HOME CURRENT ISSUE TABLE OF CONTENTS ARCHIVE SEARCH SUBSCRIPTIONS JOBS FEEDBACK HELP		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Permissions Google Scholar Articles by Acke, E. Articles by Whyte, P. PubMed PubMed Citation Articles by Acke, E. Articles by Whyte, P.

Genetic diversity among Campylobacter jejuni isolates from pets in Ireland

¹ School of Agriculture, Food Science and Veterinary Medicine, University College Dublin, Belfield, Dublin 4, Ireland
² Veterinary Teaching Hospital, Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Private Bag 11222, Palmerston North 4442, New Zealand

Correspondence: E-mail for correspondence: e.acke{at}massey.ac.nz

Campylobacter jejuni isolates obtained from pets housed in shelters and in private households were subtyped by fla typing (using DdeI and HinfI restriction enzymes) and pulsed-field gel electrophoresis (PFGE) techniques. Composite fla cluster analysis on 78 C jejuni isolates was more discriminative than either single fla typing technique with 39.7 per cent single isolate patterns. PFGE on 52 C jejuni isolates revealed 53.8 per cent single isolate patterns and was the most discriminative method applied. A database of C jejuni subtyping profiles from pets in Ireland was assembled. The presence of genetic heterogeneity detected in the C jejuni subtypes suggests that pets can acquire the organisms from multiple potential sources. In addition, heterogeneity was detected in the C jejuni subtypes obtained by different culture methods within the same pet. There was a link between isolates from dogs in close contact in the same environment, confirming that this is a potential route of infection, and clusters were detected containing both cat and dog C jejuni isolates, suggesting possible interspecies transmission.

Campylobacter species infection is the most common cause of bacterial gastroenteritis in human beings in the developed world, with Campylobacter jejuni being the most commonly isolated species (Newell and others 2000, Moore and others 2005). The handling or consumption of contaminated/undercooked meat (especially poultry), and, less commonly, drinking contaminated milk or water, are considered to be the most important sources of human campylobacteriosis (Adak and others 2005, Anon 2008, Mazick and others 2006). Pets have been shown to be carriers of Campylobacter species, and C jejuni, Campylobacter upsaliensis and Campylobacter helveticus have been the predominant species isolated (Wieland and others 2005, Workman and others 2005, Acke and others 2009b).

The epidemiology of Campylobacter species infections is highly complex, and control of human campylobacteriosis will depend on a more thorough understanding of sources, transmission routes and pathogen-host interactions. A large number of phenotypic and genotypic typing methods have been applied in epidemiological investigations on human clinical, food and animal Campylobacter species isolates over the past 20 years (Fitzgerald and others 2001, Devane and others 2005, Wieland and others 2006).

In the present study, C jejuni isolates obtained from Irish pets were genotyped using two molecular techniques: flagellin (fla) typing and pulsed-field gel electrophoresis (PFGE). The aim of the study was to assemble a database containing genetic fingerprints of C jejuni isolates obtained from Irish pet populations and to investigate the genotypic diversity in these organisms.

Materials and methods

Seventy-nine C jejuni isolates from pets were included in the study. Samples were collected from cats and dogs in shelters and private households. A total of 17 cat isolates, 60 dog isolates, and two isolates from a hamster were analysed. The shelters were located in the Republic of Ireland (shelter 1) and in Northern Ireland (shelter 2). Fifty-five isolates were collected from dogs and cats at shelter 1 during autumn 2002 to spring 2003 and in spring 2006. These animals had no signs of gastrointestinal disease. Five isolates from dogs with clinical signs of gastrointestinal disease were collected at shelter 2 in spring 2003. Nineteen isolates from household pets were also collected, from animals that were presented to the University Veterinary Hospital, University College Dublin (UCD), during 2004 to 2005. Four of these were from dogs with signs of gastrointestinal disease.

