Molyneux D , 1974. Virus-like particles in Leishmania parasites. Nature 249: 588–589.
Tarr PI , Aline RF , Smiley BL , Scholler J , Keithly J , Stuartt K , 1988. LR1: a candidate RNA virus of Leishmania. Proc Natl Acad Sci USA 85: 9572–9575.
Stuart KD , Weeks R , Guilbride L , Myler PJ , 1992. Molecular organization of Leishmania RNA virus 1. Proc Natl Acad Sci USA 89: 8596–8600.
Guilbride L , Myler PJ , Stuart K , 1992. Distribution and sequence divergence of LRV1 viruses among different Leishmania species. Mol Biochem Parasitol 54: 101–104.
Widmer G , Dooley S , 1995. Phylogenetic analysis of Leishmania RNA virus and Leishmania suggests ancient virus-parasite association. Nucleic Acids Res 23: 2300–2304.
Salinas G , Zamora M , Stuart K , Saravia N , 1996. Leishmania RNA viruses in Leishmania of the Viannia subgenus. Am J Trop Med Hyg 54: 425–429.
Saiz M et al., 1998. Short report: detection of leishmaniavirus in human biopsy samples of leishmaniasis from Peru. Am J Trop Med Hyg 58: 192–194.
de Oliveira Ramos Pereira L , Maretti-Mira AC , Rodrigues KM , Lima RB , de Oliveira-Neto MP , Cupolillo E , Pirmez C , de Oliveira MP , 2013. Severity of tegumentary leishmaniasis is not exclusively associated with Leishmania RNA virus 1 infection in Brazil. Mem Inst Oswaldo Cruz 108: 665–667.
Cantanhêde LM , da Silva Júnior CF , Ito MM , Felipin KP , Nicolete R , Salcedo JMV , Porrozzi R , Cupolillo E , de Godio Mattos Ferreira R , 2015. Further evidence of an association between the presence of Leishmania RNA virus 1 and the mucosal manifestations in tegumentary leishmaniasis patients. PLoS Negl Trop Dis 9: e0004079.
Ginouvès M , Simon S , Bourreau E , Lacoste V , Ronet C , Couppié P , Nacher M , Demar M , Prévot G , 2016. Prevalence and distribution of Leishmania RNA virus 1 in Leishmania parasites from French Guiana. Am J Trop Med Hyg 94: 102–106.
Macedo DH , Menezes-Neto A , Rugani JM , Rocha AC , Silva SO , Melo MN , Lye LF , Beverley SM , Gontijo CM , Soares RP , 2016. Low frequency of LRV1 in Leishmania braziliensis strains isolated from typical and atypical lesions in the State of Minas Gerais, Brazil. Mol Biochem Parasitol 210: 50–54.
Valencia BM , Lau R , Kariyawasam R , Jara M , Ramos AP , Chantry M , Lana JT , Boggild AK , Llanos-Cuentas A , 2022. Leishmania RNA virus-1 is similarly detected among metastatic and non-metastatic phenotypes in a prospective cohort of American tegumentary leishmaniasis. PLoS Negl Trop Dis 16: e0010162.
Adaui V et al., 2016. Association of the endobiont double-stranded RNA virus LRV1 with treatment failure for human leishmaniasis caused by Leishmania braziliensis in Peru and Bolivia. J Infect Dis 213: 112–121.
Cantanhêde LM , Fernandes FG , Melim Ferreira GE , Porrozzi R , de Godoi Mattos Ferreira R , Cupolillo E , 2018. New insights into the genetic diversity of Leishmania RNA virus 1 and its species-specific relationship with Leishmania parasites. PLoS One 13: e0198727.
Vieira-Gonçalves R , Fagundes-Silva GA , Heringer JF , Fantinatti M , Da-Cruz AM , Oliveira-Neto MP , Guerra JAO , Gomes-Silva A , 2019. First report of treatment failure in a patient with cutaneous leishmaniasis infected by Leishmania (Viannia) naiffi carrying Leishmania RNA virus: a fortuitous combination? Rev Soc Bras Med Trop 52: e20180323.
