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Copyright (c) 2021 Maira Alemán Santos, Lina Martínez-Pérez, Matilde Rivero-Rodríguez, Luis Cortés-Alemán, Alveiro Pérez-Doria, Eduar Bejarano-Martínez
This work is licensed under a Creative Commons Attribution 4.0 International License.
Detection of Leishmania spp. (Trypanosomatidae) and bloodmeal identification in sandflies from a new focus of leishmaniasis in the Colombian Caribbean.
Corresponding Author(s) : Maira Alemán Santos
Ciencia e Innovación en Salud,
2021
Abstract
Background: Although the visceral leishmaniasis (VL) is an endemic disease in the Colombian Caribbean, an increase in its distribution area has been observed in the last years, including reports of cases in new locations. Objetives: In this study, we characterized sandflies, parasites from the Leishmania genus, and some domestic vertebrates associated with the first case of VL in the rural settlement of Toro, San Juan Nepomuceno, Bolívar, Colombia. Methodology: The sandflies were subjected to DNA extraction, amplification, and sequencing for detection of Leishmania spp. infection, and identification of bloodmeals. Additionally, we determined anti-Leishmania antibody titres in canines by the indirect immunofluorescence assay technique. . Results: A total of 2178 sandflies were collected, of which 99.6% were identified as Lutzomyia evansi. Leishmania infantum and Le. braziliensis were the parasites detected in this sandfly species, with a minimum infection rate of 0.003% (3/1070), and 0.0009% (1/1070), respectively. Regarding bloodmeals, 16.73% of the Lu. evansi females had fed on Homo sapiens sapiens, 12.45% on Sus scrofa, 11.63% on Bos taurus, and 9.79% on Canis familiaris. One of the serologically assessed canines was positive for canine leishmaniasis. Conclusion: The detection of mixed bloodmeals from humans and canines in Lu. evansi evidences the epidemiological link among sandflies infected with the parasite, potential reservoirs, and human population. This would explain the appearance of the first VL case in this locality of the Colombian Caribbean.
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- Fernández J, Charry T, Bello F, Escovar J, Lozano C, Ayala M, et al. Prevalencia de leishmaniasis visceral canina en municipios de Huila–Colombia. Acta biol Colomb. 2002; 4(3): 278-285. https://revistas.unal.edu.co/index.php/revsaludpublica/article/view/18534/19446.
- Bejarano E, Uribe S, Rojas W, Darío I. Phlebotomine sand flies (Diptera: Psychodidae) associated with the appearance of urban leishmaniasis in the city of Sincelejo, Colombia. Mem Inst Oswaldo Cruz. 2002; 97(5): 645-647. Doi: http://dx.doi.org/10.1590/S0074-02762002000500010. https://www.scielo.br/scielo.php?pid=S0074-02762002000500010&script=sci_arttext.
- Cortés L. Leishmaniasis transmission focus in El Hobo, Carmen de Bolívar, Bolívar, Colombia. Biomédica. 2006; .26 Suppl 1: 236-241. https://revistabiomedica.org/index.php/biomedica/article/view/1518/1649.
- Cortés L, Fernández J. Especies de Lutzomyia en un foco urbano de leishmaniasis visceral y cutánea en El Carmen de Bolívar, Bolívar, Colombia. Biomédica. 2008; 28(3): 433-440. Doi: https://doi.org/10.7705/biomedica.v28i3.81. http://www.scielo.org.co/scielo.php?pid=S0120-41572008000300013&script=sci_arttext&tlng=pt.
- Cortes L, Pérez-Doria, Bejarano E. Flebotomíneos (Diptera: Psychodidae) antropofílicos de importancia en salud pública en Los Montes de María, Colombia. Rev Cubana Med Trop. 2009; 61(3): 6. http://scielo.sld.cu/scielo.php?script=sci_arttext&pid=S0375-07602009000300003.
- Cortés L, Pereira R. Evaluación ecoepidemiológica de la leishmaniasis en El Carmen de Bolívar. Biomédica. 2011; 31(95): 95.
- Fuya P, Pisciotti I, Pérez S, Lugo L, Ferro C. Presencia de Lutzomyia evansi (Núñez-Tovar, 1924) vector de Leishmania chagasi en área urbana de Cartagena, Colombia. Biomédica. 2011; 31(3): 111-112.
