Sanchez Clemente N, Ugarte-Gil CA, Solórzano N, Maguiña C, Pachas P, Blazes D, Bailey R, Mabey D, Moore D, 2012. Bartonella bacilliformis: a systematic review of the literature to guide the research agenda for elimination. PLoS Negl Trop Dis 6: e1819.
Pachas PE, 2001. Enfermedad de Carrión (Bartonellosis) en el Peru. Lima, Peru: Ministerio de Salud, OGE, INS.
Minnick MF, Anderson BE, Lima A, Battisti JM, Lawyer PG, Birtles RJ, 2014. Oroya fever and verruga peruana: bartonelloses unique to South America. PLoS Negl Trop Dis 8: e2919.
Pons MJ, Gomes C, del Valle-Mendoza J, Ruiz J, 2016. Carrion’s disease: more than a sand fly-vectored illness. PLoS Pathog 12: e1005863.
Gomes C, Palma N, Pons MJ, Magallon-Tejada A, Sandoval I, Tinco-Valdez C, Gutarra C, del Valle-Mendoza J, Ruiz J, Matsuoka M, 2016. Succinyl-CoA synthetase: new antigen candidate of Bartonella bacilliformis. PLoS Negl Trop Dis 10: e0004989.
Gomes C, Pons MJ, del Valle-Mendoza J, Ruiz J, 2016. Carrion’s disease: an eradicable illness? Infect Dis Poverty 5: 105.
Cáceres GA, Galati BAE, Pinto J, Paredes R, Reategui R, Perez J, Chevarría L, Yáñez H, Zorrilla V, 2000. Psychodidae (Diptera) del Perú I: phlebotominae en Huánuco, Pasco y Cusco, su relación con la enfermedad de Carrión y la leishmaniasis tegumentaria. Rev Peru Biol 7: 27–43.
Romero S, 2004. Detection of Bartonella bacilliformis by Real-Time PCR in Naturally Infected Sand Flies. Bethesda, MD: Faculty of the Department of Preventive Medicine and Biometrics Uniformed Services University of the Health Sciences.
Villaseca P, Padilla C, Ventura G, Samalvides F, Yañez H, Chevarría L, Ellis B, Rotz L, Leake J, Beati L, 1999. Importancia de la Lutzomyia peruensis en la transmisión de la enfermedad de Carrion en el Valle Sagrado de los Incas. Urubamba-Cusco, Peru. Rev Med Exp 15: 28–30.
Moo-Llanes DA, Arque-Chunga W, Carmona-Castro O, Yañez-Arenas C, Yañez-Trujillano HH, Cheverría-Pacheco L, Baak-Baak CM, Cáceres AG, 2017. Shifts in the ecological niche of Lutzomyia peruensis under climate change scenarios in Peru. Med Vet Entomol 31: 123–131.
Caceres AG, Galati EA, Le Pont F, Velasquez C, 1997. Possible role of Lutzomyia maranonensis and Lutzomyia robusta (Diptera: Psychodidae) as vectors of human bartonellosis in three provinces of region nor Oriental del Marañon, Peru. Rev Inst Med Trop São Paulo 39: 51–52.
Cáceres AG, Galati EAB, 2001. Lista de phlebotominae (Diptera: psychodidae) para el Perú y especies consideradas como vectores naturales e incriminadas en la transmisión de patógenos de la leishmaniosis tegumentaria y la enfermedad de Carrión (verruga peruana). Rev Med Exp 18: 100–106.
Ministerio de Salud, 2016. Boletin Epidemiológico del Perú. Volumen 25–Semana Epidemiológica N° 51. ISSN versión electrónica: 2415-0762. Available at: http://www.dge.gob.pe/portal/docs/vigilancia/boletines/2016/51.pdf. Accessed data May 1, 2018.
Municipalidad Provincial de Cutervo, 2015. Memoria Anual, 2015. Available at: http://www.municutervo.gob.pe/documentos/MEMORIA_ANUAL_2015.pdf. Accessed data May 1, 2018.
Young DG, Duran MA, 1994. Guide to the identification and geographic distribution of Lutzomyia sand flies in Mexico, the West Indies, central in South America (Diptera: Psychodidade). Mem Am Entomol Inst 54: 1–881.
del Valle Mendoza J et al. 2014. Diagnosis of Carrion’s disease by direct blood PCR in thin blood smear negative samples. PLoS One 9: e92283.
