1887
Research Open Access
Like 0

Abstract

Background

Climate is a major factor in the epidemiology of West Nile virus (WNV), a pathogen increasingly pervasive worldwide. Cases increased during 2018 in Israel, the United States and Europe.

Aim

We set to retrospectively understand the spatial and temporal determinants of WNV transmission in Israel, as a case study for the possible effects of climate on virus spread.

Methods

We employed a suitability index to WNV, parameterising it with prior knowledge pertaining to a bird reservoir and species, using local time series of temperature and humidity as inputs. The predicted suitability index was compared with confirmed WNV cases in Israel (2016–2018).

Results

The suitability index was highly associated with WNV cases in Israel, with correlation coefficients of 0.91 (p value = 4 × 10− 5), 0.68 (p = 0.016) and 0.9 (p = 2 × 10− 4) in 2016, 2017 and 2018, respectively. The fluctuations in the number of WNV cases between the years were explained by higher area under the index curve. A new WNV seasonal mode was identified in the south-east of Israel, along the Great Rift Valley, characterised by two yearly peaks (spring and autumn), distinct from the already known single summer peak in the rest of Israel.

Conclusions

By producing a detailed geotemporal estimate of transmission potential and its determinants in Israel, our study promotes a better understanding of WNV epidemiology and has the potential to inform future public health responses. The proposed approach further provides opportunities for retrospective and prospective mechanistic modelling of WNV epidemiology and its associated climatic drivers.

Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2020.25.46.1900629
2020-11-19
2024-11-22
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2020.25.46.1900629
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/25/46/eurosurv-25-46-6.html?itemId=/content/10.2807/1560-7917.ES.2020.25.46.1900629&mimeType=html&fmt=ahah

