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Sand Fly Vectors of American Cutaneous Leishmaniasis in Brazil

  • Elizabeth F. Rangel
  • Ralph Lainson
  • Bruno M. Carvalho
  • Simone M. Costa
  • Jeffrey J. Shaw
Chapter

Abstract

American Cutaneous leishmaniasis (ACL) in Brazil is caused by seven Leishmania species. A multitude of sand fly species are implicated in their enzootic and zoonotic transmission. This chapter catalogues the different phlebotomines involved together with their feeding habits, geographical distribution and the impact of climatic and environmental changes. Clades of the same Leishmania species are transmitted by different sand fly genera in different geographical regions. In Amazonia Psychodopygus species are L. (Viannia) ACL vectors. In the Atlantic rainforest zone and the Guyana shield region Nyssomyia species are vectors of ACL caused by L. (Viannia) species. Bichromomyia, Migonemyia and Pintomyia species are also considered to be important ACL vectors. Evidence is accumulating indicating that some parasite may be transmitted by more than one species in an ACL focus.

References

  1. Afonso MMS, Gomes AC, Meneses CRV, Rangel EF (2005) Studies on the feeding habits of Lutzomyia (N.) intermedia (Diptera: Psychodidae), vector of cutaneous leishmaniasis in Brazil. Cad Saude Publica 21:1816–1820PubMedCrossRefPubMedCentralGoogle Scholar
  2. Aguiar GM, Medeiros WM (2003) Distribuição regional e habitats das espécies de flebotomíneos do Brasil. In: Elizabeth Rangel & Ralph Lainson (org.). Flebotomíneos do Brasil. Editora Fiocruz, Rio de Janeiro. pp 291–310Google Scholar
  3. Aguiar GM, Soucasaux T (1984) Ecological aspects of Phlebotomus of Parque Nacional da Serra dos Órgãos, Rio de Janeiro. I. Monthly frequency in human baits (Diptera: Psychodidae: Phlebotominae). Mem Inst Oswaldo Cruz 79:197–209PubMedCrossRefPubMedCentralGoogle Scholar
  4. Alexander B, Oliveira EB, Haigh E, Almeida LL (2002) Transmission of Leishmania in coffee plantations of Minas Gerais, Brazil. Mem Inst Oswaldo Cruz 97:627–630PubMedCrossRefPubMedCentralGoogle Scholar
  5. Andrade MS, Valença HF, da Silva AL, Almeida EL, de Brito ME, Brandão-Filho SP (2005) Sand fly fauna in a military training area endemic for American tegumentary leishmaniasis in the Atlantic Rain Forest region of Pernambuco, Brazil. Cad Saude Publica 21:1761–1767PubMedCrossRefPubMedCentralGoogle Scholar
  6. Andrade-Filho JD, Galati EA, Falcão AL (2004) Biology of the first generation of a laboratory colony of Nyssomyia intermedia (Lutz & Neiva, 1912) and Nyssomyia neivai (Pinto, 1926) (Diptera: Psychididae). Mem Inst Oswaldo Cruz 99:597–601PubMedCrossRefPubMedCentralGoogle Scholar
  7. Andrade Filho JD, Brazil RP (2003) Relationships of new word phlebotomine sand flies (Diptera: Psychodidae) based on fossil evidence. Mem Inst Oswaldo Cruz 98(Suppl. 1):145–149CrossRefGoogle Scholar
  8. Aragão HB (1922) Leishmaniose tegumentar e a sua transmissão pelo Phlebotomus. Mem Inst Oswaldo Cruz 82:143Google Scholar
  9. Aragão HR (1927) Leishmaniose Tegumentar e sua Transmissão pelos Flebótomos. Mem Inst Oswaldo Cruz 20(2):177–185CrossRefGoogle Scholar
  10. Araújo Filho NA, Sherlock IA, Coura JR (1981) Leishmaniose Tegumentar Americana na Ilha Grande, Rio de Janeiro. V. Observações sobre a biologia dos transmissores em condições naturais. Rev Soc Bras Med Trop 14(4–6):171–183CrossRefGoogle Scholar
  11. Araujo-Pereira T, Fuzari AA, Andrade Filho JD, Pita-Pereira D, Britto C, Brazil RP (2014) Sand fly fauna (Diptera: Psychodidae: Phlebotominae) in an area of leishmaniasis transmission in the municipality of Rio Branco, State of Acre, Brazil. Parasit Vect 7(1):360CrossRefGoogle Scholar
  12. Arias JR, Freitas RA (1977a) On the vectors of cutaneous leishmaniasis in the Central Amazon of Brazil. I. Preliminary findings. Acta Amazon 7:293–294CrossRefGoogle Scholar
  13. Arias JR, Freitas RA (1977b) Flebótomos da Amazônia Central. 1. Resultados obtidos das capturas feitas com iscas humanas e eqüina (Diptera: Psychodidae). Acta Amazon 7:507–527CrossRefGoogle Scholar
  14. Arias JR, Freitas RA (1978) Sobre os vetores de leishmaniose cutânea na Amazônia Central do Brasil. 2. Incidência de flagelados em flebótomos selváticos. Acta Amazon 8:387–396CrossRefGoogle Scholar
  15. Arias JR, Miles MA, Naiff RD, Povoa MM, de Freitas RA, Biancardi CB, Castellon EG (1985) Flagellate infections of Brazilian sand flies (Diptera: Psychodidae): isolation in vitro and biochemical identification of Endotrypanum and Leishmania. Am J Trop Med Hyg 34:1098–1108CrossRefPubMedGoogle Scholar
  16. Ashford RW (2000) The leishmaniasis as emerging and reemerging zoonoses. Int J Parasitol 30:1269–1281PubMedCrossRefPubMedCentralGoogle Scholar
  17. Azeredo-Coutinho RBG, Conceição-Silva F, Schubach A, Cupolillo E, Quintella LP, Madeira MF, Pacheco RS, Valete-Rosalino CM, Mendonça SCF (2007) First report of diffuse cutaneous leishmaniasis and Leishmania amazonensis infection in Rio de Janeiro State, Brazil. Trans Roy Soc Trop Med Hyg 101:735–737PubMedCrossRefPubMedCentralGoogle Scholar
  18. Azevedo ACR (2008) Contribuição ao conhecimento da fauna de flebotomíneos do Estado do Acre com ênfase em Lutzomyia (Nyssomyia) umbratilis Ward & Fraiha, 1977, importante transmissor de leishmaniose tegumentar americana na Amazônia: biologia, morfologia, morfometria e discussão da identidade taxonômica, PnD Thesis, Instituto Oswaldo Cruz, Rio de Janeiro, 144 ppGoogle Scholar
  19. Azevedo ACR, Bessa-Luz S, Vilela ML, Rangel EF (1993) Studies on the sand fly fauna of Samuel Ecological Station, Porto Velho municipality, Rondônia State, Brazil. Mem Inst Oswaldo Cruz 88:509–512CrossRefGoogle Scholar
  20. Azevedo ACR, Costa SM, Pinto MC, Souza JL, Cruz HC, Vidal J, Rangel EF (2008) Studies on the sand fly fauna (Diptera: Psychodidae: Phlebotominae) from transmission areas of American cutaneous leishmaniasis in State of Acre, Brazil. Mem Inst Oswaldo Cruz 103:760–767PubMedCrossRefPubMedCentralGoogle Scholar
  21. Azevedo ACR, Lainson R, Afonso MMS, Rangel EF (2005) Estudio sobre Lutzomyia (Nyssomyia) umbratilis Ward & Frailha, 1977 (Psychodidae: Phlebotominae), vector de la leishmaniasis tegumentar Americana, en el Amazonas. Salud Ciencia 14:30–33Google Scholar
  22. Azevedo ACR, Rangel EF (1991) A study of sand fly species (Diptera: Psychodidae: Phlebotominae) in a focus of cutaneous leishmaniasis in the Municipality of Baturité, Ceará, Brazil. Mem Inst Oswaldo Cruz 85:251CrossRefGoogle Scholar
  23. Azevedo ACR, Rangel EF, Costa EM, David J, Vasconcelos AW, Lopes UG (1990) Natural infection of Lutzomyia (Nysomyia) whitmani (Antunes & Coutinho, 1939) by Leishmania of the braziliensis complex in Baturité, Ceará State, Northeast Brazil. Mem Inst Oswaldo Cruz 85:251PubMedCrossRefPubMedCentralGoogle Scholar
  24. Azevedo ACR, Souza NA, Meneses CRV, Costa WA, Costa SM, Lima JB, Rangel EF (2002) Ecology of sand flies (Diptera: Psychodidae: Phlebotominae) in the North of Mato Grosso, Brazil. Mem Inst Oswaldo Cruz 97(4):459–464PubMedCrossRefPubMedCentralGoogle Scholar
  25. Azevedo PCB, Lopes GN, Fonteles RS, Vasconcelos GC, Moraes JLP, Rebêlo JMM (2011) The effect of fragmentation on phlebotomine communities (Diptera: Psychodidae) in areas of ombrophilous forest in São Luís, state of Maranhão, Brazil. Neotrop Entomol 40(2):271–277PubMedCrossRefPubMedCentralGoogle Scholar
