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Home Eurosurveillance Monthly Release  1999: Volume 4/ Issue 11 Article 3
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Eurosurveillance, Volume 4, Issue 11, 01 November 1999
Research Articles
Epidemic cluster of legionnaires’ disease in Paris, June 1998

Citation style for this article: Decludt B, Guillotin L, van Gastel B, Perrocheau A, Capek L, Ledrans M, Etienne J, Carlier D, Jarraud S, Dubrou S, Reyrolle M. Epidemic cluster of legionnaires’ disease in Paris, June 1998 . Euro Surveill. 1999;4(11):pii=60. Available online:
B. Decludt1, L. Guillotin 2, B. Van Gastel 2, S. Dubrou 3, S. Jarraud 4, A. Perrocheau 1, D. Carlier 3, M. Reyrolle 4, I. Capek 1, M. Ledrans 1, J. Etienne 4
1. Institut de Veille Sanitaire, Saint-Maurice, France
2. Direction des Affaires Sanitaires et Sociales, Paris, France
3. Laboratoire d’Hygiène de la ville de Paris, Paris, France
4. Centre National de Référence des Legionella, Lyon, France

From 29 June to July 1998, four cases of legionnaires’ disease in British citizens were reported to the Réseau National de Santé Publique (RNSP) by the statutory notification system (déclaration obligatoire (DO)) and by the European Surveillance Scheme for Travel Associated Legionnaires’ disease coordinated by the European Working Group for Legionella Infections (EWGLI). One of the cases was detected by the enhanced surveillance scheme set up during the Football World Cup. All four cases had stayed in Paris in the ten days before developing symptoms. A survey was conducted in order to confirm the existence of an outbreak, to identify a common source of contamination, and to adapt control measures in response to the epidemiological situation.


Case definition

A case was defined as any person who stayed in Paris in June 1998 in the ten days before developing pneumonia associated with at least one of the following laboratory criteria: isolation of legionella, positive direct immunofluorescence, detection of legionella antigen in urine, fourfold rise in antibody titre up to a minimum of 1:128 (confirmed case), single high antibody titre (³ 256) (presumptive case). Cases confirmed to have been exposed to infection in hospital in the ten days before becoming ill were excluded.

Case finding

Active case finding was undertaken, using five sources of information:

- review of all notifications of legionnaires’ disease received in June and July 1998 at the RNSP

- search for unreported confirmed cases from the National Reference Center for Legionella (NCR) and from the microbiology laboratories in the Paris area.

- the surveillance system set up for the World Football Cup was extended to include all district health offices.

- all EWGLI’s European collaborators were alerted and public hospitals in Paris were informed.

Case interviewing

Cases who did not live in France were interviewed about the places they visited while in France. Data collection for French cases focused on places visited in June in Paris and on potential exposures related to housing, workplace, and domestic and leisure activities.

Case control study

The exploratory survey led to a hypothesis that the frequentation of a particular area of Paris could be linked to onset of disease. A case control study was therefore undertaken among cases living in France in order to determine whether visits to this area in June were associated with the occurrence of legionnaires’ disease. Cases were defined as people resident in France infected with Legionella pneumophila serogroup 1 (Lp1), confirmed or possible, who had stayed in Paris in June in the ten days before becoming ill. For each case, three controls were identified using telephone random digit dialling matched by sex, age category (30 to 60 years, >60 years), and district of residence. Controls had to have visited Paris at least once in June and had to have presented no respiratory symptoms (cough, fever) since the beginning of June. Strengths of association between factors analysed and disease were calculated in terms of matched odds ratio (OR). The stability of the association was analysed with the Mac Nemar test or the corrected test when the number of discordant pairs was <10. The OR precision was given by its 95% confidence interval, calculated with the Mantel Haenszel method.

Environmental investigation

This was carried out by the Health-Environment Service in Paris and the Laboratory for Hygiene. At first, a survey was conducted in a hotel where two cases had stayed and water samples were processed. Subsequently, it appeared that most of the other cases had visited the same geographical area but had not stayed in any common accommodation. The hypothesis of an external source of contamination, such as a cooling tower, was then raised. An environmental survey began using the official inventory of listed installations, which comprised 39 cooling towers located in this geographical area. A telephone survey identified 25 locations presenting potential risks of contamination, seven of which were classified as suspect, as malfunction had been reported in the month before cases become ill or because they were located next to the areas visited by the cases. These seven sites were inspected and water samples were collected.

Laboratory investigation

The genomic profiles of the strains isolated in patients and in water samples were determined by pulsed field gel electrophoresis (PFGE) at the National Reference Center for Legionella.


Epidemiological investigation

A total of 20 cases of legionnaires’ disease were identified in people who had visited Paris in June 1998: 11 were French residents and nine European tourists (seven British, one Danish, and one Swedish). Their mean age was 51 years (29 to 77 years) and 19 of them were men. Four patients died (20%). The cases arose between 6 June and 14 July, and 11 (55%) were clustered between 15 and 21 June (figure). Nineteen cases were confirmed (6 by culture, 11 by detection of urinary antigen, 2 by seroconversion) and one was a presumptive case. The six clinical isolates were L. pneumophila serogroup 1 (Lp1) with identical PFGE patterns. Predisposing factors for the disease were found in 17 patients: chronic renal disease and/or impaired immunity (3), diabetes (2), smoking only (12).

fig1.gif (25328 octets)


The case interviews did not reveal a common visited site apart from a hotel at which two cases stayed. Sixteen out of 19 cases (84%), about whom information was available had visited four adjoining districts north of the Seine (9th, 2nd, 8th, and/or 10th arrondissements (districts).

