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1www.eurosurveillance.org
S
Surveillance of Zika virus infection in the EU/EEA, June
2015 to January 2017
G Spiteri¹, B Sudre¹, A Septfons2,3, J Beauté¹, on behalf of the European Zika surveillance Network
1. European Centre for Disease Prevention and Control (ECDC), Stockholm, Sweden
2. Santé publique France, Paris, France
3. European Programme for Intervention Epidemiology Training (EPIET), European Centre for Disease Prevention and Control
(ECDC), Stockholm, Sweden
4. The members of the European Zika surveillance Network are listed at the end of the article
Correspondence: Gianfranci Spiteri (gianfranco.spiteri@ecdc.europa.eu)
Citation style for this article:
Spiteri G , Sudre B, Septfons A, Beauté J, on behalf of the Eur opean Zika sur veillance Network. Surveill ance of Zika virus infection in the EU/EE A, June 2015 to
January 2017. Euro Surveill. 2017;22(41):pii=17-00254. https://doi.org/10.2807/1560-7917.ES.2017.22.41.17-00254
Article submit ted on 05 Apr 2017 / accepted on 16 Jun 2017 / published on 12 Oct 2017
Surveillance of Zika virus (ZIKV) infection in the
European Union/European Economic Area (EU/EEA) was
implemented in 2016 in response to the large outbreak
reported in the Americas in 2015 associated with an
increased number of infants born with microcephaly.
Between June 2015 and January 2017, 21 EU/EEA coun-
tries reported 2,133 confirmed cases of ZIKV infection,
of whom 106 were pregnant women. Cases infected
in the Caribbean constituted 71% of reported cases.
Almost all cases (99%) were most probably infected
by mosquito bite during travel outside continen-
tal Europe, while only 1% were transmitted sexually.
Considering that 584 imported cases were reported
between May and October 2016 among residents of
areas with established presence of Aedes albopictus,
the absence of autochthonous vector-borne cases sug-
gests that Ae. albopictusis not an efficient vector for
ZIKV infection.
Introduction
Zika virus (ZIKV ) was first identified in humans in the
1950s. The first large outbreaks, however, were not
reported until 2007 from the Island of Yap (Micronesia)
in 2007 [1] and from French Polynesia in 2013–14 [2].
In 2015, an outbreak of unprecedented magnitude was
reported in the Americas temporally associated with
an increased number of infants born with microcephaly
[3]. On 1 February 2016, the World Health Organization
(WHO) declared that “the recent cluster of microceph-
aly cases and other neurological disorders reported in
Brazil, following a similar cluster in French Polynesia
in 2014, constitutes a Public Health Emergency of
International Concern” and encouraged the investiga-
tion of an association with ZIKV which at the time had
not been confirmed [4].
In March 2016, the European Union (EU) Health Security
Committee approved an interim case definition for sur-
veillance of ZIKV infection [5] and the European Centre
for Disease Prevention and Control (ECDC) proceeded to
develop surveillance at the level of the European Union/
European Economic Area (EU/EEA). The objectives were
the early detection of locally acquired cases and timely
reporting of travel-associated cases, particularly those
residing in areas in the EU/EEA where Aedes albopic-
tusorAe. aegypti are established (receptive areas), to
trigger appropriate control measures. We here report
the results of ZIK V infection surveillance among EU/
EEA residents in the period from 2015 to 2017. SinceAe.
aegypti is only established on Madeira in the EU/EEA,
it was not considered for this analysis.
Methods
Epidemiological surveillance of ZIKV infection in the
EU/EEA was implemented in 2016 and is carried out by
nominated representatives from EU/EEA countries, the
European Zika surveillance network, under the coordi-
nation of ECDC. ECDC has published interim guidance
outlining the investigation and testing of suspected
cases [6], however, some countries have implemented
their own criteria for testing and reporting over time.
Surveillance is based on weekly reporting to ECDC of
case-based or aggregated data on confirmed cases.
The option of repor ting aggregated data aims to
reduce the reporting burden on the countries, par-
ticularly in case of large local outbreaks in Europe.
Confirmed cases are defined based on (i) detection of
ZIKV nucleic acid, detection of ZIKV antigen or isola-
tion of ZIKV from a clinical specimen, (ii) detection of
ZIKV-specific IgM antibodies in a serum sample and
confirmation by neutralisation test or (iii) seroconver-
sion or fourfold increase in the titre of ZIK V-specific
antibodies in paired serum samples [5]. Case-based
data include information on age, sex, date of onset,
date of notification, importation status, probable place
of infection, place of residence, place of notification,
pregnancy status and probable mode of transmission.