  26. Balbino VQ, Coutinho-Abreu IV, Sonoda IV, Marques da Silva W, Marcondes CB (2005) Phlebotomine sandflies (Diptera: Psychodidae) of the Atlantic forest in Recife, Pernambuco state, Brazil: the species coming to human bait, and their seasonal and monthly variations over a 2-year period. Ann Trop Med Parasit 99(7):683–693PubMedCrossRefPubMedCentralGoogle Scholar
  27. Balbino VQ, Marcondes CB, Alexander B, Luna LK, Lucena MM, Mendes A, Andrade PP (2001) First report of Lutzomyia (Nyssomyia) umbratilis Ward & Frahia, 1977 outside of Amazonian Region, in Recife, State of Pernambuco, Brazil (Diptera: Psychodidae: Phlebotominae). Mem Inst Oswaldo Cruz 96(3):315–317PubMedCrossRefPubMedCentralGoogle Scholar
  28. Barbosa MG, Fé NF, Marcião AH, Silva AP, Monteiro WM, Guerra JA (2008) Sand fly fauna (Diptera: Psychodidae) in a focus of American cutaneous leishmaniasis on the urban periphery of Manaus, state of Amazonas. Rev Soc Bras Med Trop 41:485–491PubMedCrossRefPubMedCentralGoogle Scholar
  29. Barreto AC, Vexenat JA, Cuba-Cuba CA, Marsden PD (1982) Fauna flebotomínica de uma região endêmica de leishmaniose cutâneo-mucosa no Estado da Bahia. IX Reunião Anual sobre Pesquisa Básica em Doenças de Chagas, 147 ppGoogle Scholar
  30. Barretto MP (1943) Observações sobre a biologia em condições naturais dos flebótomos do estado de São Paulo (Ditera: Psychodidae). Tese de Livre-Docência, Faculdade de Medicina da USP, São Paulo, p 162Google Scholar
  31. Barretto MP (1961) Subfamilias e gêneros neotropicais da família Psychodidae Big, 1854 (Diptera). Pap Av Dep Zool S Paulo 14:211–225Google Scholar
  32. Brandão-Filho SP, Brito ME, Carvalho FG, Ishikawa EA, Cupolillo E, Floeter-Winter L, Shaw JJ (2003) Wild and synanothropic hosts of Leishmania (Viannia) braziliensis in the endemic cutaneous leishmaniasis locality of Amaraji, Pernambuco state, Brazil. Trans R Soc Trop Med Hyg 97:291–296PubMedCrossRefPubMedCentralGoogle Scholar
  33. Brandão-Filho SP, Campbell-Lendrum D, Brito ME, CR SJJD (1999) Epidemiological surveys confirm an increasing burden of cutaneous leishmaniasis in North–East Brazil. Trans Roy Soc Trop Med Hyg 93:488–494PubMedCrossRefPubMedCentralGoogle Scholar
  34. Brasil (2007) Ministério da Saúde. Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Manual de Vigilância da Leishmaniose Tegumentar Americana 2a. ed. Editora do Ministério da Saúde, BrasíliaGoogle Scholar
  35. Brito VND, Almeida ADBPF, Nakazato L, Duarte R, Souza CDO, Sousa VRF (2014) Phlebotomine fauna, natural infection rate and feeding habits of Lutzomyia cruzi in Jaciara, state of Mato Grosso, Brazil. Mem Inst Oswaldo Cruz 109(7):899–904PubMedPubMedCentralCrossRefGoogle Scholar
  36. Camargo-Neves VLF, Gomes AC, Antunes JLF (2002) Correlação da presença de espécies de flebotomíneos (Diptera: Psychodidae) com registros de casos da leishmaniose tegumentar americana no Estado de São Paulo, Brasil. Rev Soc Bras Med Trop 35(4):1–11CrossRefGoogle Scholar
  37. Campbell-Lendrum D, Dujardin JP, Martinez E, Feliciangeli MD, Perez JE, Silans LNMP, Desjeux P (2001) Domestic and peridomestic transmission of American cutaneous leishmaniasis: changing epidemiological patterns present new control opportunities. Mem Inst Oswaldo Cruz 96(2):159–162PubMedCrossRefPubMedCentralGoogle Scholar
  38. Campbell-Lendrum DH, Brandão-Filho SP, Ready PD, Davies CR (1999) Host and/or site loyalty of Lutzomyia whitmani (Diptera: Psychodidae) in Brazil. Med Vet Entomol 13:209–211PubMedCrossRefPubMedCentralGoogle Scholar
  39. Campos AM, Matavelli R, Santos CD, Moraes LS, Rebêlo JMM (2013) Ecology of phlebotomines (Diptera: Psychodidae) in a transitional area between the Amazon and the Cerrado in the state of Maranhão, Brazil. J Med Entomol 50(1):52–58PubMedCrossRefPubMedCentralGoogle Scholar
  40. Cardenas R, Sandoval CM, Rodríguez-Morales AJ, Franco-Paredes C (2006) Impact of climate variability in the occurrence of leishmaniasis in northeastern Colombia. Am J Trop Med Hyg 75(2):273–277PubMedPubMedCentralCrossRefGoogle Scholar
  41. Cardenas R, Sandoval CM, Rodríguez-Morales AJ, Vivas P (2008) Zoonoses and climate variability. The example of leishmaniasis in southern departments of Colombia. Ann New York Acad Sci 1149:326–330CrossRefGoogle Scholar
  42. Carvalho BM, Dias CMG, Rangel EF (2014) Phlebotomine sand flies (Diptera, Psychodidae) from Rio de Janeiro State, Brazil: species distribution and potential vectors of leishmaniases. Rev Bras Entomol 58(1):77–87CrossRefGoogle Scholar
  43. Carvalho BM, Rangel EF, Ready PD, Vale MM (2015) Ecological niche modelling predicts southward expansion of Lutzomyia (Nyssomyia) flaviscutellata (Diptera: Psychodidae: Phlebotominae), vector of Leishmania (Leishmania) amazonensis in South America, under climate change. PLoS One 10(11):e0143282PubMedPubMedCentralCrossRefGoogle Scholar
  44. Carvalho BM, Rangel EF, Vale MM (2017) Evaluation of the impacts of climate change on disease vectors through ecological niche modelling. Bull Ent Res 107:419–430CrossRefGoogle Scholar
  45. Carvalho BM, Maximo M, Costa WA, de Santana ALF, da Costa SM, da Costa Rego TAN, Pita-Pereira D, Rangel EF (2013) Leishmaniasis transmission in an ecotourism area: potential vectors in Ilha Grande, Rio de Janeiro State, Brazil. Parasit Vect 6:325CrossRefGoogle Scholar
  46. Carvalho RM, Valença HF, Silva FJ, Pita-Pereira D, Pereira TA, Britto C, Brazil RP, Brandão Filho SP (2010) Natural Leishmania infantum in Migonemyia migonei (França, 1920) (Diptera:Psychodidae: Phlebotominae) the putative vector of visceral leishmaniasis in Pernambuco. State, Brazil. Acta Trop 116:108–110PubMedPubMedCentralCrossRefGoogle Scholar
  47. Carvalho GM, Andrade Filho JD, Falcão AL, Rocha Lima AC, Contijo CM (2008) Naturally infected Lutzomyia sand flies in a Leishmania-endemic area of Brazil. Vector Borne Zoonotic Dis 8:407–414PubMedPubMedCentralCrossRefGoogle Scholar
  48. Casanova C, Natal D, Santos FA (2009) Survival, population size and gonotrophic cycle duration of Nyssomyia neivai (Diptera: Psychodidae) at an endemic area of American cutaneous leishmaniasis in Southeastern Brazil. J Med Entomol 46:42–50PubMedCrossRefPubMedCentralGoogle Scholar
  49. Chaves LF, Pascual M (2006) Climate cycles and forecasts of cutaneous leishmaniasis, a nonstationary vector-borne disease. PLoS Med 3(8):e295PubMedPubMedCentralCrossRefGoogle Scholar
  50. Christensen HA, Arias JR, de Vasques AM, de Freitas R (1982) Hosts of sand fly vectors of Leishmania braziliensis guyanensis in the central Amazon of Brazil. Am J Trop Med Hyg 31:239–242PubMedCrossRefPubMedCentralGoogle Scholar
  51. Costa JML, Costa AAUML, Elkhoury NA, Bezerril ACR, Barral A, Saldanha ACR (2009) Leishmaniose cutânea difusa (LCD) no Brasil após 60 anos de sua primeira descrição. Gazeta Médica da Bahia 79(Supl.3):16–24Google Scholar
  52. Costa SM, Cechinel M, Bandeira V, Zannuncio JC, Lainson R, Rangel EF (2007) Lutzomyia (Nyssomyia) whitmani s.l. (Antunes & Coutinho, 1939) (Diptera: Psychodidae: Phlebotominae) and the epidemiology of American cutaneous leishmaniasis in Brazil. Mem Inst Oswaldo Cruz 102:149–153PubMedCrossRefPubMedCentralGoogle Scholar
  53. Costa Lima AM (1932) Sobre os Phlebotomus Americanos (Diptera, Psychodidae). Mem Inst Oswaldo Cruz 26(1):15–69CrossRefGoogle Scholar
  54. da Costa SM, Luís Passos Cordeiro J, Rangel EF (2018) Environmental suitability for Lutzomyia (Nyssomyia) whitmani (Diptera: Psychodidae: Phlebotominae) and the occurrence of American cutaneous leishmaniasis in Brazil. Parasites & Vectors 11(1)Google Scholar
