![Numbers of eggs per ovitrap over time in intervention (red) and non-intervention (green) municipalities, for the years 2012, 2013 [14] and 2019. Each red and green fine line represents a trap. Smoothers (lines with grey confidence bands) were added to highlight seasonal trends](https://www.researchgate.net/profile/Diego-Parrondo/publication/353933914/figure/fig2/AS:1057484353572865@1629135325918/Numbers-of-eggs-per-ovitrap-over-time-in-intervention-red-and-non-intervention-green_Q320.jpg)
![Observed data (grey lines) and model fits (green and red lines) for numbers of eggs per ovitrap in intervention and non-intervention municipalities in the years 2012, 2013 [14] and 2019. Each grey line represents an ovitrap (i.e. the actual observations used to fit the model). The fit is visualized in the original scale, without any transformation. Graphs zoomed to the area between 0 and 400 counts. The x-range is adapted to each panel. The maximal fitted values in each year-area combination are shown on the bottom right](https://www.researchgate.net/profile/Diego-Parrondo/publication/353933914/figure/fig3/AS:1057484353568772@1629135325957/Observed-data-grey-lines-and-model-fits-green-and-red-lines-for-numbers-of-eggs-per_Q320.jpg)
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Ravasietal. Parasites Vectors (2021) 14:405
https://doi.org/10.1186/s13071-021-04903-2
RESEARCH
Eectiveness ofintegrated Aedes albopictus
management insouthern Switzerland
Damiana Ravasi1* , Diego Parrondo Monton1, Matteo Tanadini2 and Eleonora Flacio1
Abstract
Background: The exotic invasive tiger mosquito, Aedes albopictus, appeared in southern Switzerland in 2003. The
spread of the mosquito has been surveyed constantly since then, and an integrated vector management (IVM) has
been implemented to control its numbers. The control measures focus on the aquatic phase of the mosquito with
removal of breeding sites and applications of larvicides in public areas whereas private areas are reached through
extensive public information campaigns. Here, we evaluated the efficacy of the IVM.
Methods: Since all the municipalities with Ae. albopictus in southern Switzerland are currently implementing the IVM,
Italian municipalities just across the Swiss-Italian border, where Ae. albopictus is present but no coordinated inter-
vention programme is in place, served as control. Ovitraps and adult female traps were used to measure mosquito
abundance in 2019. Generalised mixed-effects models were used to model the numbers of Ae. albopictus eggs and
adult females collected. These numbers of Ae. albopictus eggs were compared to the numbers of eggs collected in
2012 and 2013 in a previous assessment of the IVM, using a hurdle model.
Results: Mean numbers of Ae. albopictus eggs and adult females in 2019 were consistently higher in the municipali-
ties not following an IVM programme. In these municipalities, there were about four times (3.8) more eggs than in
the municipalities implementing an IVM programme. Also, the numbers of eggs and adult females increased steadily
from the beginning of the Ae. albopictus reproductive season, reaching a peak in August. In contrast, the increase in
numbers of Ae. albopictus was much more contained in the municipalities implementing an IVM programme, without
reaching an evident peak. Comparison with data from 2012 and 2013 indicates that the gap between intervention
and non-intervention areas may have almost doubled in the past 6 years.
Conclusions: The results of the survey strongly support the efficacy of the IVM programme implemented in south-
ern Switzerland compared to municipalities without defined control measures. With the constant implementation of
an IVM, it appears possible to contain the numbers of Ae. albopictus at a manageable level, reducing the nuisance for
the human population and the risk of arbovirus epidemics.
Keywords: Aedes albopictus, Integrated vector management, Ovitrap, Gravid Aedes trap, Surveillance, Control
measures
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Background
Aedes albopictus, also known as the Asian tiger mos-
quito, is native to Southeast Asia and has been spreading
globally in the last 40 years. is is probably due to both
extrinsic factors, such as increase of global trade and
travel, climate change and lack of efficient control, and
intrinsic factors, such as strong physiological and eco-
logical plasticity [1, 2]. Originally, a tree-hole breeding
Open Access
Parasites & Vectors
*Correspondence: damiana.ravasi@supsi.ch
1 Laboratory of Applied Microbiology, Department of Environment,
Construction and Design, University of Applied Sciences and Arts
of Southern Switzerland, via Mirasole 22A, 6500 Bellinzona, Switzerland
Full list of author information is available at the end of the article
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Page 2 of 15
Ravasietal. Parasites Vectors (2021) 14:405
mosquito, Ae. albopictus, has managed to colonize sub-
urban and urban settings, primarily due to its adaptation
to using artificial containers (e.g. plant saucers, water-
ing cans, plastic drums and catch basins) as breeding
sites [1]. Since its first appearance in Italy in the 1990s,
the species has expanded to most areas of the country
[3] and has further spread to other European countries
passively through the various human transportation net-
works (Mosquito Maps, http:// ecdc. europa. eu/). In 2003,
it appeared for the first time in the southernmost tip of
Switzerland, in the Canton of Ticino (hereafter referred
to as Ticino), at a service area on the European Route
E35 close to the Italian border [4]. e spread of this vec-
tor in Ticino has actively been surveyed by the cantonal
Working Group for Mosquitoes (Gruppo Lavoro Zan-
zare, GLZ) and control measures have been immediately
implemented to prevent the establishment of the mos-
quito [5, 6]. Despite the containment measures, today the
mosquito is established in most urban areas of Ticino.
e establishment of Ae. albopictus in suburban and
urban areas represents a potential threat for public health
because of its vectorial competence for at least 26 differ-
ent arboviruses including dengue, chikungunya, Zika and
yellow fever viruses [7]. In the last decade, Aedes-borne
diseases have been increasing in Europe, with outbreaks
of dengue and chikungunya in several countries [8]. In
addition to the risk of virus transmission, the aggressive
daytime biting behaviour of this mosquito causes major
nuisance for people thus affecting their lifestyle, such as
restricting outdoor activities [9]. erefore, vector man-
agement becomes an important mechanism for disease
prevention and nuisance reduction. Integrated vector
management (IVM) is the approach recommended by the
international health agencies and generally accepted [10–
12]. It combines different intervention strategies, such
as physical, chemical and biological control measures,
aimed at reducing or eliminating the mosquito. rough
a multi-sectoral approach, public health entities, other
relevant agencies/organisations and the community are
involved in the decision-making process aimed at opti-
mizing the use of resources for vector control [12].
