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Introduction
Measles is one of the most infectious diseases known to man and remains
the leading cause of vaccine preventable deaths in children worldwide.
In many European countries measles is still a cause of great public
health concern (1-3). Despite the easy availability of vaccination for
its control, vaccination uptake has been sub-optimal in some countries
(4,5). However, following the successful interruption of indigenous
wild poliovirus transmission in the European Region, many countries
in the region are eager to move towards targeting measles elimination
and strengthening measles surveillance, and have started implementing
elimination strategies.
The commencement of measles surveillance in EUVAC.NET participating
countries heralded the network entering into its implementation phase
and an important step in the early stage of the measles elimination
programme (6). The following surveillance report covers the years 2001
and 2002 and aims to describe basic epidemiological features of measles
in EUVAC.NET participating countries. These include all 15 Member states
of the EU together with Iceland, Norway, Malta, and Switzerland.
Methods
The case definition used for identifying a case of measles follows the
WHO recommendations (7). Its application varies to some degree in the
various national surveillance systems depending on the stage of control
of indigenous measles (6). Data from participating countries were sent
electronically to EUVAC.NET as an Excel file. Analysis of data was carried
out using Microsoft Excel 2000. In this report, evaluation is based
on cases with disease onset dates in the corresponding years. Where
disease onset dates were not available or considered invalid, the date
of notification was used instead. In some countries minor discrepancies
with national data may arise if these include cases notified in 2001
and 2002 but with onset dates in a preceding year. Incidence rates were
based on population statistics obtained from the Population Information
page on the WHO website for the Computerized Information System for
Infectious Diseases (CISID), http://cisid.who.dk.
Epidemiological evaluation of data from sentinel surveillance systems
is included separately. All incidence rates are based on reported measles
cases and are per 105 population per year. With a few exceptions, total
numbers reported are likely to be incomplete. This report contains incidence
data that have to be interpreted cautiously because of under-reporting.
Results
Participation
For 2001, all 19 EUVAC.NET participating countries provided measles
surveillance data. Sixteen countries operating mandatory notification
systems for measles provided case-based data. In addition to data from
such notification systems, Germany and Switzerland also provided data
from sentinel surveillance systems.
In Germany, around 1 100 physicians, mostly paediatricians amounting
to 15% of all paediatricians in the country, participated in such a
system. The Swiss sentinel surveillance data involved the participation
of 3-4% of all primary care physicians. In Austria and France (4), sentinel
systems are the only surveillance systems in place for reporting measles
cases. The Austrian system involved 226 physicians and covered 8% of
the population. In France, the sentinel surveillance system involved
300 general practitioners. Voluntary reporting took place in the French
community of Belgium that provided an annual figure for measles cases.
For 2002, 17 (89%) of the EUVAC.NET countries provided data, 16 of which
contributed case-based data obtained through mandatory notification
systems. Switzerland also provided data based on a sentinel surveillance
system that involved the same proportion of physician participation
as in 2001. As in 2001, the French data provided was derived from the
sentinel surveillance system. It involved the participation of 472 general
practitioners.
Incidence - notifications and laboratory data
For 2001 and 2002, EUVAC.NET gatekeepers reported a total of 7 428 and
10 500 measles cases giving a crude incidence of 2.36 and 3.37 per 100
000 population respectively (Table 1). Confirmed cases, either by laboratory
methods or those epidemiologically confirmed constituted 44% and 27%
of the total cases for the corresponding years. Of these, 30% and 44%
were laboratory-confirmed for the successive years.

The distribution of notified measles cases varied considerably among
the participating countries. In Figure 1, reporting countries have been
grouped into low, moderate and high incidences for notified cases in
2001 and 2002. In 2001, no cases were reported from Iceland. The highest
incidence of measles notifications was reported from Germany. In 2002,
no cases were reported from Finland, Iceland and Luxembourg while the
highest incidence of measles notifications was reported from Italy.
Outbreaks and imported cases
For 2001 and 2002, 18% and 20% of reported cases respectively were outbreak-related,
i.e. occurred in outbreak situations where localised increases in the
incidence of measles were identified (7). Most were reported from Germany
(1) (95% in 2001 and 83% in 2002). No link to an outbreak could be made
in 17% of cases in 2001 and 51% in 2002. No data from Italy were available
on outbreak related cases through the mandatory notification system.
