Ecological study of hantavirus infection in wild rodents in an endemic area in Brazil

Acta Tropica

Volumn 131, Issue 1, 2014, Pages 1-10

  Oliveira, Renata Carvalho ^a   Gentile, Rosana ^a   Guterres, Alexandro ^a   Fernandes, Jorlan ^a   Teixeira, Bernardo Rodrigues ^a   Vaz, Vanderson ^a   Valdez, Fernanda Pedone ^a,b   Vicente, Luciana Helena Bassan ^a   da Costa Neto, Sócrates Fraga ^a   Bonvicino, Cibele ^a,b   D'Andrea, Paulo Sergio ^a   Lemos, Elba R S ^a  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b INSTITUTO NACIONAL DE CÂNCER   (Brazil)

Author keywords

Hantavirus; Jabora virus; Juquitiba virus; Population ecology; Rodents

Indexed keywords

ANTIBODY; DISEASE PREVALENCE; DISEASE VECTOR; POPULATION OUTBREAK; POPULATION SIZE; RODENT; VIRAL DISEASE;

AKODON MONTENSIS; ANTIGEN ANTIBODY REACTION; ARTICLE; AUTUMN; BRAZIL; BRUCEPATTERSONIUS IHERINGI; CAVIA APEREA; CAVIINAE; CONTROLLED STUDY; CRYPTONANUS CHACOENSIS; DELOMYS DORSALIS; DIDELPHIS ALBIVENTRIS; DIDELPHIS AURITA; ECOLOGY; ENDEMIC DISEASE; EUMYSOPINAE; EURYZYGOMATOMYS SPINOSUS; FEMALE; HANTAVIRUS INFECTION; JABORA VIRUS; JUQUITIBA VIRUS; LUNG INFECTION; MALE; MOUSE; MURINAE; MUS MUSCULUS; NECTOMYS SQUAMIPES; NONHUMAN; OLIGORYZOMYS NIGRIPES; OXYMYCTERUS JUDEX; POPULATION DYNAMICS; POPULATION SIZE; RATTUS RATTUS; REPRODUCTION; RNA EXTRACTION; SEASONAL VARIATION; SEROLOGY; SIGMODONTINAE; SOORETAMYS ANGOUYA; SPRING; SUMMER; TAXONOMY; THAPTOMYS NIGRITA; WINTER;

BRAZIL; SANTA CATARINA;

HANTAVIRUS; JABORA VIRUS; JUQUITIBA VIRUS; POPULATION ECOLOGY; RODENTS;

ANIMALS; ANTIBODIES, VIRAL; BRAZIL; FEMALE; HANTAVIRUS; HANTAVIRUS INFECTIONS; HANTAVIRUS PULMONARY SYNDROME; HUMANS; MALE; POPULATION DYNAMICS; PREVALENCE; RODENT DISEASES; RODENTIA; SEASONS; SEX FACTORS;

EID: 84890193455     PISSN: 0001706X     EISSN: 18736254     Source Type: Journal    
DOI: 10.1016/j.actatropica.2013.11.016     Document Type: Article

References (67)

