Iyaloo et al.171 have provided guidelines for selecting sites for mosquito control trials. Before implementing an area-wide integrated IMS-control strategy, similar paired sites should be selected according to the vector population (in terms of isolation, density, presence of competing species, etc.) and ecological factors (climate, landscape, etc.). It is recommended to target a vector population that is naturally isolated from immigration, and if possible, with a sole IMS species.
Indeed, the presence of other IMS increases the workload of monitoring based on larval/pupal indices or on egg counts in ovitraps as it implies the identification of Aedes species at immature stages (see 7.2). The selected sites should also be ecologically representative of the region to potentially expand the integrated IMS-control strategy, as well as stable, so that the variability of environmental conditions will not affect the results.171 In urban or suburban areas, socio-economic parameters should also be considered. In New Jersey, high poverty and a low education level were positively associated with a high abundance of Ae. albopictus.174 Practical considerations should also be taken into account, such as existing facilities, a manageable site size and access to the whole site. Finally, the social, ethical and legal aspects of the integrated IMS-control strategy need to be considered before implementation.171
7.2. Monitoring of Aedes mosquitoes
The monitoring of Aedes mosquitoes is crucial in order to compare infestation levels between different sites and to evaluate the effectiveness of an integrated IMS-control strategy. Several indices are traditionally used in developing countries to evaluate Aedes populations: house index
(percentage of houses with at least one active breeding sites), container index (percentage of containers with larvae), Breteau index (number of active breeding sites per 100 premises) and ovitraps index (average proportion of ovitraps with eggs).38 However, larval indices are of limited value in European countries because of differences in socio-economic and structural conditions characterizing human dwellings and the availability of breeding sites in public areas.38 The PPI (number of pupae per premise) and PHI (number of pupae per hectare) seem to be more appropriate for European urban areas, particularly the latter one applicable to public and private areas.38 Moreover, pupal indices exploit the strong correlation between the number of pupae and the number of adults in a defined area based on the low natural mortality of the pupae.
Ovitraps are the most widely used methods to monitor Aedes mosquito populations as they are inexpensive, sensitive and practical for area-wide surveys.20 Indeed, the mean number of Ae.
albopictus eggs in ovitraps was found to be positively correlated with counts from PPI, PHI and human landing catches in Italy during the chikungunya outbreak in 2007.19 In areas where several IMS occur, species must be identified from eggs, involving time-consuming labor in the laboratory (egg storage, egg hatching, larval rearing). Alternatively, MALDI-TOF MS (matrix-assisted laser desorption/ionization time of flight mass spectrometry) has been developed for easy and rapid identification of IMS.172
Sticky traps collect ovipositing and resting females, and allow direct identification of Aedes sp.
Estimates of adult populations from sticky traps were demonstrated to be highly positively correlated with estimates from ovitraps.53 Sticky traps have been used successfully worldwide for the monitoring of Ae. albopictus and Ae. aegypti.53,54,173 In Italy, the efficacy of insecticide applications has been evaluated using sticky traps and mosquito emerging traps which consist in adhesive traps designed for the collection of adults visiting and emerging from catch basins.21 BGS traps which attract mostly host-seeking adult females can also be set to monitor Aedes mosquito populations during integrated IMS-control programs.174 In New-Jersey, Ae. albopictus populations were surveyed weekly with BGS traps and ovitraps to examine the efficacy of active source reduction, insecticide applications and public education.25 BGS traps were more sensitive than ovitraps to detect Ae. albopictus early in the season and to compare treated and untreated sites. However, the deployment of BGS traps over a wide area is costly and unpractical due to need of a power-supply.
