Epidemiologia das encefalites por arbovírus na amazônia brasileira

Vasconcelos, Pedro Fernando da Costa; Travassos da Rosa, Jorge Fernando Soares; Travassos da Rosa, Amélia Paes de Andrade; Dégallier, Nicolas; Pinheiro, Francisco de Paula; Sá filho, Gregório Carrera

doi:10.1590/S0036-46651991000600007

Resumos

Os autores revêem os aspectos ecoepidemiológicos apresentados pelos virus da encefalite de St. Louis (SLE), encefalites equinas Leste (EEE), Oeste (WEE) e Venezuelana [subtipos III, Mucambo (MUC) e IV, Pixuna (PIX)], decorrentes dos estudos realizados em diversas áreas da Região Amazônica brasileira, especialmente ao longo das rodovias e projetos de desenvolvimento. Esses vírus são amplamente distribuídos na Amazônia e pelo menos quatro deles, EEE, WEE, MUC e SLE já demonstraram ser patógenos do homem. O diagnóstico da doença humana foi feito por sorologia, sendo que de MUC e SLE obteve-se também isolamento viral. O vírus PIX, parece ser o menos prevalente e foi isolado em poucas oportunidades. Virtualmente se desconhecem os vetores do PIX e WEE. As aves silvestres constituem os hospedeiros principais de todos esses vírus, exceto do MUC, para o qual constituem os roedores. O quadro clínico apresentado pelos pacientes infectados na Amazônia é discutido, comparando-o ao apresentado em outras áreas, especialmente nos EUA, onde periodicamente SLE, EEE e WEE causam surtos de doença humana. Nenhuma epidemia foi até o presente detectada, embora em 1960 uma epizootia em eqüinos causada pelo EEE tenha sido registrada em Bragança, Pará, onde em um rebanho de 500 animais ocorreu uma letalidade de 5%. Quatro outras pequenas epizootias determinadas pelo SLE ocorreram nas florestas adjacentes a Belém, envolvendo aves silvestres e animais sentinelas.

Encefalites; Arbovírus; Epidemiologia; Amazônia; Brasil

An overview of ecological, epidemiological and clinical findings of potential arthropod-borne encephalitis viruses circulating in the Amazon Region of Brazil are discussed. These viruses are the Eastern Equine Encephalitis (EEE), Western Equine Encephalitis (WEE), St. Louis Encephalitis (SLE), Mucambo (MUC) and Pixuna (PIX). These last two are subtypes (HI and IV) of Venezuelan Equine Encephalitis virus. The areas of study were the highways and projects of development, as well as places where outbreaks of human diseases caused by arboviruses had been detected. These viruses are widespread in all Amazonia, and at least four of them, EEE, WEE, SLE and MUC are pathogenic to man. EEE and WEE infections were detected by serology, while SLE and MUC by either serology and virus isolation. The PIX virus has the lowest prevalence and, it was isolated in only a few cases, one being from a laboratory infection. Wild birds are the main hosts for all these viruses, except MUC, whose major hosts are rodents. The symptoms presented by infected people were generally a mild febrile illness. Although, jaundice was observed in two individuals from whom SLE was isolated. A comparison of the clinical symptoms presented by the patients in the Amazon Region and other areas of America, especially in the USA is made. In Brazilian Amazon region epidemics have not been detected although, at least, one EEE epizootic was recorded in Bragança, Para State, in 1960. At that time, of 500 horses that were examined 61% were positive to EEE by HI and of mem 8.2% died On the other hand. SLE has caused four epizootics in a forest near Belem. Wild birds and sentinel monkeys were infected, but no human cases were reported.

