Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-02T21:55:45.106Z Has data issue: false hasContentIssue false
  • English
  • Français

Distinct genetic profiles of Leishmania (Viannia) braziliensis associate with clinical variations in cutaneous-leishmaniasis patients from an endemic area in Brazil

Published online by Cambridge University Press:  12 March 2018

Patrícia Flávia Quaresma ,
Cristiana Ferreira Alves de Brito ,
Jeronimo Marteleto Nunes Rugani ,
Janaína de Moura Freire ,
Rodrigo de Paula Baptista ,
Elizabeth Castro Moreno ,
Raquel Carvalho Gontijo ,
Felipe Dutra Rego ,
Joaquim Edemilson Diniz  and
Maria Norma Melo
...Show all authors
Patrícia Flávia Quaresma*
Affiliation:
Instituto René Rachou, Fundação Oswaldo Cruz, CEP: 30190-002, Belo Horizonte, Minas Gerais, Brazil Departamento de Parasitologia, ICB, Universidade Federal de Minas Gerais, CP: 486 – CEP: 31270-901, Belo Horizonte, Minas Gerais, Brazil
Cristiana Ferreira Alves de Brito
Affiliation:
Instituto René Rachou, Fundação Oswaldo Cruz, CEP: 30190-002, Belo Horizonte, Minas Gerais, Brazil
Jeronimo Marteleto Nunes Rugani
Affiliation:
Instituto René Rachou, Fundação Oswaldo Cruz, CEP: 30190-002, Belo Horizonte, Minas Gerais, Brazil
Janaína de Moura Freire
Affiliation:
Instituto René Rachou, Fundação Oswaldo Cruz, CEP: 30190-002, Belo Horizonte, Minas Gerais, Brazil
Rodrigo de Paula Baptista
Affiliation:
Center for Tropical & Emerging Global Diseases, University of Georgia, 30602-7394, Athens, Georgia, USA
Elizabeth Castro Moreno
Affiliation:
Departamento de Parasitologia, ICB, Universidade Federal de Minas Gerais, CP: 486 – CEP: 31270-901, Belo Horizonte, Minas Gerais, Brazil
Raquel Carvalho Gontijo
Affiliation:
Instituto René Rachou, Fundação Oswaldo Cruz, CEP: 30190-002, Belo Horizonte, Minas Gerais, Brazil
Felipe Dutra Rego
Affiliation:
Instituto René Rachou, Fundação Oswaldo Cruz, CEP: 30190-002, Belo Horizonte, Minas Gerais, Brazil
Joaquim Edemilson Diniz
Affiliation:
Secretaria Municipal de Saúde, CEP: 39475-000, São João das Missões, Minas Gerais, Brazil
Maria Norma Melo
Affiliation:
Departamento de Parasitologia, ICB, Universidade Federal de Minas Gerais, CP: 486 – CEP: 31270-901, Belo Horizonte, Minas Gerais, Brazil
Célia Maria Ferreira Gontijo
Affiliation:
Instituto René Rachou, Fundação Oswaldo Cruz, CEP: 30190-002, Belo Horizonte, Minas Gerais, Brazil
*
Author for correspondence: Patrícia Flávia Quaresma, Centro de Pesquisas René Rachou, Fundação Oswaldo Cruz, CEP: 30190-002, Belo Horizonte, Minas Gerais, Brazil. Tel.: +55 31 3349 7755, fax +55 31 3291 7795 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

American tegumentary leishmaniasis (ATL) samples obtained from the lesions of patients with typical (n = 25, 29%), atypical (n = 60, 69%) or both (n = 2%) clinical manifestations were analysed by multilocus enzyme electrophoresis, hsp70 restriction-fragment length polymorphism (PCR-RFLP), hsp70 sequencing and phylogenetics methods. The hsp70 PCR-RFLP analysis revealed two different profiles whose the most samples differed from those expected for Leishmania braziliensis and the other Leishmania species tested: of 39 samples evaluated, two (5%) had a restriction profile corresponding to L. braziliensis, and 37 (95%) had a restriction profile corresponding to a variant pattern. A 1300-bp hsp70 gene fragment was sequenced to aid in parasite identification and a phylogenetic analysis was performed including 26 consensus sequences from the ATL patient's samples and comparing to other Leishmania and trypanosomatids species. The dendrogram allowed to observe a potential population structure of L. braziliensis complex in the studied region, emphasizing that the majority of clinical samples presented a variant genetic profile. Of interest, the L. braziliensis diversity was associated with different clinical manifestations whose parasites with hsp70 variant profile were associated with atypical lesions. The results may be helpful to improve the diagnosis, treatment and control measures of the ATL in endemic areas.

