ArticlePDF Available
Assessing the risk of autochthonous yellow
fever transmission in Lazio, central Italy
Mattia Manica
, Giorgio Guzzetta
, Federico FilipponiID
, Angelo Solimini
Beniamino Caputo
, Alessandra della Torre
, Roberto RosàID
*, Stefano Merler
1Department of Biodiversity and Molecular Ecology, Research and Innovation Centre, Fondazione Edmund
Mach, San Michele all’Adige, Trento, Italy, 2Center for Information Technology, Fondazione Bruno Kessler,
Trento, Italy, 3Epilab-JRU, FEM-FBK Joint Research Unit, Trento, Italy, 4Department of Public Health and
Infectious Diseases, Laboratory affiliated to Istituto Pasteur Italia–Fondazione Cenci Bolognetti, Sapienza
University of Rome, Rome, Italy
These authors contributed equally to this work.
Yellow fever virus (YFV) causes a highly lethal mosquito-borne disease that has recently
reemerged after 30 years of low incidence due to vaccination campaigns. Large epidemics
occurred in Angola and Democratic Republic of the Congo (DRC) in 2016 through 2017
(overall about 1,000 confirmed cases and 140 deaths) and in Brazil in 2017 through 2018
(2,037 confirmed cases and 674 deaths) [1,2]. The high international connectivity of Brazil
raises concern about the potential spread of disease to other countries by infected travelers [3,
4]; this possibility was confirmed during spring 2018, with the notification of six infected trav-
elers from five European countries, two of which had a fatal outcome [5]. Recent laboratory
experiments suggest that European populations of Aedes albopictus may be competent for
transmission of YFV [6], and therefore large areas highly infested by this species in Mediterra-
nean countries are potentially exposed to the risk of outbreaks [7].
Here, we provide a quantitative assessment of the risk of YFV transmission in Lazio, the
central Italian region where the metropolitan city of Rome is located and where the largest
arboviral outbreak in continental Europe occurred in summer 2017 [8]. To do so, we adapted
a stochastic transmission model, previously developed to assess the transmission risk of chi-
kungunya virus (CHIKV) [9] in the same area, to account for relevant epidemiological dynam-
ics of YFV, using existing field data on A.albopictus abundance [10] and biting rate on
humans [11].
Study sites
The assessment of YFV transmission risk was carried out on 18 sampling sites placed along a
70 km transect representing a wide range of ecological landscapes, from low–human-popula-
tion density areas (coastal and rural sites) to highly urbanized areas (metropolitan city of
Rome). The site-specific vector abundances over time were characterized by calibrating a mos-
quito population model against observed mosquito captures [8], taking as input the average
daily temperature [12]. The average vector density between July and September was estimated
to range between 154 and 4,866 female mosquitoes/ha, whereas the human density within
sampling sites ranged from 5 to 267 inhabitants/ha. The selected sites covered a wide range of
the vector-to-host ratio (4 to 138 female mosquitoes per inhabitant; see S1 Fig).
PLOS Neglected Tropical Diseases | January 10, 2019 1 / 6
Citation: Manica M, Guzzetta G, Filipponi F,
Solimini A, Caputo B, della Torre A, et al. (2019)
Assessing the risk of autochthonous yellow fever
transmission in Lazio, central Italy. PLoS Negl Trop
Dis 13(1): e0006970.
Editor: Christopher M. Barker, University of
California, Davis, UNITED STATES
Published: January 10, 2019
Copyright: ©2019 Manica et al. This is an open
access article distributed under the terms of the
Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Funding: The authors received no specific funding
for this work.