Aggregated data include the number of cases per week
by pregnancy status and residence in receptive or non-
receptive areas for imported cases and the number of
2www.eurosurveillance.org
cases per week by probable place of infection, preg-
nancy status and mode of transmission for locally
acquired cases. Cases are reported only if diagnosed
in continental Europe (which we also take to include
Cyprus, Iceland, Ireland, Malta and the United Kingdom
(UK)) or in selected outermost regions (Azores, Canary
Islands, Madeira) [7] of the European Union. Data col-
lection star ted in June 2016 and is ongoing, but EU/EEA
countries also reported retrospectively cases of ZIK V
infection that had occurred from 2015 onwards.
For the present analysis, we extracted data from the
ZIKV sur veillance database on 14 March 2017. The anal-
ysis included description of repor ted cases over time,
by importation status, age, sex and pregnancy. Areas
where Ae. albopictus was established were defined
based on data published by the VectorNet project, a
joint initiative of the European Food Safety Authority
and ECDC that supports the collection of data on
F 1
Number of cases of Zika virus infection by place of residence (NUTS2) and established presence of Aedes albopictus as at 14
March 2017, 21 EU/EEA countriesa, week 26/2015–week 5/2017 (n = 1,881)
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Cases reported at country level
Aedes albopictus known distribution
EU/EEA Member States
Other countries
100
Number of cases
10
1
EU/EEA: European Union/European Economic Area.
a Austria, Belgium, Czech Republic, Denmark, Finland, France, Greece, Hungary, Ireland, Italy, Luxembourg, Malta, the Netherlands, Norway,
Portugal, Romania, Slovakia, Slovenia, Spain, Sweden and the United Kingdom.
Cases reported from countries where Aedes albopictus is not established in the continental part of the country are displayed at country level.
3www.eurosurveillance.org
vectors and pathogens in vectors, related to both ani-
mal and human health [8].
The k-sample median test was used to compare
medians using STATA, version 14 (StataCorp, College
Station, United States (US)).
Results
Overview
Until 13 March 2017, 21 EU/EEA countries (total popu-
lation: 375 million) reported 2,133 confirmed cases of
ZIKV infection to ECDC, with reporting dates between
week 26, 2015 (the week starting on 29 June 2015)
and week 5, 2017 (the week ending on 5 February
2017). These included 2,090 imported cases, 21
locally acquired non-vector borne cases and 22 cases
with importation status reported as unknown. France
reported the largest number of cases (1,141 cases) fol-
lowed by Spain (306 cases), the UK (199 cases) and
Belgium (128 cases). Overall, of the 1,881 cases with
known region of residence, 815 (43%) lived in areas
whereAe. albopictuswas established (Figure 1).
Place of infection
The place of infection was reported for 1,819 (87%)
of the imported cases. The largest proportion was
reported to have been infected in the Caribbean (71%).
Infections were also acquired in South America (17%)
and Central America (11%), and much smaller pro-
portions in Asia, Africa, Oceania and North America
(all < 1%). The most frequently reported places of infec-
tion were Guadeloupe (489 cases), Martinique (421
cases) and the Dominican Republic (146 cases). Table
1 shows the 10 most common countries and overseas
territories from where cases were imported. The three
F 2
Number of cases of Zika virus infection by week of reporting and probable region of infection, 21 EU/EEA countriesa, week
48/2015–week 5/2017 (n = 1,811)
0
10
20
30
40
50
60
70
80
2015 2016 2017
Number of cases
Year and week number
Caribbean
Central America
South America
Rest of the world
Start of
data collection
WHO declaration of
Pubic Health Emergency
of International Concern
EU/EEA: European Union/European Economic Area.
a Austria, Belgium, Czech Republic, Denmark, Finland, France, Greece, Hungary, Ireland, Italy, Luxembourg, Malta, the Netherlands, Norway,
Portugal, Romania, Slovakia, Slovenia, Spain, Sweden and the United Kingdom.
Excludes eight cases where the destination was reported as ‘French overseas department’.
4www.eurosurveillance.org
highest ranked places of infection varied by reporting
country. Among the three European countries reporting
most cases, France reported most cases imported from
Guadeloupe, Martinique and French Guiana, Spain
from the Dominican Republic, Colombia and Venezuela
and the UK from Barbados, Jamaica and Saint Lucia
(data not shown).
Time of infection
The first imported case was reported in week 26,
2015. The weekly number of imported cases started to
increase during the last weeks of 2015, peaking during
week 33, 2016 when 85 imported cases were reported
in one week. Other intermediate peaks were obser ved
in weeks 6 and 23, 2016 (Figure 2). Cases then declined
rapidly from week 35, 2016 onwards, although there
was a slight increase in cases around week 45, 2016.
