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Previous Article | Next Article 
Journal of Clinical Microbiology, August 1999, p. 2652-2655, Vol. 37, No. 8
0095-1137/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Single Clonal Origin of a High Proportion of Legionella
pneumophila Serogroup 1 Isolates from Patients and the Environment
in the Area of Paris, France, over a 10-Year Period
Christine
Lawrence,1,*
Monique
Reyrolle,2
Sylvie
Dubrou,3
Françoise
Forey,2
Bénedicte
Decludt,4
Claire
Goulvestre,1
Peggy
Matsiota-Bernard,1
Jerome
Etienne,2 and
Charles
Nauciel1
Laboratoire de Microbiologie, Hôpital
R. Poincaré, Garches,1 Centre
National de Référence des Légionelles, EA 1655,
Faculté de Médecine Laennec, Lyon,2
Laboratoire d'Hygiène de la Ville de Paris,
Paris,3 and Institut de veille
sanitaire, St Maurice,4 France
Received 15 January 1999/Returned for modification 12 March
1999/Accepted 18 May 1999
 |
ABSTRACT |
Arbitrarily primed PCR with three primers and pulsed-field gel
electrophoresis were used to characterize a set of 75 clinical Legionella pneumophila serogroup 1 isolates, with no
apparent epidemiological link, obtained from 24 hospitals in Paris,
France, from 1987 to 1997. Unexpectedly, 25 clinical isolates from 15 hospitals had an identical profile (termed type A) by both methods. The
same profile was subsequently found in 16 of 64 randomly selected environmental L. pneumophila serogroup 1 isolates from 15 different sites in the Paris area. There was no evidence of geographic
clustering or a peak incidence of type A isolation. Type A has not been
found in France outside the Paris area, suggesting that a particular type of L. pneumophila serogroup 1 is specifically present
in the Paris water distribution network.
| |
INTRODUCTION |
Legionella pneumophila is
a common cause of nosocomial and community-acquired pneumonia, being
transmitted by inhalation of aqueous aerosols. Most cases of
Legionnaires' disease are sporadic, but outbreaks can also occur
(1, 2, 3, 7, 8, 11, 12). L. pneumophila is
ubiquitous in the aqueous environment, and most outbreaks are linked to
contaminated hot water systems in well-defined areas (e.g., hotels,
hospitals, and whirlpool spas) and cooling towers (1, 2, 7, 11,
12, 23). Most clinical infections are due to L. pneumophila serogroup 1 (17). Strain subtyping methods
are used to confirm the environmental source of infections and include
monoclonal antibody typing, plasmid analysis, and multilocus enzyme
electrophoresis (6, 15, 16, 19). More recently, techniques
based on genomic DNA polymorphisms have been described, such as
restriction fragment length polymorphism analysis with or without the
use of probes (ribotyping), pulsed-field gel electrophoresis (PFGE),
and arbitrarily primed PCR (AP-PCR) (3, 9, 10, 13, 14, 16, 18, 21,
22, 25-27). PFGE has a high discriminatory power, readily
distinguishing epidemic from sporadic isolates. PFGE is expensive and
time-consuming in comparison with AP-PCR, which is suitable for large
sets of isolates (13, 21). The discriminatory power of
AP-PCR as an epidemiological tool for investigation of Legionnaires'
disease outbreaks has been previously evaluated with three different
primers and found to be similar to that of PFGE (13). The
DNA amplification profiles generated by AP-PCR and the DNA restriction
profiles given by PFGE were identical for epidemiologically related
L. pneumophila isolates, whereas unrelated cases generally
gave different profiles except for one cluster of four isolates from
the Paris area (13).
Molecular typing techniques have never been applied to a large set of
L. pneumophila clinical isolates collected in a large city.
In the present study we determined the AP-PCR and PFGE profiles of 75 L. pneumophila isolates from patients admitted to various Paris hospitals between 1987 and 1997. Although these patients had no
identified epidemiological link, we found that 33% of them were
infected by the same subtype.
| |
MATERIALS AND METHODS |
Strains.
A total of 75 clinical L. pneumophila
serogroup 1 isolates were studied. They were isolated from
bronchoalveolar fluid or bronchial aspirates of patients admitted to 24 hospitals in the Paris area with community-acquired (63 cases) or
hospital-acquired (12 cases) legionellosis. Legionellosis was
classified as nosocomial when it occurred more than 10 days after
hospital admission. The clinical isolates were obtained between 1987 and 1997. Culture and identification of L. pneumophila were
carried out in the microbiology laboratory of R. Poincaré
Hospital (Garches, France).
