The genetic structure of leishmania infantum populations in Brazil and its possible association with the transmission cycle of visceral leishmaniasis

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Ferreira, Gabriel Eduardo Melim ^a   dos Santos, Barbara Neves ^a   Dorval, Maria Elizabeth Cavalheiros ^b   Ramos, Tereza Pompilio Bastos ^c   Porrozzi, Renato ^a   Peixoto, Alexandre Afranio ^a   Cupolillo, Elisa ^a  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b FEDERAL UNIVERSITY OF MATO GROSSO DO SUL   (Brazil)

^c Superintendência de Vigilância em Saúde   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ARGENTINA; ARTICLE; BACTERIAL STRAIN; BRAZIL; CLUSTER ANALYSIS; DEPLETION; DISEASE CARRIER; DISEASE TRANSMISSION; GENE LOCUS; GENETIC VARIABILITY; GENOTYPE; GEOGRAPHIC DISTRIBUTION; HUMAN; INBREEDING; LEISHMANIA INFANTUM; LUTZOMYIA; LUTZOMYIA CRUZI; NONHUMAN; PARAGUAY; PARASITE TRANSMISSION; POPULATION GENETIC STRUCTURE; POPULATION STRUCTURE; VISCERAL LEISHMANIASIS; ANIMAL; ANIMAL DISEASE; DOG; DOG DISEASE; GENETICS; ISOLATION AND PURIFICATION; PARASITOLOGY; PATHOGENICITY; PHYLOGENY; POPULATION GENETICS;

CANIS FAMILIARIS; LEISHMANIA INFANTUM; LUTZOMYIA CRUZI;

MICROSATELLITE DNA; PROTOZOAL DNA;

ANIMALS; BRAZIL; DNA, PROTOZOAN; DOG DISEASES; DOGS; GENETIC VARIATION; GENETICS, POPULATION; HUMANS; INBREEDING; LEISHMANIA INFANTUM; LEISHMANIASIS, VISCERAL; MICROSATELLITE REPEATS; PHYLOGENY;

EID: 84860998532     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0036242     Document Type: Article

References (91)

1. WHO, (2010) Control of the leishmaniases: report of a meeting of the WHO Expert Commitee on the Control of Leishmaniases. Geneva: World Health Organization. xiii: 186.
2. Lainson R, Shaw JJ, (1987) The Leishmaniases in Biology and Medicine: Evolution, classification and geographical distribution; Peters W, Killick-Kendrick R, editors. London Academic Press pp. 1-120.
3. Rioux JA, Lanotte G, Serres E, Pratlong F, Bastien P, et al. (1990) Taxonomy of Leishmania. Use of isoenzymes. Suggestions for a new classification. Ann Parasitol Hum Comp 65: 111-125.
4. Kuhls K, Alam MZ, Cupolillo E, Ferreira GE, Mauricio IL, et al. (2011) Comparative microsatellite typing of New World Leishmania infantum reveals low heterogeneity among populations and its recent Old World origin. PLoS Negl Trop Dis 5: e1155.
5. Cunha AMU, (1938) Infecções experimentaes na Leishmaniose visceral americana. Memórias do Instituto Oswaldo Cruz 33: 581-598.
6. Killick-Kendrick R, Molyneux DH, Rioux JA, Lanotte G, Leaney AJ, (1980) Possible origins of Leishmania chagasi. Ann Trop Med Parasitol 74: 563-565.
7. Momen H, Grimaldi Junior G, Deane LM, (1987) Leishmania infantum, the aetiological agent of American visceral leishmaniasis (AVL)? Mem Inst Oswaldo Cruz 82: 447-448.
8. Momen H, Pacheco RS, Cupolillo E, Grimaldi Junior G, (1993) Molecular evidence for the importation of Old World Leishmania into the Americas. Biol Res 26: 249-255.
9. Shaw JJ, (1994) Taxonomy of the genus Leishmania: present and future trends and their implications. Mem Inst Oswaldo Cruz 89: 471-478.
10. Grimaldi G Jr, Tesh RB, McMahon-Pratt D, (1989) A review of the geographic distribution and epidemiology of leishmaniasis in the New World. Am J Trop Med Hyg 41: 687-725.
11. Romero GA, Boelaert M, (2010) Control of visceral leishmaniasis in Latin America - a systematic review. PLoS Negl Trop Dis 4: e584.
12. Rosypal AC, Troy GC, Zajac AM, Duncan RB Jr, Waki K, et al. (2003) Emergence of zoonotic canine leishmaniasis in the United States: isolation and immunohistochemical detection of Leishmania infantum from foxhounds from Virginia. J Eukaryot Microbiol 50 Suppl pp. 691-693.
