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Prevalence and chemotherapy of enterotoxemia (Clostridium perfringens) in

diarrheic sheep and goats

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 Iqbal et al., 2017

Research Article Open Access

Prevalence and Chemotherapy of Enterotoxemia (Clostridium perfringens) in
diarrheic Sheep and Goats
Babar Maqbool1, Muhammad Kashif Iqbal1,3, Muhammad Ijaz1, Hassaan Bin Aslam2, Hafiz
Ishfaq Ahmad1, Kashif Hussain1
1
Department of Clinical Medicine and Surgery, University of Veterinary and Animal Sciences
Lahore 54000, Pakistan
2
Department of Microbiology, University of Veterinary and Animal Sciences Lahore 54000,
Pakistan
3
Department of Clinical Veterinary Medicine, Huazhong Agricultural University Wuhan 430070,
PR China

*Corresponding Author
Muhammad Kashif Iqbal

Address: College of Veterinary Medicine, Huazhong Agricultural University Wuhan 430070, PR

China

Tel: +8613125018941 E-mail address: dr.kashif2007@gmail.com

Abstract: Entertoxemia is a fatal disease causing economic losses and health problems in small
ruminants. It is characterized by enteritis and/or enterocolitis in several animal species including
sheep, goats, horses and humans. The disease is characterized by rapid course hemorrhagic
diarrhea/dysentery, abdominal pain, convulsions and toxemia. A total of 200 diarrheic samples
from sheep and goats were collected and processed for isolation and identification and
confirmation through biochemical tests. Blood samples were collected from 10 healthy sheep and
goats and 10 infected animals for hematology. 30 positive samples were tested for in-vitro anti-
biogram of commercial antibiotics using Kirby-Bauer method. Two highly sensitive antibiotics
were evaluated in-vivo in 28 diarrheic animals for treatment efficacy. A total of 31% and 22%
prevalence of Clostridium perfringens among sheep and goats was found. Prevalence association
showed non-significant association between fecal scours among both species respectively.
Hematological parameters among both species showed significant association and revealed same
picture. Hemoglobin level and total erythrocyte count decreased significantly (P < 0.05). Packed
cell volume and total leukocyte count increased significantly (P < 0.05). Ciprofloxacin and procain
Penicillin showed maximum activity against the bacterium in-vitro and showed 100% efficacy on
in-vivo testing. This study will help controlling enterotoxemia and substantial economic losses in
small ruminants. Sensitivity trial of various antibiotics will help in choosing the most effective
antibiotics against enterotoxemia under field conditions.
Keywords: enterotoxemia; goat, enteritis; sheep