Dong-Mei L et al. 2015. Detection of Bartonella bacilliformis by real-time PCR with TaqMan-MGB probe. Microbiol China 42: 427–435.
Paiva BR, Secundino NF, Nascimento JC, Pimenta PFP, Galati EAB, Andrade HF Jr., Malafronte RS, 2006. Detection and identification of Leishmania species in field-captured phlebotomine sandflies based on mini-exon gene PCR. Acta Trop 99: 252–259.
Gomez EA, Kato H, Hashiguchi Y, 2014. Man-biting sand fly species and natural infection with the Leishmania promastigote in leishmaniasis-endemic areas of Ecuador. Acta Trop 140: 41–49.
Gomes C, Ruiz J, 2018. Carrion’s disease: the sound of silence. Clin Microbiol Rev 31: e00056–e17.
Montoya-Lerma J, Cadena H, Segura I, Travi BL, 1999. Association of Lutzomyia columbiana (Diptera: Psychodidae) with a leishmaniasis focus in Colombia due to species of the Leishmania mexicana complex. Mem Inst Oswaldo Cruz 94: 277–283.
Gomes C, Martinez-Puchol S, Pons MJ, Bazán J, Tinco C, del Valle J, Ruiz J, 2016. Evaluation of PCR approaches for detection of Bartonella bacilliformis in blood samples. PLoS Negl Trop Dis 10: e0004529.
Sant’Anna MRV, Darby AC, Brazil RP, Montoya-Lerma J, Dillon VM, Bates PA, Dillon RJ, 2012. Investigation of the bacterial communities associated with females of Lutzomyia sand fly species from South America. PLoS One 7: e42531.
Gouveia C, Asensi MD, Zahner V, Rangel EF, Oliveira SM, 2008. Study on the bacterial midgut microbiota associated to different Brazilian populations of Lutzomyia longipalpis (Lutz & Neiva) (Diptera: Psychodidae). Neotrop Entomol 37: 597–560.
Kešnerová L, Moritz R, Engel P, 2016. Bartonella apis sp. nov., a honey bee gut symbiont of the class Alphaproteobacteria. Int J Syst Evol Microbiol 66: 414–421.
Leulmi H, Bitam I, Berenger JM, Lepidi H, Rolain JM, Almeras L, Raoult D, Parola P, 2015. Competence of Cimex lectularius bed bugs for the transmission of Bartonella quintana, the agent of trench fever. PLoS Negl Trop Dis 9: e0003789.
Ramírez-Puebla ST, Rosenblueth M, Chávez-Moreno CK, de Lyra MC, Tecante A, Martínez-Romero E, 2010. Molecular phylogeny of the genus Dactylopius (Hemiptera: Dactylopiidae) and identification of the symbiotic bacteria. Environ Entomol 39: 1178–1183.
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Carrion’s disease is a neglected, vector-borne illness that affects Colombia, Ecuador, and especially Peru. The phlebotomine sand flies Lutzomyia verrucarum and Lutzomyia peruensis are the main illness vectors described, although other species may be implicated in endemic areas such as some northern Peruvian regions, in which Carrion’s disease vector has not been established. The aim of this study was to evaluate the presence of Bartonella bacilliformis DNA in Lutzomyia maranonensis from Cajamarca, northern Peru. This sand fly has not been defined as a vector yet. Centers for Disease Control and Prevention light traps were used to collect adult phlebotomine sand flies from 2007 to 2008 in the Cajamarca department. Female specimens were identified using morphological keys and were grouped into pools of five sand flies, taking into account district and sampling site (intradomicile or peridomicile). DNA was extracted, and then conventional and real-time polymerase chain reaction (RT-PCR) were performed to detect B. bacilliformis and subsequently confirmed by sequencing. A total of 383 specimens of L. maranonensis species were analyzed. Two of 76 pools were positive for B. bacilliformis by sequencing; all positives pools were from Querocotillo district. In addition, Mesorhizobium spp. were identified in two pools of sand flies, which is an α-proteobacteria phylogenetically very close to B. bacilliformis. This study presents molecular evidence that suggests L. maranonensis is naturally infected by B. bacilliformis in the Cajamarca department. Further research should determine if L. maranonensis is a vector and could transmit B. bacilliformis.
Financial support: This work was supported by the Royal Society of Tropical Medicine and Hygiene (GR000589), Programa Nacional de Innovación para la Competitividad y Productividad (Innóvate Perú)-contract 116-PNICP-PIAP-2015. J. R. had a fellowship from the program I3SNS of the ISCIII (grant number: CES11/012); C. G. had a predoctoral grant from the ISCIII (FI12/00561).
