Research Article, Vector Biol J Vol: 5 Issue: 1
A Door-to-Door Strategy for Aedes albopictus Control in Northern Italy: Efficacy, Cost-Analysis and Public Perception
Luciano Donati*, Marco Carrieri and Romeo Bellini
Sanitary Entomology & Zoology Dept., Centro Agricoltura Ambiente “G.Nicoli”, Crevalcore, Italy
Received: April 03, 2020 Accepted: April 20, 2020 Published: April 27, 2020
Citation: Donati L, Carrieri M, Bellini R (2020) A Door-to-Door Strategy for Aedes albopictus Control in Northern Italy: Efficacy, Cost-Analysis and Public Perception. Vector Biol J 5:1. doi: 10.37532/vbj.2020.5(1).137
Objective: The aim of the study was to evaluate in several Northern Italy urban localities the cost-effectiveness and the public perception of an intensive Ae. albopictus control strategy by integrating accurate inspection and treatment of private areas with the standard disinfestations of catch basins in public areas.
Methods: The applied door-to-door strategy (DtoD) includes periodical inspections of private properties with larval treatment of permanent breeding sites and removal or inactivation of occasional breeding sites, together with direct information to the residents. The effectiveness of the service was assessed in the period 2013-2015 by means of ovitraps and in the period 2015-2017 by human landing collections (HLC). Public perception was evaluated by a survey questionnaire at the end of the season.
Results: In the period 2013-2017, 94.7% of the 41,827planned inspections were managed according to the program, while 5.3% were not made due to detected specific reasons. The reduction in the Ae. albopictus’ density, when compared to similar urban areas managed with the standard mosquito control plan (regular larval treatment of breeding sites in public areas and community engagement), resulted in the range 36-62% when using ovitraps and 69-72% when using HLC. Simple questionnaires distributed to citizens’ to evaluate their perception showed that 59.3-89.2% declared the DtoD service highly effective or effective, while 3.2-13.1% declared DtoD poorly effective or ineffective. The average cost of the DtoD package was in the range 5-9 Euro/inhabitant/year, depending on the local condition, while the average cost of the standard plan at the Emilia-Romagna regional level was calculated in 1.3 Euro/inhabitant/year.
Conclusion: The tested DtoD strategy resulted very effective in the reduction of the Ae. albopictus population in urban context and has been favorably received by the resident population. On the other hand, the strategy requires a remarkable organizational effort.
Keywords: Mosquito control; Larval treatment; Source reduction; Private properties; Urban mosquitoes; Breeding sites; Efficacy evaluation; Cost-Efficacy
In some cases, Public Administrations (PAs) responsible for mosquito control, mainly Municipalities, Public Health Agencies and Regional Bureaux, have implemented monitoring and control programs specifically targeted at this species , including larval control in public areas, information campaigns, Mayor Ordinance and focal adult control. In situations where imported cases of Chikungunya, Dengue and Zika are detected, emergency measures are adopted to prevent possible outbreaks .
Nevertheless, even in the best organized programs, the results are unsatisfactory; mainly because of the insufficient rate of community participation and the lack of political will to fine citizens who disregard the Mayor Ordinance .
The Emilia-Romagna Ae. albopictus management plan is considered one of the best organized plan in Italy and it includes larval control in public road drains, monitoring by ovitraps, the Mayor Ordinance and the use of citizens’ information to obtain community participation [4,5].
In order to make available to the PAs a more effective and feasible Ae. albopictus control strategy, and following the experiences developed in other situations [7-9], we organized and pilot-tested in real operational conditions a door-to-door strategy (DtoD). In this paper, we present the DtoD strategy, the results achieved, and the costeffective evaluation.