1. Abbott K.D., Ksiazek T.G., Mills J.N. Long-term hantavirus persistence in rodent populations in central Arizona. Emerg. Infect. Dis. 1999, 5:102-112.
2. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990, 215:403-410.
3. Arai S., Song J.-W., Sumibcay L., Bennett S.N., Nerurkar V.R., Parmenter C., Cook J.A., Yates T.L., Yanagihara R. Hantavirus in northern short-tailed shrew, United States. Emerg. Infect. Dis. 2007, 13:1420-1423.
4. Beldomenico P.M., Telfer S., Gebert S., Lukomski L., Bennett M., Begon M. Poor condition and infection: a vicious circle in natural populations. Proc. R. Soc. B: Biol. Sci. 2008, 275:1753-1759.
5. Bonaventura S.M., Kravetz F.O., Suarez O.V. The relationship between food availability, space use and territoriality in Akodon azarae (Rodentia, Cricetidae). Mammalia 1992, 56:407-417.
6. Bonvicino C.R., D'Andrea P.S., Cerqueira R., Seuánez H.N. The chromosomes of Nectomys (Rodentia, Cricetidae) with 2n=52, 2n=56, and interspecific hybrids (2n=54). Cytogenet. Cell Genet. 1996, 73:190-193.
7. Bonvicino C.R., Otazu I.B., D'Andrea P.S. Karyologic evidence of diversification of the genus Thrichomys (Rodentia, Echimyidae). Cytogenet. Genome Res. 2002, 97:200-204.
8. Childs J.E., Ksiazek T.G., Spiropoulou C.F., Krebs J.W., Morzunov S., Maupin G.O., Gage K.L., Rollin P.E., Sarisky J., Enscore R.E. Serologic and genetic identification of Peromyscus maniculatus as the primary rodent reservoir for a new hantavirus in the southwestern United States. J. Infect. Dis. 1994, 169:1271-1280.
9. Chu Y.K., Goodin D., Owen R.D., Koch D., Jonsson C.B. Sympatry of 2 hantavirus strains, Paraguay, 2003-2007. Emerg. Infect. Dis. 2009, 15:1977-1980.
10. Dobson A.P., Hudson P.J. Microparasites: observed patterns in wild animal populations. Ecology of Infectious Diseases in Natural Populations 1995, 52-89. Cambridge University Press, Cambridge, UK. B.T. Grenfell, A.P. Dobson (Eds.).
11. Douglass R.J., Wilson T., Semmens W.J., Zanto S.N., Bond C.W., Van Horn R.C., Mills J.N. Longitudinal studies of Sin Nombre virus in deer mouse-dominated ecosystems of Montana. Am. J. Trop. Med. Hyg. 2001, 65:33-41.
12. Easterbrook J.D., Klein S.L. Immunological mechanisms mediating hantavirus persistence in rodent reservoirs. PLoS Pathog. 2008, 4:e1000172.
13. Engelthaler D.M., Mosley D.G., Cheek J.E., Levy C.E., Komatsu K.K., Ettestad P., Davis T., Tanda D.T., Miller L., Frampton J.W., Porter R., Bryan R.T. Climatic and environmental patterns associated with hantavirus pulmonary syndrome, four corners region, United States. Emerg. Infect. Dis. 1999, 5:87-94.
14. Firth C., Tokarz R., Simith D.B., Nunes M.R.T., Bhat M., Rosa E.S.T., Medeiros D.B., Palacios G., Vasconcelos P.F.C., Lipkin W.I. Diversity and distribution of hantaviruses in South America. J. Virol. 2012, 86:13756-13766.
15. Gannon W.L., Sikes R.S. Guidelines of the American society of mammalogists for the use of wild mammals in research. J. Mammal. 2007, 88:809-823.
16. Gentile R., Andrea P.S.D., Cerqueira R., Maroja L.S. Population dynamics and reproduction of marsupials and rodents in a Brazilian rural area: a five-year study. Stud. Neotrop. Fauna Environ. 2000, 9:1-9.
17. Gentile R., D'Andrea P.S., Cerqueira R. Home ranges of Philander frenata and Akodon cursor in a Brazilian restinga (coastal shrubland). Mastozool. Neotrop. 1997, 4:105-112.
18. Giovannoni M., Vellozo L.G.C., Kubiak G.V.L. Sobre as "ratadas" do primeiro planalto paranaense. Arq. Biol. Tecnol. 1946, 1:185-195.
