A review of the vector management methods to prevent and control outbreaks of West Nile virus infection and the challenge for Europe

Particle and Fibre Toxicology

Wim Van Bortel¹  Herve Zeller¹  Romeo Bellini² 

[1] European Centre for Disease Prevention and Control, Stockholm, Sweden;Centro Agricoltura Ambiente “G.Nicoli”, Via Argini Nord 3351, Crevalcore 40014, Italy

关键词: Europe;    Vector control;    Vector surveillance;    Vector-borne disease;    West Nile virus;   

Others  :  1183556
DOI  :  10.1186/1756-3305-7-323

 received in 2014-02-06, accepted in 2014-06-13,  发布年份 2014

【 摘 要 】

West Nile virus infection is a growing concern in Europe. Vector management is often the primary option to prevent and control outbreaks of the disease. Its implementation is, however, complex and needs to be supported by integrated multidisciplinary surveillance systems and to be organized within the framework of predefined response plans. The impact of the vector control measures depends on multiple factors and the identification of the best combination of vector control methods is therefore not always straightforward. Therefore, this contribution aims at critically reviewing the existing vector control methods to prevent and control outbreaks of West Nile virus infection and to present the challenges for Europe.

Most West Nile virus vector control experiences have been recently developed in the US, where ecological conditions are different from the EU and vector control is organized under a different regulatory frame. The extrapolation of information produced in North America to Europe might be limited because of the seemingly different epidemiology in the European region. Therefore, there is an urgent need to analyse the European experiences of the prevention and control of outbreaks of West Nile virus infection and to perform robust cost-benefit analysis that can guide the implementation of the appropriate control measures. Furthermore, to be effective, vector control programs require a strong organisational backbone relying on a previously defined plan, skilled technicians and operators, appropriate equipment, and sufficient financial resources. A decision making guide scheme is proposed which may assist in the process of implementation of vector control measures tailored on specific areas and considering the available information and possible scenarios.

