A Silent Enzootic of an Orthopoxvirus in Ghana, West Africa: Evidence for Multi-Species Involvement in the Absence of Widespread Human Disease

Mary G. Reynolds Division of Viral and Rickettsial Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Ghana Health Service, Ghana Ministry of Health, Accra, Ghana; Wildlife Division of the Forestry Commission, Accra, Ghana; Virology Department, Noguchi Memorial Institute for Medical Research, College of Health Sciences, University of Ghana, Legon, Ghana; United States Department of Agriculture, National Wildlife Research Center, Fort Collins, Colorado

Search for other papers by Mary G. Reynolds in
Current site
Google Scholar
PubMed
Close
,
Darin S. Carroll Division of Viral and Rickettsial Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Ghana Health Service, Ghana Ministry of Health, Accra, Ghana; Wildlife Division of the Forestry Commission, Accra, Ghana; Virology Department, Noguchi Memorial Institute for Medical Research, College of Health Sciences, University of Ghana, Legon, Ghana; United States Department of Agriculture, National Wildlife Research Center, Fort Collins, Colorado

Search for other papers by Darin S. Carroll in
Current site
Google Scholar
PubMed
Close
,
Victoria A. Olson Division of Viral and Rickettsial Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Ghana Health Service, Ghana Ministry of Health, Accra, Ghana; Wildlife Division of the Forestry Commission, Accra, Ghana; Virology Department, Noguchi Memorial Institute for Medical Research, College of Health Sciences, University of Ghana, Legon, Ghana; United States Department of Agriculture, National Wildlife Research Center, Fort Collins, Colorado

Search for other papers by Victoria A. Olson in
Current site
Google Scholar
PubMed
Close
,
Christine Hughes Division of Viral and Rickettsial Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Ghana Health Service, Ghana Ministry of Health, Accra, Ghana; Wildlife Division of the Forestry Commission, Accra, Ghana; Virology Department, Noguchi Memorial Institute for Medical Research, College of Health Sciences, University of Ghana, Legon, Ghana; United States Department of Agriculture, National Wildlife Research Center, Fort Collins, Colorado

Search for other papers by Christine Hughes in
Current site
Google Scholar
PubMed
Close
,
Jack Galley Division of Viral and Rickettsial Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Ghana Health Service, Ghana Ministry of Health, Accra, Ghana; Wildlife Division of the Forestry Commission, Accra, Ghana; Virology Department, Noguchi Memorial Institute for Medical Research, College of Health Sciences, University of Ghana, Legon, Ghana; United States Department of Agriculture, National Wildlife Research Center, Fort Collins, Colorado

Search for other papers by Jack Galley in
Current site
Google Scholar
PubMed
Close
,
Anna Likos Division of Viral and Rickettsial Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Ghana Health Service, Ghana Ministry of Health, Accra, Ghana; Wildlife Division of the Forestry Commission, Accra, Ghana; Virology Department, Noguchi Memorial Institute for Medical Research, College of Health Sciences, University of Ghana, Legon, Ghana; United States Department of Agriculture, National Wildlife Research Center, Fort Collins, Colorado

Search for other papers by Anna Likos in
Current site
Google Scholar
PubMed
Close
,
Joel M. Montgomery Division of Viral and Rickettsial Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Ghana Health Service, Ghana Ministry of Health, Accra, Ghana; Wildlife Division of the Forestry Commission, Accra, Ghana; Virology Department, Noguchi Memorial Institute for Medical Research, College of Health Sciences, University of Ghana, Legon, Ghana; United States Department of Agriculture, National Wildlife Research Center, Fort Collins, Colorado

Search for other papers by Joel M. Montgomery in
Current site
Google Scholar
PubMed
Close
,
Richard Suu-Ire Division of Viral and Rickettsial Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Ghana Health Service, Ghana Ministry of Health, Accra, Ghana; Wildlife Division of the Forestry Commission, Accra, Ghana; Virology Department, Noguchi Memorial Institute for Medical Research, College of Health Sciences, University of Ghana, Legon, Ghana; United States Department of Agriculture, National Wildlife Research Center, Fort Collins, Colorado

Search for other papers by Richard Suu-Ire in
Current site
Google Scholar
PubMed
Close
,
Mubarak O. Kwasi Division of Viral and Rickettsial Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Ghana Health Service, Ghana Ministry of Health, Accra, Ghana; Wildlife Division of the Forestry Commission, Accra, Ghana; Virology Department, Noguchi Memorial Institute for Medical Research, College of Health Sciences, University of Ghana, Legon, Ghana; United States Department of Agriculture, National Wildlife Research Center, Fort Collins, Colorado