EPIDEOMOLOGIA

Epidemiologia das encefalites por arbovírus na amazônia brasileira

Epidemiology of encephalitis by arboviruses in the Amazon region of Brazil

Pedro Fernando da Costa Vasconcelos^I; Jorge Fernando Soares Travassos da Rosa^I;Amélia Paes de Andrade Travassos da Rosa^I; Nicolas Dégallier^II; Francisco de Paula Ponheiro^III; Gregório Carrera Sá filho^I

^IInstituto Evandro Chagas, Laboratório de Arbovírus, Centro Colaborador da OMS em Arboviroses - Fundação SESP. Av. Almirante Barroso, 492. Caixa Postal 1128. CEP 66065 Belém, Pará, Brasil

^IIInstituto Evandro Chagas (Convênio FSESP/CNPq/ORSTOM)

^IIIPAHO/WHO, 525 Twenty-third St., Washington DC 20037, USA

RESUMO

Os autores revêem os aspectos ecoepidemiológicos apresentados pelos virus da encefalite de St. Louis (SLE), encefalites equinas Leste (EEE), Oeste (WEE) e Venezuelana [subtipos III, Mucambo (MUC) e IV, Pixuna (PIX)], decorrentes dos estudos realizados em diversas áreas da Região Amazônica brasileira, especialmente ao longo das rodovias e projetos de desenvolvimento. Esses vírus são amplamente distribuídos na Amazônia e pelo menos quatro deles, EEE, WEE, MUC e SLE já demonstraram ser patógenos do homem. O diagnóstico da doença humana foi feito por sorologia, sendo que de MUC e SLE obteve-se também isolamento viral. O vírus PIX, parece ser o menos prevalente e foi isolado em poucas oportunidades. Virtualmente se desconhecem os vetores do PIX e WEE. As aves silvestres constituem os hospedeiros principais de todos esses vírus, exceto do MUC, para o qual constituem os roedores.

O quadro clínico apresentado pelos pacientes infectados na Amazônia é discutido, comparando-o ao apresentado em outras áreas, especialmente nos EUA, onde periodicamente SLE, EEE e WEE causam surtos de doença humana. Nenhuma epidemia foi até o presente detectada, embora em 1960 uma epizootia em eqüinos causada pelo EEE tenha sido registrada em Bragança, Pará, onde em um rebanho de 500 animais ocorreu uma letalidade de 5%. Quatro outras pequenas epizootias determinadas pelo SLE ocorreram nas florestas adjacentes a Belém, envolvendo aves silvestres e animais sentinelas.

Unitermos: Encefalites; Arbovírus; Epidemiologia; Amazônia; Brasil.

SUMMARY

An overview of ecological, epidemiological and clinical findings of potential arthropod-borne encephalitis viruses circulating in the Amazon Region of Brazil are discussed. These viruses are the Eastern Equine Encephalitis (EEE), Western Equine Encephalitis (WEE), St. Louis Encephalitis (SLE), Mucambo (MUC) and Pixuna (PIX). These last two are subtypes (HI and IV) of Venezuelan Equine Encephalitis virus.

The areas of study were the highways and projects of development, as well as places where outbreaks of human diseases caused by arboviruses had been detected. These viruses are widespread in all Amazonia, and at least four of them, EEE, WEE, SLE and MUC are pathogenic to man. EEE and WEE infections were detected by serology, while SLE and MUC by either serology and virus isolation. The PIX virus has the lowest prevalence and, it was isolated in only a few cases, one being from a laboratory infection. Wild birds are the main hosts for all these viruses, except MUC, whose major hosts are rodents.

The symptoms presented by infected people were generally a mild febrile illness. Although, jaundice was observed in two individuals from whom SLE was isolated. A comparison of the clinical symptoms presented by the patients in the Amazon Region and other areas of America, especially in the USA is made.

In Brazilian Amazon region epidemics have not been detected although, at least, one EEE epizootic was recorded in Bragança, Para State, in 1960. At that time, of 500 horses that were examined 61% were positive to EEE by HI and of mem 8.2% died On the other hand. SLE has caused four epizootics in a forest near Belem. Wild birds and sentinel monkeys were infected, but no human cases were reported.

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Recebido para publicação em 21/01/1991.

Aceito para publicação em 03/10/1991.