【 授权许可】

   
2014 Bellini et al.; licensee BioMed Central Ltd.

【 参考文献 】

• [1]Hurlbut HS, Rizk F, Taylor RM, Work TH: A study of the ecology of West Nile virus in Egypt. Am J Trop Med Hygiene 1956, 5(4):579-620.
• [2]Zeller HG, Schuffenecker I: West Nile virus: an overview of its spread in europe and the Mediterranean Basin in contrast to its spread in the Americas. Eur J Clin Microbiol 2004, 23(3):147-156.
• [3]Petersen LR, Carson PJ, Biggerstaff BJ, Custer B, Borchardt SM, Busch MP: Estimated cumulative incidence of West Nile virus infection in US adults, 1999-2010. Epidemiol Infect 2013, 141:591-595.
• [4]Ladbury GA, Gavana M, Danis K, Papa A, Papamichail D, Mourelatos S, Gewehr S, Theocharopoulos G, Bonovas S, Benos A, Panagiotopoulos T: Population seroprevalence study after a west nile virus lineage 2 epidemic, Greece, 2010. Plos One 2013, 8(11):e80432.
• [5]Anderson JF, Main AJ: Importance of vertical and horizontal transmission of West Nile virus by Culex pipiens in the northeastern United States. J Infect Dis 2006, 194(11):1577-1579.
• [6]Andreadis TG, Armstrong PM, Bajwa WI: Studies on hibernating populations of Culex pipiens from a West Nile virus endemic focus in New York City: parity rates and isolation of West Nile virus. J Am Mosq Contr Assoc 2010, 26(3):257-264.
• [7]Bugbee LM, Forte LR: The discovery of West Nile virus in overwintering Culex pipiens (Diptera : Culicidae) mosquitoes in Lehigh County, Pennsylvania. J Am Mosq Contr Assoc 2004, 20(3):326-327.
• [8]Nasci RS, Savage HM, White DJ, Miller JR, Cropp BC, Godsey MS, Kerst AJ, Bennett P, Gottfried K, Lanciotti RS: West Nile virus in overwintering Culex mosquitoes, New York City, 2000. Emerg Infect Dis 2001, 7(4):742-744.
• [9]Reisen WK, Fang Y, Lothrop HD, Martinez VM, Wilson J, O'Connor P, Carney R, Cahoon-Young B, Shafii M, Brault AC: Overwintering of West Nile virus in southern California. J Med Entomol 2006, 43(2):344-355.
• [10]Tesh RB, Parsons R, Siirin M, Randle Y, Sargent C, Guzman H, Wuithiranyagool T, Higgs S, Vanlandingham DL, Bala AA, Haas K, Zerinque B: Year-round West Nile virus activity, Gulf Coast region, Texas and Louisiana. Emerg Infect Dis 2004, 10(9):1649-1652.
• [11]Hubalek Z, Halouzka J: West Nile fever - a reemerging mosquito-borne viral disease in Europe. Emerg Infect Dis 1999, 5(5):643-650.
• [12]Tsai TF, Popovici F, Cernescu C, Campbell GL, Nedelcu NI, Team I: West Nile encephalitis epidemic in southeastern Romania. Lancet 1998, 352(9130):767-771.
• [13]ECDC: Reported cases of West Nile fever for the EU and neighbouring countries. Transmission season 2013 and previous transmission seasons; latest update: 06/11/2013. http://ecdc.europa.eu/en/healthtopics/west_nile_fever/West-Nile-fever-maps/pages/index.aspx webcite
• [14]Calistri P, Giovannini A, Hubalek Z, Ionescu A, Monaco F, Savini G, Lelli R: Epidemiology of west nile in europe and in the mediterranean basin. Open Virol J 2010, 4:29-37.
• [15]Stiasny K, Aberle SW, Heinz FX: Retrospective identification of human cases of West Nile virus infection in Austria (2009 to 2010) by serological differentiation from Usutu and other flavivirus infections. Euro Surveill 2013, 18(43):20614.
• [16]Merdic E, Peric L, Pandak N, Kurolt IC, Turic N, Vignjevic G, Stolfa I, Milas J, Bogojevic MS, Markotic A: West Nile virus outbreak in humans in Croatia, 2012. Coll Antropol 2013, 37(3):943-947.
• [17]Hubalek Z, Halouzka J, Juricova Z: West Nile fever in Czechland. Emerg Infect Dis 1999, 5(4):594-595.