Zangger H , Hailu A , Desponds C , Lye LF , Akopyants NS , Dobson DE , Ronet C , Ghalib H , Beverley SM , Fasel N , 2014. Leishmania aethiopica field isolates bearing an endosymbiontic dsRNA virus induce pro-inflammatory cytokine response. PLoS Negl Trop Dis 8: e2836.
Ogg MM , Carrion R , De Carvalho Botelho AC , Mayrink W , Correa-Oliveira R , Patterson JL , 2003. Short report: quantification of Leishmaniavirus RNA in clinical samples and its possible role in pathogenesis. Am J Trop Med Hyg 69: 309–313.
Ito MM , Catanhêde LM , Katsuragawa TH , da Silva CF Jr. , Camargo LMA , de Godoi Mattos R , Vilallobos-Salcedo JM , 2015. Correlation between presence of Leishmania RNA virus 1 and clinical characteristics of nasal mucosal leishmaniosis. Braz J Otorhinolaryngol 81: 533–540.
Bourreau E et al., 2016. Presence of Leishmania RNA virus 1 in Leishmania guyanensis increases the risk of first-line treatment failure and symptomatic relapse. J Infect Dis 213: 105–111.
Scheffter SM , Ro YT , Chung IK , Patterson JL , 1995. The complete sequence of Leishmania RNA virus LRV2-1, a virus of an Old World parasite strain. Virology 212: 84–90.
Hajjaran H , Mahdi M , Mohebali M , Samimi-Rad K , Ataei-Pirkooh A , Kazemi-Rad E , Naddaf SR , Raoofian R , 2016. Detection and molecular identification of Leishmania RNA virus (LRV) in Iranian Leishmania species. Arch Virol 161: 3385–3390.
Nalçacı M , Karakuş M , Yılmaz B , Demir S , Özbilgin A , Özbel Y , Töz S , 2019. Detection of Leishmania RNA virus 2 in Leishmania species from Turkey. Trans R Soc Trop Med Hyg 113: 410–417.
Kurt Ö , Mansur N , Çavuş I , Özcan O , Burak Batir M , Gündüz C , Sezerman U , Özbilgın A , 2019. First report and in silico analysis of Leishmania virus (LRV2) identified in an autochthonous Leishmania major isolate in Turkey. New Microbiol 42: 65–67.
Tirera S et al., 2017. Unraveling the genetic diversity and phylogeny of Leishmania RNA virus 1 strains of infected Leishmania isolates circulating in French Guiana. PLoS Negl Trop Dis 11: e0005764.
Kostygov AY , Grybchuk D , Kleschenko Y , Chistyakov DS , Lukashev AN , Gerasimov ES , Yurchenko V , 2021. Analyses of Leishmania-LRV co-phylogenetic patterns and evolutionary variability of viral proteins. Viruses 13: 2305.
Correa-Cárdenas CA et al., 2020. Distribution, treatment outcome and genetic diversity of Leishmania species in military personnel from Colombia with cutaneous leishmaniasis. BMC Infect Dis 20: 938.
Parmentier L et al., 2016. Case report: severe cutaneous leishmaniasis in a human immunodeficiency virus patient coinfected with Leishmania braziliensis and its endosymbiotic virus. Am J Trop Med Hyg 94: 840–843.
de Carvalho RVH et al., 2019. Leishmania RNA virus exacerbates leishmaniasis by subverting innate immunity via TLR3-mediated NLRP3 inflammasome inhibition. Nat Commun 10: 5273.
Zangger H et al., 2013. Detection of Leishmania RNA virus in Leishmania parasites. PLoS Negl Trop Dis 7: e2006.
Ives A et al., 2011. Leishmania RNA virus controls the severity of mucocutaneous leishmaniasis. Science 331: 775–778.