1. ALICE, F.J. - Infecçăo humana pelo vírus leste de encefalite eqüina. Bol. Inst. Biol. Bahia, 3: 3-9, 1956.
2. CALISHER, C.H.; KINNEY, R.M.; LOPES, O.S.; TRENT, D.W.; MONATH, T.P. & FANCY, D.B. - Identification of a new Venezuelan equine encephalitis virus from Brazil. Amer. J. trop. Med. Hyg., 31: 1260-1272, 1982.
3. CALISHER, C.H.; MONATH, T.P.; MITCHEL, C.J.; SABATTINI, M.S.; CROPP, C.B.; KERSCHNER, J.; HUNT, A.R. & LAZUICK, J.S. - Arbovirus investigations in Argentina, 1977-1980. III. Identification and caracterization of viruses isolated, including new subtypes of western and Venezuelan equine encephalitis viruses and four new Bunyaviruses (Las Maloyas, Resistencia, Barranqueras and Antequera). Amer. J. trop. Med. Hyg., 34: 956-965, 1985.
4. CASALS, J. - Antigenic variants of eastern equine encephalitis virus. J. exp. Med., 119: 229-232, 1964.
5. CASALS, J. - The arthropod-borne groups of animal viruses. Trans. N.Y. Acad. Sci., 19: 219-235, 1959.
6. CAUSEY, O.R.; CAUSEY, C.E.; MAROJA, O.M. & MACEDO, D.G. - The isolation of arthropod-borne viruses, including members of two hitherto undescribed serological groups in the Amazon Region of Brazil. Amer. J. trop. Med. Hyg., 10: 227-249, 1961.
7. CAUSEY, O.R.; SHOPE, R.E.; SUTMOLLER, P. & LAEMMERT, H. - Epizootic eastern equine encephalitis in the Bragança Region of Pará, Brazil. Rev. serv. esp. Saúde públ., 12 (1): 39-45,1962.
8. CAUSEY, O.R. & THEILER, M. - Virus antibody on sera of residents of the Amazon Valley in Brazil. Amer. J. trop. Med. Hyg., 7: 36-41, 1958.
9. DIXON, K.E.; LLEWELLYN, C.H.; TRAVASSOS DA ROSA, A.P.A. & TRAVASSOS DA ROSA, J.F.S. - Programa multidisciplinário de vigilância de las enfermedades infecciosas con la carretera Transamazonica en Brasil. II. Epdemiologia de las infecciones por arbovirus. Bol. Ofic. sanit. panamer., 91: 200-218, 1981.
10. FLOCH, H.; BOULAN, S. & BARRAT, R. - Encéphalomyélite ŕ virus de Saint-Louis en Guyane Française. Arch. Inst. Pasteur Guyane franç., 18 (431): 1-5, 1957.
11. FULTON, F. & DUMBELL, K.R. - The serological comparison of strains of influenza virus. J. gen. Microbiol., 3: 97-111, 1949.
12. HERVÉ, J.P.; DÉGALLIER, N.; TRAVASSOS DA ROSA, A.P.A.; PINHEIRO, F.P. & SÁ FILHO, G.L. - Arboviroses, aspectos ecológicos. In: Instituto Evandro Chagas 50 anos de contribuiçăo ŕs cięncias biológicas e ŕ medicina tropical. Belém, Fundaçăo Serviços de Saúde Pública, 1986. V. 1, p. 409-437.
13. IVERSSON, L.B.; TRAVASSOS DA ROSA, A.P.A.; TRAVASSOS DA ROSA, J.F.S.; PINTO, G.H. & MACEDO, O. - Estudos sorológicos para pesquisa de anticorpos de arbovírus em populaçăo humana da regiăo do Vale do Ribeira. IV. Inquérito em escolares residentes no município de Iguape, SP (Brasil). Rev. Saúde públ. S. Paulo, 17: 423-425, 1983.
14. IVERSSON, L.B.; TRAVASSOS DA ROSA, A.P.A.; RODRIGUES, S.G. & ROSA, M.D.B. - Human disease caused by Venezuelan equine encephalitis subtype IF in Ribeira Valley, Săo Paulo, Brazil. In: Annual meeting of the american society of tropical medicine and hygiene, 39., New Orleans, 1990. Abstract. p. 143.
15. JONKERS, A.H.; DOWNS, W.G.; SPENCE, L. & AITKEN, T.H.G. - Arthropod borne encephalitis viruses in Northern South America. II. Amer. J. trop. Med. Hyg., 14: 304-308, 1965.
16. KARABATSOS, N., ed. - International catalogue of arboviruses and certain other viruses of vertebrates. 3rd. ed. San Antonio, USA, The American Society of Tropical Medicine and Hygiene, 1985.
17. LENNETTE, E.H. - Serologic reactions in viral and rickettsial infections. In: RIVERS, T.M. & HORSFALL, F.L., ed. Viral and rickettsial infections of man. 3rd. ed. Philadelphia, Lippincott 1959. p. 230-250.
18. LOPES, O.S. - Rocio (ROC) strain: SP H 34675. Amer. J. trop. Med. Hyg., 27: 418-419, 1978.
19. LOPES, O.S.; SACCHETTA, L.A.; COIMBRA, T.L.M. & PEREIRA, L.E. - St. Louis encephalitis virus in South Brazil. Amer. J. trop. Med. Hyg., 28: 583-585, 1979.
20. LUBY, J.P. - St. Louis Encephalitis. Epidem. Rev., 1: 55-73, 1979.