  55. Dias-Sversutti A, Scodro RB, Reinhold-Castro KR, Neitzke HC, Teodoro U (2007) Preliminary study on feeding preference of Nyssomyia neivai (Pinto) and Nyssomyia whitmani (Antunes & Coutinho) (Diptera: Psychodidae) in a rural area of the state of Paraná, South Brazil. Neotrop Entomol 36:953–959CrossRefGoogle Scholar
  56. de Souza AAA, Santos TV, Jennings YLL, Ishikawa EAY, Barata IR, Silva MGS, Lima JAN, Shaw J, Lainson R, Silveira FT (2016) Natural Leishmania (Viannia) spp. infections in phlebotomine sand flies (Diptera: Psychodidae) from the Brazilian Amazon region reveal new putative transmission cycles of American cutaneous leishmaniasis. Parasite 23:22PubMedPubMedCentralCrossRefGoogle Scholar
  57. de Souza A, Ishikawa E, Braga R, Silveira F, Lainson R, Shaw J (1996) Psychodopygus complexus, a new vector of Leishmania braziliensis to humans in Pará state, Brazil. Trans R Soc Trop Med Hyg 90:112–113PubMedPubMedCentralCrossRefGoogle Scholar
  58. de Souza AAA, da Rocha BI, das Gracas Soares Silva M, JAN L, YLL J, EAY I, Prevot G, Ginouves M, Silveira FT, Shaw J, Dos Santos TV (2017) Natural Leishmania (Viannia) infections of phlebotomines (Diptera: Psychodidae) indicate classical and alternative transmission cycles of American cutaneous leishmaniasis in the Guiana Shield, Brazil. Parasite 24:13PubMedPubMedCentralCrossRefGoogle Scholar
  59. Donalisio MR, Peterson AT, Costa PL, da Silva FJ, Valença HF, Shaw JJ, Brandão Filho SP (2012) Microspatial distributional patterns of vectors of cutaneous leishmaniasis in Pernambuco, northeastern Brazil. J Trop Med 2012:642910PubMedPubMedCentralCrossRefGoogle Scholar
  60. Dorval MEC, Alves TP, Oliveira AGD, Brazil RP, Galati EAB, Cunha RVD (2007) Modification of Disney trap for capture of sand flies (Diptera: Psychodidae: Phlebotominae). Mem Inst Oswaldo Cruz 102(7):877–878PubMedCrossRefPubMedCentralGoogle Scholar
  61. Dorval MEC, Alves TP, Cristaldo G, Rocha HCD, Alves MA, Oshiro ET, Oliveira AG, Brazil RP, Galati EAB, Cunha RVD (2010) Sand fly captures with Disney traps in area of occurrence of Leishmania (Leishmania) amazonensis in the State of Mato Grosso do Sul, mid-western Brazil. Rev Soc Bras Med Trop 43(5):491–495PubMedCrossRefPubMedCentralGoogle Scholar
  62. Dorval ME, Cristaldo G, Rocha HC, Alves TP, Alves MA, Oshiro ET, Brazil RP, Galati EA, Cunha RV (2009) Phlebotomine fauna (Diptera: Psychodidade) of an endemic area in the state of Mato Grosso do Sul, Brazil. Mem Inst Oswaldo Cruz 104:695–702PubMedCrossRefPubMedCentralGoogle Scholar
  63. Dujardin JC (2006) Risk factors in the spread of leishmaniases: towards integrated monitoring? Trends Parasitol 22(1):4–6PubMedCrossRefPubMedCentralGoogle Scholar
  64. Espinosa OA, Serrano MG, Camargo EP, Teixeira MM, Shaw JJ (2016) An appraisal of the taxonomy and nomenclature of trypanosomatids presently classified as Leishmania and Endotrypanum. Parasitology, ePub, 1–13.  https://doi.org/10.1017/S0031182016002092
  65. Esterre P, Chippaux JP, Lefait JF, Dedet JP (1986) Evaluation of a cutaneous leishmaniasis control program in a forest village of French Guyana. Bull World Health Organ 64:559–565PubMedPubMedCentralGoogle Scholar
  66. Fairchild GB, Hertig M (1948) An improved method for mounting small insects. Science 108(2792):20PubMedCrossRefPubMedCentralGoogle Scholar
  67. Falqueto A (1995) Especificidade alimentar de flebotomíneos em duas áreas endêmicas de leishmaniose tegumentar no estado do Espírito Santo, PhD Thesis, Fiocruz, Rio de Janeiro, 84 ppGoogle Scholar
  68. Feliciangeli MD, Ramirez Perez J, Ramirez A (1985) First Venezuelan record of Lutzomyia umbratilis Ward & Fraiha, 1977 (Diptera: Psychodidae), a proven vector of Leishmania braziliensis guyanensis. Trans R Soc Trop Med Hyg 79:878PubMedCrossRefPubMedCentralGoogle Scholar
  69. Ferreira AL, Sessa PA, Varejão JB, Falqueto A (2001) Distribution of sand flies (Diptera: Psychodidae) at different altitudes in an endemic region of American cutaneous leishmaniasis in the state of Espirito Santo, Brazil. Mem Inst Oswaldo Cruz 96:1061–1067PubMedCrossRefPubMedCentralGoogle Scholar
  70. Forattini OP, Santos MR (1952) Nota sobre infecção natural de Phlebotomus intermedius Lutz & Neiva, 1912, por formas leptomonas, em um foco ativo de leishmaniose tegumentar americana. Arq Hig S Paulo 17:171–174Google Scholar
  71. Forattini OP (1953) Nota sobre criadouros naturais de flebótomos em dependências peri-domiciliares no estado de São Paulo. Arq Fac Hig Saude Publica Univ Sao Paulo 7:157–168CrossRefGoogle Scholar
  72. Forattini OP (1954) Nota sobre a biologia de Phlebotomus (Diptera: Psychodidae) em região da Bacia do Rio Paraná (Brasil). Arq Fac Hig Saude Publica Univ Sao Paulo 8:15–136CrossRefGoogle Scholar
  73. Forattini OP (1973) Entomologia Médica, vol 4. Editora Edgard Blücher & Editora da Universidade de São Paulo, São Paulo, 658 ppGoogle Scholar
  74. Forattini OP, Pattoli DBG, Rabello EX, Ferreira OA (1972) Infecção natural de flebotomíneos em foco enzoótico de leishmaniose tegumentar no estado de São Paulo, Brasil. Rev Saude Publica 6:431–433PubMedCrossRefPubMedCentralGoogle Scholar
  75. Forattini OP, Rabello EX, Serra OP, Cotrim MD, Galati EAB, Barata JMS (1976) Observações sobre a transmissão da leishmaniose tegumentar no estado de São Paulo, Brasil. Rev Saude Publica 10:31–43PubMedCrossRefPubMedCentralGoogle Scholar
  76. França F, Lago EL, Tada S, Costa JM, Vale K, Oliveira J, Costa MA, Osaki M, Cheever L, Netto EM, Barretto AC, Johnson WD, Marsden PD (1991) An outbreak of human Leishmania (Viannia) braziliensis infection. Mem Inst Oswaldo Cruz 86:169–174PubMedCrossRefPubMedCentralGoogle Scholar
  77. Franke CR, Ziller M, Staubach C, Latif M (2002) Impact of the El Niño/Southern Oscillation on visceral leishmaniasis, Brazil. Emerg Infect Dis 8(9):914–917PubMedPubMedCentralCrossRefGoogle Scholar
  78. Galati EAB, Nunes VLB, Dorval MEC, Oshiro ET, Cristaldo G, Espínola MA, Rocha HC, Garcia WB (1996) Study of the phlebotomines (Diptera: Psychodidade) in area of cutaneous leishmaniasis in the Mato Grosso state, Brazil. Rev Saude Publica 30:115–128PubMedCrossRefPubMedCentralGoogle Scholar
  79. Gil LH, Basano AS, Souza AA, Silva MG, Barata I, Ishikawa EA, Camargo LM, Shaw JJ (2003) Recent observations on the sand fly (Diptera: Psychodidae) fauna of the state of Rondônia, western Amazonia, Brazil: the importance of Psychodopygus davisi as a vector of zoonotic cutaneous leishmaniasis. Mem Inst Oswaldo Cruz 98:751–755CrossRefPubMedGoogle Scholar
  80. Godoy RE, de Santana ALF, Graser C, Rangel EF, Vilela ML (2017) Aspects on the ecology of phlebotomine sand flies (Diptera: Psychodidae) from Guaraí, state of Tocantins, Brazil, endemic area for American cutaneous leishmaniasis. J Med Entomol 54(1):229–235PubMedCrossRefPubMedCentralGoogle Scholar
  81. Gomes AC (1994) Sand fly vectorial ecology in the state of São Paulo. Mem Inst Oswaldo Cruz 89:457–460PubMedCrossRefPubMedCentralGoogle Scholar
  82. Gomes AC, Rabello EX, Santos JFL, Galati EAB (1986) Ecological aspects of American cutaneous leishmaniasis. 4. Observation on the endophilic behavior of the sand fly and the vectorial role of Psychodopygus intermedius in the Ribeira Valley region of the S. Paulo state, Brazil. Rev Saude Publica 20:280–287CrossRefGoogle Scholar
  83. Gomes AC, Galati EA (1989) Aspectos ecológicos da leishmaniose tegumentar americana. 7. Capacidade vetorial flebotominea em ambiente florestal primário do sistema da Serra do Mar, região do Vale do Ribeira, estado de São Paulo, Brasil. Rev Saude Publica 23:136–142CrossRefGoogle Scholar
