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Journal of Clinical Microbiology, February 2000, p. 931-934, Vol. 38, No. 2
0095-1137/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Bacteremia Caused by a Strain of
Desulfovibrio Related to the Provisionally Named
Desulfovibrio fairfieldensis
Julien
Loubinoux,1
Francine
Mory,2
Ines A. C.
Pereira,3 and
Alain E.
Le Faou1,*
UMR UHP-CNRS 7565, Laboratoire de
Bactériologie-Virologie, Faculté de Médecine de
Nancy, 54505 Vandoeuvre-lès-Nancy Cedex,1
and Laboratoire de Bactériologie, Hôpital Central,
CHU de Nancy, 54035 Nancy Cedex,2 France, and
Instituto de Tecnologia Quimica e Biologica, Universidade Nova
de Lisboa, 2780-156 Oeiras, Portugal3
Received 5 August 1999/Returned for modification 22 September
1999/Accepted 19 November 1999
 |
ABSTRACT |
Eight isolates of Desulfovibrio spp. have been obtained
over 5 years from abdominal or brain abscesses or blood. In seven patients these strains were part of a mixed flora. One strain was
isolated in pure culture from the blood of a patient with peritonitis
of appendicular origin. According to the 16S rRNA gene sequences, this
strain was close to Desulfovibrio fairfieldensis. The
present report describes the fourth isolate of this recently described
species to be isolated in pure culture or as a predominant part of the
flora and to be associated with infectious processes. Thus, D. fairfieldensis may possess a higher pathogenic potential than
other Desulfovibrio species.
| |
CASE REPORT |
A 23-year-old man with gastric ulcer antecedents consulted his
practitioner for an epigastric pain, which was suspected of being of
gastric origin. On the following day, exacerbation of symptoms
necessitated hospitalization at the hospital of Saint-Avold (Lorraine
region, France). Leukocytosis and abdominal tenderness, which was
accentuated in the right iliac fossa, suggested a diagnosis of
perforating appendicitis. This was confirmed by surgery, which consisted of appendix removal and peritoneal lavage. Abdominal drainage
and empirical intravenous antibiotic therapy with cefamandole (1.5 g
per day) and metronidazole (1 g per day) permitted a full recovery.
Peritoneal fluid examined by routine bacteriological methods remained
sterile. An anaerobic culture of blood obtained at the time of
admission was positive and was sent to the Laboratory of Bacteriology
of the University Hospital of Nancy for identification of the bacterium.
Bacteriological investigations.
Blood samples were inoculated
in anaerobic blood culture vials (Vital; bioMérieux, Marcy
l'Etoile, France). Subcultures were performed on Wilkins-Chalgren
anaerobic agar at 37°C in an anaerobic chamber. Pinpoint, round,
smooth, nonhemolytic, and greyish colonies were observed after 5 days
of incubation. Gram staining of the colony showed curved gram-negative
rods. The organism was motile and asaccharolytic and tested positive in
catalase reactions but negative in oxidase, nitrate reduction, and
urease reactions. It produced H2S from sulfate. The
desulfoviridin test was positive. Growth was detected only under
anaerobic conditions at 25, 37, and 42°C. Thus, this bacterium
possessed the phenotypic properties of Desulfovibrio spp.
(16, 19).
Antibiotic susceptibility was determined by the agar dilution method
with Wilkins-Chalgren medium. Because of the slow growth of this
organism, MICs were determined after 96 h of anaerobic incubation
at 37°C (13). MIC results were interpreted with reference to the guidelines of the National Committee for Clinical Laboratory Standards. They indicated that the isolate was resistant to penicillin G (32 µg/ml), amoxicillin (32 µg/ml), amoxicillin-clavulanate (16 µg/ml), ticarcillin (256 µg/ml), ticarcillin-clavulanate (256 µg/ml), piperacillin (>256 µg/ml), piperacillin-tazobactam (>256 µg/ml), cefoxitin (>256 µg/ml), cefotetan (64 µg/ml), and
cefotaxime (256 µg/ml). It was sensitive to metronidazole (0.25 µg/ml), imipenem (0.5 µg/ml), and clindamycin (0.5 µg/ml).
