Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-29T20:42:03.077Z Has data issue: false hasContentIssue false
  • English
  • Français

American leishmaniasis epidemiology in Brazil

Published online by Cambridge University Press:  19 September 2011

Almério de Castro Gomes
Almério de Castro Gomes
Affiliation:
Faculdade de Saúde Pública, Universidade de São Paulo, Av. Dr Arnaldo, 715, 01255-São Paulo/SP, Brazil
Get access

Abstract

We have tried to demonstrate in this paper that visceral and cutaneous leishmaniasis are a great public health problem in Brazil. In relation to visceral leishmaniasis, the recognition of new foci denotes the increasing spread of endemic areas, but the areas of highest importance are located mainly at the northeastern region. It calls attention to its suburban character in cities like São Luis, Teresina and Rio de Janeiro. L. longipalpis is the only vector known for the disease in domiciliary environment. The dog constitutes the main source for L.d. chagasi, while canids such as Dusicyon vetulus and Cerdocyon thous have epidemiological roles. Other vectors for this parasite remain yet as unknown in the enzootic and sylvatic cycles.

Cutaneous leishmaniasis have a distribution in almost all the States of Brazil and, at least, two epidemiological patterns exist. The first, corresponds to the classic form of man entering in contact with the agent in virgin forests, like the Amazonian forest and so, there is a permanent risk for epidemics. The second, refers to the occurrence of this disease in areas after forest devastation as in the State of São Paulo and in other southeastern States. There are three nosological entities for the cutaneous leishmaniasis in Brazil, their agents being L.m. amazonensis, L. guyanensis and L.b. braziliensis. Five sandfly species have been incriminated as the main vectors in the transmission of the disease in different localities. They are P. flaviscutellatus, P. umbratilis, P. welcomei, P. whitmani and P. intermedius. As for the main natural reservoir of cutaneous leishmaniasis, it remains unknown the one relative to L.b. braziliensis.

Résumé

Au cours de nos travaux sur la leishmaniose viscérale et cutanée, il devient évident qu'elles réprésentent un grand problème de santé publique au Brésil nonobstant que se vraie prévalence soit encore ignorée.

En ce qui concerne à la leishmaniose viscérale, la découverte de nouveaux foyers dénote l'acroissement de la distributions des surfaces endémiques. Cependant, les plus considérables se trouvent, surtout, à la région nord-est. On signe aussi le caractère suburbain de cette maladie aux villes de São Luiz, Teresina et Rio de Janeiro. La Lutzomyia longipalpis est l'unique vecteur connu de cette maladie avec un habitat domiciliaire. Le chien rèste le principal réservoir de la Leishmania donovani chagasi mais d'autres espèces de canin, tels que le Dusicyon vetulus et le Cerdocyon thous ont un rôle epidémiologique secondaire. Au cycle biologique sylvestre, les vecteurs restent encore inconnus.

Les leishmanioses cutanées sont répandues par presque tous les états brésilens et ainsi donc, deux patrons épidémiologiques de la maladie ont été classifiés: le premier, fait rapport à la forme classique par laquelle l'home peut l'acquerir, c'est-à-dire, au contact avec l'agent, à l'Amazonie, ayant comme résultat um risque permanent d'epidémie. Le deuxiène fait égard à l'occurrence de la maladie aux régions de forêts entièrment dévastées aux États de São Paulo et d'autres de la région sud-est du pays.

On trouve au Brésil trois catégories nosologiques de la leishmaniose cutanée ayant par agents la Leishmania mexicana amazonensis, la Leishmania braziliensis guyanensis et la Leishmania braziliensis braziliensis. Cinq espèces de phlébotomes s'engagent comme vecteurs principaux en certaines régions: le Psychodopygus flaviscutellatus, le Psychodopygus umbratilis, le Psychodopygus wellcomei, le Psychodopygus whitmani et le Psychodopygus intermedius.

En ce qui concerne aux principaux réservoir de cer maladies il n'a que la L.b. braziliensis qui reste ignorée.