13. Werneck GL, (2010) Geographic spread of visceral leishmaniasis in Brazil. Cad Saude Publica 26: 644-645.
14. Alexander B, de Carvalho RL, McCallum H, Pereira MH, (2002) Role of the domestic chicken (Gallus gallus) in the epidemiology of urban visceral leishmaniasis in Brazil. Emerg Infect Dis 8: 1480-1485.
15. Jeronimo SM, Oliveira RM, Mackay S, Costa RM, Sweet J, et al. (1994) An urban outbreak of visceral leishmaniasis in Natal, Brazil. Trans R Soc Trop Med Hyg 88: 386-388.
16. Maia-Elkhoury AN, Alves WA, Sousa-Gomes ML, Sena JM, Luna EA, (2008) Visceral leishmaniasis in Brazil: trends and challenges. Cad Saude Publica 24: 2941-2947.
17. Oliveira AG, Galati EAB, Oliveira O, Oliveira GR, Espindola IAC, et al. (2006) Abundance of Lutzomyia longipalpis (Diptera: Psychodidae: Phlebotominae) and urban transmission of visceral leishmaniasis in Campo Grande, state of Mato Grosso do Sul, Brazil. Memórias do Instituto Oswaldo Cruz 101: 869-874.
18. Rangel EF, Vilela ML, (2008) Lutzomyia longipalpis (Diptera, Psychodidae, Phlebotominae) and urbanization of visceral leishmaniasis in Brazil. Cad Saude Publica 24: 2948-2952.
19. Werneck GL, (2008) Forum: geographic spread and urbanization of visceral leishmaniasis in Brazil. Introduction. Cad Saude Publica 24: 2937-2940.
20. Brazil RP, De Almeida DC, Brazil BG, Mamede SM, (1991) Chicken house as a resting site of sandflies in Rio de Janeiro, Brazil. Parassitologia 33 Suppl pp. 113-117.
21. Deane LM, Deane MP, (1954) Dogs naturally infected by Leishmania donovani in Ceara. Hospital (Rio J) 45: 703-707.
22. Dias FOP, Lorosa ES, Rebêlo JMM, (2003) Fonte alimentar sangüínea e a peridomiciliação de Lutzomyia longipalpis (Lutz & Neiva, 1912) (Psychodidae, Phlebotominae). Cadernos de Saúde Pública 19: 1373-1380.
23. Palatnik-de-Sousa CB, dos Santos WR, Franca-Silva JC, da Costa RT, Reis AB, et al. (2001) Impact of canine control on the epidemiology of canine and human visceral leishmaniasis in Brazil. Am J Trop Med Hyg 65: 510-517.
24. Antonialli SAC, Torres TG, Paranhos Filho AC, Tolezano JE, (2007) Spatial analysis of American Visceral Leishmaniasis in Mato Grosso do Sul State, Central Brazil. J Infect 54: 509-514.
25. Oliveira AL, Paniago AM, Dorval ME, Oshiro ET, Leal CR, et al. (2006) Emergent outbreak of visceral leishmaniasis in Mato Grosso do Sul State. Rev Soc Bras Med Trop 39: 446-450.
26. Oliveira CD, Assuncao RM, Reis IA, Proietti FA, (2001) Spatial distribution of human and canine visceral leishmaniasis in Belo Horizonte, Minas Gerais State, Brasil, 1994-1997. Cad Saude Publica 17: 1231-1239.
27. Silva ES, Gontijo CM, Pacheco RS, Fiuza VO, Brazil RP, (2001) Visceral leishmaniasis in the Metropolitan Region of Belo Horizonte, State of Minas Gerais, Brazil. Mem Inst Oswaldo Cruz 96: 285-291.
28. Souza GD, Santos E, Andrade Filho JD, (2009) The first report of the main vector of visceral leishmaniasis in America, Lutzomyia longipalpis (Lutz & Neiva) (Diptera: Psychodidae: Phlebotominae), in the state of Rio Grande do Sul, Brazil. Mem Inst Oswaldo Cruz 104: 1181-1182.
29. Lainson R, Rangel EF, (2005) Lutzomyia longipalpis and the eco-epidemiology of American visceral leishmaniasis, with particular reference to Brazil: a review. Mem Inst Oswaldo Cruz 100: 811-827.
30. Travi BL, Velez ID, Brutus L, Segura I, Jaramillo C, et al. (1990) Lutzomyia evansi, an alternate vector of Leishmania chagasi in a Colombian focus of visceral leishmaniasis. Trans R Soc Trop Med Hyg 84: 676-677.