• [18]Hubalek Z, Lukacova L, Halouzka J, Sirucek P, Januska J, Precechtelova J, Prochazka P: Import of West Nile virus infection in the Czech Republic. Eu J Epidemiol 2006, 21(4):323-324.
• [19]Del Giudice P, Schuffenecker I, Vandenbos F, Counillon E, Zeller H: Human West Nile virus, France. Emerg Infect Dis 2004, 10(10):1885-1886.
• [20]Papa A, Danis K, Baka A, Bakas A, Dougas G, Lytras T, Theocharopoulos G, Chrysagis D, Vassiliadou E, Kamaria F, Liona A, Mellou K, Saroglou G, Panagiotopoulos T: Ongoing outbreak of West Nile virus infections in humans in Greece, July - August 2010. Euro Surveill 2010, 15(34):19644.
• [21]Glavits R, Ferenczi E, Ivanics E, Bakonyi T, Mato T, Zarka P, Palya V: Co-occurrence of West Nile fever and circovirus infection in a goose flock in Hungary. Avian Pathol 2005, 34(5):408-414.
• [22]Rizzo C, Vescio F, Declich S, Finarelli AC, Macini P, Mattivi A, Rossini G, Piovesan C, Barzon L, Palu G, Gobbi F, Macchi L, Pavan A, Magurano F, Ciufolini MG, Nicoletti L, Salmaso S, Rezza G: West Nile virus transmission with human cases in Italy, August-September 2009. Euro Surveill 2009, 14(40):19353.
• [23]Connell J, McKeown P, Garvey P, Cotter S, Conway A, O'Flanagan D, O'Herlihy BP, Morgan D, Nicoll A, Lloyd G: Two linked cases of West Nile virus (WNV) acquired by Irish tourists in the Algarve, Portugal. Euro Surveill 2004, 8(32):2517.
• [24]Campbell GL, Ceianu CS, Savage HM: Epidemic West Nile encephalitis in Romania: waiting for history to repeat itself. Ann N Y Acad Sci 2001, 951:94-101.
• [25]Popovic N, Milosevic B, Urosevic A, Poluga J, Lavadinovic L, Nedelijkovic J, Jevtovic D, Dulovic O: Outbreak of West Nile virus infection among humans in Serbia, August to October 2012. Euro Surveill 2013, 18(43):20613.
• [26]Bofill D, Domingo C, Cardenosa N, Zaragoza J, de Ory F, Minguell S, Sanchez-Seco MP, Dominguez A, Tenorio A: Human West Nile virus infection, Catalonia, Spain. Emerg Infect Dis 2006, 12(7):1163-1164.
• [27]Kaptoul D, Viladrich PF, Domingo C, Niubo J, Martinez-Yelamos S, De Ory F, Tenorio A: West Nile virus in Spain: report of the first diagnosed case (in Spain) in a human with aseptic meningitis. Scand J Infect Dis 2007, 39(1):70-71.
• [28]Hubalek Z: European experience with the West Nile virus ecology and epidemiology: could it be relevant for the new world? Viral Immunol 2000, 13(4):415-426.
• [29]Esteves A, Almeida APG, Galao RP, Parreira R, Piedade J, Rodrigues JC, Sousa CA, Novo MT: West Nile virus in Southern Portugal, 2004. Vector-Borne Zoon Dis 2005, 5(4):410-413.
• [30]Almeida APG, Galao RP, Sousa CA, Novo MT, Parreira R, Pinto J, Piedade J, Esteves A: Potential mosquito vectors of arboviruses in Portugal: species, distribution, abundance and West Nile infection. T Roy Soc Trop Med H 2008, 102(8):823-832.
• [31]Calzolari M, Bonilauri P, Bellini R, Albieri A, Defilippo F, Maioli G, Galletti G, Gelati A, Barbieri I, Tamba M, Lelli D, Carra E, Cordioli P, Angelini P, Dottori M: Evidence of simultaneous circulation of West Nile and usutu viruses in mosquitoes sampled in Emilia-Romagna Region (Italy) in 2009. Plos One 2010, 5(12):14324.
• [32]Reusken CBEM, de Vries A, Buijs J, Braks MAH, den Hartog W, Scholte EJ: First evidence for presence of Culex pipiens biotype molestus in the Netherlands, and of hybrid biotype pipiens and molestus in northern Europe. J Vector Ecol 2010, 35(1):210-212.
