Vector surveillance in Greece

Introduction

Vector-borne diseases are an emerging threat for Greece but also for Europe. The cluster of malaria cases in 2009 and the West Nile virus outbreak in 2010 have highlighted the health risk of mosquitoes and the need to take measures to combat them. Considering the variety of vector-borne diseases, in this article we will briefly discuss those that have been a serious problem for public health in recent years and also a few diseases that pose a potential threat to our country.

 

Epidemiological Data

 

West Nile virus infection

In the summer-autumn of 2010, a West Nile virus epidemic occurred in Greece for the first time. From early August until November 2010, a total of 262 cases was diagnosed, 191 of which presented with symptoms of the central nervous system and 71 cases with mild symptoms. Thirty-five deaths occurred in elderly people with underlying disease [1].

In 2011, a total of 101 West Nile virus cases was diagnosed, 76 of which presented with symptoms of the central nervous system and 25 with mild symptoms. There were nine deaths of patients older than 65 years who had underlying disease.

In 2012, a total of 161 cases of West Nile virus was diagnosed, 109 of which presented with symptoms of the central nervous system and 52 with mild symptoms. Eighteen deaths occurred in patients older than 70 years with underlying disease [2].

The common house mosquito (Culex pipiens) has been implicated as the  West Nile virus vector in Greece, without excluding the involvement of other species in the transmission cycle. The natural virus reservoirs are different bird species.

 

Malaria

According to the World Health Organization (WHO), Greece has been malaria free since 1974. Annually, 20–50 cases are recorded and are imported from malaria-endemic countries [3]. A small number of cases that were not related to travel or residence in malaria-endemic countries were recorded in 1991, 1999, 2000, 2009 and 2010.

In 2011, 96 malaria cases were recorded, 54 of which were imported (45 were considered to be immigrants from endemic countries and nine were travelers to endemic countries) while 42 had no travel history to malaria-endemic areas (34 patients were of Greek nationality, and eight were foreigners from non-endemic countries)

In 2012, Greece recorded 92 malaria cases, 73 of which were imported (64 were considered to be immigrants from endemic countries and nine were travelers to endemic countries) [4].

Malaria is transmitted from human to human via the bite of the Anopheles mosquito. Anopheles spp. are present in almost all regions of the country and the species that have been proved to be malaria vectors in Greece are Anopheles sacharovi, Anopheles superpictus and Anopheles maculipenis.

 

Dengue fever

The last recorded outbreak of dengue in Greece was from 1925 to 1928 [5, 6]. In September 2012, a probable dengue case was reported but further investigation did not confirm the initial suspicion.

The presence of Aedes albopictus, a potential dengue vector, and the possible resettlement of Aedes aegypti, the primary vector of dengue, is reason to increase vigilance in order to prevent a dengue outbreak in our country. Dengue is transmitted from human to human via the bite of infected mosquitoes.

 

Dirofilariasis

Cases of helminth parasitism in dogs have been described in Greece. Dilofilaria is transmitted to humans via mosquito bites [7]. The helminth Dirofilaria repens usually causes subcutaneous nodules at the site of the bite and is transmitted by all known mosquito species (Anopheles spp., Culex spp. and Aedes spp.).

 

Mosquito control

In order to prevent human disease caused by the viruses and parasites mentioned above, a systematic mosquito surveillance system is required. Nowadays, it is accepted that the success of such actions depends on the implementation of an integrated mosquito management program [8, 9]. The aim of these programs is to optimize the control of mosquitoes in an economical and environmentally friendly way. Specifically, the actions that comprise such programs are: 1) entomological investigation, 2) mapping of the study areas, 3) environmental health management, 4) proper use of pesticides and 5) increased public awareness regarding the dangers and preventive measures. We must emphasize that all these actions were implemented 60 years ago when Greece eradicated malaria.

With entomological surveillance and mosquito collection, problematic areas can be identified, as well as the presence of mosquito populations, their behavior and seasonal distribution, in order to plan subsequent actions. An important factor in a mosquito control program is the mapping of breeding sites, which needs to be kept up to date. Another helpful factor is an awareness of the climatic conditions and the flight range of the different mosquito species.

Appropriate environmental health management includes the removal or modification of water bodies such as riparian areas, lakes with standing or slow-moving water bodies, irrigation and drainage canals, water tanks, rice fields and every body of water (small and large) in and around houses and the wider area of a neighborhood.

The use of insecticides is associated with the development phase of mosquitoes. Insecticides are very important for a successful control program; larvicides are used in areas where a significant number of larvae have been identified and are an integral part of entomological surveillance. The late start of a larvicide program can be an important factor in the failure of a vector control program. When adult mosquitoes are present and there is a public health risk, adulticides can be applied at ground level and, in exceptional cases, by air. It should be noted that for larvicides environmentally friendly insecticides are used (Bacillus thuringiensis israelensis, Bacillus sphaericus and diflubenzuron), while for adulticides compounds from the wider group of pyrethroids are used. The insecticide used must be selected from the list provided by the Ministry of Rural Development and Food with the approved formulations, and tested periodically for resistance growth. In order for insecticides to be effective, they should be used under appropriate climatic conditions (i.e. with caution in wind and rain). Trained staff from the regions and municipalities contributes to the success of the control programs. The Hellenic Center for Disease Control and Prevention (HCDCP), in collaboration with the Ministry of Health and the NSRF of the University of Thessaly’s ‘Integrated surveillance and control program for West Nile virus and malaria in Greece’ assist local authorities in the correct implementation of control measures.