One rectal swab was obtained from each pet and swabs were cultured using a range of specialised culture methods to optimise recovery of Campylobacter species (Acke and others 2009a). DNA was extracted and Campylobacter speciation was performed by PCR analysis at the Veterinary Public Health and Food Safety Laboratory (VPL), UCD, as previously described by Acke and others (2006, 2009a). Genotypic techniques selected for subtyping were: fla typing using DdeI and HinfI restriction enzymes, and a combined or 'composite fla analysis' of the two restriction digest enzyme patterns for each isolate. Isolates were also profiled using PFGE. The distribution of C jejuni isolates evaluated by each technique is given in Table 1. As multiple culture methods were used for each pet sample, multiple isolates were obtained from the different culture methods used (Table 1).

fla typing
fla typing is based on detection of variation between the fla genes in C jejuni. The flaA gene of Campylobacter species has extensive sequence heterogeneity, and molecular analysis of the fla genes serves as an epidemiological marker (Wassenaar and Newell 2000). Different restriction enzymes can be used (for example, DdeI and HinfI), and combining the enzyme pattern (composite analysis) has been shown to result in an increased degree of discrimination (Wassenaar and Newell 2000, Harrington and others 2003). Standard protocols as devised by Nachamkin and others (1993, 1996) were used at the VPL to carry out fla gene analysis of the C jejuni isolates using DdeI and HinfI restriction digest enzymes. Images of the fla digests after electrophoresis were captured in TIFF format using the GelDoc 1000 high-resolution image capture system and processed and analysed at the VPL.

PFGE
PFGE is a macrorestriction technique in which bacterial cells from culture are embedded in chromosomal-grade agarose blocks and lysed in situ to prevent chromosomal DNA shearing, and the bacterial chromosomes are digested by restriction enzymes that cleave the DNA infrequently. An electrophoretic field is used to separate the relatively large DNA fragments by application of pulsed electric fields from different positions on an agarose gel matrix (Newell and others 2000, Wassenaar and Newell 2000). PFGE profiling of the pet C jejuni isolates was carried out at the VPL using the standardised 'Campynet' protocol as previously described (Anon 2001). The restriction enzyme used for the samples evaluated in this study was SmaI (R6125; ProMega). PFGE gels obtained after electrophoresis were captured in TIFF format using a GelDoc 1000 high-resolution image capture system. All PFGE TIFF images were processed and analysed at the VPL. An illustration of PFGE banding patterns from C jejuni isolates in the present study is shown in Fig 1.

View larger version (53K): [in this window] [in a new window]   FIG 1 : Pulsed-field gel electrophoresis (SmaI) patterns of a selection of Campylobacter jejuni isolates from pets in Ireland. Lane M Lambda marker (G3011; Promega), Lane 1 C jejuni NCTC 11168 positive control, Lanes 2 to 6 C jejuni isolates collected in shelter 1, Lanes 2, 3, 4 Clustering isolates from two puppies and one adult dog, Lanes 5, 6 Isolates with unique banding patterns from an adult dog and a puppy

A combination of 'Dice' and 'unweighted paired group method with arithmetic mean' (UPGMA) was used for the analysis of both PFGE and fla-digest profiles (Anon 2002) with a position tolerance value of 1.5 per cent and an optimisation value of 1.0 per cent. A cut-off with isolates clustering at 90 per cent or more was used to identify genetically highly related strains in accordance with previous comparative studies (Kelly 2006, Wieland and others 2006, Keller and others 2007).

Fig 2 shows a dendrogram obtained from composite fla analysis of pet isolates. Table 2 shows the distribution of C jejuni isolates following cluster analysis for each method. The association with animal species, age of the animal and the presence of signs of gastrointestinal disease, the housing, and the time period of sample collection ('same visit' isolates) was assessed within each cluster. The time period of sample collection was assessed only in dogs housed in shelters, as most of these animals had access to the same walking areas and outdoor pens, unlike the shelter cats and private household pets with different owners.

