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INTRODUCTION
Vector borne diseases are threatening a large part of
the world human population and seem to make roots
in temperate regions previously considered at low
risk. Evidences indicate that factors driving this new
phase are currently more related to globalization of
human activities than to climate change (even if the
two aspects can not be clearly distinguished for
certain parts), including movement of people (trav-
elers, workers and refugees), animals, and gods (i.e.
used tires and ornamental plants).
Environmental changes related to new agricultural
practices and wetland restoration, influence the
wildlife species as well as the vector species compo-
sitions opening the way to new epidemiological
scenarios.
Improvements in diagnostic tests and surveillance
capacity play of course a relevant role in evidencing
the situation, especially in the case of rare or mild
diseases, which were probably much less diagnosed
in the past.
Human movements through the globe have initiated
the spread of invasive mosquito species and related
vector-borne diseases centuries ago and the ongoing
globalization is just accelerating the phenomenon
(Reiter, 1998).
Several mosquito species have been introduced
recently into Europe, such as Aedes albopictus, Ae.
aegypti, Ae. japonicus, Ae. atropalpus, Ae. trise-
riatus and Ae. koreicus, all sharing the ability to
develop in artificial containers and to rely on dry
resistant eggs.
Of these species Ae. albopictus has proven its capac-
ity to act as a vector in temperate region, being
responsible of the Chikungunya virus epidemic in
northern Italy in 2007 (Angelini et al., 2007;
Bonilauri et al., 2008), and of Dengue virus trans-
mission in France and Croatia in 2010 (La Ruche et
al., 2010; Gjenero-Margan et al., 2011).
Ae.albopictus is already established in Albania,
Bosnia and Herzegovina, Croatia, France, Greece,
Italy, Montenegro, Spain, and Switzerland, whit the
potential to expand its distribution in Europe. The
key of its successful adaptation to temperate
39
The possible role of entomological surveillance in
mosquito-borne disease prevention
R. BELLINI
1
, P. ANGELINI
2
, C. VENTURELLI
3
, M. CALZOLARI
4
, P. BONILAURI
4
, M. TAMBA
4
, M. CARRIERI
1
,
A. A
LBIERI
1
, D. PETRIC
5
1
Centro Agricoltura Ambiente “G.Nicoli”, Crevalcore, Italy
2
Public Health Department, Emilia-Romagna Region, Bologna, Italy
3
Local Public Health Unit, Public Health Department, Cesena, Italy
4
Istituto Zooprofilattico Sperimentale della Lombardia e dell’Emilia-Romagna “B. Ubertini”, Brescia, Italy
5
Laboratory for medical and veterinary entomology, Faculty of Agriculture, University of Novi Sad, Novi Sad,
Serbia
Summary - Current GIS technologies and laboratory diagnostic capacities are strongly improving the potentiality of vector
monitoring and vector-borne disease surveillance programs. When the entomological/veterinary surveillance activities are
organized and implemented with the support of a strong baseline of bio-environmental data set, they are showing to be of
high usefulness for the early detection of invasive exotic mosquito species and the definition of the colonized area; the risk
assessment of vector borne diseases such as Dengue and CHIK throughout vector density estimation at local scale; the
surveillance of arboviruses activity in large areas; and the support to epidemiological understanding of vector borne diseases.
The efficiency of the surveillance program may be optimized and related costs reduced, by the progressive introduction of
GIS satellite supported technologies, by the progressive understanding of the role played by environmental determinants, and
by the introduction of more efficient methods of sampling.
Key words: Aedes albopictus, invasive mosquito, dengue, Chikungunya, West Nile
GIORNALE ITALIANO DI MEDICINA TROPICALE VOL. 16, N. 3-4, 2011
climates is the egg diapausing mechanism enabling
the permanent establishment in temperate regions,
despite the high mortality during the winter period.
Evidences indicate that international dispersal
mainly exploits trade of used tires and of ornamental
plants to a less extent, while local dispersal is easily
obtained by ground transport vehicles. Ae.albopictus
mainly exploits man made containers thus showing
distribution mostly related to inhabited areas, while
very low presence is observed in rural and natural
areas. This distribution has important implication on
the vector related sanitary risks.
Thus it becomes necessary to develop capacities to
promptly detect introduction of new mosquito
species and pathogens, as well as to keep under
surveillance the sanitary risk related to the known
vector-pathogen systems. This should be done at the
country/regional level in a comprehensive EU coor-
dinated frame.
The entomological surveillance, when supported by
strong baseline data, may offer the capability for
early detection of arbovirus circulation in a specific
area.