21. McLEAN, D.M. - North American equine encephalitis. In: RHODES, A.J. & VAN ROOYEN, C.E., ed. Textbook of virology. 3 rd. ed. Baltimore, The Williams and Wilkins, 1962. p. 300-307.
22. METHLER, N.E. & CASALS, J. - Isolation of St. Louis encephalitis virus from man in Argentina. Acta virol., 15: 148-154, 1971.
23. MITCHELL, C.J.; MONATH, T.P.; SABATTINI, M.S.; DAFFNER, J.F.; CROPP, C.B.; CALISHER, C.H.; DARSIE, R.F. & JAKOB, W.L. - Arbovirus isolations from mosquitoes collected during and after the 1982-1983 epizootic of western equine encephalitis in Argentina. Amer. J. trop. Med. Hyg., 36: 107-113, 1987.
24. OLITSKY, P.K. & CASALS, J. - Arthropod-borne group A virus infections of man. In: RIVERS, T.M. & HORSFALL, F.L., ed. - Viral and rickettsial infections of man. 3rd. ed. Philadelphia, Lippincott, 1959. p. 286-304.
25. PINHEIRO, F.P.; LeDUC, J.W.; TRAVASSOS DA ROSA & LEITE, O.F. - Isolation of St. Louis encephalitis virus from a patient in Belém, Brazil. Amer. J. trop. Med. Hyg., 30: 145-148, 1981.
26. PINHEIRO, F.P.; TRAVASSOS DA ROSA, A.P.A.; FREITAS, R.B.; TRAVASSOS DA ROSA, J.F.S. & VASCONCELOS, P.F.C. - Arboviroses, aspectos clínico-epidemiológicos. In: Instituto Evandro Chagas: 50 anos de contribuiçőes ŕs ciencias biológicas e ŕ medicina tropical. Belém, Fundaçăo Serviços de Saúde Pública, 1986. v. 1, p. 375-408.
27. SERIE, C.; FAURAN, P. & PILO-MORON, P. - Présence de L'encéphalite de Saint-Louis en Guyane Française. Méd. Mal. infect., 3: 7-9, 1973.
28. SANMARTIN, C.; MACKENZIE, R.B.; TRAPIDO, H.; BARRETO, R.; MULLANAX, C.H.; GUTIERREZ, E. & LESMES, C. - Encephalitis equina venezolana en Colombia. Bol. Ofic. sanit. panamer., 74: 108-137, 1973.
29. SEYMOUR, C.; DICKERMAN, R.W. & MARTIN, M.S. - Venezuela equine encephalitis virus infection in neotropical bats. I. Natural infection in a Guatemalan enzootic focus. Amer. J. trop. Med. Hyg., 27: 290-296, 1978.
30. SEYMOUR, C.; DICKERMAN, R.W. & MARTIN, M.S. - Venezuela equine encephalitis virus infection in neotropical bats. II. Experimental infections. Amer. J. trop. Med. Hyg., 27: 297-306, 1978.
31. SEYMOUR, C. & DICKERMAN, R.W. - Venezuela equine encephalitis virus infection in neotropical bats. III. Experimental studies on virus excretion and non-arthropod transmission. Amer. J. trop. Med. Hyg., 27: 307-312, 1978.
32. SHOPE, R.E. - The use of a micro-hemagglutination inhibition test to follow antibody response after arthropod-borne virus infection in a community of forest animals. An. Microbiol. Rio de J., 11: 167-171, 1963.
33. SHOPE, R.E.; ANDRADE, A.H.P.; BENSABATH, G.; CAUSEY, O.R. & HUMPHREY, P.S. - The epidemiology of EEE, WEE, SLE and Turlock viruses, with special reference to birds in a tropical rain forest near Belém, Brazil. Amer. J. Epidem., 84: 467-477, 1966.
34. SHOPE, R.E.; CAUSEY, O.R.; ANDRADE, A.H.P. & THEILER, M. - The Venezuelan equine encephalitis complex of group A arthropod-borne viruses, including Mucambo and Pixuna from the Amazon Region of Brazil. Amer. J. trop. Med. Hyg., 13: 723-727, 1964.
35. SHOPE, R.E. & SATHER, G.E. - Arboviruses. In: LENNETTE, E.H. & SCHMIDT, N.J. ed. Diagnostic procedures for viral, rickettsial and chlamidial infections. 5th. ed. Washington, American Public Health Association, 1979. p. 767-814.
36. SUDIA, W.D. & NEWHOUSE, V.F. - Epidemic Venezuelan equine encephalitis in North America: a summary of virus-vector-host relationships. Amer. J. Epidem., 101: 1-13, 1975.
37. THEILER, M. & DOWNS, W.G. - The arthropod-borne viruses of vertebrates. New Haven, Yale University Press, 1973.
38. TRAVASSOS DA ROSA, J.F.S.; FREITAS, E.N.; TRAVASSOS DA ROSA, A.P.A. & PINHEIRO, F.P. - Epidemiologia do virus da encefalite de S. Louis na Amazonia. In: Simpósio Internacional sobre Arbovírus e Febres Hemorrágicas. Belém, 1981. Anais. Rio de Janeiro, Academia Brasileira de Cięncias, 1982. p. 375-383.
39. TRENT, D.W.; CLEWLEY, J.P.; FRANCE, J.K. & BISHOP, D.H.L. - Immunochemical and oligonucleotide fingerprint analyses of Venezuelan equine encephalitis complex viruses. J. gen. Virol., 43: 365-381, 1979.