Keywords

Leishmaniasis ecologyepidemiologyPhlebotominaeLeishmaniavector speciesreservoir animal
Type
Special Section: Leishmaniasis Epidemiology
Information
International Journal of Tropical Insect Science , Volume 7 , Issue 2 , April 1986 , pp. 161 - 169
Copyright
Copyright © ICIPE 1986

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Amato-Neto, V. and Blanco Filho, F. (1981) Leishmaniose visceral adquirida no Estado de Sào Paulo (Brasil). Rev. Saude publ. 15, 643–645.CrossRefGoogle Scholar
Anderson, D. C., Buckner, R. G., Glenn, R. L. and MacVean, D. W. (1980) Endemic canine leishmaniasis. Vet. Path. 17, 94–96.CrossRefGoogle ScholarPubMed
Araujo Filho, N. A. (1978) Epidemiologia da leishmaniose tegumentar americana na Ilha Grande. Rio de Janeiro. Dissertaçào de Mestrado Universidade Federal do Rio de Janeiro.Google Scholar
Arias, J. R. and Freitas, R. A. (1978) Sobre os vetores de leishmaniose cutânea na Amazônia Central do Brasil. 2—Incidència de flagelados em flebotomos selvâticos. Acta Amazon. 8, 387–396.CrossRefGoogle Scholar
Arias, J. R. and Naiff, R. D. (1981a) The opossum, Didelphis marsupialis (Marsupialis: didelphidae) as a reservoir host of Leishmania braziliensis guyanensis in the Amazon Basin of Brazil. Trans. R. Soc. trop. Med. Hyg. 75, 537–541.CrossRefGoogle ScholarPubMed
Arias, J. R. and Naiff, R. D. (1981b) The principal reservoir host of cutaneous leishmaniasis in the urban area of Manaus, Central Amazon, Brasil. Mem. Inst. Oswaldo Cruz 76, 279–286.CrossRefGoogle Scholar
Barreto, A. C., Cuba Cuba, C., Vexenat, J. A., Rosa, A. C., Marsden, P. D. and Magalhāes, A. V. (1984) Caracteristicas epidemiologicas da Leishmaniose Tegumentar Americana em uma regiāo endêmica do Estado da Bahia II. Leishmaniose canina. Rev. Soc. bras. Med. trop. 17, 59–65.CrossRefGoogle Scholar
Barretto, M. P. (1943) Observaçôes sobre a Biologia, em condiçôes naturais, dos flebotomos do Estado de Sào Paulo, Sào Paulo. These de Livre-Docência, Faculdade de Medicina da USP.Google Scholar
Bray, R. S. (1982) The zoonotic potential of reservoir of Leishmaniosis in the Old World. Ecol. Dis. 1, 257–267.Google ScholarPubMed
Castro, J. A. F., Vale, M. A., Pereira, H. F., Figueredo, P. Z. and Siqueira Filho, J. B. (1983) Calazar humano: Surto epidêmico no Municipio de Teresina, Estado do Piaui. In: Congresso da Federacion Latinoamericana de Parasitologos, p. 155. Resumos, Sao Paulo, Brasil.Google Scholar
Chance, M. L. (1979) The identification of Leishmania. Symp. Br. Soc. Parasit. 17, 55–74.Google Scholar
Coutinho, S. G., Nunes, M. P., Marzochi, M. C. A. and Tramontano, N. C. (1985) A survey for American cutaneous and visceral leishmaniasis among 1,342 dogs from areas in Rio de Janeiro (Brazil) where the human disease occur. Mem. Inst. Oswaldo Cruz 80, 17–22.CrossRefGoogle Scholar
Christensen, H. A., Arias, J. R., Vasquez, A. M. and Freitas, R. A. (1982) Hosts of sandfly vectors of Leishmania brasiliensis guyanensis in the Central Amazon of Brasil. Am. J. trop. Med. Hyg. 31, 239–242.CrossRefGoogle Scholar
Cuba Cuba, C. A., Barreto, A. C. and Marsden, P. D. (1984) Leishmania mexicana: aspectos taxonômicos y rareza de la infection humann en Très Braços, Bahia, Brasil. Rev. Soc. bras. Med. trop. 17, 115–122.CrossRefGoogle Scholar