An IVM programme was implemented in 2000 in
Ticino and gradually adapted during the years in accord-
ance to the level of the spread of Ae. albopictus [5, 6],
following the indications given in the ECDC guidelines
for the surveillance of invasive mosquitoes [13]. Cur-
rently, more than 80 municipalities are involved in the
programme, covering more than 90% of the total human
population of Ticino. e surveillance is based on the
detection and density estimation of Ae. albopictus with
oviposition traps (ovitraps), the identification of breed-
ing sites and the evaluation of reports from residents on
the presence of the mosquito [5]. e control strategy
consists of integrated measures to eliminate or reduce
the densities of Ae. albopictus and is based on the col-
laboration among GLZ, municipal authorities, Civil Pro-
tection Units and citizens. e control measures focus
on the aquatic phase of the mosquito and include the
removal of breeding sites and the use in the public areas
(mainly in catch basins) of larvicide applications sched-
uled weekly or monthly from May to October, depending
on the biocide used. To reach private areas, an extensive
information campaign is carried out every year, includ-
ing community education through information events,
door-to-door delivery of education material (leaflets),
school education and use of mass media [5]. Citizens
are strongly encouraged to remove temporary water
containers from private properties and to cover or treat
permanent water containers with obtainable Bacillus
thuringiensis var. israelensis (Bti) granules (VectoBac® G,
Valent Biosciences). e use of adulticides, less ecologi-
cally sustainable, is reserved for areas where an imported
disease case is confirmed, to prevent autochthonous
cases and outbreaks.
e monitoring and evaluation of the effectiveness of
control methods are an essential part of the IVM. Equally
important is the sharing of these evaluations, so that les-
sons can be learned and knowledge exchanged across
countries [12]. e IVM programme adopted in Ticino
was previously evaluated in 2012 and 2013 by compar-
ing relative mosquito densities between Ticino and two
neighbouring Italian provinces where ecological param-
eters are comparable but control measures were not car-
ried out in a coordinated and comprehensive manner
[14]. e seasonal and spatial abundance of Ae. albop-
ictus in sylvatic and urban environments across the
Swiss-Italian border was examined using ovitraps and a
randomised sampling scheme. e results showed that
egg data were useful to determine the efficacy of the
intervention methods employed and that in the urban
environments of the non-intervention area egg densi-
ties were 2.26 times higher compared to the intervention
area. ese findings showed that, although the spread
of Ae. albopictus in Ticino could not be stopped, partly
because of the continuous reintroduction of mosqui-
toes from Italy, the intervention programme avoided an
explosive increase.
Here, we describe the results of the latest evaluation
of the Ticino IVM programme, which was carried out in
2019, 6 years after the one effectuated by Suter and col-
laborators [14]. e design of the present study was based
on the previous investigation. Since all the municipalities
with Ae. albopictus in Ticino are currently implement-
ing the IVM, we lacked control municipalities where the
mosquito is present and no IVM programme is followed.
As in Suter etal. [14], Italian municipalities just across
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Page 3 of 15
Ravasietal. Parasites Vectors (2021) 14:405
the Swiss-Italian border, where Ae. albopictus is present
but no coordinated intervention programme is in place,
served as control. Indeed, the municipalities surveyed in
the area across the Swiss-Italian border are very similar
in many respects (e.g. history, climate, dimension and
spatial structure) and geographically very close (located
within a 7-km radius). Moreover, Ae. albopictus popula-
tions across the Swiss-Italian border have been shown
to share a very similar genetic structure [15] due to the
colonization process from North Italy to Switzerland.
Ovitraps and Gravid Aedes Traps (GAT) were used as
complementary approaches to measure indirectly and
directly adult female mosquito abundance, respectively,
and to determine the efficacy of the IVM programme in
Ticino.
Methods
Study sites anddesign
e field surveys were carried out in six small to
medium-sized towns (3000 to 16,000 inhabitants) around
the border area between Ticino in Switzerland and the
Lombardy region in Italy (Fig.1). e municipalities are
located in the historical-geographical region of Insub-
ria. e climate of this region is characterized by dry
and sunny winters, with periods of foehn wind from the
North with occasional heavy snowfall, rainfall, especially
in the transitional seasons (spring and autumn), and
sunny summers interrupted by downpours that can also
be violent. e landscape of the region features foothills
and typical components of Lombard agriculture next to
residential, industrial and commercial urbanized areas.
e particular geographical position of Insubria has been
an incentive to build strong economic relations between
Ticino and the neighbouring Italian provinces, resulting
in intense traffic across the border, with on average over
67,900 Italian workers commuting to Switzerland in a
single workday [16].
e six municipalities surveyed are located within a
radius of 7km, have similar dimension and urban struc-
ture, with a small-town centre surrounded by residential
areas, and similar climatic (Additional file1: Figure S1)
and altitudinal characteristics (255–414 m a.s.l.). e
Fig. 1 The six municipalities across the Swiss-Italian border, denoted by the thick dark grey line, surveyed in 2019. The red squares and blue
diamonds represent sampling sites in intervention and non-intervention areas, respectively. Map modified from https:// map. geoad min. ch/
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Page 4 of 15
Ravasietal. Parasites Vectors (2021) 14:405
three municipalities (i.e. Balerna, Coldrerio and Men-
drisio) in the Mendrisiotto district in Ticino follow sys-
tematically the cantonal IVM since 2009 with monthly
or weekly treatments of catch basins with diflubenzuron-
or Bti-based products, respectively [5]. e treatment
period starts at beginning mid-May, depending on the
precipitation pattern, and lasts until mid-end September.
In 2019, to encourage citizens to treat permanent breed-
ing sites on private properties, Bti-based granules (Vecto-
Bac® G) were made freely available in each municipality.
We categorized these three municipalities as “interven-
tion” areas. e three municipalities in the provinces of
Como (i.e. Maslianico and Uggiate-Trevano) and Varese
(i.e. Malnate), in Lombardy, to our knowledge, did not
follow an IVM and only applied adulticides irregularly.
ey were, therefore, categorized as “non-intervention”
areas.
e territory of each municipality was divided into
a grid of 250 × 250m cells [5, 14]. Six cells, called sam-
pling sites, were selected at random in urban context in
each municipality. An ovitrap and a Gravid Aedes Trap
(GAT, Biogents, Germany) were placed in each sampling
site at a distance of 20–100m from each other to avoid
as much as possible interference in mosquito attraction
on the ground at hidden, shaded, wind-protected loca-
tions close to vegetation. All traps were geo-referenced
and uniquely labelled. e ovitraps were the same as used
for the surveillance of Ae. albopictus in Ticino [5, 14].
Both ovitraps and GATs mimic breeding sites, attracting
container-breeding mosquitoes in search of an oviposi-
tion site [13]. Ovitraps allow the invasive mosquitoes to
deposit their eggs on a wooden slat and to fly away, while
GATs capture the mosquitoes by means of an adhesive
plastic sheet [17].
Sample collection andprocessing
Field surveys were carried out from mid-end May (cal-
endar week 21) to the beginning of October (calendar
week 41) 2019. e slats of ovitraps and the sheets of the
GATs were replaced at the same time every 14 (range 10
to 19)days with new ones [14]. As a result, ten collec-
tion rounds were executed for each ovitrap, except for
ovitraps in Uggiate-Trevano, where the survey started 2
weeks later as for the survey with all GATs.
In addition to the already established Ae. albopic-
tus and the indigenous species Aedes geniculatus, two
other invasive container-breeding mosquito species, i.e.
Aedes japonicus and Aedes koreicus, have started spread-
ing across the study area since 2013 [18]. Although Ae.
japonicus and Ae. koreicus have a lower vectorial compe-
tence and therefore lower public health significance com-
pared to Ae. albopictus [19], their presence can introduce
a confounding factor in the surveillance of Ae. albopictus.
Indeed, while eggs of Ae. geniculatus can be easily distin-
guished by morphology from the other Aedes species, it
is not possible to distinguish morphologically the eggs
of Ae. albopictus, Ae. japonicus and Ae. koreicus without
resorting to special microscopy equipment and expertise
[20].
