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Previous Article | Next Article 
Antimicrobial Agents and Chemotherapy, November 2000, p. 3133-3136, Vol. 44, No. 11
0066-4804/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Antibiotic Susceptibility Pattern of
Mycobacterium marinum
Alexandra
Aubry,1
Vincent
Jarlier,1
Sylvie
Escolano,2
Chantal
Truffot-Pernot,1 and
Emmanuelle
Cambau1,*
Laboratoire de
Bactériologie-Hygiène et Centre National de
Référence pour la Surveillance des Infections à
Mycobactéries et de leur Résistance aux
Antituberculeux,1 and Unité INSERM
U436,2 Faculté de Médecine
Pitié-Salpêtrière, Paris, France
Received 18 May 2000/Returned for modification 20 July
2000/Accepted 24 August 2000
 |
ABSTRACT |
In vitro activities of 17 antibiotics against 53 clinical strains
of Mycobacterium marinum, an atypical
mycobacterium responsible for cutaneous infections, were determined
using the reference agar dilution method. Rifampin and rifabutin
were the most active drugs (MICs at which 90% of the isolates tested
were inhibited [MIC90s], 0.5 and 0.6 µg/ml,
respectively). MICs of minocycline (MIC90, 4 µg/ml),
doxycycline (MIC90, 16 µg/ml), clarithromycin (MIC90, 4 µg/ml), sparfloxacin (MIC90, 2 µg/ml), moxifloxacin (MIC90, 1 µg/ml), imipenem
(MIC90, 8 µg/ml), sulfamethoxazole (MIC90, 8 µg/ml) and amikacin (MIC90, 4 µg/ml) were close to the susceptibility breakpoints. MICs of isoniazid, ethambutol,
trimethoprim, azithromycin, ciprofloxacin, ofloxacin, and levofloxacin
were above the concentrations usually obtained in vivo. For each drug, the MIC50, geometric mean MIC, and modal MIC were very
close, showing that all the strains had a similar susceptibility
pattern. Percent agreement (within ±1 log2 dilution)
between MICs yielded by the Etest method and by the agar dilution
method used as reference were 83, 59, 43, and 24% for minocycline,
rifampin, clarithromycin, and sparfloxacin, respectively.
Reproducibility with the Etest was low, in contrast to that with the
agar dilution method. In conclusion, M. marinum is a
naturally multidrug-resistant species for which the agar dilution
method is more accurate than the Etest for antibiotic susceptibility testing.
| |
INTRODUCTION |
Mycobacterium marinum is
an atypical photochromogenic mycobacterium belonging to group I of
Runyon's classification (18). This mycobacterium was
successively named M. piscium, M. marinum (1), M. platypoecilus, M. anabanti,
and M. balnei. Comparative sugar fermentative reaction data
together with published morphological, cultural, and pathogenic data
suggested that they were all synonymous with M. marinum
(17). M. marinum inhabits fresh and salt water and causes disease in many fish species and occasionally in humans (24, 28). Human infections are generally limited to
cutaneous diseases and are referred to as "swimming pool granuloma"
and "fish tank granuloma" in reference to the epidemiology and the inoculation mode (24, 28). The frequency of M. marinum in bacteriology laboratories is low, since less than 1%
of the mycobacterial clinical isolates belong to this species
(11). Susceptibility data on M. marinum are
scarce and rely upon the small numbers of strains and antibiotics
tested (20, 23, 25). As a consequence, intrinsic antibiotic
susceptibilities of M. marinum are not well defined, and
methods for their routine determination have not been evaluated.
In this study we looked for the antibiotic susceptibilities of 53 clinical isolates of M. marinum by determining the MICs of 17 antibiotics using the agar dilution method. Antibiotics tested were tetracyclines, rifampin, and cotrimoxazole, which were
reported to be effective for treating M. marinum
infections (8), and antimycobacterial antibiotics
active against Mycobacterium tuberculosis (isoniazid,
rifabutin, ethambutol, and aminoglycosides) or against atypical
mycobacteria (clarithromycin, azithromycin, and imipenem). In
addition, we tested fluoroquinolones, since new derivatives
(levofloxacin, sparfloxacin, and moxifloxacin) appear
particularly active against mycobacteria (15). We
compared the reference (but cumbersome) method used to a more practical and routine method of antibiotic susceptibility testing, the new stable
gradient method known as Etest.
| |
MATERIALS AND METHODS |
Bacterial strains and growth conditions.