The case of West Nile virus (WNV) is a good exam-
ple of this possibility. WNV is one of the most
extensively distributed flavivirus worldwide. A large
number of wild and domestic bird species may serve
as reservoirs of WNV, while transmission is mainly
performed by Culex species. Mammalian species,
including humans and horses, are terminal hosts,
unsuitable as virus reservoirs because of low viral
titers they develop.
Several outbreaks have been registered in Europe,
the largest were in southeastern Romania in 1996
and in Central Macedonia (Greece) in 2010.
The epidemiological picture of WNV is complex
being influenced by a number of environmental,
climatic and faunistic parameters, often obscuring
the role of vector density. The recent evidences
obtained in Europe confirm the primary vector role
of Cx. pipiens (a complex including Cx. pipiens
pipiens, Cx. pipiens molestus and intermediated
hybrids) in the amplification as well as in the human
infection. The virus is able to overwinter in temper-
ate regions developing a certain level of endemicity.
Cost benefit analysis of concurrent surveillance
methodology/systems may be conducted on case-by-
case basis providing that the optimization of meth-
ods and procedures may progressively be achieved.
It is of relevance that the European Centre for
Disease Prevention and Control (ECDC) has just
launched an initiative to produce guidelines for
implementing surveillance/monitoring of invasive
mosquitoes (ECDC, 2011) in order to assist EU
Member States and EEA/EFTA countries.
M
ATERIALS AND METHODS
Invasive mosquitoes
Thorough assessments are necessary to actively
prevent and/or control the introduction and estab-
lishment of new mosquito species in previously free
territories. One of the key issues to be carefully
analyzed is the selection of sites of possible intro-
duction through the creation of a priority check list.
This issue requires a thorough knowledge of the
region under surveillance to efficiently consider the
sites with a high risk of importation from far away
regions (i.e. used tire facilities, plant import compa-
nies, harbors, airports, freight containers, container
terminals) and from neighboring already infested
countries/regions (i.e. border crossings, rest areas
and petrol stations along traffic paths, and facilities
for local transport and trade). An adequate
balance/compromise between risk and effort must be
progressively developed on the basis of a continuous
long term managed effort.
Other key issues to be considered are the collec-
tion/trapping methods tailored not only to species
biology/behavior but also (Tab. 1) according to
analyses of cost efficacy adapted to local conditions;
the possible engagement of municipality/local
people in the monitoring activities; and the level of
information to the public.
An emergency plan should be prepared with clear
and complete organization of the surveillance and
control activities and attribution of responsibilities,
to be adopted in case of detection of invasive
species.
In Emilia-Romagna, since 2007, it has been estab-
lished a working group coordinated by the General
Direction for Health and Social Policies composed
by physicians, veterinarians and entomologists with
the aim of creating a regional surveillance and risk
R. BELLINI ET AL.
40
Table 1 - Scheme of relative usefulness of some mosquito collection methods related to newly introduced species
CO
2
trap Light trap BG sentinel Ovitrap Gravid Trap Sticky trap HLC Larval
inspection
Aedes albopictus + - ++ ++ - + +++ ++
Aedes aegypti + - ++ ++ - ++ +++ ++
Aedes japonicus +/- - -/+ -/+ + + - ++
Aedes atropalpus + - ? + - ? ++ ++
Aedes koreicus ?? ?+- ??++
Aedes triseriatus ++ ? ++ + ? ? +++ ++
Legend: - low efficacy/efficiency; + fair efficacy/efficiency in some situation; ++ good efficacy/efficiency; +++ excellent performances; ? not known
assessment system based on multidisciplinary
network with the capability of collecting data about
both vector populations dynamics and possible pres-
ence of pathogens in vectors, men and animals.
Referring to the entomological surveillance on inva-
sive mosquitoes the work of the group is dedicated
to keep under control sites potentially involved in
the introduction of new species, such as Ravenna
seaport and companies importing used tyres. Near
these sites some traps are located and entomologists
conduct periodical inspections to collect larvae in
potential breeding sites.
Established mosquitoes
In case of sanitary surveillance focused on already
widespread species (autochthonous and exotic) the
entomological surveillance may result highly effi-
cient in producing reliable information (Tab. 2).
It may be useful to distinguish between entomologi-
cal surveillance aimed at estimating the population
density distribution for the direct implication it has
on the epidemiological risk (i.e. the Ae. albopictus-
Chikungunya or Ae. albopictus-Dengue binomials),
and entomological surveillance aimed at collecting
mosquito samples to be directly screened for
pathogens.
In any case it is important to standardize trapping
techniques and to organize a network sensitive
enough to detect temporal and geographical varia-
tion of population density at the local scale and/or to
collect sufficiently significant samples to be
screened for pathogens.
