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Journal of Clinical Microbiology, February 1999, p. 358-361, Vol. 37, No. 2
Department of Equine Internal
Medicine1 and
Institute for Veterinary
Bacteriology,2 Berne, Switzerland, and
Institut Pasteur, Unité des Toxines Microbiennes, 28 F-75724 Paris Cedex 15, France3
Received 22 June 1998/Returned for modification 20 October
1998/Accepted 5 November 1998
The incidence of a new, yet unassigned toxin type of
Clostridium perfringens containing the genes for the
Different Clostridium
species are frequently isolated from horses with typhlocolitis
(14, 17) and are generally suspected to be involved in the
disease (1, 5, 13, 15). However, it is not clear which
Clostridium species and, in particular, which subtypes or
toxinotypes are the main cause of typhlocolitis and other toxic
intestinal diseases in horses. While Clostridium difficile
was reported to play an important role in the disease (1),
other reports showed a high rate of isolation of Clostridium perfringens from horses with intestinal diseases (2).
C. perfringens, which causes various diseases in different
animals, is differentiated into five subtypes (subtypes A to E)
according to the major toxins produced by each subtype (11).
Type A is subdivided further into enterotoxigenic and
nonenterotoxigenic strains (16). It has been reported that
acute colic signs and hemorrhagic gastroenterocolitis could be induced
experimentally in Shetland ponies after intravenous injection of
enterotoxin obtained from enterotoxigenic C. perfringens type A (12). However, other studies showed that
enterotoxigenic C. perfringens isolates do not play a role
in intestinal disorders of horses (2).
In addition to the C. perfringens types mentioned above, an
unassigned type of C. perfringens that produces This report describes the incidence of this novel Animals.
Ninety-nine horses of different breeds, ages, and
sexes were included in the study and were subdivided into four groups.
Group I contained 18 horses suffering from typical typhlocolitis
symptoms and presenting with all four cardinal symptoms of the disease: hemorrhagic, profuse, watery diarrhea, subfebrile body temperature (38 to 38.5°C), severe leukopenia with less than 3 × 109 cells/liter due to neutropenia, and hypoproteinemia
(less than 5 × 109 cells/liter). Of the 18 horses, 10 developed typhlocolitis during hospitalization between 2 and 5 days
after surgery for colic, 5 suffered from typhlocolitis but were
hospitalized for other reasons, and 3 with typhlocolitis were referred
to the animal hospital from their home stable. Ten of the horses with
typhlocolitis were treated with antibiotics (gentamicin and penicillin)
in combination with the nonsteroidal anti-inflammatory drug (NSAID)
flunixinum (Finadyne; Biokema, Crissier, Switzerland) 2 to 5 days prior
to the acute onset of typhlocolitis and 7 were treated with the NSAID only. All horses developed a significant leukocyte drop due to neutropenia to less than 3 × 109 cells/liter prior to the
onset of profuse, watery diarrhea. Apart from the four cardinal
symptoms, the horses suffered from an important hypovolemic iliocolitis
syndrome and anorexia. Group II contained seven horses suffering from
atypical typhlocolitis symptoms but not showing all four symptoms
characteristic of typical typhlocolitis. Five of those seven horses
developed fever (40 to 41°C) and hemorrhagic or profuse, watery
diarrhea. Two horses showed profuse, watery diarrhea, hypoproteinemia,
and subfebrile body temperatures, but the typical, severe leukocyte
drop prior to the onset of diarrhea was not present. All horses in
group II were referred to the clinic with diarrhea as the primary
concern. Prior to the onset of diarrhea four horses were treated with
the antibiotics gentamicin and penicillin in combination with the
NSAID, and three were treated with the NSAID only. Group III contained
16 horses suffering from intestinal disorders other than typhlocolitis.
