PREVALENCE OF CAMPYLOBACTER JEJUNI AND CAMPYLOBACTER COLI IN CALVES AND LAMBS WITH AND WITHOUT DIARRHEA AND THEIR PUBLIC HEALTH IMPORTANCE

Assiut Vet. Med. J. Vol. 52 No. 109 April 2006

Department of Veterinary Medicine, Faculty of Veterinary Medicine, Alexandria University.

PREVALENCE OF CAMPYLOBACTER JEJUNI AND CAMPYLOBACTER COLI IN CALVES AND LAMBS WITH AND WITHOUT DIARRHEA AND THEIR PUBLIC HEALTH IMPORTANCE

(With 3 Tables)

By A.M. KHADR; Y.N. HAGGAG* and S.A. KHALEIL ** *Dept. of Animal Hygiene and Zoonoses, Fac. of Vet. Med., Alex. University

** Dept. of Microbiology, Fac. of Vet. Med., Alex. University.

(Received at 8/3/2006)

نسبة انتشار الکامبيلوباکتر جوجيني والکامبيلوباکتر کولاي في العجول والحملان المصابة أو غير المصابة بالإسهال وأهميتهما على الصحة العامة

عادل محمد خضر،ياسر نصر حجاج،سامي عبد السلام خليل أجريت هذه الدراسة على عدد ۳۰۹ مسحة شرجية من العجول (۱۹۷) والحملان (۱۶۲) المصابة بالإسهال و السليمة ظاهريا لدراسة

نسبة انتشار الکامبيلوباکتر جوجيني والکامبيلوباکتر کولاي. وقد أسفر الفحص البکتريولوجي عن عزل الکامبيلوباکتر جوجینی من ۲4 (

۶,۳۷ ۱%) من العجول وکانت نسبة انتشار الکامبيلوباکتر جوجيني أعلى في

العجول المصابة بالإسهال (۲۳٫4%) من العجول السليمة ظاهريا (

۱۰,۸۳

%). بينما في

الأغنام تم عزل الکامبيلوباکتر جوجيني من ۱۳ (

۹,۱۰

%) من الحملان وکانت النسبة في الحملان المصابة بالإسهال ۱۲٫۲۶% بينما کانت النسبة في الحملان السليمة ظاهريا %۷,۵۲ . وقد تم عزل الکامبيلوباکتر کولاي من ۱۰ (

۸,۹۸

%) من العجول وکانت نسبة

انتشار الکامبيلوباکتر کولاي أعلى في العجول المصابة بالإسهال (

۱۷,۸۲ %) من العجول

السليمة ظاهريا (

6,67 %). بينما في الأغنام تم عزل الکامبيلوباکتر کولاي من

۱۰ ( %۷,۰ ) من الحملان وکانت النسبة في الحملان المصابة بالإسهال

۸,۱۹ % بينما

کانت النسبة في الحملان السليمة ظاهريا 6,45 %. دلت دراسة تأثير المضادات الحيوية على معزولات الکامبيلوباکتر جوجيني و الکامبيلوباکتر کولاي أن أفضلها فاعلية کان الکلورامفينيکول ويليه کل من الجنتاميسين والنيوميسين. وکانت معظم المعزولات مقاومة للسلفاميسوکسازول و الأمبيسيلين والتتراسيکلين وکانت نسبة ۷۰-۸۰%من المعزولات مقاومة للإريثرومايسين. وکانت نسبة المقاومة للمضادات الحيوية أعلى في الکامبيلوباکتر کولاي عنها في الکامبيلوباکتر جوجيني. وتلخص هذه الدراسة على أن الکامبيلوباکتر

جوجيني والکامبيلوباکتر کولاي تلعب دورا في الإسهال في العجول وأن نسبة انتشار الکامبيلوباکتر جوجيني في العجول والحملان أعلى من نسبة انتشار الکامبيلوباکتر کولاي

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وإن کانت الکامبيلوباکتر کولاي أکثر مقاومة للمضادات الحيوية. هذا وقد تم مناقشة الأهمية الصحية العامة لکل من الکامبيلوباکتر جوجيني والکامبيلوباکتر کولاي وطرق الوقاية منهما.

