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Sixty-three Cases of Mycobacterium marinum Infection
Clinical Features, Treatment, and Antibiotic Susceptibility of Causative Isolates
Alexandra Aubry, MD;
Olivier Chosidow, MD, PhD;
Eric Caumes, MD;
Jérôme Robert, MD, PhD;
Emmanuelle Cambau, MD, PhD
Arch Intern Med. 2002;162:1746-1752.
ABSTRACT
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Background Mycobacterium marinum is a nontuberculous mycobacterium
responsible for skin infections. Although cases have been seldom reported,
no series of M marinum infection has been recently
reported and the treatment is not standardized.
Methods A national survey was conducted on culture-confirmed M marinum infections that occurred in France from January 1, 1996,
to December 31, 1998. Clinical characteristics and therapeutic data were analyzed,
and the minimum inhibitory concentrations of 11 antibiotics were determined
against the causative isolates.
Results Sixty-three cases of M marinum infection were
studied. In 53 (84%) of the patients, inoculation was related to fish tank
exposure. The site of infection was mainly the upper limb (in 60 [95%] of
the 63 patients), and infection was spread to deeper structures in 18 (29%)
of the patients. All patients were treated with antibiotics (median time,
3 months), and 30 (48%) underwent surgery. Various antibiotic regimens
were prescribed, and the initial regimen was modified in 22 (35%) of the patients.
Clarithromycin, cyclines, and rifampin were the most commonly prescribed antibiotics.
Cure was observed for 55 (87%) of the patients. Failure was related to deep
structure involvement (3 of 45 vs 5 of 18 patients; P
= .04) but not to any antibiotic regimen. All strains showed the same susceptibility
pattern without acquired resistance. The 90% minimum inhibitory concentrations
of rifampin and rifabutin were far lower (0.5 and 0.06 µg/mL, respectively)
than the 90% minimum inhibitory concentrations of clarithromycin (2 µg/mL)
and the cyclines (minocycline, 4 µg/mL; and doxycycline, 8 µg/mL).
Conclusions Mycobacterium marinum infections are emerging
infections related to fish tank hobby. Because of the severity of the cases
with spread of infection, clinical awareness of M marinum infection and its associated risk factors is important so that the
diagnosis can be made and therapy can be initiated promptly.
INTRODUCTION
MYCOBACTERIUM marinum is a nontuberculous
photochromogenic mycobacterium (group I of the Runyon1
classification). Mycobacterium marinum causes disease
in many fish species from cold or warm, fresh or salted water,2
and human infection follows contact with fishes or contaminated water. First
described as "swimming-pool granuloma,"3 M marinum skin infection is often acquired from aquarium
maintenance and called "fish tank granuloma."4
The infection is commonly limited to a skin disease on the limbs but can spread
to deeper structures, resulting in tenosynovitis,5
arthritis,6 and osteomyelitis.5, 7
Disseminated infections are exceptional.8 The
incidence of M marinum infection in humans is underestimated,
but rates of up to 0.27 case per 100 000 inhabitants have been observed.9
Surgery, antibiotherapy, and cryotherapy have been recommended for the
treatment of M marinum infections,2
but none of these treatments has proved to be superior to another. Antibiotic
efficacy and its correlation to in vitro susceptibility are unknown because
cases were reported separately in the literature, no therapeutic trial has
been done, and data on M marinum susceptibility are
scarce (limited number of strains and antibiotics).10-12
The aim of the present survey, organized by the National Reference Center
for Mycobacterial Disease and Drug Resistance (NRC), was to draw recommendations
for the treatment of M marinum infection from the
data collected on the culture-positive M marinum
infections that occurred in France. From clinical records, special attention
was given to the outcome with regard to the spread of infection to deeper
structures, the antibiotics given, and additional surgery. In the laboratory,
we determined the in vitro susceptibility of M marinum
to antibiotics that were given to the patients to correlate its results to
in vivo efficacy.
PATIENTS AND METHODS
PATIENTS
Anonymous standardized forms were sent at the end of 1996 by the NRC
to dermatologists, infectious disease specialists, and microbiologists (Azay-Mycobacterium group) of university hospitals all over France.
