The role of different Culex mosquito species in the transmission of West Nile virus and avian malaria parasites in Mediterranean areas.
Culex modestus
Culex perexiguus
Culex pipiens
Passer domesticus
Haemosporidia
basic reproduction number R0
emerging infectious diseases
flavivirus
mosquitoes
vector-borne pathogens
zoonosis
Journal
Transboundary and emerging diseases
ISSN: 1865-1682
Titre abrégé: Transbound Emerg Dis
Pays: Germany
ID NLM: 101319538
Informations de publication
Date de publication:
Mar 2021
Mar 2021
Historique:
revised:
07
07
2020
received:
22
01
2020
accepted:
26
07
2020
pubmed:
5
8
2020
medline:
1
7
2021
entrez:
5
8
2020
Statut:
ppublish
Résumé
Vector-borne diseases, especially those transmitted by mosquitoes, have severe impacts on public health and economy. West Nile virus (WNV) and avian malaria parasites of the genus Plasmodium are mosquito-borne pathogens that may produce severe disease and illness in humans and birds, respectively, and circulate in an endemic form in southern Europe. Here, we used field-collected data to identify the impact of Culex pipiens, Cx. perexiguus and Cx. modestus, on the circulation of both WNV and Plasmodium in Andalusia (SW Spain) using mathematical modelling of the basic reproduction number (R
Substances chimiques
Antibodies, Viral
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
920-930Subventions
Organisme : Spanish Ministry of Science and Innovation
ID : CGL2015-65055-P
Organisme : Spanish Ministry of Science and Innovation
ID : PGC2018-095704-B-I00
Organisme : Junta de Andalucía
ID : P11-RNM-7038
Organisme : Instituto de Salud Carlos III
ID : CP13/00114
Organisme : Ministry of Science, Innovation and Universities
ID : FJCI-2017-34394
Organisme : Spanish Society of Ethology and Evolutionary Ecology
Organisme : 2017 Leonardo Grant for Researchers and Cultural Creators, BBVA Foundation
Informations de copyright
© 2020 Wiley-VCH GmbH.
Références
Alcaide, M., Rico, C., Ruiz, S., Soriguer, R., Muñoz, J., & Figuerola, J. (2009). Disentangling vector-borne transmission networks: A universal DNA barcoding method to identify vertebrate hosts from arthropod bloodmeals. PLoS One, 4, e7092. https://doi.org/10.1371/journal.pone.0007092
Angenvoort, J., Brault, A. C., Bowen, R. A., & Groschup, M. H. (2013). West Nile viral infection of equids. Veterinary Microbiology, 167(1-2), 168-180. https://doi.org/10.1016/j.vetmic.2013.08.013
Asghar, M., Hasselquist, D., Hansson, B., Zehtindjiev, P., Westerdahl, H., & Bensch, S. (2015). Hidden costs of infection: Chronic malaria accelerates telomere degradation and senescence in wild birds. Science, 347(6220), 436-438.
Atkinson, C. T., Woods, K. L., Dusek, R. J., Sileo, L. S., & Iko, W. M. (1995). Wildlife disease and conservation in Hawaii: Pathogenicity of avian malaria (Plasmodium relictum) in experimentally infected Iiwi (Vestiaria coccinea). Parasitology, 111(Suppl. 1), S59-S69.
Balenghien, T., Vazeille, M., Grandadam, M., Schaffner, F., Zeller, H., Reiter, P., … Bicout, D. J. (2008). Vector competence of some French Culex and Aedes mosquitoes for West Nile virus. Vector-Borne and Zoonotic Diseases, 8(5), 589-596.
