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Journal of Clinical Microbiology, March 1999, p. 729-733, Vol. 37, No. 3
Service de
Bactériologie-Virologie-Hygiène,
Received 15 July 1998/Returned for modification 31 August
1998/Accepted 5 November 1998
Lactobacilli recovered from the blood, cerebrospinal fluid,
respiratory tract, and gut of 20 hospitalized immunocompromised septic
patients were analyzed. Biochemical carbohydrate fermentation and total
soluble cell protein profiles were used to identify the species.
Hydrogen peroxide production was measured. Susceptibility to 19 antibiotics was tested by a diffusion method, and the MICs of
benzylpenicillin, amoxicillin, imipenem, erythromycin, vancomycin, gentamicin, and levofloxacin were determined. A small number of species
produced H2O2, and antibiotic susceptibilities
were species related. Eighteen (90%) of the isolates were
L. rhamnosus, one was L. paracasei subsp. paracasei, and one was L. crispatus. L. rhamnosus, L. paracasei subsp. paracasei isolates, and the
type strains were neither H2O2 producers nor
vancomycin susceptible (MICs, Lactobacilli are ubiquitous and
widespread commensal bacteria in the human and animal microflora. They
are widely used by humans: as adjuvants against gastrointestinal
disorders, as dietary supplements, and as biological food processors in
view of their fermentative properties (1, 15).
Severe lactobacillus infections occur as endocarditis in patients with
valve defects and as local or disseminated infections in neutropenic
patients with sepsis receiving broad-spectrum antibiotics. The
conditions of the patients in the latter group are usually leukemia
with chemotherapy, an immunocompromised state due to organ
transplantation, or AIDS (1, 2, 5, 13, 15, 22, 23, 25, 31).
The current widespread use of glycopeptides and broad-spectrum
cephalosporins for the management of sepsis may increase the rate of
occurrence of lactobacillus infections among immunocompromised patients
(5, 13).
Recent phylogenetic analyses have resulted in taxonomic changes in this
genus (6, 26, 30, 34, 36). For example, in 1989, Lactobacillus casei subsp. rhamnosus was
elevated to species status as L. rhamnosus sp.
nov., and all other members of the L. casei subspecies
except L. casei subsp. casei were grouped in
a separate species, L. paracasei sp. nov.
(7). Further changes are under way (9, 10, 30).
Since 1980, the members of the L. acidophilus group have been divided into two
subgroups, the L. acidophilus subgroup and
the L. gasseri subgroup, and the two subgroups are
divided into six species (14, 24).
Identification of Lactobacillus species to the species level
is not possible on a routine basis. Commercially available carbohydrate fermentation tests fail to identify various Lactobacillus
species. However, highly standardized whole-cell protein patterns
obtained by sodium dodecyl sulfate-polyacrylamide gel electrophoresis
(SDS-PAGE) have proved useful for Lactobacillus species
identification (27, 32). The potential value of other tests,
such as hybridization with oligonucleotide probes, is under
investigation (32).
Few studies of lactobacilli from normal and diseased vaginal and
intestinal mucosae report the species involved (11, 29). In
vitro H2O2 production by lactobacilli from the
vaginal microflora has recently been surveyed.
H2O2-producing lactobacilli predominate in the
normal vagina but are seldom found in the vaginas of patients with
bacterial vaginosis (11). H2O2 is
known to inhibit the growth of some bacteria and may be involved in the
control of the normal microflora.
Vancomycin and teicoplanin are active against most gram-positive
bacteria. However, various species (L. rhamnosus, L. casei, and
L. plantarum) are intrinsically resistant to
glycopeptides (21, 35). In contrast, most of the
lactobacilli from the vaginal flora that we have tested were
susceptible to these antibiotics (unpublished data). Our aim was to
characterize the lactobacilli isolated from 20 patients with sepsis.
The clinical status, carbohydrate fermentation profiles, whole-cell
protein patterns, ability to produce H2O2, and
antibiotic susceptibilities of the strains were analyzed.
Patients and controls.
The 20 patients were
immunocompromised adults and children hospitalized in St-Louis Hospital
between 1993 and 1995 (Table 1).
Strains.
Lactobacilli were isolated from diverse samples
taken in the course of the biological management of sepsis and were
then stored at Type strains.
The following CIP type strains were tested in
parallel as references: L. rhamnosus CIP A
157T, L. paracasei subsp.
paracasei CIP 103918T, and L. jensenii CIP 69.17T. The following six strains of the
L. acidophilus group were tested in
parallel as references: four strains from the L. acidophilus subgroup (L. acidophilus CIP 76.13T, L. crispatus CIP 102990T, L. gallinarum
CIP 103611T, and L. amylovorus CIP
102989T) and two strains from the L. gasseri subgroup (L. gasseri CIP 102991T and L. johnsonii CIP
103620T).