Received: 19 July 2017, Accepted: 12 November 2017, Published: 17 November 2017

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Introduction
Enterotoxemia is an infectious fatal disease
of small ruminants caused mostly by
Clostridium perfringens. This disease is one
of the endemic disease in Pakistan causes
mortality up to 100 percent in colostrum
feeding lambs and kids (Javed et al., 2009).
Proliferation of C. perfringens in the
ruminant gastrointestinal tract, resulting from
concentrate feeding or overeating, is
considered the pivotal step in the onset of
enterotoxemia. Overeating of grain rich diet,
grazing on grain crops, offering high quality
forage suddenly after a long period of hunger
are all the risk factors associated with this
disease. The course of disease is very short,
never more than 12 hours and death occurs 1-
9 hours after the onset of clinical signs. It
causes clonic convulsions, pasty diarrhea and
nervous signs are typical for this disease. In
goats it causes hemorrhagic enterocolitis in
contrast to sheep (Radostits et al., 1994).
Acute and chronic forms are found both in
young and adult sheep and goat (Uzal and
Kelly, 1996).
Clostridium perfringens is a Gram positive,
spore forming anaerobe bacilli that is
ubiquitous in soil, sewage and normal
intestinal flora. It is divided into five types
(types A-E) based upon their toxin
production i.e. alpha, beta, epsilon and iota
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Iqbal et al., 2017
toxin (Shimizu et al., 2002; Uzal and Songer,
2008). C. perfringens type A is the normal
inhabitant of gastrointestinal tract of normal
ruminants and can overgrow in the lumen of
the intestines after death. Thus interpreting
the positive culture results is a very difficult
phenomenon for C. perfringens isolated from
the intestines. The toxins produced are
absorbed in general circulation but it is true
that most toxins act locally. Beta toxin
produced by Clostridium perfringens type B
and C cause hemorrhagic enteritis thus
developing the diarrhea and dysentery in
young lambs and kids. Beta toxin is
inactivated by trypsin secreted by pancreas of
animals. Animal becomes prone to this
disease when colostrum is overfed that
causes inhibition of trypsin release into
intestines due to the presence of trypsin
inhibiting factor in it. C. perfringens type D
also produces different toxins of which
epsilon toxin is most potent which is
absorbed into bloodstream and damages
vascular system of intestines and increases
the permeability (HADİMLİ et al., 2012;
Songer, 1996). Diagnosis involves history,
clinical signs and gross post-mortem
examination but confirmation requires
laboratory testing. Ante-mortem examination
is not involved much in diagnosis because the
disease is so acute and fatal in all species that
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diagnosis is usually made upon necropsy
examination. Detection of toxins,
quantitative culture followed by genotyping
is useful tool for confirmatory diagnosis.
Multiplex PCR is an important tool for
diagnosis of different types of C. perfringens
on basis of toxins produced by them (Uzal
and Songer, 2008). Predisposing factors
include sudden change in diet or conditions
that slow down peristaltic movements
causing proliferation and production of high
amounts of toxins. These toxins are then
absorbed through the intestines in the blood
to cause the disease (Sumithra et al., 2013).
Treatment is usually ineffective due to acute
onset of disease in sheep. Oral and parenteral
administration of penicillin and
sulphadimidine given orally prevents further
growth of the bacterium and toxin production
(Smith and Sherman, 2011). There is also
dehydration and loss of body minerals due to
severe diarrhea/dysentery, therefore
rehydration through fluid therapy is also very
important. Other strategies are administration
of hyper immune serum. Oral yoghurt or
probiotics are beneficial to restore normal
flora of gut. For prevention and control
measures different strategies are adopted like
reducing the intake of feed which is a short
term control while waiting for the immunity
to develop; administration of antitoxin to all
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Iqbal et al., 2017
sheep as soon as the outbreak starts at the rate
of 200 IU per kg body weight; and most
important is the vaccination of sheep & goats
twice at an interval of one month and the last
vaccine just 4 weeks before lambing provides
a good passive immunity to young lambs
with 97 percent lambs having protective
antibody titer at 8 weeks of age and an
increased level at 12-16 weeks of age
(Radostits et al., 2006). The Composition of
diet may also be balanced with regards to
carbohydrates/protein level with fiber and
energy. For grazing animals, turning out to
pasture must be gradual. Vaccine is effective
for preventive program that is usually done in
January and July in Pakistan. Cross
protection is found between type B and C
because beta toxin is common to both strains.
Up till now there has been a little work done
regarding enterotoxemia in Pakistan. So far
isolation and characterization has been done
from domestic animals and human in Punjab
but specific isolation from small ruminants
(sheep and goat) and its in-vitro antibiogram
has not been done.
Materials and Methods
Experimental Design: Small ruminants