Furthermore, 64 environmental isolates were randomly chosen from a
collection of strains isolated between 1986 and 1997 by the Laboratoire
d'Hygiène de la Ville de Paris from water supplies and cooling
towers in 43 sites in the Paris area (25-km radius) including
hospitals, other buildings, and swimming pools. One to 17 isolates per
year were included (median, 4).
Clinical specimens were plated on buffered charcoal-yeast extract agar
supplemented with 
-ketoglutaric acid. Environmental strains were
isolated as recommended by the French norm for isolation of
Legionella in water (AFNOR T90-431) (5).
Serogrouping was done by direct immunofluorescence with antisera from
the Centers for Disease Control and Prevention (Atlanta, Ga.). Strains
were stored at 
80°C until use.
AP-PCR assay.
The AP-PCR assay was performed at R. Poincaré Hospital as previously described (13). Primer
B1245 was used to screen the strains. Primers IR6110 and Leg2 were used
for strains yielding the same pattern with primer B1245. Band patterns
were compared visually. Two isolates were considered to have the same
AP-PCR type when the patterns obtained with the three primers were
indistinguishable. Very weak bands (not apparent on the photographs
and/or not detected reproducibly) were not taken into account. In
doubtful cases, the amplifications were repeated after a new
extraction, and the patterns were compared after comigration on the
same agarose gel.
Chromosomal PFGE analysis.
PFGE analysis was performed by
the French National Reference Center for Legionellosis. Genomic DNA was
prepared as previously described with some modifications
(13). Briefly, legionellae were treated with proteinase K
(50 µg/ml) in TE buffer (10 mM Tris-HCl and 1 mM EDTA, pH 8) for
24 h at 55°C, and DNA was digested with 20 IU of SfiI
restriction enzyme (Boehringer Mannheim, Meylan, France) for 16 h
at 50°C. Fragments of DNA were separated in a 0.8% agarose gel
prepared and run in 0.5× Tris-borate-EDTA buffer (pH 8.3) in a
contour-clamped homogeneous field apparatus (CHEF DRII system; Bio-Rad,
Ivry sur Seine, France) with a constant voltage of 150 V. Runs were
carried out with constant pulse times (25 s) at 10°C for 11 h
and increasing pulse times (35 to 60 s) at 10°C for 11 h.
Isolates with patterns which differed by no more than three restriction
fragments were considered to have the same pulsotype, while organisms
differing by more than three restriction fragments were considered
sufficiently divergent to warrant a separate pulsotype designation
(24).
Statistical analysis.
Statistical analysis was done with
Epi-Info 5 software (Centers for Disease Control and Prevention).
Results for patients infected by type A strains were compared with the
results for patients infected by other types by using the
2 test with Yates' correction. Fisher's exact test was
used to calculate P values when expected numbers were below five.
| |
RESULTS |
Clinical isolates.
Primer B1245 was chosen to screen the 75 clinical isolates as it discriminates unrelated strains of L. pneumophila serogroup 1 (13). Unexpectedly, an
identical pattern was obtained for 28 isolates, while different
patterns were obtained for the other 47 isolates. To confirm the
molecular identity of these 28 isolates, they were compared by the
AP-PCR method, using the other two primers (IR6110 and Leg2), and by
PFGE after SfiI digestion. All these techniques gave
identical profiles for 25 of the 28 isolates, while the other isolates
were considered different from one another. This suggested that a
particular L. pneumophila type (designated type A) infected
25 (33%) of the 75 patients. The type A L. pneumophila isolates were isolated from patients admitted to 15 hospitals between
1988 and 1997 (Fig. 1). There was no
obvious peak incidence (Fig. 2A).
Patients infected by type A did not differ significantly from patients
infected by other types in terms of age, sex, risk factors, need for
mechanical ventilation, and mortality (Table 1). Among the 25 type A infections, 19 were acquired in the community and 6 were acquired in hospitals. Type A
was found in the water supply of three of the six hospitals concerned.
In the first case, a type A strain was found in eight hot water
samples, including samples from the shower and the hot water tap in the
patient's bedroom. In the second case, a type A strain was isolated
from the main hot water flow-back drain but not from two peripheral sites where nonserogroup 1 L. pneumophila was isolated. In
the last case, a type A strain was isolated from a hot water sample obtained 4 years earlier, during an epidemiological investigation conducted following the occurrence of three nosocomial cases identified on the basis of serological criteria.
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|
FIG. 1.
Geographic distribution of hospitals where L. pneumophila serogroup 1 infections were detected between 1987 and
1997 and sites where environmental L. pneumophila
serogroup 1 strains were isolated. Isolates from the same hospital are
boxed.
|
|
Environmental isolates.