Fermentation profile.
The API 50 CH test kit and API CHL
medium (bioMérieux, La Balme les Grottes, France) were used to
test the abilities of the strains to ferment 49 carbohydrates. An 18-h
culture in de Man-Rogosa-Sharpe (MRS) broth was centrifuged, and 200 µl of the sediment was introduced into API CHL medium. These samples
were then tested with the API strips according to the manufacturer's
instructions, the top of the cupule was covered with mineral oil, and
the results were read after 24 h of incubation at 37°C under
aerobic conditions.
0095-1137/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Lactobacillus Species Identification,
H2O2 Production, and Antibiotic Resistance and
Correlation with Human Clinical Status
ABSTRACT
Top
Abstract
Introduction
Materials and methods
Results
Discussion
References
256 µg/ml). L. crispatus, as well as most of the type strains of lactobacilli
which belong to the L. acidophilus group, was an
H2O2 producer and vancomycin susceptible (MICs,
<4 µg/ml).
INTRODUCTION
Top
Abstract
Introduction
Materials and methods
Results
Discussion
References
MATERIALS AND METHODS
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Abstract
Introduction
Materials and methods
Results
Discussion
References
TABLE 1.
Characteristics of 20 immunocompromised patients infected
with a Lactobacillus
80°C in the laboratory and freeze-dried in the
Bacterial Strains Collection at the Institute Pasteur (CIP). No strain
was an obligate anaerobe.
Whole-cell protein profile. An 18-h culture on an MRS agar slope was harvested, and the proteins were extracted by disruption with glass microbeads. The samples were then subjected to gel electrophoresis (SDS-PAGE) and the proteins in the gel were stained with Coomassie blue.
Computerized normalization of densitometric scans of the gels and numerical analysis were done as described by Kersters and De Ley (27). Clusters were identified by unweighted average pair group method analysis with Gelcompar software (Applied Maths, Ghent, Belgium). The similarities between the protein patterns of the isolates and the type strains were scored as the Pearson product moment correlation coefficient. In agreement with previous assays, isolates and type strains with more than 82% similarity were clustered, and their assignment to the same species or the same L. acidophilus subgroup was considered (10, 28, 32).H2O2 production. According to the qualitative method of Eschenbach et al. (11) lactobacilli were streaked onto a 20-ml MRS agar plate containing 5 mg of 3,3',5,5'-tetramethylbenzidine (TMB; T2885; Sigma), a benzidine-like chromogenic substrate of peroxidase, and 0.20 mg of horseradish peroxidase (P6782; Sigma) (11). Peroxidase generates O2 from any H2O2 produced by the lactobacilli, and the TMB stains the colonies blue in the presence of O2. After 48 h of incubation under 5% CO2 in air, colonies that produce H2O2 on MRS agar thus appear dark blue. Nonproducers are colorless. The media were used within 48 h after preparation. All strains were tested twice. The Lactobacillus type strains were used as quality controls.
Agar diffusion method for determination of antibiotic susceptibility patterns. Nineteen antibiotics were tested: benzylpenicillin, amoxicillin, cephalothin, streptomycin (10 IU), kanamycin (30 IU), gentamicin (10 IU), vancomycin, teicoplain, erythromycin, azithromycin, pristinamycin, lincomycin, rifampin, tetracycline, chloramphenicol, pefloxacin, sparfloxacin, fosfomycin, and fusidic acid (disks; Sanofi Diagnostics Pasteur, Marnes la Coquette, France). The instructions of the Comité Français de l'Antibiogramme related to streptococci were followed (34a).
Fifty microliters of the pellet of an overnight culture was diluted in MRS broth to about 107 CFU/ml. Mueller-Hinton agar plates containing 5% sheep blood (bioMérieux, Marcy l'Etoile, France) were flooded with this suspension in order to give confluent colonies and air dried for 15 min, and the disks impregnated with antibiotics were positioned on the plates. After 36 h of incubation at 37°C in air containing 5% CO2, the diameters of the bacteria-free zones were measured.MICs. Benzylpenicillin, amoxicillin, imipenem, gentamicin, erythromycin, vancomycin, and levofloxacin MICs were tested by the E-test method (Biomedical Diagnostics, Marne La Vallée, France). The inoculum, agar plates, and incubation conditions for the MIC determinations were as described above for the susceptibility assay. A large, 12-cm square Mueller-Hinton agar plate was flooded with this suspension, air dried for 15 min, and overlaid with the seven E-test antibiotic strips. After 36 h of incubation at 37°C in air containing 5% CO2, the elliptical zones of growth inhibition were examined and the MICs were interpreted as the value on the E-test strip scale where the inhibition zone intersected the edge of the strip. Staphylococcus aureus ATCC 25923 was tested simultaneously on Mueller-Hinton agar, with an overnight culture diluted in Mueller-Hinton broth.