The study involved
53 clinical strains of M. marinum that were isolated over a
period of 3 years (1995 to 1997) in bacteriology laboratories located
in all parts of France. These strains were referred to the National
Reference Centre for the Surveillance of Mycobacterial Infections and
their Resistance to Antituberculous Agents (Laboratory of Bacteriology,
Groupe Hospitalier Pitié-Salpêtrière, Paris, France),
working for the present study in collaboration with the
AZAY-Mycobacterium Group of the university hospitals of France. The
strains of M. marinum were identified on the basis of
phenetic characters as described previously (4). Strains were stored at 
80°C in Youmans broth supplemented with 20% fetal bovine serum until the MICs were determined. M. marinum ATCC
927, Mycobacterium smegmatis ATCC 19420 and mc2
155, and Escherichia coli ATCC 25922 were used as controls
for MIC determination. Mycobacteria were grown in Middlebrook 7H9 broth
for 3 to 5 days (2 days for M. smegmatis), and the culture suspension was adjusted with additional sterile distilled water to
equal a McFarland 1.0 turbidity standard (approximately 108
CFU per ml).
Antimicrobial agents.
Rifampin, ofloxacin, and levofloxacin
(Hoechst Marion Roussel, La Défense, France), rifabutin
(Pharmacia & Upjohn, Rueil Malmaison, France), ethambutol (Lederle,
Paris La Défense, France), amikacin (Bristol-Myers Squibb, Paris
La Défense, France), imipenem (Merck Sharp & Dohme Chibret,
Paris, France), minocycline (Wyeth Lederle, La Défense, France),
doxycycline (Elerte, Aubervilliers, France), azithromycin (Pfizer,
Orsay, France), clarithromycin (Abbott, Saint Rémy sur Avre,
France), ciprofloxacin and moxifloxacin (Bayer Pharma, Puteaux,
France), sparfloxacin (Rhône Poulenc Rorer, Vitry sur Seine,
France), and isoniazid, sulfamethoxazole, and trimethoprim (Roche,
Fontenay sous Bois, France) were kindly provided by the manufacturers.
Etest strips containing either rifampin, clarithromycin, sparfloxacin,
or minocycline were obtained from AB Biodisk, BMD, Marne-la-Vallée, France.
Determination of the MICs by the agar dilution method.
The
agar dilution method was performed on Mueller-Hinton agar (Difco,
Serlabo, Bonneuil sur Marne, France) supplemented with 5% Middlebrook
OADC (oleic acid, albumin, dextrose and catalase [OSI, Elancourt,
France]). The 5% (vol/vol) ratio of OADC was found optimal for
M. marinum growth by inoculating in preliminary tests 16 strains in duplicate on Mueller-Hinton agar prepared with 0% OADC
(8 of 16 grew normally), 2.5% (14 of 16 grew normally), 5% (16 of 16 grew normally), and 10% (16 of 16 grew normally).
Twofold dilutions of the antibiotics were added in order to obtain the
following final concentrations: amikacin, 0.25 to 64 µg/ml; imipenem,
0.06 to 32 µg/ml; rifampin, 0.015 to 32 µg/ml; rifabutin, 0.001 to
4 µg/ml; ethambutol, 0.03 to 8 µg/ml; azithromycin, 0.015 to 64 µg/ml; ofloxacin and ciprofloxacin, 0.06 to 128 µg/ml; sparfloxacin, levofloxacin, and moxifloxacin, 0.03 to 128 µg/ml; minocycline, doxycycline, and clarithromycin, 0.06 to 32 µg/ml; sulfamethoxazole and trimethoprim, 1 to 512 µg/ml; and isoniazid, 0.5 to 32 µg/ml. A 1/100 dilution of a McFarland 1.0 turbidity standard
suspension was inoculated with a Steers replicator delivering approximately 104 CFU per spot. Plates were incubated at
30°C in a 5% CO2 incubator. MICs for E. coli
ATCC 25922, M. smegmatis mc2 155, and M. smegmatis ATCC 19420 were determined after 24 and 48 h of
incubation, respectively. MICs for M. marinum strains were
determined after 7 days (i.e., when half of the strains had grown) or
11 days (i.e., when all of the strains had grown) of incubation. The
MIC was defined as the lowest concentration of antibiotic resulting in
complete inhibition of growth or in growth of fewer than 10 colonies
(<1% of the inoculum).