SUMMARY

The prevalence of Campylobacter jejuni and Campylobacter coli harboring in the intestine of calves and lambs with or without diarrhea was studied. A total of 309 rectal swab samples were collected from calves (167) and lambs (142) with and without diarrhea, the samples were examined bacteriologically. The bacteriological examination revealed the isolation of C. jejuni from 24 (14.37% of 167 examined calves. The prevalence was significantly higher in the diarrheic calves (23.4%) than from the apparently healthy calves (10.83%). In addition, C. jejuni was isolated from 13 (9.15%) of 142 sheep examined, where higher (but non significant) percentage (12.24%) was reported in diarrheic lambs than (7.52%) reported in apparently healthy lambs. Also, lower prevalence of C. coli was observed in examined samples of calves (8.98%) and lambs (7.04%). The prevalence of C. coli was significantly higher in diarrheic calves (17.82%) than apparently healthy calves (6.67%), and higher in diarrheic lambs (8.16%) than apparently healthy lambs (6.45%) (Non significant). Moreover, Campylobacter isolated in this study were tested for susceptibility to 9 antibiotics. None of the isolates were resistant to Chloramphenicol and high percentages of isolates were resistant to Tetracycline, Erythromycin, Ampicillin, Penicillin, Naldixic acid and Sulfamethoxazole, while drug resistance was more frequent in C. coli than C. jejuni. These results indicate that Campylobacter colonization in the intestine is very common in young calves and lambs and the bacteria play a role, at least in the aggravation of the diarrhea process. Additional studies are needed to assess the role of campylobacter in spontaneous enteric disease of calves and lambs. The results of this study demonstrate that C. jejuni is widely distributed, while C. coli is more narrowly distributed but significantly more resistant to antimicrobial. The public health importance of C. jejuni and C. coli were discussed.

Key words: Campylobacter, C. jejuni, C. coli, calves, lambs, diarrhea.

INTRODUCTION

I

Diarrhea is the most common symptom of illness in young calves and lambs. Scours can be caused by many organisms, and more than one

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causative agent can be present in the one animal. Salmonella. E coli and viruses such as Rotavirus are the most common cause of scours in young calves, but protozoa such as Cryptosporidia and Coccidia, and bacteria such as Campylobacter can also cause this problem (Radostits et al., 2000).

Campylobacter is a Gram-negative slender, curved, and motile rod. It is a microaerophilic organism, which means it has a requirement for reduced levels of oxygen. It is relatively fragile, and sensitive to environmental stresses (e.g., 21% oxygen, drying, heating, disinfectants and acidic conditions). Because of its microaerophilic characteristics the organism requires 3 to 5% oxygen and 2 to 10% carbon dioxide for optimal growth conditions (Betty et al., 1998).

It is evident that C. jejuni and C. coli are responsible factor of diarrhea in several animal species and human (Sato et al., 2004). However, the role of Campylobacter in calf diarrhea is not entirely assured. Experimental data (Al-Mashat and Taylor, 1983) indicate that infection with Campylobacter can induce diarrhea in calves. In other studies, no differences in prevalence of C. jejuni between healthy and diseased calves were observed (Busato et al., 1998).

C. jejuni is a common and important cause of bacterial diarrhea in humans, equaling or exceeding Salmonella and Shigella spp. in prevalence. C. coli is less frequent than C. jejuni as a cause of diarrheic disease in humans. The source of infection for humans in developed countries is thought to be the massive reservoir of C. jejuni and to a lesser extent C. coli in the animal population. It is assumed that man may be infected by direct contact with diseased animals suffering from Campylobacter diarrhea or by consumption of food or water contaminated by secretion or excretion of diseased animals (Acha and Szyfers, 1991; Shakespeare, 2002 and Hartmut et al., 2003).

Increasing antimicrobial resistance in Campylobacter is a recognized problem, (Sáenz et al., 2000 and Jensen and Aarestrup, 2001). The increasing uses of antibiotics in treatment of animal diseases especially enteric diseases may create more resistant strains of Campylobacter in human and animal. This work was planned to: - Study the prevalence of C. jejuni and C. coli in the feces of calves and

lambs with and without diarrhea, and its possible role in enteric diseases in animals. - Study the role of calves and lambs as a source of infection to human

with C. jejuni and C. coli.