31. de Carvalho MR, Valenca HF, da Silva FJ, de Pita-Pereira D, de Araujo Pereira T, et al. (2010) Natural Leishmania infantum infection in Migonemyia migonei (França, 1920) (Diptera:Psychodidae:Phlebotominae) the putative vector of visceral leishmaniasis in Pernambuco State, Brazil. Acta Trop 116: 108-110.
32. de Pita-Pereira D, Cardoso MA, Alves CR, Brazil RP, Britto C, (2008) Detection of natural infection in Lutzomyia cruzi and Lutzomyia forattinii (Diptera: Psychodidae: Phlebotominae) by Leishmania infantum chagasi in an endemic area of visceral leishmaniasis in Brazil using a PCR multiplex assay. Acta Trop 107: 66-69.
33. Missawa NA, Veloso MA, Maciel GB, Michalsky EM, Dias ES, (2011) Evidence of transmission of visceral leishmaniasis by Lutzomyia cruzi in the municipality of Jaciara, State of Mato Grosso, Brazil. Rev Soc Bras Med Trop 44: 76-78.
34. dos Santos SO, Arias J, Ribeiro AA, de Paiva Hoffmann M, de Freitas RA, et al. (1998) Incrimination of Lutzomyia cruzi as a vector of American visceral leishmaniasis. Med Vet Entomol 12: 315-317.
35. Mestre GL, Fontes CJ, (2007) The spread of the visceral leishmaniasis epidemic in the State of Mato Grosso, 1998-2005. Rev Soc Bras Med Trop 40: 42-48.
36. Missawa NA, Lima GB, (2006) Spatial distribution of Lutzomyia longipalpis (Lutz & Neiva, 1912) and Lutzomyia cruzi (Mangabeira, 1938) in the State of Mato Grosso. Rev Soc Bras Med Trop 39: 337-340.
37. Oliveira AG, Andrade Filho JD, Falcão AL, Brazil RP, (2003) Estudo de flebotomíneos (Diptera, Psychodidae, Phlebotominae) na zona urbana da cidade de Campo Grande, Mato Grosso do Sul, Brasil, 1999-2000. Cadernos de Saúde Pública 19: 933-944.
38. Ribeiro AL, Missawa NA, Zeilhofer P, (2007) Distribution of phlebotomine sandflies (Diptera: Psychodidae) of medical importance in Mato Grosso State, Brazil. Rev Inst Med Trop Sao Paulo 49: 317-321.
39. Araki AS, Vigoder FM, Bauzer LG, Ferreira GE, Souza NA, et al. (2009) Molecular and behavioral differentiation among Brazilian populations of Lutzomyia longipalpis (Diptera: Psychodidae: Phlebotominae). PLoS Negl Trop Dis 3: e365.
40. Vigoder FM, Araki AS, Bauzer LG, Souza NA, Brazil RP, et al. (2010) Lovesongs and period gene polymorphisms indicate Lutzomyia cruzi (Mangabeira, 1938) as a sibling species of the Lutzomyia longipalpis (Lutz and Neiva, 1912) complex. Infect Genet Evol 10: 734-739.
41. Watts PC, Hamilton JG, Ward RD, Noyes HA, Souza NA, et al. (2005) Male sex pheromones and the phylogeographic structure of the Lutzomyia longipalpis species complex (Diptera: Psychodidae) from Brazil and Venezuela. Am J Trop Med Hyg 73: 734-743.
42. Banuls AL, Hide M, Prugnolle F, (2007) Leishmania and the leishmaniases: a parasite genetic update and advances in taxonomy, epidemiology and pathogenicity in humans. Adv Parasitol 64: 1-109.
43. Ajzenberg D, Collinet F, Mercier A, Vignoles P, Darde ML, (2010) Genotyping of Toxoplasma gondii isolates with 15 microsatellite markers in a single multiplex PCR assay. J Clin Microbiol 48: 4641-4645.
44. Bruce MC, Macheso A, McConnachie A, Molyneux ME, (2011) Comparative population structure of Plasmodium malariae and Plasmodium falciparum under different transmission settings in Malawi. Malar J 10: 38.
45. Conrad M, Zubacova Z, Dunn LA, Upcroft J, Sullivan SA, et al. (2011) Microsatellite polymorphism in the sexually transmitted human pathogen Trichomonas vaginalis indicates a genetically diverse parasite. Mol Biochem Parasitol 175: 30-38.
46. Hennequin C, Thierry A, Richard GF, Lecointre G, Nguyen HV, et al. (2001) Microsatellite typing as a new tool for identification of Saccharomyces cerevisiae strains. J Clin Microbiol 39: 551-559.
