Entomological characterization of Aedes mosquitoes and arbovirus detection in Ibagué, a Colombian city with co-circulation of Zika, dengue and chikungunya viruses

Parasites and Vectors - 2021
María Cristina Carrasquilla1, Mario I. Ortiz1, Cielo León1, Silvia Rondón1, Manisha A. Kulkarni2, Benoit Talbot2, Beate Sander3, Heriberto Vásquez4, Juan Manuel Cordovez5, Camila González1
1Centro de Investigaciones en Microbiología y Parasitología Tropical (CIMPAT), Universidad de Los Andes, Bogotá, Colombia
2School of Epidemiology and Public Health, University of Ottawa, Ottawa, Canada
3Toronto General Hospital Research Institute, University Health Network, Toronto, Canada
4Secretaría de Salud de Ibagué, Ibagué, Colombia
5Grupo de Investigación en Biología Matemática y Computacional (BIOMAC), Universidad de Los Andes, Bogotá, Colombia.

Tóm tắt

Abstract Background Dengue, Zika and chikungunya are arboviruses of significant public health importance that are transmitted by Aedes aegypti and Aedes albopictus mosquitoes. In Colombia, where dengue is hyperendemic, and where chikungunya and Zika were introduced in the last decade, more than half of the population lives in areas at risk. The objective of this study was to characterize Aedes spp. vectors and study their natural infection with dengue, Zika and chikungunya in Ibagué, a Colombian city and capital of the department of Tolima, with case reports of simultaneous circulation of these three arboviruses. Methods Mosquito collections were carried out monthly between June 2018 and May 2019 in neighborhoods with different levels of socioeconomic status. We used the non-parametric Friedman, Mann–Whitney and Kruskal–Wallis tests to compare mosquito density distributions. We applied logistic regression analyses to identify associations between mosquito density and absence/presence of breeding sites, and the Spearman correlation coefficient to analyze the possible relationship between climatic variables and mosquito density. Results We collected Ae. aegypti in all sampled neighborhoods and found for the first time Ae. albopictus in the city of Ibagué. A greater abundance of mosquitoes was collected in neighborhoods displaying low compared to high socioeconomic status as well as in the intradomicile compared to the peridomestic space. Female mosquitoes predominated over males, and most of the test females had fed on human blood. In total, four Ae. aegypti pools (3%) were positive for dengue virus (serotype 1) and one pool for chikungunya virus (0.8%). Interestingly, infected females were only collected in neighborhoods of low socioeconomic status, and mostly in the intradomicile space. Conclusions We confirmed the co-circulation of dengue (serotype 1) and chikungunya viruses in the Ae. aegypti population in Ibagué. However, Zika virus was not detected in any mosquito sample, 3 years after its introduction into the country. The positivity for dengue and chikungunya viruses, predominance of mosquitoes in the intradomicile space and the high proportion of females fed on humans highlight the high risk for arbovirus transmission in Ibagué, but may also provide an opportunity for establishing effective control strategies. Graphical abstract

Từ khóa


Tài liệu tham khảo

World Health Organization. Dengue and severe dengue. 2020. https://www.who.int/es/news-room/fact-sheets/detail/dengue-and-severe-dengue. Accessed 28 Sept 2020.

Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, et al. The global distribution and burden of dengue. Nature. 2013;25:504–7.

Zeller H, Van Bortel W, Sudre B. Chikungunya: its history in Africa and Asia and its spread to new regions in 2013–2014. J Infect Dis. 2016;214:436–40.

Sam IC, Kummerer BM, Chan YF, Rogues P, Drosten C, AbuBakar S. Updates on chikungunya epidemiology, clinical disease, and diagnostics. Vector Borne Zoonotic Dis. 2015;15:223–30.

Dick GWA, Kitchen SF, Haddow AJ. Zika virus. Isolations and serological specificity. Trans R Soc Trop Med Hyg. 1952;46:509–20.

