Review Article

 

Campylobacter in Dogs and Cats; Its detection and Public Health Significance: A Review

 

Mohammed Dauda Goni1*, Ibrahim Jalo Muhammad2, Mohammed Goje3, Mustapha Goni Abatcha4, Asinamai Athliamai Bitrus5, Muhammad Adamu Abbas6

1Unit of Biostatistics and Research Methodology, Universiti Sains Malaysia, Health Campus, 16150 Kubang Kerian Kelantan, Malaysia; 2Ministry of Agriculture and Environment, IBB Secretariat Complex, Damaturu Nigeria; 3Department of Public Health and Preventive Medicine, Faculty of Veterinary Medicine, University of Maiduguri, Nigera; 4Food Technology Division, School of Industrial Technology, Universiti Sains Malaysia, 11800 Minden, Penang, Malaysia; 5Department of Pathology and Microbiology, Faculty of Veterinary Medicine, Universiti Putra Malaysia, 43400 Selangor, Malaysia; 6Department of Human Physiology, College of Health Sciences, Bayero University Kano, Nigeria..

 

Editor | Kuldeep Dhama, Indian Veterinary Research Institute, Uttar Pradesh, India.

Received | April 04, 2017; Accepted | May 29, 2017; Published | June 09, 2017

*Correspondence | Mohammed Dauda Goni, Unit of Biostatistics and Research Methodology, Universiti Sains Malaysia, Health Campus, 16150 Kubang Kerian Kelantan, Malaysia; Email: [email protected].

Citation | Goni MD, Muhammad IJ, Goje M, Abatcha MG, Bitrus AA, Abbas MA (2017). Campylobacter in dogs and cats; its detection and public health significance: A review. Adv. Anim. Vet. Sci. 5(6): 239-248.

DOI | http://dx.doi.org/10.17582/journal.aavs/2017/5.6.239.248

ISSN (Online) | 2307-8316; ISSN (Print) | 2309-3331

Copyright © 2017 Goni et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

 

INTRODUCTION

 

The genus Campylobacter is complex and diverse group of bacteria. Presently, the genus comprised of 25 species, two provisional species and eight subspecies (Man, 2011).The first Campylobacter was isolated from human in 1938 from blood samples of diarrhoeic patients (Butzler, 2004). Campylobacter were initially classified under the genus Vibrio but subsequently they were divided into three different but related genera: Campylobacter, Helicobacter and Arcobacter. They are gram negative, curved, spiral or S- shaped and are members of the order Campylobacterales, class Epsilon andphylum Proteobacteria.Campylobacter was differentiated from the genus Vibrio because they possessed some features particularly in the DNA base composition, their non-fermentative metabolism and growth under microaerophilic nature (Kersters et al., 2006).

 

Two veterinary surgeons in 1909, McFadyean and Stockman, surveyed epizootic abortions in ovine and they isolated an unknown bacterium from aborted foetuses which resembled a Vibrio (Butzler, 2004). In 1919, a scientist named Smith investigated infectious abortions of bovines in the United States and isolated a bacterium that was described as a Spirillum (Smith, 1919). After completing the study, Smith became familiar with the study of McFadyean and Stockman, and assumed what they had been studying were on similar bacteria. The first full report of Campylobacter enteritis in human was published in 1979, and later in the 1980s it was described that serotyping techniques aided by biotyping, phage typing and genotyping form the backbone of strain typing. Campylobacter jejuni was recognised in the mid-1980s as the most frequent cause of bacterial enterocolitis in man (Lior et al., 1982)

 

The breakthrough in the isolation of Campylobacter from faeces occurred in 1972 in a Veterinary research institute in Belgium. This success resulted in further general surveys from which related Vibrio were isolated from most children with diarrhoea but less from those without diarrhoea (Dekeyser et al., 1972). In 1931, it was attributed that winter dysentery in calves was due to infection with a ‘vibrio’ that they called Vibrio jejuni, and Doyle described a relevant microbe associated with swine dysentery in 1944 as the present Campylobacter (Jones et al., 1931). This advancement led to the development of selective media for the isolation of Campylobacter which became a routine in clinical microbiology (Skirrow, 1977). In 1973, Véron and Chatelain published the first taxonomic classification of Campylobacter recognising V. jejuni and V. coli in the system of classification of the genus (Herbet et al., 1982).

 

Natural Reservoirs

 

Poultry meat is considered as the primary source of Campylobacter (Skirrow, 1977). Other studies have indicated that other animals including dogs, cats and also wild birds, pigs, sheep, and cows, among others have been shown to be reservoir host for Campylobacter and it has also been isolated from faeces of exotic pets such as turtles, hamsters and monkeys (Blaser er al., 1980; Fox et al., 1983; Harvey and Greenwood, 1985; Simpson et al., 1981; Stern et al., 1992). Campylobacter was isolated from beef, rabbit meat and in pork (Little et al., 2008; Wilson et al., 2008). Beetles are also reported as vectors for Campylobacter to broiler chickens at rearing facilities (Skov et al., 2004). Certain species of Campylobacter are associated with a particular host. Dogs and cats have been shown to be associated with C. helviticus and C. upsaliensis, whileC. coli, C. hyointestinalis, and C. mucosalis are more often isolated from pigs and C. fetus subsp. fetus has been more commonly found in the intestines of sheep and cattle. Campylobacter lanienae has been found in faecal samples of cattle. Most wild birds harbour many species of thermophilic Campylobacter species (Baker et al., 2008; Blaser et al., 1983; Gebhart et al., 1983; Hatch, 1996; Inglis and Kalischuk, 2003; Kapperud and Rosef, 1983; Manser and Dalziel, 1985; Moore et al., 2002, Pearce et al., 2003).

 

Drinking water has also been incriminated as a source for the transmission of Campylobacter in cows (Hanninen et al.,1998).

 

Phenotypic and Biochemical Properties

 

Phenotypically, Campylobacter are slender, curved or spiral-rod shaped bacteria under phase contrast microscopy and measure 0.2-0.5mm wide and 0.5-8mm long with a single polar flagellum at one end that gives them the unique “cork screw” motility (Corry et al., 2001). They can be found in pairs or in chains, appearing as S- shaped or gull winged and may form coccoid or spherical bodies in aged cultures, usually more than 48 hours old. The gull wing gives them a darting motility (Vandamme et al., 1991). The optimum growth requirement for this organism is under microaerophilic conditions of 3% to 15% O2 and 3% to 10% CO2 and incubation is most suitable at 420C, however non-thermophilic species are isolated at 370C (Weese, 2011). Thermophilic Campylobacter such as C. jejuni, C. lari, C.upsaliensis and C. coli are able to grow between 370C and 42°C, but incapable of growth below 30°C with an optimum temperature of 41.5°C. While non-thermophillic Campylobacter such as C. hyointestinalis, C. helviticus, C. mucosalis and C. gracilis. (Bester et al., 2016).