Banet-Noach, C., Simanov, L., & Malkinson, M. (2003). Direct (non-vector) transmission of West Nile virus in geese. Avian Pathology, 32(5), 489-494. https://doi.org/10.1080/0307945031000154080
Beck, C., Jimenez-Clavero, M., Leblond, A., Durand, B., Nowotny, N., Leparc-Goffart, I., … Lecollinet, S. (2013). Flaviviruses in Europe: Complex circulation patterns and their consequences for the diagnosis and control of West Nile disease. International Journal of Environmental Research and Public Health, 10(11), 6049-6083. https://doi.org/10.3390/ijerph10116049
Becker, N., Petric, D., Zgomba, M., Boase, C., Madon, M., Dahl, C., & Kaiser, A. (2010). Mosquitoes and their control. Berlin, Germany: Springer Science & Business Media.
Beerntsen, B. T., James, A. A., & Christensen, B. M. (2000). Genetics of mosquito vector competence. Microbiology and Molecular Biology Reviews, 64, 115-137. https://doi.org/10.1128/MMBR.64.1.115-137.2000
Bowman, C., Gumel, A. B., Van den Driessche, P., Wu, J., & Zhu, H. (2005). A mathematical model for assessing control strategies against West Nile virus. Bulletin of Mathematical Biology, 67(5), 1107-1133. https://doi.org/10.1016/j.bulm.2005.01.002
Brugman, V., Hernández-Triana, L., Medlock, J., Fooks, A., Carpenter, S., & Johnson, N. (2018). The role of Culex pipiens L. (Diptera: Culicidae) in virus transmission in Europe. International Journal of Environmental Research and Public Health, 15(2), 389.
Dadam, D., Robinson, R. A., Clements, A., Peach, W. J., Bennett, M., Rowcliffe, J. M., & Cunningham, A. A. (2019). Avian malaria-mediated population decline of a widespread iconic bird species. Royal Society Open Science, 6(7), 182197. https://doi.org/10.1098/rsos.182197
Del Amo, J., Llorente, F., Figuerola, J., Soriguer, R. C., Moreno, A. M., Cordioli, P., … Jiménez-Clavero, M. Á. (2014). Experimental infection of house sparrows (Passer domesticus) with West Nile virus isolates of Euro-Mediterranean and North American origins. Veterinary Research, 45(1), 33.
Diekmann, O., Heesterbeek, J. A. P., & Roberts, M. G. (2009). The construction of next-generation matrices for compartmental epidemic models. Journal of the Royal Society Interface, 7(47), 873-885. https://doi.org/10.1098/rsif.2009.0386
Engler, O., Savini, G., Papa, A., Figuerola, J., Groschup, M., Kampen, H., … Johnson, N. (2013). European surveillance for West Nile virus in mosquito populations. International Journal of Environmental Research and Public Health, 10(10), 4869-4895. https://doi.org/10.3390/ijerph10104869
Fecchio, A., Chagas, C. R. F., Bell, J. A., & Kirchgatter, K. (2020). Evolutionary ecology, taxonomy, and systematics of avian malaria and related parasites. Acta Tropica, 204, 105364. https://doi.org/10.1016/j.actatropica.2020.105364
Ferraguti, M., Martínez-de la Puente, J., Bensch, S., Roiz, D., Ruiz, S., Viana, D. S., … Figuerola, J. (2018). Ecological determinants of avian malaria infections: An integrative analysis at landscape, mosquito and vertebrate community levels. Journal of Animal Ecology, 87(3), 727-740. https://doi.org/10.1111/1365-2656.12805
Ferraguti, M., Martínez-de la Puente, J., Muñoz, J., Roiz, D., Ruiz, S., Soriguer, R., & Figuerola, J. (2013). Avian Plasmodium in Culex and Ochlerotatus mosquitoes from southern Spain: Effects of season and host-feeding source on parasite dynamics. PLoS One, 8(6), e66237. https://doi.org/10.1371/journal.pone.0066237
