A European surveillance scheme for travel associated legionnaires' disease
(now called EWGLINET) was established by the European Working Group
on Legionella Infections (EWGLI) in 1987. Its objectives are to identify
cases of legionella infection in returning travellers, to detect outbreaks
and clusters of legionnaires' disease and to collaborate in the control
and prevention of further cases. Its history and current activities
are described in detail on its website (1). This paper provides results
and commentary on reports of cases that occurred in 2000 and 2001. The
impact of a major change in the cluster definition in 2001 and an increase
in reports from specific countries will be discussed.
A case of travel associated legionnaires' disease is defined as a person
- Clinical or radiological evidence of pneumonia and a laboratory diagnosis
demonstrating evidence of legionella infection (2);
- A history of travel in the 10 days before the onset of illness. Travel
is defined as staying away from home for one or more nights in accommodation
used by travellers, such as hotels, holiday apartments etc.
Details on cases ascertained by national or regional surveillance systems
of participant countries are entered into the scheme's web database.
When a new case is added, the database is searched by the coordinating
centre at CDSC for any previous cases reported to have stayed at the
same accommodation site.
From 1 January 2001, a cluster is defined by EWGLINET as 2 or more cases
associated with an accommodation site, which occur within two years
of each other. All other cases are treated as single cases. Under the
old definition, cases occurring at sites with previous cases more than
six months earlier were categorised as "linked".
Single cases are immediately notified to national collaborators and/or
the Ministry of Health. Clusters are reported to all collaborators and
the World Health Organization (WHO). In some countries public health
authorities choose to report clusters to their national organisations
of tour operators. Different levels of intervention are expected: issuing
a checklist for minimising risk of legionella infection to sites associated
with single cases, and conducting risk assessments, sampling for legionella
and implementing control measures at sites associated with clusters
(3). Closure of accommodation sites is at the discretion of public health
authorities, but tour operators sometimes withdraw from sites associated
with large or extended outbreaks of legionnaires' disease.
In 2000, 31 countries and 38 collaborating centres took part, increasing
to 33 countries and 43 centres in 2001 (figure 1). The number of cases
by year of onset has increased from 3 cases in 1987 to 360 in 2000 and
481 in 2001, the highest number reported to the scheme in any one year
Characteristics of cases
In 2000 age and sex profile of cases were similar to previous years,
with more than twice as many men as women reported. The mean age of
cases was 57 years in 2000 (median age 57 years, range 24-88 years).
In 2001 the age distribution showed similar characteristics with a mean
and median age of 59 years (range 17-96 years). The proportion of men
to women increased to 3:1 with most of the increase occurring in men
in the 50-59 and 60-70 year age groups. In women, the main decrease
occurred in the 40-59 year age groups. Most countries reported cases
in both years in proportion to the overall male/female ratio except
for France where the male to female ratio of cases was 7.3/1 in 2000
and 5.3/1 in 2001.
The number of cases diagnosed by culture has remained small, with 36
in 2000 and 34 in 2001. The urinary antigen detection method was used
to confirm 262 (73%) cases in 2000 and 378 (79%) cases in 2001 (figure
2), resulting in both an absolute and a proportionate decline in the
numbers of cases diagnosed by all other methods. Diagnosis by a four-fold
rise in antibody levels declined to 26 (5%) cases in 2001 from 36 (10%)
in 2000 compared with 61 (25%) in 1997. Cases diagnosed by single high
titre serology have remained at similarly low numbers in recent years
and accounted for 6-7% of all reports in 2000 and 2001. Use of other
techniques such as PCR accounted for 0-2% of cases in the same period.
In 2000, 117 cases (28%) were linked to L. pneumophila sgp1 infection
and 182 (50.5%) to L. pneumophila other or unknown serogroup. In 2001
these figures were 186 (21%) for L. pneumophila sgp1 and 225 (47%) for
L. pneumophila other or unknown serogroup. The remaining cases in both
years were reported as legionella with no further details. Only 2 cases
had other species detected and reported, both in 2001.
