Hantavirus infection and habitat associations among rodent populations in agroecosystems of Panama: Implications for human disease risk

American Journal of Tropical Medicine and Hygiene

Volumn 81, Issue 1, 2009, Pages 59-66

  Armién, Aníbal G ^a   Armién, Blas ^b   Koster, Frederick ^d   Pascale, Juan M ^b   Avila, Mario ^b,c   Gonzalez, Publio ^b   De La Cruz, Manuel ^b   Zaldivar, Yamitzel ^b   Mendoza, Yaxelis ^b   Gracia, Fernando ^e   Hjelle, Brian ^f   Lee, Sang Joon ^f   Yates, Terry L ^h   Salazar Bravo, Jorge ^g  

^a UNIVERSITY OF MINNESOTA   (United States)

^b Instituto Conmemorativo Gorgas de Estudios de la Salud   (Panama)

^c Ministry of Health   (Panama)

^d LOVELACE RESPIRATORY RESEARCH INSTITUTE   (United States)

^e Santo Tomas Hospital   (Panama)

^f UNIVERSITY OF NEW MEXICO HEALTH SCIENCES CENTER   (United States)

^g TEXAS TECH UNIVERSITY   (United States)

^h NONE

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; GUANINE NUCLEOTIDE BINDING PROTEIN; RECOMBINANT PROTEIN; VIRUS ANTIBODY;

AGROECOSYSTEM; ARTICLE; COTTON RAT; CROP; DISEASE TRANSMISSION; ENZYME IMMUNOASSAY; HABITAT; HANTAVIRUS; IMMUNOBLOTTING; NONHUMAN; PANAMA; RAT; RESERVOIR; RICE RAT; RISK FACTOR; SEROPREVALENCE; VIRUS INFECTION; ANIMAL; ANIMAL DISEASE; BLOOD; ECOSYSTEM; FEMALE; HUMAN; INJURY; MALE; RODENT; RODENT DISEASE; VIROLOGY; ZOONOSIS;

CHOCLO VIRUS; HANTAVIRUS; OLIGORYZOMYS FULVESCENS; RODENTIA; SIGMODON HIRSUTUS; ZYGODONTOMYS BREVICAUDA;

ANIMALS; ANTIBODIES, VIRAL; CROPS, AGRICULTURAL; ECOSYSTEM; FEMALE; HANTAVIRUS INFECTIONS; HUMANS; MALE; PANAMA; RODENT DISEASES; RODENTIA; WOUNDS AND INJURIES; ZOONOSES;

EID: 67650327629     PISSN: 00029637     EISSN: None     Source Type: Journal    
DOI: 10.4269/ajtmh.2009.81.59     Document Type: Article

References (48)