Atayde VD , da Silva Lira Filho A , Chaparro V , Zimmermann A , Martel C , Jaramillo M , Olivier M , 2019. Exploitation of the Leishmania exosomal pathway by Leishmania RNA virus 1. Nat Microbiol 4: 714–723.
Abtahi M , Eslami G , Cavallero S , Vakili M , Hosseini SS , Ahmadian S , Boozhmehrani MJ , Khamesipour A , 2020. Relationship of Leishmania RNA virus (LRV) and treatment failure in clinical isolates of Leishmania major. BMC Res Notes 13: 126.
Ginouvès M et al., 2021. Leishmaniavirus genetic diversity is not related to leishmaniasis treatment failure. Clin Microbiol Infect 27: 286.e1–286.e5.
Kariyawasam R , Lau R , Valencia BM , Llanos-Cuentas A , Boggild AK , 2020. Leishmania RNA virus 1 (LRV-1) in Leishmania (Viannia) braziliensis isolates from Peru: a description of demographic and clinical correlates. Am J Trop Med Hyg 102: 280–285.
Parra-Muñoz M , Aponte S , Ovalle-Bracho C , Saavedra CH , Echeverry MC , 2021. Detection of Leishmania RNA virus in clinical samples from cutaneous leishmaniasis patients varies according to the type of sample. Am J Trop Med Hyg 104: 233–239.
Salgado-Almario J , Hernández CA , Ovalle-Bracho C , 2019. Geographical distribution of Leishmania species in Colombia, 1985–2017. Biomedica 39: 278–290.
Corredor A et al., 1990. Distribution and etiology of leishmaniasis in Colombia. Am J Trop Med Hyg 42: 206–214.
Saravia NG , Segura I , Holguin AF , Santrich C , Valderrama L , Ocampo C , 1998. Epidemiologic, genetic, and clinical associations among phenotypically distinct populations of Leishmania (Viannia) in Colombia. Am J Trop Med Hyg 59: 86–94.
Saravia NG , Weigle K , Navas C , Segura I , Valderrama L , Valencia AZ , Escorcia B , McMahon-Pratt D , 2002. Heterogeneity, geographic distribution, and pathogenicity of serodemes of Leishmania Viannia in Colombia. Am J Trop Med Hyg 66: 738–744.
Osorio LE , Castillo CM , Ochoa MT , 1998. Mucosal leishmaniasis due to Leishmania (Viannia) panamensis in Colombia: clinical characteristics. Am J Trop Med Hyg 59: 49–52.
Ovalle-Bracho C , Londoño-Barbosa D , Salgado-Almario J , González C , 2019. Evaluating the spatial distribution of Leishmania parasites in Colombia from clinical samples and human isolates (1999 to 2016). PLoS One 14: e0214124.
Patino LH , Mendez C , Rodriguez O , Romero Y , Velandia D , Alvarado M , Pérez J , Duque MC , Ramírez JD , 2017. Spatial distribution, Leishmania species and clinical traits of cutaneous leishmaniasis cases in the Colombian army. PLoS Negl Trop Dis 11: e0005876.
Grimaldi GJ , Mcmahon-Pratt D , 1996. Monoclonal antibodies for the identification of New World Leishmania species. Mem Inst Oswaldo Cruz 91: 37–42.
Evans DA , Lanham SM , Baldwin CI , Peters W , 1984. The isolation and isoenzyme characterization of Leishmania braziliensis subsp. from patients with cutaneous leishmaniasis acquired in Belize. Trans R Soc Trop Med Hyg 78: 35–42.
Cupolillo E , Grimaldi G , Momen H , 1994. A general classification of New World Leishmania using numerical zymotaxonomy. Am J Trop Med Hyg 50: 296–311.
Rodríguez-Barraquer I , Góngora R , Prager M , Pacheco R , Montero LM , Navas A , Ferro C , Miranda MC , Saravia NG , 2008. Etiologic agent of an epidemic of cutaneous leishmaniasis in Tolima, Colombia. Am J Trop Med Hyg 78: 276–282.