To overcome some of the limitations of entomological indicators, recent studies have been done to develop simple, rapid, and highly sensitive complementary indicators to evaluate the level of human exposure to Aedes bites and the efficacy of control strategies.175 When a female mosquito bites, it injects saliva containing highly immunogenic molecules. Human antibody responses, such as IgG, to one Aedes species saliva can be measured to assess the specific exposure of individuals to this Aedes species. Specific biomarkers for Ae. albopictus and Ae. aegypti saliva proteins are being developed and have been validated in La Réunion Island and in Bolivia, respectively.175,176 Even if these biomarkers are species-specific, a cross-reactivity has been observed between Ae. albopictus and Ae. aegypti, especially in high immune responders.175
7.3. Implementing an integrated IMS-control strategy
The implementation of an integrated IMS-control strategy in Europe should take into account the target species, its ecology and the public health concern, i.e. nuisance or disease transmission.177 In the latter case, insecticide treatments and fine-scale removal of breeding sites are recommended in the areas around the reported foci as it has been already implemented in Europe to limit the transmission of chikungunya or dengue by Ae. albopictus.178,179 On the other hand, when the aim of an integrated IMS-control strategy is to achieve a medium/long-term population reduction in order to decrease the biting nuisance and the risk of an arbovirus outbreak, the timing and choice of the treatment should be determined by the population dynamics of the target species.177 For instance, methods such as insecticide spraying are more effective for rapidly reducing high-density mosquito populations or in the phase of major expansion,21 while genetic methods such as SIT are more effective at controlling low-density populations.171 The choice of the control method should consider its effectiveness, specificity, residual effect, selection for resistance and ecological impact. For example, the use of larvicides is one of the most effective methods if treatment is focused on the most productive breeding sites in an area; this may differ in urban, suburban and rural areas. Source reduction methods, which are costly and time-consuming, should involve the public in a community-based approach. More generally, the success of an integrated IMS-control strategy relies on cooperation between political decision-makers, public authorities, scientists and the general public.177,180 Finally, the implementation of an integrated IMS-control strategy has to be in line with financial and human resources.
7.4. Modeling approaches and cost-effectiveness analyses
Recently, modeling approaches have proved very helpful in optimizing integrated IMS-control strategies by testing several control methods at a theoretical level.161 Modeling studies have investigated the effectiveness of different control methods such as genetic techniques (e.g. RIDL, SIT), source reduction and/or insecticides, applied alone or in combination.161,181-183 Models have also been used to assess the effectiveness of insecticides in reducing Ae. aegypti adult abundance and to predict the evolution of insecticide resistance in mosquito populations.184 In this way, Luz et al.184 demonstrated that larval and adult controls were optimal at the beginning of the dengue season. In addition, spatial and space−time modeling approaches are very helpful in planning the implementation of an integrated IMS-control strategy (e.g. in terms of site selection and timing of treatment) by mapping the spatio-temporal distribution of IMS and exploring the influence of environmental factors.185 The effects of spatial clustering of integrated IMS-control strategies can also be assessed according to different levels of spatial coverage and control method combinations.186 Finally, cost-effectiveness analyses facilitate comparisons between integrated IMS-control strategies and can inform policy decisions.187 Several studies have underlined the benefits of a real-time vector monitoring system to orientate the vector control campaign alongside a community-based approach using with routine vertical Aedes control, including source reduction and larvicide and adulticide applications.188,189
8. CONCLUSIONS
The implementation and evaluation of integrated IMS-control strategies against Aedes mosquitoes, especially Ae. albopictus, are warranted in Europe, particularly through large-scale field trials. Of the IMS-control methods discussed in this review, several have been successfully used against Ae albopictus mainly outside of Europe. These include source reduction (2), predation by copepods (4.2), larvicide application (4.3, 4.4, 4.5, 5.1), adulticide spraying (5.2) and SIT (6.1). Mechanical methods (3) have been evaluated in large areas, but only against Ae. aegypti; lethal ovitraps or gravid traps should also be effective against Ae. albopictus. New approaches such as pyriproxyfen auto-dissemination (5.1), ATSB (5.2) or IIT (4.6) based on Wolbachia infection have shown promising results in laboratory conditions or semi-field experiments, supporting their potential for future
implementation at a larger scale. Lastly, emerging genetic methods need to be developed for Ae.
albopictus; so far only Ae. aegypti mosquitoes have been genetically modified.
