Introduction
In 1987, a European surveillance scheme for travel-associated legionnaire's
disease (now called EWGLINET) was established by the European Working
Group for Legionella Infections (EWGLI). The aims of this scheme are to
monitor levels of travel associated legionnaires' disease in Europe, detect
clusters and outbreaks, and collaborate in the control and prevention
of further cases. Its history and current activities are described in
detail on its website (www.ewgli.org).
This paper provides results and commentary on cases reported to EWGLINET
with onset in 2002.
Methods
A single case of travel associated legionnaires' disease is defined
as a person who, in the ten days before onset of illness, stayed at
or visited an accommodation site that had not been associated with any
other cases of legionnaires' disease, or a person who stayed at an accommodation
site linked to other cases of legionnaires' disease but after an interval
of at least two years1.
A cluster of travel associated legionnaires' disease is defined as
two or more cases who stayed at or visited the same accommodation site
in the ten days before onset of illness and whose onset is within the
same two-year period1.
Cases of legionnaires' disease are detected and followed-up by national
surveillance schemes, and those defined as travel-associated are reported
to the EWGLINET coordinating centre at the Communicable Disease Surveillance
Centre (CDSC) in London and are entered into the EWGLINET database.
Epidemiological, microbiological and travel histories are reported.
Upon receipt of a new case, the database is searched by the coordinating
centre for any previous cases reported to have stayed at the same accommodation
site within the last two years.
In July 2002, European guidelines were introduced to standardise the
response that countries made to EWGLINET notifications1. Different levels
of intervention are expected from the public health authorities for
sites associated with single or multiple cases. These include issuing
a checklist for minimizing risk of legionella infection at sites associated
with single cases, and conducting risk assessments, sampling for legionella
and implementing control measures at sites associated with clusters.
The guidelines have introduced a procedure whereby the country of infection
is expected to carry out a risk assessment and initial control measures
within two weeks, and sampling and full control measures within six
weeks of receipt of the notification. Both of these stages are documented
by the collaborator in the country of infection, by completion of standard
forms ('Form A' and 'Form B') which are sent to the EWGLINET coordinating
centre. If this documentation is not received in the specified time
period, EWGLINET publishes details of the cluster on its public website
(www.ewgli.org) since the coordinating centre cannot be confident that
the accommodation has adequate control measures in place. The notification
is removed once the relevant form(s) have been received confirming that
measures to minimise the risk of legionella at the site have been carried
out.
Results
Cases and Outcome
In 2002, 57 collaborators from 50 centres in 36 countries (Figure 1)
participated in EWGLINET. Twenty of these countries reported a total
of 676 cases of travel associated legionnaires' disease with onset in
2002.

Each year, cases reported to EWGLINET follow a distinctive age and
sex profile. In 2002, male cases continued to outnumber female cases
by nearly 2.5 to 1, and the peak age-group reported was 50-59 years
for both sexes. The age range for males was 13-89 years and for females
22-89 years.
As in previous years, the date of onset followed a seasonal pattern.
The number of cases increased from January through the year, with peaks
in July and September, before decreasing throughout the rest of the
year.
The proportion of 'known' outcomes (death or recovery as opposed to
'unknown' outcomes - still ill or unknown) has been decreasing steadily
since about 1995, due largely to an increase in the speed of reporting.
The number of reported deaths has remained similar in 2002 at 43 compared
with 41 in 2001, despite a large rise in the number of cases, lowering
the case fatality rate from 8.5% to 6.4%. The absolute number of recoveries
increased, but fell in percentage terms from 35.5% in 2001 to 29.7%
in 2002. The 'still ill' category remained virtually unchanged, but
the largest increase was in the 'unknown' category where absolute figures
rose from 128 to 232, and the percentage increased from 26.6% to 34.3%.
Microbiology
Use of the urinary antigen test continued to rise, with 80.5% of all
cases diagnosed by this method, compared with 78.6% in 2001. Use of
other diagnostic tests remained relatively constant. Culture of the
organism accounted for 7% of the diagnoses (the same as in 2001), serology
11.8%, and other methods 0.7%, (Figure 2). The main category of organism
detected was Legionella pneumophila serogroup 1 (68.3%). The remaining
cases were reported as 'L. pneumophila serogroup unknown' (12.7%), 'L.
pneumophila other serogroups' (2.1%), 'Legionella species unknown' (4.6%),
'Other species' (0.9%), and 'Unknown' (11.4%).

Travel
Travel associated cases are usually diagnosed after they return to their
country of residence. The main reporters of cases in 2002 were The Netherlands
(151), England and Wales (126), France (119) and Italy (68) (Figure
2).
Cases visited a total of 51 countries. The highest numbers of cases
were associated with travel to Italy (132), France (121), Spain (85)
or Turkey (83). The proportion of cases linked to clusters was similar
in three of the four main countries of infection at 25% in France and
Spain and 24% in Italy. Although Turkey had fewer associated cases,
71% of them were part of clusters (see below) (Figure 3). Sixty one
cases visited more than one European country, whilst only two visited
more than one country outside Europe. A further 63 cases (9.3%) were
associated with travel to countries outside the EWGLINET scheme, ten
of which were in travellers to the USA.