  84. Gonçalves BRD (2003) Identificação da Fauna de Flebotomíneos em Função de Casos Autóctones de LTA. Boletim Epidemiológico. Secretaria Municipal de Saúde de Porto Alegre 21(5):5Google Scholar
  85. González C, Wang O, Strutz SE, González-Salazar C, Sánchez-Cordero V, Sarkar S (2010) Climate change and risk of leishmaniasis in North America: predictions from ecological niche models of vector and reservoir species. PLoS Negl Trop Dis 4(1):e585PubMedPubMedCentralCrossRefGoogle Scholar
  86. Gouveia C, Oliveira RM, Zwetsch A, Motta-Silva D, Carvalho BM, Santana AF, Rangel EF (2012) Integrated tools for American cutaneous leishmaniasis surveillance and control: intervention in an endemic area in Rio de Janeiro, RJ, Brazil. Interdis Perspec Infect Dis 2012:1–9CrossRefGoogle Scholar
  87. Grimaldi G Jr, Momen H, Naiff RD, McMahon-Pratt D, Barrett TV (1991) Characterization and classification of leishmanial parasites from humans, wild mammals, and sand flies in the Amazon region of Brazil. Am J Trop Med Hyg 44:645–661PubMedCrossRefPubMedCentralGoogle Scholar
  88. Guerra JA, Barbosa MG, Loureiro AC, Coelho CP, Rosa GG, Coelho LI (2007) American tegumentary leishmaniasis in children: epidemiological aspects of cases treated in Manaus, Amazonas, Brazil. Cad Saude Publica 23:2215–2223PubMedCrossRefPubMedCentralGoogle Scholar
  89. Guimarães FN, Costa O (1966) Novas observações sobre a Leishmania isolada de “Oryzomys goeldi” na Amazônia (4a nota). Hospital RJ 69:161–168Google Scholar
  90. Guimarães VCFV, Costa PL, Silva FJ, Silva KT, Silva KG, Araújo AI, Rodrigues EHF, Brandão-Filho SP (2012) Phlebotomine sand flies (Diptera: Psychodidae) in São Vicente Férrer, a sympatric area to cutaneous and visceral leishmaniasis in Pernambuco, Brazil. Rev Soc Bras Med Trop 45:66–70PubMedCrossRefPubMedCentralGoogle Scholar
  91. Hlavacova J, Votypka J, Volf P (2013) The effect of temperature on Leishmania (Kinetoplastida: Trypanosomatidae) development in sand flies. J Med Entomol 50(5):955–958PubMedPubMedCentralGoogle Scholar
  92. Hoch A, Ryan L, Vexenet JA, Rosa AC, Barretto AC (1986) Isolation of Leishmania braziliensis braziliensis and other trypanosomatids from phlebotomines in mucocutaneous leishmaniasis endemic area, Bahia, Brazil. Mem Inst Oswaldo Cruz 81(Suppl):BI 44Google Scholar
  93. IPCC. Core Writing Team, Pachauri RK, Meyer LA (eds) (2014) Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC, GenevaGoogle Scholar
  94. Ishikawa EAY, Ready PD, de Souza AA, Day JC, Rangel EF, Davies CR, Shaw JJ (1999) A mitochondrial DNA phylogeny indicates close relationship between populations of Lutzomyia whitmani (Diptera: Psychodidae: Phlebotominae) from the rain-forest region of Amazônia and Northeast Brazil. Mem Inst Oswaldo Cruz 94:339–345PubMedPubMedCentralCrossRefGoogle Scholar
  95. Joetzjer E, Douville H, Delire C, Ciais P (2013) Present-day and future Amazonian precipitation in global climate models: CMIP5 versus CMIP3. Clim Dyn 41(11–12):2921–2936CrossRefGoogle Scholar
  96. Justiniano SCB, Chagas AC, Pessoa FAC, Queiroz RG (2004) Comparative biology of two populations of Lutzomyia umbratilis (Diptera: Psychodidae) of central Amazonia, Brazil, under laboratory conditions. Braz J Biol 64:227–235PubMedCrossRefPubMedCentralGoogle Scholar
  97. Lainson R (1983) The American leishmaniases: some observation on their ecology and epidemiology. Trans R Soc Trop Med Hyg 77:569–596PubMedPubMedCentralCrossRefGoogle Scholar
  98. Lainson R (1988) Ecological interactions in the transmission of the leishmaniases. Philos Trans R Soc Lond Series B 321:389–404CrossRefGoogle Scholar
  99. Lainson R, Braga RR, Souza AA, Povoa MM, Ishihawa EAY, Silveira FT (1989) Leishmania (Viannia) shawi sp.n, a parasite of monkeys, sloths and procyonids in Amazonian Brazil. Ann Parasit Hum Comp 64:200–207CrossRefGoogle Scholar
  100. Lainson R, Shaw JJ (1968) Leishmaniasis in Brazil I. Observations on enzootic rodent leishmaniasis – incrimination of Lutzomyia flaviscutellata (Mangabeira) as the vector in the lower Amazonian Basin. Trans R Soc Trop Med Hyg 62:385–395PubMedCrossRefPubMedCentralGoogle Scholar
  101. Lainson R, Shaw JJ (1970) Leishmaniasis in Brazil. V: studies on the epidemiology of cutaneous leishmaniasis in Mato Grosso state and observations on two distinct strains of Leishmania isolates from man and forest animals. Trans R Soc Trop Med Hyg 64:654–667PubMedCrossRefPubMedCentralGoogle Scholar
  102. Lainson R, Shaw JJ (1972) Leishmaniasis of the new world: taxonomic problems. Brit Med Bull 28:44–48PubMedCrossRefPubMedCentralGoogle Scholar
  103. Lainson R, Shaw JJ (1979) The role of animals in the epidemiology of South American leishmaniasis. In: Lumsden WHR, Evans DA (eds) Biology of the Kinetoplastida, vol 2. Academic Press, London, pp 1–116Google Scholar
  104. Lainson R, Shaw JJ (1987) Evolution, classification and geographic distribution. In: Peters W, Killick-Kendrick R (eds) The leishmaniases in biology and medicine, vol 1. Academic Press, London, pp 1–20Google Scholar
  105. Lainson R, Shaw JJ (1998) New World leishmaniasis. The neotropical Leishmania species. In: Cox FEG, Kreier JP, Wakelin D (eds), Topley & Wilson’s microbiology & microbiol infections, 9th edn. vol 5. Parasitology, Arnold, London, pp 242–266Google Scholar
  106. Lainson R, Shaw JJ, Póvoa M (1981a) The importance of edentates (sloths and anteaters) as primary reservoirs of Leishmania brazi-liensis guyanensis, causative agent of “pian-bois” in North Brazil. Trans R Soc Trop Med Hyg 75:611–612CrossRefPubMedGoogle Scholar
  107. Lainson R, Shaw JJ, Póvoa M (1981b) Leishmaniasis in Brazil: XVI. Isolation and identification of Leishmania species from sand flies, wild mammals and man in north Pará state, with particular reference to L. braziliensis guyanensis causative agent of “pian-bois”. Trans R Soc Trop Med Hyg 75:530–536CrossRefPubMedGoogle Scholar
  108. Lainson R, Shaw JJ, Silveira FT, de Souza AA, Braga RR, Ishikawa EA (1994) The dermal leishmaniases of Brazil, with special reference to the eco-epidemiology of the disease in Amazônia. Mem Inst Oswaldo Cruz 89:435–443PubMedPubMedCentralCrossRefGoogle Scholar
  109. Lainson R, Shaw JJ, Ward RD, Fraiha H (1973) Leishmaniasis in Brazil. IX. Considerations on the Leishmania braziliensis complex. Importance of sand flies of the genus Psychodopygus (Mangabeira) in the transmission of Leishmania braziliensis braziliensis in North Brazil. Trans R Soc Trop Med Hyg 67:184–196CrossRefGoogle Scholar
  110. Lainson R, Shaw JJ, Ward RD, Ready PD, Naiff RD (1979) Leishmaniasis in Brazil: XIII. Isolation of Leishmania from armadillos (Dasypus novemcinctus) and observation on the epidemiology of cutaneous leishmaniasis in north Pará state. Trans R Soc Trop Med Hyg 73:239–242PubMedCrossRefPubMedCentralGoogle Scholar
  111. Lainson R, Strangways-Dixon J (1964) The epidemiology of dermal leishmaniasis in British Honduras. Parte III. Reservoir-host of Leishmania mexicana among forest rodents. Trans R Soc Trop Med Hyg 58:136–153PubMedCrossRefPubMedCentralGoogle Scholar
  112. Lainson R, Ward RD, Shaw JJ (1976) Cutaneous leishmaniasis in North Brazil: Lutzomyia anduzei as a major vector. Trans R Soc Trop Med Hyg 70:171–172PubMedCrossRefPubMedCentralGoogle Scholar
  113. Le Pont F, Pajot FX (1980) La leishmaniose en Guyane Française. I. Etude de l’ecologie et du taux d’infection naturelle d’un vecteur Lutzomyia (Nyssomyia) umbratilis Ward et Fraiha, 1977 en saison sèche. Considerations epidémiologiques. Cah ORSTOM Ser Ent Med Parasitol 18:359–383Google Scholar