47. Al-Jawabreh A, Diezmann S, Muller M, Wirth T, Schnur LF, et al. (2008) Identification of geographically distributed sub-populations of Leishmania (Leishmania) major by microsatellite analysis. BMC Evol Biol 8: 183.
48. Oddone R, Schweynoch C, Schonian G, Sousa C S, Cupolillo E, et al. (2009) Development of a multilocus microsatellite typing approach for discriminating strains of Leishmania (Viannia) species. J Clin Microbiol 47: 2818-2825.
49. Reale S, Lupo T, Migliazzo A, Di Mauro C, Cipri V, et al. (2010) Multilocus microsatellite polymorphism analysis to characterize Leishmania infantum strains isolated in Sicily. Transbound Emerg Dis 57: 37-41.
50. Rougeron V, Waleckx E, Hide M, T DEM, Arevalo J, et al. (2008) PERMANENT GENETIC RESOURCES: A set of 12 microsatellite loci for genetic studies of Leishmania braziliensis. Mol Ecol Resour 8: 351-353.
51. Russell R, Iribar MP, Lambson B, Brewster S, Blackwell JM, et al. (1999) Intra and inter-specific microsatellite variation in the Leishmania subgenus Viannia. Mol Biochem Parasitol 103: 71-77.
52. Ochsenreither S, Kuhls K, Schaar M, Presber W, Schonian G, (2006) Multilocus microsatellite typing as a new tool for discrimination of Leishmania infantum MON-1 strains. J Clin Microbiol 44: 495-503.
53. Alam MZ, Kovalenko DA, Kuhls K, Nasyrova RM, Ponomareva VI, et al. (2009) Identification of the agent causing visceral leishmaniasis in Uzbeki and Tajiki foci by analysing parasite DNA extracted from patients' Giemsa-stained tissue preparations. Parasitology 136: 981-986.
54. Alam MZ, Kuhls K, Schweynoch C, Sundar S, Rijal S, et al. (2009) Multilocus microsatellite typing (MLMT) reveals genetic homogeneity of Leishmania donovani strains in the Indian subcontinent. Infect Genet Evol 9: 24-31.
55. Amro A, Schonian G, Al-Sharabati MB, Azmi K, Nasereddin A, et al. (2009) Population genetics of Leishmania infantum in Israel and the Palestinian Authority through microsatellite analysis. Microbes Infect 11: 484-492.
56. Chargui N, Amro A, Haouas N, Schonian G, Babba H, et al. (2009) Population structure of Tunisian Leishmania infantum and evidence for the existence of hybrids and gene flow between genetically different populations. Int J Parasitol 39: 801-811.
57. Gelanew T, Cruz I, Kuhls K, Alvar J, Canavate C, et al. (2011) Multilocus microsatellite typing revealed high genetic variability of Leishmania donovani strains isolated during and after a Kala-azar epidemic in Libo Kemkem district, northwest Ethiopia. Microbes Infect 13: 595-601.
58. Gelanew T, Kuhls K, Hurissa Z, Weldegebreal T, Hailu W, et al. (2010) Inference of population structure of Leishmania donovani strains isolated from different Ethiopian visceral leishmaniasis endemic areas. PLoS Negl Trop Dis 4: e889.
59. Kuhls K, Chicharro C, Canavate C, Cortes S, Campino L, et al. (2008) Differentiation and gene flow among European populations of Leishmania infantum MON-1. PLoS Negl Trop Dis 2: e261.
60. Kuhls K, Keilonat L, Ochsenreither S, Schaar M, Schweynoch C, et al. (2007) Multilocus microsatellite typing (MLMT) reveals genetically isolated populations between and within the main endemic regions of visceral leishmaniasis. Microbes Infect 9: 334-343.
61. Seridi N, Amro A, Kuhls K, Belkaid M, Zidane C, et al. (2008) Genetic polymorphism of Algerian Leishmania infantum strains revealed by multilocus microsatellite analysis. Microbes Infect 10: 1309-1315.
62. Leblois R, Kuhls K, Francois O, Schonian G, Wirth T, (2011) Guns, germs and dogs: On the origin of Leishmania chagasi. Infect Genet Evol 11: 1091-1095.
63. Pritchard JK, Stephens M, Donnelly P, (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
64. Evanno G, Regnaut S, Goudet J, (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14: 2611-2620.
65. Jakobsson M, Rosenberg NA, (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23: 1801-1806.
66. Cavalli-Sforza LL, Edwards AW, (1967) Phylogenetic analysis. Models and estimation procedures. Am J Hum Genet 19: 233-257.