19. Gubler D.J., Reiter P., Ebi K.L., Yap W., Nasci R., Patz J.A. Climate variability and change in the United States: potential impacts on vector- and rodent-borne diseases. Environ. Health Perspect. 2001, 109:223-233.
20. Hjelle B., Torres-Pérez F. Hantaviruses in the Americas and their role as emerging pathogens. Viruses 2010, 2:2559-2586.
21. Jaksic F.M., Lima M. Myths and facts on ratadas: bamboo blooms, rainfall peaks and rodent outbreaks in South America. Austral Ecol. 2003, 28:237-251.
22. Johnson A.M., Souza L.T.M., De Ferreira I.B., Pereira L.E., Ksiazek T.G., Rollin P.E., Peters C.J., Nichol S.T. Genetic investigation of novel hantaviruses causing fatal HPS in Brazil. J. Med. Virol. 1999, 535:527-535.
23. Jonsson C.B., Figueiredo L.T.M., Vapalahti O. A global perspective on hantavirus ecology, epidemiology, and disease. Clin. Microbiol. Rev. 2010, 23:412-441.
24. Kallio E.R., Begon M., Henttonen H., Koskela E., Mappes T., Vaheri A., Vapalahti O. Hantavirus infections in fluctuating host populations: the role of maternal antibodies. Proc. R. Soc. B: Biol. Sci. 2010, 277:3783-3791.
25. Kallio E.R., Klingström J., Gustafsson E., Manni T., Vaheri A., Henttonen H., Vapalahti O., Lundkvist A. Prolonged survival of Puumala hantavirus outside the host: evidence for indirect transmission via the environment. J. Gen. Virol. 2006, 87:2127-2134.
26. Kang H.J., Bennett S.N., Sumibcay L., Arai S., Hope A.G., Mocz G., Song J.-W., Cook J.A., Yanagihara R. Evolutionary insights from a genetically divergent hantavirus harbored by the European common mole (Talpa europaea). PLoS ONE 2009, 4:e6149.
27. Klein S.L., Zink M.C., Glass G.E. Seoul virus infection increases aggressive behaviour in male Norway rats. Anim. Behav. 2004, 67:421-429.
28. Klempa B., Fichet-Calvet E., Lecompte E., Auste B., Aniskin V., Meisel H., Barrière P., Koivogui L., Meulen J., Ter Krüger D.H. Novel hantavirus sequences in shrew, Guinea. Emerg. Infect. Dis. 2007, 13:3-5.
29. Lehmer E.M., Clay C.A., Wilson E., Jeor S.S., Dearing M.D. Differential resource allocation in deer mice exposed to sin nombre virus. Physiol. Biochem. Zool. 2007, 80:514-521.
30. Madhav N.K., Wagoner K.D., Douglass R.J., Mills J.N. 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. (Larchmont, NY) 2007, 7:353-364.
31. Miller S., Rottmann J. Guía Para el Reconocimiento de Mamíferos Chilenos 1976, Editora Nacional Gabriela Mistral, Santiago de Chile.
32. Mills J.N. Regulation of rodent-borne viruses in the natural host: implications for human disease. Arch. Virol. Suppl. 2005, 19:45-57.
33. Mills J.N., Amman B.R., Glass G.E. Ecology of hantaviruses and their hosts in North America. Vector Borne Zoonotic Dis. (Larchmont, NY) 2010, 10:563-574.
34. Mills J.N., Childs J.E. Ecologic studies of rodent reservoirs: their relevance for human health. Emerg. Infect. Dis. 1998, 4:529-537.
35. Mills J.N., Childs J.E., Ksiazek T.G., Peters C.J. Methods for Trapping and Sampling Small Mammals for Virologic Testing 1995, Department of Health and Human Services, Atlanta, GA.
36. Mills J.N., Ksiazek T.G., Ellis B.A., Rollin P.E., Nichol S.T., Yates T.L., Gannon W.L., Levy C.E., Engelthaler D.M., Davis T., Tanda D.T., Frampton J.W., Nichols C.R., Peters C.J., Childs J.E. 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. 1997, 56:273-284.
37. Mills J.N., Ksiazek T.G., Peters C.J., Childs J.E. Long-term studies of hantavirus reservoir populations in the southwestern United States: a synthesis. Emerg. Infect. Dis. 1999, 5:135-142.
38. Mills J.N., Schmidt K., Ellis B.A., Calderón G., Enría D.A., Ksiazek T.G. A longitudinal study of hantavirus infection in three sympatric reservoir species in agroecosystems on the Argentine Pampa. Vector Borne Zoonotic Dis. (Larchmont, NY) 2007, 7:229-240.