Of those, six untreated horses were referred to the clinic with a
history of chronic indigestion. Three horses suffered from
gastroduodenojejunitis and had been treated with the NSAID during
hospitalization. Seven horses had surgery for colic (four large-colon
and one cecal torsion and two renosplenic entrapments) and were treated
with gentamicin and penicillin in combination with the NSAID prior to
and 3 days after laparotomy. None of these 16 horses developed acute,
watery diarrhea or a leukocyte drop to less than 3 × 109
cells/liter. Group IV contained 58 control horses without intestinal disease. Of these horses, 35 were hospitalized or euthanized in the
clinic for reasons other than intestinal disorders, and 23 were
apparently healthy competition horses from a private riding stable.
None of these horses had received any medication in at least the 3 weeks prior to the study.
Sampling.
Seventy-four fecal samples from 21 horses with
intestinal disorders and from 53 control horses were taken from the
rectum and packed in plastic bags, and excess air was eliminated for transport of the samples to the bacteriology laboratory. Twenty-five specimens were taken from ingesta of the small and/or large intestine or biopsy specimens of the intestinal wall during laparotomy or immediately after euthanasia from the proximal jejunum, pelvic flexure
of the large colon, and/or apex of the cecum from 20 horses with
intestinal diseases and from 5 horses that were euthanized. Specimens
of ingesta were cultivated within 12 h. Biopsy samples were frozen
in liquid nitrogen until analysis. Each of the 99 horses provided just
one sample, whether it was feces, ingesta, or a biopsy specimen.
Bacteriological examinations.
The samples were cultured on
blood agar plates (containing 5% sheep blood) and on C. difficile-selective agar (no. 43213; bioMérieux, Marcy
l'Etoile, France) and were incubated at 37°C under anaerobic
conditions. In addition, tetrathionate broth enrichment with subsequent
subculture on Salmonella-Shigella agar and brilliant green
agar was performed to attempt isolation of Salmonella spp.
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Prevalence of
2-Toxigenic Clostridium
perfringens in Horses with Intestinal Disorders
ABSTRACT
Top
Abstract
Introduction
Materials and methods
Results
Discussion
References
-toxin and the recently described 
2-toxin in horses with
intestinal disorders is reported. The study included 18 horses
suffering from typical typhlocolitis, 7 horses with atypical
typhlocolitis, 16 horses with other intestinal disorders, and 58 horses
without intestinal disease. In total, 20 samples of ingesta of the
small and large intestines, five biopsy specimens of the intestinal
wall, and 74 fecal samples were analyzed bacteriologically. C. perfringens isolates were typed for the presence of the -,
-, 2-, and 
-toxin and enterotoxin genes by PCR, including a
newly developed PCR for the detection of the 2-toxin gene
cpb2. 2-Toxigenic C. perfringens was
detected in samples from 13 of 25 (52%) horses with typical or
atypical typhlocolitis, with a particularly high incidence in specimens
of ingesta and biopsy specimens (75%), whereas only 6 of 16 specimens
from horses with other intestinal diseases yielded 2-toxigenic
C. perfringens. No 2-toxigenic C. perfringens was found in the samples from the 58 control horses,
of which only one fecal sample contained C. perfringens
type A. Among the samples from the 15 horses with fatal cases of
typical and atypical typhlocolitis 9 (60%) were positive for
2-toxigenic C. perfringens, whereas samples from only 4 of the 10 (40%) animals with nonfatal cases of infection were
positive. We found an interesting correlation between the
antibiotic-treated horses which were positive for 2-toxigenic
C. perfringens and lethal progression of the disease. No
C. perfringens strains isolated in this study contained
genes for the - and -toxins and enterotoxin. The high incidence
of 2-toxigenic C. perfringens in samples of ingesta,
biopsy specimens of the intestinal wall, and feces from horses
suffering or dying from typhlocolitis together with the absence of this
organism in healthy horses provides strong evidence that 2-toxigenic
C. perfringens play an important role in the pathogenesis
of typhlocolitis.
INTRODUCTION
Top
Abstract
Introduction
Materials and methods
Results
Discussion
References
-toxin
and the newly discovered 2-toxin was recently described
(9). It was isolated from piglets with necrotic
enterocolitis and was also found in horses with enterocolitis
(9). Since the -toxin, which is produced by all types of
C. perfringens including nonpathogenic type A strains, is
not considered a primary cause of digestive lesions (10), it
was suggested that the 2-toxin, which is present in this new type of
C. perfringens, plays a role in causing the digestive
diseases (9).