Barrera MC , Rojas LJ , Weiss A , Fernandez O , McMahon-Pratt D , Saravia NG , Gomez MA , 2017. Profiling gene expression of antimony response genes in Leishmania (Viannia) panamensis and infected macrophages and its relationship with drug susceptibility. Acta Trop 176: 355–363.
Gómez-Zafra MJ , Navas A , Jojoa J , Murillo J , González C , Gómez MA , 2020. Immune profile of the nasal mucosa in patients with cutaneous leishmaniasis. Infect Immun 88: e00881-19.
Kariyawasam R , Mukkala AN , Lau R , Valencia BM , Llanos-Cuentas A , Boggild AK , 2019. Virulence factor RNA transcript expression in the Leishmania Viannia subgenus: influence of species, isolate source, and Leishmania RNA virus-1. Trop Med Health 47: 25.
Cupolillo E , Aguiar Alves F , Brahim L , Naiff M , Pereira L , Oliveira-Neto M , Falqueto A , Grimaldi G , 2001. Recent advances in the taxonomy of the New World leishmanial parasites. Med Microbiol Immunol (Berl) 190: 57–60.
Stevenson L , Fedorko D , Zelazny A , 2010. An enhanced method for the identification of Leishmania spp. using real-time polymerase chain reaction and sequence analysis of the 7SL RNA gene region. Diagn Microbiol Infect Dis 66: 432–435.
Kleschenko Y , Grybchuk D , Matveeva NS , Macedo DH , Ponirovsky EN , Lukashev AN , Yurchenko V , 2019. Molecular characterization of Leishmania RNA virus 2 in Leishmania major from Uzbekistan. Genes (Basel) 10: 830.
Saberi R , Fakhar M , Hajjaran H , Ataei-Pirkooh A , Mohebali M , Taghipour N , Ziaei Hezarjaribi H , Moghadam Y , Bagheri A , 2020. Presence and diversity of Leishmania RNA virus in an old zoonotic cutaneous leishmaniasis focus, northeastern Iran: haplotype and phylogenetic based approach. Int J Infect Dis 101: 6–13.
Cantanhêde LM , Mata-Somarribas C , Chourabi K , Pereira da Silva G , Dias Das Chagas B , de Oliveira R , Pereira L , Côrtes Boité M , Cupolillo E , 2021. The maze pathway of coevolution: a critical review over the Leishmania and its endosymbiotic history. Genes (Basel) 12: 657.
Gomez MA , Belew AT , Navas A , Rosales-Chilama M , Murillo J , Dillon LAL , Alexander TA , Martinez-Valencia A , El-Sayed NM , 2021. Early leukocyte responses in ex-vivo models of healing and non-healing human Leishmania (Viannia) panamensis infections. Front Cell Infect Microbiol 11: 687607.
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The endosymbiotic Leishmania RNA virus 1 (LRV1) has been associated with severity and clinical manifestations of American tegumentary leishmaniasis caused by species of the Leishmania (Viannia) subgenus. Between and within Leishmania species, and among endemic countries, the prevalence of LRV is highly variable. The LRV virus has not been detected in L. (V.) panamensis, the second-most prevalent species in Central America and Colombia. However, no systematic screening of LRV has been conducted in L. (V.) panamensis, and thus it is still controversial whether this virus is truly absent from the species. We sought to determine the prevalence of LRV1 in L. (V.) panamensis clinical strains isolated from patients with cutaneous leishmaniasis (CL), from different geographic areas of Colombia. We analyzed 219 clinical strains; 78% were L. (V.) panamensis, 18% were L. (V.) braziliensis, and 4% were L. (V.) guyanensis. Screening for LRV1 was performed by quantitative reverse transcription–polymerase chain reaction. The LRV1 was detected in 18% (7 of 40) of L. (V) braziliensis strains, and was not detected in any of the L. (V.) guyanensis or L. (V.) panamensis strains. The LRV1-positive L. (V). braziliensis strains came from the Amazon Basin. Of the seven LRV1-positive strains, two were isolated from patients with mucocutaneous leishmaniasis, and the remaining from patients with CL. Our results confirm the absence of LRV1 in L. (V.) panamensis in Colombia.