Clusters
Ninety four clusters were identified in 2002 compared with 72 in 2001.
These were defined as accommodation sites associated with a case in
2002, where one or more cases within the previous two-years had also
been associated with the same site. Most clusters involved only two
cases (60 clusters), but they ranged in size from 2-10 cases.
26 of the 94 clusters consisted of a single case reported by each of
two or more countries and would ordinarily not have been identified
without the establishment of the international database.
The clusters were located in 19 countries. Turkey had the most (27),
followed by Italy (17) and France (16). Eleven countries had just one
cluster each in 2002, three of which occurred in countries outside EWGLINET
(Dominican Republic, Russia and USA). Twelve clusters included cases
that had stayed at two or more cluster sites before onset of illness
compared with only four such incidents in 2001.
Most of the detected clusters with onset in 2002 occurred in summer,
peaking in September. A second smaller peak was also observed around
Easter time, however at least three clusters occurred every month in
2002. Over two thirds (68%) of the clusters included at least two cases
with onset within six months of each other. Sixteen clusters (17%) had
cases occurring between seven and 12 months of each other, and the remaining
14 clusters has cases occurring between 13 and 24 months of each other.
Investigations
Of the 94 clusters in 2002, 64 were notified between the introduction
of the guidelines and the end of December 2002, and involved 70 accommodation
sites. Sixty six of these sites fell within EWGLINET countries. Between
July and December 2002, 37 'Form B' reports were accepted as being completed
on time and stating that control measures were satisfactory, 17 sites
(26%) had been published on the EWGLI website, and 12 were in the process
of being investigated. Four of these published cluster sites (23.5%)
have had extra cases subsequently, and five unpublished sites (10.2%)
have also had subsequent cases.
For the whole of 2002, 128 cluster sites were investigated including
99 which were sampled, from which legionella was reported to have been
detected in 35 (35%). 146 single case sites were also investigated,
even though the guidelines do not require such sites to be investigated,
and of these 106 were sampled, and 45 (42.5%) of the sampled sites detected
legionella (Table 1).

Environmental investigations will be examined in greater detail in
a further paper.
Discussion
2002 saw the highest number of travel associated cases of legionnaires'
disease reported to EWGLINET since the scheme began in 1987. This rise
in case reports is almost certainly linked to wider use of the urinary
detection test and improved surveillance in many European countries.
The fall in the case fatality rate is also part of this general trend
whereby less seriously ill cases are being detected and reported more
regularly, and the risk of death is being considerably reduced through
more rapid diagnosis and application of appropriate antibiotic therapy,
made possible by the widespread introduction of the urinary antigen
detection test. Whilst rapid diagnosis has benefited cases, it has also
negatively impacted on epidemiological information in relation to the
outcome of cases reported as "still ill" or with unknown outcome,
and also on microbiological information because the lack of clinical
isolates prevents analysis of strain matches between patient and environmental
specimens. In order to demonstrate that a particular infection comes
from a particular site, the clinical sample must be matched with an
environmental sample, and culture is the only method by which this can
be done.
Eleven per cent of the cases reported to EWGLINET in 2002 did not have
data provided on the category of organism detected. This is not in accordance
with the reporting procedures since all cases reported to EWGLINET must
state the main method of diagnosis, and each microbiological diagnosis
should at the very least determine the organism (legionella) and species
(pneumophila). The urinary antigen detection method is highly specific
to L. pneumophila serogroup 1, and serological diagnostic methods are
capable of determining the species and serogroup of Legionella. Since
over 90% of the reported cases in 2002 were diagnosed by these methods,
the microbiological information should be available for a large majority
of the "unknown" cases. Any lack of information exchange between
laboratories and national collaborating centres should be addressed
to ensure that microbiological details are provided for all cases. This
is increasingly important as more and more accommodation sites are subject
to environmental investigations.
The main change to occur to the EWGLINET scheme in 2002 was the introduction,
on 1st July that year, of the European Guidelines for Control and Prevention
of Travel Associated Legionnaires' Disease1. These have now been successfully
implemented in the investigation of a large number of sites, including
a cluster involving ten cases who stayed at a hotel in Belgium.
There is some preference among holiday-makers for travel to particular
destinations, and this can influence which countries of infection are
most often reported to the scheme. This can have interesting effects
when the preference is country-specific. For instance, Turkey has a
market share of 24% of the total Dutch flight travel package market.
In the summer of 2002, approximately 600,000 Dutch package travellers
visited Turkey from a population base of 16 million. When this is combined
with the high frequency of Dutch reporting to the EWGLINET scheme, it
is hardly surprising that so many of the Dutch legionella cases are
associated with travel to Turkey.
Because of the bias amongst holiday-makers for travel to particular
destinations, it is useful to look at the number of EWGLINET cases associated
with travel to a particular country, relative to the total number of
visitors. The Office of National Statistics Travel and Tourism Survey2
can provide this information for UK travellers (Table 2). Whilst ten
UK tourists fell ill after visiting Turkey, giving a rate of 9.95 cases
per million UK travellers, the thirty-five UK tourists who fell ill
after visiting Spain give a rate of only 2.78 travellers because there
is so much more UK travel to Spain, than to Turkey.