- Zambrano-Hernandez P, Ayala-Sotelo M, Fuya-Oviedo P, Montenegro-Puentes C, Aya-Vanegas N, Aguilera-Jaramillo G, et al. Brote urbano de leishmaniasis visceral en Neiva, Colombia. Revista de Salud Pública. 2015; 17:514-527. https://www.scielosp.org/article/rsap/2015.v17n4/514-527/.
- SIVIGILA. (2016). Sistema Nacional de Vigilancia en Salud Pública. Información epidemiológica. Informe de eventos. https://www.ins.gov.co/buscador-eventos/Informesdeevento/Leishmaniasis%202016.pdf.
- Travi B, Vélez I, Brutus L, Segura I, Jaramillo C, Montoya J. Lutzomyia evansi, an [alternative] vector of Leishmania chagasi in a Colombian focus of visceral leishmaniasis. Trans Royal Soc Trop Med Hyg.1990; 84(5): 676-677. Doi: 10.1016/0035-9203(90)90142-2. https://pubmed.ncbi.nlm.nih.gov/2278068/.
- Rivero-Rodríguez M. Identificación de Leishmania chagasi en canis familiaris en un foco de los Montes de María. Universidad de Sucre. 2003; Tesis. 2003. https://repositorio.unisucre.edu.co/bitstream/001/50/2/T616.9364007%20R621.pdf.
- Rivero-Rodríguez M, Rodríguez-Jiménez J, Pérez-Doria A, Bejarano E. Aislamiento de Leishmania infantum a partir de Canis familiaris en área urbana del Caribe Colombiano. Rev investig vet Perú. 2018; 29(3): 923-930. Doi: http://dx.doi.org/10.15381/rivep.v29i3.13708. http://www.scielo.org.pe/scielo.php?script=sci_arttext&pid=S1609-91172018000300023.
- Montoya-Lerma J, Lane R. Factors affecting host preference of Lutzomyia evansi (Diptera: Psychodidae), a vector of visceral leishmaniasis in Colombia. Bulletin of Entomological Research. 1996; 86(01): 43-50. Doi: 10.1017/S0007485300052184. https://www.cambridge.org/core/journals/bulletin-of-entomological-research/article/abs/factors-affecting-host-preference-of-lutzomyia-evansi-diptera-psychodidae-a-vector-of-visceral-leishmaniasis-in-colombia/7DAA65B81B1A4E786F2DD0E057A64506.
- Paternina L, Verbel-Vergara D, Romero-Ricardo L, Pérez-Doria A, Paternina-Gómez M, Martínez L, et al. Evidence for anthropophily in five species of phlebotomine sand flies (Diptera: Psychodidae) from northern Colombia, revealed by molecular identification of bloodmeals. Acta trop. 2016; 153: 86-92. Doi: 10.1016/j.actatropica.2015.10.005. https://www.sciencedirect.com/science/article/abs/pii/S0001706X15301285.
- Castillo P, Bejarano E, Pérez-Doria A. Validación de las trampas CDC con Diodos Emisores de Luz (LED) en la captura de insectos flebotomíneos (Diptera: Psychodidae). Universidad De Sucre. 2011; Tesis.
- Pérez‐Doria A, Romero-Ricardo L, Bejarano E. Cambiando la forma de extraer el ADN en insectos vectores (Diptera: Psychodidae) de Leishmania spp. Memorias del XXXV Congreso de la Sociedad Colombiana de Entomología. 2008.
- Rodgers M, Popper S, Wirth D. Amplification of kinetoplast DNA as a tool in the detection and diagnosis of Leishmania. Exp Parasitol; 1990. 71(3): 267-275. Doi: https://doi.org/10.1016/0014-4894(90)90031-7. https://www.sciencedirect.com/science/article/abs/pii/0014489490900317.
- El Tai N, Osman O, El Fari M, Presber W, Schönian G. Genetic heterogeneity of ribosomal internal transcribed spacer in clinical samples of Leishmania donovani spotted on filter paper as revealed by single-strand conformation polymorphisms and sequencing. Trans Royal Soc Trop Med Hyg. 2000. 94(5): 575-579. Doi: https://doi.org/10.1016/S0035-9203(00)90093-2. https://www.sciencedirect.com/science/article/abs/pii/S0035920300900932.