View larger version (36K): [in this window] [in a new window]   FIG 2 : Dendrogram based on composite fla cluster analysis of the Campylobacter jejuni fingerprinting profiles obtained from pets in Ireland. Clusters at 90 per cent similarity cut-off are indicated by the red line and examples from Table 2 (a, b, c, d) are shown. < Six months old or younger, > Over six months old, B Shelter 2, d Shelter 1, D Diarrhoea, H Household, S Shelter 1, - No clinical signs

Assessment of the discriminatory power of each method
The discrimination index (D-index) was calculated as previously described by Hunter and Gaston (1988) to compare the discriminatory power of each typing method in order to assess the usefulness of each method in discriminating C jejuni subtypes for epidemiological studies (Table 3). The higher the D-index, the more discriminatory the method, and a D-index of at least 0.90 is desirable (Hunter and Gaston 1988).

Results

Cluster analysis of 79 profiles obtained by fla DdeI subtyping revealed 27 unique profiles (34.2 per cent of total isolates), and several clusters with multiple isolates, of which two were clusters with five isolates (each 6.3 per cent of total isolates) and one with a cluster of six isolates (7.6 per cent of total isolates). fla HinfI profile cluster analysis on 78 isolates revealed 15 unique profiles (19.2 per cent). Composite fla analysis on 78 isolates resulted in 31 unique banding patterns (39.7 per cent). The epidemiological background of the pets studied is given in the composite fla analysis dendrogram (Fig 2). Examples are shown of a cluster with two isolates containing an asymptomatic adult dog from shelter 1 and a puppy with diarrhoea from shelter 2 (example a); a cluster of three isolates from two puppies with diarrhoea in the same household (example b); a cluster of five isolates from two puppies with diarrhoea from shelter 2, two cats from shelter 1 and one healthy household dog (example c); and a cluster of six isolates from four cats from shelter 1, an adult household dog with diarrhoea and a puppy from shelter 2 with diarrhoea (example d).

Cluster analysis of 52 profiles obtained by PFGE resulted in 28 unique banding patterns (53.8 per cent) and nine clusters with two isolates (3.8 per cent each), containing shelter dogs or cats sampled in the same time period and clusters with both cat and dog isolates. There were two clusters with three isolates (5.8 per cent each) containing isolates from shelter 1 dogs sampled in the same time period. The results for each cluster analysis are summarised in Table 2.

The number of isolates obtained by different culture methods, from the same pet (Table 1), that clustered was assessed for the most discriminative methods. Nineteen of 34 (55.9 per cent) and four of 18 (22.2 per cent) isolates obtained by different methods from the same pet were in clusters for composite fla analysis and PFGE, respectively.

Discussion

Pet ownership is a recognised risk factor for campylobacteriosis in human beings (Tenkate and others 2001, Carrique-Mas and others 2005). However, with few cases of Campylobacter species infections reported where pet to human transmission was epidemiologically confirmed using molecular techniques, further studies are needed to assess the importance of pets as a reservoir (Wolfs and others 2001, Damborg and others 2004). Campylobacter species prevalences of 51.1 per cent and 75 per cent were previously reported in asymptomatic Irish shelter dogs and cats, respectively (Acke and others 2006). In dogs and cats from private households in Ireland, a prevalence of 41.5 per cent and 42.9 per cent, respectively, was reported (Acke and others 2009b). Campylobacter infections are usually asymptomatic in dogs and cats. If clinical signs develop, they occur most commonly in animals younger than six months of age and signs are usually confined to the gastrointestinal tract (Olson and Sandstedt 1987, Burnens and others 1992, Fox 2006). The severity of infection is dependent on various factors including age, previous exposure, immune status, numbers and virulence of ingested organisms, environmental and physiological stressors, and the presence of other enteric pathogens or underlying gastrointestinal disease and other conditions. The highest prevalences have been reported in young dogs and cats with signs of gastrointestinal disease living in groups (Malik and Love 1989, Burnens and others 1992, Torre and Tello 1993, Baker and others 1999, Lopez and others 2002, Sandberg and others 2002, Acke and others 2006, 2009b).