To evaluate the reproducibility with the method, independent tests were
performed for M. marinum ATCC 927 (six tests) and 37 clinical strains (two tests each).
Etest method.
A suspension, equal to a McFarland 1.0 turbidity standard suspension, was applied onto the surface of a 5%
sheep blood Mueller-Hinton agar plate (Sanofi Diagnostic Pasteur; 15 by
15 mm) using a sterile cotton swab. The plate was incubated at 30°C
in 5% CO2 as described above. The MIC was read at the
point where the zone of inhibition intersected the MIC scale on the
strip, taking into account even faint growth as recommended for other
mycobacteria (3, 27).
To evaluate the reproducibility with the method, 10 independent tests
were performed for M. marinum ATCC 927. In addition, Etests
were performed by two distinct operators, one operating under research
conditions and one under routine conditions, for 39 clinical strains.
Result analysis.
The reproducibility was evaluated on the
basis of the MIC differences in log2 dilution between the
tests with the same strain. The reproducibility value was defined as
the percentage of strains which yielded the same MIC within ±1
log2 dilution. The agreement between agar dilution and
Etest methods was the percentage of strains which yielded the same MIC
value within ±1 log2 dilution by the two methods. Category
discrepancies were evaluated using the breakpoints for determining
susceptibility and resistance categories recommended by the NCCLS for
aerobic bacteria (14). A very major interpretive discrepancy
was defined as resistance by the reference agar dilution method and
susceptibility by the Etest method, a major interpretive discrepancy
was defined as resistance by the Etest method and susceptibility by the
agar dilution method, and a minor discrepancy was defined as
intermediate susceptibility by one method and susceptibility or
resistance by the other method.
| |
RESULTS |
Agar dilution method.
The reproducibility of results with the
agar dilution method was good (>80% agreement) for all antibiotics
except for sulfamethoxazole (<50% reproducibility). The MIC results
are presented in detail in Table 1. MICs
of rifampin and rifabutin (MICs at which 90% of the isolates were
inhibited [MIC90s], 0.5 and 0.06 µg/ml, respectively) were far lower than those of other antibiotics. The MIC90s
of minocycline (4 µg/ml), doxycycline (16 µg/ml),
clarithromycin (4 µg/ml), imipenem (8 µg/ml), and
amikacin (4 µg/ml) were close to the breakpoints. MICs of isoniazid
(MIC90, 8 µg/ml), ethambutol (MIC90, 4 µg/ml), trimethoprim (MIC90, 128 µg/ml), and
azithromycin (MIC90, 128 µg/ml) were above the
breakpoints. Among the fluoroquinolones tested, MICs of sparfloxacin
(MIC90, 2 µg/ml) and moxifloxacin (MIC90, 1 µg/ml) were four- to eightfold lower than those of ciprofloxacin (MIC90, 8 µg/ml), ofloxacin (MIC90, 16 µg/ml), and levofloxacin (MIC90, 8 µg/ml). For each
antibiotic, the MICs were distributed in a narrow range (see the
examples of doxycycline and moxifloxacin in Fig.
1) with an overall standard deviation
comprised of between 1.5 and 2.6 log2 dilution. As a
consequence, modal MICs were equal to or within 1 log2
dilution of MIC50s and were close to geometric mean MICs
(Table 1). The MICs for the reference strain, ATCC 927, were within 0 to 1 dilutions of the modal MIC for 53 clinical strains.
Etest method.
We determined by Etest the MICs of rifampin,
clarithromycin, minocycline, and sparfloxacin, which were the most
active drugs against M. marinum as determined by the agar
dilution method and for which Etest strips were available. For these
four antibiotics, the ellipse inhibition zone was clear, without
trailing growth, and thus reading the MIC was not ambiguous. The
reproducibility with the Etest method for the reference strain was
100% in the case of minocycline (10 out of the 10 tests yielded the
same MICs ±1 log2) and 70% for rifampin and
clarithromycin but only 40% for sparfloxacin. The results of duplicate
tests performed by independent operators are detailed in Table
2. Again, reproducibility of results was
high for minocycline (83%), low for clarithromycin and rifampin (48%
and 46%, respectively), and very low for sparfloxacin (21%).
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TABLE 2.