References

  1. Rizzoli A, Tagliapietra V, Cagnacci F, Marini G, Arnoldi D, Rosso F, et al. Parasites and wildlife in a changing world: The vector-host- pathogen interaction as a learning case. Int J Parasitol Parasites Wildl. 2019;9:394-401.  https://doi.org/10.1016/j.ijppaw.2019.05.011  PMID: 31341772 
  2. Kraemer MUG, Reiner RC Jr, Brady OJ, Messina JP, Gilbert M, Pigott DM, et al. Past and future spread of the arbovirus vectors Aedes aegypti and Aedes albopictus. Nat Microbiol. 2019;4(5):854-63.  https://doi.org/10.1038/s41564-019-0376-y  PMID: 30833735 
  3. Braack L, Gouveia de Almeida AP, Cornel AJ, Swanepoel R, de Jager C. Mosquito-borne arboviruses of African origin: review of key viruses and vectors. Parasit Vectors. 2018;11(1):29.  https://doi.org/10.1186/s13071-017-2559-9  PMID: 29316963 
  4. Franklinos LHV, Jones KE, Redding DW, Abubakar I. The effect of global change on mosquito-borne disease. Lancet Infect Dis. 2019;19(9):e302-12.  https://doi.org/10.1016/S1473-3099(19)30161-6  PMID: 31227327 
  5. Rodrigues Faria N, Lourenço J, Marques de Cerqueira E, Maia de Lima M, Pybus O, Alcantara LC Jnr. Epidemiology of chikungunya virus in Bahia, Brazil, 2014-2015. PLoS Curr. 2016;8:ecurrents.outbreaks.c97507.  https://doi.org/10.1371/currents.outbreaks.c97507e3e48efb946401755d468c28b2  PMID: 27330849 
  6. Faria NR, Azevedo RDSDS, Kraemer MUG, Souza R, Cunha MS, Hill SC, et al. Zika virus in the Americas: Early epidemiological and genetic findings. Science. 2016;352(6283):345-9.  https://doi.org/10.1126/science.aaf5036  PMID: 27013429 
  7. Lourenço J, Maia de Lima M, Faria NR, Walker A, Kraemer MUG, Villabona-Arenas CJ, et al. Epidemiological and ecological determinants of Zika virus transmission in an urban setting. eLife. 2017;6:e29820.  https://doi.org/10.7554/eLife.29820  PMID: 28887877 
  8. Naveca FG, Claro I, Giovanetti M, de Jesus JG, Xavier J, Iani FCM, et al. Genomic, epidemiological and digital surveillance of Chikungunya virus in the Brazilian Amazon. PLoS Negl Trop Dis. 2019;13(3):e0007065.  https://doi.org/10.1371/journal.pntd.0007065  PMID: 30845267 
  9. Wu JT, Peak CM, Leung GM, Lipsitch M. Fractional dosing of yellow fever vaccine to extend supply: a modelling study. Lancet. 2016;388(10062):2904-11.  https://doi.org/10.1016/S0140-6736(16)31838-4  PMID: 27837923 
  10. Faria NR, Kraemer MUG, Hill SC, Goes de Jesus J, Aguiar RS, Iani FCM, et al. Genomic and epidemiological monitoring of yellow fever virus transmission potential. Science. 2018;361(6405):894-9.  https://doi.org/10.1126/science.aat7115  PMID: 30139911 
  11. Gutierrez B, Wise EL, Pullan ST, Logue CH, Bowden TA, Escalera-Zamudio M, et al. Evolutionary Dynamics of Oropouche Virus in South America. J Virol. 2020;94(5):e01127-19. https://doi.org/10.1128/JVI.01127-19  PMID: 31801869 
  12. Vogels CBF, Fros JJ, Göertz GP, Pijlman GP, Koenraadt CJM. Vector competence of northern European Culex pipiens biotypes and hybrids for West Nile virus is differentially affected by temperature. Parasit Vectors. 2016;9(1):393.  https://doi.org/10.1186/s13071-016-1677-0  PMID: 27388451 
  13. Gamino V, Höfle U. Pathology and tissue tropism of natural West Nile virus infection in birds: a review. Vet Res (Faisalabad). 2013;44(1):39.  https://doi.org/10.1186/1297-9716-44-39  PMID: 23731695 
  14. Pérez-Ramírez E, Llorente F, Jiménez-Clavero . Experimental infections of wild birds with West Nile virus. Viruses. 2014;6(2):752-81.  https://doi.org/10.3390/v6020752  PMID: 24531334 
  15. Petersen LR, Brault AC, Nasci RS. West Nile virus: review of the literature. JAMA. 2013;310(3):308-15.  https://doi.org/10.1001/jama.2013.8042  PMID: 23860989 
  16. Chancey C, Grinev A, Volkova E, Rios M. The global ecology and epidemiology of West Nile virus. BioMed Res Int. 2015;2015:376230.  https://doi.org/10.1155/2015/376230  PMID: 25866777 