After transportation to the laboratory, the ovitrap
wooden slats and GAT adhesive plastic sheets were
examined using a stereo microscope (EZ4 D, Leica
Microsystems, Germany) for the presence of Aedes eggs
and adults, respectively. Adult mosquito females in GATs
were identified to the species level by morphology and
enumerated. To evaluate the presence of Ae. koreicus and
Ae. japonicus in ovitraps, most (87%) of the positive ovit-
raps were analysed by matrix-assisted laser desorption/
ionization time of flight mass spectrometry (MALDI-
TOF MS). e rest of the positive ovitraps (13%) could
not be analysed because of the low number (1–3) and low
quality (dryness or other types of damage) of eggs present
on the wooden slat. For this analysis, each wooden slat
was divided into ten sectors. For each sector where eggs
were present, three to five intact eggs were randomly
picked and identified through MALDI-TOF MS with an
AXIMA Confidence mass spectrometer (Shimadzu Bio-
tech, Kyoto, Japan) following the method described in
Schaffner etal. [20].
Data analysis
e numbers of Ae. albopictus eggs and adult females
were recorded in an Excel sheet together with additional
information such as the sampling site, date, category of
area, etc. (Additional file 2: TableS1, Additional file3:
TableS2 and Additional file4: TableS3). Statistical analy-
sis was performed through the freely available software
R, version 4.0.3 [21]. All analyses are fully reproducible as
data, code and package version control tools are available
(Additional file2: TableS1, Additional file3: TableS2,
Additional file4: TableS3, Additional file5: Dataset S1,
Additional file6: Dataset S2, Additional file7: Dataset S3,
Additional file8: Text S1, Additional file9: Text S2 and
Additional file 10: Text S3). All statistical analyses are
documented in Additional file 11: Text S4, Additional
file12: Text S5, Additional file13: Text S6 and Additional
file14: Text S7.
A Spearman’s rank order correlation was used to evalu-
ate the relationship between the number of eggs per ovit-
rap and the number of Ae. albopictus adult females in the
GAT deployed in the same sampling site. Both variables
were square-root transformed.
ree modelling analyses were performed. e first two
analyses aimed at modelling the number of Ae. albopictus
eggs found in ovitraps and the number of Ae. albopictus
adult females caught with GATs in 2019, respectively. e
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Page 5 of 15
Ravasietal. Parasites Vectors (2021) 14:405
third analysis focused on the number of eggs found in
ovitraps in 2012, 2013 and 2019. e data for the years
2012 and 2013 come from the study published by Suter
etal. [14]. ese data are freely available at https:// doi.
org/ 10. 1371/ journ al. pntd. 00043 15. s001. e area moni-
tored in 2012 and 2013 (Additional file 15: Figure S2)
was larger compared to the one monitored in 2019 but it
included five of the six municipalities surveyed in 2019,
namely Balerna, Coldrerio, Mendrisio, Maslianico and
Uggiate-Trevano. Additionally, the non-intervention
municipality Malnate, surveyed in 2019, was located just
outside the southwest boundary of the area studied in
2012 and 2013. erefore, we believe that the results of
both surveys are comparable as well as representative of
the situation in the urban communities across the Swiss-
Italian border. Note that the study performed by Suter
etal. [14] collected data in both sylvatic and urban envi-
ronments. Since the present study focused on urban envi-
ronments, for the third analysis we only used the “urban”
data from Suter etal. [14] and the data collected in 2019.
e graphical analysis was performed with the ggplot2
package, version 3.3.3 [22]. All three analyses were per-
formed with the glmmTMB function from the glmmTMB
package version 1.0.2.1 [23]. Inference was performed
with likelihood ratio tests (for P-values) and profiling
likelihood methods (to estimate confidence intervals)
[24]. e level of significance was set at α = 0.05. Differ-
ent distributional families and non-nested models were
compared with information criteria [25]. Model assump-
tions were assessed via usual residuals analyses. Quad-
ratic effects were modelled via orthogonal polynomials.
First model
e response variable “number of eggs” (No..eggs.
AEDES) was modelled with a generalised mixed-effects
model. In particular, to account for the nature of the
data, a negative binomial distribution was assumed. is
allowed accounting for the fact that we are dealing with
count data and that overdispersion is present. Alternative
families where compared (Additional file 11: Text S4).
e predictor of main interest “AREA” defined whether
the trap was to be found in a sampling site under IVM
(i.e. in intervention area) or not (i.e. in non-intervention
area) and was included as a fixed effect. e other pre-
dictors were “Municipality”, “TRAP.ID.fac” (i.e. trap iden-
tity), “Day of the year”, “No..Days.ovitrap.in.field” (i.e.
number of days that the trap was deployed in the field)
and “Altitude” (i.e. altitude of the trap in meters a.s.l.).
Municipality and TRAP.ID.fac were taken as random
effects. No..Days.ovitrap.in.field was included to account
for the “exposure” effect, as not all traps stayed exactly
14days in the field (range 10 to 19days). Traps that are
left longer in the field are expected to contain more eggs.
e seasonal effect of time (i.e. date when ovitrap col-
lected, “Day of the year”) was modelled with a quadratic
effect.
e equation used to fit the model is:
Second model
e same analysis as in the first model was applied to
the response variable “number of Ae. albopictus adult
females in GAT” (No..Ad..Albo.in.GAT hereafter). As the
graphical analysis indicated that there might be an inter-
action between “Day of the year” and “AREA”, we fitted a
model that included this two-fold interaction (Additional
file12: Text S5).
Third model
e number of eggs in urban areas in 2012 and 2013
from Suter etal. [14] and the number of eggs collected
in 2019 were also modelled together. About half (45%)
of the observations in this dataset were zeros. ere-
fore, the negative binomial used for the two other analy-
ses was extended such that the excess of zeros could be
accounted for. To do that, we fitted a hurdle model, where
a part of the model focused on the presence-absence part
of the data and another part of the model focused on the
abundance (Additional file13: Text S6). e presence-
absence part of the model was modelled with binomial
family, while the abundance part of the model was mod-
elled with the truncated negative binomial family. e
predictors used here were the same as in the previous
two analyses, except for the “No..Days.ovitrap.in.field”,
not present in Suter et al. [14] data and therefore not
included. In addition, the variable “Year” (2012, 2013 and
2019) was added to the model. is model is also a gener-
alised mixed-effects model.
Results
In each of the six municipalities studied, six sampling
sites were selected and one ovitrap and one GAT were
deployed in each sampling site. e wooden slats of ovit-
raps and adhesive plastic sheets of GATs were replaced
with new ones every 2weeks (range 10–19days). In five
municipalities (i.e. Balerna, Coldrerio, Malnate, Masli-
anico and Mendrisio), ovitraps were deployed from
glmmTMB(No..eggs.AEDES ∼AREA +
poly
Day.ovitrap.collected, degree =2+
scale
(ALTITUDE)+
No..Days.ovitrap.in.field
+
(
1|TRAP.ID.fac)+(1|MUNICIPALITY)
,
family
=nbinom1,
data =d.eggs.2019)
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Page 6 of 15
Ravasietal. Parasites Vectors (2021) 14:405
mid-end May and inspected for ten consecutive rounds,
with a total of 300 wooden slats collected (5 munici-
palities × 6 sampling sites × 1 ovitrap × 10 collection
rounds). In Uggiate-Trevano, the deployment of ovitraps
started 2 weeks later and inspection was carried out for
nine rounds, with 54 wooden slats collected in total (1
municipality × 6 sampling sites × 1 ovitrap × 9 collection
rounds). Deployment of GATs also started 2 weeks after
the first deployment of ovitraps, in all six municipalities,
and traps were inspected for nine rounds, with a total of
324 adhesive sheets collected (6 municipalities × 6 sam-
pling sites × 1 GAT × 9 collection rounds).