The “classic indices” used to evaluate Stegomyia
population densities such as the House Index (HI:
percentage of houses with at least one active breed-
ing site), the Container Index (CI: percentage of
containers with larvae), and the Breteau Index (BI:
number of active breeding sites per 100 premises),
still widely used in tropical countries are of limited
value in Europe because of the high requirement of
man power and the contribution of important breed-
ing sites in public areas (i.e. road drains) on the
productivity per unit area. Other indices such as the
PPI (number of pupae/premise), the PHI (number of
pupae/hectare), the PDS (Pupal Demographic
Survey), and the API (adult productivity index),
which defines the mosquito density per unit area,
considering both public and private domains, are
well correlated with ovitraps data but more expen-
sive to perform and standardize (Carrieri et al.,
2011a). As a consequence in Emilia-Romagna the
surveillance of Ae. albopictus in urban contexts,
aimed to assess the epidemiological risk of
Chikungunya and Dengue transmission, is based on
the use of ovitraps as a tool for mosquito population
density estimation. During the favorable season
(May-October), about 2,800 ovitraps are activated in
the urban areas of 242 municipalities according to
standard criteria and checked bi-weekly.
Referring to the surveillance of mosquitoes in rural
contexts, aimed to assess the circulation of viral
pathogens, in Emilia-Romagna the WNV surveil-
lance system is based on the regular (bi-weekly)
collection of mosquitoes in the period June-October.
Mosquito collections is conducted using 90-100 CO
2
baited traps positioned in fixed stations in a grid of
10x10 km, to cover the surveillance area The
collected mosquitoes are managed in a cold chain,
pooled (max 200 individuals) by species, date and
site of collection and examined by RT-PCR pan-
Flavivirus, and in case of positivity to species
specific RT-PCR. When virus activity is low a
super-pool strategy is applied to reduce the number
of analysis (Calzolari et al., 2010).
Geographic information systems
In recent years, the use of the Geographic
Information Systems (GIS) is providing important
practical contributions to the investigation and
understanding of the spatial component of the
epidemiology of vector-borne diseases such as
malaria, trypanosomiasis, rickettsiasis and a range of
arboviral diseases. The collection and thorough
management of georeferenced epidemiological data
is useful in the investigation of possible environ-
mental/climate explanatory parameters.
Global and local indicators of spatial association
like Moran I or Getis-Ord statistics may assist in the
measure of data clustering level.
Geostatistical techniques are also used to produce
prediction surfaces and level of uncertainty for these
surfaces, which provides an indication of how good
the predictions are.
The mapping of the vector population density
geographic distribution may provide information
both on the environmental variables that drive
THE POSSIBLE ROLE OF ENTOMOLOGICAL SURVEILLANCE IN MOSQUITO-BORNE DISEASE PREVENTION
41
Table 2 - Scheme of relative usefulness of some mosquito collection methods for established mosquitoes of sanitary
importance
CO
2
trap Light trap BG sentinel Ovitrap Gravid Trap Sticky trap HLC Larval
inspection
Aedes albopictus +/- - ++ ++ - + +++ ++
Culex pipiens +++ + + - +++ - - -
Aedes japonicus +/- - -/+ -/+ + + - ++
Anopheles ++ ?-- ?+-
Legend: - low efficacy/efficiency; + fair efficacy/efficiency in some situation; ++ good efficacy/efficiency; +++ excellent performances; ? not known
species development, and on the epidemic diseases
risk level, which are essential to developing effec-
tive disease prevention programs, particularly for
Chikungunya and Dengue.
In the Emilia-Romagna Ae. albopictus surveillance
system, the universal kriging interpolation is used to
estimate the seasonal abundance of the species at
unsampled locations, while the spatial cluster analy-
sis is used to identify particular areas that had statis-
tically significant high or low mosquito density.
Model parameters obtained by variogram analysis
were used in an ArcGIS Geostatistical Analysis to
obtain prediction maps, the quality of which may be
examined by creating a prediction of standard error.
The predicted standard errors quantify the degree of
uncertainty for each location on the surface.
The extrapolation and interpolation of data need to
be conducted with caution, and the production of
computer-generated maps that appear to be more
informative than the data upon which they are
based, should be avoided. Bearing this in mind,
contour smoothed maps obtained from geostatistical
analyses and cluster maps obtained from cluster
detection can be overlaid on other smoothed infor-
mative layers to identify environmental variables
such as elevation, rainfall distribution, mean air
temperature and relative humidity, that could influ-
ence seasonal mosquito population densities in the
region. These maps can also be overlaid on epidemi-
ological data to identify health risks.