Datas de Publicação

Publicação nesta coleção
11 Set 2006
Data do Fascículo
Dez 1991

Histórico

Aceito
03 Out 1991
Recebido
21 Jan 1991

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

[1] 1. ALICE, F.J. - Infecçăo humana pelo vírus leste de encefalite eqüina. Bol. Inst. Biol. Bahia, 3: 3-9, 1956.

[2] 2. CALISHER, C.H.; KINNEY, R.M.; LOPES, O.S.; TRENT, D.W.; MONATH, T.P. & FANCY, D.B. - Identification of a new Venezuelan equine encephalitis virus from Brazil. Amer. J. trop. Med. Hyg., 31: 1260-1272, 1982.

[3] 3. CALISHER, C.H.; MONATH, T.P.; MITCHEL, C.J.; SABATTINI, M.S.; CROPP, C.B.; KERSCHNER, J.; HUNT, A.R. & LAZUICK, J.S. - Arbovirus investigations in Argentina, 1977-1980. III. Identification and caracterization of viruses isolated, including new subtypes of western and Venezuelan equine encephalitis viruses and four new Bunyaviruses (Las Maloyas, Resistencia, Barranqueras and Antequera). Amer. J. trop. Med. Hyg., 34: 956-965, 1985.

[4] 4. CASALS, J. - Antigenic variants of eastern equine encephalitis virus. J. exp. Med., 119: 229-232, 1964.

[5] 5. CASALS, J. - The arthropod-borne groups of animal viruses. Trans. N.Y. Acad. Sci., 19: 219-235, 1959.

[6] 6. CAUSEY, O.R.; CAUSEY, C.E.; MAROJA, O.M. & MACEDO, D.G. - The isolation of arthropod-borne viruses, including members of two hitherto undescribed serological groups in the Amazon Region of Brazil. Amer. J. trop. Med. Hyg., 10: 227-249, 1961.