Of the 354 and 324 times ovitraps and GATs were
inspected, traps were found altered (e.g. turned over
or with missing parts) 27 and 23 times, respectively
(Table1, Additional file2: TableS1 and Additional file3:
Table S2). From the 327 intact wooden slats and 301
intact adhesive sheets, 263 (80.4%) and 256 (85.1%) were
positive for Aedes spp. eggs and adult females, respec-
tively. MALDI-TOF MS was used to evaluate the pres-
ence of different exotic Aedes species in 229 of the 263
positive wooden slats. For the majority (200, i.e. 87%) of
the slats analysed, MALDI-TOF MS detected eggs of Ae.
albopictus only. In the remaining 29 slats, the species Ae.
japonicus and Ae. koreicus were also detected in June and
July in all the municipalities surveyed. Of the 256 positive
adhesive sheets, 249 (97%) captured only adults of Ae.
albopictus. Aedes japonicus was found on five adhesive
sheets in Balerna, Coldrerio and Mendrisio (five adults
in total) in June and July. Aedes koreicus was captured on
two adhesive sheets in Malnate and Uggiate-Trevano (six
adults in total) in June and July. ese results suggest that
the large majority of the eggs found in the ovitraps were
laid by Ae. albopictus. erefore, the eggs in the ovitraps
were all counted as Ae. albopictus eggs in the subse-
quent analyses. Moreover, a significant positive correla-
tion (rs(281) = 0.381, P < 0.0001) was observed between the
number of eggs per ovitrap and the number of Ae. albop-
ictus adult females in the GAT deployed 20–100m from
the corresponding ovitrap.
In 2019, egg counts per ovitrap per inspection rounds
of about 14days ranged from 0 to 513 in the municipali-
ties that were part of the intervention area (i.e. Balerna,
Coldrerio and Mendrisio) and from 0 to 2117 in the
municipalities not following a defined management plan
(i.e. Malnate, Maslianico and Uggiate-Trevano) (Table1).
Mean Ae. albopictus egg counts were consistently higher
in the non-intervention municipalities (Table1).
e first eggs in the season were found already in
the first period of the survey in late May to early June
(Fig. 2a). In the non-intervention municipalities, there
was a steady increase in the number of eggs with a peak
in August, followed by a decrease in September and
October, indicating the end of the reproductive season.
In the intervention municipalities, the increase in the
number of eggs was much more contained compared to
the non-intervention municipalities, without an evident
peak (Fig.2a). e model fitted well (Additional file11:
Text S4) and the fitted values agreed with the raw data
(Figs. 2a, 3a). e effect of AREA (i.e. intervention vs.
non-intervention) was clearly present and biologically
relevant (P < 0.0001). In non-intervention sites there
were about four times (3.8) more eggs than in interven-
tion sites (95% confidence interval, CI: 2.7–5.4). e
estimated variability of the random effects indicated
that there was very little variation among municipalities.
Table 1 Summary statistics of Ae. albopictus egg (ovitrap wooden slats) and adult female (GAT adhesive plastic sheets) counts in the
six municipalities examined
Municipality
(type of area) Trap type
(tot. deployed) Altered Positive
(%) Ae. albopictus egg/adult count per trap
Minimum Median Mean Maximum
Balerna Ovitrap (60) 11 38 (63.3) 0 25.0 56.8 407
(Intervention) GAT (54) 0 42 (77.8) 0 4.0 4.1 13
Coldrerio Ovitrap (60) 4 40 (66.7) 0 18.5 80.1 513
(Intervention) GAT (54) 2 43 (79.6) 0 4.0 6.3 22
Mendrisio Ovitrap (60) 0 35 (58.3) 0 13.5 59.3 401
(Intervention) GAT (54) 2 37 (68.5) 0 2.0 3.2 16
Malnate Ovitrap (60) 1 53 (88.3) 0 144.0 261.2 2,117
(Non-intervention) GAT (54) 3 48 (88.9) 0 10.0 14.2 83
Maslianico Ovitrap (60) 5 51 (85.0) 0 160.0 218.6 1,073
(Non-intervention) GAT (54) 10 40 (74.1) 0 6.0 7.7 26
Uggiate-Trevano Ovitrap (54) 6 46 (85.2) 0 184.5 223.8 864
(Non-intervention) GAT (54) 6 46 (85.2) 0 13.0 18.0 64
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Page 7 of 15
Ravasietal. Parasites Vectors (2021) 14:405
Note, however, that the variance component “municipal-
ity” is estimated based on six municipalities only. is
number does fulfil the minimal number of levels required
to obtain a sensible estimated of a variance component,
however, does not allow to estimate it with great preci-
sion [24]. As the main predictor of interest varies among
Fig. 2 Numbers of Ae. albopictus eggs per ovitrap (a) and adult females per GAT (b) over time in intervention and non-intervention municipalities.
Each line on the graphs represents a site. Note that these graphs represent the raw data. Smoothers (blue lines with grey confidence bands) were
added to highlight seasonal trends
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Page 8 of 15
Ravasietal. Parasites Vectors (2021) 14:405
municipalities, we have further inspected this limitation
of the model. In particular, we also fitted a generalised
mixed-effects model where municipality was taken as a
fixed effect. e municipality estimates were then used to
perform a post hoc test to compare the two AREA lev-
els (i.e. “intervention” against “non-intervention”). e
Fig. 3 Observed data (grey lines) and model fit (red lines) for numbers of Ae. albopictus eggs per ovitrap (a) and adults per GAT (b) in intervention
and non-intervention municipalities. Each grey line represents a site (i.e. the actual observations used to fit the model). The fit is visualized in the
original scale (i.e. without any transformation). Note that the fitted values shown here are not adjusted to correct for bias due to Jensen’s inequality
[26]. This applies to all graphs produced with fitted or predicted values here
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Page 9 of 15
Ravasietal. Parasites Vectors (2021) 14:405
results of this alternative approach are fully in agreement
with the model where municipality is taken as a random
effect. In both models, AREA plays a very relevant role.
Indeed, the estimated AREA effect was almost identical
in these two models and also the inference procedure
leads to equivalent results. Note that for the sake of brev-
ity and to avoid redundancy, the results of this alternative
but agreeing analysis are not shown in the appendices.
ere seemed to be some variation among ovitraps. To
quantify these differences among traps we looked at the
two most extreme estimated conditional modes: the
“worst” ovitrap had − 40% eggs with respect to an “aver-
age” ovitrap; the “best” ovitrap had + 140% eggs with
respect to an “average” ovitrap. Altitude did not seem to
play a relevant role (P = 0.607). e number of days of
trap deployment in the field had a significant effect (the
model predicted about 10% more eggs for each additional
day the ovitrap was deployed in the field; P = 0.003).
e number of Ae. albopictus adult females per GAT in
2019 ranged from 0 to 22 in the municipalities in inter-
vention area and from 0 to 83 in the municipalities in
non-intervention area. As for the egg counts, mean Ae.
albopictus adult female counts were consistently higher
in the non-intervention municipalities than in the inter-
vention ones (Table1). e same seasonal trend as for
eggs, with a much more contained increase and no evi-
dent peak in numbers in the intervention municipalities,
compared to the non-intervention ones, could be
observed for adult females (Figs.2b, 3b).
e model fitted well (Additional file12: Text S5) and
the fitted values agreed with the raw data (Figs.2b, 3b).
e numbers of Ae. albopictus adult females per GAT
were significantly higher in the non-intervention sites
than in the intervention ones (P < 0.0001; see Additional
file12: Text S5). However, differently from the numbers
of eggs, the ratio between non-intervention and inter-
vention was not fixed over time (Fig.4). e ratio varied
between about two at the beginning and end of the sea-
son and increased to almost four in early/mid-August.