• [33]Chaskopoulou A, Dovas CI, Chaintoutis SC, Kashefi J, Koehler P, Papanastassopoulou M: Detection and early warning of West Nile Virus circulation in Central Macedonia, Greece, using sentinel chickens and mosquitoes. Vector-Borne Zoon Dis 2013, 13(10):723-732.
• [34]Mouchet J, Rageau J, Laumond C, Hannoun C, Beytout D, Oudar J, Corniou B, Chippaux A: [Epidemiology of West Nile virus: study of a focus in Camargue. V. The fector: Culex modestus Ficalbi Diptera; Culicidae]. Ann Inst Pasteur 1970, 118(6):839-855.
• [35]Zeller H, Lenglet A, Van Bortel W: West Nile virus: the need to strengthen preparedness in Europe. Euro Surveill 2010, 15(34):19647.
• [36]WHO: WHO position statement on integrated vector management. Geneva: World Health Organization; 2008.
• [37]EU: West Nile virus and blood safety introduction to a preparedness plan. Europe: European Commission; 2012.
• [38]CDC: Epidemic/Epizootic West Nile Virus in the United States: Guidelines for Surveillance, Prevention, and Control. Fort Collins, Colorado: Fort Collins: U.S. Department of Health and Human Services, Public Health Service, Centers for Disease Control and Prevention, National Center for Infectious Diseases, Division of Vector-Borne Infectious Diseases; 2003. 3rd Revision
• [39]Connelly CR, Carlson DB: Florida Mosquito Control: The state of the mission as defined by mosquito controllers, regulators, and environmental managers. Florida: Vero Beach, FL: University of Florida, Institute of Food and Agricultural Sciences, Florida Medical Entomology Laboratory; 2009.
• [40]Brown EG: California mosquito-borne virus surveillance & response plan. California: California Department of Public Health Mosquito & Vector Control Association of California University of California; 2011.
• [41]Dale P: Runnelling procedures manual (including environmental management). Report prepared for Redland Shire Council by Pat Dale Faculty of Environmental Sciences Griffith University, August 1997 1997.
• [42]Knight RL, Walton WE, O'Meara GF, Reisen WK, Wass R: Strategies for effective mosquito control in constructed treatment wetlands. Ecol Eng 2003, 21(4–5):211-232.
• [43]Warchot A, Whelan P: Constructed Wetlands in the Northern Territory: guidelines to prevent mosquito breeding. Casuarina NT: Medical Entomology Branch, Centre for Disease Control, Department of Health and Families Services; 2008:0811. PO Box 40596
• [44]Collins FH, Washino RK: The effects of irrigation water source and crop rotation on the abundance of Culex tarsalis in California rice fields. Proc Californian Mos Vector Contr Assoc 1980, 48:103-108.
• [45]Chambers DM, Steelman CD, Schilling PE: The effect of cultural practices on mosquito adundance and distribution in the Louisiana riceland ecosystem. Mosq News 1981, 41:233-240.
• [46]Keiser J, Maltese MF, Erlanger TE, Bos R, Tanner M, Singer BH, Utzinger J: Effect of irrigated rice agriculture on Japanese encephalitis, including challenges and opportunities for integrated vector management. Acta Trop 2005, 95(1):40-57.
• [47]Lawler SP, Dritz DA: Effects of rice straw and water management on riceland mosquitoes. J Med Entomol 2006, 43(5):828-832.
• [48]Ishii T, Sohn SR: Highly polluted larval habitats of the Culex pipiens complex in central Sweden. J Am Mosq Contr Assoc 1987, 3(2):276-281.
• [49]Sanford MR, Chan K, Walton WE: Effects of inorganic nitrogen enrichment on mosquitoes (Diptera : Culicidae) and the associated aquatic community in constructed treatment wetlands. J Med Entomol 2005, 42(5):766-776.