67. Goldstein DB, Pollock DD, (1997) Launching microsatellites: a review of mutation processes and methods of phylogenetic interference. J Hered 88: 335-342.
68. Bryant D, Moulton V, (2004) Neighbor-net: an agglomerative method for the construction of phylogenetic networks. Mol Biol Evol 21: 255-265.
69. Huson DH, Bryant D, (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23: 254-267.
70. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F, (1996) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. 4.05 ed. Montpellier.
71. Dieringer D, Schlötterer C, (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Molecular Ecology Notes 3: 167-169.
72. Corander J, Marttinen P, Siren J, Tang J, (2008) Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinformatics 9: 539.
73. Rougeron V, De Meeus T, Hide M, Waleckx E, Bermudez H, et al. (2009) Extreme inbreeding in Leishmania braziliensis. Proc Natl Acad Sci U S A 106: 10224-10229.
74. Rougeron V, De Meeus T, Hide M, Waleckx E, Dereure J, et al. (2010) A battery of 12 microsatellite markers for genetic analysis of the Leishmania (Viannia) guyanensis complex. Parasitology 137: 1879-1884.
75. Nolder D, Roncal N, Davies CR, Llanos-Cuentas A, Miles MA, (2007) Multiple hybrid genotypes of Leishmania (Viannia) in a focus of mucocutaneous Leishmaniasis. Am J Trop Med Hyg 76: 573-578.
76. Nei M, Kumar S, (2000) Molecular evolution and phylogenetics New York: Oxford University Press.
77. Butlin R, (2002) Evolution of sex: The costs and benefits of sex: new insights from old asexual lineages. Nat Rev Genet 3: 311-317.
78. Pouchkina-Stantcheva NN, McGee BM, Boschetti C, Tolleter D, Chakrabortee S, et al. (2007) Functional divergence of former alleles in an ancient asexual invertebrate. Science 318: 268-271.
79. Balloux F, Lehmann L, de Meeus T, (2003) The population genetics of clonal and partially clonal diploids. Genetics 164: 1635-1644.
80. de Meeus T, Balloux F, (2005) F-statistics of clonal diploids structured in numerous demes. Mol Ecol 14: 2695-2702.
81. de Meeus T, Lehmann L, Balloux F, (2006) Molecular epidemiology of clonal diploids: a quick overview and a short DIY (do it yourself) notice. Infect Genet Evol 6: 163-170.
82. Salim B, de Meeus T, Bakheit MA, Kamau J, Nakamura I, et al. (2011) Population genetics of Trypanosoma evansi from camel in the Sudan. PLoS Negl Trop Dis 5: e1196.
83. Tibayrenc M, (1997) Are Candida albicans natural populations subdivided? Trends Microbiol 5: 253-254; discussion 254-257.
84. Tibayrenc M, Kjellberg F, Arnaud J, Oury B, Breniere SF, et al. (1991) Are eukaryotic microorganisms clonal or sexual? A population genetics vantage. Proc Natl Acad Sci U S A 88: 5129-5133.
85. Rougeron V, Banuls AL, Carme B, Simon S, Couppie P, et al. (2011) Reproductive strategies and population structure in Leishmania: substantial amount of sex in Leishmania Viannia guyanensis. Mol Ecol 20: 3116-3127.
86. Botelho AC, Natal D, (2009) First epidemiological description of visceral leishmaniasis in Campo Grande, State of Mato Grosso do Sul. Rev Soc Bras Med Trop 42: 503-508.
87. Nascimento JC, Paiva BR, Malafronte RS, Fernandes WD, Galati EAB, (2007) Natural infection of phlebotomines (Diptera: Psychodidae) in a visceral-leishmaniasis focus in Mato Grosso do Sul, Brazil. Revista do Instituto de Medicina Tropical de São Paulo 49: 119-122.
88. Desjeux P, Aranda E, Aliaga O, Mollinedo S, (1983) Human visceral leishmaniasis in Bolivia: first proven autochthonous case from 'Los Yungas'. Trans R Soc Trop Med Hyg 77: 851-852.
89. Garcia AL, Parrado R, Rojas E, Delgado R, Dujardin JC, et al. (2009) Leishmaniases in Bolivia: comprehensive review and current status. Am J Trop Med Hyg 80: 704-711.
90. Michel G, Pomares C, Ferrua B, Marty P, (2011) Importance of worldwide asymptomatic carriers of Leishmania infantum (L. chagasi) in human. Acta Trop 119: 69-75.
91. Salomon O, Sinagra A, Nevot M, Barberian G, Paulin P, et al. (2008) First visceral leishmaniasis focus in Argentina. Mem Inst Oswaldo Cruz 103: 109-111.