Mosquito-borne disease surveillance by the European Centre for Disease Prevention and Control
Corresponding author: H. Zeller, Office of the Chief Scientist, European Centre for Disease Prevention and Control, 17183 Stockholm, Sweden
For a few years, a series of traditionally tropical mosquito-borne diseases, such as chikungunya fever and dengue, have posed challenges to national public health authorities in the European region. Other diseases have re-emerged, e.g. malaria in Greece, or spread to other countries, e.g. West Nile fever. These diseases are reportable within the European Union (EU), and the European Centre for Disease Prevention and Control collects information in various ways to provide EU member states with topical assessments of disease threats, risks and trends for prompt and appropriate public health action. Using disease-specific expert networks, the European Surveillance System (TESSy) collects standardized comparable information on all statutory communicable diseases in a database. In addition, the event-based surveillance aims to detect potential public health threats early, and to allow timely response and support to blood deferral decisions for pathogens that can be transmitted through blood donation. Laboratory capacity for early detection is implemented through external quality assessments. Other activities include the development of guidelines for the surveillance of mosquito vectors, and the production of regularly updated maps on the currently known occurrence of mosquito vector species.
Vector-borne diseases pose a special challenge to public health authorities in Europe, owing to their complex nature, i.e. the biological complexity of their transmission system. Most of these diseases also show particular epidemiological features, such as seasonality and periods of pathogen persistence without detection of the disease (asymptomatic human infections, presence of reservoir hosts, and persistence in vectors and their progeny). Many aspects of the transmission cycle are strongly influenced by environmental conditions, which are changing (including climate, agricultural practices, land use, and urbanization), and might allow for (re-)emergence or (re-)introduction in a suitable setting . Moreover, vector-borne diseases tend to become ‘globalized’ through increasing population mobility and migration, travel, and trade, which results in the rapid and worldwide spread of vectors and the pathogens that they transmit .
In the European region, tropical mosquito-borne diseases (MBDs), such as chikungunya (CHIK) fever, dengue, malaria, and West Nile (WN) fever, have attracted recent attention: on the one hand, travel-related cases of some of these diseases, such as dengue, are increasingly being recorded in Europe; and on the other hand, the risk of local transmission has increased with the recent spread of invasive Aedes mosquitoes such as Aedes albopictus, a potential vector of CHIK and dengue viruses. In the European Union (EU), these diseases are included in the list of the communicable diseases to be covered by epidemiological surveillance . The European Centre for Disease Prevention and Control (ECDC) collects information in various ways to provide EU member states with topical assessments of disease threats, risks and trends for prompt and appropriate public health action.
Types of Surveillance Activity
To understand and assess the risks associated with different MBDs in member states, data are needed on disease, pathogen presence (in reservoir hosts), and the occurrence of vectors . An overview of the types of surveillance activity and the number of outputs per year for malaria, dengue, CHIK fever, WN fever and Rift Valley fever (RVF) since 2009 is presented in Table 1.