 

When subjected to oxidase test, all species of Campylobacter are positive with the exception of C. gracilis and non-spore forming Campylobacter. The G+C content of DNA of members of this genus is relatively low ranging from 29 – 46 mol% (Harvey and Greenwood, 1985). The members are also indole negative and the activities of catalase and nitrate reduction vary with the species involved (Ursing et al., 1983).

 

Catalase activity on C. upsaliensis is either negative or weakly positive and has the ability to reduce nitrates to nitrites. However, hippurate and urea are not hydrolyzed and therefore there is no production of H2S in iron/metabisulphite medium or triple sugar iron agar. Most Campylobacter grow in 1% glycine and 1% bile and majority are capable of anaerobic growth in the presence of 0.1% trimethylamine N-oxide hydrochloride.

 

Methods of Identification and Detection

 

Culture based methods for Campylobacter

 

The isolation of Campylobacter from faecal samples is difficult because the plates are easily overgrown by commensals of the flora of the faeces and by the fact that Campylobacter are fastidious (Kulkarni et al., 2002). Enrichment broths are commonly used rather than direct plating and may increase the rate of detection by 30% compared to Campylobacter Blood Free Selective Agar (CCDA) alone (Baker et al., 1999; Maher et al., 2003; Acke et al., 2009). However, isolation using an enrichment procedure also has its shortcomings as it is known to result in a higher bacterial load

 

Table 1: Phenotypic and biochemical properties of Campylobacter species

 

Species	Catalase	Oxidase	Growth at:		Urease	Hydrolysis of:
			250C	420C		Hippurate	Indoxyl acetate
C. coli	+	+	_	+	_	_	+
C. concisus	_	_	_	V	_	_	_
C. curvus	_	V	_	V	_	V	V
C. fetus subsp. fetus	+	+	+	V	_	_	_
C. gracilis	V	_	_	V	_	_	V
C. helviticus	_	V	_	+	_	_	+
C. hyointestinalis subsp. hyointestinalis	+	V	V	+	_	_	_
C. jejuni subsp doyley	V	+	_	_	_	+	+
C. jejuni subsp. Jejuni	+	+	_	+	_	+	+
C. lari	+	+	_	+	V	_	_
C. mucosalis	_	_	_	+	_	_	_
C. sputorum	V	V	_	+	V	_	_
C. upsaliensis	_	+	_	V	_	_	+

 

+: positive reaction; -: negative reaction; V: variable reaction

Sources: (On, 1996; Yamazaki-Matsune et al., 2007)

 

flora which can contaminate the plates and also prolong the incubation time (Fleming, 1983).

 

There is no standard method for the isolation of the Campylobacter species based on culture methods and techniques employed differ among laboratories. In 1972, Butzler used the membrane filtration technique for the isolation of the organism from faeces (Dekeyser et al., 1972). Isolation of the organism became easier when Skirrow in 1977 introduced a selective medium for the isolation of C. jejuni and C.coli which are the main causes of Campylobacter gastroenteritis (Skirrow, 1977).

 

Basically two methods are often used for the isolation of Campylobacter from culture based methods which are culture on a selective agar after a filtration step and culture without filtration. A 0.45µm pore sized cellulose triacetate membrane filter is used for the culture method using membrane filtration as described by (Steel and Mc Dermott, 1984). Samples are prepared as suspension using Brucella broth or normal saline. Few drops of the suspension are then placed on the surface of the membrane filter which is placed on the blood agar media and allowed to filter passively through the membrane filter for 20-30 minutes. The pores of the membrane filter allow only the passage of Campylobacter which are relatively slender in size while other bacteria and facultative anaerobes are excluded (Modolo and Giuffrida, 2004). No antibiotic is used on the blood agar which facilitates the growth of cultivatable Campylobacter in the sample. The inoculated plates are then incubated at 370C for non-thermophilic and 420C for thermophilic Campylobacter under microaerophilic conditions for 48h. Suspected Campylobacter colonies are subcultured on selective media. On the contrary, some studies found that membrane filtration has the limitation that it could not detect co-infection of Campylobacter species because smaller sized organisms can be filtered through (Goossens et al., 1990; Koene et al., 2004).

 

For the culture of Campylobacter on selective media without filtration, faecal samples are streaked directly onto a selective blood free agar (such as charcoal cefoperazone deoxycholate agar CCDA) supplemented with antibiotics and incubated under microaerophilic conditions at 42oC for 48h. After incubation, suspected colonies are cultured on blood agar filter and isolates are identified by Gram stain, motility and biochemical tests as shown in Table 1 (Chon et al., 2014).

 

The Capetown protocol is employed to detect the presence of non-jejuni and non-coli Campylobacter. In this method, it combines procedures of culturing the sample on antibiotic free blood agar using the membrane filtration and incubation under microaerophilic environment. In 1977 in South Africa, the adoption of this method increased the rate of isolation of Campylobacter from 7.1% to 21.8% (Coker et al., 2002). The incubation period for the isolation of Campylobacter is significant because certain species like C. jejuni can be grown in 48 h while C. upsaliensis requires 96h to grow (Jamie et al., 2002). This effect was shown by (Hald et al., 2004) who found higher occurrence of C.jejuni when compared to C. upsaliensis and later found C. upsaliensis higher in occurrence than C. jejuni when the incubation period was extended to 96h although the different population sampled may also be a factor for the variation in the results (Hald et al., 2004). Temperature too has a vital role in the detection of Campylobacter species which ranges between 370C and 420C equivalent to the body temperature of humans and chicken respectively (Engvall et al., 2003).

 

Molecular Detection of Campylobacter

 

Several studies conducted on the detection of the presence of Campylobacter are cumbersome culture-based methods that are known to have low recovery yields and to potentially underestimate the number of species in a given sample because of their fastidious growth requirements. Biochemical test depend on biochemical pathways and their disruption can lead to product failure leading to false result. These results give unclear prevalence and densities of Campylobacter species (Yamazaki-Matsune et al., 2007). Hippurate hydrolysis is the most popular phenotypic characterisation test that is used to distinguish between C. jejuni and the other Campylobacter species including C. coli however the test could provide false negative responses (Van Dyke et al., 2010).

 

In the recent years a rapid, simple and practical molecular assay for the identification of Campylobacter species has been sought. This is important due to their low cost and potential application in large scale screening programs. (Denis et al., 1999) observed that biochemical test provide only 34% efficiency compared to 100% with the PCR. This approach has significantly increased the detection frequency of C. jejuni (8.1% versus 5.3%) and recovery rates of C. jejuni were significantly increased with the molecular screening approach-guided culture in comparison to conventional culture (Humphries and Linscott, 2015).