Deane, L. M. (1956) Leishmaniose Visceral no Brasil. Estudos Sobre Reservatorio e Transmissores Realizados no Estado do Ceara. Rio de Janeiro, Serviço Nacional de Educaçào Sanitaria.Google Scholar
Deane, L. M. and Deane, M. P. (1954) Encontro de Leishraanias nas visceras e na pele de uma raposa em zona endêmica de calazar, nos arredores de Sobral, Ceará. Hospital, Rio de Janeiro 45, 419–121.Google ScholarPubMed
Deane, M. P. and Deane, L. M. (1955) Observaçōes sobre a transmissào da leishmaniose visceral no Cearā. Hospital, Rio de Janeiro 48, 344–364.Google Scholar
Forattini, O. P. (1960) Sobre os réservatorios naturais de leishmaniose tegumentar americana. Rev. Inst. Med. trop. Sāo Paulo 2, 195–203.Google Scholar
Forattini, O. P. (1973) Entomologia Médica, Vol. 4. Blucher, Sāo Paulo.Google Scholar
Forattini, O. P. (1980) Biogeografia, origem e distribuiçào da domiciliaçào de triatomineos no Brasil. Rev. Saude publ., Sāo Paulo 14, 265–299.CrossRefGoogle Scholar
Forattini, O. P., Pattoli, D. B. G., Rabello, E. X. and Ferreira, O. A. (1972a) Infecçôes naturais de mamiferos silvestres em area endêmica de leishmaniose tegumentar do Estado de Sāo Paulo, Brasil. Rev. Saude publ., Sāo Paulo 6, 255–256.CrossRefGoogle Scholar
Forattini, O. P., Pattoli, D. B. G., Rabello, E. X. and Ferreira, O. A. (1972b) Infecçāo natural de flebotomineos em foco enzootico de leishmaniose tegumentar no Estado de Sāo Paulo, Brasil. Rev. Saude publ., Sāo Paulo 6, 431–33.CrossRefGoogle Scholar
Forattini, O. P., Pattoli, D. B. G., Rabello, E. X. and Ferreira, O. A. (1973) Nota sobre infecçāo natural de Oryzomys capito laticeps em foco enzotico de leishmaniose tegumentar no Estado de Sāo Paulo. Rev. Saúde públ., Sāo Paulo 7, 181–184.CrossRefGoogle ScholarPubMed
Forattini, O. P., Rabello, E. X., Serra, O. P., Cotrim, M. D., Galati, E. A. B. and Barata, J. M. S. (1976) Observaçōes sobre a transmisSāo da leishmaniose tegumentar no Estado de Sāo Paulo, Brasil. Rev. Saude publ., Sāo Paulo 10, 31–43.CrossRefGoogle Scholar
Gardener, P. J. (1977) Taxonomy of the Genus Leishmania: a review of Nomenclature and Classification. Trop. Dis. Bull. 74, 1069–1088.Google Scholar
Gomes, A. C. de (1985) Aspectos epidemiolôgicos sobre a transmisSāo da Leishmaniose tegumentar na regiāo do Vale do Ribeira, Estado de Sāo Paulo, Brasil. Sāo Paulo These de Livre-Docência, Faculdade de Saude Publica da USP.Google Scholar
Gomes, A. C. de, Rabello, E. X., Santos, J. L. F. and Galati, E. A. B. (1980) Aspectos ecologicos da leishmaniose tegumentar americana. 1—Estudo experimental da frequência de flebotomineos em biotopos artificials, com referenda especial a Psychodopygus intermedius. Rev. Saude publ, Sāo Paulo 14, 540–556.CrossRefGoogle Scholar
Gomes, A. C. de, Rabello, E. X., Santos, J. L. F. and Galati, E. A. B. (1982) Aspectos ecológicos da leishmaniose tegumentar americana. 2—Ecotopo artificial como abrigo de Psychodopygus intermedius e observaçōes sobre alimentaçāo de reproduçāo sob influência de fatores físicos naturais. Rev. Saúde públ., Sāo Paulo 10, 149–159.CrossRefGoogle Scholar
Gomes, A. C. de, Rabello, E. X., Santos, J. L. F. and Galati, E. A. B. (1983) Aspectos ecologicos da leishmaniose tegumentar americana. 3—Observaçōes naturais sobre o ritmo diá;rio da atividade de Psychodopygus intermedius em ambiente florestal e extraflorestal. Rev. Saude publ., Sāo Paulo 17, 23–30.Google Scholar