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- Study the susceptibility of Campylobacter isolated from calves and

lambs to a panel of 9 antibiotics.

MATERIALS and METHODS

1- Collection of samples:

Rectal swab samples were collected from 120 apparently healthy calves and 47 calves suffering from diarrhea (the calves were 15 days to 6 months age). Also, 93 rectal swab samples were collected from apparently healthy lambs (one week to 3 months age) and 49 from lambs suffering from diarrhea. The samples were collected from Behera and Alexandria Provences. The animals were raised individually or in small groups. 2- Bacteriological examination of samples:

Rectal swab samples were inoculated into sterile tube containing brucella broth to preserve the viability of the organism during transportation to the laboratory. The samples were examined for C. jejuni or C. coli by streaking on Skirrow medium contained, 5-7% horse blood and campylobacter selective supplements (Oxoid). Plates were incubated at 42°C for 48 h in an atmosphere of 5% oxygen, 10% carbon dioxide, and 85% nitrogen in standard anaerobe jars. Then the bacterial isolates were purified and identified by using colonial, morphological and biochemical characteristics (Koneman et al., 1988 and Quinn et al., 2002). 3- In-vetro antibiotic sensitivity testing:

The technique was carried out using the disc diffusion method according to Bopp et al. (1985). Bacterial isolates (10 from each) were tested for resistance using gradient disk diffusion MIC to Neomycin (30 ug), Gentamycin (10 ug), Ampicillin (10 ug), Streptomycin (10 ug), Naldixic acid (30 ug), Erythromycin (15 ug), Chloramphenicol (30 ug) and Sulfamethoxazole (25 ug), Tetracycline (30 ug) by Oxoid. Three colonies of Campylobacter organisms were inoculated into tubes containing 5 ml Muller Hiton broth (Oxoid), then incubated for eight hours under reduced oxygen tension at 37°C. The turbidity was adjusted to match that of the standard McFarland 0.5 barium sulfate tube (0.5 ml of 1.175% barium chloride hydrate at 99 ml of 1% sulfuric acid) by adding sterile saline solution. The suspension was then inoculated evenly on 150-mm Mueller-Hinton agar plates supplemented with 5% defibrinated sheep blood Antibiotic disc were placed on the surface of agar plate in a radial pattern with the lowest concentration toward the

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center. The plates were incubated for 72 h. at 37°C under the microaerophilic conditions, and the inhibitory zone diameters were measured.

RESULTS

The prevalence of C. jejuni and C. coli in rectal swab samples collected from calves and lambs (Table 1).

Isolates of C. jejuni were recovered from 11 (23.4%) of the 47 diarrheic calves which was significantly higher than from 13 (10.83%) of the 120 apparently healthy calves. Total number of positive samples for C. jejuni was 24 (14.37% of 167 rectal swab samples from calves. C. coli was recovered from 7 (17.82%) of the 47 diarrheic calves which was significantly higher than apparently healthy calves (6.67%). Totally, C. coli was isolated from 15 (8.98%) of examined samples of calves.

Isolates of C. jejuni were recovered from 6 (12.24% of the 49 diarrheic lambs and from 7 (7.52% of 93 apparently healthy sheep. Totally, C. jejuni was isolated from 13 (9.15%) of 142 lamb's fecal samples. C. coli was recovered from 4 (8.16%) of the diarrheic lambs and from 6 (6.45%) of apparently healthy sheep. Totally, C. coli was isolated from 10 (7.04%) of samples collected from lambs.

Table 1: Prevalence of Campylobacter jejuni and Campylobacter coli in rectal swab samples collected from calves and lambs.