 

Different PCR assays have been developed and designed using single primer sets to detect and identify Campylobacter species (Inglis and Kalischuk, 2003; Wang et al., 2002; Klena et al., 2004) developed two multiplex PCR assay that are sophisticated approach in the simultaneous detection and identification of Campylobacter that were effectively used. The findings of the various studies showed PCR techniques to be effective, precise and quick in the diagnosis of Campylobacter (Vilardo et al., 2006).

(Steinbruecker et al., 2001) compared three different methods for Campylobacter identification which included normal biochemical techniques, Gas Liquid Chromatography (GLC) and PCR, and noted PCR techniques to be the most sensitive method. PCR tests have been developed for the detection and identification directly from pathological and food sample (Abu-Halaweh et al., 2005). This method is accurate, automated and robust like all other real-time PCR. In addition, it is more cost-effective compared to the two-tube real-time assay, which is also a time consuming assay.

 

Identification of Campylobacter species is important for epidemiological and antibiotic resistance surveillance purposes (Steinbrueckner et al., 2001). Several methodologies have been documented for identification of Campylobacter thatinclude using rRNA gene sequences multiplex PCR with gyrA and pflA genes or the cadF and ceuE gene (Nayak et al., 2005; Gorkiewicz et al., 2003). Multiplex real-time PCR has been used for rapid detection and identification of C. coli and C. jejuni from other Campylobacter species, employing a TaqMan probe targeting three different genes, orfA, hipO, and 16S rRNA respectively. 23S rRNA, ceuE, and mapA are frequently used genes for PCR confirmation of C. jejuni and C.coli (Gonzalez et al., 2000).

 

A colony multiplex PCR was developed and optimized to simultaneous identify the 23S rRNA from Campylobacter spp.; the hipO gene (hippuricase) from C. jejuni subsp. jejuni; the glyA gene (serine hydroxymethyltransferase) from C. coli, C. lari, and C. upsaliensis; and the sapB2 gene (surface layer protein) from C. fetus subsp. fetus. The multiplex PCR protocol was capable of detecting the type strains and clinical isolates from all five species with a high degree of specificity (Wang et al., 2002).

Campylobacter species can be detected by PCR assays using single primer (monoplex PCR) set that have been developed and also using multiple primers (multiplex PCR) for detecting several species (Yamazaki-Matsune et al., 2007; Inglis and Kalischuk, 2003).

 

Epidemiology

 

Prevalence of Campylobacter

 

Campylobacter is now regarded as the most frequent cause of food poisoning in humans and these bacteria are found in the digestive tract of most domestic animals. They are ubiquitous and can be found in various places and habitats including farms, urbanised areas, slaughter houses, companion animals, water, wild birds, mammals and farm production animals. The prevalence can be high in cattle, swine and poultry exceeding 80% from faecal samples (Economou et al., 2015; Aung et al., 2015: Stanley and Jones, 2003).

 

Household pets are known to be carriers of Campylobacter spp. in their guts, with incidences as high as 92% in stool samples when analyzed either through culturing or molecular methods such as PCR and PFGE (Hald et al., 2004; Waldenstrom et al., 2002). The carriage rate in stray dogs was higher (23.8%) than the pet dogs (2.7%) with C. jejuni (86.8%)most commonly isolated followed by C. upsaliensis (9.3%) then C. coli (3.9%) in a study done in Taiwan (Tsai et al., 2007). Studies conducted in Denmark and Spain on canine species showed carriage rates of C. jejuni at 20.1% and 35.2% respectively while C. upsaliensis constituted the majority of the isolates at 75% and 58.8% respectively (Carbonero et al., 2012). Campylobacter upsaliensis, C.jejuni and C.helveticus are most common species of Campylobacter in dogs and cats, however multiple species can be harboured at the same time in a single dog or cat (Hald et al., 2004; Koene et al., 2004; Moser et al., 2001; Shen et al., 2001).

 

Table 2: Prevalence rate of Campylobacter species across the globe from different studies

 

Author	Prevalence	Species isolated	Country
Baker et al., 1999	Dogs 43% (43/289) Cats 7.6 % (15/195)	Dogs: C. upsaliensis, C. jejuni and C. coli Cats: C. jejuni and C. upsaliensis	Australia
Steinhauserova et al., 2000	15.1% (19/126)	C. upsaliensis, C. jejuni and C. coli	Czech Rep.
Workman et al., 2005	Dogs 46.9% (61/130) Cats 37.3% (19/51)	Dogs: C. jejuni, C. coli and C. helviticus Cats: C. upsaliensis and C.helviticus	Barbados
Carbonero et al., 2012	102/290 (35.2%)	C. jejuni and C.upsaliensis	Spain
Parsons et al., 2010	38% (96/249)	C. jejuni and C.upsaliensis	UK
Engvall, 2003	45/84 (53.6%)		Sweden
Hald, 2004	278/366 (76.0%)		Denmark
Tsai, 2007	2.8% (27/928)	C. upsaliensis, C. jejuni and C. coli	China
Stavisky, 2011	42.9% (63/147)		UK
Rossi, 2008	19/63 (30.2%)	Dogs: C. upsaliensis, C. jejuni, C. helveticus and C. lari Cats: C. helveticus, C. jejuni and C. upsaliensis	Italy
Kumar, 2012	51% (50/100)		India
Rodrigues et al., 2015	Dogs 19.4% (20/103) Cats 11.7% (2/17)	Dogs: C. jejuni and C. coli Cats: C. coli	Brazil
Karshima, 2016	81/341 (23.8%)	C. jejuni and C. coli	Nigeria
Bojanić et al., 2016	Dogs 36% Cats 16%	Dogs: C. jejuni, C. upsaliensis, C. lariandCampylobacter helveticus Cats: C. jejuni, C. upsaliensis, andC. helveticus	New Zealand
Mohammedet al., 2016	Dogs: 14.8% (15/101) Cats: 23.2% (20/86)	Dogs: : C. jejuni, C. upsaliensis, andC. helveticus Cats: C. jejuni, C. upsaliensis, andC. helveticus	Malaysia

 

The occurrence of Campylobacter from the faecal samples of children indicated 6.87% (11/160) of the faecal samples as positive for Campylobacter spp. However, a study conducted in Brazil on dogs and cats showed that 18.3% (22/120) of the pet samples tested were positive for Campylobacter spp. One hundred and twenty (120) faecal samples analysed were from 103 dogs and 17 cats with there carriage rate at 19.41% (20/103) and 11.7% (2/17) respectively (Rodrigues et al., 2015).