Materials and Methods
Pilot trials were conducted in operational conditions involving six small towns in the period 2013-2017 (Table 1), with the support of the Emilia-Romagna Region, the six Municipalities and the Life Conops EU project (www.conops.gr).When possible, the DtoD strategy was applied to the whole target urban area to minimize mosquito immigration from external areas.
|DtoD areas||S.Giovanni P.to||ha 80.45
no. AU 398
no. ovitraps 11
no. AU 806
no. ovitraps 15
no. AU 1,120
no. ovitraps 25
no. HLCs 20
no. AU 1,205
no. HLCs 130
|S.Agata B.se||ha 10.08
no. AU 45
|Castello d’Argile||ha 51.71
no. AU 388
no. ovitraps 10
no. AU 394
no. ovitraps 10
|S.Pietro in C.le||//||//||ha 26.27
no. AU 208
no. ovitraps 10
no. HLCs 15
no. AU 281
no. ovitraps 10
no. HLCs 14
no. AU 983
no. HLCs 96
no. AU 1,004
no. HLCs 80
no. AU 392
no. HLCs 35
no. AU 812
no. HLCs 45
|Control areas||no. ovitraps 31||no. ovitraps 30||no. ovitraps 31
no. HLCs 10
|no. HLCs 123||no. HLCs 80|
Table 1: Urban areas surface extension (ha), private properties (no.), ovitraps (no.) and HLC sessions (no.) under door-to-door trial in the period 2012-2017.
Please refer to the Table 1 which clearly explains the urban areas surface extension (ha), Access Unit (AU) (no.), ovitraps (no.) and HLC sessions (no.) under door-to-door trial in the period 2012-2017.
The applied DtoD strategy consists of the following actions:
• six larval control treatments in public road drains in the period April-September, using manual pump spraying Diflubenzuron (Arysta LifeScience France) or Vectomax®FG (and , Sumitomo Chemical Italia) or Aquatain AMF ™ (polydimethylsiloxane, Bleu Line Italia);
• six DtoD interventions in the period April-September, including source removal, larval treatment of permanent breeding sites using the same products as in public areas and direct information to the residents;
• the introduction of predatory copepods in the large permanent containers;
• the activation of a green phone line to support citizen contact;
• organization of a database to store the contact phone number of each resident, the most appropriate timing for the visits and the number and exact locations of permanent breeding sites in each property;
• communication campaigns including on-site meetings, web news, notes on the major local aggregation points, a personal letter sent by the Municipality to each resident, the notice of the next date of the visit by the Alert System (this is a system some Municipalities have put in place to directly communicate with citizens through SMS if need be).
Because of the high Ae. albopictus carrying-capacity of the urban areas in Northern Italy , it became necessary to develop an intensive DtoD strategy fixing a minimum threshold of properties to be visited in each turn to 95%.
In order to achieve this, the work was organized to take place during late afternoon hours and on Saturdays, when the probability of finding the residents at home was higher.
On few occasions, the operators were supported by the Local Police service in a bid to ensure they were allowed entrance into the properties of residents refusing to let them in.
Properties that, at the first highly accurate inspection conducted at the beginning of the season, had no breeding sites were excluded from successive visits within the season.
The effectiveness of the DtoD in reducing the Ae. albopictus population density was evaluated by two methods:
• In the period 2013-2015, ovitraps checked biweekly  were used in DtoD treated areas in comparison with similar areas where only public road drains were treated;
• While in the period 2015-2017, human landing collection (HLC) sessions were conducted in parallel on the same days and at the same time in DtoD treated vs control areas (Table 1).
HLC session of 15 min each in late afternoons was performed in fixed positions by single operators equipped with manual batteryoperated aspirators during the peak of female Ae. albopictus activities (data not published).
Operators rotated around sampling stations to avoid bias due to difference in personal attraction to mosquitoes.
The residents ’ perception was evaluated by multiple choice questionnaires kept anonymous and distributed door-to-door at the end of the season in DtoD treated areas, in the period 2012-2017.
The cost analysis was based on real cost of hiring personnel, products, equipment and information campaign.