Table 1. Types of surveillance activity at the European Centre for Disease Prevention and Control and the number of outputs (for mosquito-borne diseases: malaria (Mal), dengue (DEN), chikungunya (CHIK), West Nile fever (WN) and Rift Valley fever (RVF)) per year, 2009–2012
|Annual epidemiological report||Summary of epidemiology of diseases in EU/EEA countries||1||1||1||1|| http://ecdc.europa.eu/en/publications/surveillance_reports/annual_epidemiological_report/Pages/epi_index.aspx |
|West Nile maps||Areas affected by human West Nile disease||–||1||26||24|| http://ecdc.europa.eu/en/healthtopics/west_nile_fever/West-Nile-fever-maps/Pages/index.aspx |
|Threat reports||Threats considered at the daily round table||6 (Mal, WN, DEN)||8 (WN, DEN, CHIK, RVF)||5 (Mal, WN)||3 (Mal, WN, DEN)|| http://ecdc.europa.eu/en/publications/surveillance_reports/Communicable-Disease-Threats-Report/Pages/Communicable-Disease-Threats-Report.aspx |
|Risk assessments||Assessments of threats of public health importance||–||1 (WN)||4 (Mal, WN)||3 (DEN, WN)|| http://ecdc.europa.eu/en/publications/technical_reports/evd/Pages/evd.aspx |
|Vector maps||Vector distribution updatesa||1||2||3||3||http://www.vbornet.eu/; http://ecdc.europa.eu/en/activities/diseaseprogrammes/emerging_and_vector_borne_diseases/Pages/VBORNET_maps.aspx|
|Technical reports||Guidelines; case definitions; mission reports; expert consultations||2 (CHIK, WN)||1||2 (MBD, WN)||6 (Mal, MBD, WN, DEN)|| http://ecdc.europa.eu/en/publications/all_publications/evd/Pages/evd.aspx |
The European Surveillance System (TESSy) comprises a database and disease-specific expert networks, which collect standardized comparable information on all statutory communicable diseases and surveillance systems across the EU member states and European Economic Area (EEA) countries . The ECDC Annual Epidemiological Report, which has been published since 2007, gives a yearly overview of the situation regarding communicable diseases in the EU and EEA countries. It provides information on trends and seasonality, age and gender distributions, and relevant events .
Event-based surveillance is part of the ECDC mandate. It aims to detect potential public health threats early, and allow for timely responses. The sources of information include several websites and a large number of web pages retrieved through specialized search engines . Threats are summarized in threat reports; threats potentially affecting more than one member state lead to joint risk assessments, such as those on the 2012 dengue outbreak in Madeira .
Other epidemiological reports
The ECDC's programme on MBDs also develops complementary activities and outputs, such as expert consultations and field missions, guidelines, and technical reports. The aim of the programme is to better understand the triggers of MBD, enhance the surveillance of mosquito vectors and the diseases that they transmit, improve communication about MBD risks, and develop the appraisal of vector control strategies. For example, the ECDC recently provided European countries with guidelines for the surveillance of invasive mosquitoes, and supports the production of regularly updated maps on the currently known occurrence of mosquito vector species (e.g. A. albopictus and Aedes aegypti) at regional administrative levels (NUTS3), based on published and expert data in the EU [8, 9].
Laboratory capacity for surveillance in Europe
The diagnostic capacity within Europe is a key component of surveillance for the early detection and surveillance of these MBDs. For some viruses, such as RVF, CHIK and yellow fever (YF) viruses, there are no or a very limited number of commercial assays. For this reason, the ECDC is funding the European Network for Diagnosis of Viral Imported Diseases, which provides support related to laboratory diagnostics and assists EU member states, candidate countries and the EEA countries in detecting and characterizing these pathogens. The network organizes external quality assessments (EQAs), and offers advice and support to the EQA participants to help them improve their techniques and procedures. In recent years, EQAs have been organized for YF, WN fever, dengue, CHIK fever, and, latterly, RVF; 30 laboratories, including 22 laboratories from Europe, have participated in these [10-13].
WN Fever Surveillance
The first outbreak of WN fever, which is caused by an arbovirosis initially identified in Africa in the 1930s, was reported in horses and humans in France in the 1960s . After that, the disease was considered to constitute a minor risk for humans and horses in Europe, because only a few cases appeared sporadically. However, the disease re-emerged in 1996, with a large outbreak in humans in Romania . In 1999, the disease was, for the first time, detected in New York city, and it then spread towards the Americas . Owing to the huge impact of the disease on human and animal health in North America, and to the recurrent detection of cases in humans and/or horses in Europe and the Mediterranean basin, WN virus infection was included in 2008 in the list of notifiable diseases in the EU . In 2011, 24 EU/EEA countries reported cases in TESSy. The reporting is compulsory in 19 member states. It is comprehensive (based on cases occurring within the whole population) and passive (physicians, laboratories or hospitals take the initiative to report data to the health department) in 18 EU countries. Sixteen countries use the EU case definition for surveillance to report the data. Some countries have implemented an active surveillance system from June to October in areas considered to be at risk when mosquitoes are active, e.g. southern France and Veneto Region in Italy .