fla DdeI cluster analysis of the pet isolates in this study revealed a higher number of 'single isolate patterns' than fla HinfI cluster analysis (Table 2). The calculated D-index for fla DdeI was higher than for fla HinfI cluster analysis results (Table 3), confirming that the use of the restriction enzyme DdeI gave more discriminatory banding profiles than those obtained with the HinfI enzyme. Digestion of fla typing PCR products with DdeI generates more bands than digestion with HinfI, resulting in enhanced discrimination (Newell and others 2000, Wassenaar and Newell 2000, Oberhelman and others 2003, Schouls and others 2003). Composite fla cluster analysis was more discriminative than either single fla typing technique (Table 2, 3). fla typing has been widely applied in the subtyping of human C jejuni infections and is considered a useful first-choice subtyping method as it is cheaper, more widely available, less time-consuming and less labour-intensive to perform than other methods (Harrington and others 2003). However, fla typing is a method with rather poor discriminatory potential compared with other molecular methods such as PFGE (Wassenaar and Newell 2000), and as inter-laboratory standardisation (Harrington and others 2003) and genetic instability are problems, combination with a different method is recommended (Newell and others 2000). Although PFGE was performed on fewer C jejuni isolates collected from a smaller number of pets in the present study, the percentage of isolates in the 'single isolate' group and the calculated D-index were higher compared with the fla typing methods, suggesting superior discrimination between subtypes (Table 2, 3). PFGE, together with restriction fragment length polymorphism, random amplification of polymorphic DNA and amplified fragment length polymorphism fingerprinting (AFLP), is a highly discriminatory subtyping technique (Duim and others 2001, Lehner and others 2000, Petersen and Newell 2001). These techniques are time-consuming, cumbersome and may be costly where specialised equipment is required (Hein and others 2003). The use of different PFGE conditions and different enzymes can result in variation in PFGE profiles from the same DNA preparation. Genetic instability from extensive subculturing of Campylobacter species could also result in significant changes in PFGE banding patterns (On 1998).

Genetic diversity was detected between C jejuni isolates from Irish pets as illustrated by the number of single isolate profiles obtained by each technique (Table 2). This agrees with results reported in Switzerland by Wieland and others (2005, 2006), where AFLP fingerprinting analysis of C jejuni isolates collected from dogs, cats and other sources revealed heterogeneity among the strains. The presence of this heterogeneity suggests many different potential sources of infection could be involved, for example, environmental sources, birds or food sources (Wieland and others 2005, Keller and others 2007).

The main routes of transmission of infection with Campylobacter organisms in pets are ingestion of undercooked/raw food (especially liver, chicken, tripe and unpasteurised milk), drinking contaminated water, and direct (fresh faeces from infected animals) or indirect (contaminated feeding/water bowls, other implements and the environment) contact with other animals (Fox 2006). In the present study, several isolates from dogs and cats formed clusters, suggesting that transmission between animal species is possible. Several isolates collected from dogs sampled in the same housing environment were also found to be in clusters. In addition, the time period in which the samples were collected from dogs in the shelters was the same for several clustering isolates (Table 2, Fig 2). As the dogs had access to the same outdoor walking areas and close contact in the kennels was possible, exposure and reinfection by the same strain of C jejuni in the environment is likely. Also, in two puppies with diarrhoea in the same household, an identical C jejuni strain was detected (Fig 2). This confirms the role of close contact and the presence of environmental reservoirs in the epidemiology of Campylobacter species infections in pets (Devane and others 2005, Keller and others 2007). As puppies and kittens generally have higher Campylobacter species isolation rates, especially if they have clinical signs of gastrointestinal disease (Acke and others 2006, 2009b), adequate hygiene measures should be implemented in households and kennel environments to prevent lateral spread of potentially pathogenic and zoonotic pathogens.

Interestingly, in a number of pets in the present study, different genotypic profiles were observed within the same pet when multiple culture methods were used, suggesting the presence of multiple strains of C jejuni within the individual host (Table 1). This also illustrates the importance of study design and how the application of a combination of methods may result in an increased number of C jejuni subtypes, and shows that pets may be concurrently infected with more than one strain at the same time, which may be detected only by using several isolation methods.