Competing interests: The authors have declared
that no competing interests exist
Transmission dynamics
The stochastic transmission model previously developed for CHIKV [9] was adapted to model
YFV transmission. Briefly, the overall model includes a temperature-driven model providing
the abundance of A.albopictus and was calibrated to mosquito-capture data, coupled with a
disease-transmission model, and was informed with available estimates on epidemiological
parameters for YFV and was initialized with a single imported infection in a fully susceptible
population. At the end of a patient’s incubation period, we sampled the occurrence of clinical
symptoms from a binomial distribution. In baseline simulations, we assumed that only symp-
tomatic patients (including both mild and severe cases) are able to transmit the virus. Fatal
outcome was modeled as a binomial process at the end of the infectious period for symptom-
atic individuals, given that severe symptoms develop in a small fraction of patients only after
the end of the viremic period [13]. The outcome of the importation of a single infected case
was evaluated at different times between May 1st and November 15th. To account for both sto-
chastic effects and the uncertainty in epidemiological parameters, we evaluated model simula-
tions by repeatedly sampling parameters from known distributions. The total number of
simulations for each study site was set to 30,000 (i.e., about 1,000 per week of importation).
Full details on the model’s structure are described in the S1 File.
We estimated the basic reproduction numbers over time, the probability of occurrence of
an outbreak, and the expected number of yellow fever (YF) cases and fatalities, under the
assumption of no disease control (either by vaccination or by vector management
The basic reproduction number R
represents the average number of secondary cases trans-
mitted by a typical infector during the entire period of infectivity; a value larger than 1 implies
potential for a sustained epidemic in the population. R
was computed for different times of
importation from standard equations [14,15], after adjusting to consider only symptomatic
cases (see S2 File). R
never exceeded the epidemic threshold in urban sites. However, some
coastal and rural sites had an average value of R
of about 2.1 at the peak, with an epidemic sea-
son (i.e., the time span over which R
exceeds 1) that extended from mid-July to the end of
Depending on the site, the average probability of autochthonous symptomatic YF cases
throughout the study period ranged between 1.0% and 11.8% (Fig 1); large outbreaks, here
defined as those involving more than 50 symptomatic cases, were unlikely (less than 0.65% in
all sites). The risk of YFV autochthonous transmission was uneven during the mosquito breed-
ing season but remained relatively stable between mid-July and mid-September in all sites.
However, the probability of occurrence of a large outbreak was higher for importations occur-
ring in mid-July, due to the broader time window during which transmission was possible.
Coastal and rural sites, characterized by high vector-to-host ratios, had a higher probability of
autochthonous transmission (up to 33.1%) and large outbreaks (up to 9.0%) compared to met-
ropolitan sites (maximum probability of autochthonous transmission: 25.9%; maximum prob-
ability of large outbreaks: 4.0%). The average probability of observing at least one death ranged
between 7.1% and 12.3% and that of observing more than 10 deaths was below 0.5% for all
sites; however, peak probabilities of observing at least one death reached 27.6% for importa-
tions occurring in mid-July in coastal and rural sites (see S2 Fig).
Given the observed importation of YFV in Europe via infected travelers [5] and the laboratory
competence of European A.albopictus populations to transmit this virus [6], we quantified the
risk of YFV transmission for Lazio, Italy, a region that was affected by a CHIKV outbreak
PLOS Neglected Tropical Diseases | January 10, 2019 2 / 6
during the summer of 2017 [9]. We showed that, given one imported case in urban areas, the
risk of transmission is generally low and limited to sporadic cases. However, for some coastal
and rural sites there is a nonnegligible potential for large outbreaks, especially if importation
Fig 1. Autochthonous symptomatic YF cases. Probability of autochthonous symptomatic YF cases estimated by the model in 18 sites in Lazio region (Italy),
conditional to the introduction of a single imported case at different times of the year and disaggregated by number of secondary cases. Font colors for site
IDs represent the geographic classification of the site. Blue: coastal, red: urban, green: rural. YF, yellow fever.