- De Almeida M, Steurer F, Koru O, Herwaldt B, Pieniazek N, da Silva A. Identification of Leishmania spp. by molecular amplification and DNA sequencing analysis of a fragment of the rRNA internal transcribed spacer 2. J Clin Microbiol. 2011; 49(9):3143-9. Doi: 10.1128/JCM.01177-11.
- Sanger F. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA. 1983; 74(12):5463-7.Doi: 10.1073/pnas.74.12.5463. https://www.pnas.org/content/74/12/5463.
- Katoh K, Standley D. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013; 30(4): 772-780. Doi:10.1093/molbev/mst010. https://academic.oup.com/bioinformatics/article/26/15/1899/188098?login=true.
- Darriba D, Taboada G, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods. 2012; 9(8): 772. Doi:10.1038/nmeth.2109. https://pubmed.ncbi.nlm.nih.gov/22847109/.
- Huelsenbeck J, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001; 17(8): 754-755. Doi: https://doi.org/10.1093/bioinformatics/17.8.754. https://pubmed.ncbi.nlm.nih.gov/11524383/.
- Kent R, Norris D. Identification of mammalian blood meals in mosquitoes by a multiplexed polymerase chain reaction targeting cytochrome B. Am J Trop Med Hyg. 2005; 73(2): 336-342. https://www.ajtmh.org/content/journals/10.4269/ajtmh.2005.73.336.
- Camargo M. Fluorescent antibody test for the serodiagnosis of American trypanosomiasis. Technical modification employing preserved culture forms of Trypanosoma cruzi in a slide test. Rev Inst Med Trop Sao Paulo. 1966; 8(5): 227-234. https://pubmed.ncbi.nlm.nih.gov/4967348/.
- Ministerio de la Protección Social y Salud. Guía protocolo para la vigilancia en Salud Pública de leishmaniasis Instituto Nacional de Salud de Colombia, Subdirección de Vigilancia y Control en Salud Pública, Protocolo de vigilancia y control de Leishmaniasis. 2010; PRO-R02.003.0000-016, 29.
- Killick-Kendrick R. Studies and criteria for the incrimination of vectors and reservoir hosts of the leishmaniases. Proceedings of the International Workshop on Research on Control Strategies for the Leishmaniases. 1998; Ottawa, 1-4 June 280-282.
- WHO. Control of the leishmaniasis: report of a meeting of the WHO Expert Committee on the Control of leishmaniases. WHO Technical Report Series, 949. 2010; Geneva, 22–26 March.
- Pérez-Doria A, Oviedo E, Bejarano E. Lutzomyia (Diptera: Psychodidae) from the reserva Serranía de Coraza y Montes de María, Colombia. Rev. Colomb Entomol. 2008; 34(1): 98-101. http://www.scielo.org.co/scielo.php?script=sci_arttext&pid=S0120-04882008000100013.
- Romero L, Lastre N, Pérez-Doria A, Bejarano E. Lutzomyia abonnenci and Lutzomyia olmeca (Diptera: Psychodidae), New Records for the Department. Acta biol.Colomb. 2013; 18 (2). http://www.scielo.org.co/scielo.php?script=sci_arttext&pid=S0120-548X2013000200014.
- Zambrano H, Ayala S, Fuya O, Barrazab O, Rodríguez T. Cartagena: nuevo foco de leishmaniasis visceral urbana en Colombia. Revista Ciencia en Desarrollo. 2016; 7(1): 83-91. http://www.scielo.org.co/pdf/cide/v7n1/v7n1a11.pdf.
- Travi B, Adler G, Lozano M, Cadena H, Montoya-Lerma J. Impact of habitat degradation on phlebotominae (Diptera: Psychodidae) of tropical dry forests in Northern Colombia. J Med Entomol. 2002; 39(3): 451-456. Doi: 10.1603/0022-2585-39.3.451. https://academic.oup.com/jme/article-abstract/39/3/451/834931.
- Montoya-Lerma J, Cadena H, Oviedo M, Ready PD, Barazarte R, Travi B. Comparative vectorial efficiency of Lutzomyia evansi and L. longipalpis for transmitting Leishmania chagasi. Acta Trop. 2003; 85:19-29. Disponible en: https://www.sciencedirect.com/science/article/pii/S0001706X02001894. https://www.sciencedirect.com/science/article/abs/pii/S0001706X02001894.