R
ESULTS
Invasive mosquitoes
The experience matured in Europe in the case of Ae.
albopictus invasion (VBORNET vector maps:
http://ecdc.europa.eu) indicates that, where attempts
to early detect and eliminate the invasive species
when still confined to a limited area at the beginning
of the colonization process have been implemented
locally, without a country level of coordination and
support (in Italy, Switzerland, Spain) only limited
temporarily successes were achieved. Even in
Southern France where a more organized plan was
deployed the species is rapidly spreading. This is
probably because the large number of vehicles
coming from infested Italian areas bringing inadver-
tently mosquitoes on board directly into the towns,
where the species is difficult to locate in the initial
colonization phase. Huge efforts and investments
are deemed necessary to organize a preventative
program in the case the invasive species has already
achieved a wide distribution range in the continent,
with high population density pushing continuously
for expansion.
Ae. japonicus has also been introduced, probably via
the used tire or the ornamental plants trade (the way
of introduction has been hypothesized), from the
original Asian area to USA and Central Europe
(Austria, Belgium, France-eradicated, Slovenia,
Switzerland and Germany) where it is spreading
(Schaffner et al., 2009; Becker et al., 2011;
Schneider, 2011). This species has been tested a lab
competent vector for several arboviruses (i.e. West
Nile and Japanese encephalitis), and found positive
in the field (i.e. West Nile in the US), but its real
medical importance remains to be clarified.
Looking at the distribution the species has achieved
in the US (see at http://www.rci.rutgers.edu/~insects
/ojdist.htm), where the invasion started about 10
years before than in Europe, it seems that the species
has the potential to colonize large part of Europe.
Aedes aegypti originated in Africa has progressively
colonized tropical and subtropical areas around the
world. It is highly anthropophagic and synanthropic
and notorious as the vector of the yellow fever,
chikungunya and dengue viruses. In the first half of
last century it was present in southern Europe and
involved in deleterious dengue epidemics in Athens
in the 1927-28 (Theiler et al., 1960), but disap-
peared afterwards. Nowadays it is spreading along
the Black See cost (since 2004), was introduced to
Madeira (2004) and in the Netherlands (2010). In
the Netherlands, Ae. aegypti was found at a
company that imports used tires and presumably
imported by a tire shipment from Miami together
with Ae. albopictus. It is currently intolerant to cold
temperatures (no diapausing eggs) that will limit
possible northerly spread in Europe.
Another exotic species that recently showed up in
Europe is Ae. koreicus, a poorly known species with
Asian distribution, recently detected in Belgium
during a research study (Modirisk, 2009) and in
northeastern Italy (Capelli et al., 2011). The rele-
vance of this species in terms of possible sanitary
impact is largely unknown.
The one Nearctic species invasive to Europe, Ae.
atropalpus, was first observed in Italy in 1996
(Romi et al., 1997), at used tires storage company,
and was most probably collaterally eradicated by the
treatments against Ae. albopictus. Since that, it is
observed in France (2003) and Netherlands (2009,
2010). The species is native to Central and North
America, up to southeastern Canada, and probably
would have high potential for establishing itself in
Europe. In United States is mainly considered a
nuisance species that readily bites humans. There, it
is found positive for WNV in nature but vector
status of this species is still unclear.
One more temperate climate, Neartic species native
to North America (Southern Canada and the eastern
United States, south to the Florida keys and west to
Utah and Idaho) that has potential to invade Europe
is Ae. triseriatus. This species is the most widely
distributed tree hole-breeding mosquito in North
America. The larvae develop occasionally in artifi-
cial containers such as wooden tubs, barrels, and
watering troughs. Females are included in second
tier of mosquitoes causing nuisance in the USA
(McKnight, 2005). Ae. triseriatus is vector of La
R. BELLINI ET AL.
42
Crosse virus and potential vector of West Nile virus
in North America. In Europe, it is intercepted only
once, in France (2004) in used tyres imported from
USA, but is potentially hazardous species having the
diapause in egg stage.
From the available evidences it is clear that
container breeding species are the most favorites to
be passively introduced and established in new
regions. This pose a number of questions related on
the possible regulation of the international trade of
goods that may be exploited by these species, which
appears to be the best strategy to develop in order to
reduce the risk of new invasions.
It may also be underlined that surveillance programs
based on ovitraps are of limited usefulness in term
of detection of possible new species because of the
difficulties in discriminating the species at the egg
stage, and the amount of labor required in egg hatch-
ing and larval development to achieve older stages
(larva or adult).