A case patient was defined as a patient with a culture-positive infection
with M marinum. All cases diagnosed and treated between
January 1, 1996, and December 31, 1998, were reported, and the corresponding
strain was sent to the NRC laboratory (Laboratory of Bacteriology, Groupe
Hospitalier Pitié-Salpêtrière, Paris, France).
The following information was collected: patient characteristics (sex
and age), immune and human immunodeficiency virus status, fish tank and swimming
hobbies, injury and contact with fishes, infection history, site and clinical
type of the lesions, spread of infection to deeper structures (tendon, joint,
or bone), antimicrobial therapy (name of the antibiotic and date of start
and discontinuation), surgery, and clinical outcome. Forms were filled in
by the clinicians and microbiologists in charge of the patient. Additional
data were collected, when needed, by telephone or written correspondence between
the NRC and the clinician or microbiologist. An antibiotic regimen was eligible
for efficacy evaluation if it had been given for at least 15 days. Outcome
was defined as cure when no sign of infection was observed at the end of treatment
or significant improvement was noticed at the end of the follow-up, and as
failure when no improvement, after effects, or relapse was observed.
STRAINS
The strains of M marinum were grown on Löwenstein-Jensen
medium on arrival at the NRC laboratory. They were identified based on the
phenotypic characteristics, as previously described,13
and then stored at -80°C in Youmans broth, supplemented with 20%
fetal bovine serum. The minimum inhibitory concentrations (MICs) of 11 antibiotics
(rifampin, rifabutin, ethambutol hydrochloride, amikacin, doxycycline, minocycline,
clarithromycin, ofloxacin, levofloxacin, ciprofloxacin, and sparfloxacin)
were determined by the agar dilution method in Mueller-Hinton agar supplemented
with 5% Middlebrook OADC (oleic acid, albumin, dextrose, and catalase [Fisher
Scientific International, Elancourt, France]), as previously described.14
ANALYSES
Data were computerized and analyzed using computer software (Epi Info
6.1; Centers for Disease Control and Prevention, Atlanta, Ga). When appropriate,
differences between categories were analyzed using the  2 test
for quantitative values and the t test for qualitative
values.
RESULTS
GENERAL CHARACTERISTICS OF THE PATIENTS
Culture-confirmed infection with M marinum
was reported for 66 patients from 1996 to 1998 in France. The incidence of M marinum infection in France was, therefore, about 0.04
case per 100 000 inhabitants per year. Three cases were excluded because
of insufficient information on patient outcome. The 63 cases included in the
study distributed as 10 cases in 1996, 28 in 1997, and 25 in 1998. The patients
included 37 males and 26 females, and their median age was 46 years (range,
4-77 years). A total of 31 hospitals, distributed in all areas of France,
reported cases. Exposure to a fish tank in a household with indoor or outdoor
aquariums was reported for 53 patients (84%), and death of the tank fishes
was reported in 15 of the 23 informed cases. Injury or contact with a fish
spine or oysters was reported for 5 patients, and swimming pool hobby was
reported for 1. The source of infection was unknown for 4 patients. Four patients
had the human immunodeficiency virus, including 2 who had the acquired immunodeficiency
syndrome.
CLINICAL CHARACTERISTICS
Clinical characteristics by treatment outcome are presented in Table 1. Among the 27 patients with a recorded
history of infection, the median time between inoculation and the appearance
of lesions was 16 days (range, 0-292 days). The site of the skin lesions was
the upper limb in 60 (95%) of the 63 patients. Only 3 patients had skin lesions
on the lower limb: a hospitalized child, an old woman who owns a fish tank
but did not do its maintenance herself, and a child who went to a swimming
pool. More than 1 skin lesion was observed in 32 (67%) of 48 patients informed
about this item. The clinical description of the skin lesions was reported
for 61 patients. Nodules were observed in 41 (67%) of the patients, including
a sporotrichoid aspect in 16 (39% of the nodules). The other skin lesions
were ulcers, abscesses, and pustules. Adenitis was observed in 10 patients.
Deep structure infection (tendon, joint, or bone) was reported in addition
to skin lesions for 18 patients: tenosynovitis in 15, arthritis in 7, and
osteitis in 3 (arthritis being combined with osteitis in 3 patients and with
tenosynovitis in 4) (Figure 1). Deep structure infection was more common in females than in males (11 of 26
females vs 7 of 37 males; P = .04) but was not related
with other characteristics.