Compared to the numbers of eggs, there was more vari-
ation among municipalities belonging to the same area
group. Neither the altitude nor the number of days of
trap deployment in the field seemed to play a relevant
role (P = 0.095 and P = 0.566, respectively). ere was
non-negligible variability among traps (“worst” GAT:
−80% adults with respect to an “average” GAT; “best”
trap: + 190% adults with respect to an “average” GAT).
e difference between the intervention and non-inter-
vention areas was quite evident also when we compared
the numbers of eggs per ovitrap among 2012, 2013 [14]
and 2019 (Fig.5). Furthermore, this difference seems to
have massively increased after 2013. e model included
the three-fold interaction among time of the year (day),
year and AREA. In other words, the data strongly
Fig. 4 Evolution of the non-intervention/intervention ratio over time for the number of Ae. albopictus adult females per GAT. The non-linear effect
of time is approximated with a quadratic function
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Page 10 of 15
Ravasietal. Parasites Vectors (2021) 14:405
Fig. 5 Numbers of eggs per ovitrap over time in intervention (red) and non-intervention (green) municipalities, for the years 2012, 2013 [14] and
2019. Each red and green fine line represents a trap. Smoothers (lines with grey confidence bands) were added to highlight seasonal trends
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
Page 11 of 15
Ravasietal. Parasites Vectors (2021) 14:405
supported the hypothesis that the seasonal bow-shaped
pattern differed among years and among AREA levels.
e model fit also showed that more eggs were consist-
ently found in the non-intervention than intervention
sites and that the non-intervention/intervention ratio
appears to have dramatically increased from 2013 to 2019
(Fig.6). e non-intervention/intervention ratio was not
fixed but varied over the time in 2012 and 2013, as well
as across years. As this model is composed of two parts,
it is not possible to show a simple graph of the evolu-
tion of the ratio over time and across years (Additional
file13: Text S6). However, the graph with the fitted values
(Fig.6) is very useful to understand what is happening
over time. Indeed, the peak in the non-intervention sites
went from fewer than 150 eggs in 2012 and 2013 to about
330 in 2019 (Fig.6). On the other hand, the increase for
intervention sites was much more moderate (i.e. from
about 65 to about 100). e actual observations (i.e. the
raw data) went up to more than 2000 in 2019, which
compressed the graph. erefore, the graphs in Fig. 6
are zoomed to the area of interest (i.e. between ) and 400
counts) to better compare curves.
In this model, altitude seemed to play a role (P = 0.051),
with an expected negative effect on the numbers of eggs.
ere was some relevant variability among traps and
among municipalities (Additional file13: Text S6). e
presence/absence process seemed to be affected more
by municipality than by trap (Additional file13: Text S6).
e abundance, contrarily, seemed to be affected by trap
more than by municipality (Additional file13: Text S6).
Note that, although the increase of the ratio over year
seems to be very strong, additional years are required to
draw robust conclusions about this trend. A future rep-
etition of this study is indeed planned with a larger num-
ber of locations on both sides of the border.
Discussion
e 2019 survey highlighted a conspicuous difference
between intervention and non-intervention municipali-
ties in the seasonal distribution of numbers of both eggs
and adult females of Ae. albopictus. In the non-interven-
tion municipalities, there was a steady increase in the
number of eggs and adults starting in June with a peak
in August, followed by a decrease in September and/or
October, indicating the end of the mosquito reproductive
season. In the intervention municipalities, the increase
in the number of eggs and adults was much more con-
tained, without an evident peak. is very clear pattern
strongly supports the efficacy of the IVM programme
Fig. 6 Observed data (grey lines) and model fits (green and red lines) for numbers of eggs per ovitrap in intervention and non-intervention
municipalities in the years 2012, 2013 [14] and 2019. Each grey line represents an ovitrap (i.e. the actual observations used to fit the model). The fit is
visualized in the original scale, without any transformation. Graphs zoomed to the area between 0 and 400 counts. The x-range is adapted to each
panel. The maximal fitted values in each year-area combination are shown on the bottom right
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
Page 12 of 15
Ravasietal. Parasites Vectors (2021) 14:405
implemented in Ticino, helping in keeping the numbers
of Ae. albopictus very stable during the reproductive
season.
In 2019, the number of Ae. albopictus eggs in the urban
environment was 3.8 times higher in non-intervention
sites than in intervention sites. Compared to the situa-
tion in 2012 and 2013, with a proportion of 2.26 [14], the
divergence between non-intervention and intervention
areas seems to have dramatically increased (note, how-
ever, that these two ratios are not formally compared).
In the Italian communities, where no IVM programme
was implemented, we noticed a striking increase in the
number of eggs per ovitrap, with an average of about 50
eggs in 2012 and 2013 to more than 200 eggs in 2019. e
fitted model showed a peak in eggs per ovitrap from less
than 150 in 2012 and 2013 to about 330 in 2019. In com-
parison, in the Swiss sites following an IVM programme,
the increase was much more moderate, with an average
of about 20 eggs per ovitrap in 2012 and 2013, to between
57 and 80 eggs in 2019, while the fitted model showed a
moderate increase in the peak of eggs from about 65 in
2012 and 2013 to about 100 eggs per ovitrap in 2019.
ese observations strongly suggest that the IVM pro-
gramme implemented in Ticino helped keep the num-
bers of Ae. albopictus almost stable over the years in the
urban environment. Contrarily, the absence of an IVM
programme in the Italian communities across the border
seems to lead to a deterioration of the situation, with an
increase in numbers of Ae. albopictus. Further evalua-
tions of the control system in the coming years will allow
confirming whether this is a consolidated trend.
In 2013, Suter etal. [14] observed that few ovitraps
(30%) in Ticino were positive for Ae. albopictus ear-
lier in the warm season, in early/mid-June, while in
Italy many traps (62%) were already positive during
the same period. A possible explanation was the posi-
tive impact of control treatments at the end of the 2012
season and before the start of the 2013 season in low-
ering mosquito reproduction in Ticino. Another sug-
gested possibility was that mosquito populations in
Ticino, rather than being stable overwintering popula-
tions, were annually re-introduced from Italy, so that
their numbers managed to pick up only later in the
season. In early/mid-June 2019, in contrast, half of the
ovitraps (50%) in Ticino were already positive for Ae.
albopictus, and most ovitraps (80%) were positive in
the non-intervention areas. It seems, therefore, that in
2019 the numbers of tiger mosquitoes in Ticino picked
up faster compared to 2013. is could be due to the
presence of more stable overwintering populations
in 2019 compared to those of 2013. However, at the
beginning of the 2019 survey, between end of May and
beginning of June, very few ovitraps (7%) were positive
in Ticino, while half of the traps (58%) were positive in
the non-intervention municipalities. A likely explana-
tion is that the larvicide treatments in Ticino at the end
of the 2018 reproduction season reduced the number of
mosquitoes laying diapausing eggs. is, in addition to
the impact of control treatments at the start of the 2019
season, slowed down the annual reconstitution of mos-
quito populations in the intervention areas contrasting
to the non-intervention areas.