Duffy MR, Chen T-H, Hancock WT, Powers AM, Kool JL, Lanciotti RS, et al. Zika virus outbreak on Yap Island, federated states of Micronesia. N Engl J Med. 2009;360:2536–43.

Pan American Health Organization. Countries and territories of the Americas with confirmed autochthonous cases of Zika virus (vector borne transmission), 2015–2017. 2018. http://ais.paho.org/phip/viz/ed_zika_countrymap.asp. Accessed 16 Jan 2020.

Instituto Nacional de Salud-Ministerio de Salud y Protección Social. Boletín Epidemiológico Semanal. 2019. https://www.ins.gov.co/buscador-eventos/BoletinEpidemiologico/2019_Boletin_epidemiologico_semana_52.pdf. Accessed 27 Apr 2019.

Paixão ES, Teixeira MG, Rodrigues LC. Zika, chikungunya and dengue: the causes and threats of new and re-emerging arboviral diseases. BMJ Glob Health. 2017;3:e000530. https://doi.org/10.1136/bmjgh-2017-000530.

Padilla JC, Lizarazo FE, Murillo O, Mendigaña F, Pachón E, Vera M. Epidemiología de las principales enfermedades transmitidas por vectores en Colombia, 1990–2016. Biomedica. 2017;37:27–40.

Castrillon JC, Castaño JC, Urcuqui S. Dengue en Colombia: 10 años de evolución. Rev Chil Infectol. 2015;32:142–249.

Padilla JC, Rojas DP, Saenz-Gómez R. Dengue en Colombia, Epidemiología de la reemergencia a la hiperendemia. 1st ed. Bogotá: Guías de impresión Ltda; 2012.

Sistema Nacional de Vigilancia en Salud Pública. Instituto Nacional de Salud. 2021 https://www.ins.gov.co/Direcciones/Vigilancia/Paginas/SIVIGILA.aspx.  Accessed 29 July 2021.

Martínez M, Gómez S. Chikungunya en Colombia, el inicio de la transmisión autóctona. IQEN. 2014;19:261–79. https://www.ins.gov.co/buscador-eventos/IQEN/IQEN%20vol%2019%202014%20num%2018.pdf.

Rodriguez-Morales J, Patiño-Valencia S, Villamil-Gómez WE, Alvarado-Socarras JA, Jimenez-Canizales CE. Situación del Zika en Colombia: experiencia de miembros de la Red Colombiana de Colaboración en Zika (RECOLZIKA). Acta Méd Peruana. 2016;33:79–81.

Instituto Nacional de Salud-Ministerio de Salud y Protección Social. Boletín Epidemiológico Semanal. 2014. https://www.ins.gov.co/buscador-eventos/BoletinEpidemiologico/2014%20Boletin%20epidemiologico%20semana%2053.pdf. Accessed 11 May 2021.

Instituto Nacional de Salud-Ministerio de Salud y Protección Social. Boletín Epidemiológico Semanal. 2015. https://www.ins.gov.co/buscador-eventos/BoletinEpidemiologico/2015%20Boletin%20epidemiologico%20Semana%2052.pdf. Accessed 11 May 2021.

Instituto Nacional de Salud-Ministerio de Salud y Protección Social. Boletín Epidemiológico Semanal. 2016. https://www.ins.gov.co/buscador-eventos/BoletinEpidemiologico/2016%20Bolet%C3%ADn%20epidemiol%C3%B3gico%20semana%2052%20-.pdf. Accessed 11 May 2021.

Instituto Nacional de Salud-Ministerio de Salud y Protección Social. Boletín Epidemiológico Semanal. 2017. https://www.ins.gov.co/buscador-eventos/BoletinEpidemiologico/2017%20Bolet%C3%ADn%20epidemiol%C3%B3gico%20semana%2052.pdf.. Accessed 11 May 2021.

Instituto Nacional de Salud-Ministerio de Salud y Protección Social. Boletín Epidemiológico Semanal. 2018a. https://www.ins.gov.co/buscador-eventos/BoletinEpidemiologico/2018%20Bolet%C3%ADn%20epidemiol%C3%B3gico%20semana%2052.pdf. Accessed 13 Aug 2020.