As underlined in previous studies, before implementing an integrated IMS-control strategy, entomological surveys are necessary to monitor the IMS and to select similar paired sites for large-scale trials. This allows the efficacy of control methods to be evaluated by determining if there has been a decrease in the adult population and/or egg oviposition in the treated site compared to the control site. Finally, tools such as mapping and modeling should be developed in order to optimize integrated IMS-control strategy, and cost-effectiveness analyses should be carried out to guide policy decisions.
In conclusion, there is a large range of vector control methods against Aedes mosquitoes.
Traditional methods such as source reduction, public education and insecticide application are routinely implemented by municipilaties to reduce Aedes populations, but with limited success, probably because of a poor participation of communities, and a lack of coordination and syncronised implementation. Innovative approaches such as pyriproxyfen auto-dissemination, genetic or Wolbachia based methods have to be sufficiently developped to demonstrate their efficacy and sustainability, and could be considered in programs of combined implementation afterwards.
As a general rule, an integrated IMS-control strategy requires the coordinated involvement of local authorities, private partners, organized society and communities. A high level of public cooperation is necessary from the beginning of integrated IMS-control programs, and only a continued support from both communities and local authorities can achieve a long-term effect. A key to success might be to customize integrated IMS-control strategy to each community according to the local Aedes infestations (key containers, infestation level, seasonal activity) and the specific socioeconomics characteristics of the locality.
ACKNOWLEDGMENTS
This work was funded by the Autonomous Province of Trento (Italy), Research funds for Grandi Progetti, Project LExEM (Laboratory of Excellence for Epidemiology and Modelling, http://www.lexem.eu). It was also partially funded by EU Grant FP7-261504 EDENext and is catalogued by the EDENext Steering Committee as EDENext337 (http://www.edenext.eu). The
contents of this publication are the sole responsibility of the authors and do not necessarily reflect the views of the European Commission.
REFERENCES
1 Deblauwe I, Sohier C, Schaffner F, Rakotoarivony LM and Coosemans M, Implementation of surveillance of invasive mosquitoes in Belgium according to the ECDC guidelines. Parasit Vectors 7:201 (2014).
2 Medlock JM, Hansford KM, Schaffner F, Versteirt V, Hendrickx G, Zeller H and Van Bortel W, A Review of the Invasive Mosquitoes in Europe: Ecology, Public Health Risks, and Control Options.
Vector Borne Zoonotic Dis 12:435-447 (2012).
3 Schaffner F, Medlock JM and Van Bortel W, Public health significance of invasive mosquitoes in Europe. Clin Microbiol Infect 19:685-692 (2013).
4 Schaffner F, Bellini R, Petric D, Scholte E-J, Zeller H and Rakotoarivony LM, Development of guidelines for the surveillance of invasive mosquitoes in Europe. Parasit Vectors 6:209 (2013).
5 Kampen H and Werner D, Out of the bush: the Asian bush mosquito Aedes japonicus japonicus (Theobald, 1901) (Diptera, Culicidae) becomes invasive. Parasit Vectors 7:59 (2014).
6 Versteirt V, Pecor JE, Fonseca DM, Coosemans M and Van Bortel W, Confirmation of Aedes koreicus (Diptera: Culicidae) in Belgium and description of morphological differences between Korean and Belgian specimens validated by molecular identification. Zootaxa 3191:21-32 (2012).
7 Montarsi F, Martini S, Dal Pont M, Delai N, Milone NF, Mazzucato M, Soppelsa F, Cazzola L, Cazzin S, Ravagnan S, Ciocchetta S, Russo F and Capelli G, Distribution and habitat
characterization of the recently introduced invasive mosquito Aedes koreicus (Hulecoeteomyia koreica), a new potential vector and pest in north-eastern Italy. Parasit Vectors 6:292 (2013).