 

The zoonotic potential of Campylobacter from household pets to humans is still a major concern and is yet to be ascertained if it is transmitted through direct physical contact. However, it still remains a speculation but direct transmission of human with C. jejuni has been established. The prevalence of Campylobacter has been found to be higher in younger pets than older ones (Damborg et al., 2004; Hald et al., 2004). Similarly, in Nigeria a study conducted showed adult dogs and puppies recorded detection rates of 25.8% and 16.4% respectively while the prevelance rates by females and males respectively varied significantly (p<0.05, OR=0.4027, 95% CI=1.437-4.290) (Karshima and Bobbo, 2016). Various studies that reported the prevalence rate across the globe are shown in Table 2.

 

Public Health Significance

 

Campylobacter jejuni is the most common specie of Campylobacter isolatedfromdogs and cats, This is a vital result from a public health perspective, because C. jejuni is the species most frequently associated with human gastroenteritis (Moore et al., 2005). The campylobacteriosis of great public health importance is Campylobacter enteritis caused by C. jejuni and C. coli (Coker et al., 2002).The incidence of Campylobacter in human is high, and often infection is through consumption of contaminated raw or under-cooked meat products and other potential reservoirs. This disease is particularly observed during travelling and hence the term “travellers’ diarrhoea” (Sanders et al., 2002). In England and Wales, nearly 13,000 cases of travellers’ diarrhoea have been confirmed to be caused by C. coli (Tam et al., 2003).

 

In most developing countries, national surveillance programs for campylobacteriosis are lacking despite the substantial burden of disease (Fullerton et al., 2007). The majority of Campylobacter spp. are considered emerging organisms and have virulence genes typically found in known C. jejuni and coli indicating a role in human illness. Direct contact with animals including with kittens, puppies, cattle, chickens and pigs is a frequently identified risk factor for campylobacteriosis. Considering that asymptomatic carriage is very common in these animals, risk through direct exposure is not surprising (Friedman et al., 2004). Campylobacter can be found in water especially untreated; their presence in surface water and shallow wells is likely due to contamination by wild bird faeces, manure run-off from dairy or poultry farms, or human sewage (Clark et al., 2003; Olson et al., 2008). Most cases of Campylobacter infections in man are often attributed to consumption of raw milk, undercooked poultry and meat are identified as the main reservoirs. Poor food hygiene that leads to cross-contamination of uncooked food can cause human disease (Gras et al., 2012; Wilson et al., 2008).

 

Antibiotic Resistance

 

Campylobacter species like other emerging zoonotic disease-causing organisms are reported to be increasingly resistant to antibiotics mainly due to their widespread overuse in animals (Tauxe, 1997). Antibiotics are often regarded as one of the wonders of the 20th century; however the wonders raised by the issue of antibiotic resistance cannot be overemphasized (Davies and Davies, 2010). The potential development of resistance by these microbes have compromised the benefits of antimicrobial agents (Davies and Davies, 2010). Resistant Campylobacter species can be transferred to humans through direct ingestion of conatminated food or through contact with animals. The World Health Organization has suggested a halt in use of antibiotic as growth promoters that belong to an antimicrobial class used in human medicine. The continued usage of excess antibiotics in animals makes animals more susceptible to acquisition of the resistant strains of the organism (Angulo et al., 2004). The public health consequences of antibiotic use in animals can be evaluated more importantly when consideration of each pathogen-antibiotic situation (Son, 2005). Multidrug resistance has been reported in both Campylobacter species from various studies (Kabeya et al., 2004; Son et al., 2007).

 

Prevalence of Antibiotic Resistant Campylobacter

 

Occurrence of Campylobacter varies according to animal species and geographical location, with poultry meat recording the highest prevalence compared to beef and pork. (Son et al., 2007) in a study in the United States at a poultry processing plant showed the prevalence of antibiotic resistant Campylobacter recovered from broiler carcasses to be 99.5% to one or more antibiotics. On the other hand 28.4% were resistant to two or more antibiotics for  Campylobacter (Son et al., 2007). The resistance displayed by Campylobacter to tetracycline was very high in C. jejuni (99.5%) and C.coli (96.3%).

 

Similarly, a study conducted in Slovenia showed the occurrence of antibiotic resistance was higher in C. coli (75.9 %) than in C. jejuni (38.5 %) isolates. The resistance rate observed to enrofloxacin, nalidixic acid, erythromycin and tetracycline were 58.2, 49.1, 14.5 and 12.7 %, respectively. Eleven percent of Campylobacter isolated were resistant to erythromycin and ciprofloxacin and 12.7 % of the isolates were resistant to tetracycline and quinolones (Kurincic et al., 2005).

 

(Mackiw et al., 2012) in his study showed the highest rate of antibiotic resistance of Campylobacter isolates at 97.9% to ciprofloxacin, 64.3% of the same isolates were resistant to tetracycline and 9.1% were resistant to erythromycin and 6.3% to gentamicin. However, 7.0% of the 143 resistant Campylobacter strains were found to be resistant to at least three unrelated antibiotics (Mackiw et al., 2012).

 

A study on the prevalence of antibiotic resistance in dogs conducted in India showed all the isolates of Campylobacter were resistant to streptomycin, ampicillin, amoxicillin, aztreonam, lincomycin, tetracycline, oxytetracycline and penicillin. Only 2 isolates out of the total isolates used in the study were resistant to the entire 19 antibiotic used. Isolates had a high rate of resistance (97.35%) to Cefotaxim, chloramphenicol, floxacin, ciprofloxacin, cefaclor, nitrofurazone, norfloxacin, gentamicin, amikacin and enrofloxacin (Kulkarni et al., 2002).

 

CONCLUSION

 

It can be concluded that the occurrence of Campylobacter species in dogs and cats is of great public health significance due to there close contact with humans and therefore they serves as potential reserviour for human campylobacteriosis. The prevalence rate vary across the globe. PCR is the most reliable and sensitive method of detection. Good management and controlling the population of stray dogs and cats are key factors in preventing the spread of Campylobacter in these animal species. Antibiotic resistance in Campylobacter not only increases the risk of treatment failure in both humans and animals but also spreads antibiotic resistance genes.

 

ACKNOWLEDGEMENT


 

The authors would like to acknowledge the USM Global Fellowship awarded to the first 
author. 


 

CONFLICT OF INTEREST

 

There is no conflict of interest in this review to declare.

 

AUTHORS’ CONTRIBUTION

 

All the authors contributed equally for plan of review, article collection and manuscript writing.