Established species
In the case of Dengue and Chikungunya viruses,
both strictly connected to the binomial
Ae.albopictus/human, the vector population density
play a key role in the epidemiological equation
(Fine, 1981; Reisen, 1989).
m b Sm V Sv p i
R
0
= ____________________
(- loge p )
where:
m is the mean number of bites per human per day;
b corresponds to 1/GC, were GC is the duration of
the gonotrophic cycle;
Sm is the species vector competence;
V is the period during which the infected host has a
sufficient viremia to infect the mosquito vector;
Sv is the proportion of the human population sensi-
tive to the infection;
p is the female mosquito daily survival rate;
i is the duration of the extrinsic incubation period of
the virus in the vector.
Of course the number of bites/human/day depends
on several factors, some of which relate to the
human socio-economic condition determining the
level of exposure to mosquito bites, including the
vector population density.
We may directly influence vector density through
mosquito control campaigns.
In this context it is important to know if the vector
density in a certain area may be able to sustain an
epidemic in case the introduction of the virus
through a viremic person. Thus an adequate system
of quantitative monitoring has been implemented in
the Emilia-Romagna region to provide real time data
at a fine geographic scale through the use of ovitraps
positioned in a statistical sound network using the
Taylor model (Albieri et al., 2010; Carrieri et al.,
2011b).
The number of ovitraps to produce values of
Relative variation in the range 0.2 < D < 0.3 has
been considered sufficient (about 2,800 ovitraps).
This method provides several advantages over other
methods, including high sensitivity, ease of field
management, and low management costs. Ovitrap
data reliability, in terms of quantitative estimation of
adult population densities, is controversial and ques-
tionable in the tropics while it seems sufficiently
sensitive and precise in temperate regions (Tab. 3)
(Carrieri et al., 2011a, 2011c).
This system has also some disadvantages such as the
strict selectivity for container breeding species, the
unavailability of adults for virus screening, the diffi-
culty in determining species at the egg stage (so in
case a new Aedes species is introduced the system
may not be able to discriminate the eggs).
Standard ovitraps currently in use allow a biweekly
inspection requiring 10-11 checks per season,
producing data that are processed with GIS geosta-
tistical analysis to obtain maps, as the one reported
in Figure 1, with information which are regularly
publicized on a dedicated website
(www.zanzaratigreonline.it).
In the case of WNV surveillance plan in Emilia-
Romagna, the entomological and veterinary surveil-
lance, when properly organized, have proven useful
to early detect the virus circulation 3-4 weeks before
the appearance of human cases (Fig. 2). When vali-
dated for a sufficient number of years the surveil-
lance system may allow for the adoption of public
health measures only in case they are really needed.
THE POSSIBLE ROLE OF ENTOMOLOGICAL SURVEILLANCE IN MOSQUITO-BORNE DISEASE PREVENTION
43
Table 3 - Pearson product moment correlations (R) between mosquito population indices and the mean number of
eggs/ovitraps/week collected the week before, the week of and the week after the inspection (from Carrieri et al.
2011a)
Population Indices Mean number of eggs/week/ovitrap
Previous week Inspection week Week after inspection
HI - House Index 0.0867 -0.1117 -0.3778
CI - Container Index 0.3194 0.0482 -0.4175
BI - Breteau Index 0.0623 -0.1465 -0.4313
PPI – Pupae/premise -0.0289 -0.2553 -0.5118
PHI - Pupae/ha 0.1703 0.3396 0.8622*
*P < 0.01. HI: percent of houses with at least one positive container. CI: percent of infested containers. BI: Number of positive containers/100 houses. PPI:
number of pupae per premise. PHI: number of pupae per hectare.
These measures include the information campaign
regarding personal protection precautions to be
adopted by citizen in risky areas, eventually vector
control operations, policy on blood and organs
donations.
The WNV surveillance plan in the Emilia-Romagna
region detect another arbovirus which resulted
highly active in the last three years (2009-2011):
Usutu virus (USUV). This virus seems to co-circu-
late with the WNV, using Cx. pipiens as the main
vector, and several birds species as hosts. Its
epidemiology needs to be investigated to clarify the
role of non-bird hosts and of Ae. albopictus as possi-
ble secondary vector (Weissenböck et al., 2003,
Tamba et al., 2011).
C
ONCLUSIONS
Vector monitoring and vector-borne disease surveil-
lance programs when applied in a properly orga-
nized way, are showing to be of high usefulness for
the: (i) early detection of invasive exotic mosquito
species and relative infested area definition; (ii) risk
R. BELLINI ET AL.
44
wee
k
31 33 35 37 39 41 43 45 28 30 32 34 36 38 40 42
Mosquitoes
Humans
Horses
Birds
442927 25 23 21
0
2
4
6
8
10
12
14
PCR positive samples or mosquito
pools number
19
Figure 1 - Choropleth map of Aedes albopictus mean egg density (number of eggs/ovitrap/week) during the season
2011 in the Emilia-Romagna Region (Italy) calculated for 10 be-weekly data. Legend values are subdivided into
quartiles; wired polygons represent municipalities with sampling designs that were not statistically efficient for
measuring true population densities for RV
< 0.3.