Financial support: This work was financed by the NIH, National Institute of Allergy and Infectious Diseases, Tropical Medicine Research Centers (grant no. U19AI129910) and the Colombian National Programa Nacional de Ciencia, Tecnología e Innovación en Salud of Ministerio de Ciencia, Tecnología e Innovación (contract no. 848-2019, code no. 222984368586). The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Ethics statement: This study was approved and monitored by the Institutional Review Board (IRB) for Ethical Conduct of Research Involving Human Subjects of the CIDEIM (approval code no. CIEIH1274) in accordance with national and international guidelines for the conduct of clinical studies. Samples and data used in this study were collected previously from patients recruited under other IRB-approved study protocols at CIDEIM. Before including and using patient information, all informed consent forms were reviewed; only data and samples from those who provided written authorization for use in future studies were included.
Authors’ addresses: Mariana Rosales-Chilama, Olga L. Fernández, and María Adelaida Gómez, Centro Internacional de Entrenamiento e Investigaciones Médicas-CIDEIM, Cali, Columbia, and Universidad Icesi, Cali, Colombia, E-mails: mrosales@cideim.org.co, ofernandez@cideim.org.co, and mgomez@cideim.org.co. Monica Y. Oviedo, Centro Internacional de Entrenamiento e Investigaciones Médicas-CIDEIM, Cali, Colombia, E-mail: monica.yari.oviedo@gmail.com. Yury K. Quintero, Centro Internacional de Entrenamiento e Investigaciones Médicas-CIDEIM, Cali, Colombia, and Universidad Industrial de Santander, Bucaramanga, Colombia, E-mail: katherquim@hotmail.com.
Molyneux D , 1974. Virus-like particles in Leishmania parasites. Nature 249: 588–589.
Tarr PI , Aline RF , Smiley BL , Scholler J , Keithly J , Stuartt K , 1988. LR1: a candidate RNA virus of Leishmania. Proc Natl Acad Sci USA 85: 9572–9575.
Stuart KD , Weeks R , Guilbride L , Myler PJ , 1992. Molecular organization of Leishmania RNA virus 1. Proc Natl Acad Sci USA 89: 8596–8600.
Guilbride L , Myler PJ , Stuart K , 1992. Distribution and sequence divergence of LRV1 viruses among different Leishmania species. Mol Biochem Parasitol 54: 101–104.
Widmer G , Dooley S , 1995. Phylogenetic analysis of Leishmania RNA virus and Leishmania suggests ancient virus-parasite association. Nucleic Acids Res 23: 2300–2304.
Salinas G , Zamora M , Stuart K , Saravia N , 1996. Leishmania RNA viruses in Leishmania of the Viannia subgenus. Am J Trop Med Hyg 54: 425–429.
Saiz M et al., 1998. Short report: detection of leishmaniavirus in human biopsy samples of leishmaniasis from Peru. Am J Trop Med Hyg 58: 192–194.
de Oliveira Ramos Pereira L , Maretti-Mira AC , Rodrigues KM , Lima RB , de Oliveira-Neto MP , Cupolillo E , Pirmez C , de Oliveira MP , 2013. Severity of tegumentary leishmaniasis is not exclusively associated with Leishmania RNA virus 1 infection in Brazil. Mem Inst Oswaldo Cruz 108: 665–667.
Cantanhêde LM , da Silva Júnior CF , Ito MM , Felipin KP , Nicolete R , Salcedo JMV , Porrozzi R , Cupolillo E , de Godio Mattos Ferreira R , 2015. Further evidence of an association between the presence of Leishmania RNA virus 1 and the mucosal manifestations in tegumentary leishmaniasis patients. PLoS Negl Trop Dis 9: e0004079.