Ferraguti, M., Martínez-de La Puente, J., Roiz, D., Ruiz, S., Soriguer, R., & Figuerola, J. (2016). Effects of landscape anthropization on mosquito community composition and abundance. Scientific Reports, 6, 29002. https://doi.org/10.1038/srep29002
Ferraguti, M., Martínez-de la Puente, J., Soriguer, R., Llorente, F., Jiménez-Clavero, M. Á., & Figuerola, J. (2016). West Nile virus-neutralizing antibodies in wild birds from southern Spain. Epidemiology & Infection, 144(9), 1907-1911. https://doi.org/10.1017/S0950268816000133
Figuerola, J., Soriguer, R., Rojo, G., Tejedor, C. G., & Jiménez-Clavero, M. Á. (2007). Seroconversion in wild birds and local circulation of West Nile virus, Spain. Emerging Infectious Diseases, 13(12), 1915. https://doi.org/10.3201/eid1312.070343
Funk, S., Nishiura, H., Heesterbeek, H., Edmunds, W. J., & Checchi, F. (2013). Identifying transmission cycles at the human-animal interface: The role of animal reservoirs in maintaining gambiense human african trypanosomiasis. PLoS Computational Biology, 9(1), e1002855. https://doi.org/10.1371/journal.pcbi.1002855
García-Bocanegra, I., Arenas-Montes, A., Napp, S., Jaén-Téllez, J. A., Fernández-Morente, M., Fernández-Molera, V., & Arenas, A. (2012). Seroprevalence and risk factors associated to West Nile virus in horses from Andalusia, Southern Spain. Veterinary Microbiology, 160(3-4), 341-346. https://doi.org/10.1016/j.vetmic.2012.06.027
Garcia-Bocanegra, I., Jaen-Tellez, J. A., Napp, S., Arenas-Montes, A., Fernandez-Morente, M., Fernandez-Molera, V., & Arenas, A. (2011). West Nile fever outbreak in horses and humans, Spain, 2010. Emerging Infectious Diseases, 17(12), 2397. https://doi.org/10.3201/eid1712.110651
Gómez-Díaz, E., & Figuerola, J. (2010). New perspectives in tracing vector-borne interaction networks. Trends in Parasitology, 26(10), 470-476. https://doi.org/10.1016/j.pt.2010.06.007
Gutiérrez-López, R., Martínez-de la Puente, J., Gangoso, L., Soriguer, R. C., & Figuerola, J. (2015). Comparison of manual and semi-automatic DNA extraction protocols for the barcoding characterization of hematophagous louse flies (Diptera: Hippoboscidae). Journal of Vector Ecology, 40(1), 11-15. https://doi.org/10.1111/jvec.12127
Gutiérrez-López, R., Martínez-de la Puente, J., Gangoso, L., Soriguer, R., & Figuerola, J. (2020). Plasmodium transmission differs between mosquito species and parasite lineages. Parasitology, 147(4), 441-447.
Gutiérrez-López, R., Martínez-de la Puente, J., Gangoso, L., Yan, J., Soriguer, R., & Figuerola, J. (2019). Experimental reduction of host Plasmodium infection load affects mosquito survival. Scientific Reports, 9(1), 8782. https://doi.org/10.1038/s41598-019-45143-w
Hellgren, O., Bensch, S., & Malmqvist, B. (2008). Bird hosts, blood parasites and their vectors - Associations uncovered by molecular analyses of black fly blood meals. Molecular Ecology, 17, 1605-1613. https://doi.org/10.1111/j.1365-294X.2007.03680.x
Hellgren, O., Waldenström, J., & Bensch, S. (2004). A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. Journal of Parasitology, 90, 797-802. https://doi.org/10.1645/GE-184R1
Huppert, A., & Katriel, G. (2013). Mathematical modelling and prediction in infectious disease epidemiology. Clinical Microbiology and Infection, 19(11), 999-1005. https://doi.org/10.1111/1469-0691.12308
Jupp, P. G., & McIntosh, B. M. (1970). Quantitative experiments on the vector capability of Culex (Culex) univittatus Theobald with West Nile and Sindbis viruses. Journal of Medical Entomology, 7, 371-373.