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Table 1. Clinical Characteristics of Patients With a Mycobacterium marinum Infection With Regard to the Outcome
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Nodular lesion of Mycobacterium marinum infection with
tenosynovitis of the finger.
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A histologic examination was done in 51 (81%) of the 63 patients. Pathologic
typical findings of mycobacterial infection were reported for 29 (81%) of
the 36 written results that were transmitted.
TREATMENT
All 63 patients received antibiotics. The median duration of antibiotic
therapy was 3 months (range, 1-25 months). The duration was significantly
longer for patients with deeper structure infections than for patients with
infections limited to the skin and soft tissue (median duration, 7
vs 4 months; P = .004).
One single antibiotic regimen was prescribed for 41 patients, 2 successive
regimens were prescribed for 15 patients, and 3 successive regimens were prescribed
for 7 patients. The number of successive regimens was not related to general
or clinical characteristics (data not shown).
A total of 132 antibiotic prescriptions were given to the 63 patients,
ie, a mean of 2 antibiotic prescriptions per patient. The most frequently
prescribed antibiotics were clarithromycin, cyclines, including minocycline
and doxycycline, rifampin, and ethambutol. All patients received at least
1 of these antibiotics. The antibiotics administered and the number of their
courses are listed in Table 2
by treatment outcome and the severity of the infection (spread to deeper structures).
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Table 2. Antibiotic Courses Given to Patients With a Mycobacterium marinum Infection With Regard to the Spread of Infection
and the Outcome*
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Antibiotic therapy was given as a monotherapy in 23 patients (37%) and
as a combination of at least 2 drugs in 40 patients (63%). Antibiotics prescribed
as a monotherapy were cyclines for 19 patients (minocycline for 14 and doxycycline
for 5) and clarithromycin for 4 patients. Monotherapy was significantly associated
with infection limited to skin and soft tissue (20 of 45 vs 3 of 18 patients; P = .04). Frequent drug combinations were clarithromycin
plus rifampin (n = 20), cyclines plus clarithromycin (n = 11 [n = 4 with doxycycline
and n = 7 with minocycline]), rifampin plus ethambutol (n = 8), and cyclines
plus rifampin (n = 6 [n = 3 with doxycycline and n = 3 with minocycline]).
Cyclines were prescribed more for infection limited to skin and soft
tissue than for infection spread to deeper structures. In contrast, rifamycins
(rifampin and rifabutin) and ethambutol were prescribed more for infection
spread to deeper structures than infection limited to skin and soft tissue;
clarithromycin was equally prescribed in both cases (Table 2).
In addition to antibiotics, 30 patients underwent surgery for excision
or debridement, including 17 with infection limited to skin and soft tissue
and 13 with infection spread to deeper structures. Conversely, no surgery
was performed for 5 patients with deep structure infection (2 with arthritis,
1 with tenosynovitis, 1 with tenosynovitis and arthritis, and 1 with osteitis,
tenosynovitis, and arthritis) and for 28 with infection limited to the skin
and soft tissue. Surgery was indeed associated with deep structure infection
(13 of 18 vs 17 of 45 patients; P = .01) but not
with other characteristics (sex, age, aspect and site of the lesion, and outcome).
OUTCOME
The outcome was evaluated for the 63 patients: 55 (87%) were cured and
8 (13%) experienced treatment failure. The patients in whom treatment failed
are described in Table 3. Failure
was significantly related to infection spread to deeper structures (3 of 45
vs 5 of 18 patients; P = .04) and to the skin lesion
aspect of the ulcer (4 of 6 vs 4 of 49 patients; P
= .02). Infections in human immunodeficiency virus–positive patients
(n = 4) were not different from those in human immunodeficiency virus–negative
patients with regard to the source of infection, clinical characteristics,
and outcome.
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Table 3. Characteristics of Patients With Mycobacterium
marinum Infection in Whom Treatment Failed*
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The efficacy of antibiotic therapy was evaluated by the number of failures
according to the number of prescriptions and the severity of the infection
(spread to deeper structures). Failure was not related to the prescription
of one specific antibiotic or regimen or to the duration of the treatment
(median, 6 vs 5 months; P = .13).