Ginouvès M , Simon S , Bourreau E , Lacoste V , Ronet C , Couppié P , Nacher M , Demar M , Prévot G , 2016. Prevalence and distribution of Leishmania RNA virus 1 in Leishmania parasites from French Guiana. Am J Trop Med Hyg 94: 102–106.
Macedo DH , Menezes-Neto A , Rugani JM , Rocha AC , Silva SO , Melo MN , Lye LF , Beverley SM , Gontijo CM , Soares RP , 2016. Low frequency of LRV1 in Leishmania braziliensis strains isolated from typical and atypical lesions in the State of Minas Gerais, Brazil. Mol Biochem Parasitol 210: 50–54.
Valencia BM , Lau R , Kariyawasam R , Jara M , Ramos AP , Chantry M , Lana JT , Boggild AK , Llanos-Cuentas A , 2022. Leishmania RNA virus-1 is similarly detected among metastatic and non-metastatic phenotypes in a prospective cohort of American tegumentary leishmaniasis. PLoS Negl Trop Dis 16: e0010162.
Adaui V et al., 2016. Association of the endobiont double-stranded RNA virus LRV1 with treatment failure for human leishmaniasis caused by Leishmania braziliensis in Peru and Bolivia. J Infect Dis 213: 112–121.
Cantanhêde LM , Fernandes FG , Melim Ferreira GE , Porrozzi R , de Godoi Mattos Ferreira R , Cupolillo E , 2018. New insights into the genetic diversity of Leishmania RNA virus 1 and its species-specific relationship with Leishmania parasites. PLoS One 13: e0198727.
Vieira-Gonçalves R , Fagundes-Silva GA , Heringer JF , Fantinatti M , Da-Cruz AM , Oliveira-Neto MP , Guerra JAO , Gomes-Silva A , 2019. First report of treatment failure in a patient with cutaneous leishmaniasis infected by Leishmania (Viannia) naiffi carrying Leishmania RNA virus: a fortuitous combination? Rev Soc Bras Med Trop 52: e20180323.
Zangger H , Hailu A , Desponds C , Lye LF , Akopyants NS , Dobson DE , Ronet C , Ghalib H , Beverley SM , Fasel N , 2014. Leishmania aethiopica field isolates bearing an endosymbiontic dsRNA virus induce pro-inflammatory cytokine response. PLoS Negl Trop Dis 8: e2836.
Ogg MM , Carrion R , De Carvalho Botelho AC , Mayrink W , Correa-Oliveira R , Patterson JL , 2003. Short report: quantification of Leishmaniavirus RNA in clinical samples and its possible role in pathogenesis. Am J Trop Med Hyg 69: 309–313.
Ito MM , Catanhêde LM , Katsuragawa TH , da Silva CF Jr. , Camargo LMA , de Godoi Mattos R , Vilallobos-Salcedo JM , 2015. Correlation between presence of Leishmania RNA virus 1 and clinical characteristics of nasal mucosal leishmaniosis. Braz J Otorhinolaryngol 81: 533–540.
Bourreau E et al., 2016. Presence of Leishmania RNA virus 1 in Leishmania guyanensis increases the risk of first-line treatment failure and symptomatic relapse. J Infect Dis 213: 105–111.
Scheffter SM , Ro YT , Chung IK , Patterson JL , 1995. The complete sequence of Leishmania RNA virus LRV2-1, a virus of an Old World parasite strain. Virology 212: 84–90.
Hajjaran H , Mahdi M , Mohebali M , Samimi-Rad K , Ataei-Pirkooh A , Kazemi-Rad E , Naddaf SR , Raoofian R , 2016. Detection and molecular identification of Leishmania RNA virus (LRV) in Iranian Leishmania species. Arch Virol 161: 3385–3390.
Nalçacı M , Karakuş M , Yılmaz B , Demir S , Özbilgin A , Özbel Y , Töz S , 2019. Detection of Leishmania RNA virus 2 in Leishmania species from Turkey. Trans R Soc Trop Med Hyg 113: 410–417.