PLOS Neglected Tropical Diseases | January 10, 2019 3 / 6
occurs during the second half of July. In practice, given the severity of disease caused by YFV,
it is likely that ongoing local transmission will be promptly identified and limited by integrated
control measures (not included in our model); nonetheless, this result confirms the impor-
tance of early outbreak detection capacity [16]. As previously shown for CHIKV [9], the higher
risk in coastal and rural sites is related to lower human population densities, which tend to
increase the vector-to-host ratio. One of the rural sites with highest estimated YFV transmis-
sion risk is Fiumicino, where the largest Italian international airport is located. This increases
the chance of presence of potentially infected travelers compared to other rural areas. It is rele-
vant to note that our estimates of vector abundance and vector mortality rates are based on
temperatures recorded during 2017. In addition, a precise quantification of risks is subject to
many uncertainties on epidemiological parameters of YFV transmission in European A.albo-
pictus mosquitoes. These uncertainties include, but are not limited to, their dependence on
temperature, potential variability across different strains of the virus, and deviations between
laboratory measures and actual conditions in the field.
Another open question concerns the potential infectiousness of asymptomatic cases, which
is difficult to prove as they are mostly identified a posteriori using serological investigations.
Relaxing the assumption that asymptomatic individuals do not transmit and assuming in the
extreme opposite case that they transmit at the same rate as symptomatic patients, the esti-
mated risks would be much higher. For example, the peak probability of local transmission
would exceed 60% in some metropolitan sites and 80% in coastal and rural ones.
Recent estimates suggest that two YF cases were imported in Italy in 2017 [3]; the number
of imported cases for 2018 might be slightly larger due to a higher incidence of infection in
Brazil in 2018 (by about 50%) [2]. Imported cases are more likely to arrive during the Brazilian
summer, which corresponds to the European winter, when mosquito populations are not
active, and in crowded urban areas with lower vector-to-host ratios. This largely reduces the
likelihood of an importation in Italy at a time and site of favorable conditions for transmission.
Nonetheless, YF cases were confirmed in Brazil throughout June through September 2017, so
the possibility of importation during the European summer is not to be completely discarded.
Furthermore, many other areas of the world are at risk of YFV outbreaks because of their
international connectivity and insufficient vaccination coverage [4]: the possible expansion of
YFV to countries with year-round (rather than seasonal) transmission might significantly
increase the chances of importation in Europe during the summer in the near future.
Finally, we note that the estimated risk of locally transmitted symptomatic cases of YFV in
the considered study area is in the same order of magnitude of dengue (see S3 File). Although
introductions of dengue virus (DENV) are currently much more frequent (and indeed local
transmission of DENV has repeatedly been detected in France and Croatia [17]), the higher
severity of YF and the intrinsic stochasticity by which cases arrive over time and space suggest
that the risk of local YFV transmission should not be neglected.
Overall, the present work reveals a low, but nonnegligible risk of YFV transmission in Euro-
pean areas characterized by substantial A.albopictus infestation and medium-to-low human
density. Considering the severity of YF, this result highlights the need for public health author-
ities to ensure early diagnosis (not trivial since YF has not been reported in Italy since the 19th
century [18]), prompt notification of infected cases and swift responses targeting mosquito
populations through vector control interventions and the human population via reactive vacci-
nation campaigns. The recent unexpected rise of YF has caused a worldwide shortage in vac-
cine stockpiles, which has led to the adoption of fractional dosing immunization during the
PLOS Neglected Tropical Diseases | January 10, 2019 4 / 6
recent Brazilian outbreaks [19]. Although this approach seems to have been effective in con-
trolling the epidemics locally, many questions remain open [19]. More generally, the availabil-
ity of YFV vaccine stockpiles at the global scale may be an important challenge to outbreak
control in the future. For these reasons, public health authorities might consider preventive
general-purpose risk reduction measures such as larviciding, given their demonstrated cost-
effectiveness in simultaneously preventing outbreaks of different arboviruses, even in areas
with limited risks [20].
Supporting information
S1 Fig. Map of the study sites. Location of the 18 sites for which mosquito abundance esti-
mates were available. The study sites are located along a 70 km transect encompassing the met-
ropolitan city of Rome, Lazio region, Italy. Four sticky traps were placed within each site and
weekly mosquito collection lasted from July to November 2012 [9]. The area of circles repre-
sents the estimated peak vector-to-host ratio of each site, averaged across the period July
through September. Dark grey areas indicate human density higher than 10 inhabitants/ha.