Kilpatrick, A. M., Daszak, P., Jones, M. J., Marra, P. P., & Kramer, L. D. (2006). Host heterogeneity dominates West Nile virus transmission. Proceedings Biological Sciences, 273(1599), 2327-2333.
Kilpatrick, A. M., Kramer, L. D., Campbell, S. R., Alleyne, E. O., Dobson, A. P., & Daszak, P. (2005). West Nile virus risk assessment and the bridge vector paradigm. Emerging Infectious Diseases, 11(3), 425. https://doi.org/10.3201/eid1103.040364
Kilpatrick, A. M., LaDeau, S. L., & Marra, P. P. (2007). Ecology of West Nile virus transmission and its impact on birds in the western hemisphere. The Auk, 124, 1121-1136. https://doi.org/10.1093/auk/124.4.1121
Kimura, M., Darbro, J. M., & Harrington, L. C. (2010). Avian malaria parasites share congeneric mosquito vectors. Journal of Parasitology, 96, 144-151. https://doi.org/10.1645/GE-2060.1
Komar, N., Burns, J., Dean, C., Panella, N. A., Dusza, S., & Cherry, B. (2001). Serologic evidence for West Nile virus infection in birds in Staten Island, New York, after an outbreak in 2000. Vector-Borne and Zoonotic Diseases, 1(3), 191-196. https://doi.org/10.1089/153036601753552558
Llorente, F., García-Irazábal, A., Pérez-Ramírez, E., Cano-Gómez, C., Sarasa, M., Vázquez, A., & Jiménez-Clavero, M. Á. (2019). Influence of flavivirus co-circulation in serological diagnostics and surveillance: A model of study using West Nile, Usutu and Bagaza viruses. Transboundary and Emerging Diseases, 66(5), 2100-2106. https://doi.org/10.1111/tbed.13262
Malkinson, M., & Banet, C. (2002). The role of birds in the ecology of West Nile virus in Europe and Africa. In J. S. Mackenzie, A. D. T. Barrett, & V. Deubel (Eds.), Japanese Encephalitis and West Nile Viruses (pp. 309-322). Berlin, Germany: Springer.
Martínez-de la Puente, J., Ferraguti, M., Ruiz, S., Roiz, D., Llorente, F., Pérez-Ramírez, E., … Figuerola, J. (2018). Mosquito community influences West Nile virus seroprevalence in wild birds: Implications for the risk of spillover into human populations. Scientific Reports, 8(1), 2599. https://doi.org/10.1038/s41598-018-20825-z
Martínez-de la Puente, J., Ferraguti, M., Ruiz, S., Roiz, D., Soriguer, R., & Figuerola, J. (2016). Culex pipiens forms and urbanization: Effects on blood feeding sources and transmission of avian Plasmodium. Malaria Journal, 15, 589. https://doi.org/10.1186/s12936-016-1643-5
Martínez-de la Puente, J., Martínez, J., Rivero-de Aguilar, J., Herrero, J., & Merino, S. (2011). On the specificity of avian blood parasites: Revealing specific and generalist relationships between Haemosporidians and biting midges. Molecular Ecology, 20, 3275-3287. https://doi.org/10.1111/j.1365-294X.2011.05136.x
Marzal, A., Ricklefs, R. E., Valkiūnas, G., Albayrak, T., Arriero, E., Bonneaud, C., … Bensch, S. (2011). Diversity, loss, and gain of malaria parasites in a globally invasive bird. PLoS One, 6, e21905. https://doi.org/10.1371/journal.pone.0021905
Medeiros, M. C., Anderson, T. K., Higashiguchi, J. M., Kitron, U. D., Walker, E. D., Brawn, J. D., … Hamer, G. L. (2014). An inverse association between West Nile virus serostatus and avian malaria infection status. Parasites & Vectors, 7(1), 415. https://doi.org/10.1186/1756-3305-7-415
Merino, S., Moreno, J., Sanz, J. J., & Arriero, E. (2000). Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus). Proceedings Biological Sciences, 267(1461), 2507-2510.