A concern in the 2012 and 2013 survey was the use
of egg counts from ovitraps to estimate and compare
Ae. albopictus densities. Ovitrap data are considered
appropriate to assess presence/absence of Ae. albopictus
in a given site but not for adult population estimation
because the relationship between the two parameters
might be affected by several factors. For example, a single
female mosquito might lay eggs at multiple breeding sites
or the ovitraps may compete with nearby sites [13]. In
2019, gravid Aedes traps (GATs) were deployed in paral-
lel to the ovitraps to compare the two surveillance meth-
ods. Both methods showed variability among traps in the
same municipality and within traps themselves, with a
higher variability among GATs. A possible explanation
could be variability in the presence of breeding sites other
than traps during the study period, with an effect more
accentuated on the GATs, since individuals are captured
with this method. Nevertheless, a significant positive cor-
relation was found between eggs in ovitraps and number
of Ae. albopictus adult females as shown by other studies
[9, 27, 28]. e numbers of Ae. albopictus adult females
per GAT followed the same trend as the numbers of eggs
per ovitrap, being significantly higher in the non-inter-
vention sites than in the intervention ones, with a ratio
of non-intervention/intervention areas varying between
two and four over the season. erefore, we concluded
that both egg and adult data are useful to determine
the efficacy of intervention methods employed, or lack
thereof.
It could be problematic to estimate the numbers of
Ae. albopictus by using ovitraps because of the increas-
ing presence of other invasive Aedes species, such as Ae.
japonicus and Ae. koreicus, whose eggs cannot be clearly
morphologically discerned from the eggs of Ae. albopic-
tus and, therefore, could consequently introduce a bias
in the evaluation of egg counts. However, the identifica-
tion of randomly picked eggs through MALDI-TOF MS,
combined with the morphological species determination
of adults, confirmed that most mosquitoes found at the
sampling sites were tiger mosquitoes. ereby, the influ-
ence of other Aedes species on the results was negligible.
Regardless, the containment measures adopted for Ae.
albopictus also apply to other container-breeding Aedes
species. erefore, by lowering the density of the other
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Page 13 of 15
Ravasietal. Parasites Vectors (2021) 14:405
depositing mosquitoes we were not introducing a bias in
the data.
In terms of public health risk, a main concern related
to the presence and abundance of the tiger mosquito is
its role as a vector of arboviruses. Outbreaks of chikun-
gunya and dengue viruses have already occurred in Italy
and France [8]. In Switzerland, autochthonous cases of
chikungunya and dengue viruses have not been reported
so far and we are not aware of autochthonous cases in
the Italian communities included in the present study.
However, the number of imported cases in Switzerland,
including Ticino, increases regularly (https:// www. bag.
admin. ch) as it does in the neighbouring Italian regions
(https:// www. epice ntro. iss. it/ arbov irosi/ bolle ttini) and
in other European countries. In 2008, after the 2007 chi-
kungunya epidemic in the Emilia-Romagna region of
northern Italy, Carrieri and collaborators [29] calculated
the epidemic risk threshold in terms of numbers of eggs
per ovitrap above which an arbovirus epidemic may ini-
tiate, in presence of imported human cases. A threshold
of 250–450 and 451–750 eggs per ovitrap in 14days was
calculated for an epidemic of E1-A226V mutated and
non-mutated form of the chikungunya virus, respec-
tively [30]. In Ticino intervention areas, the mean num-
ber of eggs per ovitrap in 14days in 2019 was between
57 and 80, while in non-intervention areas across the Ital-
ian border it was about 200. Maximum number of eggs
per ovitrap in Ticino was between 400 and 500, while in
non-intervention areas across the Italian border it was
about 1000. Although the geographical characteristics of
the Emilia-Romagna region are different from the area
monitored in the present work, we perceive that the risk
of an arbovirus epidemic is much more probable in the
non-intervention areas. Moreover, even with the lower
number of Ae. albopictus in Ticino, a study carried out
in 2018 in six municipalities of the canton estimated that
the risk of outbreak in the case of the introduction of chi-
kungunya, dengue or Zika viruses was present in all the
municipalities investigated [31]. Consequently, a strategy
for preventing and managing potential arbovirus out-
breaks, as well as the surveillance and control activities of
Ae. albopictus according to the situation and level of epi-
demic risks, has been recently elaborated for Ticino [32].
e scope of this work was to evaluate the effective-
ness of integrated control practices in the field, where
not all variables can be controlled. As an observational
study, we must be aware that differences between
intervention sites and non-intervention sites could
be explained by other yet unknown factors differ-
ing between Switzerland and Italy. is is particularly
important given the fact that 36 sites inspected were
grouped in six municipalities. Ideally, larger sample
sizes will be required to strengthen the evidence in
favour of IVM programmes, which requires consider-
able sampling and logistic efforts. Note that following
an experimental approach, namely setting up untreated
control sites in Ticino, where all municipalities follow
an IVM programme, would be ethically unfeasible. e
non-intervention control sites selected in Italy were
very similar and geographically close to the interven-
tion sites in Ticino.
Our results are in accordance with previous studies
on integrated control strategies (e.g. [33–35]). ese
results strongly support the hypothesis that IVM
plays an essential role in reducing the nuisance for the
human population. In addition, from a public health
point of view, it might limit both the risk of autochtho-
nous transmission and the size of potential epidemics,
as shown by Guzzetta et al. [36]. According to Balda-
cchino etal. [9], the most effective integrated control
includes door-to-door education. e door-to-door
education and treatment actions were included in the
Ticino IVM between 2008 and 2010 [5]. During this
period, breeding sites in private domains were removed
directly by GLZ, Civil Protection Units or municipal-
ity workers after agreement with the residents. With
the gradual spread of the mosquito to larger areas,
this fine-scale approach became less and less sustain-
able. erefore, the part of the IVM regarding private
domains currently focuses on a less fine but constant
approach over the years with extensive public informa-
tion campaigns carried out every year, including for
example information events and door-to-door deliv-
ery of education material [5]. In addition, the munici-
palities can issue a specific ordinance not permitting
neglected breeding sites for the tiger mosquito on the
municipality territory. Consequently, the GLZ and the
municipality workers are allowed to conduct inspec-
tions to verify the presence of breeding sites in private
domains and report violations of the ordinance.
Reintroductions of mosquitoes in Ticino from across
the border are probably occurring every year. From our
data, it is not possible to tell the effect of these reintro-
ductions on the quantities of Ae. albopictus in Ticino.
However, the results indicate that with the implemen-
tation of an IVM programme, it is possible to contain
the numbers of Ae. albopictus at a manageable level,
irrespective of possible constant reintroduction of indi-
viduals from outside the intervention areas. Although
it would certainly be desirable to undertake concerted
actions across the Swiss-Italian Insubria region, with
the development and implementation of a transna-
tional action plan for the surveillance and control of Ae.
albopictus, it is possible to achieve containment of the
vector also without cross-border concerted measures.