from various private public hospitals and
govt. veterinary hospitals, and farms located
in the outskirts of district Lahore were
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included. The diarrhea was categorized into
semisolid (score 1), loose (score 2) and
watery (score 3).
Sample collection: A total of 200 samples
from diseased and dead small ruminants
(n=100 sheep; n=100 goats) showing clinical
sign and history of acute diarrhea,
respectively were collected. The diarrheic
samples were collected by inserting aseptic
cotton swabs directly into the rectum of the
animals, while for dead animals intestine
tissue were collected.
Isolation and Identification of
perfringens: Reinforced Clostridial Medium
(RCM) agar (Oxoid Limited, Hampshire,
England), as recommended by
International Organization
Standardization (ISO) 1978, was used to
selectively isolate C. perfringens from fecal
and intestinal samples. Identification of the
microorganisms was done on the basis of the
colony characteristics, Gram’s staining and
morphological features according
instructions as described in Bergey’s manual
(Vos et al., 2011). The selected isolates were
further characterized by performing various
biochemical tests including
liquefaction, nitrate reduction, lecithinase
activity, double hemolysis on blood agar
(García and Heredia, 2011) and lactose
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Iqbal et al., 2017
fermentation (Lindström et al., 2011;
Skariyachan et al., 2010).
Hematological Studies: Five ml blood
sample was be collected from 10 animals
(n=5 sheep; n=5 goats) positive for C.
perfringens (enterotoxaemia) and 10 animals
(n=5 sheep; n=5 goats) negative for C.
perfringens directly from the jugular vein
into sterilized vacutainers coated with EDTA
at the rate of 1 mg/mL of blood for measuring
hemoglobin (Hb), packed cell volume (PCV),
total erythrocyte count (TEC), and total
leukocyte count (TLC) using hematological
C. analyzer.
Antibiotic Susceptibility Testing: The
isolated C. perfringens cultures were
the
subjected to antibiotic sensitivity testing
for
against antibiotics (Table 1) by using the
antibiotics sensitivity discs (HiMedia
Laboratories Pvt. Limited, Mumbai, India)
according to the standards procedures
recommended by Clinical Laboratory
Standards Institute (CLSI) (Hecht et al.,
to
2007). Antibiotic susceptibility test was
performed according to Kirby Bauer method.
The evaluation of antibiotics was against 30
confirmed isolates of C. perfringens (n=15
gelatin
sheep; n=15 goat) was based on zone of
inhibition (ZI). On the basis of in vitro
antibiotic results, two highly sensitive
antibiotics were further assessed for in vivo
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trials. Each antibiotic was injected in 14
diarrheic animals (n=7 sheep; n=7 goat)
positive for C. perfringens.
Statistical analysis: Prevalence of C.
perfringens was evaluated by Pearson’s chi-
square test whereas data on antibiotic
sensitivity and hematology was be analyzed
by Student’s t-test, using SPSS (statistical
product and service solutions). P < 0.05 was
considered significant.
Results
Prevalence of Cl. perfringens in sheep and
goats: A total of 200 animals (n=100 sheep;
n=100 goats) suspected for enterotoxemia
were sampled coprologically for presence of
Cl. perfringens, amongst them 52 were found
positive for the Cl. perfringens. The overall
prevalence of Cl. perfringens was found to be
26% (52/200) as given in table 2. The
diarrheic samples collected from sheep were
categorized on the basis of their consistency
into three types i.e. semisolid, loose and
watery and were given score numbers as
score-1 score-2 and score-3 respectively.
Overall prevalence of Cl. perfringens in
score-1 (semisolid), score-2 (loose) and
score-3 (watery) was calculated as 26.31%,
26.08% and 25.49% respectively. Similarly,
prevalence of Cl. perfringens in sheep was
31% while prevalence of Cl. perfringens in
sheep in Score-1, Score-2 and Score-3 was
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Iqbal et al., 2017
calculated as 34.78%, 29.87% and 30%,
respectively. The overall prevalence of Cl.
perfringens in goats was 21% while
prevalence in Score-1, Score-2 and Score-3
was calculated as 20.59%, 22.22% and
19.04%, respectively.
Hematological studies: In our experiment,
values of Hemoglobin (Hb) and Total
Erythrocyte Count (TEC) decreased
significantly (P<0.05) while the values of
Packed Cell Volume (PCV) and Total
Leukocyte Count (TLC) increased
significantly (P<0.05) in the diseased sheep.
On measuring the hematological parameters
of the affected goats, it was found that the
values of Hemoglobin and TEC were
decreased significantly (P<0.05) while the
values of PCV and TLC increased
significantly (P<0.05) as shown in table 5.
Antibiotic susceptibility: The isolates
capable of causing enterotoxemia in sheep
and goats were selected for testing in vitro
antibiotic susceptibility profile against 11
antibiotics. Efficacy of drugs was evaluated
according to the standard zone of inhibition
of antibiotics as provided by Andrews
(2009). By using Kirby Bauer method the
diameter (mm) of zone of inhibition around
Cl. perfringens isolates are given in table III.
It shows the interpretation of the results
according to standards of diameter of zone of
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 Iqbal et al., 2017