Hommel, M. (1978) The Genus Leishmania: Biology of the parasite and clinical aspects. Bull. Inst. Pasteur, Paris 75, 5–102.Google Scholar
Hueck, K. (1972) As Florestas da America do Sul; Ecologia, Composiçāo e Imporlância Econômica. Univ. Brasilia, Sāo Paulo.Google Scholar
Iversson, L. B., Camargo, M. E., Rocha e Silva, E. O., Chieffi, P. P. and Barros, J. A. C. (1979) Investigaçāo epidemiologica de um caso de Leishmaniose visceral autoctone da Grande Sāo Paulo, Brasil. Rev. Saúde públ., Sāo Paulo 13, 159–167.CrossRefGoogle Scholar
Iversson, L. B., Camargo, M. E., Villanova, A., Reichmann, M. L. A. B., Andrade, E. A. and Tolezano, J. E. (1983) Inquérito sorológico para pesquisa de leishmaniose visceral em populaçāo canina urbana do município de Sāo Paulo, Brasil. Rev. Inst. Med. trop. Sāo Paulo 25, 310–317.Google Scholar
Killick-Kendrick, R., Molyneux, D. H. and Rioux, J. A. (1980) Possible origins of Leishmania chagasi. Ann. trop. Med. Parasit. 74, 563–565.CrossRefGoogle ScholarPubMed
Lainson, R. (1981) Epidemiologia e ecologia da Leishmaniose tegumentar na Amazonia. Hiléia méd. 3, 35–10.Google Scholar
Lainson, R. (1983) The american leishmaniasis: some observation on their ecology and epidemiology. Trans. R. Soc. trop. Med. Hyg. 77, 569–596.CrossRefGoogle ScholarPubMed
Lainson, R. and Shaw, J. J. (1968) Leishmaniasis in Brasil. I—Observations on enzootic rodent leishmaniasis-incrimination of Lutzomyia flavisculellata (Mangabeira) as the vector in the lower Amazonian basin. Trans. R. Soc. trop. Med. Hyg. 62, 385–395.Google Scholar
Lainson, R. and Shaw, J. J. (1969a) Some reservoir-host of Leishmania in wild isolated from man and rodents. Trans. R. Soc. trop. Med. Hyg. 63, 408–109.CrossRefGoogle Scholar
Lainson, R. and Shaw, J. J. (1969b) Leishmaniasis in Brazil: III—Cutaneous leishmaniasis in an opossum, Marmosa murina (Marsupialia, Didelphidae) from the lower Amazon region. Trans. R. Soc. trop. Med. Hyg. 63, 738–740.CrossRefGoogle Scholar
Lainson, R. and Shaw, J. J. (1970) Leishmaniasis in Brazil: V—Studies on the epidemiology of cutanedous leishmaniasis in Mato Grosso States, and observations on two distinct strains of Leishmania isolated from man and forest animals. Trans. R. Soc. trop. Med. Hyg. 64, 654–667.CrossRefGoogle Scholar
Lainson, R. and Shaw, J. J. (1979) The role of animals in the epidemiology of South American Leishmaniasis. In Biology of the Kinetoplastida (Edited by Lumisden, W. H. R. and Evans, D. A.), Vol. 2, pp. 1–116. Academic Press, London.Google Scholar
Lainson, R., Shaw, J. J., Ward, R. D. and Fraiha, (1973) Leishmaniasis in Brazil: Considerations on the Leishmania braziliensis complex: Importance of the sandflies of the genus Psychodopygus (Mangabeira) in the transmission of L. braziliensis braziliensis in north Brazil. Trans. R. Soc. trop. Med. Hyg. 67, 184–196.CrossRefGoogle Scholar
Lainson, R., Ward, R. D. and Shaw, J. J. (1976) Cutaneous Leishmaniasis in north Brazil: Lutzomyia anduzei as a major vector. Trans. R. Soc. trop. Med. Hyg. 70, 171–172.CrossRefGoogle ScholarPubMed
Lainson, R., Shaw, J. J., Ward, R. D., Ready, P. D. and Naiff, R. D. (1979) Leishmaniasis in Brazil: XIII. Isolation of Leishmania from armadillos (Dasypus novemcinclus ) and observations on the epidemiology of cutaneous leishmaniasis in North Para State. Trans. R. Soc. trop. Med. Hyg. 73, 239–242.CrossRefGoogle ScholarPubMed