Among the 12 cases admitted to hospital in France, four were excluded from the case control study (residence in Scotland, could not be traced, died with no family, Lp5-6 infection). Eight cases and 24 controls were included.

Visits to the 2nd, 8th, 9th, or 10th districts of Paris were significantly associated with the onset of disease (OR = 15 (95% confidence interval (CI): 1.3-166.9)). The matched OR could not be calculated for limited time spent at work or at home but the association remained significant (p=0.002). When the suspect area was limited to the 2nd and 9th districts or to the 9th district alone, the risk remained high but the confidence interval reached the limit of the significance threshold (table).

Table: Comparison of the visits of the districts or homes and workplaces between cases and controls




Matched P value or OR (95% CI)

N=8 (%)

N=24 (%)

Area 2°, 8°, 9°, 10° districts


7 (87)

7 (29)

15 (1.3-166.9)

Home or workplace

6 (75)

2 (8)


Area 2° and 9° districts


5 (62)

6 (25)

10 (0.8-124.9)

Home or workplace

4 (50)

1 (4)


9° district


4 (50)

4 (17)

5 (0.8-31.4)

Home or workplace

3 (37)

1 (4)

9 (0.9-86.5)


Environmental findings

L. pneumophila strains isolated in the hotel (hot water tank) visited by two of the cases belonged to a serogroup different from the cases’ serogroup and could therefore not be linked to the outbreak. Contamination with legionella was detected in six of the seven air conditioning cooling towers inspected (3.102 to 2.106 unité formant colonies (ufc/L)). Lp1 (2.104 to 106 ufc/L) was identified in three sites. The Lp1 strain isolated in one of the sites in the 2nd district presented a genomic pattern similar to the six strains isolated from cases.

Control and prevention measures

Preventive control measures were taken while the environmental investigation proceeded in view of the urgency of the situation. An official letter was sent to all owners of cooling towers in the 2nd and 9th districts requesting them to clean and disinfect the installations. Water samples subsequently tested for the presence of legionella showed that the procedure had been effective.


The results of all investigations (epidemiological, microbiological, and environmental) suggest that dissemination of water aerosols infected with legionella from a cooling tower was the source of the outbreak.

The closeness in time and space of cases in comparison with previous data confirmed the epidemic nature of this episode. Most cases had visited a limited area of Paris but had not stayed in any one place, raising the hypothesis of an external environmental source of contamination and providing a rationale for conducting the environmental survey. The case control study, despite its limits, confirmed that visiting an area of four adjoining districts was significantly associated with disease. The hypothesis that a single source of contamination was responsible was supported by the indistinguishable electrophoresis patterns of the strains isolated from six cases. Environmental sampling enabled us to identify a site infected by the epidemic strain. Furthermore, the site and the patients’ electrophoresis patterns did not correspond to any frequently identified strains in the Paris area. All these factors strongly suggest that this site was the source of the epidemic, although we cannot be certain that it was the sole source of contamination.

Many outbreaks of legionnaires’ disease have been associated with hot water distribution systems, showers, whirlpool baths, and decorative fountains (1-2). During outbreaks in the community, exposure to cooling towers or evaporative condensers infected with legionella has often been found (3-4), but many apparently sporadic cases could be linked to intermittent exposure to common sources, such as cooling towers (5).

It is difficult to estimate the real number of cases linked to this outbreak since cases of legionnaires’ disease in the community are underreported and/or underdiagnosed, in spite of reinforcement of the surveillance in 1997 and the stimulation to report during the Football World Cup. Less severe clinical forms may have gone unnoticed.

The general contamination of the visited sites stresses the need for preventive disinfecting of cooling towers. Their owners should be made aware of the risks for public health that may be linked with operating these equipments.


The circumstances in which this outbreak occurred and the conditions in which the investigation was carried out are an opportunity to remind readers:

- the benefit of notification of any case of legionnaires’ disease (acquired in the community or in hospital) and of reducing delay between diagnosis and notification,

- various microbiological methods available for diagnosing legionnaires’ disease, detection tests for urinary antigen, and searching for bacteria,

- the importance of European collaboration on legionnaires’ disease surveillance,

- the value of maintaining air conditioning cooling towers and increasing professional awareness.

Acknowledgements : We wish to thank all the district offices, clinicians, and microbiologists who collaborated in the survey.

This article has been published in the Bulletin Epidemiologique Hebdomadaire 1999, 21:83-5


1. Jernigan DB, Hofmann J, Certon MS, Genese CA, Nuorti JP, Fields BS, et al. Outbreak of legionnaires’ disease among cruise ship passengers exposed to a contaminated whirlpool spa. Lancet 1996; 347: 494-9.

2. Hlady WG, Mullen RC, Mintz CS, Shelton BG, Hopkins RS, Daikos GL. Outbreak of legionnaires’ disease linked to a decorative fountain by molecular epidemiology. Am J Epidemiol 1993; 138: 555-62.

3. Centre de Santé Publique du Québec. Epidémie de légionellose dans la région de Québec, Canada, Mai-Juin 1996. Rapport mars 1997.

4. Fiore AE, Nuorti JP, Levine OS, Marx A, Weltman AC, Yearger S, et al. Epidemic legionnaires' disease two decades later: old sources, new diagnostic methods. Clin Infect Dis 1998; 26: 426-33.

5. Bophal RS, Diggle P, Rowlingson. Pinpointing clusters of apparently sporadic cases of legionnaires’ disease. BMJ 1992; 304: 1022-7.

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