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Journal of Clinical Microbiology, March 2004, p. 1363-1364, Vol. 42, No. 3
0095-1137/04/$08.00+0 DOI: 10.1128/JCM.42.3.1363-1364.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.
Occurrence of Campylobacter jejuni in Pets Living with Human Patients Infected with C. jejuni
Peter Damborg,1 Katharina E. P. Olsen,2 Eva Møller Nielsen,2 and Luca Guardabassi1*
Department of Veterinary Microbiology, The Royal Veterinary and Agricultural University, 1870 Frederiksberg C,1
Department of Gastrointestinal and Parasitic Infections, Statens Serum Institut, 2300 Copenhagen S, Denmark2
Received 14 October 2003/
Returned for modification 27 November 2003/
Accepted 6 December 2003

ABSTRACT
Campylobacter jejuni was recovered from four dogs (11%) and
four cats (33%) living with Danish human patients infected with
C. jejuni. Pulsed-field gel electrophoresis (PFGE) analysis
revealed the occurrence of the same quinolone-resistant strain
in a girl and her dog.
C. jejuni isolates with closely related
(>95% similarity) PFGE profiles occurred in humans and pets
from different Danish counties.

INTRODUCTION
Various risk analysis studies have shown evidence that pet ownership
is a significant risk factor for
Campylobacter infections in
humans (
1,
5,
6). Direct evidence of transmission of a
Campylobacter jejuni strain between a human and a dog living in the same household
was recently shown based on amplified fragment length polymorphism
(
12). However, the actual importance of pets as a source of
Campylobacter infections in humans remains unclear.
In this study, the occurrence of Campylobacter spp. was investigated in pets (i.e., dogs and cats) living together with human patients infected with C. jejuni. Among 137 patients contacted, 54 (39%) were pet owners and 45 (33%) agreed to participate in the study. Fecal samples collected from pets living with these patients were cultured (48 h, 37°C) on mCCDA agar (SSI Diagnostika, Hilleroed, Denmark) under microaerobic conditions. Campylobacter was recovered from six dogs (16%) and five cats (42%). Based on phenotypic (hippurate hydrolysis, indoxyl acetate hydrolysis, and oxidase and catalase production) and multiplex PCR identification (13), C. jejuni was present in 8 of the 11 pets positive for Campylobacter, including four dogs (11%) and four cats (33%) (Table 1). The three remaining pets carried Campylobacter coli (n = 1) or Campylobacter lari (n = 2). The occurrence of C. jejuni was significantly higher in pets living with patients less than 17 years of age (37%) than in those living with older patients (4%) (Fisher exact test, P = 0,004). Although this study cannot explain the reason for this difference, a likely explanation is that either human-to-pet or pet-to-human transmission of C. jejuni occurs more frequently between young patients and their pets.
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TABLE 1. Description of the eight human-pet pairs where C. jejuni was found in both the human patient and the pet
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The genetic relatedness of
C. jejuni isolates from pets and
humans was determined by pulsed-field gel electrophoresis (PFGE)
analysis with
SmaI and
KpnI (Medinova, Glostrup, Denmark) (
8).
A 2-year-old girl and her dog (pair 1) shared the same strain,
as evidenced by the identical
SmaI (Fig.
1) and
KpnI profiles
found in the human and the animal isolate (Table
1). The isolates
from another young patient and his puppy (pair 3) had very similar
SmaI profiles (Fig.
1) but distinct
KpnI profiles (Table
1).
In the remaining six cases, the PFGE profiles of animal and
human isolates differed by one or more bands (data not shown).
A cluster analysis including other canine strains previously
isolated in Denmark (
4) revealed the occurrence of closely related
(>95% similarity)
SmaI profiles in humans and pets from different
Danish counties (data not shown). In addition to the two human
isolates with the same
SmaI profile as that of the corresponding
pet isolates, a third human isolate showed an
SmaI profile closely
related to those of two canine isolates from a different geographical
area. However, most strains with identical or closely related
SmaI profiles showed distinct
KpnI profiles, indicating that
the detection of identical
SmaI profiles does not necessarily
reflect the occurrence of the same strain in different populations.
The strain isolated from the 2-year-old girl and her dog (pair
1) was resistant to nalidixic acid and ciprofloxacin. The recovery
of quinolone-resistant isolates from Danish patients is associated
mainly with travel (
2). However, the case reported in this study
was not associated with travel, since the girl did not travel
in the period preceding the manifestation of clinical symptoms.
Both the girl and the dog had never been treated with quinolones,
indicating that the strain was not selected by exposure of one
of the two individuals to quinolones but rather was acquired
from an external source. As an alternative to transmission,
environmental exposure to contaminated sources (e.g., soil,
water, etc.) could have caused the presence of the same strain
in the two hosts. Even though the dog was fed a commercial diet,
acquisition from a common food source was also possible, since
the dog was occasionally given human food scraps.
This study shows that C. jejuni occurs frequently among pets living with human patients infected with C. jejuni, especially children. Transmission appears to be uncommon, since there was only one case among 45 cases studied (2%) where isolates from a patient and a pet living in the same household showed identical SmaI and KpnI profiles. However, the frequency of transmission could be underestimated due to a number of factors. First, some strains could be undetected in pets due to the time interval between the analyses of human and pet samples (4 to 30 days, 11 days on average). Second, the occurrence of mixed C. jejuni populations (4) could not be detected, as only one isolate was obtained from each positive sample. Finally, an epidemiological relationship could exist between human and pet isolates having indistinguishable SmaI profiles but different KpnI profiles (e.g., pair 3) or SmaI profiles differing by only one band (e.g., pair 6), since small genetic rearrangements may determine variations in the PFGE profiles of C. jejuni (7, 10, 11). It should be noted that, according to the criteria established by Tenover et al. for interpreting PFGE patterns (10), an epidemiological relationship could exist between isolates having up to six band differences. However, such criteria are not applicable in the present study, because PFGE profiles generally contained fewer than 10 distinct bands (Fig. 1).
In addition to the possible transmission of C. jejuni by direct contact, pet animals can contribute to the dissemination of this pathogen in the environment. Pets can shed Campylobacter for long periods (over 1 year) (4) and usually do not show clinical symptoms (3, 9). In this study, five out of eight pets carrying C. jejuni did not show signs of diarrhea, and one dog appeared to be colonized by the same strain for at least 27 days (data not shown). Accordingly, pets could play an important role in the propagation of this pathogen, especially in urban areas, where direct pet-to-pet contact or exposure to feces from other pets is likely to occur.