Reproducibility of results with the Etest as evaluated by
the determination of MICs by two different operators for 39 clinical strains of Mycobacterium marinum
|
|
The percentages of agreement between the MICs yielded by Etest and
those yielded by agar dilution are shown in Table
3. Etest MICs were in good agreement with
agar dilution MICs for minocycline only (83% agreement). Agreement was
lower for rifampin (59%), sparfloxacin (43%), and clarithromycin
(24%). When agar dilution and Etest MICs were converted into
interpretative categories using NCCLS breakpoints, there was about 90%
agreement for rifampin, minocycline, and clarithromycin and 58%
agreement for sparfloxacin (Table 4). No
very major discrepancy and very few major discrepancies were observed
for clarithromycin, although Etest regularly underestimated by 2 to 3 dilutions the MIC of this drug. In the case of sparfloxacin, Etest
tended to overestimate or at the opposite to underestimate the MICs by
2 to 3 dilutions. Since sparfloxacin MICs were close to the
susceptibility breakpoint for most of the strains, this led to minor
(28%) or in some cases major (15%) discrepancies.
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TABLE 4.
Distribution of category discrepancies by a comparison of
Etest results to agar dilution results for 54 strains of M.
marinum
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| |
DISCUSSION |
Our primary objective was the determination of in vitro
susceptibilities of M. marinum, since published studies on
antibiotic susceptibility are scarce, involving 10 to 20 strains per
study. Moreover, very few data are available on new
antimycobacterial agents, such as new macrolides, imipenem,
and fluoroquinolones (19). To date no method has been
recommended as the standard for determining the in vitro susceptibility
of M. marinum. In some studies, the methods used were those
designed for slowly growing mycobacteria, such as the proportion method
on solid media and in BACTEC liquid media (10). In contrast,
in other studies, the methods used for antibiotic susceptibility
testing of M. marinum were those designed for rapidly
growing mycobacteria, such as broth microdilution (14), disk
diffusion, agar disk elution (22), or agar dilution using a
Steers replicator (20, 25). M. marinum grows
rapidly enough, indeed, to be tested by the method used for rapidly
growing mycobacteria, despite the fact that it belongs to the slowly
growing mycobacteria on the basis on genetic and mycolic acid analysis
(5, 21). We confirmed the rapid growth of M. marinum and showed that its growth required a lower level of OADC
supplementation than is required for other slowly growing mycobacteria.
Consequently, we used as a reference the agar dilution method using a
Steers replicator (25) for its convenience and because of
the large worldwide experience of this method of testing antibiotic
activity that has been acquired with nonfastidious organisms.
The present study allowed us to delineate the susceptibility pattern of
M. marinum towards antituberculous drugs and new drugs which
have been shown to be active against other antimycobacterial species.
Clearly, M. marinum is susceptible to rifampin, rifabutin, and amikacin but resistant to isoniazid and ethambutol. With regard to
susceptibilities to fluoroquinolones, on one hand M. marinum is resistant to ofloxacin, ciprofloxacin, and
levofloxacin, and on the other hand the majority of the strains were
susceptible to moxifloxacin and sparfloxacin (MIC50 and
geometric mean MIC, 0.5 and 1 µg/ml, respectively). As described
previously for M. tuberculosis and atypical mycobacteria
(12), fluoroquinolones were arranged from that with the
lowest MIC to that with the highest MIC as follows: moxifloxacin,
sparfloxacin, levofloxacin, ciprofloxacin, and ofloxacin. The
results also confirmed the moderate susceptibility of M. marinum to tetracyclines (20, 23, 25) and the higher activity of minocycline than of doxycycline (MICs being constantly twofold lower). A majority of strains were susceptible to
clarithromycin, to sulfamethoxazole, and to imipenem, but modal
MICs of these drugs were close to the breakpoints. Finally,
M. marinum was found to be resistant to
azithromycin and to trimethoprim.
The geometric mean MIC, the modal MIC, and the MIC50 for
each antibiotic taken separately were close, and the geometric standard deviations were very low (Table 1), strongly suggesting a homogeneous susceptibility pattern for the M. marinum species. This
fact was confirmed by the narrow MIC distribution for each
antibiotic, as shown for doxycycline and moxifloxacin in Fig. 1.
The susceptibility pattern of M. marinum described herein
likely corresponds to the wild-type susceptibility pattern. Until now,
no relapse due to the selection of a resistant mutant has been
reported, and acquired resistance is not known for M. marinum.