To obtain a more precise identification of this bacterium, the complete
16S rRNA gene (16S rDNA) sequence of the isolate was
determined as
described previously (
13,
17). The 16S rDNA
sequences of the
reference strains
Desulfovibrio desulfuricans Essex 6 (type
strain, ATCC 29577; isolated from soil),
D. desulfuricans MB
(ATCC 27774; isolated from sheep rumen), and
Desulfomonas
pigra (type strain, ATCC 29098; isolated from human feces) were
also
determined for comparison. Briefly, DNA extracts were obtained
from 500 µl of bacterial suspension in TE buffer (10 mM Tris-HCl,
1 mM EDTA [pH 8]) by the standard phenol-chloroform-isoamyl alcohol
method. The 16S rDNA (about 1,500 nucleotides) was amplified by
PCR
with the consensus terminal primers 27f and 1525r (
17).
PCR
products were purified with the Wizard PCR Preps DNA Purification
System (Promega Corp., Madison, Wis.) according to the manufacturer's
instructions. 16S rDNA sequencing was performed in an automated
DNA
sequencer (model 373A DNA sequencer; Applied Biosystems Inc.,
Foster
City, Calif.) by the dye-labeled dideoxy chain-termination
method (Dye
Terminator Cycle Sequencing Ready Reaction Kit; Applied
Biosystems
Inc.) with terminal and internal primers specific for
16S rDNA
(
17). However, the 900r consensus primer was unable
to
amplify a DNA segment and was then modified according to the
D. desulfuricans MB sequence (GenBank accession no.
M34113).
A total
of 1,542 continuous nucleotides of 16S rDNA were determined,
and these
corresponded to
Escherichia coli 16S rDNA sequence positions
8 to 1540 (
2). The complete 16S rDNA sequence of the
clinical
isolate was compared to all bacterial sequences available from
the GenBank database by using the Blast, version 2.0, program
(National
Center for Biotechnology Institute) and showed 99.9%
similarity
(corresponding to 2 nucleotide differences) to that
of
Desulfovibrio fairfieldensis (GenBank accession no.
U42221).
The sequence of reference strain
D. desulfuricans MB had
97.2%
similarity (corresponding to 43 nucleotide differences) to the
sequence of the same strain deposited in the GenBank database
(accession no.
M34113). This previously deposited sequence
was
identical to that determined for
D. desulfuricans Essex 6
except for one
nucleotide.
Seven other
Desulfovibrio clinical strains have been
isolated in Nancy, France, over a 5-year period. These seven strains
and the strain described above were recovered from seven patients,
designated patients 1 to 7 (Table
1). The
strains from these
patients were labeled D1 to D7, according to patient
number, except
for those from patient 3, from whom two strains were
isolated;
the two strains from patient 3 were labeled D31 and D32,
respectively
(Table
2). Five strains
(strains D1, D2, D31, D5, and D7) were
isolated from abscesses, and
three strains (strains D32, D4, and
D6) were isolated from blood. These
eight clinical isolates differed
according to their catalase, nitrate
reduction, and urease reactions.
Only one isolate was in pure culture
(strain D4), and this strain
could be isolated from the patient
described above. The 16S rDNA
sequences of these seven clinical
isolates were also determined.
Nucleotide sequence accession numbers.
The sequences of
reference strains Desulfomonas pigra, D. desulfuricans Essex 6, and D. desulfuricans MB and of
Desulfovibrio clinical isolate D4 can be recovered from the
GenBank database under accession nos. AF192152, AF192153, AF192154, and AF192155, respectively.
The sulfate-reducing eubacteria represent a class of anaerobic
microorganisms that conduct dissimilatory sulfate reduction.
In this
process, sulfate acts as an oxidizing agent for the dissimilation
of
organic matter, and the reduced sulfur is released into the
external
environment as sulfide, a toxic and corrosive compound.
Thus, these
bacteria have detrimental industrial and environmental
impacts, such as
anaerobic corrosion of steel. They have mostly
been isolated from
environmental sources (
16), but they are
also present in the
intestinal tracts (
6,
16) and mouths
(
18) of
humans and animals. The predominant species in humans
belong to the
genus
Desulfovibrio (
5,
20).