Instituto Nacional de Salud, Ministerio de Salud y Protección Social. Informe de evento. Dengue. 2016. https://www.ins.gov.co/buscador-eventos/Informesdeevento/DENGUE%202017.pdf.. Accessed 19 Aug 2020.

Vélez ID, Quiñones ML, Suárez M, Olano V, Murcia LM, Correa E, et al. Presencia de Aedes albopictus en Leticia, Amazonas, Colombia. Biomédica. 1998;18:192–8.

Cuéllar-Jiménez ME, Velásquez-Escobar OL, González-Obando R, Morales-Reichmann CA. Detección de Aedes albopictus (Skuse) (Diptera : Culicidae) en la ciudad de Cali, Valle del Cauca, Colombia. Biomedica. 2007;27:273–9.

Carvajal JJ, Honorio NA, Díaz SP, Ruiz ER, Asprilla J, Ardila S, et al. Detección de Aedes albopictus (Skuse) (Diptera: Culicidae) en el municipio de Istmina, Chocó, Colombia. Biomedica. 2016;36:438–46.

Ortiz-Canamejoy K, Villota AC. Primera evidencia de Aedes albopictus en el departamento del Putumayo, Colombia. MedUNAB. 2018;21:10–5.

Camacho-Gómez M, Zulueta LP. Primer reporte de Aedes (Stegomyia) albopictus (Skuse) en la Orinoquia colombiana. Biomedica. 2019;39:785–97.

Echeverry-Cárdenas E, López-Castañeda C, Carvajal-Castro JD, Aguirre-Obando OA. Potential geographic distribution of the tiger mosquito Aedes albopictus (Skuse, 1894) (Diptera: Culicidae) in current and future conditions for Colombia. PLoS Negl Trop Dis. 2021;15:e0008212.

Dzul-Manzanilla F, Martínez NE, Cruz-Nolasco M. Evidence of vertical transmission and co-circulation of chikungunya and dengue viruses in field populations of Aedes aegypti (L.) from Guerrero, Mexico. Trans R Soc Trop Med Hyg. 2016;110:141–4.

Aragão CF, Pinheiro VC, Nunes Neto JP, Silva EV, Pereira GJ, Nascimento BL, et al. Natural infection of Aedes aegypti by chikungunya and dengue type 2 virus in a transition area of north-northeast Brazil. Viruses. 2019;11(12):1126.

Alcaldía Municipal de Ibagué. 2020. https://www.ibague.gov.co/portal/seccion/contenido/index.php?type=3&cnt=53f. Accessed 21 Jul 2020.

Departamento Administrativo Nacional de Estadística. Preguntas frecuentes sobre estratificación. 2017. https://www.dane.gov.co/index.php/servicios-al-ciudadano/servicios-informacion/estratificacion-socioeconomica#preguntas-frecuentes. Accessed 29 July 2021.

Instituto de Hidrología, Meteorología y Estudios Ambientales. 2020. http://dhime.ideam.gov.co/atencionciudadano/. Accessed 13 Oct 2020.

Forattini O. Culicidologia médica: Identificação, biologia, epidemiologia, vol. 2. São Paulo: Editora Universidade de São Paulo; 2002.

Santos CS, Pie MR, da Rocha TC, Navarro-Silva MA. Molecular identification of blood meals in mosquitoes (Diptera, Culicidae) in urban and forested habitats in southern Brazil. PLoS One. 2019;14:e0212517.

Lane J. Neotropical Culicidae, vol. 1–2. São Paulo: University of São Paulo; 1953.

Santiago GA, Vergne E, Quiles Y, Cosme J, Vazquez J, Medina JF, et al. Analytical and clinical performance of the CDC Real Time RT-PCR assay for detection and typing of dengue virus. PLoS Negl Trop Dis. 2013;7:e2311.