Base layers elaborated from ISTAT data ( Spatial data processing and map
layout generation were done using QGIS ( ISTAT, Istituto Nazionbale
di Statistica; QGIS, Quantum Geographic Information System.
S2 Fig. YF fatal cases. Probability of fatal outcome due to autochthonous YF transmission
estimated by the model in 18 sites in Lazio region (Italy), conditional to the introduction of a
single imported case at different times of the year and disaggregated by the number of expected
deaths. YF, yellow fever.
S1 File. YF model description. YF, yellow fever.
S2 File. YF basic reproductive number (R
). YF, yellow fever.
S3 File. Results for dengue transmission.
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... Furthermore, there are no data on the dynamics of arbovirus dispersal in areas where the main mosquito vector is Aedes albopictus, a more exophilic species compared to A. aegypti and characterized by longer flight ranges [9,10]. The widespread and abundant presence of A. albopictus in temperate, non-endemic areas of Europe, the USA, northern China, the Korean Peninsula, and southern Australia [11] has created conditions for transmission of arboviral tropical diseases such as dengue [12], chikungunya [13,14], and potentially Zika [15] and yellow fever [16]. The expected expansion of its habitat [17] in the future will put an even larger territory at risk of sustained arboviral transmission. ...
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Background: The spatial spread of many mosquito-borne diseases occurs by focal spread at the scale of a few hundred meters and over longer distances due to human mobility. The relative contributions of different spatial scales for transmission of chikungunya virus require definition to improve outbreak vector control recommendations. Methods: We analyzed data from a large chikungunya outbreak mediated by the mosquito Aedes albopictus in the Lazio region, Italy, consisting of 414 reported human cases between June and November 2017. Using dates of symptom onset, geographic coordinates of residence, and information from epidemiological questionnaires, we reconstructed transmission chains related to that outbreak. Results: Focal spread (within 1 km) accounted for 54.9% of all cases, 15.8% were transmitted at a local scale (1-15 km) and the remaining 29.3% were exported from the main areas of chikungunya circulation in Lazio to longer distances such as Rome and other geographical areas. Seventy percent of focal infections (corresponding to 38% of the total 414 cases) were transmitted within a distance of 200 m (the buffer distance adopted by the national guidelines for insecticide spraying). Two main epidemic clusters were identified, with a radius expanding at a rate of 300-600 m per month. The majority of exported cases resulted in either sporadic or no further transmission in the region. Conclusions: Evidence suggest that human mobility contributes to seeding a relevant number of secondary cases and new foci of transmission over several kilometers. Reactive vector control based on current guidelines might allow a significant number of secondary clusters in untreated areas, especially if the outbreak is not detected early. Existing policies and guidelines for control during outbreaks should recommend the prioritization of preventive measures in neighboring territories with known mobility flows to the main areas of transmission.
... In non-endemic countries like Italy, the spread of arboviruses is facilitated by the flux of travelers that included sick individuals (i.e., viremic) arriving from endemic areas, increasing the risk of local outbreaks of dengue, chikungunya and yellow fever [4][5][6]. Predictive models [6] and surveillance data suggest that the majority of imported cases involve Italian residents travelling in tropical areas for holidays or business or members from long established communities of migrants returning to Italy after visiting friends and relatives in their home country, as it was with the case of the chikungunya outbreak in 2007 [7]. One of the key factors in preventing the expansion of local outbreaks obviously includes the public health system preparedness to act and respond once early cases have been clinically discovered [8]. ...