2-toxigenic
C. perfringens type in horses with typical symptoms of
typhlocolitis, horses with atypical typhlocolitis, and horses suffering
from other intestinal disorders. The results obtained with fecal
samples, specimens of ingesta from the small and large intestines, as
well as biopsy specimens of the intestinal walls of diseased and
control horses were compared. All samples were also analyzed for the
occurrence of C. difficile, since its role as a nosocomial
pathogen in horses with typhlocolitis, especially in association with
antibiotics, has been described (1, 3, 5, 13).
MATERIALS AND METHODS
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Abstract
Introduction
Materials and methods
Results
Discussion
References
-toxin gene cpa and the enterotoxin gene
cpe, strain ATCC 3626 for cpa and -toxin gene
cpb, and strain NCTC 8346 for cpa and -toxin
gene etx, as described previously (4, 8). As a
control for the 2-toxin gene cpb2 we used our
2-toxigenic internal reference strain C. perfringens E
482/97, isolated from a horse, and strain C. perfringens S
1040/95, isolated from a piglet that died of necrotizing enteritis.
Both strains contain the - and 2-toxin genes and are devoid of
the genes for the other major C. perfringens toxins, the
- and -toxins and enterotoxin. As a control for C. difficile toxin A and toxin B, strain ATCC 43255 was used.
Preparation of bacterial specimens and PCR amplifications. Template DNA from bacterial cultures was obtained by a direct lysis method. About 10 colonies were taken from primary cultures and were suspended in 450 µl of lysis buffer (0.1 M Tris-HCl [pH 8.5], 0.05% Tween 20, 0.24 mg of proteinase K [Boehringer Mannheim, Mannheim, Germany] per ml). Two to three colonies were taken from pure cultures and suspended in 450 µl of lysis buffer. The samples were incubated at 60°C for 1 h and then heated at 97°C for 15 min in order to inactivate the proteinase K.
The specific oligonucleotide primers for PCR amplification of the toxin genes are listed in Table 1. PCR assays were performed with the DNA Thermal Cycler Gene Amp 9600 (Perkin-Elmer Cetus, Norwalk, Conn.). The reactions were performed in 50-µl volumes containing 5.0 µl of lysate, 45.0 µl of Taq PCR mixture (10 mM Tris-HCl [pH 8.3], 1.5 mM MgCl2, 50 mM KCl, 0.005% Tween 20, 0.005% Nonidet P-40 detergent, each deoxynucleoside triphosphate at a concentration of 170 µM, 0.25 µM each oligonucleotide primer, and 1.25 U of Taq DNA polymerase [Boehringer Mannheim]). The reactions were subjected to 35 cycles of amplification consisting of 30 s of denaturation at 94°C, 30 s for primer annealing at the respective temperature (Table 1), and 30 s of chain extension at 72°C. The ramping time used to raise the temperature from the annealing temperature to 72°C is given in Table 1. PCRs for the detection of the C. perfringens-, -, and -toxins and enterotoxin genes were described
previously (4). For the detection of the 2-toxin gene
cpb2 by PCR, we have developed a pair of specific primers, P319BETA2 and P320BETA2 (Table 1), which match nucleotide positions 377 to 392 and 950 to 935, respectively, of the DNA sequence of cbp2 in the GenBank/EMBL database accession no. L77965)
(9). This primer pair amplified a specific 573-bp internal
fragment of the cpb2 gene from our 2-toxigenic internal
reference strain C. perfringens E 482/97 and from strain S
1040/95. No fragment was amplified with primers P319BETA2 and P320BETA2
from the reference strains of C. perfringens type A, type B,
type C, type D, or type E or from enterotoxigenic C. perfringens or from the type strains of the Clostridium
species C. difficile, C. chauvoei, C. septicum, C. sordelli, C. sporogenes,
C. novii, C. haemolyticum, C. tetani, and C. histolyticum, showing the specificity of this primer
pair for the 2-toxin gene cpb2 (8a). PCR
identification of the toxin A and toxin B genes of C. difficile was done as described previously (18). PCR
products were analyzed by applying 20 µl on a 0.7% agarose gel
(agarose type II medium EEO; no. A-6877; Sigma, St. Louis, Mo.) for
electrophoresis and were visualized with ethidium bromide and UV light.