Nevertheless, a paediatric sentinel surveillance system has monitored
a large outbreak which took place mostly during the first half of 2002
(2,3).
A known link to an imported case was reported in 70% and 86% of cases
in 2001 and 2002 respectively. Of these, there were 37 and 84 imported
cases for the consecutive years amounting to 0.7% and 0.9% of all cases
with known link to an imported case respectively. The rest were cases
believed to have been infected within their own country. In 2001, eight
cases (22%) were imported from another European country namely Belgium,
France, Germany, Spain and the United Kingdom (UK). Fifty-one percent
of the imported cases were from Asia. In 2002, there were 52 (62%) imported
cases from within Europe followed by Asia with 20 (24%) cases. Italy
was implicated as the source of infection in 40% of all importations
within Europe followed by Austria (8%) and Germany (6%).
Age distribution and seasonality
In 2001 and 2002, measles was reported in both children and adults with
the 1-9 year age group (Figure 2) accounting for 52% and 65% of the
cases respectively. The proportion of laboratory confirmed cases generally
increased with increasing age group (Figure 2). The majority of cases
were reported in the first half of the year (75% in 2001 and 90% in
2002) (Figure 3).


Vaccination status
Information on vaccination status was provided in 56% and 72% of the
total measles cases in 2001 and 2002 respectively. In 2001, half of
the reported measles cases occurred in unvaccinated children (table
2). This proportion increased to 66% in 2002.

Morbidity and mortality
Data on known hospitalisation status increased from 69% in 2001 to 89%
in 2002. In 2001, there were 278 cases that were hospitalised in connection
with measles representing 5% of all cases with known hospitalisation
status. Most cases were reported from Germany (44%) and Italy (40%).
In 2002, hospitalised cases amounted to 822 representing 9% of all cases
with known hospitalisation status. Of these, 83% were reported from
Italy.
In 2001, encephalitis as a severe complication of measles was reported
in 21 cases giving an incidence of 283 per 100 000 measles cases. All
were reported from Germany. Most cases (71%) were in the 1-9 year age
group, four cases were in older age groups and in one case the age was
unknown. Twelve cases were unvaccinated, three cases had a history of
vaccination and in the remaining six cases the vaccination status was
unknown. One death directly attributed to measles in an 8-month-old
male was also reported from Germany.
Encephalitis was reported in six cases in 2002 giving an incidence of
57 per 100 000 measles cases. Five cases were reported from Germany
and one from Switzerland. They were aged 8, 12, 16, 19, 24, and 39 years.
Three cases were unvaccinated and in the other three the vaccination
status was unknown. A case of subacute sclerosing panencephalitis in
a six-year-old male was identified in Norway in 2002. The child is believed
to have suffered from measles in his country of origin before being
adopted in Norway. This case was not included as a measles case in the
EUVAC.NET database. There were no deaths reported in 2002. However,
in the UK, measles may have been a contributory factor in the death
of an adult with severe lung disease who was also confirmed as having
the infection (8).
Data from Sentinel Surveillance Systems
For 2001, Austria reported 13 cases giving an extrapolated crude incidence
of 2.0 per 100 000 population. Germany reported 878 cases with an extrapolated
crude incidence rate of about 14 per 100 000 population. Both France
and Switzerland reported 22 cases each, extrapolated to 8 460 and 700
cases respectively. Based on these figures the estimated crude incidence
rates are 12 per 100 000 population for France (4) and 9.77 per 100
000 for Switzerland. For 2002, the Swiss sentinel system reported an
extrapolated 500 cases and a crude incidence rate of 7 per 100 000 population.
The French sentinel system reported 12 cases giving an extrapolated
5 190 cases and an incidence of 8 per 100 000 population. The above
estimates were based on population figures obtained by national surveillance
centres.
Discussion
Most participating countries have provided case-based measles data derived
from routine notification systems. Whilst in the greater part of participating
countries notification is statutory (9) and universal case reporting
is widely used for surveillance, under-reporting is common and must
be taken into account when interpreting data. Some participating countries
have sentinel surveillance systems in place. Where the incidence of
disease is relatively high, such systems may even be more accurate than
a deficient universal notification system. However, as the disease incidence
declines, estimates using sentinel surveillance systems become less
valid and therefore less suitable for surveillance purposes in the elimination
phase.