Cases repor ted as infected in the Caribbean peaked
during week 6 and weeks 21–36, 2016, cases infected
in South America between weeks 1 and 10, 2016, and
cases infected in Central America between weeks 33
and 35, 2016. The date of onset was reported for 1,608
cases (75%). The median lag between date of onset
and date of notification was one week and ranged
between 0 and 14 weeks.
Demographics
Of the 2,133 cases, 1,048 were female, 696 were male,
and for 389 (18%) sex was not repor ted (Table 2).
Among those for whom sex was reported, 60% were
female. Among all female cases, pregnancy status
was reported for 92%; 106 ZIKV-infected women were
reported to be pregnant. Age was reported for 1,738
cases (81%). Of these, four were aged one month or
younger, while the largest proportion was 25–34 (29%)
and 35–44 years-old (23%). The median age was 38
years and did not vary by sex (p = 0.2, k-sample test).
Pregnant women were younger (median age: 31 years)
when compared with non-pregnant women (median
age: 39 years, p < 0.01, k-sample test). The overall male-
to-female ratio was 0.7; it was lowest among 15–24
year-olds (0.4).
Mode of transmission
Nearly 99% of cases with reported mode of transmis-
sion were infected by mosquito bite during travel out-
side continental Europe. Among the impor ted cases,
one case of mother-to-child transmission was reported
associated with maternal travel to Brazil. There were
no locally acquired vector-borne ZIKV infections among
reporting countries during the period under surveil-
lance. Sexual transmission was reported for 20 cases,
all locally acquired, from six countries (France: 12
cases, Italy: two cases, the Netherlands: two cases,
Portugal: one case, Spain: two cases and the UK: one
case). Of the 20 cases where sex was the repor ted
mode of transmission, 19 were women. Their ages
ranged from 17 to 63 years (median: 33 years). The
age and sex of one case were not reported. Three of
the women infected through sexual transmission were
pregnant. One locally acquired case of mother-to-child
transmission was repor ted from Spain.
Discussion
The demographic data of cases repor ted in this study
were very similar to those reported among US travel-
lers (60% women) [9]: considering the risk of severe
pregnancy outcomes [10], it is expected that women
of reproductive age, and particularly pregnant women,
are more frequently tested. In our study, approximately
16% of infected women of reproductive age were preg-
nant, which is suggestive of increased testing in preg-
nant women. Indeed, the male-to-female sex ratio for
persons of reproductive age (15–49 years) was 0.7.
Other possible reasons for this pattern could reflect
health-seeking behaviour among women, particularly
those of child-bearing age, differences in exposure
to mosquito bites and possibly sexual transmission,
which has been reported more often from men to
women than from women to men [11]. The proportion
of sexually transmitted cases was approximately 1%,
similar to what has been reported from the US, and
in line with suggestions of limited potential for sexual
transmission [12,13].
T 1
Most commonly reported destination countries and
overseas territories in imported cases of Zika virus
infection, 21 EU/EEA countries, week 26/2015 to week
5/2017 (n = 2,090)
Rank Destination country Number %
1Guadeloupe 489 26.9
2Martinique 421 23.1
3Dominican Republic 146 8.0
4Colombia 83 4.6
5Mexico 81 4.5
6Brazil 68 3.7
7Barbados 53 2.9
8Venezuela 52 2.9
9Nicaragua 51 2.8
10 Suriname 48 2.6
Other 327 18.0
Total documented 1,819 100
Not documented 271 NA
Total 2,090 NA
EU/EEA: European Union/European Economic Area. NA: not ap-
plicable.
Data as at 14 March 2017. Percentages are based on the cases with
documented destination. Excludes cases reported with unknown
importation status (Belgium: 19 cases, France: three cases), cases
with reported sexual transmission (20 cases) and one mother-
to-child transmission in the EU/EEA. The total number of cases
with documented destination includes eight cases where the
destination was reported as ‘French overseas department’.
5www.eurosurveillance.org
A study from France reported that around 30% of
imported cases were residents in areas where Ae.
albopictus was established during the vector activity
period [14]. Our data indicated an even higher propor-
tion (43%): in addition to France, all Greek, Italian,
Maltese and Slovenian travellers, and almost half of
the Spanish travellers (45%) resided in such areas.
The absence of local transmission despite the large
number of cases among travellers (many of whom may
have been viraemic) returning to these areas between
the beginning of May and the end of October (584
cases among returning travellers during that time
period) suggests thatAe. albopictusis probably not an
efficient vector for ZIK V, as reported in other studies
[15,16]. Nevertheless, surveillance should continue
asAe. albopictushas been implicated in the 2007 ZIKV
outbreak in Gabon [17] and possibly in Mexico [18].