 

REFERENCE

 

Abu-Halaweh M., Bates J., Patel B. K. (2005). Rapid detection and differentiation of pathogenic Campylobacter jejuni and Campylobacter coli by real-time PCR. Res. Microbiol. 156(1): 107-114. https://doi.org/10.1016/j.resmic.2004.08.008

Acke E., McGill K., Golden O., Jones B., Fanning S., Whyte P. (2009). A comparison of different culture methods for the recovery of Campylobacter species from pets. Zoonoses and Public Health. 56(9‐10), 490-495. https://doi.org/10.1111/j.1863-2378.2008.01205.x

Angulo F., Nargund V., Chiller T. (2004). Evidence of an Association Between Use of Anti‐microbial Agents in Food Animals and Anti‐microbial Resistance Among Bacteria Isolated from Humans and the Human Health Consequences of Such Resistance. J. Vet. Med. Series B. 51(8‐9), 374-379. https://doi.org/10.1111/j.1439-0450.2004.00789.x

Aung W. W., Saleha A. A., Zunita Z., Murugaiyah M., Aliyu A. B., Goni D. M., Mohamed A. M. (2015). Occurrence of Campylobacter in Dairy and Beef Cattle and Their Farm Environment in Malaysia. Pakistan Vet. J. 35(4), 470-473.

Baker J., Barton M. D., Lanser J. (1999). Campylobacter species in cats and dogs in South Australia. Australian Vet. J. 77(10), 662-666. https://doi.org/10.1111/j.1751-0813.1999.tb13159.x

Baker J., Barton M. D., Lanser J. (2008). Campylobacter species in cats and dogs in South Australia. Australian Vet. J. 77(10): 662-666. https://doi.org/10.1111/j.1751-0813.1999.tb13159.x

Bester L. A., Khan N., Essack S. Y., Phulukdaree A. (2016). Efficacy of Phenotypic, PCR and MALDI-ToF Identification Methods for Campylobacter spp. Medical Technol. SA. 30(1): 49-51.

Blaser M. J., LaForce F. M., Wilson N. A., Wang W. L. L. (1980). Reservoirs for human campylobacteriosis. J. Inf. Diseases. 141(5): 665-669. https://doi.org/10.1093/infdis/141.5.665

Blaser M. J., Taylor D. N., Feldman R. A. (1983). Epidemiology of Campylobacterjejuni infections. Epidemiol. Rev. 5:157-176. https://doi.org/10.1093/oxfordjournals.epirev.a036256

Bojanić K., Midwinter A., Marshall J., Rogers L., Biggs P., Acke E. (2016). Isolation of Campylobacter spp. from Client‐Owned Dogs and Cats, and Retail Raw Meat Pet Food in the Manawatu, New Zealand. Zoonoses and public health. https://doi.org/10.1111/zph.12323

Butzler J. P. (2004). Campylobacter, from obscurity to celebrity. Clin. Microbiol. Infect. 10(10): 868-876. https://doi.org/10.1111/j.1469-0691.2004.00983.x

Carbonero A., Torralbo A., Borge C., García-Bocanegra I., Arenas A., Perea A. (2012). Campylobacter spp., C. jejuni and C. upsaliensis infection-associated factors in healthy and ill dogs from clinics in Cordoba, Spain. Screening tests for antimicrobial susceptibility. Comp. Immunol. Microbiol. Infect. Dis. 35(6): 505-512. https://doi.org/10.1016/j.cimid.2012.05.002

Chon J. W., Kim Y. J., Kim H. S., Kim D. H., Kim H., Song K. Y., Seo K. H. (2014). Supplementation of Bolton broth with triclosan improves detection of Campylobacter jejuni and Campylobactercoli in chicken carcass rinse. Int. J. Food Microbiol. 181: 37-39. https://doi.org/10.1016/j.ijfoodmicro.2014.04.006

Clark C. G., Price L., Ahmed R., Woodward D. L., Melito P. L., Rodgers F. G., Ellis A. (2003). Characterization of waterborne outbreak–associated Campylobacterjejuni, Walkerton, Ontario. Emerging Infect. Dis. 9(10): 1232. https://doi.org/10.3201/eid0910.020584

Coker A. O., Isokpehi R. D., Thomas B. N., Amisu K. O., Obi C. L. (2002). Human campylobacteriosis in developing countries. Emerging Infect. Dis. 8(3): 237-244. https://doi.org/10.3201/eid0803.010233

Corry J., Atabay H. (2001). Poultry as a source of Campylobacter and related organisms. J. App. Microbiol. 90(S6): 96S-114S.https://doi.org/10.1046/j.1365-2672.2001.01358.x.

Damborg P., Olsen K. E., Nielsen E. M., Guardabassi L. (2004) Occurrence of Campylobacterjejuni in pets living with human patients infected with C. jejuni. J. Clin. Microbiol. 42(3): 1363-1364. https://doi.org/10.1128/JCM.42.3.1363-1364.2004

Davies J., Davies D. (2010). Origins and evolution of antibiotic resistance. Microbiol. Mol. Biol. Rev. 74(3): 417-433. https://doi.org/10.1128/MMBR.00016-10

Dekeyser P., Gossuin-Detrain M., Butzler J., Sternon J. (1972). Acute enteritis due to related vibrio: first positive stool cultures. J. Inf. Dis. 125(4): 390-392. https://doi.org/10.1093/infdis/125.4.390

Denis, M., Soumet, C., Rivoal, K., Ermel, G., Blivet, D., Salvat, G., and Colin, P. (1999). Development of am‐PCR assay for simultaneous identification of Campylobacter jejuni and C. coli. Letters Appl. Microbiol. 29(6), 406-410.

Economou V., Zisides N., Gousia P., Petsios S., Sakkas H., Soultos N., Papadopoulou C. (2015). Prevalence and antimicrobial profile of Campylobacter isolates from free-range and conventional farming chicken meat during a 6-year survey. Food Control. 56: 161-168. https://doi.org/10.1016/j.foodcont.2015.03.022

Engvall E. O., Brändström B., Andersson L., Båverud V., Trowald-Wigh G., Englund L. (2003). Isolation and identification of thermophilic Campylobacter species in faecal samples from Swedish dogs. Scandinavian J. Infect. Dis. 35(10): 713-718. https://doi.org/10.1080/00365540310014558

Fleming M. (1983). Association of Campylobacterjejuni with enteritis in dogs and cats. Vet. Rec. 113(16): 372-374. https://doi.org/10.1136/vr.113.16.372

Fox J. G., Hering A. M., Ackerman J. I., Taylor N. S. (1983). The pet hamster as a potential reservoir of human campylobacteriosis. J. Inf. Dis. 147(4): 784. https://doi.org/10.1093/infdis/147.4.784

Friedman C. R., Hoekstra R. M., Samuel M., Marcus R., Bender J., Shiferaw B., Hardnett F. (2004). Risk factors for sporadic Campylobacter infection in the United States: a case-control study in FoodNet sites. Clin. Infect. Dis. 38(Supplement 3): S285-S296. https://doi.org/10.1086/381598

Fullerton K. E., Ingram L. A., Jones T. F., Anderson B. J., McCarthy P. V., Hurd S., Hayes T. (2007). Sporadic Campylobacter infection in infants: a population-based surveillance case-control study. Pediatr. Infect. Dis. J. 26(1): 19-24. https://doi.org/10.1097/01.inf.0000247137.43495.34

Gebhart C., Ward G., Chang K., Kurtz H. (1983). Campylobacterhyointestinalis (new species) isolated from swine with lesions of proliferative ileitis. American J. Vet. Res. 44(3): 361.