Desulfovibrio spp. have been associated with proliferative
bowel disease in
animals (
3,
4,
10,
11), and they have been
implicated
in ulcerative colitis in humans because of the toxic effects
of
sulfide, which inhibits butyrate oxidation by colonic epithelial
cells (
5,
7,
14,
20). However, their role in human disease
remains speculative, and their isolation from clinical samples
is
seldom described. To date, only eight cases of human infection
with
Desulfovibrio spp. have been documented.
D. desulfuricans has been isolated from blood (
15), and
Desulfovibrio vulgaris has been isolated from an
intra-abdominal abscess (
8).
Desulfovibrio spp.
have been recovered from appendiceal tissue and peritoneal
fluid
(
1) and from a brain abscess (
12), and three
Desulfovibrio strains have recently been isolated from a
pyogenic liver abscess
(
17), blood (
13), and a
urine specimen (
9). The latter
three strains have
provisionally been named
Desulfovibrio fairfieldensis (
17) because of their unique 16S rDNA
sequences.
According to phenotypic characters and 16S rDNA sequences, the eight
Desulfovibrio clinical strains isolated in Nancy can
be
distributed into three groups: strains D1 and D2 are related
to
D. desulfuricans Essex 6 (99.4% 16S rDNA similarity),
strains
D31 and D32 are related to
D. desulfuricans MB
(99.9% 16S rDNA
similarity), and strains D4, D5, D6, and D7 are
related to
D. fairfieldensis (99.9% 16S rDNA similarity for
D4 and D5 and 99.1%
16S rDNA similarity for D6 and D7). The strains in
each group
show less than 97.3% 16S rDNA similarity with strains of
another
group (Table
3). It has been
suggested that a 16S rDNA sequence
similarity of <98% is evidence
that strains belong to separate
species (
17). However, it
remains to be determined by more complete
phenotypic and genotypic
analyses whether these three groups of
strains represent different
species of
Desulfovibrio.
The isolation of
Desulfovibrio spp. from human clinical
samples might seldom occur because of an absence of systematic searches
for the bacteria, the slow and fastidious growth of these bacteria,
and
the presence of mixed flora. Thus, their prevalence in human
diseases
may be underestimated. In our series, the outcomes for
the seven
patients were always favorable once appropriate therapy
was undertaken.
As is often the case in anaerobic infections,
a mixed flora was
generally involved.
Desulfovibrio spp. may be
present in
abdominal abscesses as part of the anaerobic intestinal
flora. These
abscesses are associated with factors that favor
infection, such as
cirrhosis and previous intestinal surgery,
suggesting that
Desulfovibrio strains are opportunistic agents
with somewhat
limited
pathogenicities.
Desulfovibrio strains have seldom been isolated in pure
culture from clinical samples.
D. desulfuricans has been
reported
in blood (
15). The four additional isolates were
from an hepatic
abscess, blood, and urine (
9,
13,
17) and
from blood, as
reported above. These four strains have provisionally
been labeled
D. fairfieldensis and have almost identical 16S
rDNA sequences,
despite a few phenotypic differences, such as esculin
hydrolysis,
growth at 25°C, and antibiotic susceptibility profile
(differences
in resistance or susceptibility to
amoxicillin-clavulanate, imipenem,
ciprofloxacin, and chloramphenicol).
They were sensitive to clindamycin
and metronidazole, two drugs
commonly used for the treatment of
anaerobic infections. These four
isolates may represent different
strains of the same species
which remains to be ascertained by
further studies. Compared to other
Desulfovibrio spp.,
D. fairfieldensis may have
unique properties that confer some invasive power and
make this newly
described bacterium a potential human
pathogen.
| |
ACKNOWLEDGMENTS |
We are indebted to J. Le Gall for comments and support throughout
this study and thank A. Lozniewski for a critical review of the manuscript.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Laboratoire de
Virologie, Hôpital de Brabois-adultes, CHU de Nancy, Route de
Neufchâteau, 54511 Vandoeuvre-lès-Nancy Cedex. Phone: (33)
383153469. Fax: (33) 383153474. E-mail:
a.lefaou{at}chu-nancy.fr.
| |
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Journal of Clinical Microbiology, February 2000, p. 931-934, Vol. 38, No. 2
0095-1137/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
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Abstract
Case Report