39. Nichol S.T., Spiropoulou C.F., Morzunov S., Rollin P.E., Ksiazek T.G., Feldmann H., Sanchez A., Childs J., Zaki S., Peters C.J. Genetic identification of a hantavirus associated with an outbreak of acute respiratory illness. Science 1993, 262:914-917.
40. Nimer E. Climatologia do Brasil 1989, IBGE, Departamento de Recursos Naturais e Estudos Ambientais, Rio de Janeiro. 2nd ed.
41. Oliveira R.C., Teixeira B.R., Mello F.C., Pereira A.P., Duarte A.S., Bonaldo M.C., Bonvicino C.R., D'Andrea P.S., Lemos E.R.S. Genetic characterization of a Juquitiba-like viral lineage in Oligoryzomys nigripes in Rio de Janeiro, Brazil. Acta Trop. 2009, 112:212-218.
42. Oliveira R.C., Padula P.J., Gomes R., Martinez V.P., Bellomo C., Bonvicino C.R., Freire e Lima D.I., Bragagnolo C., Caldas A.C.S., D'Andrea P.S., de Lemos E.R.S. Genetic characterization of hantaviruses associated with sigmodontine rodents in an endemic area for hantavirus pulmonary syndrome in southern Brazil. Vector Borne Zoonotic Dis. 2011, 11:301-314.
43. Ostfeld R.S. The ecology of territoriality in small mammals. Trends Ecol. Evol. (Personal Ed.) 1990, 5:411-415.
44. Owen R.D., Goodin D.G., Koch D.E., Chu Y.-K., Jonsson C.B. Spatiotemporal variation in Akodon montensis (Cricetidae: Sigmodontinae) and hantaviral seroprevalence in a subtropical forest ecosystem. J. Mammal. 2010, 91:467-481.
45. Padula P.J., Rossi C.M., Della Valle M.O., Martínez P.V., Colavecchia S.B., Edelstein A., Miguel S.D., Rabinovich R.D., Segura E.L. Development and evaluation of a solid-phase enzyme immunoassay based on Andes hantavirus recombinant nucleoprotein. J. Med. Microbiol. 2000, 49:149-155.
46. Palma R.E., Polop J.J., Owen R.D., Mills J.N. Ecology of rodent-associated hantaviruses in the southern cone of South America: Argentina, Chile, Paraguay, and Uruguay. J. Wildl. Dis. 2012, 48:267-281.
47. Pereira C. Sobre as "ratadas" no Sul do Brasil e o ciclo vegetativo das taquaras. Arq. Inst. Biol. São Paulo 1941, 12:175-200.
48. Raboni S.M., Hoffmann F.G., Oliveira R.C., Teixeira B.R., Bonvicino C.R., Stella V., Carstensen S., Bordignon J., D'Andrea P.S., Lemos E.R.S., Nunes C. Phylogenetic characterization of hantaviruses from wild rodents and hantavirus pulmonary syndrome cases in the state of Paraná (southern Brazil). J. Gen. Virol. 2009, 90:2166-2171.
49. Raboni S.M., Probst C.M., Bordignon J., Zeferino A., dos Santos C.N.D. Hantaviruses in central South America: phylogenetic analysis of the S segment from HPS cases in Paraná, Brazil. J. Med. Virol. 2005, 76:553-562.
50. Rizzini C.T. Tratado de Fitogeografia do Brasil: Aspectos Ecológicos, Sociológicos e Florísticos 1997, Âmbito Cultural, Rio de Janeiro. 2nd ed.
51. Robinson J.G., Redford K.H. Body size, diet, and population density of neotropical forest mammals. Am. Nat. 1986, 128:665-680.
52. Rosa E.S.T., Mills J.N., Padula P.J., Elkhoury M.R., Ksiazek T.G., Mendes W.S., Santos E.D., Araújo G.C.B., Martinez V.P., Rosa J.F.S.T., Edelstein A., Vasconcelos P.F.C. Newly recognized hantaviruses associated with hantavirus pulmonary syndrome in northern Brazil: partial genetic characterization of viruses and serologic implication of likely reservoirs. Vector Borne Zoonotic Dis. 2005, 5:11-19.
53. Sage R.D., Pearson O.P., Sanguinetti J., Pearson A.K. Ratada 2001: a rodent outbreak following the flowering of bamboo (Chusquea culeou) in southern argentina. The Quintessential Naturalist: Honoring the Life and Legacy of Oliver P. Pearson 2007, 177-224. California Scholarship Online, Berkeley, Los Angeles, London. D. Kelt, L.P. Enrique, J. Salazar-Bravo, J.L. Patton (Eds.).