  17. Murgue B, Zeller H, Deubel V. The ecology and epidemiology of West Nile virus in Africa, Europe and Asia. Curr Top Microbiol Immunol. 2002;267:195-221.  https://doi.org/10.1007/978-3-642-59403-8_10  PMID: 12082990 
  18. Johnson N, Fernández de Marco M, Giovannini A, Ippoliti C, Danzetta ML, Svartz G, et al. Emerging mosquito-borne threats and the response from European and Eastern Mediterranean countries. Int J Environ Res Public Health. 2018;15(12):E2775.  https://doi.org/10.3390/ijerph15122775  PMID: 30544521 
  19. Haussig JM, Young JJ, Gossner CM, Mezei E, Bella A, Sirbu A, et al. Early start of the West Nile fever transmission season 2018 in Europe. Euro Surveill. 2018;23(32):1800428.  https://doi.org/10.2807/1560-7917.ES.2018.23.32.1800428  PMID: 30107869 
  20. European Centre for Disease Prevention and Control (ECDC). Communicable disease threats report - Week 50, 9-15 December 2018. Stockholm: ECDC; 2018. Available from: https://www.ecdc.europa.eu/sites/default/files/documents/communicable-disease-threats-report-15-december-2018.pdf
  21. Wimberly MC, Lamsal A, Giacomo P, Chuang T-W. Regional variation of climatic influences on West Nile virus outbreaks in the United States. Am J Trop Med Hyg. 2014;91(4):677-84.  https://doi.org/10.4269/ajtmh.14-0239  PMID: 25092814 
  22. Kilpatrick AM, Meola MA, Moudy RM, Kramer LD. Temperature, viral genetics, and the transmission of West Nile virus by Culex pipiens mosquitoes. PLoS Pathog. 2008;4(6):e1000092.  https://doi.org/10.1371/journal.ppat.1000092  PMID: 18584026 
  23. Mordecai EA, Cohen JM, Evans MV, Gudapati P, Johnson LR, Lippi CA, et al. Detecting the impact of temperature on transmission of Zika, dengue, and chikungunya using mechanistic models. PLoS Negl Trop Dis. 2017;11(4):e0005568.  https://doi.org/10.1371/journal.pntd.0005568  PMID: 28448507 
  24. Brady OJ, Golding N, Pigott DM, Kraemer MUG, Messina JP, Reiner RC Jr, et al. Global temperature constraints on Aedes aegypti and Ae. albopictus persistence and competence for dengue virus transmission. Parasit Vectors. 2014;7(1):338 https://doi.org/10.1186/1756-3305-7-338  PMID: 25052008 
  25. Ciota AT, Matacchiero AC, Kilpatrick AM, Kramer LD. The effect of temperature on life history traits of Culex mosquitoes. J Med Entomol. 2014;51(1):55-62.  https://doi.org/10.1603/ME13003  PMID: 24605453 
  26. Aharonson-Raz K, Lichter-Peled A, Tal S, Gelman B, Cohen D, Klement E, et al. Spatial and temporal distribution of West Nile virus in horses in Israel (1997-2013)--from endemic to epidemics. PLoS One. 2014;9(11):e113149.  https://doi.org/10.1371/journal.pone.0113149  PMID: 25402217 
  27. Paz S. The West Nile Virus outbreak in Israel (2000) from a new perspective: the regional impact of climate change. Int J Environ Health Res. 2006;16(1):1-13.  https://doi.org/10.1080/09603120500392400  PMID: 16507476 
  28. Lustig Y, Kaufman Z, Mendelson E, Orshan L, Anis E, Glazer Y, et al. Spatial distribution of West Nile virus in humans and mosquitoes in Israel, 2000-2014. Int J Infect Dis. 2017;64:20-6.  https://doi.org/10.1016/j.ijid.2017.08.011  PMID: 28882664 
  29. Bassal R, Shohat T, Kaufman Z, Mannasse B, Shinar E, Amichay D, et al. The seroprevalence of West Nile Virus in Israel: A nationwide cross sectional study. PLoS One. 2017;12(6):e0179774.  https://doi.org/10.1371/journal.pone.0179774  PMID: 28622360 
  30. Orshan L, Bin H, Schnur H, Kaufman A, Valinsky A, Shulman L, et al. Mosquito vectors of West Nile fever in Israel. J Med Entomol. 2008;45(5):939-47.  https://doi.org/10.1093/jmedent/45.5.939  PMID: 18826039 
  31. Malkinson M, Banet C, Weisman Y, Pokamunski S, King R, Drouet M-T, et al. Introduction of West Nile virus in the Middle East by migrating white storks. Emerg Infect Dis. 2002;8(4):392-7.  https://doi.org/10.3201/eid0804.010217  PMID: 11971773 