Lainson, R., Shaw, J. J., Ready, P. D., Miles, M. A. and Povoa, M. (1981) Leishmaniasis in Brasil: XVI—Isolation and identification of Leishmania species from sandflies, wild mammals and man in north Para State, with particular reference to L. braziliensis guyanensis causative agent of ‘pain bois’. Trans. R. Soc. trop. Med. Hyg. 75, 530–536.CrossRefGoogle Scholar
Lainson, R., Shaw, J. J., Miles, M. A. and Póvoa, M. M. (1982) Leishmaniasis in Brazil: XVII-Enzymic characterization of a Leishmania from the armadillos, Dasypus novemcinctus. Trans. R. Soc. trop. Med. Hyg. 76, 810–811.CrossRefGoogle ScholarPubMed
Lainson, R., Shaw, J. J., Silveira, F. T. and Fraiha, H. (1983) Leishmaniasis in Brazil: XIX—Visceral leishmaniasis in the Amazon Region, and the presence of Lutzomyia longipalpis on the Island of Marajo, Para State. Trans. R. Soc. trop. Med. Hyg. 77, 323–330.CrossRefGoogle ScholarPubMed
Lima, L. C. R., Marzochi, M. C. A. and Sabroza, P. C. (1981) Flebotomineos em area de ocorrência de leishmaniose tegumentar no Bairro de Campo Grande, Rio de Janeiro, Brasil. Rev. bras. Malar. 33, 64–74.Google Scholar
Marzochi, M. C. A. de, Sabroza, P. C., Toledo, L. M., Marzochi, K. B., Tramontano, N. C. and Rangel Filho, F. F. (1985) Leishmaniose visceral na cidade do Rio de Janeiro, Brasil. Cadernos de Saude pùbl. Rio de Janeiro 15–17.Google Scholar
Mattos, E. A. (1981) Bionomia dos flebotomineos de Perobas, Municipios de Viana. (ES), area de leishmaniose tegumentar americana. Belo Horizonte Dissertaçāo de Mestrado em Parasitologia, Inst. Ciências Biologicas da UFMG.Google Scholar
Mayrink, W., Willians, P., Coelho, M. V., Dias, M., Vianna-Martins, A., Magalhà, P. A., Da-Costa, C. A., Falcào, A. R., Melo, M. N. and Falcāo, A. L. (1979) Epidemiology of dermal leishmaniasis in the Rio Doce Valley, State of Minas Gérais, Brazil. Ann. trop. Med. Parasit. 73, 123–137.Google Scholar
Nery-Guimarāes, R. F. and Azevedo, M. (1964) Roedores silvestres (Orymys Goëldi) da Amazonia com infecçāo natural por Leishmania. Hospital, Rio de Janeiro 66, 280–285.Google Scholar
Nery-Guimarāes, R. F., Azevedo, A. and Damasceno, R. (1968) Leishmaniose tegumentar zoonose de roedores silvestres da Amazonia. Mem. Inst. Oswaldo Cruz 66, 151–168.CrossRefGoogle Scholar
Rego Junior, F. A., Nunes, V. L. B., Pereira, M. J. S., Cavalheiros, M. E. M., Silva, R. P. and Barros, E. (1983) Ocorrência de casos de Leishmaniose em càes no municipio de Corumbā, Estado de Mato Grosso do Sul. In Congresso da Federacion Latinoamericana de Para-sitologos p. 2. Resumos, Sāo Paulo, Brasil.Google Scholar
Pessoa, S. B. and Barreto, M. P. (1944) Leishmaniose Tegumentar Americana. Ministério da Educaçāo e Saude, Rio de Janeiro.Google Scholar
Rangel, E. F., Souza, N. A., Wermelinger, E. D. and Barbosa, A. F. (1984) Infecçào natural de Lutzomyia intermedia Lutz & Neiva, 1912, em area endêmica de leishmaniose tegumentar no Estado do Rio de Janeiro. Mem. Inst. Oswaldo Cruz 79, 395–396.CrossRefGoogle ScholarPubMed