Both MICs and susceptibility patterns were determined for benzylpenicillin, amoxicillin, vancomycin, gentamicin, and erythromycin. Only the MICs of imipenem and levofloxacin were measured.| |
RESULTS |
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Abstract
Introduction
Materials and methods
Results
Discussion
References
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Patients. The 20 patients (15 males and 5 females; age range, 2 to 80 years; median age, 27 years) had severe underlying conditions, as indicated in Table 1. Seven patients had undergone autologous, homologous bone marrow or cord blood transplantation, one had undergone a kidney transplantation, seven were receiving antimitotic chemotherapy, two had septic shock, and two had AIDS (Table 1). Eighteen patients were granulocytopenic. Sixteen patients were treated with several systemic antibiotics, and nine were treated with oral antibiotics.
Lactobacilli were isolated from the blood of 12 patients: 7 with persistent lactobacillus septicemia (a lactobacillus was also isolated from cerebrospinal fluid samples from one of these patients) and 5 for whom only one blood sample was cultured. Lactobacilli were isolated from the respiratory tracts of two patients and from the stools or throats of six patients during treatment for total bacterial decontamination. Antibiotic regimens were designed according to lactobacillus susceptibility in vitro. Four patients died over the next few days, and one had a lactobacillemia relapse.Carbohydrate fermentation.
Table
2 summarizes the results of the API CH 50 test.
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Cluster analysis of whole-cell protein profiles. The results of cluster analysis of the protein profiles of the strains from patients and the type strains are presented in Fig. 1.
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H2O2 production by lactobacilli. The findings from studies of H2O2 production by the lactobacilli tested are presented in Table 2.
Only one isolate, isolate 1294, either L. crispatus or L. gasseri, generated H2O2. Among the type strains studied, the only H2O2 producers were the members of the L. acidophilus group, but not L. acidophilusT itself, and L. jenseniiT (data not shown).Antibiotic susceptibility patterns determined by disc diffusion method. The mean diameters of the zones of inhibition (± standard deviations) were as follows: amoxicillin, 22.5 (± 6.4) mm; streptomycin, 12.1 (± 5.4) mm; kanamycin, 10.1 (±5.3) mm; gentamicin, 17.6 (±5.6) mm; erythromycin, 31.0 (±7.8) mm; azithromycin, 27.4 (±8.2) mm; pristinamycin, 27.7 (±5.5) mm; lincomycin, 22.6 (±10.5) mm; rifampin, 30.2 (±10) mm; tetracycline, 24.0 (±3) mm; and chloramphenicol, 23.0 (±4.8) mm. Fosfomycin and fusidic acid did not give inhibition zones for any strain tested. These results were similar to those for members of the normal vaginal flora studied simultaneously (data not shown).
For the strains from patients, the mean diameter of the zone of inhibition (±standard deviation) were as follows: benzylpenicillin, 22.5 (±6.4) mm; cephalothin, 13.4 (±9) mm; and vancomycin, no growth inhibition except for the strain from one patient (strain 1294). The diameters of the zones of inhibition for these antibiotics were significantly larger with normal vaginal lactobacillus. The findings for teicoplanin were similar to those for vancomycin. Among the quinolones, the mean (± standard deviation) diameter-for pefloxacin was 12.7 (±4) mm, and that for sparfloxacin was 24.3 (±5.2) mm. Both of these diameters are significantly larger than those found for normal vaginal lactobacilli (data not shown).MIC results.
The ranges of the MICs of benzylpenicillin,
imipenem, and vancomycin were narrow: the MICs at which 50 and
90% of strains are inhibited were 0.5 and 2 µg/ml,
respectively, for benzylpenicillin, 1 and 2 µg/ml, respectively,
for imipenem, and 256 and 256 µg/ml, respectively, for
vancomycin. For 19 (95%) isolates, all 18 L. rhamnosus strains and 1 L. paracasei
strain), vancomycin MICs were 256 µg/ml.
256 µg/ml, and the MICs for the L. acidophilus group were
2 µg/ml. The MICs of levofloxacin for L. rhamnosus and L. paracasei subsp.
paracasei were 4 µg/ml, and those for the
L. acidophilus group were all 32
µg/ml.
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DISCUSSION |
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Abstract
Introduction
Materials and methods
Results
Discussion
References
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The prevalence of L. rhamnosus in patients (up to 90%) is consistent with recent reports of disseminated lactobacillus infections in immunocompromised hosts (5, 15, 22, 25, 33). Our patients had severe underlying conditions (acute leukemia, neoplasia, organ transplantation, or AIDS) and received various systemic and oral antibiotics, including glycopeptides for 13 of them (65%) (Table 1).