Figure 2 - Seasonal dynamic of WNV positivity obtained during the 2009 and 2010 seasons.
assessment of vector borne diseases such as Dengue
and CHIK throughout vector density estimation at
local scale; (iii) surveillance of arboviruses activity
in large areas; (iv) support to epidemiological
understanding of vector borne diseases.
The entomological surveillance may be conve-
niently integrated with medical and veterinary
surveillance activities to produce a more compre-
hensive understanding of the situation and to better
planning the use of resources.
When integrated with meteorology, environmental
spatial techniques and informatics/statistics the ento-
mological surveillance may be able to produce
output of information that go to a fine scale, allow-
ing explanation or hypothesis to understand
observed phenomena.
Modeling may produce the best outcome in term of
explanation and/or prediction when monitor-
ing/surveillance are well planned on statistical bases
and on baseline knowledge of biology of the
involved species and ecology of the interested terri-
tory.
The capacity to early detect the presence of invasive
species and define the size of the colonized area is
fundamental to increase the chances of elimination
of invaders at the beginning of the colonization
process with much less efforts than it would need in
case of wide infested areas. A number of elimina-
tions of new populations of Ae. albopictus have
been achieved in Italy, France and Serbia when the
species was confined to a used tire company and
surrounding area or border crossing.
It has been demonstrated on several occasions
within different countries and environmental condi-
tions that it is possible, and perhaps highly conve-
nient in term of cost-benefit balance, to eliminate an
invading mosquito species by promptly applying
intensive suppression methods if the colonized area
is still well delimited.
A country level specific evaluation of the most prob-
able way/sites of entry of the species could be
conducted to assist a focused surveillance plan
aimed at the prompt detection and elimination of the
species. Cost comparative analysis of this approach
compared with the control cost (including the sani-
tary cost and risk) in case of wide colonization of
the country may produce an indication of the finan-
cial support to be invested in the preventative
measures.
The main concern the southern Europe countries are
facing is named Ae. aegypti, tropical widely present
species, which recently implanted a bridgehead in
Madeira island and Abkhazia (Almeida et al., 2007).
Frequent and rapid connections from these areas to
climate prone regions pose a clear risk of introduc-
tion and establishment in the continent. It may be of
significance to recall that this species was quite
commonly found in the Mediterranean ports until
the beginning of the 19
th
century, and still is one of
the major vector of Dengue worldwide. A coordi-
nate international effort aimed at the elimination of
Ae. aegypti from Madeira and Abkhazia must be
evaluated as a preventative measure to protect
southern Europe.
The ability of European countries to obtain data on
the presence and abundance of invasive species and
to develop efficient control programs and tools for
their evaluation needs to be rapidly and consistently
improved in order to increase the chances for early
detection and elimination of invaders at the begin-
ning of the colonization process.
Where the invading species is established on a large
area (large town or region), monitoring of popula-
tion abundance is needed with standardized methods
on a long term basis to perform a risk assessment of
arbovirus transmission such as dengue and
Chikungunya, obtain data about the evolution of the
vector density and guiding the planning of informa-
tion/control campaigns.
On the basis of the current available technology the
possibilities to develop well focused and cost benefit
surveillance programs are certainly increasing with
important benefit for the prevention of vector borne
diseases.
WNV surveillance based on mosquito collection
coupled with the rapid laboratory screening for
arbovirus presence has proven reliable in terms of
sensitiveness and precociousness in the detection of
virus circulation. This is particularly useful in the
case of periodical incursion of the virus in a
geographic area, with silent periods sometimes last-
ing many years. By adopting an active entomologi-
cal surveillance it is possible to assist the public
health authorities in the target adoption of preventa-
tive measures only in case of real need.
The efficiency of the surveillance program may be
optimized and related costs reduced, by the intro-
duction of GIS satellite supported technologies, by
the progressive understanding of the role played by
environmental determinants, and by the introduction
of more efficient methods of sampling.
Depending from the collection methods utilized, the
entomological surveillance may provide information
on the possible activity of other arboviruses. In the
case of CO
2
baited traps, considering their efficacy
in collecting several haematophagous species, it is
possible to maintain under surveillance not only
mosquito borne viruses, but sand fly, biting midge
and black fly borne pathogens as well.