  114. Lucena DT (1953) Flebótomos do Nordeste. Morfologia de algumas espécies e sua distribuição. Papéis Avulsos de Zoologia 11:89–107Google Scholar
  115. Luz E, Membrive N, Castro EA, Dereure J, Pratlong F, Dedet JA, Pandey A, Thomaz-Soccol V (2000) Lutzomyia whitmani (Diptera: Psychodidae) as vector of Leishmania (V.) braziliensis in Paraná state, Southern Brazil. Ann Trop Med Parasitol 94:623–631PubMedCrossRefPubMedCentralGoogle Scholar
  116. Marcondes CB (1996) A redescription of Lutzomyia (Nyssomyia) intermedia (Lutz & Neiva, 1912) and resurrection of L. neivai (Pinto, 1926) (Diptera: Psychodidae: Phlebotominae). Mem Inst Oswaldo Cruz 91:457–462CrossRefGoogle Scholar
  117. Marcondes CB, Day JC, Ready PD (1997) Introgression between Lutzomyia intermedia and both Lu. neivai and Lu. whitmani and their roles as vectors of Leishmania braziliensis. Trans R Soc Trop Med Hyg 91:725–726PubMedPubMedCentralCrossRefGoogle Scholar
  118. Marcondes CB, Alexander B (2003) Correlation of male genital filaments and female spermathecal ducts in new world sand flies of the Lutzomyia intermedia species complex (Diptera: Psychodidae, Phlebotominae). Mem Inst Oswaldo Cruz 98:611–613PubMedCrossRefPubMedCentralGoogle Scholar
  119. Marcondes CB, Borges PSS (2000) Distinction of males of Lutzomyia intermedia (Lutz & Neiva, 1912) complex by ratios between dimensions and by an artificial neural network (Diptera, Psychodidae, Phlebotominae). Mem Inst Oswaldo Cruz 95:685–688PubMedCrossRefPubMedCentralGoogle Scholar
  120. Marcondes CB, Conceição MB, Portes MG, Simão BP (2005) Phlebotomine sand flies in a focus of dermal leishmaniasis in the eastern region of the Brazilian state of Santa Catarina: preliminary results (Diptera: Psychodidae). Rev Soc Bras Med Trop 38:353–355PubMedCrossRefPubMedCentralGoogle Scholar
  121. Marcondes CB, Lozovei AL, Falqueto A, Brazil RP, Galati EAB, Aguiar GM, Souza NA (1999) Influence of altitude, latitude and season of collection (Bergmann’s rule) on the dimension of Lutzomyia intermedia (Lutz & Neiva, 1912) (Diptera, Psychodidae, Phlebotominae). Mem Inst Oswaldo Cruz 94:693–700PubMedCrossRefPubMedCentralGoogle Scholar
  122. Marcondes CB, Lozovei L, Vilela JH (1998) Distribuição geográfica de flebotomíneos do complexo Lutzomyia intermedia (Lutz & Neiva, 1912) (Diptera, Psychodidae) geographic distribution of phlebotomine sandflies of the Lutzomyia intermedia (Lutz & Neiva, 1912) complex (Diptera, Psychodidae). Rev Soc Bras Med Trop 31(1):51–58PubMedCrossRefPubMedCentralGoogle Scholar
  123. Marcondes CB, Santos-Neto LG, Lozovei AL (2001) Ecology of phlebotomine sand flies (Diptera: Psychodidae) in Brazilian Atlantic Forest. Rev Soc Bras Med Trop 34:255–260PubMedCrossRefPubMedCentralGoogle Scholar
  124. Margonari CS, Dias-Forte CL, Dias ES (2004) Genetic variability in geographical populations of Lutzomyia whitmani elucidated by RAPD-PCR. J Med Entomol 41:187–192PubMedPubMedCentralCrossRefGoogle Scholar
  125. Martins AV, Williams P, Falcão A (1978) American sand flies. Academia Brasileira de Ciências, Rio de JaneiroGoogle Scholar
  126. Mayrink W, Williams P, Coelho MV, Dias M, Martins AV, Magalhães PA, Costa CA, Falcão AR, Melo MN, Falcão AL (1979) Epidemiology of dermal leishmaniasis in the Rio Doce Valley, state of Minas Gerais, Brazil. Ann Trop Med Parasitol 73:123–137PubMedCrossRefPubMedCentralGoogle Scholar
  127. McIntyre S, Rangel EF, Ready PR, Carvalho BM (2017) Species-specific ecological niche modelling predicts different range contractions for Lutzomyia intermedia and a related vector of Leishmania braziliensis following climate change in South America. Parasit Vect 10:157CrossRefGoogle Scholar
  128. McMichael AJ (2004) Environmental and social influences on emerging infectious diseases: past, present and future. Phil Trans Roy Soc London B 359:1049–1058PubMedPubMedCentralCrossRefGoogle Scholar
  129. Meneses CR, Cupolillo E, Monteiro F, Rangel EF (2005) Micro-geographical variation among male populations of the sand fly, Lutzomyia (Nyssomyia) intermedia, from an endemic area of American cutaneous leishmaniasis in the state of Rio de Janeiro, Brazil. Med Vet Entomol 19:38–47PubMedPubMedCentralCrossRefGoogle Scholar
  130. Moo-Llanes D, Ibarra-Cerdeña CN, Rebollar-Téllez EA, Ibáñez-Bernal S, González C, Ramsey JM (2013) Current and future niche of North and Central American sand flies (Diptera: Psychodidae) in climate change scenarios. PLoS Negl Trop Dis 7(9):e2421PubMedPubMedCentralCrossRefGoogle Scholar
  131. Moschin JC, Ovallos FG, Sei IA, Galati EA (2013) Ecological aspects of phlebotomine fauna (Diptera, Psychodidae) of Serra da Cantareira, Greater São Paulo Metropolitan region, state of São Paulo, Brazil. Rev Bras Epi 16(1):190–201CrossRefGoogle Scholar
  132. Naiff RD, Freitas RA, Naiff MF, Arias JR, Barrett TV, Momen H, Grimaldi Junior G (1991) Epidemiological and nosological aspects of Leishmania naiffi Lainson & Shaw, 1989. Mem Inst Oswaldo Cruz 86:317–321PubMedCrossRefPubMedCentralGoogle Scholar
  133. Nery LCR, Lorosa ES, Franco AMR (2004) Feeding preference of the sand flies Lutzomyia umbratilis and L. spathotrichia (Diptera: Psychodidae, Phlebotominae) in an urban forest patch in the city of Manaus, Amazonas, Brazil. Mem Inst Oswaldo Cruz 99(6):571–574PubMedCrossRefPubMedCentralGoogle Scholar
  134. Nieves E, Pimenta PF (2002) Influence of vertebrate blood meals on the development Leishmania (Viannia) braziliensis and Leishmania (Leishmania) amazonensis in the sand fly Lutzomyia migonei (Diptera: Psychodidae). Am J Trop Med Hyg 67(6):640–647PubMedPubMedCentralCrossRefGoogle Scholar
  135. Nunes VLB, Galati EAB, Cardozo C, Rocca MEG, Andrade AROD, Santos MFDC, Aquino RB, Rosa DD (2008) Estudo de flebotomíneos (Diptera, Psychodidae) em área urbana do município de Bonito, Mato Grosso do Sul, Brasil. Rev Bras Entomol 52(3):446–451CrossRefGoogle Scholar
  136. Oliveira DM, Reinhold-Castro KR, Bernal MVZ, Legriffon CMO, Lonardoni MVC, Teodoro U, Silveira TGV (2011) Natural infection of Nyssomyia neivai by Leishmania (Viannia) spp in the state of Paraná, southern Brazil, detected by multiplex polymerase chain reaction. Vector Borne Zoonotic Dis 11:137–143PubMedCrossRefPubMedCentralGoogle Scholar
  137. Oliveira MR, Macedo VO, de Carvalho EM, Barral A, Marotti JG, Bittencourt A, de Abreu MV, Orge M de La G, Lessa Hde A, Marsden PD (1995) An evolutionary study of mucosal leishmaniasis (a 7 to 17-year follow-up) due to Leishmania (Viannia) braziliensis in Três Braços, Bahia. Rev Soc Bras Med Trop 28:325–332PubMedCrossRefPubMedCentralGoogle Scholar
  138. Passos VNA, Silva RE, Falcão AL (1991) Fauna flebotomínica de municípios da região metropolitana de Belo Horizonte. Rev Soc Bras Med Trop 24(Suppl. 11):107Google Scholar
  139. Patz JA, Thaddeus KG, Geller N, Vittor AY (2000) Effects of environmental change on emerging parasitic diseases. Int J Parasitol 30:1395–1405PubMedCrossRefPubMedCentralGoogle Scholar
  140. Pereira Filho AA, Bandeira MDCA, Fonteles RS, Moraes JLP, Lopes CRG, Melo MN, Rebêlo JMM (2015) An ecological study of sand flies (Diptera: Psychodidae) in the vicinity of Lençóis Maranhenses National Park, Maranhão, Brazil. Parasit Vect 8(1):442CrossRefGoogle Scholar
  141. Pessôa SB, Pestana BR (1940) Infecção natural de “Phlebotomus migonei” por formas em leptomonas provavelmente da “Leishmania brasiliensis”. Acta Méd Rio de Janeiro 5:106–111Google Scholar
  142. Pessôa SB, Coutinho JO (1941) Infecção natural e experimental dos flebótomos pela Leishmania braziliensis no estado de São Paulo. Hospital 20:25–35Google Scholar