The findings in this report document a widely varied incidence rate
for measles in the different EUVAC.NET participating countries. While
some countries have reported incidence rates of less than 0.1 per 100
000 population per year, indicating a near-elimination situation, the
disease is still endemic in other countries. Compared to 2001, there
was a 41% increase in the case-based reported measles cases in 2002.
While reports of measles cases from Germany dropped by 23%, cases reported
from Italy increased six fold, greatly contributing to the increase
in the total number of cases.
Although no relationship with vaccination coverage for measles is attempted
in this report, it is assumed that differences in incidences are due
to varying degrees of success in vaccination programmes. Overall, 66%
of those reported with measles in 2002 were unvaccinated compared with
50% in the previous year. Paradoxically, a large proportion of measles
occurring in unvaccinated children was reported from countries known
to have moderate-to-high vaccination coverage such as Denmark (10),
Norway (11), and The Netherlands (12). This is due to an accumulated
cohort of susceptible individuals to the disease (ie no history of measles
or vaccination) over time following the introduction of MMR vaccination
in the national vaccination programme. This is known to occur during
the so called 'honeymoon period'; the name given when the very low incidence
currently suggests that a disease is disappearing, yet without any sign,
groups of unprotected individuals are forming the source of possible
future outbreaks. This becomes particularly relevant when pockets of
unvaccinated individuals accumulate.
Many participating countries are regularly reporting data to EUVAC.NET
and the quality of data on the status of importation, vaccination and
hospitalisation has improved in 2002. However, others still need to
have regular reporting and improvement of data quality in place. The
importance of strengthening surveillance systems by vigorous case investigation
forms part of the strategy to interrupt the indigenous transmission
of measles within Europe. Apart from the collection of additional data
on measles cases reported under routine surveillance, enhanced surveillance
also requires timely national case-based reporting on at least a monthly
basis. In addition, as vaccination coverage increases and measles reaches
a near-elimination phase in Europe, it becomes increasingly important
to investigate suspected cases. Hence, rapid laboratory confirmation
is an essential tool of enhanced surveillance. Such high quality surveillance
is crucial to monitor trends, identify the target population for vaccination
programmes and determine whether coverage objectives are being reached.
EUVAC.NET is committed to facilitate the improvement of measles surveillance
and together with its future plans to collect data on vaccination coverage
it will be contributing to the elimination of measles within the region
by 2010.
Remerciements / Acknowledgements
Nous remercions tous les correspondants nationaux de EUVAC.NET qui ont
contribué à la collecte des données de ce réseau
de surveillance. / We would like to thank all EUVAC.NET gatekeepers
and reporters who have contributed data to this surveillance network:
Reinhild Strauss, Federal Ministry for Health and Women, Austria; Tinne
Lernout, Scientific Institute of Public Health, Belgium; Irja Davidkin,
National Public Health Institute, Finland; Isabel Bonmarin, Institut
de la Veille Sanitaire, France; Anette Siedler, Robert Koch-Institut,
Germany; Takis Panagiotopoulos, National Centre for Surveillance and
Intervention, Greece; Gudrún Sigmundsdóttir, Directorate
of Health, Iceland; Darina O'Flanagan, Margaret Fitzgerald and Sarah
Gee, National Disease Surveillance Centre, Ireland; Loredana Vellucci,
Ministry of Health, Italy; Pierrette Huberty-Krau, Direction de la Santé,
Luxembourg; Andrew Amato Gauci and Jackie Maistre Melillo, Health Division,
Malta; Susan van den Hof and Hester de Melker, National Institute of
Public Health and the Environment (RIVM), The Netherlands; Øistein
Løvoll, National Institute of Public Health, Norway; Maria Da
Graça Gregório de Freitas and Helena Alves Pereira, National
Institute of Health, Portugal; Carmen Amela, Instituto de Salud Carlos
III, Spain; Hans Blystad, Swedish Institute for Infectious Disease Control,
Sweden; Jean-Luc Richard, Swiss Federal Office of Public Health, Switzerland;
Joanne White, Health Protection Agency, Communicable Disease Surveillance
Centre, UK.
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