ECDC is engaged in stimulating the awareness and
the capacities of European countries to organize and
conduct surveillance and control of mosquito vector-
borne diseases. The European Spatial Agency (ESA)
is also on the ground by promoting better exploita-
tion of remote sensing satellite capacities in the field
of vector surveillance and by supporting the
VECMAP initiative inside the Integrated
Applications Promotion (IAP) ESA ESTEC, an inte-
grated spatial tool and service for modeling the
distribution of mosquito vectors of disease.
THE POSSIBLE ROLE OF ENTOMOLOGICAL SURVEILLANCE IN MOSQUITO-BORNE DISEASE PREVENTION
45
ACKNOWLEDGEMENT
We thank for the support and assistance in the project
management the members of the Emilia-Romagna Vector
Surveillance Commission (Baldelli Raffaella, Cagarelli
Roberto, Dottori Michele, Natalini Silvano, Poglayen
Giovanni, Venturini Diana) and of the Emilia-Romagna
Coordination Group on Aedes albopictus (Balducci Paolo,
Bandini Roberto, Baruffaldi Andrea, Battistini Giuliana,
Bedeschi Lino, Casaletti Gianni, Chiatante Alessandro,
Caroli Clara, Cocconi Fausto, Fabbri Chiara, Farina
Marco, Gaiani Massimo, Giovannini Federica, Guagliata
Cristiano, Guidi Gabriele, Mascali Zeo Silvia, Mattei
Giovanna, Merli Enrico, Moretti Massimo, Patergnani
Matteo, Po Claudio, Scarpellini Paola, Signorini Valter,
Tassinari Massimo, Varini Davide).
R
EFERENCES
ALBIERI A., CARRIERI M., ANGELINI P.,
BALDACCHINI F., VENTURELLI C., MASCALI
ZEO S., BELLINI R. (2010). Quantitative
monitoring of Aedes albopictus in Emilia-Romagna,
Northern Italy: cluster investigation and
geostatistical analysis. Bulletin of Insectology,
63(2): 209-216.
ALMEIDA A.P., GONÇALVES Y.M., NOVO M.T.,
SOUSA C.A., MELIM M., GRACIO A.J. (2007).
Vector monitoring of Aedes aegypti in the
Autonomous Region of Madeira, Portugal. Euro
Surveillance, 12(46):pii=3311. Available online:
http://www.eurosurveillance.org/ViewArticle.aspx?
ArticleId=3311
ANGELINI R., FINARELLI A.C., ANGELINI P., PO C.,
PETROPULACOS K., MACINI P., FIORENTINI
C., FORTUNA C., VENTURI G., ROMI R.,
MAJORI G., NICOLETTI L., REZZA G.,
CASSONE A. (2007). An outbreak of chikungunya
fever in the province of Ravenna, Italy. Euro
Surveillance 12(36):pii=3260. Available online:
http://www.eurosurveillance.org/ViewArticle.aspx?
ArticleId=3260
BECKER N., HUBER K., PLUSKOTA B., KAISER A.
(2011). Ochlerotatus japonicus japonicus – a newly
established neozoan in Germany and a revised list of
the German mosquito fauna. European Mosquito
Bulletin, 29: 88-102.
BONILAURI P., BELLINI R., CALZOLARI M.,
ANGELINI R., VENTURI L., FALLACARA F.,
CORDIOLI P., ANGELINI P., VENTURELLI C.,
MERIALDI G., DOTTORI M. (2008).
Chikungunya Virus in Aedes albopictus, Italy.
Emerging Infectious Diseases, 14: 852-853.
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. (2010). Evidence of
simultaneous circulation of West Nile and Usutu
viruses in mosquitoes sampled in Emilia-Romagna
region (Italy) in 2009. PLoS ONE, 5(12): e14324.
CAPELLI G., DRAGO A., MARTINI S., MONTARSI F.,
SOPPELSA M., DELAI N., RAVAGNAN S.,
MAZZON L., SCHAFFNER F., MATHIS A., DI
LUCA M., ROMI R., RUSSO F. (2011). First report
in Italy of the exotic mosquito species Aedes
(Finlaya) koreicus, a potential vector of arboviruses
and filariae. Parasites & Vectors, 4: 188
doi:10.1186/1756-3305-4-188
CARRIERI M., ANGELINI P., VENTURELLI C.,
MACCAGNANI B., BELLINI R. (2011a). 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. Journal of
Medical Entomology (in print).
CARRIERI M., ALBIERI A., ANGELINI P.,
BALDACCHINI F., VENTURELLI C., MASCALI
ZEO S., BELLINI R. (2011b). Surveillance of the
chikungunya vector Aedes albopictus (Skuse) in
Emilia-Romagna (northern Italy): organizational
and technical aspects of a large scale monitoring
system. Journal of Vector Ecology, 36(1): 108-116.