C. jejuni

C. coli Animal

No of No of % of No of No of % of

samples +ve +ve samples +ve +ve Cattle | Diarrhea 47 / 11 / 23.4 47 7 17.82

Healthy 120 13 10.83 120 86.67 Total

167 24 14.37 167 / 15 8.98 X

4.34

2.08 0.037 (P<0.05)

0.094 (P>0.05) Diarrhea 49 16 | 12.24

4 8.16 Healthy 93 7 7.52 93 6 6.45 Total

142 13 9.15 142 10 7.04 x

0.86

0.14 0.354 (P>0.05)**

0.705 (P>0.05) x is chi square

P is probability * Significant difference ** Approach significance

*** Non significant

Sheep

49

Гр

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In-vetro antimicrobial sensitivity

As shown in Table (2), C. jejuni isolated from cattle and sheep were sensitive to Chloramphenicol (100%) followed by Gentamycin and Neomycin. All C. jejuni isolated from cattle and sheep were resistant to Sulfamethoxazole, Penicillin, Ampicillin, Erythromycin and Tetracycline.

As shown in Table (3), all C. coli isolated from cattle were sensitive to Chloramphenicol followed by Gentamycin and Neomycin but show high resistance to Erythromycin, Tetracycline, Penicillin, Sulfamethoxazole, Ampicillin and Naldixic acid. The percentages of resistant strains were higher in C. coli than C. jejuni

Table 2: Antimicrobial sensitivity of Campylobacter jejuni isolated

from calves (n=10) and lambs (n=10):

0

7

70

30

Antimicrobial

Calves

Lambs Sensitive Moderate | Resistant Sensitive Moderate Resistant No % No % No

No % No

No Neomycin

16 604 4000 550 55000

6 60 / 4 Gentamycin

70

30 o

3 Ampicillin

002 208 1800 101 10990 Erythromycin

0 0 330 77000220 880 Chloramphenicol 9 90 1 100 019 90 110 00 Nalidixic acid 1 10 13 30 6 600 0 4 406 60 Sulfamethoxazole 0 0 2 20 8 800 0 2 | 2018 | 80 Tetracycline

0 0 1 10 9 900 0 2 201 8 80 penicillin

0 0 0 0 10 100 0 0 0 0 10 100 n=number of examined isolates.

0

Table 3: Antimicrobial sensitivity of Campylobacter coli isolated from

calves (n=10) and lambs (n=10):

20 0

9

Antimicrobial

Calves

Lambs Sensitive Moderate Resistant Sensitive Moderate Resistant

No % No % No 1 % No % No % No % Neomycin 1660 1330 110 5503

2 Gentamycin 770 220 110 6604 Ampicillin 002 208 80001

90 Erythromycin 0 0 1 10 9 90 100 1 10 9 90 Chloramphenicol 7

0 Nalidixic acid TOTO 2 | 2018 | 80 OTOTI10 9 90 Sulfamethoxazole 001 10 990 002 208 80 Tetracycline

0 0 1 10 9 900 101 109 90 penicillin 10 0 0 0 10 100 0 0 0 0 10 100

n=number of examined isolates.

o

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DISCUSSION

I

Campylobacter spp. have been recognized as a cause of diarrhea in cattle and sheep (Radoststits et al., 2000). In this study, rectal swab samples were collected from calves and lambs with and without diarrhea and used for isolation of C. jejuni and C. coli.

As shown in Table (1) C. jejuni was isolated from 24 out of 167 examined samples of calves (14.37%). Nearly similar isolation rates were reported by Hoar et al. (1999) and Beach et al. (2002). However, higher isolation rates were reported by Adesiyun et al. (1992), Giacoboni et al. (1993) and Pezzato et al. (2003) who isolated C. jejuni at rates from 11 to 54%. On the contrary lower rates of isolation were reported by Das et al. (1993) and Rosef et al. (1983). The prevalence of Campylobacter species in cattle varies from very low to 100% (Rosef et al., 1983; Warner et al., 1986 and Busato et al., 1999). The difference in prevalence may be due to epidemiological situation, season, the age of animals, and the method of diagnosis (Busato et al., 1999 and Sato et al., 2004).

The data presented in Table (1) revealed that C. jejuni was isolated from examined sheep samples at a percentage of 9.15%. This bacteria was isolated from sheep feces by many previous studies like Turkson et al. (1988) and Adesiyun et al. (1992).