Keywords

Atypical lesionsBrazilcutaneous leishmaniasishsp70 geneLeishmania braziliensisparasite diversity
Type
Research Article
Information
Parasitology , Volume 145 , Issue 9 , August 2018 , pp. 1161 - 1169
Check for updates
Copyright
Copyright © Cambridge University Press 2018 

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

Aslett, M, Aurrecoechea, C, Berriman, M, Brestelli, J, Brunk, BP, Carrington, M, Depledge, DP, Fischer, S, Gajria, B, Gao, X, Gardner, MJ, Gingle, A, Grant, G, Harb, OS, Heiges, M, Hertz-Fowler, C, Houston, R, Innamorato, F, Iodice, J, Kissinger, JC, Kraemer, E, Li, W, Logan, FJ, Miller, JA, Mitra, S, Myler, PJ, Nayak, V, Pennington, C, Phan, I, Pinney, DF, Ramasamy, G, Rogers, MB, Roos, DS, Ross, C, Sivam, D, Smith, DF, Srinivasamoorthy, G, Stoeckert, CJ Jr, Subramanian, S, Thibodeau, R, Tivey, A, Treatman, C, Velarde, G and Wang, H (2010) TriTrypDB: a functional genomic resource for the Trypanosomatidae. Nucleic Acids Research 38, D457–D462.Google Scholar
Baptista, C, Schubach, AO, Madeira, MF, Leal, CA, Pires, MQ, Oliveira, FS, Conceição-Silva, F, Rosalino, CM, Salgueiro, MM and Pacheco, RS (2009) Leishmania (Viannia) braziliensis genotypes identified in lesions of patients with atypical or typical manifestations of tegumentary leishmaniasis: evaluation by two molecular markers. Experimental Parasitology 121(4), 317–322.Google Scholar
Boite, MC, Mauricio, IL, Miles, MA and Cupolillo, E (2012) New insights on taxonomy, phylogeny and population genetics of Leishmania (Viannia) parasites based on multilocus sequence analysis. PLoS Neglected Tropropical Diseases 6, e1888.Google Scholar
Convit, J, Ulrich, M, Pérez, M, Hung, J, Castillo, J, Rojas, H, Viquez, A, Araya, LN and Lima, HD (2005) Atypical cutaneous leishmaniasis in Central America: possible interaction between infectious and environmental elements. Transactions of the Royal Society of Tropical Medicine and Hygiene 99(1), 13–17.Google Scholar
Costa-Silva, MF, Gomes, LI, Martins-Filho, OA, Rodrigues-Silva, R, Freire, JM, Quaresma, PF, Pascoal-Xavier, MA, Mendes, TA, Serakides, R, Zauli, DA, Campi-Azevedo, AC, Melo, MN, Gontijo, CM, Peruhype-Magalhães, V and Teixeira-Carvalho, A (2014) Gene expression profile of cytokines and chemokines in skin lesions from Brazilian Indians with localized cutaneous leishmaniasis. Molecular Immunology 57(2), 74–85.Google Scholar
Cupolillo, E, Grimaldi, G Jr. and Momen, H (1994). A general classification of New World Leishmania using numerical zymotaxonomy. The American Journal of Tropical Medicine and Hygiene 50, 296–311.Google Scholar
da Silva, LA, de Sousa, CS, da Graça, GC, Porrozzi, R and Cupolillo, E (2010) Sequence analysis and PCR-RFLP profiling of the hsp70 gene as a valuable tool for identifying Leishmania species associated with human leishmaniasis in Brazil. Infection, Genetics and Evolution 10(1), 77–83.Google Scholar
Downing, T, Imamura, H, Decuypere, S, Clark, TG, Coombs, GH, Cotton, JA, Hilley, JD, de Doncker, S, Maes, I, Mottram, JC, Quail, MA, Rijal, S, Sanders, M, Schönian, G, Stark, O, Sundar, S, Vanaerschot, M, Hertz-Fowler, C, Dujardin, JC and Berriman, M (2011) Whole genome sequencing of multiple Leishmania donovani clinical isolates provides insights into the evolution and mechanisms of drug resistance. Genome Research 21(12), 2143–2156.Google Scholar