For infections limited to skin and soft tissue, cure was observed in
42 (93%) of 45 patients, including 20 undergoing monotherapy (16 received
cyclines and 4 received clarithromycin). The 3 patients in whom treatment
failed had received similar antibiotics as those who were cured (Table 3).
For infections spread to deeper structures, treatment with a combination
of 2 antibiotics, among cyclines, clarithromycin, and rifampin, resulted in
cure of most (13 of 18 patients). However, 4 of the 5 patients in whom treatment
failed (patients 4, 5, 6 and 8, detailed in Table 3) were also treated with a combination of clarithromycin
with rifampin, rifabutin, or cyclines for a minimum of 2 months. Of these
4 patients, 3 had received corticosteroids before the diagnosis. Unfortunately,
because we did not record the information on corticosteroid therapy for all
the patients, we could not evaluate it as a risk factor.
ANTIBIOTIC MICs
The MICs were determined for the 11 antibiotics that were given to the
patients (rifampin, rifabutin, ethambutol, amikacin, doxycycline, minocycline,
clarithromycin, and fluoroquinolones [including ofloxacin, levofloxacin, ciprofloxacin,
and sparfloxacin]) against all the strains isolated from the 63 patients but
2 (because of insufficient growth). For each antibiotic, the MICs were distributed
in a narrow range, and the modal MIC was close to the 50% MIC and to the geometric
mean MIC (Table 4). The MICs of
rifampin and rifabutin were lower than the MICs of the other antibiotics (90%
MIC of 0.5 and 0.06 µg/mL, respectively). The MICs of the cyclines,
clarithromycin, amikacin, and ethambutol were moderate values close to 4 µg/mL.
Among the fluoroquinolones, the MICs of sparfloxacin were 2- to 4-fold lower
than the MICs of ciprofloxacin, levofloxacin, and ofloxacin.
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Table 4. Minimum Inhibitory Concentrations of 11 Antibiotics Against
61 Strains of Mycobacterium marinum*
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There was no difference between the geometric mean MICs for strains
isolated from patients who were cured and the geometric mean MICs for strains
isolated from patients in whom treatment had failed (data not shown). Acquired
resistance to an antibiotic was not observed in strains isolated from either
cured patients or patients in whom treatment had failed.
COMMENT
We reported 63 cases of culture-confirmed M marinum infection during a 3-year period. It is, to our knowledge, the largest
series reported in the literature.15-16
Infectious diseases caused by nontuberculous mycobacteria, including M marinum and Mycobacterium ulcerans, that cause skin infections have increased in healthy and in immunocompromised
patients in the past decade and may be considered as emerging infections.17 Infection with M marinum
follows contact with a fish tank or shellfish and results in skin infections
because the M marinum optimal growth temperature
is 30°C.2 The incubation period is difficult
to evaluate because patients with a fish tank in the household might be contaminated
at each cleaning. The median incubation time of 16 days that we report is
not different from that reported by Jernigan and Farr18
(21 days). From the literature, only half of the M marinum cases reported were associated with aquarium exposure,18
in contrast to 53 (84%) of the cases associated with a fish tank in the present
study. Fish tank hobby is obviously the main risk factor for M marinum infection, although the prevalence of infection among fish
tank owners is not known. However, M marinum is rarely
isolated from dead fishes or tank water.19-21
As confirmed by the report of only 1 case in our study, swimming pool–associated
cases are rare because of the implementation of swimming pool water–disinfecting
practices.22
Infection was more frequent in males than in females, as reported in
other studies,23 but in contrast with the study
by Edelstein.3 The clinical presentation in
our patients was relatively similar to that from other studies for the site
and the aspect of the lesions. In most cases, the upper limb was affected,
which is related to fish tank exposure. The most common clinical appearance
was a cutaneous nodule with a frequent sporotrichoid aspect, as reported in
other studies.24 In our survey, the spread
of infection to deeper structures concerned one third of the patients, contrary
to other studies, in which it was rare.3 Because
our study was restricted to culture-confirmed M marinum cases of infection, it is probable that severe cases, which are more
frequently investigated, were reported preferentially. These severe cases
justify the search for the most effective therapy. Spread to deeper structures
(arthritis, tenosynovitis, and osteitis) was more frequent in females than
in males. This might be explained by the prescription of corticosteroids before
the diagnosis, which is common in the case of female rheumatic disease and
might have facilitated the spread of infection.25
Optimal treatment of M marinum infection has
not been established yet. The infection probably resolves spontaneously in
some cases, although complete resolution may take up to 2 years.2, 26
Surgery, cryotherapy, x-ray therapy, electrodesiccation, and different antibiotic
regimens have been reported to cure the infected patients.3
The choice of the therapy seemed to be based more on personal experience and
the preference of individual researchers than on the demonstrated efficacy
of one or another therapy.3 Recent clinical
reports27 suggest that antibiotic therapy alone
is enough to cure most of the patients and that additional surgical debridement
cures the remaining patients.