Authors’ addresses: Gabriela M. Ulloa, Centro de Investigación e Innovación, Facultad de Ciencias de la Salud, Universidad Peruana de Ciencias Aplicadas, Lima, Peru, and Emerge, Emerging Diseases and Climate Change Research Unit, School of Public Health and Administration, Universidad Peruana Cayetano Heredia, Lima, Peru, E-mail: gulloau92@gmail.com. Fernando Vásquez-Achaya and Juana del Valle Mendoza, Centro de Investigación e Innovación, Facultad de Ciencias de la Salud, Universidad Peruana de Ciencias Aplicadas, Lima, Peru, E-mails: fernando.vasquez.achaya@gmail.com and juana.delvalle@upc.edu.pe. Cláudia Gomes and Joaquim Ruiz, ISGlobal, Hospital Clínic—Universitat de Barcelona, Barcelona, Spain, E-mails: claudiasofiapgomes@gmail.com and joruiz.trabajo@gmail.com. Luis J. del Valle, Departament d’Enginyeria Agroalimentària i Biotecnologia, Universitat Politècnica de Catalunya, Barcelona, Spain, E-mail: luis.javier.del.valle@upc.edu. Maria J. Pons, Microbiología molecular y Genómica bacteriana, Universidad Cientifica del Sur, Lima, Peru, E-mail: ma.pons.cas@gmail.com.
Sanchez Clemente N, Ugarte-Gil CA, Solórzano N, Maguiña C, Pachas P, Blazes D, Bailey R, Mabey D, Moore D, 2012. Bartonella bacilliformis: a systematic review of the literature to guide the research agenda for elimination. PLoS Negl Trop Dis 6: e1819.
Pachas PE, 2001. Enfermedad de Carrión (Bartonellosis) en el Peru. Lima, Peru: Ministerio de Salud, OGE, INS.
Minnick MF, Anderson BE, Lima A, Battisti JM, Lawyer PG, Birtles RJ, 2014. Oroya fever and verruga peruana: bartonelloses unique to South America. PLoS Negl Trop Dis 8: e2919.
Pons MJ, Gomes C, del Valle-Mendoza J, Ruiz J, 2016. Carrion’s disease: more than a sand fly-vectored illness. PLoS Pathog 12: e1005863.
Gomes C, Palma N, Pons MJ, Magallon-Tejada A, Sandoval I, Tinco-Valdez C, Gutarra C, del Valle-Mendoza J, Ruiz J, Matsuoka M, 2016. Succinyl-CoA synthetase: new antigen candidate of Bartonella bacilliformis. PLoS Negl Trop Dis 10: e0004989.
Gomes C, Pons MJ, del Valle-Mendoza J, Ruiz J, 2016. Carrion’s disease: an eradicable illness? Infect Dis Poverty 5: 105.
Cáceres GA, Galati BAE, Pinto J, Paredes R, Reategui R, Perez J, Chevarría L, Yáñez H, Zorrilla V, 2000. Psychodidae (Diptera) del Perú I: phlebotominae en Huánuco, Pasco y Cusco, su relación con la enfermedad de Carrión y la leishmaniasis tegumentaria. Rev Peru Biol 7: 27–43.
Romero S, 2004. Detection of Bartonella bacilliformis by Real-Time PCR in Naturally Infected Sand Flies. Bethesda, MD: Faculty of the Department of Preventive Medicine and Biometrics Uniformed Services University of the Health Sciences.
Villaseca P, Padilla C, Ventura G, Samalvides F, Yañez H, Chevarría L, Ellis B, Rotz L, Leake J, Beati L, 1999. Importancia de la Lutzomyia peruensis en la transmisión de la enfermedad de Carrion en el Valle Sagrado de los Incas. Urubamba-Cusco, Peru. Rev Med Exp 15: 28–30.
Moo-Llanes DA, Arque-Chunga W, Carmona-Castro O, Yañez-Arenas C, Yañez-Trujillano HH, Cheverría-Pacheco L, Baak-Baak CM, Cáceres AG, 2017. Shifts in the ecological niche of Lutzomyia peruensis under climate change scenarios in Peru. Med Vet Entomol 31: 123–131.