- Travi B, Montoya J, Gallego J, Jaramillo C, Llano R, Velez I. Bionomics of Lutzomyia evansi (Diptera: Psychodidae) vector of visceral leishmaniasis in northern Columbia. J Med Entomol. 1996; 33(3): 278-285. Doi: 10.1093/jmedent/33.3.278. https://academic.oup.com/jme/article-abstract/33/3/278/892083.
- Gonzalez C, Leon C, Paz A, Lopez M, Molina G, Toro D, Tovar C. Diversity patterns, Leishmania DNA detection, and bloodmeal identification of Phlebotominae sand flies in villages in northern Colombia. PLoS One. 2018; 13(1): e0190686. Doi:10.1371/journal.pone.0190686. https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0190686.
- Romero Ricardo L, Pérez-Doria A, Rodríguez J, Vergara J, Montesino A, Martínez L, Bejarano E. Lutzomyia evansi como vector permisivo de Leishmania braziliensis y Leishmania infantum en el departamento de Bolívar, Colombia. Biomédica. 2015; 35: 185.
- Pérez-Doria, A. Búsqueda de infección natural con parásitos causantes de leishmaniasis cutánea en poblaciones flebotomíneas (Diptera: Psychodidae) en los Montes de María, Sucre, Colombia. Programa de maestría en microbiología, Universidad de Córdoba. 2011; Tesis.
- Pérez-Doria A, Romero L, Martínez M, Rivero M, Bejarano E. Aislamiento y tipificación de una cepa de Leishmania braziliensis (Viannia) a partir de Lutzomyia evansi en el municipio de Colosó, Sucre. Biomédica. 2015; 35(Suplemento No. 4, XVI. Congreso Colombiano de Parasitología y Medicina Tropical), 112.
- Hall D, Beevor P, Cork A, Nesbitt B, Vale G. 1-Octen-3-ol. A potent olfactory stimulant and attractant for tsetse isolated from cattle odours. International Journal of Tropical Insect Science. 1984; 5(5): 335-339. Doi: https://doi.org/10.1017/S1742758400008626. https://link.springer.com/article/10.1017/S1742758400008626.
- Afonso M, Duarte R, Miranda J, Caranha L, Rangel E. Studies on the feeding habits of Lutzomyia (Lutzomyia longipalpis) (Lutz & Neiva, 1912) (Diptera: Psychodidae: Phlebotominae) populations from endemic areas of American visceral leishmaniasis in northeastern Brazil. J Trop Med. 2012; 2012:858657. Doi: 10.1155/2012/858657. https://www.hindawi.com/journals/jtm/2012/858657/.
- Chiluiza Piedra P. Detección de la infección natural de Leishmania spp. En especímenes de Lutzomyia spp, y determinación molecular de los hospederos de los que se alimentan en las provincias de Esmeraldas y Chimborazo. Quito: Universidad de las Américas. 2016. http://dspace.udla.edu.ec/bitstream/33000/4860/1/UDLA-EC-TIB-2016-01.pdf.
References
Fernández J, Charry T, Bello F, Escovar J, Lozano C, Ayala M, et al. Prevalencia de leishmaniasis visceral canina en municipios de Huila–Colombia. Acta biol Colomb. 2002; 4(3): 278-285. https://revistas.unal.edu.co/index.php/revsaludpublica/article/view/18534/19446.
Bejarano E, Uribe S, Rojas W, Darío I. Phlebotomine sand flies (Diptera: Psychodidae) associated with the appearance of urban leishmaniasis in the city of Sincelejo, Colombia. Mem Inst Oswaldo Cruz. 2002; 97(5): 645-647. Doi: http://dx.doi.org/10.1590/S0074-02762002000500010. https://www.scielo.br/scielo.php?pid=S0074-02762002000500010&script=sci_arttext.
Cortés L. Leishmaniasis transmission focus in El Hobo, Carmen de Bolívar, Bolívar, Colombia. Biomédica. 2006; .26 Suppl 1: 236-241. https://revistabiomedica.org/index.php/biomedica/article/view/1518/1649.