The reach of the DtoD service application has been monitored during the whole period by collecting data on the property access rate and the breeding sites number (Table 2).
|Year||No. planned inspections in subsequent rounds||% inspections managed (± SD)||Mean no. permanent breeding sites/property (± SD)||Mean operational time/property in minutes (± SD)|
|2013||4,030||90.4 (± 3.8)||4.3 (± 3.7)||5.7 (± 1.4)|
|2014||5,935||93.0 (± 1.7)||5.0 (± 5.2)||4.8 (± 2.6)|
|2015||7,884||93.7 (± 3.8)||5.1 (± 4.6)||5.9 (± 1.8)|
|2016||13,071||95.1 (± 3.1)||4.9 (± 4.4)||5.4 (± 6.9)|
|2017||10,867||96.2 (± 3.7)||4.4 (± 3.5)||5.4 (± 2.3)|
Table 2: Number and rate of door-to-door application (including properties without breeding sites), average number of breeding sites treated and average time spent.
Efficacy evaluation by ovitraps
Ovitraps were positioned in the urban areas, in DtoD treated as well as in control areas, from May to the beginning of October, at densities in the range of 0.03-0.3 ovitrap/ha (Table 3).
|Door-to-Door areas||Control areas|
|Year||No. ovitraps||No. masonite
|Total no. eggs||No. eggs/ovitrap/
|No. ovitraps||No. masonite
|Total no. eggs||No.
eggs/ovitrap/ 14days (±SD)
|2013||21||155||38,021||248.7 (± 134.4)||31||273||116,864||408.3 (± 201.6)|
|2014||25||198||28,309||133.3 (± 81.1)||30||261||94,966||355.5 (± 197.1)|
|2015||45||363||144,165||384.0 (± 212.5)||31||272||138,323||597.2 (± 410.7)|
|Total||91||716||210,495||274.9 (± 191.2)||92||806||350,153||454.4 (± 304.4)|
|SS||D. of F.||MS||F||p|
Table 3: Data collected by ovitraps positioned in door-to-door vs control urban areas and ANOVA.
Two way Anova and block Anova (Area*Month F1,3=10.19 and p<0.05) showed a significant effect of DtoD when compared to control areas (where only breeding sites present in public areas were treated) (Table 3).
Egg density reduction rate was about 39% in 2013, 62% in 2014 and 36% in 2015 (global average reduction rate in the three years period was 39%).
Efficacy evaluation by HLC
Data collected by HLC sessions are presented in Table 4.
|Door-to-Door areas||Control areas|
|2015||49||186||3.8 (± 4.2)||10||124||12.4 (± 8.8)|
|2016||261||929||3.6 (± 4.9)||123||1,607||13.1 (± 14.8)|
|2017||125||364||2.9 (± 3.4)||80||758||9.5 (± 9.0)|
|Total||435||1,479||3.4 (± 4.5)||213||2,489||11.7 (± 12.8)|
|SS||D. of F.||MS||F||p|
Table 4: Data collected by HLC sessions in door-to-door vs control urban areas and ANOVA.
Two way Anova and block Anova (area*month F1,3=22.55 and p<0.02) showed a significant effect of DtoD when compared to control areas (Table 4).
The average rate of reduction was about 69% in 2015, 72% in 2016 and 69% in 2017(global average reduction in the three years period was 71%).
Citizens’ perception as evaluated by questionnaires
Three main questions were presented to residents at the end of the season:
What are their opinions on the efficacy of DtoD, expressed by ticking one of the five possible answers: highly effective, effective, not completely effective, poorly effective, and ineffective?
What are their opinions on the efficacy compared to the previous year when DtoD was not applied (question proposed in the first year of DtoD application only): less mosquitoes, same mosquitoes, more mosquitoes?
What is their willingness to have the DtoD service in the next year: yes or no?
In the period 2012-2017, 11,609 questionnaires were distributed to residents in the DtoD treated villages, obtaining a recovery rate of 35.2% (range 20.7-42.1%).
The percentage of citizens declaring the DtoD service highly effective or effective was in the range 59.3-89.2%, while the percentage declaring DtoD poorly effective or ineffective fell in the range 3.2-13.1% (Figure 1).
The second question was presented to residents in villages where the DtoD was being conducted for the first time; in the period 2014-2017.The answers on the perception of the presence of mosquitoes compared to the previous year are reported in Figure 2.
About 80% of the respondents declared fewer mosquitos in the year of DtoD application, about 16% declared same or more mosquitoes, and about 4% declared more mosquitoes than the previous year.
The third question had a large majority of the citizens declaring in favour of having the DtoD service in the next year (Figure 3).