1. Zaki SR, Greer PW, Coffield LM, Goldsmith CS, Nolte KB, Foucar K, Feddersen RM, Zumwalt RE, Miller GL, Khan AS, 1995. Hantavirus pulmonary syndrome: pathogenesis of an emerging infectious disease. Am J Pathol 146: 552-579.
2. Schmaljohn C, Hjelle B, 1997. Hantaviruses: a global disease problem. Emerg Infect Dis 3: 95-104. (Pubitemid 127431667)
3. Nichol ST, Spiropoulou CF, Morzunov S, Rollin PE, Ksiazek TG, Feldmann H, Sanchez A, Childs J, Zaki S, Peters CJ, 1993. Genetic identification of a hantavirus associated with an outbreak of acute respiratory illness. Science 262: 914-917. (Pubitemid 24014083)
4. Johnson AM, Bowen MD, Ksiazek TG, Williams RJ, Bryan RT, Mills JN, Peters CJ, Nichol ST, 1997. Laguna negra virus associated with HPS in western Paraguay and Bolivia. Virology 238: 115-127. (Pubitemid 27497268)
5. Padula PJ, Colavecchia SB, Martinez VP, Gonzalez Della Valle MO, Edelstein A, Miguel SD, Russi J, Riquelme JM, Colucci N, Almiron M, Rabinovich RD, 2000. Genetic diversity, distribution, and serological features of hantavirus infection in five countries in South America. J Clin Microbiol 38: 3029-3035. (Pubitemid 30640593)
6. Suzuki A, Bisordi I, Levis S, Garcia J, Pereira LE, Souza RP, Sugahara TK, Pini N, Enria D, Souza LT, 2004. Identifying rodent hantavirus reservoirs, Brazil. Emerg Infect Dis 10: 2127-2134. (Pubitemid 39587336)
7. Padula P, Figueroa R, Navarrete M, Pizarro E, Cadiz R, Bellomo C, Jofre C, Zaror L, Rodriguez E, Murua R, 2004. Transmission study of Andes hantavirus infection in wild sigmodontine rodents. J Virol 78: 11972-11979. (Pubitemid 39390782)
8. Botten J, Mirowsky K, Ye C, Gottlieb K, Saavedra M, Ponce L, Hjelle B, 2002. Shedding and intracage transmission of Sin Nombre hantavirus in the deer mouse (Peromyscus maniculatus) model. J Virol 76: 7587-7594. (Pubitemid 34760982)
9. Safronetz D, Drebot MA, Artsob H, Cote T, Makowski K, Lindsay LR, 2008. Sin Nombre virus shedding patterns in naturally infected deer mice (Peromyscus maniculatus) in relation to duration of infection. Vector Borne Zoonotic Dis 8: 97-100. (Pubitemid 351271589)
10. Chaparro J, Vega J, Terry W, Vera JL, Barra B, Meyer R, Peters CJ, Khan AS, Ksiazek TG, 1998. Assessment of person-to-person transmission of hantavirus pulmonary syndrome in a Chilean hospital setting. J Hosp Infect 40: 281-285. (Pubitemid 28552395)
11. Padula PJ, Edelstein A, Miguel SD, Lopez NM, Rossi CM, Rabinovich RD, 1998. Epidemic outbreak of hantavirus pulmonary syndrome in Argentina: molecular evidence of person to person transmission of Andes virus. Medicina (B Aires) 58 (Suppl 1): 27-36. (Pubitemid 128524533)
12. Armstrong LR, Zaki SR, Goldoft MJ, Todd RL, Khan AS, Khabbaz RF, Ksiazek TG, Peters CJ, 1995. Hantavirus pulmonary syndrome associated with entering or cleaning rarely used, rodent-infested structures. J Infect Dis 172: 1166.
13. Douglass RJ, Kuenzi AJ, Williams CY, Douglass SJ, Mills JN, 2003. Removing deer mice from buildings and the risk for human exposure to Sin Nombre virus. Emerg Infect Dis 9: 390-392. (Pubitemid 36330885)
14. Kuenzi AJ, Douglass RJ, Bond CW, 2000. Sin Nombre virus in deer mice captured inside homes, southwestern Montana. Emerg Infect Dis 6: 386-388. (Pubitemid 30643661)
15. Fulhorst CF, Milazzo ML, Armstrong LR, Childs JE, Rollin PE, Khabbaz R, Peters CJ, Ksiazek TG, 2007. Hantavirus and arena-virus antibodies in persons with occupational rodent exposure. Emerg Infect Dis 13: 532-538. (Pubitemid 46525098)
16. Mills JN, Ksiazek TG, Ellis BA, Rollin PE, Nichol ST, Yates TL, Gannon WL, Levy CE, Engelthaler DM, Davis T, Tanda DT, Frampton JW, Nichols CR, Peters CJ, Childs JE, 1997. Patterns of association with host and habitat: antibody reactive with Sin Nombre virus in small mammals in the major biotic communities of the southwestern United States. Am J Trop Med Hyg 56: 273-284. (Pubitemid 27181013)