inhibition of different antibiotics against the day and 6 (85.71%) after 5th day. 1 sheep was
15 isolates of Cl. perfringens. Data showed not cured; hence the overall efficacy of
that Cl. perfringens was most sensitive to penicillin is 85.71% in goats.
procaine penicillin followed by
Discussion
ciprofloxacin, ceftriaxone, chloramphenicol,
metronidazole, amoxicillin, ampicillin, Sheep and goats population is susceptible to

tetracycline, xytertracycline, lincomycinand, many fatal diseases, one of which is

erythromycin in both sheep and goats. Out of enterotoxemia which is a fatal devastating

the 11 drugs, ciprofloxacin and procain disease of small ruminants and is endemic in

penicillin that showed higher in vitro Pakistan (Hussain et al., 2014). The current

antibiotic sensitivity against Cl. perfringens research was conducted in order to study

were selected for in vivo therapeutic trials in some basic epidemiological parameters on

14 live animals (n= 7 sheep; n= 7 goats). The the prevalence of enterotoxemia, its effects

results for in vivo antibiotic trials against Cl. on hematology and chemotherapeutic trials

perfringens in diarrheic sheep and goats are of commonly used injectable antibiotics

given in table. Among sheep, 3 (42.86%) against Cl. perfringens.

animals were recovered after 2nd day, 6 The overall prevalence of Cl. perfringens in
rd th
(85.71%) after 3 day and 7 (100%) after 4 small ruminants was found to be 26% in the
day making 100% overall efficacy of present study. These findings are in close
ciprofloxacin. Penicillin administration agreement with the results of (Rahaman et al.,
showed 2 (28.57%) animals were recovered 2013), who reported Cl. perfringens 32.1%
nd rd
after 2 day, 5 (71.43%) after 3 day, 6 prevalent in sheep and goats of Khuzestan
th th
(85.71%) after 4 day and 7 (100%) after 5 province diagnosed bacteriologically.
day. So overall efficacy of penicillin is 100% (Hussain and El Sanousi, 2013) examined
in sheep. In goats, 3 (42.86%) were cured fecal samples of domestic ruminants, equines
nd rd
after 2 day, 5 (71.43%) after 3 day, 6 and chicken and noted 23.8% prevalence of
th th
(85.71%) after 4 day and 7 (100%) after 5 Cl. perfringens in Khartoum State, Iran,
day; hence the overall efficacy of which is also closely resembled with present
ciprofloxacin is 100%. In case of penicillin findings. The prevalence of Cl. perfringens in
nd
therapy, 2 (28.57%) were cured after 2 day, the diarrheic samples obtained from sheep
rd th
4 (57.14%) after 3 day, 5 (71.43%) after 4 was found to be 31%. The prevalence of Cl.
6

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 Iqbal et al., 2017

perfringens is much closely similar to the isolates, all the isolates were susceptible to
findings of (Fayez et al., 2013), who the penicillin, ciprofloxacin and ceftriaxone
determined 30.41% prevalence of Cl. and none of the isolates was resistant or
perfringens from the intestinal samples of intermediate. In goats, all the isolates were
sheep in Al-Ahsa, Kingdom of Saudi Arabia. susceptible to ciprofloxacin. Out of 15
(Moussa and Hessan, 2011) also found isolates 14 were sensitive to penicillin and
26.5% prevalence of Cl. perfringens in adult one was resistant and none of isolate was
sheep in Saudi Arabia, which is in a close intermediate. Upon in-vivo trials,
accordance to the current study. There is lack ciprofloxacin and penicillin were 100%
of literature regarding the fecal score-wise efficacious in sheep. While in goats,
prevalence of Cl. perfringens in world as ciprofloxacin was 100% efficacious but
found in the present study. penicillin was 87% efficacious. A similar
Current study findings regarding study revealed similar results in which, C.
haematological study showed that the perfringens showed the highest sensitivity to
haemoglobin significantly decreased in sheep ciprofloxacin, while were resistant against
and goats with enterotoxemia. Total ampicillin (Singh et al., 2005).
erythrocytic count was also significantly
Conclusion
decreased in both sheep and goats with
enterotoxemia. These results are supported This study will help for controlling
by the hematological examination carried out enterotoxemia and substantial economic
by (Nasir et al., 2013). Furthermore, the losses in small ruminants. Sensitivity trial of
current findings showed that packed cell various antibiotics will help in choosing the
volume was increased significantly in sheep most effective antibiotics against
and goats suffering from enterotoxemia. enterotoxemia under field conditions.
Total leukocytic count was also found to be
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Table 1: List of antibiotics used for antibiotic susceptibility testing