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RESULTS |
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Top
Abstract
Introduction
Materials and methods
Results
Discussion
References
|
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PCR analysis of the reference strains for the different
toxin types of C. perfringens showed the presence of the
-toxin gene cpa in all C. perfringens
reference strains as well as in our 2-toxigenic internal reference
strain C. perfringens E 482/97 and in strain S 1040/95. The
-toxin gene etx was found in the reference strains of
type B (ATCC 3626) and type D (NCTC 8346). The -toxin gene
cpb was found in the reference strain of type B (ATCC 3626).
The enterotoxin gene cpe was found in enterotoxigenic type A
strain NCTC 10239. The 2-toxin gene cpb2 was detected by
PCR in our 2-toxigenic internal reference strain C. perfringens E 482/97 and in strain S 1040/95. PCR analysis of
C. difficile ATCC 43255 showed the presence of the two genes
for toxins A and B. These results thus confirm the specificity of the
analytical methods.
The results of bacteriological and PCR examinations are given in Tables
2 and 3. C. perfringens was
isolated from 5 of 21 (24%) fecal samples from 21 horses with
intestinal diseases. All these isolates proved to harbor the 2-toxin
gene cpb2 and the -toxin gene cpa (Table 2).
Feces from 4 of the 21 (19%) horses contained C. difficile,
and 12 (57%) further horses were negative for both C. perfringens and C. difficile. All isolated
C. perfringens strains were devoid of the - and
-toxin and enterotoxin genes, as assessed by PCR. Examination of
feces from the 53 control horses without intestinal disease showed that
they contained no 2-toxigenic C. perfringens isolates and
no C. difficile isolates. A C. perfringens type A
strain without an enterotoxin gene was isolated from one of these
control animals.
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The results of bacteriological examinations of specimens of intestinal
ingesta or biopsy specimens of the intestinal wall (small and large
intestine) revealed that of 20 specimens from 20 different horses with
intestinal disease, 14 specimens proved to be positive for
2-toxigenic C. perfringens (Table 2). One horse with
typical typhlocolitis which was positive for 2-toxigenic C. perfringens also contained nontoxigenic C. difficile.
Both 2-toxigenic C. perfringens and toxigenic C. difficile (containing the genes for toxins A and B) were isolated
from one horse with atypical typhlocolitis, and one horse was negative
for C. perfringens and C. difficile. C. difficile alone was isolated from two of eight horses with
intestinal diseases other than typhlocolitis. All specimens of ingesta
from the five horses from the control group (group IV) were
bacteriologically negative for C. perfringens and C. difficile.
In total, 2-toxigenic C. perfringens was isolated from
samples from 13 of 25 (52%) horses with typical or atypical
typhlocolitis (Table 3). Samples from two
horses from this group contained C. perfringens type A and
six contained C. difficile; of the latter, two were found to
contain C. difficile in combination with 2-toxigenic C. perfringens. In horses with other intestinal diseases,
the incidence of 2-toxigenic C. perfringens was 6 of 16 (37%) animals. C. perfringens type A was isolated from the
specimen from one animal in this group, and C. difficile was
isolated from two samples. 2-Toxigenic C. perfringens was
not isolated from any of the 58 horses in the control group, and
C. perfringens type A was found only once. All C. perfringens strains analyzed were devoid of the - and -toxin
and enterotoxin genes.
|
Among the animals in group I (typical typhlocolitis), 8 of 18 horses
died or were subjected to euthanasia due to severe shock or laminitis.
Of these, 4 were positive for 2-toxigenic C. perfringens and had been medicated with an NSAID and antibiotics (gentamicin and
penicillin). All horses in group II (atypical typhlocolitis) died or
were euthanized (n = 7); five of them were positive for 2-toxigenic C. perfringens. Four of these five animals
were treated with an NSAID and antibiotics.