Gonzalez I., Garcia T., Antolin A., Hernandez P. E., Martin R. (2000). Development of a combined PCR‐culture technique for the rapid detection of Arcobacter spp. in chicken meat. Letters in Applied Microbiol. 30(3): 207-212. https://doi.org/10.1046/j.1472-765x.2000.00696.x

Goossens H., Vlaes L., De Boeck M., Levy J., De Mol P., Butzler J.-P., Vandamme P. (1990). Is “Campylobacterupsaliensis” an unrecognised cause of human diarrhoea? The Lancet. 335(8689): 584-586. https://doi.org/10.1016/0140-6736(90)90359-D

Gorkiewicz G., Feierl G., Schober C., Dieber F., Köfer J., Zechner R., Zechner E. L. (2003). Species-specific identification of campylobacters by partial 16S rRNA gene sequencing. J. Clin. Microbiol. 41(6): 2537-2546. https://doi.org/10.1128/JCM.41.6.2537-2546.2003

Gras L. M., Smid J. H., Wagenaar J. A., de Boer A. G., Havelaar A. H., Friesema I. H., van Pelt W. (2012). Risk factors for campylobacteriosis of chicken, ruminant, and environmental origin: a combined case-control and source attribution analysis. PLoS One. 7(8): e42599. https://doi.org/10.1371/journal.pone.0042599

Hald B., Pedersen K., Wainø M., Jørgensen J. C., Madsen M. (2004). Longitudinal study of the excretion patterns of thermophilic Campylobacter spp. in young pet dogs in Denmark. J. Clin. Microbiol. 42(5): 2003-2012. https://doi.org/10.1128/JCM.42.5.2003-2012.2004

Hänninen M. L., Niskanen M., Korhonen L. (1998). Water as a Reservoir for Campylobacterjejuni Infection in Cows Studied by Serotyping and Pulsed‐field Gel Electrophoresis (PFGE). J. Vet. Med. Series B. 45(1‐10): 37-42.

Harvey S., Greenwood J. (1985). Isolation of Campylobacterfetus from a pet turtle. J. Clin. Microbiol. 21(2): 260-261.

Hatch J. J. (1996). Threats to public health from gulls (Laridae). Int. J. Environ. Health Res. 6(1): 5-16. https://doi.org/10.1080/09603129609356867

Hébert G., Hollis D., Weaver R., Lambert M., Blaser M., Moss C. (1982). 30 years of campylobacters: biochemical characteristics and a biotyping proposal for Campylobacter jejuni. J. Clin. Microbiol. 15(6): 1065-1073.

Holmberg M., Rosendal T., Engvall E. O., Ohlson A., Lindberg A. (2015). Prevalence of thermophilic Campylobacter species in Swedish dogs and characterization of C. jejuni isolates. Acta Veterinaria Scandinavica. 57(1): 19. https://doi.org/10.1186/s13028-015-0108-0

Humphries R. M., Linscott A. J. (2015). Laboratory diagnosis of bacterial gastroenteritis. Clin. Microbiol. Rev. 28(1): 3-31. https://doi.org/10.1128/CMR.00073-14

Inglis G. D., Kalischuk L. D. (2003). Use of PCR for direct detection of Campylobacter species in bovine feces. Applied Environ. Microbiol. 69(6): 3435-3447. https://doi.org/10.1128/AEM.69.6.3435-3447.2003

Jaime A. L., Joan S., Lee B., Nancy S., Sydney M. H., Eleanor L., Laurene M. (2002). Campylobacterupsaliensis: another pathogen for consideration in the United States. Clin. Infect. Dis. 34(11), e59-e60. https://doi.org/10.1086/340266

Jones F., Orcutt M., Little R. B. (1931). Vibrios (Vibrio jejuni, n. sp.) associated with intestinal disorders of cows and calves. J. Exp. Med. 53(6): 853-863. https://doi.org/10.1084/jem.53.6.853

Kabeya H., Maruyama S., Morita Y., Ohsuga T., Ozawa S., Kobayashi Y., Mikami T. (2004). Prevalence of Arcobacter species in retail meats and antimicrobial susceptibility of the isolates in Japan. Int. J. Food Microbiol. 90(3): 303-308 https://doi.org/10.1016/S0168-1605(03)00322-2.

Kapperud G., Rosef, O. (1983). Avian wildlife reservoir of Campylobacterfetus subsp. jejuni, Yersinia spp., and Salmonella spp. in Norway. Appl. Environ. Microbiol. 45(2): 375-380.

Karshima S. N., Bobbo, A. A. (2016). Isolation and PCR Characterisation of Thermophilic Campylobacter Species in Dogs Presented to Selected Veterinary Clinics in Jos, Nigeria. Alexandria J. Vet. Sci. 50(1): 70-77. https://doi.org/10.5455/ajvs.221754

Kersters K., De Vos P., Gillis M., Swings J., Vandamme P., Stackebrandt, E. (2006). Introduction to the Proteobacteria. In The prokaryotes (pp. 3-37). Springer New York. https://doi.org/10.1007/0-387-30745-1_1

Klena J. D., Parker C. T., Knibb K., Ibbitt J. C., Devane P. M., Horn S. T., Konkel M. E. (2004). Differentiation of Campylobacter coli, Campylobacter jejuni, Campylobacter lari, and Campylobacter upsaliensis by a multiplex PCR developed from the nucleotide sequence of the lipid A gene lpxA. J. Clin. Microbiol. 42(12): 5549-5557. https://doi.org/10.1128/JCM.42.12.5549-5557.2004

Koene M., Houwers D., Dijkstra J., Duim B., Wagenaar J. (2004). Simultaneous presence of multiple Campylobacter species in dogs. J. Clin. Microbiol. 42(2): 819-821. https://doi.org/10.1128/JCM.42.2.819-821.2004

Kulkarni S., Lever S., Logan J., Lawson A., Stanley J., Shafi M. (2002). Detection of Campylobacter species: a comparison of culture and polymerase chain reaction based methods. J. Clin. Pathol. 55(10): 749-753. https://doi.org/10.1136/jcp.55.10.749

Kurincic M., Berce I., Zorman T., Mozina S. S. (2005). The prevalence of multiple antibiotic resistance in Campylobacter spp. from retail poultry meat. Food Tech. Biotech. 43(2): 157-163.