Sr. No. Antibiotic disc tested Disc Concentration

1. Tetracycline 30 mcg/disc
2. Chloramphenicol 25 mcg/disc
3. Metronidazole 5 mcg/disc
4. Penicillin 10 U/disc
5. Ampicillin 10 mcg/disc
6. Amoxicillin 30 mcg/disc
7. Erythromycin 15 mcg/disc
8. Ciprofloxacin 30 mcg/disc
9. Lincomycin 10 mcg/disc
10. Ceftriaxone 30 mcg/disc

Table 1: Prevalence of Cl. perfringens in diarrheic sheep and goats

No. of Positive Odd Ratio/ MH Chi-sq
Species/Score 95% CI
Animal N % reciprocal P-value
Species
Lambs 100 31 31.0 22.53-40.56
1.16/0.87 -
Kids 100 21 21.0 19.87-37.39
Total 200 52 26.0 23.49-36.10
Overall Fecal Score
Score-1 57 15 26.31 11.47-25.08
Score-2 92 24 26.08 29.21-58.02 - P˂0.001
Score-3 51 13 25.49 36.57-68.55
Total 200 52 26.0 23.49-36.10
Sheep
Score-1 23 08 34.78 11.99-31.93
Score-2 47 14 29.87 20.61-62.11 - P˂0.007
Score-3 30 09 30.00 34.97-79.89
Goats
Score-1 34 07 20.58 6.74-24.91
Score-2 45 10 22.22 26.96-65.66 - P˂0.003
Score-3 21 14 19.04 26.13-69.36
[Score-1 (Semisolid feces), Score-2 (Loose feces), Score-3 (Watery feces)]
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 Iqbal et al., 2017

Table 2: Influence of Cl. perfringens on various hematological parameters in sheep and goats

(Mean ± SD)

Hematological Lambs Kids

parameters Healthy Infected P-Value Healthy Infected P-Value
Hemoglobin (g/dl) 11.87±0.43 9.28 ± 1.24 0.001* 11.86±1.12 9.47±1.27 0.003*
PCV (%) 36.46 ± 1.3 41.54 ± 2.16 0.001* 27.49±1.78 39.17±2.32 0.004*
TEC (1012/l) 10.95±0.68 8.39 ± 0.37 0.001* 12.80±2.17 10.76±2.07 0.017*
TLC (109/l) 9.73±0.48 11.27 ± 1.26 0.017* 13.34±1.83 15.67±1.94 0.039*
(*Indicates the significant difference from the healthy)

Table 3: In-vitro antibiotic sensitivity against Cl. perfringens in sheep and goats
Remarks
Antibiotics No. of Sensitive Intermediate Resistant
Sensitive Discs samples No. of ZI No. of ZI No. of
ZI (mm)
isolates (mm) isolates (mm) isolates
Sheep
Procaine Penicillin 15 14 >16 01 14-16 - <13
Ciprofloxacin 15 13 >19 01 17-19 01 <16
Ceftriaxone 15 11 >28 02 26-28 02 <25
Chloramphenicol 15 10 >19 03 17-19 02 <16
Metronidazole 15 10 >16 03 14-16 02 <13
Amoxicillin 15 11 >20 02 18-20 02 <17
Ampicillin 15 09 >14 04 12-14 02 <11
Tetracycline 15 10 >14 04 12-14 01 <11
Oxytertracycline 15 08 >17 04 16-17 03 <15
Lincomycin 15 10 >22 04 12-21 01 <11
Erythromycin 15 08 >18 04 14-17 02 <13
Goats
Procaine Penicillin 15 12 >16 03 14-16 - <13
Ciprofloxacin 15 13 >19 01 17-19 01 <16
Ceftriaxone 15 12 >28 02 26-28 01 <25
Chloramphenicol 15 11 >19 02 17-19 02 <16
Metronidazole 15 10 >16 03 14-16 02 <13
Amoxicillin 15 11 >20 02 18-20 02 <17
Ampicillin 15 09 >14 03 12-14 03 <11
Tertracycline 15 11 >14 03 12-14 01 <11
Oxytertracycline 15 08 >17 04 16-17 03 <15
Lincomycin 15 13 >22 01 12-21 01 <11
Erythromycin 15 07 >18 05 14-17 02 <13
ZI= zone of inhibition
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