA, Vettorello KC, Porto MA, Mohrdieck R, Ranieri TM, Schermann MT, Sperb AF, Paz FZ, Nunes ZM, Romano AP, Costa ZG, Gomes SL, Flannery B (2014) Surveillance for yellow Fever virus in non-human primates in southern Brazil, 2001–2011: a tool for prioritizing human populations for vaccination. PLoS Negl Trop Dis 8:e2741

    Article  PubMed  PubMed Central  Google Scholar 

  2. Babaniyi O, Mazaba-Liwewe ML, Masaninga F, Mwaba P, Mulenga D, Songolo P, Mweene-Ndumba I, Rudatsikira E, Siziya S (2016) Prevalence of yellow fever in North-Western Province of Zambia. Int J Public Health Epidemiol 8(1):29–32

    Google Scholar 

  3. Babaniyi OA, Mwaba P, Songolo P, Mazaba-Liwewe ML, Mweene-Ndumba I, Masaninga F, Rudatsikira E, Siziya S (2015) Seroprevalence of Zika virus infection specific IgG in Western and North-Western Provinces of Zambia. Int J Public Health Epidemiol 4(1):110–114

    Google Scholar 

  4. Buechler CR, Bailey AL, Weiler AM, Barry GL, Breitbach ME, Stewart LM, Jasinska AJ, Freimer NB, Apetrei C, Phillips-Conroy JE, Jolly CJ, Rogers J, Friedrich TC, O’Connor DH (2017) Seroprevalence of Zika Virus in Wild African Green Monkeys and Baboons. mSphere. https://doi.org/10.1128/mSphere.00392-16

    Article  PubMed  PubMed Central  Google Scholar 

  5. Bueno MG, Martinez N, Abdalla L, Duarte Dos Santos CN, Chame M (2016) Animals in the Zika Virus life cycle: what to expect from megadiverse Latin American Countries. PLoS Negl Trop Dis 10:e0005073

    Article  PubMed  PubMed Central  Google Scholar 

  6. Cao-Lormeau VM, Blake A, Mons S, Lastere S, Roche C, Vanhomwegen J, Dub T, Baudouin L, Teissier A, Larre P, Vial AL, Decam C, Choumet V, Halstead SK, Willison HJ, Musset L, Manuguerra JC, Despres P, Fournier E, Mallet HP, Musso D, Fontanet A, Neil J, Ghawché F (2016) Guillain-Barré Syndrome outbreak associated with Zika virus infection in French Polynesia: a case-control study. Lancet 387:1531–1539

    Article  PubMed  PubMed Central  Google Scholar 

  7. Carr M, Kawaguchi A, Sasaki M, Gonzalez G, Ito K, Thomas Y, Hang’ombe BM, Mweene AS, Zhao G, Wang D, Orba Y, Ishii A, Sawa H (2017) Isolation of a simian immunodeficiency virus from a malbrouck (Chlorocebus cynosuros). Arch Virol 162:543–548

    Article  CAS  PubMed  Google Scholar 

  8. Chua CL, Chan YF, Andu ESGS, Rovie-Ryan JJ, Sitam FT, Verasahib K, Sam IC (2019) Little evidence of Zika Virus infection in wild long-tailed macaques, Peninsular Malaysia. Emerg Infect Dis 25:374–376

    Article  PubMed  PubMed Central  Google Scholar 

  9. Coffey LL, Pesavento PA, Keesler RI, Singapuri A, Watanabe J, Watanabe R, Yee J, Bliss-Moreau E, Cruzen C, Christe KL, Reader JR, von Morgenland W, Gibbons AM, Allen AM, Linnen J, Gao K, Delwart E, Simmons G, Stone M, Lanteri M, Bakkour S, Busch M, Morrison J, Van Rompay KK (2017) Zika virus tissue and blood compartmentalization in acute infection of Rhesus Macaques. PLoS One 12:e0171148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. de Oliveira-Filho EF, Oliveira RAS, Ferreira DRA, Laroque PO, Pena LJ, Valença-Montenegro MM, Mota RA, Gil LHVG (2018) Seroprevalence of selected flaviviruses in free-living and captive capuchin monkeys in the state of Pernambuco. Brazil. Transbound Emerg Dis 65(4):1094–1097