Search for other papers by Mubarak O. Kwasi in
Current site
Google Scholar
PubMed
Close
,
J. Jeffrey Root Division of Viral and Rickettsial Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Ghana Health Service, Ghana Ministry of Health, Accra, Ghana; Wildlife Division of the Forestry Commission, Accra, Ghana; Virology Department, Noguchi Memorial Institute for Medical Research, College of Health Sciences, University of Ghana, Legon, Ghana; United States Department of Agriculture, National Wildlife Research Center, Fort Collins, Colorado

Search for other papers by J. Jeffrey Root in
Current site
Google Scholar
PubMed
Close
,
Zach Braden Division of Viral and Rickettsial Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Ghana Health Service, Ghana Ministry of Health, Accra, Ghana; Wildlife Division of the Forestry Commission, Accra, Ghana; Virology Department, Noguchi Memorial Institute for Medical Research, College of Health Sciences, University of Ghana, Legon, Ghana; United States Department of Agriculture, National Wildlife Research Center, Fort Collins, Colorado

Search for other papers by Zach Braden in
Current site
Google Scholar
PubMed
Close
,
Jason Abel Division of Viral and Rickettsial Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Ghana Health Service, Ghana Ministry of Health, Accra, Ghana; Wildlife Division of the Forestry Commission, Accra, Ghana; Virology Department, Noguchi Memorial Institute for Medical Research, College of Health Sciences, University of Ghana, Legon, Ghana; United States Department of Agriculture, National Wildlife Research Center, Fort Collins, Colorado

Search for other papers by Jason Abel in
Current site
Google Scholar
PubMed
Close
,
Cody Clemmons Division of Viral and Rickettsial Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Ghana Health Service, Ghana Ministry of Health, Accra, Ghana; Wildlife Division of the Forestry Commission, Accra, Ghana; Virology Department, Noguchi Memorial Institute for Medical Research, College of Health Sciences, University of Ghana, Legon, Ghana; United States Department of Agriculture, National Wildlife Research Center, Fort Collins, Colorado

Search for other papers by Cody Clemmons in
Current site
Google Scholar
PubMed
Close
,
Russell Regnery Division of Viral and Rickettsial Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Ghana Health Service, Ghana Ministry of Health, Accra, Ghana; Wildlife Division of the Forestry Commission, Accra, Ghana; Virology Department, Noguchi Memorial Institute for Medical Research, College of Health Sciences, University of Ghana, Legon, Ghana; United States Department of Agriculture, National Wildlife Research Center, Fort Collins, Colorado

Search for other papers by Russell Regnery in
Current site
Google Scholar
PubMed
Close
,
Kevin Karem Division of Viral and Rickettsial Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Ghana Health Service, Ghana Ministry of Health, Accra, Ghana; Wildlife Division of the Forestry Commission, Accra, Ghana; Virology Department, Noguchi Memorial Institute for Medical Research, College of Health Sciences, University of Ghana, Legon, Ghana; United States Department of Agriculture, National Wildlife Research Center, Fort Collins, Colorado

Search for other papers by Kevin Karem in
Current site
Google Scholar
PubMed
Close
, and
Inger K. Damon Division of Viral and Rickettsial Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Ghana Health Service, Ghana Ministry of Health, Accra, Ghana; Wildlife Division of the Forestry Commission, Accra, Ghana; Virology Department, Noguchi Memorial Institute for Medical Research, College of Health Sciences, University of Ghana, Legon, Ghana; United States Department of Agriculture, National Wildlife Research Center, Fort Collins, Colorado

Search for other papers by Inger K. Damon in
Current site
Google Scholar
PubMed
Close
Restricted access

Human monkeypox has never been reported in Ghana, but rodents captured in forested areas of southern Ghana were the source of the monkeypox virus introduced into the United States in 2003. Subsequent to the outbreak in the United States, 204 animals were collected from two commercial trapping sites in Ghana. Animal tissues were examined for the presence of orthopoxvirus (OPXV) DNA using a real-time polymerase chain reaction, and sera were assayed for antibodies against OPXV. Animals from five genera (Cricetomys, Graphiurus, Funiscirus, and Heliosciurus) had antibodies against OPXV, and three genera (Cricetomys, Graphiurus, and Xerus) had evidence of OPXV DNA in tissues. Additionally, 172 persons living near the trapping sites were interviewed regarding risk factors for OPXV exposure, and their sera were analyzed. Fifty-three percent had IgG against OPXV; none had IgM. Our findings suggest that several species of forest-dwelling rodents from Ghana are susceptible to naturally occurring OPXV infection, and that persons living near forests may have low-level or indirect exposure to OPXV-infected animals, possibly resulting in sub-clinical infections.