Genotyping of isolates by highly discriminatory and reproducible methods and the assembly of Campylobacter genotype databases is essential and would aid in the identification of contamination sources and in tracing back the routes of transmission between the environment, reservoirs and human beings, increasing the understanding of the epidemiology of campylobacteriosis (Devane and others 2005, Keller and others 2007). Future work with the database assembled in the present study will include comparison of the obtained C jejuni genotypes isolated from pets with those isolated from human clinical samples and retail-sourced food, to determine the role of pets as a reservoir for C jejuni infections in human beings.

Acknowledgements

The authors thank all staff of the University Veterinary Hospital for their help with the sampling process. They also thank the personnel in the VPL and the Veterinary Microbiology Laboratory, UCD, for their help with the processing of the samples. They acknowledge Small Animal Clinical Studies, UCD, and 'safefood', the Food Safety Promotion Board Ireland, for funding this investigation.

Provenance: not commissioned; externally peer reviewed

References

ANON (2001) CAMPYNET. A network for the harmonisation and standardisation of molecular typing methods for camplylobacters. http://campynet.vetinst.dk. Accessed December 17, 2009

ANON (2002) Zoonoses report: United Kingdom 2002. Department for Environment, Food and Rural Affairs. www.defra.gov.uk/foodfarm/farmanimal/diseases/atoz/zoonoses/documents/reports/zoonoses2002.pdf. Accessed December 4, 2009

ANON (2008) Campylobacteriosis in Ireland, 2006. Health Protection Surveillance Centre. www.hpsc.ie/hpsc/EPI-Insight/Volume92008/File,2887,en.PDF. Accessed December 4, 2009

ACKE, E., MCGILL, K., GOLDEN O., JONES, B. R., FANNING, S. & WHYTE, P. (2009a) A comparison of different culture methods for the recovery of Campylobacter species from pets. Zoonoses and Public Health 56,477 -489

ACKE, E., MCGILL, K., GOLDEN O., JONES, B. R., FANNING, S. & WHYTE, P. (2009b) Prevalence of thermophilic Campylobacter species in household cats and dogs in Ireland. Veterinary Record 164,44 -47

ACKE, E., WHYTE, P., JONES, B. R., MCGILL, K., COLLINS, J. D. & FANNING, S. (2006) Prevalence of thermophilic Campylobacter species in cats and dogs in two animal shelters in Ireland. Veterinary Record 158, 51-54

ADAK, G. K., MEAKINS, S. M., YIP, H., LOPMAN, B. A. & O'BRIEN, S. J. (2005) Disease risks from foods, England and Wales, 1996-2000. Emerging Infectious Diseases 11, 365-372[Medline]

BAKER, J., BARTON, M. D. & LANSER, J. (1999) Campylobacter species in cats and dogs in South Australia. Australian Veterinary Journal 77, 662-666[Medline]

BURNENS, A. P., ANGÉLOZ-WICK, B. & NICOLET, J. (1992) Comparison of Campylobacter carriage rates in diarrheic and healthy pet animals. Zentralblatt für Veterinärmedizin. Reihe B 39,175 -180

CARRIQUE-MAS, J., ANDERSSON, Y., HJERTQVIST, M., SVENSSON, A., TORNER, A. & GIESECKE, J. (2005) Risk factors for domestic sporadic campylobacteriosis among young children in Sweden. Scandinavian Journal of Infectious Diseases 37, 101-110[Medline]

DAMBORG, P., OLSEN, K. E., MØLLER NIELSEN, E. & GUARDABASSI, L. (2004) Occurrence of Campylobacter jejuni in pets living with human patients infected with C jejuni. Journal of Clinical Microbiology 42,1363 -1364[Abstract/Free Full Text]

DEVANE, M. L., NICOL, C., BALL, A., KLENA, J. D., SCHOLES, P., HUDSON, J. A., BAKER, M. G., GILPIN, B. J., GARRETT, N. & SAVILL, M. G. (2005) The occurrence of Campylobacter subtypes in environmental reservoirs and potential transmission routes. Journal of Applied Microbiology 98,980 -990[Medline]

DUIM, B., VANDAMME, P. A., RIGTER, A., LAEVENS, S., DIJKSTRA, J. R. & WAGENAAR, J. A. (2001) Differentiation of Campylobacter species by AFLP fingerprinting. Microbiology 147,2729 -2737[Abstract/Free Full Text]