Data from the indicator-based surveillance are collected retrospectively on a yearly basis. Because WN fever is detected every year in several EU countries, and can be transmitted through blood transfusion and organ transplantation, it was necessary to develop a complementary system for the collection of information about WN cases and its rapid communication. This information is required for timely implementation of: (i) personal and collective response measures in the case of an outbreak; and (ii) safety measures for blood donations for people living in or with travel history to areas with ongoing transmission of WN virus to humans . Thus, the ECDC launched the WN mapping project in 2011. During the transmission season, weekly updates of the number and spatial distribution of WN human cases reported in the EU, neighbouring countries and countries bordering the Mediterranean Sea are made publicly available on the ECDC website. WN cases are collected through the event-based surveillance and validated with the countries' health authorities. In 2011, only confirmed cases, as per the EU case definition, were included in the maps for the EU countries; in 2012, both confirmed and probable cases with positive laboratory test results were displayed. As well as improving the timeliness and availability of information about the WN cases, this tool has contributed greatly to improving the awareness of the people involved in the surveillance and the coverage of the surveillance system. Actually, more countries and more areas within countries detected cases in 2012 than in 2011 and 2010, even though the total number of cases was much lower than in 2010 and slightly higher than in 2011. By improving the reporting of WN cases in Europe, this tool and its developments will help to achieve the objective of WN fever surveillance, i.e. ‘to ensure early identification of cases in humans and animals at risk, to implement protective measures in good time’ . In the area of research, it also allows hypothesis generation from a wider knowledge base in cases where the occurrence of WN outbreaks was considered to be quite unpredictable.
Dengue and CHIK Fever Surveillance
Dengue is endemic in most of tropical and subtropical regions, including several European Overseas Territories. Dengue is by far the most important mosquito-borne viral disease affecting humans worldwide; tens of millions of cases occur each year, resulting in approximately 20 000–25 000 deaths, mainly in children. CHIK fever is widespread in tropical and subtropical regions in Africa and Asia, and is absent from the Americas. A. aegypti is not present in the EU, with the exception of Madeira, where it was identified in 2005 . The species is also present around the Black Sea . However, A. albopictus, a secondary vector of dengue and an important vector of CHIK virus, is well established and expanding in several European countries . In recent years, locally acquired cases of dengue and CHIK fever have been reported, and have shown that such tropical vector-borne disease can also spread in Europe in areas where competent Aedes mosquito vectors are present. An outbreak of CHIK fever occurred in 2007 in Italy, two indigenous cases were detected in 2010 in France [20, 21], and several locally acquired cases of dengue occurred in Croatia and France in 2010 [22, 23]. In October 2012, Madeira (Portugal) reported a large outbreak of dengue (DEN 1) infection .
For dengue and CHIK fever, respectively, 22 and 20 countries out of 30 EU/EEA countries report data to TESSy. Dengue reporting is compulsory in 19 countries, and 11 countries use the EU case definition for surveillance to report the data. CHIK fever is reported from ten countries according to the EU case definition. In most countries, data are passively collected through laboratories, physicians, and hospitals. Some countries, such as France and Italy, implement active surveillance during the mosquito season from June to October [16, 24, 25].
There are large variations in the notification rate for dengue between countries, reflecting the travel destination preferences of EU nationals. The overall notification rate for dengue was quite stable in 2008 and 2009, at 0.11 per 100 000 as compared with 0.25 per 100 000 in 2010; this was directly linked to an increase in the number of travel-related dengue cases. In that year, there was a significant increase in dengue transmission in several tropical countries, mainly in the Caribbean, Central/South America, and Asia. Travellers were at significantly more risk of acquiring dengue, and could also have contributed to its spread, as reported in France or Croatia [22, 23]. Most of the cases were reported in the 25–44-year and 45–60-year age groups, who are possibly more inclined to travel. Interestingly, the notification rate was higher in males than in females for these 3 years. The overall notification rate for CHIK fever was lower than that for dengue (0.01–0.02 per 100 000) for the years 2008–2010, and most of the cases were reported in the same age groups. Unlike with dengue, the overall notification rate was higher in females than in males in the last 4 years. The numbers of patients with CHIK fever reported from June to September in countries at risk of local transmission was ten times higher in 2010 than in the other years.