8 Scholte EJ, Dik M, Justicia AI, Den Hartog W, Schoelitsz B, Brooks M, Braks M and Steeghs M, Findings and control of two invasive exotic mosquito species, Aedes albopictus and Ae.
atropalpus (Diptera: Culicidae) in the Netherlands, 2011. Euro Mosq Bull 30:1-14 (2012).
9 Wheeler AW and Petrie WD, An overview of Aedes aegypti and Aedes albopictus control in the British Overseas Territory of the Cayman Islands. Euro Surveill 12:E071122.3. (2007).
10 Bousses P, Dehecq JS, Brengues C and Fontenille D, Updated inventory of mosquitoes (Diptera:
Culicidae) of the island of La Reunion, Indian Ocean. Bull Soc Pathol Exot 106:113-125 (2013).
11 Urdaneta-Marquez L and Failloux A-B, Population genetic structure of Aedes aegypti, the principal vector of dengue viruses. Infect Genet Evol 11:253-261 (2011).
12 Carrieri M, Bellini R, Maccaferri S, Gallo L, Maini S and Celli G, Tolerance thresholds for Aedes albopictus and Aedes caspius in Italian urban areas. J Am Mosq Control Assoc 24:377-386 (2008).
13 Chebabi Abramides G, Roiz D, Guitart R, Quintana S and Gimenez N, Control of the Asian tiger mosquito (Aedes albopictus) in a firmly established area in Spain: risk factors and people's involvement. Trans R Soc Trop Med Hyg 107:706-714 (2013).
14 Randolph SE and Rogers DJ, The arrival, establishment and spread of exotic diseases: patterns and predictions. Nat Rev Microbiol 8:361-371 (2010).
15 Rezza G, Nicoletti L, Angelini R, Romi R, Finarelli AC, Panning M, Cordioli P, Fortuna C, Boros S, Magurano F, Silvi G, Angelini P, Dottori M, Ciufolini MG, Majori GC and Cassone A, CHIKV study group, Infection with chikungunya virus in Italy: an outbreak in a temperate region.
Lancet 370:1840-1846 (2007).
16 Tomasello D and Schlagenhauf P, Chikungunya and dengue autochthonous cases in Europe, 2007-2012. Travel Med Infect Dis 11:274-284 (2013).
17 Calzolari M, Bonilauri P, Bellini R, Caimi M, Defilippo F, Maioli G, Albieri A, Medici A, Veronesi R, Pilani R, Gelati A, Angelini P, Parco V, Fabbi M, Barbieri I, Lelli D, Lavazza A, Cordioli P and Dottori M, Arboviral Survey of Mosquitoes in Two Northern Italian Regions in 2007 and 2008.
Vector Borne Zoonotic Dis 10:875-884 (2010).
18 Handbook for Integrated Vector Management. World Health Organization, Geneva, Switzerland (2012).
19 Carrieri M, Angelini P, Venturelli C, Maccagnani B and Bellini R, Aedes albopictus (Diptera:
Culicidae) Population Size Survey in the 2007 Chikungunya Outbreak Area in Italy. II: Estimating Epidemic Thresholds. J Med Entomol 49:388-399 (2012).
20 Chebabi Abramides G, Roiz D, Guitart R, Quintana S, Guerrero I and Gimenez N, Effectiveness of a multiple intervention strategy for the control of the tiger mosquito (Aedes albopictus) in Spain. Trans R Soc Trop Med Hyg 105:281-288 (2011).
21 Caputo B, Ienco A, Manica M, Petrarca V, Rosà R and della Torre A, New adhesive traps to monitor urban mosquitoes with a case study to assess efficacy of insecticide control strategies in temperate areas. Parasit Vectors 8:134 (2015).22 Duvallet G and de Gentile L, Protection personnelle antivectorielle. IRD Editions, Marseille, France (2012).
23 Debboun M and Strickman D, Insect repellents and associated personal protection for a reduction in human disease. Med Vet Entomol 27:1-9 (2013).