FITZGERALD, C., HELSEL, L. O., NICHOLSON, M. A., OLSEN, S. J., SWERDLOW, D. L., FLAHART, R., SEXTON, J. & FIELDS, P. I. (2001) Evaluation of methods for subtyping Campylobacter jejuni during an outbreak involving a food handler. Journal of Clinical Microbiology 39,2386 -2390[Abstract/Free Full Text]

FOX, J. G. (2006) Enteric bacterial infections: Campylobacter, gastric Helicobacter and intestinal and hepatic Helicobacter infections. In Infectious Diseases of the Dog and Cat. 3rd edn. Ed C. E. Greene. W. B. Saunders. pp339 -354

HARRINGTON, C. S., MORAN, L., RIDLEY, A. M., NEWELL, D. G. & MADDEN, R. H. (2003) Inter-laboratory evaluation of three flagellin PCR/RFLP methods for typing Campylobacter jejuni and C coli: the CAMPYNET experience. Journal of Applied Microbiology 95,1321 -1333[Medline]

HEIN, I., MACH, R. L., FARNLEITNER, A. H. & WAGNER, M. (2003) Application of single-strand conformation polymorphism and denaturing gradient gel electrophoresis for fla sequence typing of Campylobacter jejuni. Journal of Microbiological Methods 52,305 -313[Medline]

HUNTER, P. R. & GASTON, M. A. (1988) Numerical index of the discriminatory ability of typing systems: an application of Simpson's index of diversity. Journal of Clinical Microbiology 26,2465 -2466[Abstract/Free Full Text]

KELLER, J., WIELAND, B., WITTWER, M., STEPHAN, R. & PERRETEN, V. (2007) Distribution and genetic variability among Campylobacter spp isolates from different animal species and humans in Switzerland. Zoonoses and Public Health 54, 2-7

KELLY, L. (2006) A study of the epidemiology and antimicrobial resistance of Campylobacter in the Irish food chain and human population. MSc thesis. National University of Ireland

LEHNER, A., SCHNECK, C., FEIERL, G., PLESS, P., DEUTZ, A., BRANDL, E. & WAGNER, M. (2000) Epidemiologic application of pulsed-field gel electrophoresis to an outbreak of Campylobacter jejuni in an Austrian youth centre. Epidemiology and Infection 125,13 -16[Medline]

LÓPEZ, C. M., GIACOBONI, G., AGOSTINI, A., CORNERO, F. J., TELLECHEA, D. M. & TRINIDAD, J. J. (2002) Thermotolerant Campylobacters in domestic animals in a defined population in Buenos Aires, Argentina. Preventive Veterinary Medicine 55, 193-200[Medline]

MALIK, R. & LOVE, D. N. (1989) The isolation of Campylobacter jejuni/coli from pound dogs and canine veterinary patients in a veterinary hospital. Australian Veterinary Practitioner 19,16 -18

MAZICK, A., ETHELBERG, S., MØLLER NIELSEN, E., MOLBAK, K. & LISBY, M. (2006) An outbreak of Campylobacter jejuni associated with consumption of chicken, Copenhagen, 2005. Eurosurveillance 11,137 -139[Medline]

MOORE, J. E., CORCORAN, D., DOOLEY, J. S., FANNING, S., LUCEY, B., MATSUDA, M. & OTHERS (2005) Campylobacter. Veterinary Research 36,351 -382[Medline]

NACHAMKIN, I., BOHACHICK, K. & PATTON, C. M. (1993) Flagellin gene typing of Campylobacter jejuni by restriction fragment length polymorphism analysis. Journal of Clinical Microbiology 31,1531 -1536[Abstract/Free Full Text]

NACHAMKIN, I., UNG, H. & PATTON, C. M. (1996) Analysis of HL and O serotypes of Campylobacter strains by the flagellin gene typing system. Journal of Clinical Microbiology 34,277 -281[Abstract/Free Full Text]