Ready, P. D., Lainson, R. and Shaw, J. J. (1983a) Leishmaniasis in Brazil: XX—Prevalence of ‘enzootic rodent leishmaniasis’ (Leishmania mexicana amazonensis), and apparent absence of ‘pian bois’ (Le. braziliensis guyanensis), in plantations of introduced tree species and in other non-climax forests in Amazonia. Trans. R. trop. Med. Hyg. 77, 775–785.CrossRefGoogle ScholarPubMed
Ready, P. D., Ribeiro, A. L., Lainson, R., Alencar, J. E. and Shaw, J. J. de (1983b) Presence of Psychodopygus wellcomei (Diptera: Psychodidae), a proven vector of Leishmania braziliensis in Ceara State. Mem. Inst. Oswaldo Cruz 78, 235–236.CrossRefGoogle ScholarPubMed
Ready, P. D., Lainson, R. and Shaw, J. J. (1984) Habitat and seasonality of Psychodopygus wellcomei help incriminate it as vector of Leishmania braziliensis in Amazonia and northeast Brazil. Trans. R. Soc. trop. Med. Hyg. 78, 543–544.CrossRefGoogle ScholarPubMed
Ryan, L. and Brazil, R. P. (1984) Leishmania infections in Lutzomyia longipalpis (Diptera: Psychodidae) on the Island of Sāo Luis, Maranhào State, Brazil. Mem. Inst. Oswaldo Cruz 79, 383–384.CrossRefGoogle ScholarPubMed
Shaw, J. J. and Lainson, R. (1968) Leishmaniasis in Brazil: II—Observations on enzootic rodents leishmaniasis in the lower Amazon region. The feeding habits of the vector Lutzomyia flaviscutellata in reference to man, rodents and other animals. Trans. R. Soc. trop. Med. Hyg. 62, 396–405.CrossRefGoogle Scholar
Sherlock, I. A., Miranda, J. C., Sadigursky, M. and Grimaldi, G. Jr (1984) Natural infection of the opossum Didelphis albiventris (Marsupialia, Didelphidae) with Leishmania donovani in Brazil. Mem. Inst. Oswaldo Cruz 79, 511.CrossRefGoogle ScholarPubMed
Silva, A. R., Costa, J. M., Mochel, A., Carneiro, E. W. B. and Brasil, R. (1983) Leishmaniose visceral na Ilha de Sāo Luiz. I—Aspectos clinicos e terapêuticos (Nota prévia). In Congresso Brasileiro de Medicina Tropical, Vol. 19, p. 57. Resumo dos trabalhos, Sociedade Brasileira de Medicina Tropical, Rio de Janeiro.Google Scholar
Silveira, F. T., Lainson, R., Shaw, J. J. and Póvoa, M. M. (1982) Leishmaniasis in Brazil: XVIII—Further evidence incrimination the fox Cerdocyon thous (L) as a reservoir of Amazonian visceral leishmaniasis. Trans. R. Soc. trop. Med. Hyg. 76, 830–832.CrossRefGoogle ScholarPubMed
Sucam, (1984) Dados sobre leishmaniose. In Reuniāo Nacional Sobre Pesquisa em Leishmaniose, 1st edn.Facul-dade de Medicina da USP, Sāo Paulo.Google Scholar
Ward, R. D. (1977) New World Leishmaniasis: a review of the epidemiological changes in the last three decades. In Proceedings of the International Congress of Entomology, Washington.Google Scholar
Ward, R. D., Shaw, J. J., Lainson, R. and Fraiha, H. (1973a) Leishmaniasis in Brazil: VIII—Observations on the phlebotomine fauna of area highly endemic for cutaneous leishmaniasis in the Serra dos Carajās, Para State. Trans. R. Soc. trop. Med. Hyg. 67, 174–183.CrossRefGoogle ScholarPubMed
Ward, R. D., Lainson, R. and Shaw, J. J. (1973b) Further evidence of the role of Lutzomyia flaviscutellatus (Mangabeira) as the vector of Leishmania mexicana amazonensis in Brazil. Trans. R. Soc. trop. Med. Hyg. 67, 608–609.Google Scholar
Yoshida, E. L. A., Silva, R. L., Cortez, L. S. Jr and Corrêa, F. M. A. (1979) Encontre de espécie do gênero Leishmania em Didelphis Marsupialis aurita no Estado de Sāo Paulo, Brasil. Nota Prévia. Rev. Inst. Med. trop. Sāo Paulo 21, 110–113.Google Scholar