The results illustrated in Table (1) showed that C. coli was isolated from examined samples of calves and lambs at a percentage of 8.98 and 7.04%, respectively. Nearly similar result was recorded by Terzolo (1988) and Kakkar and Dogra (1990), and lower result was reported by Rosef et al. (1983). On the other hand higher result was recorded by Terzolo (1988) and Giacoboni et al. (1993).

The prevalence of C. jejuni was higher than C. coli in calves and lambs (Table 1). This support the observation of Rosef et al. (1983) and Busato et al. (1999) who reported that C. coli is less frequently involved in animal than C. jejuni. However, the epidemiological features of both are similar and some times not further differentiated in the literature (Busato et al., 1999).

As shown in Table (1), the prevalence of C. jejuni and C. coli was significantly higher in calves and lambs suffering from diarrhea. The study provided evidence of significant associations between diarrhea and infection with C. jejuni and C coli. This support the observations of previous studies where; Diker et al. (1990); Busato et al. (1998), Acha et al. (2004) and Dodson and Lejeune (2005) who isolated

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Campylobacter from enteric diseases in calves. Further more, in experimental study, oral inoculation of campylobacter was able to produce enteritis in calves (Al-Mashat and Taylor, 1983). Kerr (2004) mentioned that C. jejuni can cause mild to moderate diarrhea in calves that is often thick and contain mucous and or blood. In the other hand, Busato et al. (1998) could not find differences in prevalence of C. jejuni between healthy and diseased calves. This result (no significant differences between diarrheic and healthy) was observed in sheep in this study (Table 1).

Campylobacteriosis is acute or chronic infection of humans and animals, transmission from animals to human has been known for C. jejuni and C. coli. The infection in man manifested by acute enteritis, abdominal pain, diarrhea in most cases stool contain blood, pus or mucous, fever up to 40 °C and in few cases vomiting. Abdominal symptoms may lead to laparotomy or appendectomy (Acha and Szyfers, 1991, Shakespeare, 2002 and Hartmut et al., 2003).

An in-vetro antibiotic sensitivity test was done against isolated strains of Campylobacter using a panel of 9 antibiotics (Table, 2 and 3). C. jejuni and C. coli were sensitive to Chloramphenicol. This support the data reported by Diker et al., (1990) who treated cases of bovine diarrhea due to Campylobacter successfully with Chloramphenicol. In addition, high percentage of isolates of C. jejuni and C. coli were resistant to Ampicillin, Penicillin, Tetracycline, Erythromycin, Naldixic acid and Sulfamethoxazole but drug resistance was more frequent in C. coli than C. jejuni. These findings are agree with that recorded by Thwaites and Frost (1999), Chuma et al. (2001) and Bae et al. (2005) who reported hat there are multiple-antibiotic resistance in C. coli, but disagree with Leatherbarrow (2004) who demonstrated that there was a very low prevalence of resistance among the C. coli isolates. It is known that C. jejuni and C. coli have different susceptibility profiles, but resistance traits are known to be readily transferred among species of Campylobacter (Bodeis et al., 2002 and Sato et al., 2004).

However, because of the susceptibility tests for Campylobacter species are not standardized and the use of antibiotics in the animals may promote the emergence of multi-antibiotic resistant mutant of campylobacter species (Betty et al., 1998 and Shakespeare, 2002). In addition, Campylobacter is one of the microorganisms of moderate intrinsic susceptibility which require only one mutation to become resistant (Wiedemann and Heisig, 1994).

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In conclusion:

Due to the presence of Campylobacter in the small intestine of diarrhea calves, a contribution of these bacteria within the pathogene of calf diarrhea is possible. Final evaluation of their pathogenic importance is only positive by means of virulence tests. The results of this study demonstrate that C. jejuni is widely distributed among cattle farms, while C. coli is narrowly distributed but significantly more resistant to antimicrobial. In addition, calves and lambs especially those suffering from diarrhea are a potential source of C. jejuni and C. coli for human, which can be transmitted to man in-contact. So, the following hygienic measures should be under-taken, periodical cleaning and disinfection of animal houses, hand washing and immersion in a mild antiseptic after handling of infected animals, hygienic disposal of animal excreta and attention should be paid to food and water given to animals.

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