Jalal S, Malekshahi S, Ghalejoogh ZY, Ghavvami N, Jandaghi N, Shahsiah R, et al. Detection and typing of human papilloma viruses by nested multiplex polymerase chain reaction assay in cervical cancer. Jundishapur J Microbiol. 2015;8:e26441.

Molaei G, Andreadis TG, Armstrong PM, Anderson JF, Vossbrinck CR. Host feeding patterns of Culex mosquitoes and West Nile virus transmission, northeastern United States. Emerg Infect Dis. 2006;12:468–74.

Centers for Disease Control and Prevention (CDC). Mosquito Surveillance Software. 2020. https://www.cdc.gov/westnile/resourcepages/mosqSurvSoft.html#:~:text=The%20simplest%20estimate%2C%20the%20minimum,goals%20of%20the%20surveillance%20program. Accessed 13 Aug 2020.

Instituto Nacional de Salud-Ministerio de Salud y Protección Social. Boletín Epidemiológico Semanal. 2018. https://www.ins.gov.co/buscador-eventos/BoletinEpidemiologico/2018%20Bolet%C3%ADn%20epidemiológico%20semana%2042.pdf. Accessed 31 Aug 2020.

Instituto Nacional de Salud-Ministerio de Salud y Protección Social. Boletín Epidemiológico Semanal. 2018. https://www.ins.gov.co/buscador-eventos/BoletinEpidemiologico/2018%20Bolet%C3%ADn%20epidemiológico%20semana%2045.pdf. Accessed 31 Aug 2020.

Instituto Nacional de Salud-Ministerio de Salud y Protección Social. Boletín Epidemiológico Semanal. 2019. https://www.ins.gov.co/buscador-eventos/BoletinEpidemiologico/2019%20Bolet%C3%ADn%20epidemiol%C3%B3gico%20semana%205.pdf. Accessed 31 Aug 2020.

Instituto Nacional de Salud-Ministerio de Salud y Protección Social. Boletín Epidemiológico Semanal. 2019. https://www.ins.gov.co/buscador-eventos/BoletinEpidemiologico/2019%20Bolet%C3%ADn%20epidemiológico%20semana%2010.pdf. Accessed 31 Aug 2020.

Instituto Nacional de Salud-Ministerio de Salud y Protección Social. Boletín Epidemiológico Semanal. 2020. https://www.ins.gov.co/buscador-eventos/BoletinEpidemiologico/2020_Boletin_epidemiologico_semana_15.pdf. Accessed 13 Aug 2020.

Instituto Nacional de Salud-Ministerio de Salud y Protección Social. Boletín Epidemiológico Semanal. 2020. https://www.ins.gov.co/buscador-eventos/BoletinEpidemiologico/2020_Boletin_epidemiologico_semana_24.pdf. Accessed 13 Aug 2020.

dos Reis IC, Gibson G, Ayllón T, Tavares AM, Galvão de Araújo JM, da Silva Monteiro E, et al. Entomo-virological surveillance strategy for dengue, Zika and chikungunya arboviruses in field-caught Aedes mosquitoes in an endemic urban area of the Northeast of Brazil. Acta Trop. 2019;197:105061.

Costa-da-Silva AL, Ioshino RS, Petersen V, Lima AF, Cunha M, dos Passos M, et al. First report of naturally infected Aedes aegypti with chikungunya virus genotype ECSA in the Americas. PLoS Negl Trop Dis. 2017;11:e0005630.

Costa Monteiro FJ, Paixão Mourão FR, D’Athaide Ribeiro ES, da Silva Rêgo MO, da Costa Frances PA, Picanço Souto RN, et al. Prevalence of dengue, Zika and chikungunya viruses in Aedes (Stegomyia) aegypti (Diptera: Culicidae) in a medium-sized city, Amazon, Brazil. Rev Inst Med Trop São Paulo. 2020;62:e10.

Cevallos V, Ponce P, Waggoner JJ, Pinsky BA, Coloma J, Quiroga C, et al. Zika and chikungunya virus detection in naturally infected Aedes aegypti in Ecuador. Acta Trop. 2018;177:74–80.