Author Notes

*Address correspondence to Mary G. Reynolds, Division of Viral and Rickettsial Diseases, Centers for Disease Control and Prevention, 1600 Clifton Road NE, Mailstop G-43 Atlanta, GA 30333. E-mail: nzr6@cdc.gov
†These authors contributed equally to this article.

Financial support: This study was supported by the Centers for Disease Control and Prevention, with participation from U.S. Department of Agriculture–Animal and Plant Health Inspection Service and the government of the Republic of Ghana.

Authors' addresses: Mary G. Reynolds, Darin S. Carroll, Victoria A. Olson, Christine Hughes, Anna Likos, Zach Braden, Jason Abel, Cody Clemmons, Russell Regnery, Kevin Karem, and Inger K. Damon, Division of Viral and Rickettsial Diseases, Centers for Disease Control and Prevention, Atlanta, GA, E-mails: nzr6@cdc.gov, zuz4@cdc.gov, vao9@cdc.gov, bvp6@dc.gov, abl5@cdc.gov, zab5@cdc.gov, jza5@cdc.gov, buq4@cdc.gov, rur1@cdc.gov, kdk6@cdc.gov, and iad7@cdc.gov. Jack Galley, Ghana Health Service, Ghana Ministry of Health Accra, Ghana, E-mail: jgalley@hotmail.com. Joel M. Montgomery, U.S. Naval Medical Research Center Detachment Peru, American Embassy Unit 3800, Lima, Peru, E-mail: joel.montgomery@med.navy.mil. Richard Suu-Ire, Wildlife Division of the Forestry Commission Accra Zoo, Accra, Ghana, E-mail: suuire@hotmail.com. Mubarak O. Kwasi, Virology Unit, Noguchi Memorial Institute for Medical Research, College of Health Sciences, University of Ghana, Legon, Ghana, E-mail: mosei-kwasi@noguchi.mimcom.net. J. Jeffrey Root, Animal and Plant Health Inspection Service, Wildlife Services, U.S. Department of Agriculture, National Wildlife Research Center, Fort Collins, CO, E-mail: jeff.root@aphis.usda.gov.

  • 1.

    Ladnyj ID, Ziegler P, Kima E, 1972. A human infection caused by monkeypox virus in Basankusu Territory, Democratic Republic of the Congo. Bull World Health Organ 46: 593597.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2.

    Foster SO, Brink EW, Hutchins DL, Pifer JM, Lourie B, Moser CR, Cummings EC, Kuteyi OE, Eke RE, Titus JB, Smith EA, Hicks JW, Foege WH, 1972. Human monkeypox. Bull World Health Organ 46: 569576.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    Marennikova SS, Seluhina EM, Mal'ceva NN, Cimiskjan KL, Macevic GR, 1972. Isolation and properties of the causal agent of a new variola-like disease (monkeypox) in man. Bull World Health Organ 46: 599611.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Arita I, Jezek Z, Khodakevich L, Ruti K, 1985. Human monkeypox: a newly emerged orthopoxvirus zoonosis in the tropical rain forests of Africa. Am J Trop Med Hyg 34: 781789.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Khodakevich L, Jezek Z, Kinzanzka K, 1986. Isolation of monkeypox virus from wild squirrel infected in nature. Lancet 1: 9899.

  • 6.

    Breman JG, Nakano JH, Coffi E, Godfrey H, Gautun JC, 1977. Human poxvirus disease after smallpox eradication. Am J Trop Med Hyg 26: 273281.

  • 7.

    Hutin YJ, Williams RJ, Malfait P, Pebody R, Loparev VN, Ropp SL, Rodriguez M, Knight JC, Tshioko FK, Khan AS, Szczeniowski MV, Esposito JJ, 2001. Outbreak of human monkeypox, Democratic Republic of Congo, 1996 to 1997. Emerg Infect Dis 7: 434438.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    Khodakevich L, Szczeniowski M, Manbu-ma-Disu, Jezek Z, Marennikova S, Nakano J, Messinger D, 1987. The role of squirrels in sustaining monkeypox virus transmission. Trop Geogr Med 39: 115122.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Levine RS, Peterson AT, Yorita KL, Carroll D, Damon IK, Reynolds MG, 2007. Ecological niche and geographic distribution of human monkeypox in Africa. PLoS One 2: e176.