Kurt Ö , Mansur N , Çavuş I , Özcan O , Burak Batir M , Gündüz C , Sezerman U , Özbilgın A , 2019. First report and in silico analysis of Leishmania virus (LRV2) identified in an autochthonous Leishmania major isolate in Turkey. New Microbiol 42: 65–67.
Tirera S et al., 2017. Unraveling the genetic diversity and phylogeny of Leishmania RNA virus 1 strains of infected Leishmania isolates circulating in French Guiana. PLoS Negl Trop Dis 11: e0005764.
Kostygov AY , Grybchuk D , Kleschenko Y , Chistyakov DS , Lukashev AN , Gerasimov ES , Yurchenko V , 2021. Analyses of Leishmania-LRV co-phylogenetic patterns and evolutionary variability of viral proteins. Viruses 13: 2305.
Correa-Cárdenas CA et al., 2020. Distribution, treatment outcome and genetic diversity of Leishmania species in military personnel from Colombia with cutaneous leishmaniasis. BMC Infect Dis 20: 938.
Parmentier L et al., 2016. Case report: severe cutaneous leishmaniasis in a human immunodeficiency virus patient coinfected with Leishmania braziliensis and its endosymbiotic virus. Am J Trop Med Hyg 94: 840–843.
de Carvalho RVH et al., 2019. Leishmania RNA virus exacerbates leishmaniasis by subverting innate immunity via TLR3-mediated NLRP3 inflammasome inhibition. Nat Commun 10: 5273.
Zangger H et al., 2013. Detection of Leishmania RNA virus in Leishmania parasites. PLoS Negl Trop Dis 7: e2006.
Ives A et al., 2011. Leishmania RNA virus controls the severity of mucocutaneous leishmaniasis. Science 331: 775–778.
Atayde VD , da Silva Lira Filho A , Chaparro V , Zimmermann A , Martel C , Jaramillo M , Olivier M , 2019. Exploitation of the Leishmania exosomal pathway by Leishmania RNA virus 1. Nat Microbiol 4: 714–723.
Abtahi M , Eslami G , Cavallero S , Vakili M , Hosseini SS , Ahmadian S , Boozhmehrani MJ , Khamesipour A , 2020. Relationship of Leishmania RNA virus (LRV) and treatment failure in clinical isolates of Leishmania major. BMC Res Notes 13: 126.
Ginouvès M et al., 2021. Leishmaniavirus genetic diversity is not related to leishmaniasis treatment failure. Clin Microbiol Infect 27: 286.e1–286.e5.
Kariyawasam R , Lau R , Valencia BM , Llanos-Cuentas A , Boggild AK , 2020. Leishmania RNA virus 1 (LRV-1) in Leishmania (Viannia) braziliensis isolates from Peru: a description of demographic and clinical correlates. Am J Trop Med Hyg 102: 280–285.
Parra-Muñoz M , Aponte S , Ovalle-Bracho C , Saavedra CH , Echeverry MC , 2021. Detection of Leishmania RNA virus in clinical samples from cutaneous leishmaniasis patients varies according to the type of sample. Am J Trop Med Hyg 104: 233–239.
Salgado-Almario J , Hernández CA , Ovalle-Bracho C , 2019. Geographical distribution of Leishmania species in Colombia, 1985–2017. Biomedica 39: 278–290.
Corredor A et al., 1990. Distribution and etiology of leishmaniasis in Colombia. Am J Trop Med Hyg 42: 206–214.
Saravia NG , Segura I , Holguin AF , Santrich C , Valderrama L , Ocampo C , 1998. Epidemiologic, genetic, and clinical associations among phenotypically distinct populations of Leishmania (Viannia) in Colombia. Am J Trop Med Hyg 59: 86–94.
Saravia NG , Weigle K , Navas C , Segura I , Valderrama L , Valencia AZ , Escorcia B , McMahon-Pratt D , 2002. Heterogeneity, geographic distribution, and pathogenicity of serodemes of Leishmania Viannia in Colombia. Am J Trop Med Hyg 66: 738–744.