Cortés L, Fernández J. Especies de Lutzomyia en un foco urbano de leishmaniasis visceral y cutánea en El Carmen de Bolívar, Bolívar, Colombia. Biomédica. 2008; 28(3): 433-440. Doi: https://doi.org/10.7705/biomedica.v28i3.81. http://www.scielo.org.co/scielo.php?pid=S0120-41572008000300013&script=sci_arttext&tlng=pt.
Cortes L, Pérez-Doria, Bejarano E. Flebotomíneos (Diptera: Psychodidae) antropofílicos de importancia en salud pública en Los Montes de María, Colombia. Rev Cubana Med Trop. 2009; 61(3): 6. http://scielo.sld.cu/scielo.php?script=sci_arttext&pid=S0375-07602009000300003.
Cortés L, Pereira R. Evaluación ecoepidemiológica de la leishmaniasis en El Carmen de Bolívar. Biomédica. 2011; 31(95): 95.
Fuya P, Pisciotti I, Pérez S, Lugo L, Ferro C. Presencia de Lutzomyia evansi (Núñez-Tovar, 1924) vector de Leishmania chagasi en área urbana de Cartagena, Colombia. Biomédica. 2011; 31(3): 111-112.
Zambrano-Hernandez P, Ayala-Sotelo M, Fuya-Oviedo P, Montenegro-Puentes C, Aya-Vanegas N, Aguilera-Jaramillo G, et al. Brote urbano de leishmaniasis visceral en Neiva, Colombia. Revista de Salud Pública. 2015; 17:514-527. https://www.scielosp.org/article/rsap/2015.v17n4/514-527/.
SIVIGILA. (2016). Sistema Nacional de Vigilancia en Salud Pública. Información epidemiológica. Informe de eventos. https://www.ins.gov.co/buscador-eventos/Informesdeevento/Leishmaniasis%202016.pdf.
Travi B, Vélez I, Brutus L, Segura I, Jaramillo C, Montoya J. Lutzomyia evansi, an [alternative] vector of Leishmania chagasi in a Colombian focus of visceral leishmaniasis. Trans Royal Soc Trop Med Hyg.1990; 84(5): 676-677. Doi: 10.1016/0035-9203(90)90142-2. https://pubmed.ncbi.nlm.nih.gov/2278068/.
Rivero-Rodríguez M. Identificación de Leishmania chagasi en canis familiaris en un foco de los Montes de María. Universidad de Sucre. 2003; Tesis. 2003. https://repositorio.unisucre.edu.co/bitstream/001/50/2/T616.9364007%20R621.pdf.
Rivero-Rodríguez M, Rodríguez-Jiménez J, Pérez-Doria A, Bejarano E. Aislamiento de Leishmania infantum a partir de Canis familiaris en área urbana del Caribe Colombiano. Rev investig vet Perú. 2018; 29(3): 923-930. Doi: http://dx.doi.org/10.15381/rivep.v29i3.13708. http://www.scielo.org.pe/scielo.php?script=sci_arttext&pid=S1609-91172018000300023.
Montoya-Lerma J, Lane R. Factors affecting host preference of Lutzomyia evansi (Diptera: Psychodidae), a vector of visceral leishmaniasis in Colombia. Bulletin of Entomological Research. 1996; 86(01): 43-50. Doi: 10.1017/S0007485300052184. https://www.cambridge.org/core/journals/bulletin-of-entomological-research/article/abs/factors-affecting-host-preference-of-lutzomyia-evansi-diptera-psychodidae-a-vector-of-visceral-leishmaniasis-in-colombia/7DAA65B81B1A4E786F2DD0E057A64506.
Paternina L, Verbel-Vergara D, Romero-Ricardo L, Pérez-Doria A, Paternina-Gómez M, Martínez L, et al. Evidence for anthropophily in five species of phlebotomine sand flies (Diptera: Psychodidae) from northern Colombia, revealed by molecular identification of bloodmeals. Acta trop. 2016; 153: 86-92. Doi: 10.1016/j.actatropica.2015.10.005. https://www.sciencedirect.com/science/article/abs/pii/S0001706X15301285.
Castillo P, Bejarano E, Pérez-Doria A. Validación de las trampas CDC con Diodos Emisores de Luz (LED) en la captura de insectos flebotomíneos (Diptera: Psychodidae). Universidad De Sucre. 2011; Tesis.