NEWELL, D. G., FROST, J. A., DUIM, B., WAGENAAR, J. A., MADDEN, R. H., VAN DER PLAS, J. & ON, S. L. W. (2000) New developments in the subtyping of Campylobacter species. In Campylobacter. 2nd edn. Eds I. Nachamkin, M. J. Blaser. ASM Press. pp 27-44

OBERHELMAN, R. A., GILMAN, R. H., SHEEN, P., CORDOVA, J., TAYLOR, D. N., ZIMIC, M. & OTHERS (2003) Campylobacter transmission in a Peruvian shantytown: a longitudinal study using strain typing of Campylobacter isolates from chickens and humans in household clusters. Journal of Infectious Diseases 187,260 -269[Medline]

OLSON, P. & SANDSTEDT, K. (1987) Campylobacter in the dog: a clinical and experimental study. Veterinary Record 121,99 -101

ON, S. L. (1998) In vitro genotypic variation of Campylobacter coli documented by pulsed-field gel electrophoretic DNA profiling: implications for epidemiological studies. FEMS Microbiology Letters 165,341 -346[Medline]

PETERSEN, L. & NEWELL, D. G. (2001) The ability of fla-typing schemes to discriminate between strains of Campylobacter jejuni. Journal of Applied Microbiology 91,217 -224[Medline]

SANDBERG, M., BERGSJØ, B., HOFSHAGEN, M., SKJERVE, E. & KRUSE, H. (2002) Risk factors for Campylobacter infection in Norwegian cats and dogs. Preventive Veterinary Medicine 55,241 -253[Medline]

SCHOULS, L. M., REULEN, S., DUIM, B., WAGENAAR, J. A., WILLEMS, R. J., DINGLE, K. E., COLLES, F. M. & VAN EMBDEN, J. D. (2003) Comparative genotyping of Campylobacter jejuni by amplified fragment length polymorphism, multilocus sequence typing, and short repeat sequencing: strain diversity, host range, and recombination. Journal of Clinical Microbiology 41,15 -26[Abstract/Free Full Text]

TENKATE, T. D. & STAFFORD, R. J. (2001) Risk factors for Campylobacter infection in infants and young children: a matched case-control study. Epidemiology and Infection 127,399 -404[Medline]

TORRE, E. & TELLO, M. (1993) Factors influencing fecal shedding of Campylobacter jejuni in dogs without diarrhea. American Journal of Veterinary Research 54, 260-262[Medline]

WASSENAAR, T. M. & NEWELL, D. G. (2000) Genotyping of Campylobacter spp. Applied and Environmental Microbiology 66,1 -9[Free Full Text]

WIELAND, B., REGULA, G., DANUSER, J., WITTWER, M., BURNENS, A. P., WASSENAAR, T. M. & STÄRK, K. D. (2005) Campylobacter spp in dogs and cats in Switzerland: risk factor analysis and molecular characterization with AFLP. Journal of Veterinary Medicine. Series B: Infectious Diseases and Veterinary Public Health 52,183 -189

WIELAND, B., WITTWER, M., REGULA, G., WASSENAAR, T. M., BURNENS, A. P., KELLER, J. & STÄRK, K. D. (2006) Phenon cluster analysis as a method to investigate epidemiological relatedness between sources of Campylobacter jejuni. Journal of Applied Microbiology 100,316 -324[Medline]

WOLFS, T. F., DUIM, B., GEELEN, S. P., RIGTER, A., THOMSON-CARTER, F., FLEER, A. & WAGENAAR, J. A. (2001) Neonatal sepsis by Campylobacter jejuni: genetically proven transmission from a household puppy. Clinical Infectious Diseases 32, E97-E99[Medline]

WORKMAN, S. N., MATHISON, G. E. & LAVOIE, M. C. (2005) Pet dogs and chicken meat as reservoirs of Campylobacter spp in Barbados. Journal of Clinical Microbiology 43,2642 -2650[Abstract/Free Full Text]

This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Permissions Google Scholar Articles by Acke, E. Articles by Whyte, P. PubMed PubMed Citation Articles by Acke, E. Articles by Whyte, P.