Lior H., Woodward D., Edgar J., Laroche L., Gill P. (1982). Serotyping of Campylobacterjejuni by slide agglutination based on heat-labile antigenic factors. J. Clin. Microbiol. 15(5): 761-768.

Little C., Richardson J., Owen R., De Pinna E., Threlfall E. (2008). Campylobacter and Salmonella in raw red meats in the United Kingdom: Prevalence, characterization and antimicrobial resistance pattern, 2003–2005. Food Microbiol. 25(3): 538-543. https://doi.org/10.1016/j.fm.2008.01.001

Maćkiw E., Korsak D., Rzewuska K., Tomczuk K., Rożynek E. (2012). Antibiotic resistance in Campylobacterjejuni and Campylobactercoli isolated from food in Poland. Food Ctrl. 23(2): 297-301.

Maher M., Finnegan C., Collins E., Ward B., Carroll C., Cormican M. (2003). Evaluation of culture methods and a DNA probe-based PCR assay for detection of Campylobacter species in clinical specimens of feces. J. Clin. Microbiol. 41(7): 2980-2986. https://doi.org/10.1128/JCM.41.7.2980-2986.2003

Man S. M. (2011). The clinical importance of emerging Campylobacter species. Nat. Rev. Gastroenterol. Hepatol. 8(12): 669-685. https://doi.org/10.1038/nrgastro.2011.191

Manser P., Dalziel R. (1985). A survey of Campylobacter in animals. Epidemiol. Infect. 95(1): 15-21. https://doi.org/10.1017/s0022172400062239

Modolo J. R. , Giuffrida R. (2004). Campylobacterupsaliensis isolated from young dogs with and without diarrhea. Rev. Sociedade Brasileira de Med. Trop. 37(1): 72-73. https://doi.org/10.1590/S0037-86822004000100021

Mohammed D. G., Saleha A. A., Dhaliwal G. K., Zakaria Z., Bitrus A. A., Jalo I. M., Aung W. W., Mohamed M. A., Aliyu A. B. (2016). Occurrence of Campylobacter in Dogs and Cats in Selangor Malaysia and Their Associated Risk Factors. Malaysian J. Microbiol. MJM839-16. In press

Moore J. E., Corcoran D., Dooley J. S., Fanning S., Lucey B., Matsuda M., O’Riordan L. (2005). Campylobacter. Vet. Res. 36(3): 351-382. https://doi.org/10.1051/vetres:2005012

Moore J. E., Gilpin D., Crothers E., Canney A., Kaneko A., Matsuda M. (2002). Occurrence of Campylobacter spp. and Cryptosporidium spp. in seagulls (Larus spp.). Vector Borne Zoonotic Dis. 2(2): 111-114. https://doi.org/10.1089/153036602321131913

Moser I., Rieksneuwöhner B., Lentzsch P., Schwerk P., Wieler L. (2001). Genomic Heterogeneity and O-Antigenic Diversity of Campylobacterupsaliensis and Campylobacterhelveticus Strains Isolated from Dogs and Cats in Germany. J. Clin. Microbiol. 39(7): 2548-2557. https://doi.org/10.1128/JCM.39.7.2548-2557.2001

Nayak R., Stewart T. M., Nawaz M. S. (2005). PCR identification of Campylobacter coli and Campylobacter jejuni by partial sequencing of virulence genes. Mol. Cell. Probes. 19(3): 187-193. https://doi.org/10.1016/j.mcp.2004.11.005

Olson C. K., Ethelberg S., Pelt W. v., Tauxe R. V., Nachamkin I., Szymanski C., Blaser M. (2008). Epidemiology of Campylobacterjejuni infections in industrialized nations. Campylobacter (Ed. 3), 163-189.

On S. (1996). Identification methods for campylobacters, helicobacters, and related organisms. Clin. Microbiol. Rev. 9(3): 405-422.

Parsons B., Porter C., Ryvar R., Stavisky J., Williams N., Pinchbeck G., Radford A. (2010). Prevalence of Campylobacter spp. in a cross-sectional study of dogs attending veterinary practices in the UK and risk indicators associated with shedding. Vet. J. 184(1): 66-70. https://doi.org/10.1016/j.tvjl.2009.01.009

Pearce R., Wallace F., Call J., Dudley R., Oser A., Yoder L., Luchansky J. (2003). Prevalence of Campylobacter within a swine slaughter and processing facility. J. Food Protect. 66(9): 1550-1556. https://doi.org/10.4315/0362-028X-66.9.1550

Rajesh Kumar R., Verma A. K., Kurnar A., Srivastava M., Lal H. P. (2012). Prevalence and Antibiogram of Campylobacter Infections in Dogs of Mathura, India. Asian J. Anim. Vet. Adv. 7(5): 434-440. https://doi.org/10.3923/ajava.2012.434.440

Rodrigues C. G., Melo R. T., Fonseca B. B., Martins P. A., Ferreira F. A., Araújo M. B., Rossi D. A. (2015). Occurrence and characterization of Campylobacter spp. isolates in dogs, cats and children. Pesquisa Veterinária Brasileira. 35(4): 365-370. https://doi.org/10.1016/j.matchar.2015.10.023

Rossi M., Hänninen M., Revez J., Hannula M., Zanoni R. (2008). Occurrence and species level diagnostics of Campylobacter spp., enteric Helicobacter spp. and Anaerobiospirillum spp. in healthy and diarrheic dogs and cats. Vet. Microbiol. 129(3): 304-314. https://doi.org/10.1016/j.vetmic.2007.11.014

Sanders J., Isenbarger D., Walz S., Pang L., Scott D., Tamminga C., Pitarangsi C. (2002). An observational clinic-based study of diarrheal illness in deployed United States military personnel in Thailand: presentation and outcome of Campylobacter infection. American J. Trop. Med. Hygiene. 67(5): 533-538. https://doi.org/10.4269/ajtmh.2002.67.533

Shen Z., Feng Y., Dewhirst F., Fox J. (2001). Coinfection of Enteric Helicobacter spp. and Campylobacter spp. in Cats. J. Clin. Microbiol. 39(6): 2166-2172. https://doi.org/10.1128/JCM.39.6.2166-2172.2001

Simpson J., Burnie A., Ferguson S., Brunton W. A. T. (1981). Isolation of thermophilic campylobacters from two populations of dogs. Vet. Res. Commun. 5(1): 63-66. https://doi.org/10.1007/BF02214969

Skirrow M. (1977). Campylobacter enteritis: a” new” disease. Brit. Med. J. 2(6078): 9. https://doi.org/10.1136/bmj.2.6078.9

Skov M., Spencer A., Hald B., Petersen L., Nauerby B., Carstensen B., Madsen M. (2004). The role of litter beetles as potential reservoir for Salmonellaenterica and thermophilic Campylobacter spp. between broiler flocks. Avian Dis. 48(1): 9-18. https://doi.org/10.1637/5698

Smith T. (1919). The etiological relation of Spirilla (Vibrio fetus) to bovine abortion. J Exp. Med. 30(4): 313-323. https://doi.org/10.1084/jem.30.4.313

Son I. (2005). Prevalence, genetic diversity and antimicrobial resistance patterns of Arcobacter and Campylobacter on broiler carcasses during processing (Doctoral dissertation, University of Georgia).