  143. Peterson AT, Shaw J (2003) Lutzomyia vectors for cutaneous leishmaniasis in Southern Brazil: ecological niche models, predicted geographic distributions and climate change effects. Int J Parasitol 33:919–931PubMedCrossRefPubMedCentralGoogle Scholar
  144. Pinheiro MPG, da Silva JHT, Inacio CLS, de Melo MDFF (2016a) Anthropophily of Lutzomyia wellcomei (Diptera: Psychodidae) in an Atlantic Forest Conservation Unit in Northeast Brazil. J Med Entomol 53(6):1444–1448PubMedCrossRefPubMedCentralGoogle Scholar
  145. Pinheiro MPG, Silva JHT, Cavalcanti KB, de Azevedo PRM (2013) Ecological interactions among phlebotomines (Diptera: Psychodidae) in an agroforestry environment of northeast Brazil. J Vect Ecol 38(2):307–316CrossRefGoogle Scholar
  146. Pinheiro MPG, de Medeiros Silva MM, Júnior JBS, da Silva JHT, de Lima AM, De Melo MDFF (2016b) Sand flies (Diptera, Psychodidae, Phlebotominae), vectors of Leishmania protozoa, at an Atlantic Forest Conservation Unit in the municipality of Nísia Floresta, Rio Grande do Norte state, Brazil. Parasit Vect 9(1):83CrossRefGoogle Scholar
  147. Pirmez C, Oliveira-Neto MP, Franco A, Meneses C, Rangel E, Mayrink A, Gonçalves AJ, Fernandes O, Grimaldi G (1997) Edentates as a possible reservoir of L. (V.) braziliensis in an endemic area of Rio de Janeiro. Mem Inst Oswaldo Cruz 92(Suppl. I):119Google Scholar
  148. Pita-Pereira D, Alves CR, Souza MB, Brazil RP, Bertho AL, Figueiredo AB, Britto CC (2005) Identification of naturally infected Lutzomyia intermedia and Lutzomyia migonei with Leishmania (Viannia) braziliensis in Rio de Janeiro (Brazil) revealed by a PCR multiplex non-isotopic hybridisation assay. Trans R Soc Trop Med Hyg 99:905–913PubMedCrossRefPubMedCentralGoogle Scholar
  149. Pita-Pereira D, Souza GD, Araújo Pereira T, Zwetsch A, Britto C, Rangel EF (2011) Lutzomyia (Pintomyia) fischeri (Diptera: Psychodidae: Phlebotominae), a probable vector of American cutaneous leishmaniasis: detection of natural infection by Leishmania (Viannia) DNA in specimens from the municipality of Porto Alegre (RS), Brazil, using multiplex PCR assay. Acta Trop 120(3):273–275PubMedCrossRefPubMedCentralGoogle Scholar
  150. Pita-Pereira D, Souza GD, Zwetsch A, Alves CR, Britto C, Rangel EF (2009) First report of Lutzomyia (Nyssomyia) neivai (Diptera: Psychodidae: Phlebotominae) naturally infected by Leishmania (Viannia) braziliensis in a periurban area of South Brazil using a multiplex polymerase chain reaction assay. Am J Trop Med Hyg 80:593–595PubMedPubMedCentralCrossRefGoogle Scholar
  151. Queiroz MFM, Varjão JR, Moraes SCD, Salcedo GE (2012) Analysis of sandflies (Diptera: Psychodidae) in Barra do Garças, State of Mato Grosso, Brazil, and the influence of environmental variables on the vector density of Lutzomyia longipalpis (Lutz & Neiva, 1912). Rev Soc Bras Med Trop 45(3):313–317PubMedPubMedCentralCrossRefGoogle Scholar
  152. Queiroz RG, Vasconcelos IA, Vasconcelos AW, Pessoa FA, Souza RN, David JR (1994) Cutaneous leishmaniasis in Ceará state in Northeasten Brazil: incrimination of Lutzomyia whitmani (Diptera: Psychodidae) as a vector of Leishmania braziliensis in Baturité municipality. Ann J Trop Med Hyg 50:693–698CrossRefGoogle Scholar
  153. Rangel EF (1995) Tropical Diseases, Society and the Environment. SAREC Documentation/TDR, pp 103–110Google Scholar
  154. Rangel EF, Costa SM, Carvalho BM (2014) Environmental changes and the geographic spreading of American cutaneous leishmaniasis in Brazil. In: Claborn D (ed) Leishmaniasis–trends in epidemiology, diagnosis and treatment. InTech, RijekaGoogle Scholar
  155. Rangel EF, Lainson R (2003) Transmissores de Leishmaniose Tegumentar Americana. In: Elizabeth Rangel & Ralph Lainson (org.). Flebotomíneos do Brasil. Editora Fiocruz, Rio de Janeiro, pp 291–310Google Scholar
  156. Rangel EF, Lainson R (2009) Proven and putative vectors of American cutaneous leishmaniasis in Brazil: aspects of their biology and vectorial competence. Mem Inst Oswaldo Cruz 104(7):937–954PubMedPubMedCentralCrossRefGoogle Scholar
  157. Rangel EF, Ryan L, Lainson R, Shaw JJ (1985) Observations on the sandfly (Diptera: Psychodidae) fauna of Além Paraiba, State of Minas Gerais, Brazil, and the isolation of a parasite of the Leishmania braziliensis complex from Psychodopygus hirsuta hirsuta. Mem Inst Oswaldo Cruz 80:373–374PubMedCrossRefPubMedCentralGoogle Scholar
  158. Rangel EF, Azevedo ACR, Andrade CA, Souza NA, Wermelinger ED (1990) Studies on sand fly fauna (Diptera: Psychodidae) in a foci of cutaneous leishmaniasis in Mesquita, Rio de Janeiro state, Brazil. Mem Inst Oswaldo Cruz 85:39–45PubMedCrossRefPubMedCentralGoogle Scholar
  159. Rangel EF, Azevedo ACR, Orosko S, Lima JB, Souza NA, Pereira T, Meneses CRV, Costa WA, Cupollilo E, Brahim L (1998) Lutzomyia (Nyssomyia) umbratilis (Ward & Fraiha, 1977) and the ecology of American cutaneous leishmaniasis in Mato Grosso state. I Bienal de Pesquisa da Fundação Oswaldo Cruz, Fiocruz, Rio de Janeiro, 122 ppGoogle Scholar
  160. Rangel EF, Meneses CRV, Cupolillo E, Azevedo ACR, Costa WA, Costa SM (1999) Aspectos da ecologia de Lutzomyia intermedia (Lutz & Neiva, 1912) e a fauna flebotomínica (Diptera: Psychodidae) em área de transmissão da Leishmania (V.) braziliensis no Rio de Janeiro. Rev Soc Bras Med Trop 32(Suppl. 1):115Google Scholar
  161. Rangel EF, Souza NA, Wermelinger ED, Barbosa AF, Andrade CA (1986) Biology of Lutzomyia intermedia Lutz & Neiva, 1912 and Lutzomyia longipalpis Lutz & Neiva, 1912 (Diptera: Psychodidae) under experimental conditions. I. Feeding aspects of larvae and adults. Mem Inst Oswaldo Cruz 81:431–438PubMedCrossRefGoogle Scholar
  162. Rangel EF, Lainson R, Souza AA, Ready P, Azevedo ACR (1996) Variation between geographical populations of Lutzomyia (Nyssomyia) whitmani (Antunes & Coutinho, 1939) sensu lato (Diptera: Psychodidae: Phlebotominae) in Brazil. Mem Inst Oswaldo Cruz 91:43–50PubMedPubMedCentralCrossRefGoogle Scholar
  163. Rangel EF, Barbosa AF, Andrade CA, Souza NA, Wermelinger ED (1992) Development of Leishmania (Viannia) braziliensis Viannia, 1991 in Lutzomyia intermedia (Lutz & Neiva, 1912) (Diptera: Psychodidae) under experimental conditions. Mem Inst Oswaldo Cruz 87:235–238PubMedCrossRefPubMedCentralGoogle Scholar
  164. Ready P (2008) Leishmaniasis emergence and climate change. Rev Sci Tech L’Off Int Epiz 27(2):399–412CrossRefGoogle Scholar
  165. Ready PD, Fraiha H, Lane RP, Arias JR, Pajot FX (1982) On distinguishing the female of Psychodopygus wellcomei, a vector of mucocutaneous leishmaniasis, from other squamiventris series females. I. Characterization of Ps. squamiventris squamiventris and Ps. s. maripaensis stat. nov. (Diptera: psychodidae). Ann Trop Med Parasitol 76:201–214PubMedCrossRefPubMedCentralGoogle Scholar
  166. Ready PD, Lainson R, Shaw JJ (1983) 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 eastern Amazonia. Trans R Soc Trop Med Hyg 77:775–785PubMedCrossRefPubMedCentralGoogle Scholar
  167. Ready PD, Lainson R, Shaw JJ (1984) Habitat and seasonality of Psychodopygus wellcomei help incriminate it as a vector of Leishmania in Amazônia and Northeast Brazil. Trans R Soc Trop Hyg 78:543–544CrossRefGoogle Scholar
  168. Ready PD, Lainson R, Shaw JJ, Souza AA (1991) DNA probes for distinguishing Psychodopygus wellcomei from Psychodopygus complexux (Diptera: Psychodidae). Mem Inst Oswaldo Cruz 86:41–49PubMedPubMedCentralCrossRefGoogle Scholar