24 Banks SD, Murray N, Wilder-Smith A and Logan JG, Insecticide-treated clothes for the control of vector-borne diseases: a review on effectiveness and safety. Med Vet Entomol 28:14-25 (2014).
25 Fonseca DM, Unlu I, Crepeau T, Farajollahi A, Healy SP, Bartlett-Healy K, Strickman D, Gaugler R., Hamilton G, Kline D and Clark GG, Area-wide management of Aedes albopictus. Part 2:
Gauging the efficacy of traditional integrated pest control measures against urban container mosquitoes. Pest Manag Sci 69:1351-1361(2013).
26 Richards SL, Ghosh SK, Zeichner BC and Apperson CS, Impact of source reduction on the spatial distribution of larvae and pupae of Aedes albopictus (Diptera : Culicidae) in suburban
neighborhoods of a Piedmont community in North Carolina. J Med Entomol 45:617-628 (2008).
27 Dowling Z, Armbruster P, LaDeau SL, DeCotiis M, Mottley J and Leisnham PT, Linking Mosquito Infestation to Resident Socioeconomic Status, Knowledge, and Source Reduction Practices in Suburban Washington, DC. Ecohealth 10:36-47 (2013).
28 Carrieri M, Angelini P, Venturelli C, Maccagnani B and Bellini R, Aedes albopictus (Diptera:
Culicidae) Population Size Survey in the 2007 Chikungunya Outbreak Area in Italy. I.
Characterization of Breeding Sites and Evaluation of Sampling Methodologies. J Med Entomol 48:1214-1225 (2011).
29 Versteirt V, Schaffner F, Garros C, Dekoninck W, Coosemans M and Van Bortel W, Introduction and Establishment of the Exotic Mosquito Species Aedes japonicus japonicus (Diptera:
Culicidae) in Belgium. J Med Entomol 46:1464-1467 (2009).
30 Yee DA, Kneitel JM and Juliano SA, Environmental Correlates of Abundances of Mosquito Species and Stages in Discarded Vehicle Tires. J Med Entomol 47:53-62 (2010).
31 Nazareth T, Teodosio R, Porto G, Goncalves L, Seixas G, Silva AC and Sousa CA, Strengthening the perception-assessment tools for dengue prevention: a cross-sectional survey in a
temperate region (Madeira, Portugal). BMC Public Health 14 (2014).
32 Unlu I, Farajollahi A, Strickman D and Fonseca DM, Crouching Tiger, Hidden Trouble: Urban Sources of Aedes albopictus (Diptera: Culicidae) Refractory to Source-Reduction. Plos One 8:e77999 (2013).
33 Carrieri M, Bacchi M, Bellini R and Maini S, On the competition occurring between Aedes albopictus and Culex pipiens (Diptera : Culicidae) in Italy. Environ Entomol 32:1313-1321 (2003).
34 Costanzo KS, Mormann K and Juliano SA, Asymmetrical competition and patterns of abundance of Aedes albopictus and Culex pipiens (Diptera : Culicidae). J Med Entomol 42:559-570 (2005).
35 Unlu I, Faraji A, Indelicato N and Fonseca DM, The hidden world of Asian tiger mosquitoes:
immature Aedes albopictus (Skuse) dominate in rainwater corrugated extension spouts. Trans R Soc Trop Med Hyg 108:699-705 (2014).
36 Boyer S, Foray C and Dehecq J-S, Spatial and temporal heterogeneities of Aedes albopictus density in La Reunion Island: rise and weakness of entomological indices. PloS One 9:e91170 (2014).
37 Marciel-de-Freitas R and Lourenço-de-Oliveira R, Does targeting key-containers effectively reduce Aedes aegypti population density? Trop Med Int Health 16:965-973 (2011).
38 Petric D, Bellini R, Scholte E-J, Rakotoarivony LM and Schaffner F, Monitoring population and environmental parameters of invasive mosquito species in Europe. Parasit Vectors 7:187 (2014).