• [50]Chaves LF, Keogh CL, Vazquez-Prokopec GM, Kitron UD: Combined sewage overflow enhances oviposition of Culex quinquefasciatus (Diptera: Culicidae) in urban areas. J Med Entomol 2009, 46(2):220-226.
• [51]Santha CR, Martyn RD, Neill WH, Strawn K: Control of submersed weeds by grass carp in waterlily production ponds. J Aquat Plant Manage 1994, 32:29-33.
• [52]FAO: Interactions between fish and aquatic macrophytes in inland waters. Queensland, Australia: Food and Agriculture Organization of the United Nations; 2000.
• [53]WHO: Update of annotated bibliography of papers relating to the control of moquitoes by the use of fish for the years 1965-1981. Geneva: WHO; 1985.
• [54]Bellini R, Veronesi R, Rizzoli M: Efficacy of various fish species (Carassius auratus (L), Cyprinus carpio (L), Gambusia affinis (Baird and Girard) in the control of rice field mosquitoes in northern Italy. Bull Soc Vector Ecol 1994, 19(2):87-99.
• [55]WHO: The use of fish for mosquito control. Geneva: WHO; 2003.
• [56]Haq S: Developing larvivorous fish network for mosquito control in urban areas: a case study. ICMR Bull 2003, 33(7):69-73.
• [57]FAO: Culture of fish in rice fields. Edited by Halwart M, Gupta VM. Rome: FAO; 2004.
• [58]Kay B, Vu SN: New strategy against Aedes aegypti in Vietnam. Lancet 2005, 365(9459):613-617.
• [59]Hurst T, Ryan P, Brown M, Kay B: Fushing for a mosquito control agent. Arbovirus Res Aust 2005, 9:143-147.
• [60]Marten GG, Nguyen M, Mason BJ, Ngo G: Natural control of Culex quinquefasciatus larvae in residential ditches by the copepod Macrocyclops albidus. J Vector Ecol 2000, 25(1):7-15.
• [61]Soumare MKF, Cilek JE: The effectiveness of Mesocyclops longisetus (Copepoda) for the control of container-inhabiting mosquitoes in residential environments. J Am Mosq Contr Assoc 2011, 27(4):376-383.
• [62]Chevillon C, Bernard C, Marquine M, Pasteur N: Resistance to Bacillus sphaericus in Culex pipiens (Diptera : Culicidae) interaction between recessive mutants and evolution in southern France. J Med Entomol 2001, 38(5):657-664.
• [63]Nielsen-LeRoux C, Rao DR, Murphy JR, Carron A, Mani TR, Hamon S, Mulla MS: Various levels of cross-resistance to Bacillus sphaericus strains in Culex pipiens (Diptera : Culicidae) colonies resistant to B.sphaericus strain 2362. Appl Environ Microb 2001, 67(11):5049-5054.
• [64]Mulla MS, Thavara U, Tawatsin A, Chomposrf J, Su TY: Emergence of resistance and resistance management in field populations of tropical Culex quinquefasciatus to the microbial control agent Bacillus sphaericus. J Am Mosq Contr Assoc 2003, 19(1):39-46.
• [65]Commission Regulation (EC) No 1451/2007 of 4 December 2007 on the second phase of the 10-year work programme referred to in Article 16(2) of Directive 98/8/EC of the European Parliament and of the Council concerning the placing of biocidal products on the market http://eur-lex.europa.eu/legal-content/EN/TXT/?qid=1405494848373&uri=CELEX:02007R1451-20130901 webcite
• [66]WHO: Ultra-Low-Volume application of insecticides for vector control. Geneva: WHO; 1985.
• [67]Mount GA, Biery TL, Haile DG: A review of ultralow-volume aerial sprays of insecticide for mosquito control. J Am Mosq Contr Assoc 1996, 12(4):601-618.
• [68]Mount GA: A critical review of ultralow-volume aerosols of insecticide applied with vehicle-mounted generators for adult mosquito control. J Am Mosq Contr Assoc 1998, 14(3):305-334.
• [69]WHO: Space spray application of insecticides for vector and public health pest control. A practitioner’s guide. Geneva, Switzerland: WHOPES; 2003.