Therefore, on the basis of in vitro susceptibilities, candidates for
treatment of M. marinum can be chosen. Cases of success have
seldom been reported after treatment of M. marinum
infections by rifampin (7, 8), and MICs of the rifamycins
and rifampin and rifabutin are indeed the lowest and are close to those
found for M. tuberculosis. Minocycline and to a lesser
extent doxycycline, clarithromycin, imipenem, and amikacin are serious
candidates for the treatment of M. marinum infections, since
their MICs are in the range of blood levels. Moreover, these MICs are
close to those found for other atypical mycobacteria, such as M. avium, and rapidly growing mycobacteria, for which in vitro
activity has been correlated with in vivo efficacy (6, 26).
The activities of sparfloxacin and moxifloxacin, even if higher than
those of other fluoroquinolones, remained lower than those against
M. tuberculosis, and thus in vivo efficacy should be
carefully assessed. Pharmacokinetic considerations might also influence
the therapeutic value of the antibiotics. However, all the antibiotics
with good in vitro activity cited above also have a very high
intracellular penetration and extravascular distribution.
Our second objective was the evaluation of a routine method for
susceptibility testing of M. marinum. Etest has been
demonstrated to be an accurate and precise method of MIC determination
for bacteria other than mycobacteria (2). The results
yielded by the Etest method were shown to agree with those yielded by
the agar dilution method for rapidly growing and some slowly growing mycobacterial species (3, 9, 13, 16, 27). In the present study on M. marinum, the level of agreement between results
for Etest and those for agar dilution was high only for minocycline (83% agreement) but in contrast was low for rifampin,
sparfloxacin, and clarithromycin. The low agreement rates found for
M. marinum were not expected, since more than 70% agreement
was reported between results for Etest and those for agar dilution for
M. fortuitum and M. chelonae
(3) and for M. avium (16), and Etest
MICs determined in the present study were close to those reported by Flynn et al. (9). If reproducibility of results with the
Etest was excellent for minocycline, it was poor for
clarithromycin, rifampin, and sparfloxacin. Consequently, we
cannot recommend the Etest method for antibiotic susceptibility
testing of M. marinum. Nevertheless, no acquired resistance
has been described so far, and routine susceptibility testing seems
unnecessary except for relapse cases, as for other atypical
mycobacteria (24).
In conclusion, we described the wild-type susceptibility pattern of
M. marinum for 17 antibiotics. Among these antibiotics, rifampin, rifabutin, tetracyclines (particularly minocycline), amikacin, imipenem, and clarithromycin are good candidates for testing
in vivo efficacy.
| |
ACKNOWLEDGMENTS |
We thank for their technical assistance Pascale Bonafous,
Claudine Wichlacz, Lysiane Jeanson, Murielle Renard, and Michel Szpytma. We also thank Jacques Grosset and Nacer Lounis for their helpful advice. The protocol was defined with the collaboration of
Olivier Chosidow (Service de Medecine Interne, Hôpital
Pitié-Salpêtrière) and Eric Caumes (Service de
Maladies Infectieuses, Hôpital
Pitié-Salpêtrière). The study was organized with the
collaboration of the members of the AZAY-Mycobacterium Group (a group
of mycobacteriologists working in university hospitals). The following
laboratories (and microbiologists) kindly sent the strains of M. marinum included in the study: CHU Amiens (H. Laurans), CHU Angers
(E. Carpentier), CHG Arles (B. Hautefort), Centre Medico-chirurgical de
Bligny (C. Boval-Gallet), CHU Brest (M. L. Abalain), CHU Caen (M. Fines and B. Malbruny), Laboratoire Lescaroux Chateauroux (M. Drochon), CHU Clermont Ferrand (J. Sirot), CHU Lille (C. Savage), CHU Limoges (C. Martin), CHG Nancy (A. Didion), CHU Nice (A. Gouby), CHU Paris-Cochin (G. Paul), CHU Paris-Henri Mondor (L. Desforges), CHU
Paris-Pitié-Salpêtrière, CHU Reims (O. Bajolet-Laudinat), CHU Saint Etienne (A. Carricajo), and CHU Toulouse
(R. Bauriaud).
This work was supported by a grant from Association Claude Bernard.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Faculté de
Médecine Pitié-Salpêtrière, 91, Boulevard de
l'Hôpital, 75634 Paris Cedex 13, France. Phone: (33) 1 40 77 97 46. Fax: (33) 1 45 82 75 77. E-mail:
cambau{at}chups.jussieu.fr.
| |
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Antimicrobial Agents and Chemotherapy, November 2000, p. 3133-3136, Vol. 44, No. 11
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Copyright © 2000, American Society for Microbiology. All rights reserved.
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Abstract
Introduction