    Article  PubMed  Google Scholar 

  11. Diallo D, Sall AA, Diagne CT, Faye O, Ba Y, Hanley KA, Buenemann M, Weaver SC, Diallo M (2014) Zika virus emergence in mosquitoes in southeastern Senegal, 2011. PLoS One 9:e109442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Domingo C, Patel P, Yillah J, Weidmann M, Méndez JA, Nakouné ER, Niedrig M (2012) Advanced yellow fever virus genome detection in point-of-care facilities and reference laboratories. J Clin Microbiol 50:4054–4060

    Article  PubMed  PubMed Central  Google Scholar 

  13. Duffy MR, Chen TH, Hancock WT, Powers AM, Kool JL, Lanciotti RS, Pretrick M, Marfel M, Holzbauer S, Dubray C, Guillaumot L, Griggs A, Bel M, Lambert AJ, Laven J, Kosoy O, Panella A, Biggerstaff BJ, Fischer M, Hayes EB (2009) Zika virus outbreak on Yap Island, Federated States of Micronesia. N Engl J Med 360:2536–2543

  14. Favoretto S, Araujo D, Oliveira D, Duarte N, Mesquita F, Zanotto P, Durigon E (2016) First detection of Zika virus in neotropical primates in Brazil: a possible new reservoir. bioRxiv Apr. 20. https://doi.org/10.1101/049395

  15. Foy BD, Kobylinski KC, Chilson Foy JL, Blitvich BJ, Travassos da Rosa A, Haddow AD, Lanciotti RS, Tesh RB (2011) Probable non-vector-borne transmission of Zika virus, Colorado, USA. Emerg Infect Dis 17:880–882

    Article  PubMed  PubMed Central  Google Scholar 

  16. Fritzell C, Rousset D, Adde A, Kazanji M, Van Kerkhove MD, Flamand C (2018) Current challenges and implications for dengue, chikungunya and Zika seroprevalence studies worldwide: a scoping review. PLoS Negl Trop Dis 12:e0006533

    Article  PubMed  PubMed Central  Google Scholar 

  17. Gao D, Lou Y, He D, Porco TC, Kuang Y, Chowell G, Ruan S (2016) Prevention and control of Zika as a mosquito-borne and sexually transmitted disease: a mathematical modeling analysis. Sci Rep 6:28070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Hallmaier-Wacker LK, Munster VJ, Knauf S (2017) Disease reservoirs: from conceptual frameworks to applicable criteria. Emerg Microb Infect 6:e79

    Article  Google Scholar 

  19. Hirsch AJ, Smith JL, Haese NN, Broeckel RM, Parkins CJ, Kreklywich C, DeFilippis VR, Denton M, Smith PP, Messer WB, Colgin LM, Ducore RM, Grigsby PL, Hennebold JD, Swanson T, Legasse AW, Axthelm MK, MacAllister R, Wiley CA, Nelson JA, Streblow DN (2017) Zika Virus infection of rhesus macaques leads to viral persistence in multiple tissues. PLoS Pathog 13:e1006219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Ikejezie J, Shapiro CN, Kim J, Chiu M, Almiron M, Ugarte C, Espinal MA, Aldighieri S (2017) Zika virus transmission-region of the Americas, May 15, 2015–December 15, 2016. Am J Transplant 17:1681–1686

    Article  Google Scholar 

  21. Keasey SL, Pugh CL, Jensen SM, Smith JL, Hontz RD, Durbin AP, Dudley DM, O’Connor DH, Ulrich RG (2017) Antibody responses to Zika virus infections in environments of flavivirus endemicity. Clin Vaccine Immunol 24(4). pii: e00036-17. https://doi.org/10.1128/CVI.00036-17

  22. Kindhauser MK, Allen T, Frank V, Santhana RS, Dye C (2016) Zika: the origin and spread of a mosquito-borne virus. Bull World Health Org 94:675–686C

    Article  PubMed  Google Scholar 

  23. Lanciotti RS, Kosoy OL, Laven JJ, Velez JO, Lambert AJ, Johnson AJ, Stanfield SM, Duffy MR (2008) Genetic and serologic properties of Zika virus associated with an epidemic, Yap State, Micronesia, 2007. Emerg Infect Dis 14:1232–1239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Lim SK, Lim JK, Yoon IK (2017) An update on Zika Virus in Asia. Infect Chemother 49:91–100

    Article  PubMed  PubMed Central  Google Scholar 

  25. Maeda A, Maeda J (2013) Review of diagnostic plaque reduction neutralization tests for flavivirus infection. Vet J 195:33–40