• [70]Bonds JAS: Ultra-low-volume space sprays in mosquito control: a critical review. Med Vet Entomol 2012, 26(2):121-130.
• [71]Latham M, Barber J: Mosquito control in Florida with focus on aerial adulticiding. Outlook Pest Manag 2007, 18:178-183.
• [72]Thomas D, Weedermann M, Billings L, Hoffacker J, Washington-Allen RA: When to spray: a time-scale calculus approach to controlling the impact of West Nile virus. Ecol Soc 2009, 14(2):21.
• [73]Kline DL: Traps and trapping techniques for adult mosquito control. J Am Mosq Contr Assoc 2006, 22(3):490-496.
• [74]Kline DL: Semiochemicals, traps/targets and mass trapping technology for mosquito management. J Am Mosq Contr Assoc 2007, 23(2):241-251.
• [75]Kaufman PE, Butler JF, Nelson C: Evaluation of the Mosquito Sentinel 360 trap in Florida residential environments. J Am Mosq Contr Assoc 2008, 24(4):528-533.
• [76]Smith JP, Cope EH, Walsh JD, Hendrickson CD: Ineffectiveness of mass trapping for mosquito control in St. Andrews State Park, Panama City Beach, Florida. J Am Mosq Contr Assoc 2010, 26(1):43-49.
• [77]Loeb M, Elliott SJ, Gibson B, Fearon M, Nosal R, Drebot M, D'Cuhna C, Harrington D, Smith S, George P, Eyles J: Protective behavior and West Nile virus risk. Emerg Infect Dis 2005, 11(9):1433-1436.
• [78]WHO: Global collaboration for development of pesticides for public health (GCDPP): repellents and toxicants for personal protection. Edited by WHOPES. Geneva: WHO; 2000.
• [79]Peterson C, Coats J: Insect repellents. Past present and future. Pest Outlook 2001, 12:154-158.
• [80]Showyin LR: Recent developments on personal protection methods against vectors. Malaysia; 2005:473-475.
• [81]Tawatsin A, Wratten SD, Scott RR, Thavara U, Techadamrongsin Y: Repellency of volatile oils from plants against three mosquito vectors. J Vector Ecol 2001, 26(1):76-82.
• [82]Fradin MS, Day JF: Comparative efficacy of insect repellents against mosquito bites. New Engl J Med 2002, 347(1):13-18.
• [83]Andrade CFS, Cabrini I: Electronic mosquito repellers induce increased biting rates in Aedes aegypti mosquitoes (Diptera: Culicidae). J Vector Ecol 2010, 35(1):75-78.
• [84]Enayati A, Hemingway J, Garner P: Electronic mosquito repellents for preventing mosquito bites and malaria infection. Cochrane Database of Systematic Reviews 2007, 2:Art. No.: CD005434.
• [85]Chaskopoulou A, Latham MD, Pereira RM, Connelly R, Bonds JAS, Koehler PG: Efficacy of aerial ultra-low volume applications of two novel water-based formulations of unsynergized pyrethroids against riceland mosquitoes in Greece. J Am Mosq Contr Assoc 2011, 27(4):414-422.
• [86]WHO: WHO specifications and evaluations for public health pesticides: Bacillus thuringiensis subspecies israelensis strain AM65-52. Geneva: WHO; 2007.
• [87]WHO: Safety of pyrethroids for public health use. Geneva: WHO; 2005.
• [88]Carr WC, Iyer P, Gammon DW: A dietary risk assessment of the pyrethroid insecticide resmethrin associated with its use for West Nile virus mosquito vector control in California. Sci World J 2006, 6:279-290.
• [89]Peterson RKD, Macedo PA, Davis RS: A human-health risk assessment for West Nile virus and insecticides used in mosquito management. Environ Health Persp 2006, 114(3):366-372.
• [90]Schleier JJ, Macedo PA, Davis RS, Shama LM, Peterson RKD: A two-dimensional probabilistic acute human-health risk assessment of insecticide exposure after adult mosquito management. Stoch Env Res Risk A 2009, 23(5):555-563.