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Background Aedes albopictus is an aggressive invasive mosquito species that represents a serious health concern not only in tropical areas, but also in temperate regions due to its role as vector of arboviruses. Estimates of mosquito biting rates are essential to account for vector-human contact in models aimed to predict the risk of arbovirus autochthonous transmission and outbreaks, as well as nuisance thresholds useful for correct planning of mosquito control interventions. Methods targeting daytime and outdoor biting Ae. albopictus females (e.g., Human Landing Collection, HLC) are expensive and difficult to implement in large scale schemes. Instead, egg-collections by ovitraps are the most widely used routine approach for large-scale monitoring of the species. The aim of this work was to assess whether ovitrap data can be exploited to estimate numbers of adult biting Ae. albopictus females and whether the resulting relationship could be used to build risk models helpful for decision-makers in charge of planning of mosquito-control activities in infested areas. Method Ovitrap collections and HLCs were carried out in hot-spots of Ae. albopictus abundance in Rome (Italy) along a whole reproductive season. The relationship between the two sets of data was assessed by generalized least square analysis, taking into account meteorological parameters. Result The mean number of mosquito females/person collected by HLC in 15′ (i.e., females/HLC) and the mean number of eggs/day were 18.9 ± 0.7 and 39.0 ± 2.0, respectively. The regression models found a significant positive relationship between the two sets of data and estimated an increase of one biting female/person every five additional eggs found in ovitraps. Both observed and fitted values indicated presence of adults in the absence of eggs in ovitraps. Notably, wide confidence intervals of estimates of biting females based on eggs were observed. The patterns of exotic arbovirus outbreak probability obtained by introducing these estimates in risk models were similar to those based on females/HLC (R0 > 1 in 86% and 40% of sampling dates for Chikungunya and Zika, respectively; R0 < 1 along the entire season for Dengue). Moreover, the model predicted that in this case-study scenario an R0 > 1 for Chikungunya is also to be expected when few/no eggs/day are collected by ovitraps. Discussion This work provides the first evidence of the possibility to predict mean number of adult biting Ae. albopictus females based on mean number of eggs and to compute the threshold of eggs/ovitrap associated to epidemiological risk of arbovirus transmission in the study area. Overall, however, the large confidence intervals in the model predictions represent a caveat regarding the reliability of monitoring schemes based exclusively on ovitrap collections to estimate numbers of biting females and plan control interventions.
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We assessed the ability of a French population of Aedes albopictus to transmit yellow fever virus (YFV). Batches of 30 to 40 female mosquitoes were analysed at 7, 14 and 21 days post-exposure (dpe). Bodies, heads and saliva were screened for YFV. Infectious viral particles were detected in bodies and heads at 7, 14 and 21 dpe whereas the virus was found in saliva only from 14 dpe. Our results showed that Ae. albopictus can potentially transmit YFV. © 2016, European Centre for Disease Prevention and Control (ECDC). All rights reserved.
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Aedes albopictus is a tropical invasive species which in the last decades spread worldwide, also colonizing temperate regions of Europe and US, where it has become a public health concern due to its ability to transmit exotic arboviruses, as well as severe nuisance problems due to its aggressive daytime outdoor biting behaviour. While several studies have been carried out in order to predict the potential limits of the species expansions based on eco-climatic parameters, few studies have so far focused on the specific effects of these variables in shaping its micro-geographic abundance and dynamics. The present study investigated eco-climatic factors affecting Ae. albopictus abundance and dynamics in metropolitan and sub-urban/rural sites in Rome (Italy), which was colonized in 1997 and is nowadays one of the most infested metropolitan areas in Southern Europe. To this aim, longitudinal adult monitoring was carried out along a 70 km-transect across and beyond the most urbanized and densely populated metropolitan area. Two fine scale spatiotemporal datasets (one with reference to a 20m circular buffer around sticky traps used to collect mosquitoes and the second to a 300m circular buffer within each sampling site) were exploited to analyze the effect of climatic and socio-environmental variables on Ae. albopictus abundance and dynamics along the transect. Results showed an association between highly anthropized habitats and high adult abundance both in metropolitan and sub-urban/rural areas, with “small green islands” corresponding to hot spots of abundance in the metropolitan areas only, and a bimodal seasonal dynamics with a second peak of abundance in autumn, due to heavy rains occurring in the preceding weeks in association with permissive temperatures. The results provide useful indications to prioritize public mosquito control measures in temperate urban areas where nuisance, human-mosquito contact and risk of local arbovirus transmission are likely higher, and highlight potential public health risks also after the summer months typically associated with high mosquito densities