39 Jacups SP, Rapley LP, Johnson PH, Benjamin S and Ritchie SA, Bacillus thuringiensis var.
israelensis Misting for Control of Aedes in Cryptic Ground Containers in North Queensland, Australia. Am J Trop Med Hyg 88:490-496 (2013).
40 Bartlett-Healy K, Hamilton G, Healy S, Crepeau T, Unlu I, Farajollahi A, Fonseca D, Gaugler R, Clark GG and Strickman D, Source Reduction Behavior as an Independent Measurement of the Impact of a Public Health Education Campaign in an Integrated Vector Management Program for the Asian Tiger Mosquito. Int J Environ Res Public Health 8:1358-1367 (2011).
41 Grantham A, Anderson AL and Kelley T, Door to Door Survey and Community Participation to Implement a New County Mosquito Control Program in Wayne County, North Carolina, USA. Int J Environ Res Public Health 6:2150-2159 (2009).
42 Healy K, Hamilton G, Crepeau T, Healy S, Unlu I, Farajollah A and Fonseca DM, Integrating the Public in Mosquito Management: Active Education by Community Peers Can Lead to Significant Reduction in Peridomestic Container Mosquito Habitats. PLoS One 9:e108504 (2014).
43 Kittayapong P, Thongyuan S, Olanratmanee P, Aumchareoun W, Koyadun S, Kittayapong R and Butraporn P, Application of eco-friendly tools and eco-biosocial strategies to control dengue vectors in urban and peri-urban settings in Thailand. Pathog Glob Health 106:446-454 (2012).
44 Brown D, Sustainable mosquito control in California: a template for the world, in Vector biology, ecology and control, ed. by Atkinson PW. Springer Science+Buisness Media, Dordrecht, the Netherlands, pp.203-207 (2010).
45 Kline DL, Semiochemicals, traps/targets and mass trapping technology for mosquito management. J Am Mosq Control Assoc 23:241-51 (2007).
46 Mackay AJ, Amador M and Barrera R, An improved autocidal gravid ovitrap for the control and surveillance of Aedes aegypti. Parasit Vectors 6:225 (2013).
46 Zeichner BC and Debboun M, The lethal ovitrap: a response to the resurgence of dengue and chikungunya. U.S. Army Med Dep J Jul-Sep:4-11 (2011).
48 Perich MJ, Kardec A, Braga IA, Portal IF, Burge R, Zeichner BC, Brogdon WA and Wirtz RA, Field evaluation of a lethal ovitrap against dengue vectors in Brazil. Med Vet Entomol 17:205-210 (2003).
49 Ritchie SA, Rapley LP, Williams C, Johnson PH, Larkman M, Silcock RM, Long SA and Russell RC, A lethal ovitrap-based mass trapping scheme for dengue control in Australia: I. Public
acceptability and performance of lethal ovitraps. Med Vet Entomol 23:295-302 (2009).
50 Sant'ana AL, Roque RA and Eiras AE, Characteristics of grass infusions as oviposition attractants to Aedes (Stegomyia) (Diptera : culicidae). J Med Entomol 43:214-220 (2006).
51 Darriet F, Zumbo B, Corbel V and Chandre F, [Influence of plant matter and NPK fertilizer on the biology of Aedes aegypti (Diptera: Culicidae)]. Parasite 17:149-154 (2010).
52 Trexler JD, Apperson CS, Gemeno C, Perich MJ, Carlson D and Schal C, Field and laboratory evaluations of potential oviposition attractants for Aedes albopictus (Diptera : Culicidae). J Am Mosq Control Assoc 19:228-234 (2003).
52 Trexler JD, Apperson CS, Gemeno C, Perich MJ, Carlson D and Schal C, Field and laboratory evaluations of potential oviposition attractants for Aedes albopictus (Diptera : Culicidae). J Am Mosq Control Assoc 19:228-234 (2003).