European mosquito populations have shown some
competence for ZIKV particularly at higher tempera-
tures under laboratory conditions [19].
The trends in reported cases reflected the progres-
sion of the epidemic in the Americas, starting in South
America in early 2016 and then progressing to the
Caribbean and eventually to Central America in late
2016. Most cases were associated with travel to the
Caribbean which may be explained by the travel pat-
tern of European residents, the stage of the epidem-
ics at the time of major holiday periods and the higher
intensity of the epidemics in insular settings [20]. Using
a mathematical model developed for dengue importa-
tion, a study estimated between 116 and 355 sympto-
matic ZIKV infections imported to Europe by travellers
from Brazil in 2016 [21]. Our surveillance data covered
approximately 60% of the EU/EEA population, and 68
ZIKV infections with a probable origin in Brazil were
reported, which, when extrapolated to the whole EU/
EEA population, is consistent with the lower limits of
the prediction.
Interestingly, our data show that surveillance in the
EU/EEA was able to capture the cases returning from
Africa, Asia and Oceania. Surveillance of the cases
imported to the EU/EEA could therefore serve as an
indicator (although probably not a very sensitive one)
of emerging and ongoing transmission, particularly in
countries with limited testing capacity, and it could
contribute to the evidence base used for the WHO ZIKV
country classif ications.
European surveillance data may underestimate the
importation of ZIKV cases in Europe. It is likely that
most cases were tested after developing symptoms
and asymptomatic ZIK V cases, particularly in non-
pregnant women, are therefore likely to be under-rep-
resented. It is also likely that cases are underestimated
in areas and countries without established Ae. albop-
ictus populations as well as, in countries with
established populations, at times when Ae. albop-
ictus is not active. In addition, some groups may be
tested less frequently, e.g. travellers returning from
countries without documented transmission. Other
groups may be more likely to be tested, e.g. pregnant
women. Laboratory capacities vary across countries
and access to testing can therefore not be expected
to be uniform across Europe. Data on the diagnostic
method used for diagnosis were not available and we
can therefore not know what proportion of cases were
T 2
Main characteristics of the cases of Zika virus infection,
21 EU/EEA countriesa, week 26/2015–week 5/2017
(n = 2,133)
Characteristic Number %
Sex
Female 1,048 60.1
Male 696 39.9
Not documented 389
Age group (years)
0–4 13 0.8
5–14 51 2.9
15–24 138 7.9
25–34 499 28.7
35–44 401 23.1
45–54 282 16.2
55–64 236 13.6
≥ 65 118 6.8
Not documented 395
Region visited
Africa 40.2
Asia 15 0.8
Caribbean 1,278 70.6
Central America 205 11 .3
Oceania 3 0.2
North America 30.2
South America 303 16.7
No travel 21
Not documented 301
Mode of transmission
Mosquito 1,715 98.7
Mother-to-child 20.1
Sexual 20 1.2
Not documented 396
Pregnancy statusb
Pregnant 105 16.0
Not pregnant 551 84.0
Not documented 52
EU/EEA: European Union/European Economic Area; NA: not
applicable.
aAustria, Belgium, Czech Republic, Denmark, Finland, France,
Greece, Hungary, Ireland, Italy, Luxembourg, Malta, the
Netherlands, Nor way, Portugal, Romania, Slovakia, Slovenia,
Spain, Sweden and the United Kingdom.
bIncludes only female individuals aged 15–49 years (n = 708). In
addition, one pregnant woman was reported with unknown age.
Data as at 14 March 2017. Percentage is calculated over
documented values, and for region visited, among cases
travelling abroad.
6www.eurosurveillance.org
diagnosed through nucleic acid amplification testing,
isolation or serology. It is likely that most of the diag-
noses during the period under surveillance were made
through nucleic acid amplification testing; however,
the impact of serology and cross-reactions with other
circulating arboviruses such as dengue virus and chi-
kungunya virus cannot be to assessed. Finally, further
testing and validation of cases might mean that some
cases have been reclassified or excluded since the
extraction of the data on 14 March 2017.
Conclusion
ECDC rapidly implemented surveillance of ZIKV infec-
tion following the Health Security Committee deci-
sion, with two-thirds of EU/EEA countries reporting
their cases ever y week. These data were used to pro-
duce a ZIKV infection surveillance atlas, which was
updated each week. In addition, key results were dis-
cussed on a weekly basis at ECDC and presented in the
Communicable Disease Threat Repor t [22].