Molaei, G., Andreadis, T. G., Armstrong, P. M., Anderson, J. F., & Vossbrinck, C. R. (2006). Host feeding patterns of Culex mosquitoes and West Nile virus transmission, northeastern United States. Emerging Infectious Diseases, 12(3), 468.
Muñoz, J., Ruiz, S., Soriguer, R., Alcaide, M., Viana, D. S., Roiz, D., … Figuerola, J. (2012). Feeding patterns of potential West Nile virus vectors in south-west Spain. PLoS One, 7(6), e39549. https://doi.org/10.1371/journal.pone.0039549
National Academies of Sciences, Engineering, and Medicine. (2016). Global health impacts of vector-borne diseases: Workshop summary. National Academies Press. Retrieved from https://www.ncbi.nlm.nih.gov/books/NBK355538/?report=reader
Nishiura, H., Hoye, B., Klaasen, M., Bauer, S., & Heesterbeek, H. (2009). How to find natural reservoir hosts from endemic prevalence in a multi-host population: A case study of influenza in waterfowl. Epidemics, 1(2), 118-128. https://doi.org/10.1016/j.epidem.2009.04.002
Patz, J., Graczyk, T. K., Geller, N., & Vittor, A. Y. (2000). Effects of environmental change on emerging parasitic diseases. International Journal for Parasitology, 30, 1395-1405. https://doi.org/10.1016/S0020-7519(00)00141-7
Pawelek, K. A., Niehaus, P., Salmeron, C., Hager, E. J., & Hunt, G. J. (2014). Modeling dynamics of Culex pipiens complex populations and assessing abatement strategies for West Nile virus. PLoS One, 9(9), e108452. https://doi.org/10.1371/journal.pone.0108452
Pérez-Ramírez, E., Llorente, F., & Jiménez-Clavero, M. Á. (2014). Experimental infections of wild birds with West Nile virus. Viruses, 6(2), 752-781. https://doi.org/10.3390/v6020752
Randolph, S. E., & Dobson, A. D. (2012). Pangloss revisited: A critique of the dilution effect and the biodiversity-buffers-disease paradigm. Parasitology, 139(7), 847-863. https://doi.org/10.1017/S0031182012000200
Rivero, A., & Gandon, S. (2018). Evolutionary ecology of avian malaria: Past to present. Trends in Parasitology, 34, 712-726. https://doi.org/10.1016/j.pt.2018.06.002
Rizzoli, A., Bolzoni, L., Chadwick, E. A., Capelli, G., Montarsi, F., Grisenti, M., … Rosà, R. (2015). Understanding West Nile virus ecology in Europe: Culex pipiens host feeding preference in a hotspot of virus emergence. Parasites & Vectors, 8, 213. https://doi.org/10.1186/s13071-015-0831-4
Sacks, J. M., Bolin, S. R., & Crowder, S. V. (1989). Prevalence estimation from pooled samples. American Journal of Veterinary Research, 50, 205-206.