CARRIERI M., ANGELINI P., VENTURELLI C.,
MACCAGNANI B., BELLINI R. (2011c). Aedes
albopictus (Diptera: Culicidae) population size
survey in the 2007 Chikungunya outbreak area in
Italy. II: Estimating epidemic thresholds. Journal of
Medical Entomology (accepted).
ECDC (2011). Invasive mosquitoes: guidelines for
implementing monitoring. Tender No OJ/06/04/2011
Proc/2011/023 of 6 April 2011.
FINE P.E.M. (1981). Epidemiological principles of
vector-mediated transmission. pp. 77-91. In J. J.
McKelvey Jr., B. F. Eldridge, and K. Maramorosch
(eds.), Vectors of disease agents. Praeger, New
York.
GJENERO-MARGAN I., ALERAJ B., KRAJCAR D.,
LESNIKAR V., KLOBUCAR A., PEM-NOVOSEL
I., KURECIC-FILIPOVIC S., KOMPARAK S.,
MARTIC R., DURICIC S., BETICA-RADIC L.,
OKMADZIC J., VILIBIC-CAVLEK T., BABIC-
ERCEG A., TURKOVIC B., AVSIC-ZUPANC T.,
RADIC I., LJUBIC M., SARAC K., BENIC N.,
MLINARIC-GALINOVIC G. (2011).
Autochthonous dengue fever in Croatia, August-
September 2010. Euro Surveillance, 16(9),
pii=19805
LA RUCHE G., SOUARÈS Y., ARMENGAUD A.,
PELOUX-PETIOT F., DELAUNAY P., DESPRÈS
P., LENGLET A., JOURDAIN F., LEPARC-
GOFFART I., CHARLET F., OLLIER L.,
MANTEY K., MOLLET T., FOURNIER J.P.,
TORRENTS R., LEITMEYER K., HILAIRET P.,
ZELLER H., VAN BORTEL W., DEJOUR-
SALAMANCA D., GRANDADAM M.,
GASTELLU-ETCHEGORRY M. (2010). First two
autochthonous dengue virus infections in
metropolitan France, September 2010. Euro
Surveillance, 15(39):pii=19676. Available online:
R. BELLINI ET AL.
46
http://www.eurosurveillance.org/ViewArticle.aspx?
ArticleId=19676
MCKNIGHT S. (2005). What are the Primary Nuisance
Mosquitoes of North America? Wing Beats, 16(3):
30-32
MODIRISK (2009). Mosquito vectors of disease: spatial
biodiversity, drivers of change, and risk. Report
available at: http://www.belspo.be/belspo/ssd/
science/pr_biodiversity_en.stm
REISEN W.K. (1989). Estimation of vectorial capacity:
relationship to disease transmission by malaria and
arbovirus vectors. Bulletin of the Society for Vector
Ecology, 14(1): 67-70.
REITER P. (1998). Aedes albopictus and the world trade
in used tires, 1988-1995: The shape of things to
come. Journal of the American Mosquito Control
Association, 14: 83-94.
ROMI R., SABATINELLI G., GIANNUZZI SAVELLI
L., RARIS M., ZAGO M., MALATESTA R.
(1997). Identification of a North American mosquito
species, Aedes atropalpus (Diptera: Culicidae), in
Italy. Journal of the American Mosquito Control
Association, 13(3): 245-246.
SCHAFFNER F., KAUFMANN K., HEGGLIN D.,
MATHIS A. (2009). The invasive mosquito Aedes
japonicus in Central Europe. Medical and
Veterinary Entomology, 23: 448-451.
SCHNEIDER K. (2011). Breeding of Ochlerotatus
japonicus japonicus (Diptera: Culicidae) 80 km
north of its known range in southern Germany.
European Mosquito Bulletin, 29: 129-132.
TAMBA M., BONILAURI P., BELLINI R.,
CALZOLARI M., ALBIERI A., SAMBRI V.,
DOTTORI M., ANGELINI P. (2011). Detection of
Usutu virus within a West Nile virus surveillance
program in Northern Italy. Vector-Borne and
Zoonotic Diseases, 11(5): 551-557.
THEILER M., CASALS J., MOUTOUSSES C. (1960).
Etiology of the 1927-28 epidemic of Dengue in
Greece. Proceedings of the Society for Experimental
Biology and Medicine, 103: 244-246.
WEISSENBÖCK H., KOLODZIEJEK J., FRAGNER K.,
KUHN R., PFEFFER M., NOWOTNY N. (2003)
Usutu virus activity in Austria, 2001–2002.
Microbes and Infection, 5(12):1132-1136.
THE POSSIBLE ROLE OF ENTOMOLOGICAL SURVEILLANCE IN MOSQUITO-BORNE DISEASE PREVENTION
47