YF, a viral disease that is also transmitted by Aedes mosquitoes in sub-Saharan Africa and in South America, is another reportable disease in the EU. Since 2007, one imported case has been reported in the EU, in 2009, with an unclear travel history . Although imported cases are rare, non-vaccinated travellers visiting affected areas without the effective protection of YF vaccination expose themselves to risk of infection.
With the expansion of the geographical distribution of RVF virus in Africa and in the Middle East, the disease requires attention, because suitable host, vectors and environmental conditions for additional epidemics probably exist on other continents. The disease at the human–animal interface affects primarily animals, and animal cases have to be reported to the Office International des Epizooties. Seventeen of 30 EU/EEA countries report human cases in TESSy. The reporting is compulsory in 16 countries, and nine countries use the EU 2008 case definition. No human RVF cases were reported in continental Europe in 2007, but a few cases were reported from Mayotte, a French department in the Indian Ocean, in 2008 during an outbreak in the region .
Malaria is caused by one of the five Plasmodium parasites: Plasmodium falciparum, Plasmodium vivax, Plasmodium ovale, Plasmodium malariae, and Plasmodium knowlesi. It is an old disease of continental Europe, and was eliminated in the 1970s by a combination of early detection and treatment of cases, mosquito vector control by indoor residual spraying of houses and larviciding of breeding sites, environmental modifications, and human habitat modifications. In the countries directly neighbouring Europe, malaria transmission is currently steeply declining, and there is a target of malaria elimination by 2015 .
Twenty-six of 30 EU/EEA countries report data to TESSy, and in 23 countries the reporting is compulsory. Seventeen countries use the EU case definition for surveillance to report the data, which are, in most countries, passively collected through laboratories, physicians, and hospitals. Over the last 5 years (2006–2010), no clear trend has been observed in the number of reported malaria cases, which has fluctuated around one per 100 000 population per year. Nearly all malaria cases (>99%) are reported as imported—the definition of imported cases refers to cases imported to continental Europe—and are primarily notified by EU/EEA countries that have strong ties with endemic areas. The seasonality and age distribution most likely reflect travel patterns to malaria-endemic countries. Outside continental Europe, some countries or territories are endemic for malaria (e.g. Mayotte and French Guiana), and for these, data are not collected through TESSy.
Sporadic local transmission of malaria is reported in the EU, but a specific problem appeared in Greece, where the presence of seasonal workers from P. vivax-endemic countries in agricultural areas where competent Anopheles species are present resulted in onwards local transmission [28-32]. To cope with this specific problem, active case detection has been set up to enable early detection of symptomatic cases among these migrants, and to decrease the possibility of onwards transmission from imported cases. Likewise, in Germany an increase in the number of malaria cases imported from Pakistan was reported in 2012, but this did not result in onwards transmission . Currently, migration flows and increasing international travel result in malaria importations into Europe. Local transmission of P. vivax remains possible in the EU, where the Anopheles vectors are present, and stresses the need for surveillance, preparedness and prevention within EU and EEA countries, including improvements in access to healthcare for seasonal workers.
The future challenge in implementing mosquito and MBD surveillance and reporting is to improve and harmonize EU-wide coverage and data collection. In addition, coordinated and enhanced human, veterinary, entomological and environmental surveillance is needed in all member states at risk of MBDs, together with increased scientific and technical support from the ECDC. Sustainability of surveillance is a major challenge for these diseases with unpredictable occurrence. In addition, surveillance of human cases needs to be backed up by the implementation of surveillance of vectors and the assessment of vector control measures.
We would like to acknowledge the contribution of experts in the EU member states and beyond who provide data for surveillance of these diseases.
The authors declare that they have no competing interests.