54. Sauvage F., Langlais M., Yoccoz N.G., Pontier D. Modelling hantavirus in fluctuating populations of bank voles: the role of indirect transmission on virus persistence. J. Anim. Ecol. 2003, 72:1-13.
55. Schmaljohn C., Hjelle B. Hantaviruses: a global disease problem. Emerg. Infect. Dis. 1997, 3:95-104.
56. Suárez O.V., Cueto G.R., Cavia R., Gómez Villafañe I.E., Bilenca D.N., Edelstein A., Martínez P., Miguel S., Bellomo C., Hodara K., Padula P.J., Busch M. Prevalence of infection with hantavirus in rodent populations of central Argentina. Mem. Inst. Oswaldo Cruz 2003, 98:727-732.
57. Suzán G., Marcé E., Giermakowski J.T., Mills J.N., Ceballos G., Ostfeld R.S., Armién B., Pascale J.M., Yates T.L. Experimental evidence for reduced rodent diversity causing increased hantavirus prevalence. PLoS ONE 2009, 4:e5461.
58. Suzuki A., Bisordi I., Levis S., Garcia J., Pereira L.E., Souza R.P., Sugahara T.K.N., Pini N., Enria D., Souza L.T.M. Identifying rodent hantavirus reservoirs, Brazil. Emerg. Infect. Dis. 2004, 10:2127-2134.
59. Tersago K., Verhagen R., Leirs H. Temporal variation in individual factors associated with hantavirus infection in bank voles during an epizootic: implications for Puumala virus transmission dynamics. Vector Borne Zoonotic Dis. (Larchmont, NY) 2011, 11:715-721.
60. Travassos da Rosa E.S., Medeiros D.B.A., Nunes M.R.T., Simith D.B., de Souza Pereira A., Elkhoury M.R., Lavocat M., Marques A.R.A., Via A.V., D'Andrea P., Bonvicino C.R., Lemos E.R.S., Vasconcelos P.F.C. Pygmy rice rat as potential host of castelo dos sonhos hantavirus. Emerg. Infect. Dis. 2011, 17:1527-1530.
61. Travassos Da Rosa E.S., Medeiros D.B.A., Nunes M.R.T., Simith D.B., Pereira A.D.S., Elkhoury M.R., Santos E.D., Lavocat M., Marques A.A., Via A.V.G., Kohl V.A., Terças A.C.P., D'Andrea P., Bonvícino C.R., Sampaio De Lemos E.R., Vasconcelos P.F.C. Molecular epidemiology of Laguna Negra virus, Mato Grosso State, Brazil. Emerg. Infect. Dis. 2012, 18:982-985.
62. Travassos da Rosa E.S., Sampaio de Lemos E.R., de Almeida Medeiros D.B., Simith D.B., de Souza Pereira A., Elkhoury M.R., Mendes W.S., Vidigal J.R.B., de Oliveira R.C., D'Andrea P.S., Bonvicino C.R., Cruz A.C.R., Nunes M.R.T., da Costa Vasconcelos P.F. Hantaviruses and hantavirus pulmonary syndrome, Maranhao, Brazil. Emerg. Infect. Dis. 2010, 16:1952-1955.
63. Vieira E.M., Paise G., Machado P.H.D. Feeding of small rodents on seeds and fruits: a comparative analysis of three species of rodents of the Araucaria forest, southern Brazil. Acta Theriol. (Warsz) 2006, 51:311-318.
64. Weksler M., Bonvicino C.R. Taxonomy of pigmy rice rats genus oligoryzomys bangs, 1900 (Rodentia, Sigmodontinae) of the Brazilian cerrado. Arq. Mus. Nac. 2005, 63:113-130.
65. Wolff J.O. Social behaviour. Advances in the Study of Peromyscus (Rodentia) 1989, 366. Texas Tech University Press, Lubbock. G.L.J. Kirkland, J.N. Layne (Eds.).
66. Yadav P.D., Vincent M.J., Nichol S.T. Thottapalayam virus is genetically distant to the rodent-borne hantaviruses, consistent with its isolation from the Asian house shrew (Suncus murinus). Virol. J. 2007, 4:80.
67. Yates T.L., Mills J.N., Parmenter C., Ksiazek a., Parmenter T.G., Vande Castle R.R., Calisher J.R., Nichol C.H., Abbott S.T., Young K.D., Morrison J.C., Beaty M.L., Dunnum B.J., Baker J.L., Salazar-Bravo R.J., Peters J.C.J. The ecology and evolutionary history of an emergent disease: hantavirus pulmonary syndrome. Bioscience 2002, 52:989.