To identify a possible environmental
source, we applied the same molecular methods to 64 environmental
strains isolated in the Paris area between 1986 and 1997 (Table
2). AP-PCR with primer B1245 gave the
type A pattern with 25 isolates. AP-PCR with the other two primers, and
PFGE after SfiI digestion, confirmed that 16 isolates
collected from 15 sites over an 11-year period had the type A pattern.
There was no evidence of geographic clustering (Fig. 1). L. pneumophila isolates belonging to type A were regularly recovered
from Paris environmental samples (from zero to five times a year, with
no obvious peak incidence) (Fig. 2B) in hot water supplies, cooling
towers, and a swimming pool (Table 2).
Comparison of the type A PFGE profile with profiles in the data bank of
the French National Reference Center for Legionellosis (containing more
than 250 PFGE profiles of clinical L. pneumophila serogroup
1 strains, 33 of which were isolated in the Paris area) indicated that
the type A profile was not found outside the Paris area.
| |
DISCUSSION |
Various molecular methods based on genomic DNA polymorphisms of
L. pneumophila serogroup 1 can be used to discriminate
between epidemic and nonepidemic isolates (9, 10, 13, 14, 16, 18,
21, 22, 25-27). The finding that 25 sporadic clinical L. pneumophila isolates from the Paris area had identical AP-PCR patterns led us to suspect that the method lacked discriminatory power.
However, a second molecular method, PFGE, which analyzes different
portions of the Legionella genome, confirmed the strict identity of the 25 isolates. Unpublished results obtained by one of us
(J.E.) show that PFGE, used to type more than 250 clinical L. pneumophila serogroup 1 isolates, has a discriminatory power of
over 95% and that strains with the same pulsotype are most often
epidemiologically related. The assumption, based on investigations of
Legionnaires' disease outbreaks, that clinical L. pneumophila isolates with identical PFGE types come from a single
source should thus be reconsidered if the cases occur in large cities
such as Paris. Indeed, 33% of our L. pneumophila serogroup
1 clinical isolates and 25% of the Paris environmental isolates had
the same pattern (designated type A) by AP-PCR, with three different
primers, and by PFGE. Six cases were considered definitely nosocomial
but occurred in six different hospitals, further suggesting that a common environmental localized source was not involved. In the 19 cases
considered to be community-acquired, no retrospective epidemiological
study was undertaken to identify a possible common source. The latter
cases were not clustered geographically or chronologically but occurred
in various parts of Paris, and the incidence remained stable over the
10-year study period, suggesting that the infection was endemic rather
than epidemic and that contamination of water sources is widespread in
Paris. These results were confirmed by the presence of type A strains
in various sites throughout the Paris area over a long period. This is
the first time, to our knowledge, that dissemination of a single clone
of L. pneumophila serogroup 1 throughout a water
distribution network has been described. The fact that apparently
unrelated isolates of L. pneumophila can display the same
PFGE pattern has already been reported (21); such isolates
can be found at sites separated by up to 60 km (14). It has
also been shown, in Los Angeles County, that environmental strains
exhibiting the same molecular markers as strains isolated from patients
can be found at sites distinct from the site of infection
(3). Our study emphasizes the need for molecular epidemiologic studies to include a large number of control strains to
establish the validity of a given marker in a given area. It also
suggests that molecular epidemiologic studies can only be used in
conjunction with clinical epidemiologic findings and cannot stand on
their own.
Moreover, it is also known that a single type of L. pneumophila can persist in the same water supply system for at
least 10 years (4). Our results and other published data
indicate that certain types of L. pneumophila are better
suited to persistence in the environment (20). The similar
proportions of type A strains among clinical and environmental isolates
in this study suggest that the high incidence of type A infections is
due more to the abundance of this strain in the environment than to
greater pathogenicity. Taken together, our results show that type A is
ubiquitous and constantly present in the L. pneumophila
population of the Paris water supply network. The spread of this type
from a water catchment or storage site is one possible explanation.
Molecular analysis of all isolates from patients with legionellosis
acquired in large cities should throw new light on the diversity of
L. pneumophila.
| |
ACKNOWLEDGMENT |
This work was supported by a grant from the Programme Hospitalier
de Recherche Clinique (AOM 96134).
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Laboratoire de
Microbiologie, Hôpital R. Poincaré, 104 Bd. R. Poincaré, 92380 Garches, France. Phone: 33 1 47 10 79 48. Fax: 33 1 47 10 79 49. E-mail: christine.lawrence{at}rpc.ap-hop-paris.fr.
| |
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Journal of Clinical Microbiology, August 1999, p. 2652-2655, Vol. 37, No. 8
0095-1137/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
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Abstract
Introduction