17. Mills JN, Childs JE, 1998. Ecologic studies of rodent reservoirs: their relevance for human health. Emerg Infect Dis 4: 529-537. (Pubitemid 28553678)
18. Mills JN, Ksiazek TG, Peters CJ, Childs JE, 1999. Long-term studies of hantavirus reservoir populations in the southwestern United States: a synthesis. Emerg Infect Dis 5: 135-142. (Pubitemid 29124784)
19. Glass GE, Shields T, Cai B, Yates TL, Parmenter R, 2007. Persistently highest risk areas for hantavirus pulmonary syndrome: potential sites for refugia. Ecol Appl 17: 129-139. (Pubitemid 46596864)
20. Yahnke CJ, Meserve PL, Ksiazek TG, Mills JN, 2001. Patterns of infection with Laguna Negra virus in wild populations of Calomys laucha in the central Paraguayan chaco. Am J Trop Med Hyg 65: 768-776. (Pubitemid 34049471)
21. Vincent MJ, Quiroz E, Gracia F, Sanchez AJ, Ksiazek TG, Kitsutani PT, Ruedas LA, Tinnin DS, Caceres L, Garcia A, Rollin PE, Mills JN, Peters CJ, Nichol ST, 2000. Hantavirus pulmonary syndrome in Panama: identification of novel hantaviruses and their likely reservoirs. Virology 277: 14-19. (Pubitemid 30951081)
22. Bayard V, Kitsutani PT, Barria EO, Ruedas LA, Tinnin DS, Munoz C, de Mosca IB, Guerrero G, Kant R, Garcia A, Caceres L, Gracio FG, Quiroz E, de Castillo Z, Armien B, Libel M, Mills JN, Khan AS, Nichol ST, Rollin PE, Ksiazek TG, Peters CJ, 2004. Outbreak of hantavirus pulmonary syndrome, Los Santos, Panama, 1999-2000. Emerg Infect Dis 10: 1635-1642. (Pubitemid 39201516)
23. Ruedas LA, Salazar-Bravo J, Tinnin DS, Armien B, Caceres L, Garcia A, Diaz MA, Gracia F, Suzan G, Peters CJ, Yates TL, Mills JN, 2004. Community ecology of small mammal populations in Panama following an outbreak of hantavirus pulmonary syndrome. J Vector Ecol 29: 177-191. (Pubitemid 39008161)
24. Salazar-Bravo J, Armien B, Suzan G, Armien A, Ruedas LA, Avila M, Zaldivar Y, Pascale JM, Gracia F, Yates TL, 2004. Serosurvey of wild rodents for hantaviruses in Panama, 2000-2002. J Wildl Dis 40: 103-109. (Pubitemid 39026760)
25. Suzan G, Giermakowski JT, Marce E, Suzan-Azpiri H, Armien B, Yates TL, 2006. Modeling hantavirus reservoir species dominance in high seroprevalence areas on the Azuero Peninsula of Panama. Am J Trop Med Hyg 74: 1103-1110. (Pubitemid 351627424)
26. Armien B, Pascale JM, Bayard V, Munoz C, Mosca I, Guerrero G, Armien A, Quiroz E, Castillo Z, Zaldivar Y, Gracia F, Hjelle B, Koster F, 2004. High seroprevalence of hantavirus infection on the Azuero Peninsula of Panama. Am J Trop Med Hyg 70: 682-687. (Pubitemid 38802402)
27. Williams RJ, Bryan RT, Mills JN, Palma RE, Vera I, De Velasquez F, Baez E, Schmidt WE, Figueroa RE, Peters CJ, Zaki SR, Khan AS, Ksiazek TG, 1997. An outbreak of hantavirus pulmonary syndrome in western Paraguay. Am J Trop Med Hyg 57: 274-282. (Pubitemid 27407263)
28. Calderon G, Pini N, Bolpe J, Levis S, Mills J, Segura E, Guthmann N, Cantoni G, Becker J, Fonollat A, Ripoll C, Bortman M, Benedetti R, Enria D, 1999. Hantavirus reservoir hosts associated with peridomestic habitats in Argentina. Emerg Infect Dis 5: 792-797. (Pubitemid 30022464)
29. Torres-Perez F, Navarrete-Droguett J, Aldunate R, Yates TL, Mertz GJ, Vial PA, Ferres M, Marquet PA, Palma RE, 2004. Peridomestic small mammals associated with confirmed cases of human hantavirus disease in southcentral Chile. Am J Trop Med Hyg 70: 305-309. (Pubitemid 38366537)
30. 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: 42-46. (Pubitemid 41270307)
31. Wood S, Sebastian K, Sherr SJ, 2000. Pilot Analysis of Global Ecosystems: Agroecosystems. A Joint Study by the International Food Policy Research Institute and the World Resources Institute. Washington, DC: International Food Research Policy Institute.
32. Mills JN, Yates T, Childs JE, Parmenter RR, Ksiazek TG, Rollin PE, Peters CJ, 1995. Guidelines for working with rodents potentially infected with hantavirus. J Mammalogy 76: 716-722.