The use of natural mosquito enemies such as mosquitofish (Gambusia) should not be overlooked.

Of particular importance to mosquito control is an increase in public awareness. Active participation of the public in implementation of certain measures regarding the environment is really important. HCDCP has successfully organized meetings in schools over the years in order to inform students about the protective measures that can be taken against mosquitoes.

 

Entomological Surveillance of HCDCP

HCDCP implemented entomological surveillance programs in 2011 and 2012 in order to observe any variability in the mosquito populations and calculate the mosquito West Nile infection rate.

 

METHODOLOGY

In 2011, HCDCP, in co-operation with the company Ecodevelopment, conducted entomological surveillance in the region of Central Macedonia, which was the center of the 2011 epidemic. Sixty CO2 traps were placed in fixed locations. The mosquitoes collected were identified to genus level by Ecodevelopment and sent to the Laboratory of Parasitology, Entomology and Tropical Diseases (NSPH) so that they could be tested further for West Nile virus infection. In addition, Ecodevelopment carried out a study that mapped where the main mosquito breeding sites were throughout Greece, and the probability of significant hatchings of Culex spp., Anopheles spp., Aedes detritus and Aedes caspius was calculated. In 2012, HCDCP co-operated with three companies (Ecodevelopment, Bioapplications and Axiven-Apolimantiki) to implement entomological surveillance and almost all of mainland Greece was covered. The area that each company worked at and the number of traps placed are shown in Table 1.

 

Table 1: Number of traps per study area and subcontractor, Entomological Surveillance HCDCP, 2012

Subcontractor Trap Number
Geographical area Trap number
Ecodevelopment Central Macedonia 50
East Macedonia- Thrace 25
Bioapplications Attica 30
Sterea Hellas 20
Thessaly 30
Axiven- Apolimantiki Peloponnese 30
Epirus 20

 

Source: Malwest

 

Figure 1:Trap placement stations, Entomological Surveillance HCDCP 2012 (Source: Malwest)

july2013gr_KURIWS_THEMA_IMAGE_1

In both 2011 and 2012, the study lasted 6 months (May–October). Traps were placed every 15 days, except in July and August when the frequency was every 10 days.

In 2012, the mosquitoes collected, similarly to 2011, were identified to  genus level and sent to the Laboratory of Parasitology, Entomology and Tropical Diseases at the National School and the Laboratory of Microbiology at the Medical School of Athens, in order to test them further for the presence of West Nile virus.

RESULTS

The dominant mosquito genus collected was Culex, followed by Aedes, while the lowest population distribution was observed for Anopheles.

In the majority of the study areas, the highest mosquito populations were observed between 10-20 July and 20 August-10 September.

The mosquito infection rate (MIR) for Greece for the period May to October 2012 was 2.04. According to the CDC, 2.04 indicates some viral activity and increased vigilance and control are recommended.

 

CURRENT STATUS

During 2013, a small-scale entomological surveillance program has been implanted by HCDCP in collaboration with Malwest.

A small number of mosquito traps is being monitored in co-operation with the subcontractors of the respective mosquito control programs, and the mosquitoes collected are being tested for West Nile virus infection. According to the research protocol, the region of Central Macedonia, and the regional unit of Messinia and Dodecanese, are being monitored, in collaboration with the subcontractors Ecodevelopment, Bioapplications and Apolimantiki. HCDCP and Malwest have excellent co-operation with the above mentioned companies, which they want to thank.

Additionally, staff from the University of Thessaly is monitoring the regional unit of Thessaly, and similarly HCDCP staff in collaboration with the Department of Parasitology, Entomology and Tropical Diseases at NSPH are monitoring the Attica region.

The program started at the end of May 2013 and will last until mid-October 2013.

 

REFERENCES
  1. Danis K, Papa A, Theocharopoulos C, et al. 2011. Outbreak of West Nile virus infection in Greece. Emerg Infec Dis 17:1868-1872.
  2. Center for Disease Control and Prevention. 2012.  Report of Epidemiological Surveillance infection by West Nile virus in Greece. Available at:
  3. Vakali A, Patsoula E, Spanacos G, et al. 2012. Malaria in Greece 1975 to 2010. Eurosurveillance 17:pii20322.
  4. Center for Disease Control and Prevention. 2012. Report of Epidemiological Surveillance, Malaria in Greece. Available at:
  5. Lambrechts L, Scott TW, Gubler DJ. 2010. Consequences of the expanding global distribution of Aedes albopictus for dengue virus transmission. PLoS Negl Trop Dis 4:e646.
  6. Copanaris P. 1928. L’épidemie de dengue en Grèce au cours de l’été 1928. Bull Office International d’Hygiene Publique 20:1590-1601.
  7. Vakalis N, Vougioukas N, Patsoula E, et al. 2002. Genotypic assignment of infection by Dirofilaria repens. Parasitol Int 2:163-169
  8. Joint Statement on Mosquito Control in the United States from the US Environmental Protection Agency (EPA) and the US Centers for Disease Control and Prevention (CDC). Available at: http://www.epa.gov/pesticides/health/mosquitoes/mosquitojoint.htm
  9. World Health Organization. Handbook for Integrated Vector Control Management. Available at: http://whqlibdoc.who.int/publications/2012/9789241502801_eng.pdf

 

Annita Vakali,
Department of Epidemiological Surveillance and Interventions, HCDCP