Caceres AG, Galati EA, Le Pont F, Velasquez C, 1997. Possible role of Lutzomyia maranonensis and Lutzomyia robusta (Diptera: Psychodidae) as vectors of human bartonellosis in three provinces of region nor Oriental del Marañon, Peru. Rev Inst Med Trop São Paulo 39: 51–52.
Cáceres AG, Galati EAB, 2001. Lista de phlebotominae (Diptera: psychodidae) para el Perú y especies consideradas como vectores naturales e incriminadas en la transmisión de patógenos de la leishmaniosis tegumentaria y la enfermedad de Carrión (verruga peruana). Rev Med Exp 18: 100–106.
Ministerio de Salud, 2016. Boletin Epidemiológico del Perú. Volumen 25–Semana Epidemiológica N° 51. ISSN versión electrónica: 2415-0762. Available at: http://www.dge.gob.pe/portal/docs/vigilancia/boletines/2016/51.pdf. Accessed data May 1, 2018.
Municipalidad Provincial de Cutervo, 2015. Memoria Anual, 2015. Available at: http://www.municutervo.gob.pe/documentos/MEMORIA_ANUAL_2015.pdf. Accessed data May 1, 2018.
Young DG, Duran MA, 1994. Guide to the identification and geographic distribution of Lutzomyia sand flies in Mexico, the West Indies, central in South America (Diptera: Psychodidade). Mem Am Entomol Inst 54: 1–881.
del Valle Mendoza J et al. 2014. Diagnosis of Carrion’s disease by direct blood PCR in thin blood smear negative samples. PLoS One 9: e92283.
Dong-Mei L et al. 2015. Detection of Bartonella bacilliformis by real-time PCR with TaqMan-MGB probe. Microbiol China 42: 427–435.
Paiva BR, Secundino NF, Nascimento JC, Pimenta PFP, Galati EAB, Andrade HF Jr., Malafronte RS, 2006. Detection and identification of Leishmania species in field-captured phlebotomine sandflies based on mini-exon gene PCR. Acta Trop 99: 252–259.
Gomez EA, Kato H, Hashiguchi Y, 2014. Man-biting sand fly species and natural infection with the Leishmania promastigote in leishmaniasis-endemic areas of Ecuador. Acta Trop 140: 41–49.
Gomes C, Ruiz J, 2018. Carrion’s disease: the sound of silence. Clin Microbiol Rev 31: e00056–e17.
Montoya-Lerma J, Cadena H, Segura I, Travi BL, 1999. Association of Lutzomyia columbiana (Diptera: Psychodidae) with a leishmaniasis focus in Colombia due to species of the Leishmania mexicana complex. Mem Inst Oswaldo Cruz 94: 277–283.
Gomes C, Martinez-Puchol S, Pons MJ, Bazán J, Tinco C, del Valle J, Ruiz J, 2016. Evaluation of PCR approaches for detection of Bartonella bacilliformis in blood samples. PLoS Negl Trop Dis 10: e0004529.
Sant’Anna MRV, Darby AC, Brazil RP, Montoya-Lerma J, Dillon VM, Bates PA, Dillon RJ, 2012. Investigation of the bacterial communities associated with females of Lutzomyia sand fly species from South America. PLoS One 7: e42531.
Gouveia C, Asensi MD, Zahner V, Rangel EF, Oliveira SM, 2008. Study on the bacterial midgut microbiota associated to different Brazilian populations of Lutzomyia longipalpis (Lutz & Neiva) (Diptera: Psychodidae). Neotrop Entomol 37: 597–560.
Kešnerová L, Moritz R, Engel P, 2016. Bartonella apis sp. nov., a honey bee gut symbiont of the class Alphaproteobacteria. Int J Syst Evol Microbiol 66: 414–421.
Leulmi H, Bitam I, Berenger JM, Lepidi H, Rolain JM, Almeras L, Raoult D, Parola P, 2015. Competence of Cimex lectularius bed bugs for the transmission of Bartonella quintana, the agent of trench fever. PLoS Negl Trop Dis 9: e0003789.
Ramírez-Puebla ST, Rosenblueth M, Chávez-Moreno CK, de Lyra MC, Tecante A, Martínez-Romero E, 2010. Molecular phylogeny of the genus Dactylopius (Hemiptera: Dactylopiidae) and identification of the symbiotic bacteria. Environ Entomol 39: 1178–1183.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 534 | 461 | 83 |
Full Text Views | 658 | 7 | 0 |
PDF Downloads | 306 | 4 | 0 |