An outcome of illness was reported for 74% of cases in 2000 and 73%
in 2001. Deaths were reported for 23 cases in 2000, and 41 cases in
2001, case fatality rates of 6.4% and 8.5% respectively. Cases reported
as still ill at the time of report or known to have recovered were similar
in both years (32% and 29.5% still ill, and 35.5% and 35% recovery in
2000 and 2001 respectively). Cases were further classified as having
a known outcome (recovery or death) or unknown outcome (still ill or
unknown). In 2000, 42% had a known outcome, and 44% in 2001. This compares
with an average of 65% with a known outcome between 1992 and 1999 (figure
Infections are usually diagnosed after cases return to their country
of residence and 18 countries reported cases in either 2000 or 2001.
The Netherlands reported the greatest number of cases: 103 (29%) in
2000 and 118 (24.5%) in 2001 (figure 4) followed by England and Wales,
91 (25%) cases in 2000 and 89 (18.5%) cases in 2001. France almost doubled
and Italy more than doubled the number of cases reported in 2001 compared
with the previous year.
Median interval between onset of illness and report of the case to EWGLINET
were 33 days in 2000. This was reduced to 23 days in 2001 (figure 3).
A median of 38 days was calculated between 1992 and 1999. The Pearson's
correlation coefficient between the proportion of known outcomes and
the median delay to report was -1.2 (p=0.010; 95% CI [-2.077; 0.337]),
indicating a decrease of 1.2% in known outcome for every day's reduction
in the time from onset to report of a case.
It was notable that 4 countries in 2001 were responsible for reporting
71% of the cases: the Netherlands, England and Wales, France and Italy.
The travel patterns for cases from these countries were distinct, with
87% of Italy's cases travelling in Italy and 66% of France's in France.
In contrast, only 4% of Dutch cases and 8% of English cases travelled
in their own country. The Dutch traveled to a far wider range of countries,
28% of them to Turkey and 11% to more than one European country, while
29% of the English traveled to Spain, 13% to Turkey and 16% to countries
outside of Europe.
Cases with onset in 2000 stayed at an average of 1.7 accommodation sites
in 56 countries. For the first time, France was the most visited country
with 55 cases (15%) traveling only in France. Fifty-four (15%) cases
visited only Spain, 40 (11%) only Turkey and 36 (10%) cases only Italy.
Forty two (12%) cases travelled in more than one country in Europe,
mostly through France, Italy and Spain and a further 89 cases to other
European countries. Nine cases were associated with Mexico, the remaining
35 (10%) cases with countries outside the EWGLINET scheme.
Cases with onset in 2001 visited an average of 1.5 sites in 46 countries.
Italy was the most visited country for the first time with 91 (19%)
cases travelling only in Italy. France was associated with 86 (18%)
cases travelling only in France, Turkey with 78 (16%) cases and Spain
with 74 (15%) cases only in Spain. Twenty-five cases travelled to more
than one country in Europe, mostly through France, Italy, Germany and
Spain; the remaining 42 cases with other European countries. Eleven
cases were associated with travel to Mexico, and a further 74 (15%)
cases with countries outside the EWGLINET scheme.
Rates of infection in travellers from the United Kingdom were calculated
using data from the Office for National Statistics Travel and Tourism
Survey (4) (table 2). The highest rates of travel associated legionnaires'
disease were in travellers visiting Mexico and Turkey in both years,
and the lowest rates were in France and the United States.
In 2000, 254 (71%) cases stayed at only one accommodation site in the
two to ten days before onset. The remaining 106 (29%) cases visited
between two and eight sites and between one and five countries per incubation
period. In 2001, 373 cases (77.5%) cases had stayed at only one site,
the remainder again staying at between two and eight sites in one to
Cases used a variety of types of accommodation. Hotels and hotel apartments
were still the most popular with 77% and 78% of cases staying in at
least one such site during their incubation period in 2000 and 2001
respectively. As in 1999 (3), many itineraries included stays at smaller
sites, such as bed and breakfast, farmhouse and camping accommodation.
Travellers visiting these smaller sites were often touring and moving
on every few days. Business travel was also reported. These cases typically
spent short visits in large city hotels or at motels while on the road.