In our study, all patients were treated with antibiotics. To our knowledge,
no study has compared different antibiotic regimens. In the literature, various
antibiotics have been used, including cyclines, a combination of sulfamethoxazole
and trimethoprim, rifampin plus ethambutol, and, more rarely, clarithromycin,
levofloxacin, and amikacin.3, 23, 28-29
Cure and failure have been described with all of these drugs.23, 29
The optimal duration of therapy also varied markedly in the literature, ranging
from 6 weeks to 1 years.30 In our study,
the duration of therapy ranged from 1 to 25 months (median, 3 months).
This duration was significantly longer for patients with infection spread
to deeper structures, except for the patients in whom treatment failed. In
these latter patients, the duration of treatment was too short.
To draw recommendations for a standardized treatment, we sought to evaluate
the outcome by antibiotic regimens. Fifty-five (87%) of the patients were
cured after therapy that included clarithromycin, rifampin, or cyclines. However,
patients in whom treatment failed were observed among those treated with the
same antibiotics. Consequently, a favorable treatment outcome could not be
related to any specific antibiotic, consistent with the literature review.3, 23, 30
No treatment failure was related to a strain of M
marinum with acquired resistance to any antibiotic. Acquired resistance
has been described in patients with mycobacterial infections only for drugs
with a potent activity, such as streptomycin sulfate in patients with tuberculosis31 or clarithromycin in patients with Mycobacterium avium infection.32 Acquired
resistance has not been described for M marinum yet.
This might indicate that none of the antibiotics given has a potent activity
against M marinum. This is confirmed by the in vitro
susceptibility results of this study, which showed that M marinum has a natural multidrug resistance pattern, as suspected
by the results of other studies.12, 14, 33
Rifamycins, rifampin, and rifabutin are the only antibiotics that have
low MICs and MICs close to those found for Mycobacterium
tuberculosis. However, this was not fully correlated with the in vivo
efficacy because 5 patients (who underwent a total of 5 courses of rifampin
and 2 of rifabutin) in whom treatment failed had received rifamycins with
a long duration of therapy (9, 7, 6, 4, and 4 months). The MICs of minocycline,
doxycycline, clarithromycin, and amikacin were moderate values close to those
reported for other atypical mycobacteria. Comparable values of MICs were observed
for clarithromycin and amikacin against M avium and
for cyclines and amikacin against rapidly growing mycobacteria,34-35
which have been correlated with in vivo efficacy.32, 36
Only 2 treatment failures were observed with cyclines, but most of the patients
treated by cyclines, and especially by cyclines alone, had infection limited
to the skin and soft tissue. The MICs of ethambutol, ciprofloxacin, ofloxacin,
and levofloxacin were far above the concentration break points and, consequently,
in vivo efficacy was less probable. Failure was indeed observed in half of
the patients treated with these antibiotics. The activity of the new fluoroquinolone,
sparfloxacin (even its MICs were lower than those of the classic fluoroquinolones),
has still to be demonstrated; in our study, 3 patients were treated with sparfloxacin,
and treatment failed in 1.
Surgery seemed frequently inadequate to Chow et al.27
In our study, surgery was consistently done for most of the infections spread
to deeper structures but also for 17 (38%) of the 45 patients with infections
limited to skin and soft tissue, without clear benefit (surgery was performed
in 5 of the 8 patients in whom treatment failed) and with unknown adverse
effects. The place of surgery in the treatment of M marinum infection needs to be evaluated with regard to the severity of the
infection.