Pérez‐Doria A, Romero-Ricardo L, Bejarano E. Cambiando la forma de extraer el ADN en insectos vectores (Diptera: Psychodidae) de Leishmania spp. Memorias del XXXV Congreso de la Sociedad Colombiana de Entomología. 2008.
Rodgers M, Popper S, Wirth D. Amplification of kinetoplast DNA as a tool in the detection and diagnosis of Leishmania. Exp Parasitol; 1990. 71(3): 267-275. Doi: https://doi.org/10.1016/0014-4894(90)90031-7. https://www.sciencedirect.com/science/article/abs/pii/0014489490900317.
El Tai N, Osman O, El Fari M, Presber W, Schönian G. Genetic heterogeneity of ribosomal internal transcribed spacer in clinical samples of Leishmania donovani spotted on filter paper as revealed by single-strand conformation polymorphisms and sequencing. Trans Royal Soc Trop Med Hyg. 2000. 94(5): 575-579. Doi: https://doi.org/10.1016/S0035-9203(00)90093-2. https://www.sciencedirect.com/science/article/abs/pii/S0035920300900932.
De Almeida M, Steurer F, Koru O, Herwaldt B, Pieniazek N, da Silva A. Identification of Leishmania spp. by molecular amplification and DNA sequencing analysis of a fragment of the rRNA internal transcribed spacer 2. J Clin Microbiol. 2011; 49(9):3143-9. Doi: 10.1128/JCM.01177-11.
Sanger F. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA. 1983; 74(12):5463-7.Doi: 10.1073/pnas.74.12.5463. https://www.pnas.org/content/74/12/5463.
Katoh K, Standley D. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013; 30(4): 772-780. Doi:10.1093/molbev/mst010. https://academic.oup.com/bioinformatics/article/26/15/1899/188098?login=true.
Darriba D, Taboada G, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods. 2012; 9(8): 772. Doi:10.1038/nmeth.2109. https://pubmed.ncbi.nlm.nih.gov/22847109/.
Huelsenbeck J, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001; 17(8): 754-755. Doi: https://doi.org/10.1093/bioinformatics/17.8.754. https://pubmed.ncbi.nlm.nih.gov/11524383/.
Kent R, Norris D. Identification of mammalian blood meals in mosquitoes by a multiplexed polymerase chain reaction targeting cytochrome B. Am J Trop Med Hyg. 2005; 73(2): 336-342. https://www.ajtmh.org/content/journals/10.4269/ajtmh.2005.73.336.
Camargo M. Fluorescent antibody test for the serodiagnosis of American trypanosomiasis. Technical modification employing preserved culture forms of Trypanosoma cruzi in a slide test. Rev Inst Med Trop Sao Paulo. 1966; 8(5): 227-234. https://pubmed.ncbi.nlm.nih.gov/4967348/.
Ministerio de la Protección Social y Salud. Guía protocolo para la vigilancia en Salud Pública de leishmaniasis Instituto Nacional de Salud de Colombia, Subdirección de Vigilancia y Control en Salud Pública, Protocolo de vigilancia y control de Leishmaniasis. 2010; PRO-R02.003.0000-016, 29.
Killick-Kendrick R. Studies and criteria for the incrimination of vectors and reservoir hosts of the leishmaniases. Proceedings of the International Workshop on Research on Control Strategies for the Leishmaniases. 1998; Ottawa, 1-4 June 280-282.
WHO. Control of the leishmaniasis: report of a meeting of the WHO Expert Committee on the Control of leishmaniases. WHO Technical Report Series, 949. 2010; Geneva, 22–26 March.
Pérez-Doria A, Oviedo E, Bejarano E. Lutzomyia (Diptera: Psychodidae) from the reserva Serranía de Coraza y Montes de María, Colombia. Rev. Colomb Entomol. 2008; 34(1): 98-101. http://www.scielo.org.co/scielo.php?script=sci_arttext&pid=S0120-04882008000100013.
Romero L, Lastre N, Pérez-Doria A, Bejarano E. Lutzomyia abonnenci and Lutzomyia olmeca (Diptera: Psychodidae), New Records for the Department. Acta biol.Colomb. 2013; 18 (2). http://www.scielo.org.co/scielo.php?script=sci_arttext&pid=S0120-548X2013000200014.