The experience gained from the implementation of the DtoD service in small villages in Northern Italy raised several important issues to be considered when planning an intervention of this type.
A close collaboration with the involved Municipalities in order to inform and ask for active participation of the citizens is essential to achieving the required high rate of properties coverage.
In our case, residents were largely welcoming to the operators, with a very low rate of refusal in the range of 1-2%. The mean rates of refusal showed a tendency to increase slightly with the prolongation of the service: 0.9% in the first year, 1.1% in the second year, and 1.4% in the following years.
The Local Police was involved in few occasions only, to enforce access to properties where the conditions of the backyards were considered possible important breeding sites for Ae. albopictus but the owner would not allow access.
The rate of DtoD coverage tended to increase with the year of application (Table 2) because of the collection of comprehensive contact information allowing the planning of personalized timing of the visits.
In Municipalities where the Alert System was available, the citizens were informed few days before each visit, and the service proceeded smoothly.
The mean operational time per property tended to decrease with the year of application and in the course of the same season, because of the more proficient planning of the visit allowed by the organization of a database with specific information on each resident (Table 5).
|Year||First turn||Second turn||Third turn||Fourth turn||Fifth turn||Sixth turn||Seasonal average|
Table 5: Mean operational time (min) per property in door-to-door service (full package service included).
Because of the high Ae. albopictus carrying-capacity of the villages in Northern Italy, the rate of coverage was planned in such a way as to reach 95% of the entire properties to be treated in each turn.
The mean rate of coverage achieved in the whole period was not far from the planned target (94.7 ± 3.8% SD against 95.00% planned), while the efficacy in the reduction of Ae. albopictus population density as estimated by ovitraps and HLC was lower than expected. Ovitraps showed a reduction in the mean number of eggs/ovitrap collected by 39%, 62% and 36% in 2013, 2014 and 2015 respectively (Table 3).
HLC showed a reduction in the mean number of females/session collected by 69%, 72% and 69% in 2015, 2016 and 2017 respectively (Table 4).
In 2015, the only year when we employed the two efficacy evaluation methods, the ovitraps estimated egg reduction by 35%, while HLC estimated female reduction by 69%.
Previous studies comparing ovitraps and HLC data in Italy found a significant correlation between the two methods [6,13], but this was not the case in our situation. The reason might be due to the probable increase in the number of females laying eggs in ovitraps as a result of the important reduction in the availability of oviposition sites in the DtoD areas, thus influencing the correlation between the two monitoring methods.
Both ovitrap and HLC indicate effectiveness in the reduction of the Ae. albopictus population density well below the 95% corresponding rate of treated properties. We hypothesized that cryptic breeding sites and incomplete larval mortality in treated breeding sites, together with the immigration of females from external areas, might have played a significant role.
The residents’ perception as derived from the survey show a high rate of satisfaction, with 70-80% of the citizens responding positively on the effectiveness of the service (Figures 1-3).
The real costs paid for the DtoD service are shown in the Table 6. The main costs are for personnel and for the management and quality assurance, while the cost for larvicidal products is low. The management costs show a tendency to decrease in successive years, thanks to the acquired detailed information on each property organized in a database.
|Municipality||Year||Cost for field workers (%)||Cost for other activities (%)*||Cost for larvicidal product (%)||Total cost (€)||No. Inhabitants in the DtoD areas||Cost per capita (€)|
|S.Pietro in Casale||2015||47.3||52.2||0.5||5,460.00||615||8.88|
Table 6: Breakdown of costs and unit cost paid for the door-to-door service. (*) including programming, coordination, operator training, support, copepod distribution, evaluation of effectiveness of services.
The average real costs paid annually by Emilia-Romagna Public Administrations to support the standard Ae. albopictus control plan was 1.3 euros per inhabitant with significant variation at the municipality level . The DtoD service, with the modalities described and based on the general conditions in the Italian villages, will require a cost in the range of 5-9 euros/inhabitant/year, depending on the population density and the urban condition (Table 6).