[7] 7. CAUSEY, O.R.; SHOPE, R.E.; SUTMOLLER, P. & LAEMMERT, H. - Epizootic eastern equine encephalitis in the Bragança Region of Pará, Brazil. Rev. serv. esp. Saúde públ., 12 (1): 39-45,1962.

[8] 8. CAUSEY, O.R. & THEILER, M. - Virus antibody on sera of residents of the Amazon Valley in Brazil. Amer. J. trop. Med. Hyg., 7: 36-41, 1958.

[9] 9. DIXON, K.E.; LLEWELLYN, C.H.; TRAVASSOS DA ROSA, A.P.A. & TRAVASSOS DA ROSA, J.F.S. - Programa multidisciplinário de vigilância de las enfermedades infecciosas con la carretera Transamazonica en Brasil. II. Epdemiologia de las infecciones por arbovirus. Bol. Ofic. sanit. panamer., 91: 200-218, 1981.

[10] 10. FLOCH, H.; BOULAN, S. & BARRAT, R. - Encéphalomyélite ŕ virus de Saint-Louis en Guyane Française. Arch. Inst. Pasteur Guyane franç., 18 (431): 1-5, 1957.

[11] 11. FULTON, F. & DUMBELL, K.R. - The serological comparison of strains of influenza virus. J. gen. Microbiol., 3: 97-111, 1949.

[12] 12. HERVÉ, J.P.; DÉGALLIER, N.; TRAVASSOS DA ROSA, A.P.A.; PINHEIRO, F.P. & SÁ FILHO, G.L. - Arboviroses, aspectos ecológicos. In: Instituto Evandro Chagas 50 anos de contribuiçăo ŕs cięncias biológicas e ŕ medicina tropical. Belém, Fundaçăo Serviços de Saúde Pública, 1986. V. 1, p. 409-437.

[13] 13. IVERSSON, L.B.; TRAVASSOS DA ROSA, A.P.A.; TRAVASSOS DA ROSA, J.F.S.; PINTO, G.H. & MACEDO, O. - Estudos sorológicos para pesquisa de anticorpos de arbovírus em populaçăo humana da regiăo do Vale do Ribeira. IV. Inquérito em escolares residentes no município de Iguape, SP (Brasil). Rev. Saúde públ. S. Paulo, 17: 423-425, 1983.

[14] 14. IVERSSON, L.B.; TRAVASSOS DA ROSA, A.P.A.; RODRIGUES, S.G. & ROSA, M.D.B. - Human disease caused by Venezuelan equine encephalitis subtype IF in Ribeira Valley, Săo Paulo, Brazil. In: Annual meeting of the american society of tropical medicine and hygiene, 39., New Orleans, 1990. Abstract. p. 143.

[15] 15. JONKERS, A.H.; DOWNS, W.G.; SPENCE, L. & AITKEN, T.H.G. - Arthropod borne encephalitis viruses in Northern South America. II. Amer. J. trop. Med. Hyg., 14: 304-308, 1965.

[16] 16. KARABATSOS, N., ed. - International catalogue of arboviruses and certain other viruses of vertebrates. 3rd. ed. San Antonio, USA, The American Society of Tropical Medicine and Hygiene, 1985.

[17] 17. LENNETTE, E.H. - Serologic reactions in viral and rickettsial infections. In: RIVERS, T.M. & HORSFALL, F.L., ed. Viral and rickettsial infections of man. 3rd. ed. Philadelphia, Lippincott 1959. p. 230-250.

[18] 18. LOPES, O.S. - Rocio (ROC) strain: SP H 34675. Amer. J. trop. Med. Hyg., 27: 418-419, 1978.

[19] 19. LOPES, O.S.; SACCHETTA, L.A.; COIMBRA, T.L.M. & PEREIRA, L.E. - St. Louis encephalitis virus in South Brazil. Amer. J. trop. Med. Hyg., 28: 583-585, 1979.

[20] 20. LUBY, J.P. - St. Louis Encephalitis. Epidem. Rev., 1: 55-73, 1979.