Eleven cases in 2000 and four in 2001 were associated with stays on
ferries or ships.
In 2000, 28 clusters were detected and associated with 70 cases, 19%
of the total reports (table 1). Of these clusters, 10 (36%) would not
have been detected without EWGLINET since each included only one national
from different countries. The clusters detected were small, ranging
in size from 2 to 5 cases. As in previous years, most of the clusters
occurred in the most visited countries. For example, Spain had the most
clusters (6), 2 of which were large with 5 cases each. Turkey had 5
clusters, France 4, and Italy 3. Countries outside of the EWGLINET scheme
were involved in 4 clusters, 2 in Mexico and 1 each in Morocco and Moldova.
Of the 70 cases associated with clusters, 10 deaths (14%) were reported.
Under the new cluster definition, 72 clusters were detected in 2001
and associated with 149 cases, 31% of the total reports (table 1). Without
EWGLINET, 23 (32%) clusters would not have been detected. The largest
cluster identified, in Spain, involved 8 cases and 3 further clusters,
in Spain and Turkey, involved 5 or 6 cases. Fifty-two of the clusters
had 2 cases associated with them. Turkey had the most clusters identified
(20). Half of all cases reported as travelling in Turkey were associated
with a cluster.
In 2001, 3 clusters were identified outside of the EWGLINET scheme,
2 in Mexico and 1 in the US. Amongst the clusters in the collaborating
countries, 4 involved multiple sites, 3 of them involving nationals
from the same country who travelled on the same itinerary: Turkey in
2 multiple clusters, Germany and Italy in the third. In a fourth cluster,
two nationals from different countries followed a similar travel pattern
at different times in Italy. Eleven (7%) of the 149 cases associated
with clusters were reported to have died.
In 2001, 43 of the 72 clusters identified (60%) would have met the old
definition. This means that EWGLINET 'gained' 29 extra clusters. France
was the country most affected by the new definition with eight 'additionnal'
clusters identified. Spain had 6, Italy 4 and Greece 3.
Greater use of the electronic database was made in 2001 for reporting
the results of environmental investigations at accommodation sites associated
with cases. Over 200 such reports were received in 2001 compared with
less than 40 in 2000. However, many of these reports were for investigations
carried out in previous years. Hence the following results only include
environmental investigations known to have been carried out recently:
55 investigations were carried out in 2000 and 140 in 2001 (table 3).
Of these 20 were for the 28 clusters detected in 2000 and 31 for the
72 clusters detected in 2001. Legionellae were detected in 9 of the
20 sites associated with clusters in 2000 and 15 of the 31 sites in
In 3 of the sites associated with single cases in 2000, a clinical isolate
from a case was indistinguishable by subgrouping and molecular subtyping
analysis from the environmental isolate. This occurred five times in
2001. For cluster sites in 2000, no such comparison could be made. However,
in 2001 clinical and environmental isolates were indistinguishable from
each other in 2 cluster sites, 1 in Norway and 1 in Italy. Control measures
were reported in just under half of all the investigations carried out
in both years, although information on the closure and re-opening of
sites was not very evident or reliable.
The EWGLINET surveillance scheme continued to expand in 2000 and
2001 with substantial increases in the numbers of cases reported together
with more information on environmental investigations. The rise in cases
is thought to be due to the improved detection and reporting from national
surveillance schemes, typified by the activities of France, Italy and
the Netherlands, rather than any new increase in overall incidence.
The Netherlands has now replaced England and Wales as the most frequent
reporter of cases. The comparison of the travel habits of cases from
France and Italy compared with those from the Netherlands, England and
Wales is interesting. Cases from England, Wales and the Netherlands
were almost all acquired abroad, whereas cases from France and Italy
mainly acquired their infection within their home country. Thus, improved
control measures in these latter two countries will substantially benefit
their own residents as well as nationals from other countries who visit
France and Italy in significant numbers. The different seasonal distribution
seen in 2001 may be the result of the high number of cases reported
by France and Italy, perhaps related to their different national habits
As in previous years (3) the marked increase in the use of the urinary
antigen detection test may also be contributing to the rise in the number
of cases reported. The test offers a rapid diagnostic facility compared
with other methods, allowing detection and reporting at an earlier stage
of illness. The correlation between the rise in the use of urinary antigen
detection test and the rise in the number of cases with an unknown or
'still ill' outcome at the time of report is noteworthy. The rising
proportion of cases with these outcomes means that a number of deaths
may not be reported and the case fatality ratio seen in EWGLINET may
consequently be a large underestimation. The level of data completion
in this area would be improved with follow up surveys of the collaborators
and/or the reporting local health authorities.