33. Mendez E, 1993. Los Roedores de Panama. Panama: Impresora Pacifico, S.A.
34. Reid FA, 1997. A Field Guide to the Mammals of Central America and Southeast Mexico. New York: Oxford University Press.
35. Hjelle B, Jenison S, Torrez-Martinez N, Herring B, Quan S, Polito A, Pichuantes S, Yamada T, Morris C, Elgh F, Lee HW, Artsob H, Dinello R, 1997. Rapid and specific detection of Sin Nombre virus antibodies in patients with hantavirus pulmonary syndrome by a strip immunoblot assay suitable for field diagnosis. J Clin Microbiol 35: 600-608. (Pubitemid 27083846)
36. Mills JN, Johnson JM, Ksiazek TG, Ellis BA, Rollin PE, Yates TL, Mann MO, Johnson MR, Campbell ML, Miyashiro J, Patrick M, Zyzak M, Lavender D, Novak MG, Schmidt K, Peters CJ, Childs JE, 1998. A survey of hantavirus antibody in small-mammal populations in selected United States national parks. Am J Trop Med Hyg 58: 525-532. (Pubitemid 28183268)
37. Mills JN, Schmidt K, Ellis BA, Calderon G, Enria DA, Ksiazek TG, 2007. A longitudinal study of hantavirus infection in three sympatric reservoir species in agroecosystems on the Argentine pampa. Vector Borne Zoonotic Dis 7: 229-240. (Pubitemid 47205940)
38. Pini N, Levis S, Calderon G, Ramirez J, Bravo D, Lozano E, Ripoll C, St Jeor S, Ksiazek TG, Barquez RM, Enria D, 2003. Hantavirus infection in humans and rodents, northwestern Argentina. Emerg Infect Dis 9: 1070-1076. (Pubitemid 37071547)
39. Calisher CH, Wagoner KD, Amman BR, Root JJ, Douglass RJ, Kuenzi AJ, Abbott KD, Parmenter C, Yates TL, Ksiazek TG, Beaty BJ, Mills JN, 2007. Demographic factors associated with prevalence of antibody to Sin Nombre virus in deer mice in the western United States. J Wildl Dis 43: 1-11. (Pubitemid 46510638)
40. McIntyre NE, Chu YK, Owen RD, Abuzeineh A, De la Sancha N, Dick CW, Holsomback T, Nisbett RA, Jonsson C, 2005. A longitudinal study of Bayou virus, hosts, and habitat. Am J Trop Med Hyg 73: 1043-1049. (Pubitemid 43038252)
41. Madhav NK, Wagoner KD, Douglass RJ, Mills JN, 2007. Delayed density-dependent prevalence of Sin Nombre virus antibody in Montana deer mice (Peromyscus maniculatus) and implications for human disease risk. Vector Borne Zoonotic Dis 7: 353-364. (Pubitemid 47536180)
42. Douglass RJ, Calisher CH, Wagoner KD, Mills JN, 2007. Sin Nombre virus infection of deer mice in Montana: characteristics of newly infected mice, incidence, and temporal pattern of infection. J Wildl Dis 43: 12-22. (Pubitemid 46510639)
43. Suzan G, Armien AG, Mills JN, Marce E, Ceballos G, Avila M, Salazar-Bravo J, Ruedas LA, Armien B, Yates T, 2008. Epidemiological considerations of rodent community composition in fragmented landscapes in Panama. J Mammal 89: 684-690. (Pubitemid 351842440)
44. Glass GE, Livingstone W, Mills JN, Hlady WG, Fine JB, Biggler W, Coke T, Frazier D, Atherley S, Rollin PE, Ksiazek TG, Peters CJ, Childs JE, 1998. Black Creek Canal virus infection in Sigmodon hispidus in southern Florida. Am J Trop Med Hyg 59: 699-703. (Pubitemid 28524524)
45. Escutenaire S, Chalon P, De Jaegere F, Karelle-Bui L, Mees G, Brochier B, Rozenfeld F, Pastoret PP. 2002. Behavioral, physiologic, and habitat influences on the dynamics of Puumala virus infection in bank voles (Clethrionomys glareolus). Emerg Infect Dis 8: 930-936.
46. Glass GE, Childs JE, Korch GW, LeDuc JW, 1988. Association of intraspecific wounding with hantaviral infection in wild rats (Rattus norvegicus). Epidemiol Infect 101: 459-1412 (Pubitemid 18243454)
47. Hinson ER, Shone SM, Zink MC, Glass GE, Klein SL, 2004. Wounding: the primary mode of Seoul virus transmission among male Norway rats. Am J Trop Med Hyg 70: 310-317. (Pubitemid 38366538)
48. Kuenzi AJ, Douglass RJ, White D Jr, Bond CW, Mills JN, 2001. Antibody to Sin Nombre virus in rodents associated with peridomestic habitats in west central Montana. Am Trop Med Hyg 64: 137-146. (Pubitemid 32565841)