[21] 21. McLEAN, D.M. - North American equine encephalitis. In: RHODES, A.J. & VAN ROOYEN, C.E., ed. Textbook of virology. 3 rd. ed. Baltimore, The Williams and Wilkins, 1962. p. 300-307.

[22] 22. METHLER, N.E. & CASALS, J. - Isolation of St. Louis encephalitis virus from man in Argentina. Acta virol., 15: 148-154, 1971.

[23] 23. MITCHELL, C.J.; MONATH, T.P.; SABATTINI, M.S.; DAFFNER, J.F.; CROPP, C.B.; CALISHER, C.H.; DARSIE, R.F. & JAKOB, W.L. - Arbovirus isolations from mosquitoes collected during and after the 1982-1983 epizootic of western equine encephalitis in Argentina. Amer. J. trop. Med. Hyg., 36: 107-113, 1987.

[24] 24. OLITSKY, P.K. & CASALS, J. - Arthropod-borne group A virus infections of man. In: RIVERS, T.M. & HORSFALL, F.L., ed. - Viral and rickettsial infections of man. 3rd. ed. Philadelphia, Lippincott, 1959. p. 286-304.

[25] 25. PINHEIRO, F.P.; LeDUC, J.W.; TRAVASSOS DA ROSA & LEITE, O.F. - Isolation of St. Louis encephalitis virus from a patient in Belém, Brazil. Amer. J. trop. Med. Hyg., 30: 145-148, 1981.

[26] 26. PINHEIRO, F.P.; TRAVASSOS DA ROSA, A.P.A.; FREITAS, R.B.; TRAVASSOS DA ROSA, J.F.S. & VASCONCELOS, P.F.C. - Arboviroses, aspectos clínico-epidemiológicos. In: Instituto Evandro Chagas: 50 anos de contribuiçőes ŕs ciencias biológicas e ŕ medicina tropical. Belém, Fundaçăo Serviços de Saúde Pública, 1986. v. 1, p. 375-408.

[27] 27. SERIE, C.; FAURAN, P. & PILO-MORON, P. - Présence de L'encéphalite de Saint-Louis en Guyane Française. Méd. Mal. infect., 3: 7-9, 1973.

[28] 28. SANMARTIN, C.; MACKENZIE, R.B.; TRAPIDO, H.; BARRETO, R.; MULLANAX, C.H.; GUTIERREZ, E. & LESMES, C. - Encephalitis equina venezolana en Colombia. Bol. Ofic. sanit. panamer., 74: 108-137, 1973.

[29] 29. SEYMOUR, C.; DICKERMAN, R.W. & MARTIN, M.S. - Venezuela equine encephalitis virus infection in neotropical bats. I. Natural infection in a Guatemalan enzootic focus. Amer. J. trop. Med. Hyg., 27: 290-296, 1978.

[30] 30. SEYMOUR, C.; DICKERMAN, R.W. & MARTIN, M.S. - Venezuela equine encephalitis virus infection in neotropical bats. II. Experimental infections. Amer. J. trop. Med. Hyg., 27: 297-306, 1978.

[31] 31. SEYMOUR, C. & DICKERMAN, R.W. - Venezuela equine encephalitis virus infection in neotropical bats. III. Experimental studies on virus excretion and non-arthropod transmission. Amer. J. trop. Med. Hyg., 27: 307-312, 1978.

[32] 32. SHOPE, R.E. - The use of a micro-hemagglutination inhibition test to follow antibody response after arthropod-borne virus infection in a community of forest animals. An. Microbiol. Rio de J., 11: 167-171, 1963.

[33] 33. SHOPE, R.E.; ANDRADE, A.H.P.; BENSABATH, G.; CAUSEY, O.R. & HUMPHREY, P.S. - The epidemiology of EEE, WEE, SLE and Turlock viruses, with special reference to birds in a tropical rain forest near Belém, Brazil. Amer. J. Epidem., 84: 467-477, 1966.

[34] 34. SHOPE, R.E.; CAUSEY, O.R.; ANDRADE, A.H.P. & THEILER, M. - The Venezuelan equine encephalitis complex of group A arthropod-borne viruses, including Mucambo and Pixuna from the Amazon Region of Brazil. Amer. J. trop. Med. Hyg., 13: 723-727, 1964.

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