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Page 14 of 15
Ravasietal. Parasites Vectors (2021) 14:405
Conclusions
In 2019, Ae. albopictus egg numbers in urban environ-
ment were about four times higher in non-intervention
sites, on the Italian side of the Swiss-Italian border than
in intervention sites in Ticino. e numbers of Ae. albop-
ictus adult females followed the same trend. In addition,
the comparison with the previous survey carried out in
2012 and 2013 indicates that this proportion seems to
have almost doubled in the past 6 years. We acknowledge
that other unknown factors might explain the difference
in mosquito densities, and further studies are required
to collect additional evidence (this is especially true for
the increasing trend in ratios observed here). Neverthe-
less, the results here support the effectiveness of the IVM
programme implemented in Ticino. us, the integration
of control measures targeting the aquatic phase of the
mosquito (i.e. removal of breeding sites and treatment
of permanent ones with larvicides) and different public
education strategies seem to help in keeping the numbers
of Ae. albopictus almost stable during the reproductive
season of the mosquito. In addition, the perpetuation of
these measures seems to help keeping the numbers of Ae.
albopictus almost stable even over the years in the urban
environment. ese are relatively simple measures that,
if constantly maintained over the years, show their effec-
tiveness in keeping the mosquito population in check.
Abbreviations
GAT : Gravid Aedes trap; GLZ: Gruppo Lavoro Zanzare; IVM: Integrated vector
management; MALDI-TOF MS: Matrix-assisted laser desorption/ionization time
of flight mass spectrometry.
Supplementary Information
The online version contains supplementary material available at https:// doi.
org/ 10. 1186/ s13071- 021- 04903-2.
Additional le1: Figure S1. Comparison of monthly average (a),
minimum (b) maximum (c) temperatures and precipitations (d) between
intervention and non-intervention areas.
Additional le2: TableS1. Data from ovitraps with Aedes albopictus egg
counts, in csv format. Variables included are WGS84.LAT (latitude of trap);
WGS84.LNG (longitude of trap); ALTITUDE (altitude of trap); AREA (type of
area, i.e. intervention or non-intervention); MUNICIPALITY; Date.when.ovit-
rap.installed; Date.when.ovitrap.collected; No..Days.ovitrap.in.field; Week.
when.ovitrap.collected; No..eggs.AEDES; No..Eggs.AEDES.in.14.days; TRAP.
ID.fac (trap identity); Day.ovitrap.collected and no.eggs.normalised.14.days.
Additional le3: TableS2. Data from Gravid Aedes Traps (GATs) with
Aedes albopictus female counts, in csv format. Variables included are
WGS84.LAT (latitude of trap); WGS84.LNG (longitude of trap); ALTITUDE
(altitude of trap); AREA (type of area, i.e. intervention or non-intervention);
MUNICIPALITY; Date.when.GAT.installed; Date.when.GAT.collected; No..
Days.GAT.in.field; Week.when.GAT.collected; No..Ad..Albo.in.GAT; No..Ad..
Albo.in.14.days; TRAP.ID.fac (trap identity) and Day.GAT.collected.
Additional le4: TableS3. Aedes albopictus egg counts from 2012, 2013
[14] and 2019 in csv format. Variables included are AREA (type of area,
i.e. intervention or non-intervention); MUNICIPALITY; TRAP.ID.fac (trap
identity); DATE; N.ALBOPICTUS (number of Ae. albopictus eggs); ALTITUDE
(altitude of trap); Year; Day (day of the year) and study (Flacio = present
study; Suter = Suter et al. [14]).
Additional le5: Dataset S1. Data from ovitraps with Aedes albopictus
egg counts in 2019, in RDS format (https:// www.r- proje ct. org/https://
www.r-project.org/).
Additional le6: Dataset S2. Data from Gravid Aedes Traps (GATs) with
Aedes albopictus female counts in 2019, in RDS format (https:// www.r-
proje ct. org/).
Additional le7: Dataset S3. Aedes albopictus egg counts from 2012,
2013 [14] and 2019 in RDS format (https:// www.r- proje ct. org/).
Additional le8: Text S1. R-script for the analysis of the number of Aedes
albopictus eggs collected in 2019. This R-script has been extracted from
the corresponding Rmarkdown file (https:// rmark down. rstud io. com/). It
allows for the full reproducibility of the analysis.
Additional le9: Text S2. R-script for the analysis of the number of Aedes
albopictus adult females collected in 2019. This R-script has been extracted
from the corresponding Rmarkdown file (https:// rmark down. rstud io.
com/). It allows for the full reproducibility of the analysis.
Additional le10: Text S3. R-script for the analysis of the number of
Aedes albopictus eggs collected in 2012, 2013 [14] and 2019. This R-script
has been extracted from the corresponding Rmarkdown file (https:// rmark
down. rstud io. com/). It allows for the full reproducibility of the analysis.
Additional le11: Text S4. This pdf file documents the full analysis of the
number of Aedes albopictus eggs collected in 2019. This pdf was created
with Rmarkdown and allows for the full reproducibility of the analysis.
Additional le12: Text S5. This pdf file documents the full analysis of
the number of Aedes albopictus adult females collected in 2019. This pdf
was created with Rmarkdown and allows for the full reproducibility of the
analysis.
Additional le13: Text S6. This pdf file documents the full analysis of the
number of Aedes albopictus eggs collected in 2012, 2013 [14] and 2019.
This pdf was created with Rmarkdown and allows for the full reproduc-
ibility of the analysis.
Additional le14: Text S7. This pdf file documents additional data analy-
ses of the number of Aedes albopictus eggs collected in 2019 performed at
a reviewer’s request. This pdf was created with Rmarkdown and allows for
the full reproducibility of the analysis.
Additional le15: Figure S2. Study area in the 2012 and 2013 evaluation
of the Ticino intervention programme [14]. The map was prepared using
the geographic information system (GIS) software ArcGIS version 10.0
(ESRI Inc., USA).
Acknowledgements
We thank the municipalities and the local residents involved in the survey for
their kind collaboration. Many thanks to Stefania Cazzin, Nikoleta Anicic and
all the other collaborators at the Laboratory of Applied Microbiology for their
assistance in the field and laboratory work. We also thank three anonymous
reviewers for their helpful comments and suggestions and Dr. Major S. Dhillon
for the English editing.
Authors’ contributions
DPM and EF designed the study and selected the study sites. DPM conducted
the fieldwork. MT, DR and DPM analysed the data. DR drafted the manuscript.
All authors read and approved the final manuscript.
Funding
Not applicable.
Availability of data and materials
All data generated or analysed during this study are included in this published
article and its supplementary information files.
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
Page 15 of 15
Ravasietal. Parasites Vectors (2021) 14:405
Declarations
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
Author details
1 Laboratory of Applied Microbiology, Department of Environment, Construc-
tion and Design, University of Applied Sciences and Arts of Southern Switzer-
land, via Mirasole 22A, 6500 Bellinzona, Switzerland. 2 Zurich Data Scientists
GmbH, Sihlquai 131, 8005 Zurich, Switzerland.
Received: 13 November 2020 Accepted: 28 July 2021
References
1. Paupy C, Delatte H, Bagny L, Corbel V, Fontenille D. Aedes albopictus,
an arbovirus vector: from the darkness to the light. Microbes Infect.
2009;11:1177–85.
2. Medlock JM, Hansford KM, Schaffner F, Versteirt V, Hendrickx G, Zel-
ler H, et al. A review of the invasive mosquitoes in Europe: ecology,
public health risks, and control options. Vector Borne Zoonotic Dis.
2012;12:435–47.
3. Knudsen AB, Romi R, Majori G. Occurrence and spread in Italy of Aedes
albopictus, with implications for its introduction into other parts of
Europe. J Am Mosq Control Assoc. 1996;12:177–83.