Both fermentation profiles and protein profiles were reliable for the identification to the species level of all the isolates except the isolate belonging to the L. acidophilus group (Table 2; Fig. 1).
H2O2 was produced by one isolate, either L. crispatus or L. gasseri, by five of the six type strains of the L. acidophilus group, and by L. jenseniiT (Table 2). It was also produced by 80% of the normal vaginal isolates that we studied simultaneously (data not shown), in agreement with previous data (11).
The disk diffusion method and the E test gave concordant results. However, previous studies of cephalosporins determined that the MICs were much higher by the E test than by the dilution method with agar (8, 20).
The median MICs of benzylpenicillin and amoxicillin for L. rhamnosus and L. paracasei subsp. paracasei were two times higher than those for the L. acidophilus group, and those of imipenem were four times higher (Table 3).
The MICs at which 90% of strains are inhibited for erythromycin and gentamicin were similar for all lactobacilli (0.06 and 4 µg/ml, respectively) (Table 3). A synergistic bactericidal effect between the penicillins and gentamicin has been demonstrated previously (3, 16).
The MICs of vancomycin are species related: the MICs for L. rhamnosus and L. paracasei subsp.
paracasei were 256 µg/ml, whereas those for the
L. acidophilus group were 2 µg/ml
(Table 3). L. caseiT and L. rhamnosusT have cell wall peptigoglycan
precursors that end in a depsipeptide D-alanine-D-lactate instead of the dipeptide
D-alanine-D-alanine, the target for vancomycin
activity (4, 18).
The activities of the oral antibiotics used for the treatment of urinary tract infections were assessed with lactobacilli. The high levels of resistance to fosfomycin, norfloxacin, ofloxacin, and ciprofloxacin have been described before (17, 20). L. rhamnosus had low-level resistance to pefloxacin and sparfloxacin and was susceptible to levofloxacin. These are the first tests of the in vitro susceptibility of L. rhamnosus to levofloxacin to be published: the low levofloxacin MICs for L. rhamnosus are in contrast to the high-level resistance of the L. acidophilus group (Table 3). Most studies of the antibiotic susceptibilities of lactobacilli do not report on those for the Lactobacillus species. Thus, our results might help in the determination of the antibiotic susceptibilities of the Lactobacillus species.
Sixty-five percent of our patients were on oral or parenteral glycopeptides (Table 1). In studies of oral glycopeptide treatment human volunteers had increased levels of fecal carriage of vancomycin-resistant enterococci and lactobacilli (37). The pathogenicity of L. rhamnosus selected by the use of glycopeptides may be due to many factors such as its exploitation of mucosal defects and its colonization properties. Seventy-five percent of our patients had digestive tract mucosal alterations as a consequence of various conditions: mucositis following antimitotic chemotherapy, digestive graft-versus-host disease after bone marrow transplantation, protracted diarrhea with AIDS, septic shock, or gut carcinoma (Table 1). In liver transplant patients, biliary anastomosis is an independent risk factor for lactobacillus bacteremia (31). Platelet aggregation and endothelial cell binding have been demonstrated with L. rhamnosus strains responsible for endocarditis (19).
The L. rhamnosus isolates from patients with clinical infections and milk products studied by Klein et al. (28) were unrelated according to their total soluble protein patterns. The comparison of L. rhamnosus isolates from patients with bacteremia and of the probiotic strain of L. rhamnosus GG performed by Saxelin et al. (33) showed various fermentation patterns. Our L. rhamnosus isolates belonged to various clusters according to their randomly amplified polymorphic DNA patterns (12).
Every lactobacillus isolate from immunocompromised patients with sepsis was identified to the species level according to its fermentation profile (Table 2). However, in a simultaneous study of normal vaginal isolates, fermentation profiles gave no identification for 40% of the isolates, and determination of the whole-cell protein pattern was necessary for their identification (data not shown).
The prevalence of the various Lactobacillus species is significantly different in immunocompromised patients with disseminated infections and the normal vaginal microflora (data not shown). H2O2 production and glycopeptide MICs are species related: H2O2 production and susceptibility to glycopeptides are common characteristics of the L. acidophilus group. These characteristics are not found in L. rhamnosus or L. paracasei subsp. paracasei. Identification of Lactobacillus species to the species level will help to elucidate the conditions for the emergence of infections by different species and will prompt study into species-related properties.
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FOOTNOTES |
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* Corresponding author. Mailing address: Service de Microbiologie, Hôpital Saint-Louis, 1 avenue Vellefaux, 75475 Paris Cedex 10, France. Phone: 33 1 42 49 93 48. Fax: 33 1 42 49 92 00.
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REFERENCES |
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Abstract
Introduction
Materials and methods
Results
Discussion
References
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Journal of Clinical Microbiology, March 1999, p. 729-733, Vol. 37, No. 3
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