Garcia, AL, Kindt, A, Bermudez, H, Llanos-Cuentas, A, De Doncker, S, Arevalo, J, Tintaya, KWQ and Dujardin, JC (2004) Culture-independent species typing of neotropical Leishmania for clinical validation of a PCR-based assay targeting Heat Shock Protein 70 genes. Journal of Clinical Microbiology 42, 2294–2297.Google Scholar
Guimarães, LH, Machado, PR, Lago, EL, Morgan, DJ, Schriefer, A, Bacellar, O and Carvalho, EM (2009) Atypical manifestations of tegumentary leishmaniasis in a transmission area of Leishmania braziliensis in the state of Bahia, Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene 103(7), 712–715.Google Scholar
Guimarães, LH, Queiroz, A, Silva, JA, Silva, SC, Magalhães, V, Lago, EL, Machado, PRL, Bacellar, O, Wilson, ME, Beverley, SM, Carvalho, EM and Schriefer, A (2016) Atypical manifestations of cutaneous leishmaniasis in a region endemic for Leishmania braziliensis: clinical, immunological and parasitological aspects. PLoS Neglected Tropical Diseases 10(12), e0005100.Google Scholar
Herrera, G, Hernández, C, Ayala, MS, Flórez, C, Teherán, AA and Ramírez, JD (2017) Evaluation of a multilocus sequence typing (MLST) scheme for Leishmania (Viannia) braziliensis and Leishmania (Viannia) panamensis in Colombia. Parasites and Vectors 10(1), 236.Google Scholar
Kuhls, K, Cupolillo, E, Silva, SO, Schweynoch, C, Boité, MC, Melo, MN, Mauricio, I, Miles, M, Wirth, T and Schönian, G (2013) Population structure and evidence for both clonality and recombination among Brazilian strains of the subgenus Leishmania (Viannia). PLoS Neglected Tropical Diseases 7(10), e2490.Google Scholar
Lescure, FX, Bonnard, P, Chandenier, J, Schmit, JL and Douadi, Y (2002) Atypical cutaneous leishmaniasis. Presse Medicale 31(6), 259–261.Google Scholar
Meireles, CB, Maia, LC, Soares, GC, Teodoro, IPP, Gadelha, MDSV, da Silva, CGL and de Lima, MAP (2017) Atypical presentations of cutaneous leishmaniasis: a systematic review. Acta Tropica 172, 240–254.Google Scholar
Mitropoulos, P, Konidas, P and Durkin-Konidas, M (2009) New world cutaneous leishmaniasis: updated review of current and future diagnosis and treatment. Journal American Academy Demartology 63, 309–322.Google Scholar
Nicolle, C (1908) Isolament et culture des corps de Leishman. Les archives de l'Institut Pasteur Tunis 3, 55–56.Google Scholar
Nolder, D, Roncal, N, Davies, CR, Llanos-Cuentas, A and Miles, MA (2007) Multiple hybrid genotypes of Leishmania (Viannia) in a focus of mucocutaneous leishmaniasis. The American Journal of Tropical Medicine and Hygiene 76(3), 573–578.Google Scholar
Novy, FG and McNeal, WJ (1903) The cultivation of Trypanosoma brucei: A preliminary note. Journal of the American Medical Association 41, 1266–1268.Google Scholar
Oddone, R, Schweynoch, C, Schönian, G, de Sousa, CS, Cupolillo, E, Espinosa, D, Arevalo, J, Noyes, H, Mauricio, I and Kuhls, K (2009) Development of a multilocus microsatellite typing approach for discriminating strains of Leishmania (Viannia) species. Journal of Clinical Microbiology 47(9), 2818–2825.Google Scholar