Instituto Nacional de Salud, Ministerio de Salud y Protección Social. Informe de evento. Dengue. 2018. https://www.ins.gov.co/buscador-eventos/Informesdeevento/DENGUE_2018.pdf. Accessed 19 Aug 2020.

Instituto Nacional de Salud, Ministerio de Salud y Protección Social. Informe de evento. Dengue. 2019. https://www.ins.gov.co/buscador-eventos/Informesdeevento/DENGUE_2019.pdf. Accessed 19 Aug 2020.

Instituto Nacional de Salud, Ministerio de Salud y Protección Social. Informe de evento. Dengue. 2017. https://www.ins.gov.co/buscador-eventos/Informesdeevento/DENGUE%202017.pdf Accessed 19 Aug 2020.

Boshell J, Groot H, Gacharna M, Márquez G, González M, Gaitán M, et al. Dengue en Colombia. Biomedica. 1986;6:101–6.

Mendez JA, Usme-Ciro JA, Domingo C, Rey G, Sánchez JA, Tenorio A, et al. Phylogenetic history demonstrates two different lineages of dengue type 1 virus in Colombia. Virol J. 2010;7:226.

Instituto Nacional de Salud-Ministerio de Salud y Protección Social. Boletín Epidemiológico Semanal. 2019. https://www.ins.gov.co/buscador-eventos/BoletinEpidemiologico/2019%20Bolet%C3%ADn%20epidemiológico%20semana%2018.pdf. Accessed 23 April 2020.

Gasut P, Couderc T, Lepuit M, Roque P, Ng LFP. Chikungunya virus pathogenesis and immunity. Vector Borne Zoonotic Dis. 2015;15:241–9.

Pearson T, Barney G. Zika virus: Immunity and vaccine development. Cell. 2016;177:625–63.

World Health Organization. Global strategy for dengue prevention and control 2012–2020. Geneva: WHO Geneva; 2012.

Mulligan K, Dixon J, Sinn CHJ, Elliott SJ. Is dengue a disease of poverty? A systematic review. Pathog Glob Health. 2015;109:10–8.

Gubler DJ. Dengue, urbanization and globalization: the unholy trinity of the 21st century. Trop Med Health. 2001;39:3–11.

Charette M, Berrang-Ford L, Llanos-Cuentas AE, Cárcamo C, Kulkarni M. What caused the 2012 dengue outbreak in Pucallpa, Peru? A socio-ecological autopsy. Soc Sci Med. 2017;174:122–32.

Jaramillo-Martinez G, Vasquez-Serna H, Chavarro-Ordoñez R, Rojas-Gomez O, Jimenez C. Ibagué Saludable: a novel tool of Information and communication technologies for surveillance, prevention and control of dengue, chikungunya, Zika and other vector-borne diseases in Colombia. J Infect Public Health. 2018;11:145–6.

Tempelis CH. Host-feeding patterns of mosquitoes, with a review of advances in analysis of blood meals by serology. J Med Entomol. 1975;11:635–53.

Scott TW, Chow E, Strickman D, Kittayapong P, Wirtz RA, Lorenz LH, et al. Blood-feeding patterns of Aedes aegypti (Diptera: Culicidae) collected in a rural Thai Village. J Med Entomol. 1993;30:922–7.

Tinker ME, Olano VA. Ecología del Aedes aegypti en un pueblo de Colombia Sur América. Biomedica. 1993;13:5–14.

Ponlawat A, Harrington LC. Blood feeding patterns of Aedes aegypti and Aedes albopictus in Thailand. J Med Entomol. 2005;42:844–9.

Scott TW, Amerasinghe PH, Morrison AC, Lorenz LH, Clark GG, Strickman D, et al. Longitudinal studies of Aedes aegypti (L.) (Diptera: Culicidae) in Thailand and Puerto Rico: blood feeding frequency. J Med Entomol. 2000;37:89–101.