Taken together, from a total of 25 horses with typical and atypical
typhlocolitis, 14 were treated with antibiotics and 9 harbored
2-toxigenic C. perfringens. Of these animals all eight horses which had received antibiotic treatment and yielded
2-toxigenic C. perfringens died. Among the animals in
group III (n = 16), 10 horses were euthanized, and four
of these were positive for 2-toxigenic C. perfringens and
received antibiotic and anti-inflammatory therapy (gentamicin,
penicillin, and NSAID).
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DISCUSSION |
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Top
Abstract
Introduction
Materials and methods
Results
Discussion
References
|
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Bacteriological examination of feces, specimens of intestinal
ingesta, or biopsy specimens of the intestinal wall from horses with
intestinal disorders and subsequent toxin gene typing of the isolated
Clostridium spp. by PCR showed a high incidence of a new,
yet unassigned type of C. perfringens containing the
-toxin gene cpa and the 2-toxin gene cpb2.
Since the -toxin is produced by all C. perfringens
isolates and does not seem to play a major role in enteric diseases
(10), we attribute the pathogenicities of these C. perfringens isolates to the 2-toxin. This newly characterized 2-toxigenic C. perfringens is different from C. perfringens type C (which contains the -toxin), which is
involved in necrotizing enteritis of pigs and which was also recently
reported in horses with enterocolitis (7). C. perfringens type C was not found in this study. We found
2-toxigenic C. perfringens mainly in horses with typical
and atypical typhlocolitis, representing 52% of the isolates. To a
lesser extent they were also isolated from horses with other intestinal
disorders, in which they represented 37% of the isolates. No
2-toxigenic C. perfringens was found in healthy horses or
in horses that were hospitalized for reasons other than intestinal
problems. C. perfringens type A was found only incidentally.
No enterotoxigenic C. perfringens was found in this study,
confirming the observations of Beckmann et al. (2), who
showed that enterotoxigenic C. perfringens does not play a
role in intestinal disorders of horses. It is important that, apart
from 2-toxigenic C. perfringens, only a few C. perfringens type A isolates, which are assumed to be of low
significance for enteric disorders, were found. C. difficile, which was also reported to be associated with
typhlocolitis (13), was found in some horses, often together
with 2-toxigenic C. perfringens.
A particularly high incidence of 2-toxigenic C. perfringens was found in specimens of intestinal ingesta and
biopsy specimens of the intestinal wall from horses with typical or
atypical typhlocolitis (75%), and a lower incidence was found in
horses with other intestinal disorders (62%). These data indicate a
correlation between the presence of 2-toxigenic C. perfringens in specimens of intestinal ingesta and biopsy
specimens of the intestinal wall from horses with typhlocolitis. The
data also suggest that 2-toxigenic C. perfringens might
be particularly fatal in combination with antibiotic treatment.
Preliminary in vitro experiments indicate that gentamicin enhances
expression of the 2-toxin. Hence, 2-toxigenic C. perfringens not only may play an important role in the
pathogenesis of equine typhlocolitis and other intestinal disorders of
equines but also might be involved in the fatal progression of
typhlocolitis in horses.
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ACKNOWLEDGMENTS |
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We are grateful to Peter Tschudi, Carol Suter, and Sandra Zumwald for excellent technical assistance and to André Burnens for help with data analysis.
This investigation was supported by Foundation Research 3R (Reduction Refinement and Replacement of animal experimentation) project 37/92 and by the research account of the Institute for Veterinary Bacteriology.
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FOOTNOTES |
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* Corresponding author. Mailing address: Institute for Veterinary Bacteriology, University of Berne, Laenggasstrasse 122, CH-3012 Berne, Switzerland. Phone: 41 31 631 2484. Fax: 41 31 631 2634. E-mail: jfrey{at}vbi.unibe.ch.
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Abstract
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References
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Journal of Clinical Microbiology, February 1999, p. 358-361, Vol. 37, No. 2
0095-1137/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
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(2003). Immunohistochemical Localization of Clostridium perfringens {beta}2-Toxin in the Gastrointestinal Tract of Horses. Vet Pathol
40: 376-381
[Abstract] [Full Text]
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