Osorio LE , Castillo CM , Ochoa MT , 1998. Mucosal leishmaniasis due to Leishmania (Viannia) panamensis in Colombia: clinical characteristics. Am J Trop Med Hyg 59: 49–52.
Ovalle-Bracho C , Londoño-Barbosa D , Salgado-Almario J , González C , 2019. Evaluating the spatial distribution of Leishmania parasites in Colombia from clinical samples and human isolates (1999 to 2016). PLoS One 14: e0214124.
Patino LH , Mendez C , Rodriguez O , Romero Y , Velandia D , Alvarado M , Pérez J , Duque MC , Ramírez JD , 2017. Spatial distribution, Leishmania species and clinical traits of cutaneous leishmaniasis cases in the Colombian army. PLoS Negl Trop Dis 11: e0005876.
Grimaldi GJ , Mcmahon-Pratt D , 1996. Monoclonal antibodies for the identification of New World Leishmania species. Mem Inst Oswaldo Cruz 91: 37–42.
Evans DA , Lanham SM , Baldwin CI , Peters W , 1984. The isolation and isoenzyme characterization of Leishmania braziliensis subsp. from patients with cutaneous leishmaniasis acquired in Belize. Trans R Soc Trop Med Hyg 78: 35–42.
Cupolillo E , Grimaldi G , Momen H , 1994. A general classification of New World Leishmania using numerical zymotaxonomy. Am J Trop Med Hyg 50: 296–311.
Rodríguez-Barraquer I , Góngora R , Prager M , Pacheco R , Montero LM , Navas A , Ferro C , Miranda MC , Saravia NG , 2008. Etiologic agent of an epidemic of cutaneous leishmaniasis in Tolima, Colombia. Am J Trop Med Hyg 78: 276–282.
Barrera MC , Rojas LJ , Weiss A , Fernandez O , McMahon-Pratt D , Saravia NG , Gomez MA , 2017. Profiling gene expression of antimony response genes in Leishmania (Viannia) panamensis and infected macrophages and its relationship with drug susceptibility. Acta Trop 176: 355–363.
Gómez-Zafra MJ , Navas A , Jojoa J , Murillo J , González C , Gómez MA , 2020. Immune profile of the nasal mucosa in patients with cutaneous leishmaniasis. Infect Immun 88: e00881-19.
Kariyawasam R , Mukkala AN , Lau R , Valencia BM , Llanos-Cuentas A , Boggild AK , 2019. Virulence factor RNA transcript expression in the Leishmania Viannia subgenus: influence of species, isolate source, and Leishmania RNA virus-1. Trop Med Health 47: 25.
Cupolillo E , Aguiar Alves F , Brahim L , Naiff M , Pereira L , Oliveira-Neto M , Falqueto A , Grimaldi G , 2001. Recent advances in the taxonomy of the New World leishmanial parasites. Med Microbiol Immunol (Berl) 190: 57–60.
Stevenson L , Fedorko D , Zelazny A , 2010. An enhanced method for the identification of Leishmania spp. using real-time polymerase chain reaction and sequence analysis of the 7SL RNA gene region. Diagn Microbiol Infect Dis 66: 432–435.
Kleschenko Y , Grybchuk D , Matveeva NS , Macedo DH , Ponirovsky EN , Lukashev AN , Yurchenko V , 2019. Molecular characterization of Leishmania RNA virus 2 in Leishmania major from Uzbekistan. Genes (Basel) 10: 830.
Saberi R , Fakhar M , Hajjaran H , Ataei-Pirkooh A , Mohebali M , Taghipour N , Ziaei Hezarjaribi H , Moghadam Y , Bagheri A , 2020. Presence and diversity of Leishmania RNA virus in an old zoonotic cutaneous leishmaniasis focus, northeastern Iran: haplotype and phylogenetic based approach. Int J Infect Dis 101: 6–13.
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