4. Wymann MN, Flacio E, Radczuweit S, Patocchi N, Lüthy P. Asian tiger
mosquito (Aedes albopictus)—a threat for Switzerland? Euro Surveill.
2008;13:8058.
5. Flacio E, Engeler L, Tonolla M, Lüthy P, Patocchi N. Strategies of a thirteen-
year surveillance programme on Aedes albopictus (Stegomyia albopicta) in
southern Switzerland. Parasit Vectors. 2015;8:208.
6. Flacio E, Engeler L, Tonolla M, Müller P. Spread and establishment of Aedes
albopictus in southern Switzerland between 2003 and 2014: an analysis of
oviposition data and weather conditions. Parasit Vectors. 2016;9:304.
7. Bonizzoni M, Gasperi G, Chen X, James AA. The invasive mosquito species
Aedes albopictus: current knowledge and future perspectives. Trends
Parasitol. 2013;29:460–8.
8. Barzon L. Ongoing and emerging arbovirus threats in Europe. J Clin Virol.
2018;107:38–47.
9. Baldacchino F, Bussola F, Arnoldi D, Marcantonio M, Montarsi F, Capelli G,
et al. An integrated pest control strategy against the Asian tiger mosquito
in northern Italy: a case study. Pest Manag Sci. 2017;73:87–93.
10. European Mosquito Control Association (EMCA). Guidelines for the con-
trol of mosquitoes of public health importance in Europe. Speyer. 2011.
11. European Centre for Disease Prevention and Control (ECDC). Vector
control with a focus on Aedes aegypti and Aedes albopictus mosquitoes:
literature review and analysis of information. Stockholm: ECDC; 2017. p.
57.
12. World Health Organization (WHO). Handbook for integrated vector
management. Geneva: World Health Organization; 2012.
13. European Centre for Disease Prevention and Control (ECDC). Guidelines
for the surveillance of invasive mosquitoes in Europe. ECDC Technical
Report, Stockholm: ECDC; 2012. p. 95.
14. Suter TT, Flacio E, Feijoó Fariña B, Engeler L, Tonolla M, Regis LN, et al.
Surveillance and control of Aedes albopictus in the Swiss-Italian border
region: differences in egg densities between intervention and non-
intervention areas. PLoS Negl Trop Dis. 2016;10:e0004315.
15. Sherpa S, Blum MGB, Capblancq T, Cumer T, Rioux D, Després L. Unravel-
ling the invasion history of the Asian tiger mosquito in Europe. Mol Ecol.
2019;28:2360–77.
16. Swiss Confederation. Federal Statistical Office. Cross-border commuters
[Internet]. [cited 2020 Sep 22]. https:// www. bfs. admin. ch/ bfs/ en/ home/
stati stics/ work- income/ emplo yment- worki ng- hours/ emplo yed- perso ns/
swiss- forei gn- natio nals/ cross- border- commu ters. html.
17. Ritchie SA, Buhagiar TS, Townsend M, Hoffmann A, Van Den Hurk AF,
McMahon JL, et al. Field validation of the Gravid Aedes Trap (GAT)
for collection of Aedes aegypti (Diptera: Culicidae). J Med Entomol.
2014;51:210–9.
18. Suter TT. The Asian tiger mosquito Aedes albopictus in Switzerland: biol-
ogy, surveillance and control. PhD Thesis, Basel University; 2016.
19. Kampen H, Werner D. Out of the bush: the Asian bush mosquito Aedes
japonicus japonicus (Theobald, 1901) (Diptera, Culicidae) becomes inva-
sive. Parasit Vectors. 2014;7:59.
20. Schaffner F, Kaufmann C, Pflüger V, Mathis A. Rapid protein profiling
facilitates surveillance of invasive mosquito species. Parasit Vectors.
2014;7:142.
21. R Core Team. R: A language and environment for statistical computing
[Internet]. Vienna: R Foundation for Statistical Computing; 2019. https://
www.r- proje ct. org/.
22. Wickham H. ggplot2: Elegant graphics for data analysis. New York:
Springer; 2016.
23. Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen
A, et al. glmmTMB balances speed and flexibility among packages for
zero-inflated generalized linear mixed modeling. R J. 2017;9:378–400.
24. Bates DM. lme4: Mixed-effects modeling with R [Internet]. 2010. p. 131.
http:// webcom. upmf- greno ble. fr/ LIP/ Perso/ DMull er/ M2R/R_ et_ Mixed/
docum ents/ Bates- book. pdf
25. Pinheiro JC, Bates DM. Mixed-effects models in S and S-PLUS. New York:
Springer; 2006. p. 528.
26. Nakagawa S, Johnson PCD, Schielzeth H. The coefficient of deter-
mination R2 and intra-class correlation coefficient from generalized
linear mixed-effects models revisited and expanded. J R Soc Interface.
2017;14:20170213.
27. Facchinelli L, Valerio L, Pombi M, Reiter P, Costantini C, Della TA. Develop-
ment of a novel sticky trap for container-breeding mosquitoes and evalu-
ation of its sampling properties to monitor urban populations of Aedes
albopictus. Med Vet Entomol. 2007;21:183–95.
28. Lau SM, Chua TH, Sulaiman W-Y, Joanne S, Lim YA-L, Sekaran SD, et al. A
new paradigm for Aedes spp. surveillance using gravid ovipositing sticky
trap and NS1 antigen test kit. Parasit Vectors. 2017;10:151.
29. Carrieri M, Angelini P, Venturelli C, Maccagnani B, Bellini R. Aedes albopic-
tus (Diptera: Culicidae) population size survey in the 2007 chikungunya
outbreak in Italy. II: estimating epidemic thresholds. J Med Entomol.
2012;49:388–99.
30. Bellini R, Carrieri M. Dengue, chikungunya e valutazione del rischio.
Ecoscienza. 2014;2:66–7.
31. Ravasi D, Parrondo Monton D, Guidi V, Flacio E. Evaluation of the public
health risk for autochthonous transmission of mosquito-borne viruses in
southern Switzerland. Med Vet Entomol. 2020;34:244–50.
32. Fouque F, Guidi V, Lazzaro M, Ravasi D, Martinetti-Lucchini G, Merlani G,
et al. Emerging Aedes-borne infections in southern Switzerland: prepar-
edness planning for surveillance and intervention. Travel Med Infect Dis.
2020;37:101748.
33. Abramides GC, Roiz D, Guitart R, Quintana S, Guerrero I, Giménez N.
Effectiveness of a multiple intervention strategy for the control of the
tiger mosquito (Aedes albopictus) in Spain. Trans R Soc Trop Med Hyg.
2011;105:281–8.
34. Fonseca DM, Unlu I, Crepeau T, Farajollahi A, Healy SP, Bartlett-Healy K,
et al. Area-wide management of Aedes albopictus. Part 2: Gauging the
efficacy of traditional integrated pest control measures against urban
container mosquitoes. Pest Manag Sci. 2013;69:1351–61.
35. Gavaudan S, Duranti A, Barchiesi F, Ruschioni S, Antognini E, Calandri E,
et al. Seasonal monitoring of Aedes albopictus: practical applications and
outcomes. Vet Ital. 2014;50:109–16.
36. Guzzetta G, Trentini F, Poletti P, Baldacchino FA, Montarsi F, Capelli G, et al.
Effectiveness and economic assessment of routine larviciding for preven-
tion of chikungunya and dengue in temperate urban settings in Europe.
PLoS Negl Trop Dis. 2017;11:e0005918.
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