Sambri, V., Capobianchi, M., Charrel, R., Fyodorova, M., Gaibani, P., Gould, E., … Landini, M. P. (2013). West Nile virus in Europe: Emergence, epidemiology, diagnosis, treatment, and prevention. Clinical Microbiology and Infection, 19(8), 699-704. https://doi.org/10.1111/1469-0691.12211
Sánchez-Seco, M. P., Rosario, D., Domingo, C., Hernández, L., Valdés, K., Guzmán, M. G., & Tenorio, A. (2005). Generic RT-nested-PCR for detection of flaviviruses using degenerated primers and internal control followed by sequencing for specific identification. Journal of Virological Methods, 126(1-2), 101-109. https://doi.org/10.1016/j.jviromet.2005.01.025
Santiago-Alarcon, D., Palinauskas, V., & Schaefer, H. M. (2012). Diptera vectors of avian Haemosporidian parasites: Untangling parasite life cycles and their taxonomy. Biological Reviews, 87(4), 928-964. https://doi.org/10.1111/j.1469-185X.2012.00234.x
Schuler, L. A., Khaitsa, M. L., Dyer, N. W., & Stoltenow, C. L. (2004). Evaluation of an outbreak of West Nile virus infection in horses: 569 cases (2002). Journal of the American Veterinary Medical Association, 225, 1084-1089. https://doi.org/10.2460/javma.2004.225.1084
Sergeant, E. S. G. (2019). Epitools epidemiological calculators. Ausvet Pty Ltd. Retrieved from http://epitools.ausvet.com.au
Tolle, M. A. (2009). Mosquito-borne diseases. Current Problems in Pediatric and Adolescent Health Care, 39(4), 97-140. https://doi.org/10.1016/j.cppeds.2009.01.001
U.S. Geological Survey. (2000). West Nile moves bird-to-bird in lab. Retrieved from https://archive.usgs.gov/archive/sites/www.usgs.gov/newsroom/article.asp-ID=562.html
Valkiūnas, G. (2005). Avian malaria parasites and other Haemosporidia. New York, NY: CRC Press.
Valkiūnas, G. (2011). Haemosporidian vector research: Marriage of molecular and microscopical approaches is essential. Molecular Ecology, 20(15), 3084-3086. https://doi.org/10.1111/j.1365-294X.2011.05187.x
Valkiūnas, G., Žiegytė, R., Palinauskas, V., Bernotienė, R., Bukauskaitė, D., Ilgūnas, M., … Iezhova, T. A. (2015). Complete sporogony of Plasmodium relictum (lineage pGRW4) in mosquitoes Culex pipiens pipiens, with implications on avian malaria epidemiology. Parasitology Research, 114(8), 3075-3085. https://doi.org/10.1007/s00436-015-4510-3
Van Riper, III, C., Van Riper, S. G., Goff, M. L., & Laird, M. (1986). The epizootiology and ecological significance of malaria in Hawaiian landbirds. Ecological Monographs, 56, 327-344.
Vázquez, A., Ruiz, S., Herrero, L., Moreno, J., Molero, F., Magallanes, A., … Tenorio, A. (2011). West Nile and Usutu viruses in mosquitoes in Spain, 2008-2009. The American Journal of Tropical Medicine and Hygiene, 85(1), 178-181. https://doi.org/10.4269/ajtmh.2011.11-0042
Vázquez, A., Sánchez-Seco, M.-P., Palacios, G., Molero, F., Reyes, N., Ruiz, S., … Tenorio, A. (2012). Novel flaviviruses detected in different species of mosquitoes in Spain. Vector-Borne and Zoonotic Diseases, 12(3), 223-229. https://doi.org/10.1089/vbz.2011.0687
Ventim, R., Ramos, J. A., Osório, H., Lopes, R. J., Pérez-Tris, J., & Mendes, L. (2012). Avian malaria infections in western European mosquitoes. Parasitology Research, 111, 637-645. https://doi.org/10.1007/s00436-012-2880-3
Vogels, C. B., Göertz, G. P., Pijlman, G. P., & Koenraadt, C. J. (2017). Vector competence of European mosquitoes for West Nile virus. Emerging Microbes & Infections, 6(1), 1-13. https://doi.org/10.1038/emi.2017.82
Vorou, R. M., Papavassiliou, V. G., & Tsiodras, S. (2007). Emerging zoonoses and vector-borne infections affecting humans in Europe. Epidemiology and Infections, 135, 1231-1247. https://doi.org/10.1017/S0950268807008527
Wonham, M. J., de-Camino-Beck, T., & Lewis, M. A. (2004). An epidemiological model for West Nile virus: Invasion analysis and control applications. Proceedings Biological Sciences, 271(1538), 501-507.
Zannoli, S., & Sambri, V. (2019). West Nile Virus and Usutu virus co-circulation in Europe: Epidemiology and implications. Microorganisms, 7(7), 184. https://doi.org/10.3390/microorganisms7070184