A further effect in the rise of the urinary antigen detection method
is that mainly only L. pneumophila infections are identified. It is
useful for clinicians and public health authorities to bear in mind
that a clinical specimen for culture may provide a positive diagnosis
in a suspected case where the result of the urinary antigen method is
negative. A higher number of cases diagnosed by culture would not only
provide better opportunities to match clinical and environmental isolates
for identifying sources of infection but would also detect other species
or serogroups of legionella infections.
The rates of infection calculated for visitors from the United Kingdom
(the only group for whom comprehensive information on the number of
travellers making trips abroad is available) indicate that countries
such as Mexico and Turkey are associated with a disproportionate number
of cases compared with the number of people from the UK visiting them.
Mexico is growing as a tourist destination whereas Turkey has experienced
an increase in popularity over the last ten years or so. Their high
rates of infection per million tourists should be addressed through
a greater emphasis on hotel legionella prevention programmes, in order
to minimise risk to people taking holidays there.
The response to clusters in the country of infection has been enhanced
in the last two years by the change in cluster definition at the start
of 2001. The large increase in clusters identified, 29 of which would
not have been identified as such under the old definition, has ensured
that in more instances an accommodation site will have a risk assessment
and environ- mental sampling conducted. Many of the linked cases that
the old definition would have identified have been absorbed into these
'new' clusters. In the notification to the country of infection those
cases identified as single rather than linked under the new definition
were flagged as having stayed at a site associated with a previous case
more than two years earlier, allowing that country to respond according
to its own public health policy. The clusters identified in 2000 and
2001 also demonstrate clearly the value of the international collaboration
in detecting otherwise unnoticed public health risks. One third of all
clusters would not have been identified without EWGLINET, as the cluster
cases each came from a different country.
The large proportion of cases whose itineraries included visits to more
than one site in a country or more continue to add to the logistic and
resource demands placed on local public health and environmental authorities
within the collaborating scheme. Response to single case reports varies
across the collaborating scheme. Authorities in Italy and Spain for
example investigate all sites associated with single cases (risk assessment
and/or environmental sampling) while other countries typically issue
the standard checklist of good practice in legionella control (5) the
minimum action required by EWGLINET.
A major undertaking throughout 2000 and 2001 was the development of
the European Guidelines for Control and Prevention of Travel Associated
Legionnaires' Disease that became operational in July 2002 (6). During
the creation of these guidelines a consensus arose within the collaborating
countries on the management of clusters from 2002, and the importance
of reporting environmental investigations from the country of infection
became more evident. This is reflected in the increased activity both
at the co-ordinating centre in London in entering pre-2000 and 2001
reports into the electronic database and in the rise in reporting of
investigations in 2001 by the collaborating countries. A full analysis
of these reports will be published separately.
A significant proportion of cluster sites, and also of single sites
had legionellae isolated from samples. This information is important
for assessing the impact of control measures at a site, as well as for
providing evidence for any legal action arising from an infection. However,
interpretation of the significance of environmental data results is
limited when there are no matching clinical isolates from associated
cases. The environmental investigations reported show that investigation
and reporting processes take varying amounts of time, depending on the
structure of public health services in each country. The European guidelines
are expected to improve the investigation reports, especially for cluster
sites, and should facilitate useful and interesting data in future years.
This work is funded by the European Commission DG SANCO General Health
and Consumer Protection.
We would like to thank all the collaborators (7) for reporting their
cases and all the people involved in public health control and prevention
programmes for travel associated legionnaires' disease.