• [91]Andis MD, Sackett SR, Carroll MK, Bordes ES: Strategies for the emergency control of arboviral epidemics in New Orleans. J Am Mosq Contr Assoc 1987, 3(2):125-130.
• [92]Mutebi JP, Delorey MJ, Jones RC, Plate DK, Gerber SI, Gibbs KP, Sun GH, Cohen NJ, Paul WS: The impact of adulticide applications on mosquito density in Chicago, 2005. J Am Mosq Contr Assoc 2011, 27(1):69-76.
• [93]Palmisano CT, Taylor V, Caillouet K, Byrd B, Wesson DM: Impact of West Nile virus outbreak upon St. Tammany Parish Mosquito Abatement District. J Am Mosq Contr Assoc 2005, 21(1):33-38.
• [94]Simpson JE: Emergency mosquito aerial spray response to the 2004 Florida hurricanes Charley, Frances, Ivan, and Jeanne: an overview of control results. J Am Mosq Contr Assoc 2006, 22(3):457-463.
• [95]Reddy MR, Spielman A, Lepore TJ, Henley D, Kiszewski AE, Reiter P: Efficacy of resmethrin aerosols applied from the road for suppressing Culex vectors of West Nile virus. Vector-Borne Zoon Dis 2006, 6(2):117-127.
• [96]Trout RT, Brown GC, Potter MF, Hubbard JL: Efficacy of two pyrethroid insecticides applied as barrier treatments for managing mosquito (Diptera : Culicidae) populations in suburban residential properties. J Med Entomol 2007, 44(3):470-477.
• [97]Lothrop H, Lothrop B, Palmer M, Wheeler S, Gutierrez A, Gomsi D, Reisen WK: Evaluation of pyrethrin and permethrin ground ultra-low volume applications for adult Culex control in rural and urban environments of the Coachella Valley of California. J Am Mosq Contr Assoc 2007, 23(2):190-207.
• [98]Carney RM, Husted S, Jean C, Glaser C, Kramer V: Efficacy of aerial spraying of mosquito adulticide in reducing incidence of West Nile virus, California, 2005. Emerg Infect Dis 2008, 14(5):747-754.
• [99]Lothrop HD, Lothrop BB, Gomsi DE, Reisen WK: Intensive early season adulticide applications decrease arbovirus transmission throughout the Coachella Valley, Riverside County. California. Vector-Borne Zoon Dis 2008, 8(4):475-489.
• [100]Elnaiem DEA, Kelley K, Wright S, Laffey R, Yoshimura G, Reed M, Goodman G, Thiemann T, Reimer L, Reisen WK, Brown D: Impact of aerial spraying of pyrethrin insecticide on Culex pipiens and Culex tarsalis (Diptera: Culicidae) abundance and West Nile virus infection rates in an urban/suburban area of Sacramento County. California. J Med Entomol 2008, 45(4):751-757.
• [101]Macedo PA, Schleier JJ, Reed M, Kelley K, Goodman GW, Brown DA, Peterson RKD: Evaluation of efficacy and human health risk of aerial ultra-low volume applications of pyrethrins and piperonyl butoxide for adult Mosquito management in response to West Nile virus activity in Sacramento County. California. J Am Mosq Contr Assoc 2010, 26(1):57-66.
• [102]Averett E, Neuberger JS, Hansen G, Fox MH: Evaluation of West Nile virus education campaign. Emerg Infect Dis 2005, 11(11):1751-1753.
• [103]WHO: Guidelines for cost-effectiveness analysis of vector control. Geneva: WHO; 1993.
• [104]Zohrabian A, Meltzer MI, Ratard R, Billah K, Molinari NA, Roy K, Scott RD, Petersen LR: West Nile virus economic impact, Louisiana, 2002. Emerg Infect Dis 2004, 10(10):1736-1744.
• [105]Barber LM, Schleier JJ, Peterson RKD: Economic cost analysis of West Nile virus outbreak, Sacramento County, California, USA, 2005. Emerg Infect Dis 2010, 16(3):480-486.
• [106]Domanovic D, Giesecke J: How to define an area where transmission of arthropod-borne disease is occurring? Euro Surveill 2012, 17(20):20171.
• [107]ECDC: West Nile virus risk assessment tool. Stockholm: European Centre for Disease Prevention and Control; 2013.