  • 10.

    2003. Update: multistate outbreak of monkeypox – Illinois, Indiana, Kansas, Missouri, Ohio, and Wisconsin, 2003. MMWR Morb Mortal Wkly Rep 52: 642646.

  • 11.

    Hutson CL, Lee KN, Abel J, Carroll DS, Montgomery JM, Olson VA, Li Y, Davidson W, Hughes C, Dillon M, Spurlock P, Kazmierczak JJ, Austin C, Miser L, Sorhage FE, Howell J, Davis JP, Reynolds MG, Braden Z, Karem KL, Damon IK, Regnery RL, 2007. Monkeypox zoonotic associations: insights from laboratory evaluation of animals associated with the multi-state US outbreak. Am J Trop Med Hyg 76: 757768.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Li Y, Olson VA, Laue T, Laker MT, Damon IK, 2006. Detection of monkeypox virus with real-time PCR assays. J Clin Virol 36: 194203.

  • 13.

    Olson VA, Laue T, Laker MT, Babkin IV, Drosten C, Shchelkunov SN, Niedrig M, Damon IK, Meyer H, 2004. Real-time PCR system for detection of orthopoxviruses and simultaneous identification of smallpox virus. J Clin Microbiol 42: 19401946.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Karem KL, Reynolds M, Braden Z, Lou G, Bernard N, Patton J, Damon IK, 2005. Characterization of acute-phase humoral immunity to monkeypox: use of immunoglobulin M enzyme-linked immunosorbent assay for detection of monkeypox infection during the 2003 North American outbreak. Clin Diagn Lab Immunol 12: 867872.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Bhalotra S, Heady C, 2000. Determinants of Child Farm Labor in Ghana and Pakistan: a Comparative Study. Cambridge, UK: University of Cambridge.

  • 16.

    Karem KL, Reynolds M, Hughes C, Braden Z, Nigam P, Crotty S, Glidewell J, Ahmed R, Amara R, Damon IK, 2007. Monkeypox-induced immunity and failure of childhood smallpox vaccination to provide complete protection. Clin Vaccine Immunol 14: 13181327.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Carroll DS, Mills JN, Montgomery JM, Bausch DG, Blair PJ, Burans JP, Felices V, Gianella A, Iihoshi N, Nichol ST, Olson JG, Rogers DS, Salazar M, Ksiazek TG, 2005. Hantavirus pulmonary syndrome in Central Bolivia: relationships between reservoir hosts, habitats, and viral genotypes. Am J Trop Med Hyg 72: 4246.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Bennett M, Crouch AJ, Begon M, Duffy B, Feore S, Gaskell RM, Kelly DF, McCracken CM, Vicary L, Baxby D, 1997. Cowpox in British voles and mice. J Comp Pathol 116: 3544.

  • 19.

    Begon M, Hazel SM, Baxby D, Bown K, Cavanagh R, Chantrey J, Jones T, Bennett M, 1999. Transmission dynamics of a zoonotic pathogen within and between wildlife host species. Proc Biol Sci 266: 19391945.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Karem KL, Reynolds M, Olson V, Li Y, Damon IK, 2006. Monkeypox outbreak diagnostics and implications for vaccine protective effect. Nat Med 12: 495496.

  • 21.

    Jezek Z, Nakano JH, Arita I, Mutombo M, Szczeniowski M, Dunn C, 1987. Serological survey for human monkeypox infections in a selected population in Zaire. J Trop Med Hyg 90: 3138.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Reynolds MG, Davidson WB, Curns AT, Conover CS, Huhn G, Davis JP, Wegner M, Croft DR, Newman A, Obiesie NN, Hansen GR, Hays PL, Pontones P, Beard B, Teclaw R, Howell JF, Braden Z, Holman RC, Karem KL, Damon IK, 2007. Spectrum of infection and risk factors for human monkeypox, United States, 2003. Emerg Infect Dis 13: 13321339.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Baxby D, Hessami M, Ghaboosi B, Ramyar H, 1975. Response of camels to intradermal inoculation with smallpox and camelpox viruses. Infect Immun 11: 617621.

  • 24.

    Lourie B, Nakano JH, Kemp GE, Setzer HW, 1975. Isolation of poxvirus from an African Rodent. J Infect Dis 132: 677681.

Past two years Past Year Past 30 Days
Abstract Views 60317 59517 12963
Full Text Views 1917 276 114
PDF Downloads 742 48 6
 

 

 

 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save