    Article  PubMed  Google Scholar 

  26. Marano G, Pupella S, Vaglio S, Liumbruno GM, Grazzini G (2016) Zika virus and the never-ending story of emerging pathogens and transfusion medicine. Blood Transfus 14:95–100

    PubMed  PubMed Central  Google Scholar 

  27. Mattar S, Ojeda C, Arboleda J, Arrieta G, Bosch I, Botia I, Alvis-Guzman N, Perez-Yepes C, Gerhke L, Montero G (2017) Case report: microcephaly associated with Zika virus infection, Colombia. BMC Infect Dis 17:423

    Article  PubMed  PubMed Central  Google Scholar 

  28. Morales MA, Fabbri CM, Zunino GE, Kowalewski MM, Luppo VC, Enría DA, Levis SC, Calderón GE (2017) Detection of the mosquito-borne flaviviruses, West Nile, Dengue, Saint Louis Encephalitis, Ilheus, Bussuquara, and Yellow Fever in free-ranging black howlers (Alouatta caraya) of Northeastern Argentina. PLoS Negl Trop Dis 11:e0005351

    Article  PubMed  PubMed Central  Google Scholar 

  29. Moreira-Soto A, Carneiro IO, Fischer C, Feldmann M, Kümmerer BM, Silva NS, Santos UG, Souza BFCD, Liborio FA, Valença-Montenegro MM, Laroque PO, da Fontoura FR, Oliveira AVD, Drosten C, de Lamballerie X, Franke CR, Drexler JF (2018) Limited evidence for infection of Urban and Peri-urban Nonhuman Primates with Zika and Chikungunya Viruses in Brazil. https://doi.org/10.1128/mSphere.00523-17

    Article  PubMed  PubMed Central  Google Scholar 

  30. Osuna CE, Lim SY, Deleage C, Griffin BD, Stein D, Schroeder LT, Omange RW, Best K, Luo M, Hraber PT, Andersen-Elyard H, Ojeda EF, Huang S, Vanlandingham DL, Higgs S, Perelson AS, Estes JD, Safronetz D, Lewis MG, Whitney JB (2016) Zika viral dynamics and shedding in rhesus and cynomolgus macaques. Nat Med 22:1448–1455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Parra B, Lizarazo J, Jiménez-Arango JA, Zea-Vera AF, González-Manrique G, Vargas J, Angarita JA, Zuñiga G, Lopez-Gonzalez R, Beltran CL, Rizcala KH, Morales MT, Pacheco O, Ospina ML, Kumar A, Cornblath DR, Muñoz LS, Osorio L, Barreras P, Pardo CA (2016) Guillain-Barré syndrome associated with Zika virus infection in Colombia. N Engl J Med 375:1513–1523

    Article  PubMed  Google Scholar 

  32. Plowright RK, Parrish CR, McCallum H, Hudson PJ, Ko AI, Graham AL, Lloyd-Smith JO (2017) Pathways to zoonotic spillover. Nat Rev Microbiol 15:502–510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Sasaki M, Ishii A, Orba Y, Thomas Y, Hang’ombe BM, Moonga L, Mweene AS, Ogawa H, Nakamura I, Kimura T, Sawa H (2013) Human parainfluenza virus type 3 in wild nonhuman primates, Zambia. Emerg Infect Dis https://doi.org/10.3201/eid1909.121404

    Article  PubMed  PubMed Central  Google Scholar 

  34. Stiasny K, Kiermayr S, Holzmann H, Heinz FX (2006) Cryptic properties of a cluster of dominant flavivirus cross-reactive antigenic sites. J Virol 80:9557–9568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Takashima I, Morita K, Chiba M, Hayasaka D, Sato T, Takezawa C, Igarashi A, Kariwa H, Yoshimatsu K, Arikawa J, Hashimoto N (1997) A case of tick-borne encephalitis in Japan and isolation of the virus. J Clin Microbiol 35:1943–1947

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Terzian ACB, Zini N, Sacchetto L, Rocha RF, Parra MCP, Del Sarto JL, Dias ACF, Coutinho F, Rayra J, da Silva RA, Costa VV, Fernandes NCCA, Réssio R, Díaz-Delgado J, Guerra J, Cunha MS, Catão-Dias JL, Bittar C, Reis AFN, Santos INPD, Ferreira ACM, Cruz LEAA, Rahal P, Ullmann L, Malossi C, Araújo JP, Widen S, de Rezende IM, Mello É, Pacca CC, Kroon EG, Trindade G, Drumond B, Chiaravalloti-Neto F, Vasilakis N, Teixeira MM, Nogueira ML (2018) Evidence of natural Zika virus infection in neotropical non-human primates in Brazil. Sci Rep 8:16034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Wolfe ND, Kilbourn AM, Karesh WB, Rahman HA, Bosi EJ, Cropp BC, Andau M, Spielman A, Gubler DJ (2001) Sylvatic transmission of arboviruses among Bornean orangutans. Am J Trop Med Hyg 64:310–316