Zambrano H, Ayala S, Fuya O, Barrazab O, Rodríguez T. Cartagena: nuevo foco de leishmaniasis visceral urbana en Colombia. Revista Ciencia en Desarrollo. 2016; 7(1): 83-91. http://www.scielo.org.co/pdf/cide/v7n1/v7n1a11.pdf.
Travi B, Adler G, Lozano M, Cadena H, Montoya-Lerma J. Impact of habitat degradation on phlebotominae (Diptera: Psychodidae) of tropical dry forests in Northern Colombia. J Med Entomol. 2002; 39(3): 451-456. Doi: 10.1603/0022-2585-39.3.451. https://academic.oup.com/jme/article-abstract/39/3/451/834931.
Montoya-Lerma J, Cadena H, Oviedo M, Ready PD, Barazarte R, Travi B. Comparative vectorial efficiency of Lutzomyia evansi and L. longipalpis for transmitting Leishmania chagasi. Acta Trop. 2003; 85:19-29. Disponible en: https://www.sciencedirect.com/science/article/pii/S0001706X02001894. https://www.sciencedirect.com/science/article/abs/pii/S0001706X02001894.
Travi B, Montoya J, Gallego J, Jaramillo C, Llano R, Velez I. Bionomics of Lutzomyia evansi (Diptera: Psychodidae) vector of visceral leishmaniasis in northern Columbia. J Med Entomol. 1996; 33(3): 278-285. Doi: 10.1093/jmedent/33.3.278. https://academic.oup.com/jme/article-abstract/33/3/278/892083.
Gonzalez C, Leon C, Paz A, Lopez M, Molina G, Toro D, Tovar C. Diversity patterns, Leishmania DNA detection, and bloodmeal identification of Phlebotominae sand flies in villages in northern Colombia. PLoS One. 2018; 13(1): e0190686. Doi:10.1371/journal.pone.0190686. https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0190686.
Romero Ricardo L, Pérez-Doria A, Rodríguez J, Vergara J, Montesino A, Martínez L, Bejarano E. Lutzomyia evansi como vector permisivo de Leishmania braziliensis y Leishmania infantum en el departamento de Bolívar, Colombia. Biomédica. 2015; 35: 185.
Pérez-Doria, A. Búsqueda de infección natural con parásitos causantes de leishmaniasis cutánea en poblaciones flebotomíneas (Diptera: Psychodidae) en los Montes de María, Sucre, Colombia. Programa de maestría en microbiología, Universidad de Córdoba. 2011; Tesis.
Pérez-Doria A, Romero L, Martínez M, Rivero M, Bejarano E. Aislamiento y tipificación de una cepa de Leishmania braziliensis (Viannia) a partir de Lutzomyia evansi en el municipio de Colosó, Sucre. Biomédica. 2015; 35(Suplemento No. 4, XVI. Congreso Colombiano de Parasitología y Medicina Tropical), 112.
Hall D, Beevor P, Cork A, Nesbitt B, Vale G. 1-Octen-3-ol. A potent olfactory stimulant and attractant for tsetse isolated from cattle odours. International Journal of Tropical Insect Science. 1984; 5(5): 335-339. Doi: https://doi.org/10.1017/S1742758400008626. https://link.springer.com/article/10.1017/S1742758400008626.
Afonso M, Duarte R, Miranda J, Caranha L, Rangel E. Studies on the feeding habits of Lutzomyia (Lutzomyia longipalpis) (Lutz & Neiva, 1912) (Diptera: Psychodidae: Phlebotominae) populations from endemic areas of American visceral leishmaniasis in northeastern Brazil. J Trop Med. 2012; 2012:858657. Doi: 10.1155/2012/858657. https://www.hindawi.com/journals/jtm/2012/858657/.
Chiluiza Piedra P. Detección de la infección natural de Leishmania spp. En especímenes de Lutzomyia spp, y determinación molecular de los hospederos de los que se alimentan en las provincias de Esmeraldas y Chimborazo. Quito: Universidad de las Américas. 2016. http://dspace.udla.edu.ec/bitstream/33000/4860/1/UDLA-EC-TIB-2016-01.pdf.