FOOTNOTES
* Corresponding author. Mailing address: Department of Veterinary Microbiology, The Royal Veterinary and Agricultural University, Stigbøjlen 4, 1870 Frederiksberg C, Denmark. Phone: 45-35282745. Fax: 45-35282755. E-mail:
lg{at}kvl.dk.


REFERENCES
1 - Adak, G. K., J. M. Cowden, S. Nicholas, and H. S. Evan. 1995. The public-health laboratory service national case-control study of primary indigenous sporadic cases of Campylobacter infection. Epidemiol. Infect. 115:15-22.[Medline]
2 - Emborg, H.-D., and O. E. Heuer (ed.). 2003. DANMAP 2002: use of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from food animals, foods and humans in Denmark. Danish Veterinary Institute, Copenhagen, Denmark.
3 - Gondrosen, B., T. Knaevelsrud, and K. Dommarsnes. 1985. Isolation of thermophilic campylobacters from Norwegian dogs and cats. Acta Vet. Scand. 26:81-90.[Medline]
4 - Hald, B., K. Pedersen, M. Wainø, and M. Madsen. Longitudinal study of the excretion patterns of thermophilic Campylobacter spp. in young pet dogs in Denmark. J. Clin. Microbiol., in press.
5 - Kapperud, G., E. Skjerve, N. H. Bean, S. M. Ostroff, and J. Lassen. 1992. Risk factors for sporadic Campylobacter infections: results of a case-control study in southeastern Norway. J. Clin. Microbiol. 30:3117-3121.[Abstract/Free Full Text]
6 - Neimann, J., J. Engberg, K. Mølbak, and H. C. Wegener. 2003. A case-control study of risk factors for sporadic campylobacter infections in Denmark. Epidemiol. Infect. 130:353-366.[Medline]
7 - On, S. L. W., E. M. Nielsen, J. Engberg, and M. Madsen. 1998. Validity of SmaI-defined genotypes of Campylobacter jejuni examined by SalI, KpnI, and BamHI polymorphisms: evidence of identical clones infecting humans, poultry, and cattle. Epidemiol. Infect. 120:231-237.[CrossRef][Medline]
8 - Ribot, E. M., C. Fitzgerald, K. Kubota, B. Swaminathan, and T. J. Barrett. 2001. Rapid pulsed-field gel electrophoresis protocol for subtyping of Campylobacter jejuni. J. Clin. Microbiol. 39:1889-1894.[Abstract/Free Full Text]
9 - Skirrow, M. B. 1981. Campylobacter enteritis in dogs and catsa new zoonosis. Vet. Res. Commun. 5:13-19.[CrossRef][Medline]
10 - Tenover, F. C., R. D. Arbeit, R. V. Goering, P. A. Mickelsen, B. E. Murray, D. H. Persing, and B. Swaminathan. 1995. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J. Clin. Microbiol. 33:2233-2239.[Medline]
11 - Wassenaar, T. M., B. Geilhausen, and D. G. Newell. 1998. Evidence of genomic instability in Campylobacter jejuni isolated from poultry. Appl. Environ. Microbiol. 64:1816-1821.[Abstract/Free Full Text]
12 - Wolfs, T. F. W., B. Duim, S. P. M. Geelen, A. Rigter, F. Thomson-Carter, A. Fleer, and J. A. Wagenaar. 2001. Neonatal sepsis by Campylobacter jejuni: genetically proven transmission from a household puppy. Clin. Infect. Dis. 32:E97-E99.[CrossRef][Medline]
13 - Zorman, T., and S. S. Mozina. 2002. Classical and molecular identification of thermotolerant campylobacters from poultry meat. Food Technol. Biotechnol. 40:177-184.
Journal of Clinical Microbiology, March 2004, p. 1363-1364, Vol. 42, No. 3
0095-1137/04/$08.00+0 DOI: 10.1128/JCM.42.3.1363-1364.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.
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