Instituto de Hidrología, Meteorología y Estudios Ambientales. 2017. http://www.ideam.gov.co/web/tiempo-y-clima/clima. Accessed 29 July 2021.

Gubler DJ. Dengue and dengue hemorrhagic fever. Clin Microbiol Rev. 1998;11:480–96.

Heintze C, Velazco M, Kroeger A. What do community-based dengue control programmes achieve? A systematic review of published evaluations. Trans R Soc Trop Med Hyg. 2007;101:317–25.

Vazquez-Prokopec GM, Galvin WA, Kelly R, Kitron U. A new, Cost-effective, battery-powered aspirator for adult mosquito collections. J Med Entomol. 2009;46:1256–9.

Maia MF, Robinson A, John A, Mgando J, Simfukwe E, Moore SJI. Comparison of the CDC Backpack aspirator and the Prokopack aspirator for sampling indoor- and outdoor-resting mosquitoes in southern Tanzania. Parasites Vectors. 2011;4:124.

Pérez-Castro R, Castellanos JE, Olano VA, Matiz MI, Jaramillo JF, Vargas SL, et al. Detection of all four dengue serotypes in Aedes aegypti female mosquitoes collected in a rural area in Colombia. Mem Inst Oswaldo Cruz. 2016;111:233–40.

Koyoc-Cardeña E, Medina-Barreiro A, Cohuo-Rodríguez A, Pavía-Ruz N, Lenhart A, Ayora-Talavera G, et al. Estimating absolute indoor density of Aedes aegypti using removal sampling. Parasites Vectors. 2019;12:250.

Clark GG, Seda H, Gubler DJ. Use of a CDC backpack aspirator for surveillance of Aedes aegypti in San Juan, Puerto Rico. J Am Mosq Control Assoc. 1994;10:119–24.

Ball ST. The BG-Sentinel trap as a suitable tool for Aedes aegypti surveillance in Far North Queensland, Australia. Dissertation. Queensland: James Cook University; 2010.

Johnson PH, Spitzauer V, Ritchie SA. Field sampling rate of BG-Sentinel traps for Aedes aegypti (Diptera: Culicidae) in suburban Cairns Australia. J Med Entomol. 2012;29:29–34.

Li Y, Su X, Zhou G, Zhang H, Puthiyakunnon S, Shuai S, Cai S, et al. Comparative evaluation of the efficiency of the BG-Sentinel trap, CDC light trap and mosquito-oviposition trap for the surveillance of vector mosquitoes. Parasites Vectors. 2016;9:446.

Maciel-de-Freitas R, Eiras AE, Lourenço-de-Oliveira R. Field evaluation of effectiveness of the BG-Sentinel, a new trap for capturing adult Aedes aegypti (Diptera: Culicidae). Mem Inst Oswaldo Cruz. 2006;101:321–5.

Williams CR, Long SA, Russell RC, Ritchie SA. Field efficacy of the BG-Sentinel compared with CDC Backpack Aspirators and CO2-baited EVS traps for collection of adult Aedes aegypti in Cairns, Queensland, Australia. J Am Mosq Control Assoc. 2006;22:296–300.

Sivagnaname N, Gunasekaran K. Need for an efficient adult trap for the surveillance of dengue vectors. Indian J Med Res. 2012;136:739–49.

de Lamballerie X, Leroy E, Charrel RN, Ttsetsarkin K, Higgs S, Gould EA. Chikungunya virus adapts to tiger mosquito via evolutionary convergence: a sign of things to come? Virol J. 2008;5:33–6.

Foster WA, Walker ED. Mosquitoes (Culicidae). In: Mullen GR, Durden LA, editors. Medical and veterinary entomology. 2nd ed. London: Academic Press; 2009.

Wong PS, Li MZ, Chong CS, Ng LC, Tan CH. Aedes (Stegomyia) albopictus (Skuse): A potential vector of Zika virus in Singapore. PLoS Negl Trop Dis. 2013;7:e2348.

Thông tin
Thông tin xuất bản

Parasites and Vectors

Thông tin tác giả