  169. Ready PD, Lainson R, Shaw JJ, Ward D (1986) The ecology of Lutzomyia umbratilis (Ward & Fraiha, 1977) (Diptera: Psychodiade), the major vector to man of Leishmania braziliensis guyanensis in north-eastern Amazonian Brazil. Bull Entomol Res 76:21–40CrossRefGoogle Scholar
  170. Ready PD, Day JC, Souza AA, Rangel EF, Davies CR (1997) Mitochondrial DNA characterization of populations of Lutzomyia whitmani (Diptera: Psychodiade) incriminated in the peridomestic and silvatic transmission of Leishmania species in Brazil. Bull Ent Res 87:187–195CrossRefGoogle Scholar
  171. Ready PD, Souza AA, Rebêlo JMM, Day JC, Silveira FT, Campbell-Lendum D, Davies CR, Costa JML (1998) Phylogenetic species and domesticity of Lutzomyia whitmani at the south-east boundary of Amazonian Brazil. Bull Entomol Res 87:187–195CrossRefGoogle Scholar
  172. Rebêlo JMM, Júnior A, Nascimento A, Silva O, Moraes JLP (2010) Occurrence of sand flies (Diptera, Psychodidae) in leishmaniasis foci in an ecotourism area around the Lençóis Maranhenses National Park, Brazil. Cad Saude Publ 26(1):195–198CrossRefGoogle Scholar
  173. Rocha LS, Falqueto A, dos Santos CB, Ferreira AL, da Graça GC, Grimaldi G, Cupolillo E (2010) Survey of natural infection by Leishmania in sand fly species collected in southeastern Brazil. Trans R Soc Trop Med Hyg 104(7):461–466PubMedCrossRefPubMedCentralGoogle Scholar
  174. Rocha NMM, Melo MN, Babá EH, Dias M, Michalick MSM, Da Costa CA, Williams P, Mayrink W (1988) Leishmania braziliensis braziliensis isolated from Akodon arviculoides captured in Ca-ratinga, Minas Gerais, Brazil. Trans R Soc Trop Med Hyg 82:68PubMedCrossRefPubMedCentralGoogle Scholar
  175. Rodrigues ACM, Melo LM, Magalhães RD, de Moraes NB, Júnior ADS, Bevilagua CML (2016) Molecular identification of Lutzomyia migonei (Diptera: Psychodidae) as a potential vector for Leishmania infantum (Kinetoplastida: Trypanosomatidae). Veterinary Parasitogy 220:28–32CrossRefGoogle Scholar
  176. Ryan L, Lainson R, Shaw JJ (1987a) Leishmaniasis in Brazil. XXIV. Natural flagellate infections of sandflies (Diptera: Psychodidae) in Pará state, with particular reference to the role of Psychodopygus wellcomei as the vector of Leishmania braziliensis braziliensis in the Serra dos Carajás. Trans R Soc Trop Med Hyg 81:353–359CrossRefPubMedGoogle Scholar
  177. Ryan L, Lainson R, Shaw JJ, Braga RR, Ishikawa EA (1987b) Leishmaniasis in Brazil. XXV. Sandfly vectors of Leishmania in Pará State, Brazil. Med Vet Entomol 1:383–395CrossRefPubMedGoogle Scholar
  178. Ryan L, Vexenet A, Marsden PD, Lainson R (1990) The importance of rapid diagnoses of new cases of cutaneous leishmaniasis in pinpointing the sand fly vector. Trans R Soc Trop Med Hyg 84:786PubMedCrossRefPubMedCentralGoogle Scholar
  179. Scarpassa VM, Alencar RB (2012) Lutzomyia umbratilis, the main vector of Leishmania guyanensis, represents a novel species complex? PLoS One 7(5):e37341PubMedPubMedCentralCrossRefGoogle Scholar
  180. Scarpassa VM, Alencar RB (2013) Molecular taxonomy of the two Leishmania vectors Lutzomyia umbratilis and Lutzomyia anduzei (Diptera: Psychodidae) from the Brazilian Amazon. Parasit Vect 6(1):258CrossRefGoogle Scholar
  181. Sergent ED, Sergent ET, Parrot L, Donatieu A, Béguet M (1921) Transmission du clou de Biskra par le phlébotome (Phlebotomus papatasi Scop.) C R Acad Sci 173:1030–1032Google Scholar
  182. Shaw J (2007) The leishmaniases – survival and expansion in a changing world. A mini- review. Mem Inst Oswaldo Cruz 102:541–547PubMedCrossRefPubMedCentralGoogle Scholar
  183. Shaw J (2008) How climatic and environmental variations affect the eco-epidemiology of the leishmaniases and their control. III Workshop de Genética e Biologia Molecular de Insetos Vetores de Doenças Tropicais, 13 ppGoogle Scholar
  184. Shaw JJ, Ishikawa EAY, Lainson R, Braga RR, Silveira FT (1991) Cutaneous leishmaniasis of man due to Leishmania (Viannia) shawi Lainson, de Souza, Póvoa, Ishikawa & Silveira in Pará state, Brazil. Ann Parasitol Hum Comp 66:243–246PubMedCrossRefPubMedCentralGoogle Scholar
  185. Shaw JJ, Lainson R (1968) Leishmaniasis in Brazil: II. Observations on enzootic rodent 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 62:396–405PubMedCrossRefPubMedCentralGoogle Scholar
  186. Shaw JJ, Lainson R (1972) Leishmaniasis in Brazil: VI. Observations on the seasonal variations of Lutzomyia flaviscutellata in different types of forest and its relationship to enzootic rodent leishmaniasis (Leishmania mexicana amazonensis). Trans Roy Soc Trop Med Hyg 66(5):709–717PubMedCrossRefPubMedCentralGoogle Scholar
  187. Shaw JJ, Lainson R, Ryan L, Braga RR, Me-Mahon-Pratt D, David JR (1987) Leishmaniasis in Brazil. XXII. The identification of Leishmania braziliensis braziliensis in wild-caught neotropical sand flies using monoclonal antibodies. Trans R Soc Trop Med Hyg 81:69–72CrossRefPubMedGoogle Scholar
  188. Shaw JJ, Lainson R, Ward RD (1972) Leishmaniasis in Brazil. VII. Further observations on the feeding habitats of Lutzomyia flaviscutellata (Mangabeira) with particular reference to its biting habits at different heights. Trans R Soc Trop Med Hyg 66:718–723PubMedCrossRefPubMedCentralGoogle Scholar
  189. Shaw JJ, de Faria DL, Basano SA, Corbett CE, Rodrigues CJ, Ishikawa EA, Camargo LM (2007) The aetiological agents of American cutaneous leishmaniasis in the municipality of Monte Negro, Rondônia state, western Amazonia, Brazil. AnnTrop Med Parasitol 101:681–688CrossRefGoogle Scholar
  190. Sherlock I, Carneiro M (1962) Algumas fêmeas de Phlebotomus do Brasil (Diptera: Psychodidae). Mem Inst Oswaldo Cruz 60:423–435PubMedCrossRefPubMedCentralGoogle Scholar
  191. Silva AM, de Camargo NJ, dos Santos DR, Massafera R, Ferreira AC, Postai C, Cristóvão EC, Konolsaisen JF, Bisetto A Jr, Perinazo R, Teodoro U, Galati EA (2008) Diversity, distribution and abundance of sand flies (Diptera: Psychodidae) in Paraná state, Southern Brazil. Neotrop Entomol 37:209–225PubMedPubMedCentralCrossRefGoogle Scholar
  192. Silva DF, Vasconcelos SD (2005) Phlebotomine sand flies in fragments of rain forest in Recife, Pernambuco state. Rev Soc Bras Med Trop 38:264–266PubMedCrossRefPubMedCentralGoogle Scholar
  193. Silva DT, Starke-Buzetti WA, Alves-Martin MF, Paixão MS, Tenório MS, Lopes MLM (2014a) Comparative evaluation of several methods for Canine Visceral Leishmaniasis diagnosis. Rev Bras Parasitol Vet 23(2):179–186PubMedCrossRefPubMedCentralGoogle Scholar
  194. Silva TR, Assis MD, Freire MP, Rego FD, Gontijo CM, Shimabukuro PH (2014b) Molecular detection of Leishmania in sand flies (Diptera: Psychodidae: Phlebotominae) collected in the Caititu Indigenous Reserve of the Municipality of Lábrea, State of Amazonas, Brazil. J Med Entomol 51:1276–1282PubMedCrossRefPubMedCentralGoogle Scholar
  195. Silveira FT, Souza AA, Lainson R, Shaw JJ, Braga RR, Ishikawa EE (1991) Cutaneous leishmaniasis in the Amazon region: natural infection of the sandfly Lutzomyia ubiquitalis (Psychodidae: Phlebotominae) by Leishmania (Viannia) lainsoni in Pará State, Brazil. Mem Inst Oswaldo Cruz 86:127–130CrossRefPubMedGoogle Scholar
  196. Souza CM, Pessanha JE, Barata RA, Monteiro EM, Costa DC, Dias ES (2004) Study on phlebotomine sand fly (Diptera: Psychodidae) fauna in Belo Horizonte, state of Minas Gerais, Brazil. Mem Inst Oswaldo Cruz 99:795–803PubMedCrossRefPubMedCentralGoogle Scholar
  197. Souza Freitas MT, Ríos-Velasquez CM, Costa CRL, Figueirêdo CAS, Aragão NC, da Silva LG, Batista MVA, Balbino TCL, Pessoa FAC, Queiroz BV (2015) Phenotypic and genotypic variations among three allopatric populations of Lutzomyia umbratilis, main vector of Leishmania guyanensis. Parasit Vect 8(1):448CrossRefGoogle Scholar