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are deeply grateful to the then Zambia Wildlife Authority (ZAWA), now the Department of National Parks and Wildlife, Ministry of Tourism and Arts, for assistance with sample collection in Zambia. ZIKV RNAs of DaKAR 41525 and FSS 13025 were kindly provided by Professor Scott C. Weaver, UTMB.

Funding

This study was supported by grants for Scientific Research (C), (B) from the Ministry of Education, Culture, Sports, Science and Technology, Japan (MEXT) /Japan Society for the Promotion of Science (JSPS) KAKENHI (JP15K07715, JP16H05805, JP17H03910); and grants for Scientific Research on Innovative Areas and International Group from the MEXT/JSPS KAKENHI (JP16H06431, JP16H06429, JP16K21723), and the Japan Initiative for Global Research Network of Infectious Diseases (J-GRID) from Japan Agency for Medical Research and Development (AMED) (JP18fm0108008).

Author information

Authors and Affiliations

  1. Division of Molecular Pathobiology, Research Center for Zoonosis Control, Hokkaido University, N20, W10, Kita-Ku, Sapporo, 001-0020, Japan

    Christida E. Wastika, Michihito Sasaki, Paulina D. Anindita, Yasuko Orba & Hirofumi Sawa

  2. Laboratory of Public Health, Graduate School of Veterinary Medicine, Hokkaido University, N18, W9, Kita-ku, Sapporo, 060-0818, Japan

    Kentaro Yoshii, Shintaro Kobayashi & Hiroaki Kariwa

  3. Department of Para-clinical Studies, School of Veterinary Medicine, University of Zambia, P.O. Box 32379, Lusaka, 10101, Zambia

    Bernard M. Hang’ombe

  4. Department of Disease Control, School of Veterinary Medicine, University of Zambia, P.O. Box 32379, Lusaka, 10101, Zambia

    Aaron S. Mweene

  5. Hokudai Center for Zoonosis Control in Zambia, Research Center for Zoonosis Control, Hokkaido University, P.O. Box 32379, Lusaka, 10101, Zambia

    Yuki Eshita

  6. National Virus Reference Laboratory, School of Medicine, University College Dublin, Dublin 4, Ireland

    Michael J. Carr

  7. Global Station for Zoonosis Control, Global Institution for Collaborative Research and Education (GI-CoRE), Hokkaido University, N20, W10, Kita-ku, Sapporo, 001-0020, Japan

    Michael J. Carr, William W. Hall & Hirofumi Sawa

  8. Centre for Research in Infectious Diseases, School of Medicine, University College Dublin, Dublin 4, Ireland

    William W. Hall

  9. Global Virus Network, 725 West Lombard St, Baltimore, MD, 21201, USA

    William W. Hall & Hirofumi Sawa

  10. Global Virus Network Affiliate Centre of Excellence, University of Zambia, P.O. Box 32379, Lusaka, 10101, Zambia

    Bernard M. Hang’ombe, Aaron S. Mweene & Hirofumi Sawa

  11. Africa Centre of Excellence for Infectious Diseases of Humans and Animals, P.O. Box 32379, Lusaka, 10101, Zambia

    Bernard M. Hang’ombe, Aaron S. Mweene, William W. Hall & Hirofumi Sawa

Authors
  1. Christida E. Wastika
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michihito Sasaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kentaro Yoshii
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Paulina D. Anindita
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bernard M. Hang’ombe
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Aaron S. Mweene
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Shintaro Kobayashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Hiroaki Kariwa
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Michael J. Carr
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. William W. Hall
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Yuki Eshita
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Yasuko Orba
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Hirofumi Sawa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hirofumi Sawa.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.

Additional information

Handling Editor: Tatjana Avsic-Zupanc.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 262 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wastika, C.E., Sasaki, M., Yoshii, K. et al. Serological evidence of Zika virus infection in non-human primates in Zambia. Arch Virol 164, 2165–2170 (2019). https://doi.org/10.1007/s00705-019-04302-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-019-04302-0

Search

Navigation