We envisage three main obstacles to the large-scale application of the DtoD service in Italy: the economic sustainability, the legislation regarding the provision of a public service in private properties due to public health emergencies, and the high risk of resistance due to the intensive selective pressure to which the local mosquito population may be submitted .
The work that produced the results presented in this paper has been made possible by the support of the Life Conops project “Development & demonstration of management plans against - the climate change enhanced - invasive mosquitoes in S. Europe” (www.conops.gr, LIFE12 ENV/GR/000466), co-founded by the EU Environmental Funding Programme LIFE+ Environment Policy and Governance; the Regional Health Authority of Emilia-Romagna; and the Municipalities of S. Giovanni in Persiceto, S.Agata Bolognese, Castello d’Argile, S.Pietro in Casale, Bentivoglio and Galliera. We thank Donatella Allegro, Claudia Benazzi, Alessandro Corazza, Fabio Cremonini, Salvatore Esposito, Nicola Fiorani, Donatella Galazzi, Mattia Gherardi, Claudia Manferdini, Fabiana Ruffoni and Luca Sabattini for their hard work and dedication in the field activities.
- Angelini P, Macini P, Finarelli AC, Pol C, Venturelli C, et al. (2008) Chikungunya epidemic outbreak in Emilia-Romagna (Italy) during summer 2007. Parassitologia 50: 97–98.
- Carrieri M, Bellini R, Maccaferri S, Gallo L, Maini S, et al. (2008) Tolerance thresholds for Aedes albopictus and Aedes caspius in Italian urban areas. J Am Mosq Control Assoc 24: 377–386.
- Venturi G, Di Luca M, Fortuna C, Remoli ME, Riccardo F, et al. (2017) Detection of a chikungunya outbreak in Central Italy, August to September 2017. Euro Surveill 22.
- Regione Emilia Romagna. Per una strategia integrata di lotta alla zanzara tigre. Linee guida per gli operatori dell’Emilia-Romagna. 2019. Available from the Emilia Romagna Department of Health, Bologna [accessed March 31, 2020].
- Regione Emilia-Romagna. Piano regionale arbovirosi. 2019. Available from the Emilia Romagna Department of Health, Bologna [accessed March 31, 2020].
- Carrieri M, Angelini P, Venturelli C, Maccagnani B, Bellini R (2012) 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.
- Grantham A, Anderson AL, Kelley T (2009) 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.
- Abramides GC, Roiz D, Guitart R, Quintana S, Guerrero I, et al. (2011) 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.
- Elsinga J, van der Veen HT, Gerstenbluth I, Burgerhof JGM, Dijkstra A, et al. (2017) Community participation in mosquito breeding site control: an interdisciplinary mixed methods study in Curaçao. Parasites & Vectors 10: 434-446.
- Veronesi R, Carrieri M, Maccagnani B, Maini S, Bellini R (2015) Macrocyclops albidus (Copepoda: Cyclopidae) for the biocontrol of Aedes albopictus and Culex pipiens in Italy. J Am Mosq Control Assoc 31: 32-43.
- Carrieri M, Angelini P, Venturelli C, Maccagnani B, Bellini R (2011) 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.
- Carrieri M, Albieri A, Angelini P, Baldacchini F, Venturelli C, et al. (2011) Surveillance of the chikungunya vector Aedes albopictus (Skuse) in Emilia-Romagna (Northern Italy): organizational and technical aspects of a large scale monitoring system. J Vector Ecol 36: 108-116.
- Manica M, Rosà R, della Torre A, Caputo B (2017) From eggs to bites: do ovitrap data provide reliable estimates of Aedes albopictus biting females? PeerJ 5: e2998.
- Canali M, Rivas-Morales S, Beutels P, Venturelli C (2017) The cost of arbovirus disease prevention in Europe: area-wide integrated control of Tiger Mosquito, Aedes albopictus, in Emilia-Romagna, Northern Italy. Int J Environ Res Public Health 14: 444.
- Pichler V, Bellini R, Veronesi R, Arnoldi D, Rizzoli A, et al. (2018) First evidence of resistance to pyrethroid insecticides in Italian Aedes albopictus populations 26 years after invasion. Pest Manag Sci 74: 1319-1327.