Oliveira, FS, Valete-Rosalino, CM, Pacheco, SJ, Costa, FA, Schubach, AO and Pacheco, RS (2013) American tegumentary leishmaniasis caused by Leishmania (Viannia) braziliensis: assessment of parasite genetic variability at intra- and inter-patient levels. Parasites and Vectors 6, 189.Google Scholar
Pereira, CG, Silva, ALN, Castilhos, P, Mastrantonio, EC, Souza, RA, Romão, PR, Rezende, RJ, Pena, JDO, Beletti, M and Souza, MA (2009) Different isolates from Leishmania braziliensis complex induce distinct histopathological features in a murine model of infection. Veterinary Parasitology 165, 231–240.Google Scholar
Quaresma, PF, Rêgo, FD, Botelho, HA, da Silva, SR, Moura-Júnior, AJ, Teixeira-Neto, RG, Madeira, FM, Carvalho, MB, Paglia, AP, Melo, MN and Gontijo, CM (2011) Wild, synanthropic and domestic hosts of Leishmania in an endemic area of cutaneous leishmaniasis in Minas Gerais State, Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene 105(10), 579–585.Google Scholar
Queiroz, A, Sousa, R, Heine, C, Cardoso, M, Guimarães, LH, Machado, PR, Carvalho, EM, Riley, LW, Wilson, ME and Schriefer, A (2012) Association between an emerging disseminated form of leishmaniasis and Leishmania (Viannia) braziliensis strain polymorphisms. Journal of Clinical Microbiology 50(12), 4028–4034.Google Scholar
Rêgo, FD, Rugani, JMN, Shimabukuro, PHF, Tonelli, GB, Quaresma, PF and Gontijo, CMF (2015) Molecular detection of Leishmania in phlebotomine sand flies (Diptera: Psychodidae) from a cutaneous leishmaniasis focus at Xakriabá Indigenous Reserve, Brazil. PLoS ONE 10(4), e0122038.Google Scholar
Reithinger, R, Dujardin, JC, Louzir, H, Pirmez, C, Alexander, B and Brooker, S (2007) Cutaneous leishmaniasis. The Lancet Infectious Diseases 7(9), 581–596.Google Scholar
Rogers, MB, Downing, T, Smith, BA, Imamura, H, Sanders, M, Svobodova, M, Volf, P, Berriman, M, Cotton, JA and Smith, DF (2014) Genomic confirmation of hybridisation and recent inbreeding in a vector-isolated Leishmania population. PLoS Genetics 10, e1004092.Google Scholar
Rougeron, V, Meeûs, TD, Hide, M, Waleckx, E, Bermudez, H, Arevalo, J, Llanos-Cuentas, A, Dujardin, JC, De Doncker, S, Le Ray, D, Ayala, FJ and Bañuls, AL (2009) Extreme inbreeding in Leishmania braziliensis. Proceedings of the National Academy of Sciences 106, 10224–10229.Google Scholar
Rougeron, V, De Meeus, T, Hide, M, Waleckx, E, Dereure, J, Arevalo, J, Llanos-Cuentas, A and Banuls, AL (2010) A battery of 12 microsatellite markers for genetic analysis of the Leishmania (Viannia) guyanensis complex. Parasitology 137, 1879–1884.Google Scholar
Schriefer, A, Schriefer, ALF, Góes-Neto, A, Guimarães, LH, Carvalho, LP, Almeida, RP, Machado, PR, Lessa, HA, de Jesus, AR, Riley, LW and Carvalho, EM (2004) Multiclonal Leishmania braziliensis population structure and Its clinical implication in a region of endemicity for American tegumentary leishmaniasis. Infection and Immunity 72(1), 508–514.Google Scholar
Schriefer, A, Guimarães, LH, Machado, PR, Lessa, M, Lessa, HA, Lago, E, Ritt, G, Góes-Neto, A, Schriefer, ALF, Riley, LW and Carvalho, EM (2009) Geographic clustering of leishmaniasis in northeastern Brazil. Emerging Infectious Diseases journal 15(6), 871–876.Google Scholar
Tamura, K, Stecher, G, Peterson, D, Filipski, A and Kumar, S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.Google Scholar