Prevention of ZIK V in Europe is challenging as the vast
majority of cases are imported and, apart from travel
health clinics, there are limited oppor tunities to provide
targeted prevention advice. Efforts need to be made to
strengthen travel health advice before peak travel peri-
ods, targeting particularly pregnant women and their
partners. Surveillance of ZIKV at the European level has
proven to be beneficial during a rapidly evolving global
public health emergency, with active participation of
the majority of EU/EEA countries. Fur ther development
of the system will aim to capture pregnancy outcome to
provide understanding of the impact of ZIKV in Europe.
The European ZIK V surveillance system could serve as
a model for future emerging infections.
Members of the European Zika surveillance Network
Stephan W. Aberle, Medical University of Vienna, Center for
Virology, Vienna, Austria. Marjan Van Esbroeck, National
Reference Center for Arboviruses, Antwerp, Belgium.
Helena Šebestová, National Institute of Public Health, Czech
Republic. Anders Koch, Statens Serum Institut, Copenhagen,
Denmark. Jussi Sane, Infectious Disease Control Unit,
Department of Health Security, National Institute for Health
and Welfare, Helsinki, Finland. Stella Laporal, Santé pub-
lique France, Paris, France. Danai Pervanidou, Hellenic
Center for Disease Control and Prevention, Athens, Greece.
Bognár Zsófia, National Center for Epidemiology, Budapest,
Hungary
Sarah Jackson, Health Protection Surveillance Centre,
Dublin, Ireland. Caterina Rizzo, Istituto Superiore di Sanità,
Rome, Italy. Tanya Melillo, Infectious Disease Prevention
and Control Unit, Msida, Malta. Janneke W. Duijster, National
Institute for Public Health and the Environment (RIVM),
Bilthoven, Netherlands. Bernardo R. Guzmán-Herrador,
Department of Infectious Disease Epidemiology, Norwegian
Institute of Public Health, Oslo, Norway. Marina Ramos,
Directorate-General of Health, Lisbon, Portugal. Ionel Iosif,
National Institute of Public Health, Bucharest, Romania.
Maja Sočan, National Institute of Public Health, Ljubljana,
Slovenia. Beatriz Fernandez-Martinez, Spanish National
Centre of Epidemiology, Madrid, Spain. Elsie Ydring, Public
Health Agency of Sweden, Stockholm, Sweden. Joanne
Freedman, Public Health England, London, United Kingdom.
Acknowledgements
We would like to thank all collaborators at the national, re-
gional and local level for reporting their cases. In addition
we would like to thank the following persons for their con-
tribution to Zika surveillance in Europe: Daniela Schmid,
Austrian Agency for Health and Food Safety, Austria; Hana
Zelena, Public Health Institute Ostrava, Czech Republic;
Etienne Lucas and Julien Durand, Santé publique France,
France; Kassiani Gkolfinopoulou, Annita Vakali, Theano
Georgakopoulou, and Agoritsa Baka, Hellenic Center for
Disease Control and Prevention, Anna Papa, National
Reference Centre for Arboviruses and Haemorrhagic Fever
viruses, Thessaloniki, Greece; Antonino Bella, Maria Grazia
Caporali, Giulietta Venturi, Claudia Fortuna, Antonello
Amendola, Eleonora Benedetti, Maria Elena Remoli,
Giovanni Rezza, Department of Infectious Diseases, Istituto
Superiore di Sanità, Rome Italy; Patrizia Parodi, Ministry of
Health, Rome, Italy; Maria Louise Borg, Infectious Disease
Prevention and Control Unit, Malta; Line Vold; Hans Blystad,
Tone Bruun, Dagny Haug Dorenberg, Norwegian Institute
of Public Health, Norway; Alina Daniela Zaharia, National
Institute of Public Health, Romania; Emma J Aarons, Public
Health England, United Kingdom.
We are also grateful to current and former ECDC colleagues:
Wim Van Bortel and Hervé Zeller for their contribution to the
development of the surveillance system, Valentina Lazdina
and Catalin Albu for data management support and Silviu
Lucian Ionescu for his support in GIS.
Conflict of interest
None declared.
Authors’ contributions
GS and JB led the development of the sur veillance system
and reporting protocols and analysed the data. GS wrote
the first draft of the manuscript. BS contributed to the de-
velopment of the surveillance system and production of the
manuscript. AS contributed to the development of the sur-
veillance system, provided data and contributed to the de-
velopment of the manuscript. Colleagues from the European
Zika Surveillance Network contributed to the development
of the surveillance system, collected and reported data and
provided scientific input to the manuscript.
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