  32. Leshem Y, Yom-Tov Y. Routes of migrating soaring birds. Ibis. 2008;140(1):41-52.  https://doi.org/10.1111/j.1474-919X.1998.tb04539.x 
  33. Obolski U, Perez PN, Villabona-Arenas CJ, Thézé J, Faria NR, Lourenço J. MVSE: An R-package that estimates a climate-driven mosquito-borne viral suitability index. Methods Ecol Evol. 2019;10(8):1357-70.  https://doi.org/10.1111/2041-210X.13205  PMID: 32391139 
  34. Giovanetti M, Faria NR, Lourenço J, Goes de Jesus J, Xavier J, Claro IM, et al. Genomic and epidemiological surveillance of Zika virus in the Amazon Region. Cell Rep. 2020;30(7):2275-2283.e7.  https://doi.org/10.1016/j.celrep.2020.01.085  PMID: 32075736 
  35. Brady OJ, Godfray HCJ, Tatem AJ, Gething PW, Cohen JM, McKenzie FE, et al. Vectorial capacity and vector control: reconsidering sensitivity to parameters for malaria elimination. Trans R Soc Trop Med Hyg. 2016;110(2):107-17.  https://doi.org/10.1093/trstmh/trv113  PMID: 26822603 
  36. Perez-Guzman PN, Carlos Junior Alcantara L, Obolski U, de Lima MM, Ashley EA, Smithuis F, et al. Measuring mosquito-borne viral suitability in Myanmar and implications for local Zika virus transmission. PLoS Curr. 2018;10:7a.  https://doi.org/10.1371/currents.outbreaks.7a6c64436a3085ebba37e5329ba169e6  PMID: 31032144 
  37. Yang HM, Macoris MLG, Galvani KC, Andrighetti MTM, Wanderley DMV. Assessing the effects of temperature on the population of Aedes aegypti, the vector of dengue. Epidemiol Infect. 2009;137(8):1188-202.  https://doi.org/10.1017/S0950268809002040  PMID: 19192322 
  38. Anis E, Grotto I, Mendelson E, Bin H, Orshan L, Gandacu D, et al. West Nile fever in Israel: the reemergence of an endemic disease. J Infect. 2014;68(2):170-5.  https://doi.org/10.1016/j.jinf.2013.10.009  PMID: 24183889 
  39. Lustig Y, Gosinov R, Zuckerman N, Glazer Y, Orshan L, Sofer D, et al. Epidemiologic and phylogenetic analysis of the 2018 West Nile virus (WNV) outbreak in Israel demonstrates human infection of WNV lineage I. Euro Surveill. 2019;24(1):1800662.  https://doi.org/10.2807/1560-7917.ES.2019.24.1.1800662  PMID: 30621816 
  40. Kain MP, Bolker BM. Can existing data on West Nile virus infection in birds and mosquitos explain strain replacement? Ecosphere. 2017;8(3):e01684.  https://doi.org/10.1002/ecs2.1684 
  41. Reisen WK, Milby MM, Meyer RP, Pfuntner AR, Spoehel J, Hazelrigg JE, et al. Mark-release-recapture studies with Culex mosquitoes (Diptera: Culicidae) in southern California. J Med Entomol. 1991;28(3):357-71.  https://doi.org/10.1093/jmedent/28.3.357  PMID: 1875362 
  42. Simpson JE, Hurtado PJ, Medlock J, Molaei G, Andreadis TG, Galvani AP, et al. Vector host-feeding preferences drive transmission of multi-host pathogens: West Nile virus as a model system. Proc Biol Sci. 2012;279(1730):925-33.  https://doi.org/10.1098/rspb.2011.1282  PMID: 21849315 
  43. Jones CE, Lounibos LP, Marra PP, Kilpatrick AM. Rainfall influences survival of Culex pipiens (Diptera: Culicidae) in a residential neighborhood in the mid-Atlantic United States. J Med Entomol. 2012;49(3):467-73.  https://doi.org/10.1603/ME11191  PMID: 22679852 
  44. Moudy RM, Meola MA, Morin L-LL, Ebel GD, Kramer LD. A newly emergent genotype of West Nile virus is transmitted earlier and more efficiently by Culex mosquitoes. Am J Trop Med Hyg. 2007;77(2):365-70.  https://doi.org/10.4269/ajtmh.2007.77.365  PMID: 17690414 
  45. Wonham MJ, de-Camino-Beck T, Lewis MA. An epidemiological model for West Nile virus: invasion analysis and control applications. Proc Biol Sci. 2004;271(1538):501-7.  https://doi.org/10.1098/rspb.2003.2608  PMID: 15129960 
/content/10.2807/1560-7917.ES.2020.25.46.1900629
Loading

Data & Media loading...

Supplementary data

Submit comment
Close
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error