In upcoming years, the incidence of M marinum
infections might increase,17 as fish tank hobby
and aquarium tourism increase in popularity. In addition to the treatment
evaluation, preventative strategies should be developed for fish tank activity,
such as wearing gloves when cleaning the tank.18
AUTHOR INFORMATION
Accepted for publication November 15, 2001.
This study was supported by University of Paris VI (research group UPRES
EA 1541), association Raoul Follereau, and association Claude Bernard, all
located in Paris, France.
This study was presented in part at the 40th Interscience Conference
on Antimicrobial Agents and Chemotherapy, Toronto, Ontario, September 19,
2000.
This study was organized with the collaboration of the Groupe pour l'Etude
et le Traitement des Infections à Mycobactéries and the Groupe
Azay-Mycobactéries (groups of mycobacteriologists working in university
hospitals) and with clinicians from the dermatology and infectious diseases
departments of university hospitals. Vincent Jarlier, MD, PhD, and Jacques
Grosset, MD, PhD, directors of the NRC, contributed to the design of the study
and provided helpful discussion regarding the results. The following colleagues
collected the data and sent the strains of Mycobacterium marinum
and the information on patients included in the study: X. Gisconti, MD (Albi);
Y. Douadi, MD, P. Esquenet, MD, H. Laurans, MD, C. Lok, MD, J.-L. Schmitt,
MD (Amiens); E. Carpentier, MD, J.-L. Verret, MD (Angers); B. Hautefort, MD
(Arles); C. Boval-Gallet, MD (Bligny); M.-S. Doutre, MD, B. Geniaux, MD, P.
Mouton, MD, J. Texier-Maugein, MD (Bordeaux); M.-L. Abalain, MD (Brest); A.
Dompmartin, MD, M. Fines, MD, B. Malbruny, MD (Caen); M. Drochon, MD (Chateauroux);
F. Goudron, MD, J. Sirot, MD (Clermont Ferrand); E. Hachulla, MD, C. Savage,
MD, J.-M. Bonnet-Blanc, MD (Lille); C. Martin, MD (Limoges); C. Grange-Blanquie,
MD (Marmande); M.-J. Gevaudan, MD (Marseille); J.-F. Cuny, MD, A. Didion,
MD (Metz); P. Canton, MD, M. Dailloux, MD (Nancy); P. Bemer-Melchior, MD (Nantes);
A. Le Coustumier, MD (Neufchateau); F. Guillouët-Salvador, MD (Nice);
A. Gouby, MD, B. Guillot, MD, J. Jourdan, MD (Nimes); B. Cadot, MD (Orsay);
P. Di Maria, MD (Paris); G. Paul, MD, X. Puechal, MD, P. Robin, MD (Paris-Cochin);
M. Bagot, MD, I. Bournerias, MD, L. Desforges, MD, H. Kenesi, MD, P. Wolkenstein,
MD (Paris-Henri Mondor); X. Liote, MD, M.-J. Sanson Le Pors, MD (Paris-Lariboisière);
C. Truffot-Pernot, MD (Paris-Pitié-Salpêtrière); F. Caux,
MD, C. Dumontier, MD, V. Lalande, MD (Paris Saint-Antoine); O. Bajolet-Laudinat,
MD, I. Beguinot, MD, P. Bernard, MD, L. Brasme, MD, A. Strady, MD (Reims);
A. Carricajo, MD, H. Rousset, MD (Saint-Etienne); R. Bauriaud, MD, E. Bonnet,
MD, J. Gallardo, MD, V. Marc, MD, S. Sicard, MD (Toulouse); E. Buy, MD, J.
Unanué, MD (Villeneuve sur Lot).
Corresponding author and reprints: Emmanuelle Cambau, MD, PhD, Bactériologie,
Faculté de médecine Pitié-Salpêtrière, 91
boulevard de l'hôpital, 75634 Paris CEDEX 13, France (e-mail: cambau{at}chups.jussieu.fr).
From the Laboratoire de Bactériologie, Centre National de Référence
pour la Surveillance des Infections à Mycobactéries et de leur
Résistance aux Antituberculeux (Drs Aubry, Robert, and Cambau), and
the Services de Médecine Interne (Dr Chosidow) and Maladies Infectieuses
(Dr Caumes), Groupe Hospitalier Pitié-Salpêtrière, Assistance
Publique-Hôpitaux de Paris, Paris, France.
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