France and Italy have begun to report more cases associated with internal
travel within their own country; this has greatly increased their number
of case reports to the coordinating centre (76 out of 121 cases travelling
in France in 2002 were French, whilst 60 out of 132 cases were Italians
travelling in Italy). This has an effect on the main countries of infection
reported to the scheme, as described above. However, it also highlights
the fact that many countries do not notify EWGLINET of travel-associated
cases in their own country by their own residents, and EWGLINET may
therefore be missing an unknown number of clusters.
The EWGLI guidelines have now been successfully introduced in all EU
member states, with support from the Ministry of Health in each country.
Norway, Turkey and a large number of the accession countries have also
agreed to use them. In the majority of countries, the guidelines are
functioning well, and clusters of cases of legionnaires' disease are
being investigated and dealt with promptly. Turkey has adapted less
successfully to the introduction of the guidelines and, as a result,
has had more sites published on the EWGLI website to date than any other
country. Assistance has been offered by EWGLINET to help countries such
as Turkey reach the standard achieved by the majority. However, the
fact that overall, nine of the cluster sites in Europe in 2002 have
yielded additional cases subsequent to satisfactory control and prevention
measures being reported is of concern. The countries involved should
investigate the reason for these breakdowns, otherwise the long term
credibility of the procedures adopted in the guidelines may be called
into question.
Investigations that include sampling are now expected for all cluster
sites, and they have shown a number of accommodation sites to be positive
for legionella. Whilst these sites cannot conclusively be proven as
the source of infection in the absence of clinical isolates for comparison,
the presence of legionella is highly suggestive of the sites being the
source. However, the proportion of positive legionella detections from
water samples varies widely between countries, suggesting that some
laboratories may be more successful than others in identification of
the organism rather than an absence of the organism itself in the tested
samples.
Closure of accommodation sites is at the discretion of local public
health authorities, but the introduction of the guidelines has standardised
the responses expected of the implicated sites. Tour operators and individual
members of the public may withdraw from sites associated with large
or extended outbreaks of legionnaires' disease, or when the accommodation
name is posted on the EWGLI website. Sites that contract with the large
tour operators face significant consequences if their name appears on
the website, and they are therefore normally amenable to implementing
the control measures expected of them. The cost of the measures is probably
far lower than the loss of business should the tour operators withdraw.
The one major outbreak in Belgium in 2002 demonstrated how well the
EWGLINET system can work to detect and respond to clusters. The cluster
was centred around hotel 'X' in Belgium and consisted of ten cases,
six English, three French and one Scottish. Each case visited at least
two of seven independent hotels, except for one case who visited only
hotel X, which was additionally the only hotel visited by all of the
other cases. The hotel was closed whilst investigations were carried
out. An indistinguishable strain of L. pneumophila serogroup 1 was isolated
from a patient sample from one of the outbreak cases and from water
samples from the hotel X's water system. It is very important to establish
this confirmatory link between cases and the source of infection, particularly
when cases may have stayed at several hotels before onset of illness
and when some of these hotels may also be linked to other clusters.
The fact that this scenario is occurring more frequently than in previous
years highlights one of the problems of an ever increasing database
of accommodation sites. Many sites will feature in clusters simply by
chance because of their use by tour operators and tourists alike.
Because of the trend for an increasing number of cases being reported
to EWGLINET each year, it is important to consider what may happen to
the scheme in future years. If the average increase in the number of
cases each year from 1993-2002 is taken (121.3% each year), and then
assumed for the years 2003 - 2008, EWGLINET could be dealing with over
2000 cases in 2008. Obviously there are many variables which can affect
this. The projection assumes continuous growth of the scheme at the
current rate, a continued increase in the uptake of urinary antigen
testing, additional countries joining the scheme and contributing new
cases, and an increase in surveillance by existing countries. The projection
also assumes a reduction in the level of under diagnosis, a reduction
in the level of under reporting, and it assumes that the impact of the
guidelines is delayed until the true level of incidence is obtained.
If the number of cases does continue increasing in line with this projection,
this has large implications for workload, both for the co-ordinating
country and for the collaborators in the countries of report and infection,
the latter of whom must ensure that each cluster is investigated thoroughly.
The increase in multi-site clusters additionally threatens to increase
the workload for all involved. However, the increase in cases reported
to EWGLINET should be seen as a positive development, and not just as
a problem to be overcome. It demonstrates that case detection by national
surveillance schemes for legionnaires' disease is improving, which allows
for more rapid and complete ascertainment of clusters, and this in turn
gives an opportunity for countries to respond to outbreaks in a more
timely and efficient manner.
Acknowledgments
This work is funded by the European Commission DG SANCO General Health
and Consumer Protection.
We would like to thank all the collaborators3 for reporting their cases
and all the people involved in public health control and prevention
programs for travel associated legionnaires' disease.
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