  198. Souza Freitas MT, Ríos-Velasquez CM, da Silva LG, Costa CRL, Marcelino A, Leal-Balbino TC, Balbino VQ, Pessoa FAC (2016) Analysis of the genetic structure of allopatric populations of Lutzomyia umbratilis using the period clock gene. Acta Trop 154:149–154PubMedPubMedCentralCrossRefGoogle Scholar
  199. Souza MB, Cardoso PG, Sanavria A, Marzochi MCA, de Carvalho RW, Ribeiro PC, Ponte CS, Meira AM, Meródio JC (2003) Fauna flebotomínica do município de Bom Jardim, Região Serrana do estado do Rio de Janeiro, Brasil. Rev Bras Parasitol Vet 12:150–153Google Scholar
  200. Souza NA, Andrade-Coelho CA, Vilela ML, Peixoto AA, Rangel EF (2002) Seasonality of Lutzomyia intermedia and Lutzomyia whitmani (Diptera: Psychodidae: Phlebotominae), occurring sympatrically in area of cutaneous leishmaniasis in the state of Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz 97:759–765PubMedCrossRefPubMedCentralGoogle Scholar
  201. Souza NA, Vilela ML, Andrade-Coelho CA, Rangel EF (2001) The Phlebotominae sand fly (Diptera: Psychodidae) fauna of two Atlantic Rain Forest Reserves in the state of Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz 96:319–324PubMedCrossRefPubMedCentralGoogle Scholar
  202. Souza-Rocha L, Falqueto A, dos Santos CB, Grimaldi G Jr, Cupolillo E (2007) Genetic structure of Lutzomyia (Nyssomyia) intermedia population from two ecologic regions in Brazil where transmission of Leishmania (Viannia) braziliensis reflects distinct eco-epidemiologic features. Am J Trop Med Hyg 76:559–565PubMedPubMedCentralCrossRefGoogle Scholar
  203. Teodoro U, Salvia Filho VL, de Lima EM, Spinosa RP, Barbosa OC, Ferreira MEMC, Verzignassi TG (1993) Flebotomíneos em áreas de transmissão de leishmaniose na região norte do estado do Paraná - Brasil: variação sazonal e atividade noturna. Rev Saude Publica 27:190–194PubMedCrossRefPubMedCentralGoogle Scholar
  204. Teodoro U, Silveira TG, dos Santos DR, dos Santos ES, dos Santos AR, de Oliveira O, Kuhl JB, Alberton D (2003) Influence of rearrangement and cleaning of the peridomiciliary area and building disinsectization on sand fly population density in the municipality of Doutor Camargo, Paraná state, Brazil. Cad Saude Publica 19:1801–1813PubMedCrossRefPubMedCentralGoogle Scholar
  205. Tojal da Silva AC, Cupolillo E, Volpini AC, Almeida R, Romero GA (2006) Species diversity causing human cutaneous leishmaniasis in Rio Branco, State of Acre, Brazil. Tropical Med Int Health 11:1388–1398CrossRefGoogle Scholar
  206. Vexenat JA, Barretto AC, Rosa AC (1986) Infecção experimental de Lutzomyia whitmani em cães infectados com Leishmania braziliensis braziliensis. Inst Oswaldo Cruz 81:125–126CrossRefGoogle Scholar
  207. Vieira VR, Azevedo ACR, Alves JRC, Guimarães AE, Aguiar GM (2015) Ecological aspects of phlebotomine sand flies (Diptera, Psychodidae, Phlebotominae) in areas of American Cutaneous Leishmaniasis, in the Municipality of Paraty, Rio de Janeiro, Brazil. I-index of abundance by location and type of capture. J Med Entomol 52(5):886–895PubMedPubMedCentralCrossRefGoogle Scholar
  208. Vilela ML, Azevedo ACR, Costa SM, Costa WA, Silva DM, Grajauskas AM, Moreira-de-Carvalho B, Paes LRDNB, Kozlowsky D, Rangel EF (2008) Sand fly survey in the influence área of Peixe Angical Hydroelectric Plant, state of Tocantins, Brazil. In: 6th International Symposium on Phlebotomine Sandflies, Lima, 95 ppGoogle Scholar
  209. Vilela ML, Azevedo ACR, Afonso MMS, Silva DM, Rangel EF (2006) Estudos dos vetores das leishmanioses na área de influência do Aproveitamento Hidroelétrico Peixe Angical, estado de Tocantins. XLII Congresso da Sociedade Brasileira de Medicina Tropical. Rev Soc Bras Med Trop 39(Suppl. I):76Google Scholar
  210. Vilela ML, Azevedo ACR, Motta-Silva D, Costa WA, Rangel EF (2007) Estudos dos vetores das leishmanioses em áreas de influência do Aproveitamento Hidroelétrico Peixe Angical, estado de Tocantins. XLIII Congresso da Sociedade Brasileira de Medicina Tropical. Rev Soc Bras Med Trop 40(Suppl. I):127Google Scholar
  211. Vilela ML, Azevedo CG, Carvalho BM, Rangel EF (2011) Phlebotomine fauna (Diptera: Psychodidae) and putative vectors of leishmaniases in impacted area by hydroelectric plant, state of Tocantins, Brazil. PLoS One 6(12):e27721PubMedPubMedCentralCrossRefGoogle Scholar
  212. Vilela ML, Pita-Pereira D, Azevedo AC, Godoy RE, Britto C, Rangel EF (2013) The phlebotomine fauna (Diptera: Psychodidae) of Guaraí, state of Tocantins, with an emphasis on the putative vectors of American cutaneous leishmaniasis in rural settlement and periurban areas. Mem Inst Oswaldo Cruz 108(5):578–585PubMedPubMedCentralCrossRefGoogle Scholar
  213. Walsh JF, Molyneux DH, Birley MH (1993) Deforestation: effects on vector-borne disease. Parasitology 106(Suppl):55–75CrossRefGoogle Scholar
  214. Ward RD, Fraiha H (1977) Lutzomyia umbratilis, a new species of sand fly from Brazil (Diptera: Psychodidae). J Med Entomol 14:313–317CrossRefGoogle Scholar
  215. Ward RD, Lainson R, Shaw JJ (1973a) Further evidence of the role of Lutzomyia flaviscutellata (Mangabeira) as the vector of Leishmania mexicana amazonensis in Brazil. Trans R Soc Trop Med Hyg 67:608–609PubMedCrossRefPubMedCentralGoogle Scholar
  216. Ward RD, Lainson R, Shaw JJ (1977) Experimental transmissions of Leishmania mexicana amazonensis Lainson & Shaw, between hamsters by the bite of Lutzomyia flaviscutellata (Mangabeira). Trans R Soc Trop Med Hyg 71:265–266PubMedCrossRefPubMedCentralGoogle Scholar
  217. Ward RD, Shaw JJ, Lainson R, Fraiha H (1973b) Leishmaniasis in Brazil. VIII. Observations on the phlebotomine fauna of an area highly endemic for cutaneous leishmaniasis in the Serra dos Carajás, Pará state. Trans R Soc Trop Med Hyg 67:174–183PubMedPubMedCentralCrossRefGoogle Scholar
  218. WHO (2010) World Health Organization. Control of the leishmaniases: report of a meeting of the WHO Expert Committee on the Control of Leishmaniases, Geneva, 22–26 March 2010 (WHO Technical Report Series, n° 949). WHO Press, GenebraGoogle Scholar
  219. Wijers DJB, Linger R (1966) Man-biting sand flies in Surinam (Dutch Guiana): Phlebotomus anduzei as a possible vector of Leishmania braziliensis. Ann Trop Med Parasitol 60:501–508CrossRefGoogle Scholar
  220. Wilkes TJ, Ready PD, Lainson R, Killick-Kendrick R (1984) Biting periodicities of nulliparous and parous females of Psychodopygus wellcomei. Trans R Soc Trop Med Hyg 78:846–847PubMedCrossRefPubMedCentralGoogle Scholar
  221. Woodward A, Smith KR, Campbell-Lendrum D, Chadee DD, Honda Y, Liu Q, Olwoch J, Revich B, Sauerborn R, Chafe Z, Confalonieri U, Haines A (2014) Climate change and health: on the latest IPCC report. Lancet 383:1185–1189PubMedCrossRefPubMedCentralGoogle Scholar
  222. Young DC, Duncan NA (1994) Guide to the identification and geographic distribution of Lutzomyia sand flies in México, the West Indies, Central and South America (Diptera: Psychodidae). Mem Ann Entomol Institut 54:1–881Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Elizabeth F. Rangel
    • 1
  • Ralph Lainson
    • 2
  • Bruno M. Carvalho
    • 1
  • Simone M. Costa
    • 1
  • Jeffrey J. Shaw
    • 3
  1. 1.Instituto Oswaldo CruzFundação Oswaldo CruzRio de JaneiroBrazil
  2. 2.Instituto Evandro ChagasBelémBrazil
  3. 3.Instituto de Ciências Biomédicas, Universidade de São PauloSão PauloBrazil

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