Son I., Englen M. D., Berrang M. E., Fedorka-Cray P. J., Harrison M. A. (2007). Antimicrobial resistance of Arcobacter and Campylobacter from broiler carcasses. Int. J. Antimicrob. Agents. 29(4): 451-455. https://doi.org/10.1016/j.ijantimicag.2006.10.016

Stanley K., Jones K. (2003). Cattle and sheep farms as reservoirs of Campylobacter. J. Appl. Microbiol. 94(s1): 104-113. https://doi.org/10.1046/j.1365-2672.94.s1.12.x

Stavisky J., Radford A. D., Gaskell R., Dawson S., German A., Parsons B., Pinchbeck G. (2011). A case–control study of pathogen and lifestyle risk factors for diarrhoea in dogs. Prevent. Vet. Med. 99(2): 185-192. https://doi.org/10.1016/j.prevetmed.2011.02.009

Steele T. W., McDermott S. N. (1984). The use of membrane filters applied directly to the surface of agar plates for the isolation of Campylobacterjejuni from feces. Pathol. 16(3): 263-265. https://doi.org/10.3109/00313028409068535

Steinbrueckner B., Ruberg F., Kist M. (2001). Bacterial Genetic Fingerprint: a Reliable Factor in the Study of the Epidemiology of HumanCampylobacter Enteritis?. J. Clin. Microbiol. 39(11): 4155-4159. https://doi.org/10.1128/JCM.39.11.4155-4159.2001.

Steinhauserova I., Fojtikova K., Klimes J. (2000). The incidence and PCR detection of Campylobacterupsaliensis in dogs and cats. Letters Appl. Microbiol. 31(3): 209-212. https://doi.org/10.1046/j.1365-2672.2000.00799.x

Stern N., Nachamkin I., Blaser M., Tompkins L. (1992). Reservoirs for Campylobacterjejuni and approaches for intervention in poultry. American Society Microbiol. Washington, DC(USA). 1992.

Tam C., O’Brien S., Adak G., Meakins S., Frost J. (2003). Campylobactercoli—an important foodborne pathogen. J. Infect. 47(1): 28-32. https://doi.org/10.1016/S0163-4453(03)00042-2

Tauxe R. V. (1997). Emerging foodborne diseases: an evolving public health challenge. Emerg. Inf. Dis. 3(4): 425. https://doi.org/10.3201/eid0304.970403

Tsai H.-J., Huang H.-C., Lin C.-M., Lien Y.-Y., Chou C.-H. (2007). Salmonellae and campylobacters in household and stray dogs in northern Taiwan. Vet. Res. Commun. 31(8): 931-939. https://doi.org/10.1007/s11259-007-0009-4

Ursing J., Walder M., Sandstedt K. (1983). Base composition and sequence homology of deoxyribonucleic acid of thermotolerant Campylobacter from human and animal sources. Current Microbiol. 8(5): 307-310. https://doi.org/10.1007/BF01577733

Van Dyke M. I., Morton V. K., McLellan N. L., Huck P. M. (2010). The occurrence of Campylobacter in river water and waterfowl within a watershed in southern Ontario, Canada. J. Appl. Microbiol. 109(3): 1053-1066. https://doi.org/10.1111/j.1365-2672.2010.04730.x

Vandamme P., De Ley J. (1991). Proposal for a new family, Campylobacteraceae. Int. J. System. Bacteriol. 41(3): 451-455.

Vilardo M. D. C. B., Thomé J. D. D. S., Esteves W. T. C., Filgueiras A. L. L., Oliveira S. S. D. (2006). Application of biochemical and polymerase chain reaction assays for identification of Campylobacter isolates from non-human primates. Memórias do Instituto Oswaldo Cruz. 101(5): 499-501. https://doi.org/10.1590/S0074-02762006000500003

Waldenström J., Broman T., Carlsson I., Hasselquist D., Achterberg R. P., Wagenaar J. A., Olsen B. (2002). Prevalence of Campylobacterjejuni, Campylobacterlari, and Campylobactercoli in different ecological guilds and taxa of migrating birds. Appl. Environ. Microbiol. 68(12): 5911-5917. https://doi.org/10.1128/AEM.68.12.5911-5917.2002

Wang G., Clark C. G., Taylor T. M., Pucknell C., Barton C., Price L., Rodgers F. G. (2002). Colony multiplex PCR assay for identification and differentiation of Campylobacterjejuni, C. coli, C. lari, C. upsaliensis, and C. fetus subsp. fetus. J. Cl. Microbiol. 40(12): 4744-4747. https://doi.org/10.1128/JCM.40.12.4744-4747.2002

Weese J. S. (2011). Bacterial enteritis in dogs and cats: diagnosis, therapy, and zoonotic potential. Vet. Clinics North America. Small Anim. Pract. 41(2): 287. https://doi.org/10.1016/j.cvsm.2010.12.005

Wilson D. J., Gabriel E., Leatherbarrow A. J., Cheesbrough J., Gee S., Bolton E., Diggle P. J. (2008). Tracing the source of campylobacteriosis. PLoS Genetics. 4(9): e1000203. https://doi.org/10.1371/journal.pgen.1000203

Workman S. N., Mathison G. E., Lavoie M. C. (2005). Pet dogs and chicken meat as reservoirs of Campylobacter spp. in Barbados. J. cl. Microbiol. 43(6): 2642-2650.

Yamazaki-Matsune W., Taguchi M., Seto K., Kawahara R., Kawatsu K., Kumeda Y., Tsukamoto T. (2007). Development of a multiplex PCR assay for identification of Campylobactercoli, Campylobacterfetus, Campylobacterhyointestinalis subsp. hyointestinalis, Campylobacterjejuni, Campylobacterlari and Campylobacterupsaliensis. J. Med. Microbiol. 56(11): 1467-1473. https://doi.org/10.1099/jmm.0.47363-0