Skip to main content

Prevalence of thermophilic Campylobacter species in Swedish dogs and characterization of C. jejuni isolates

Abstract

Background

The aims of this study were to investigate the prevalence of Campylobacter species in Swedish dogs, to identify the species of the Campylobacter isolates and to genotype the C. jejuni isolates. Young and healthy dogs were targeted and the sampling was performed at 11 veterinary clinics throughout Sweden from October 2011 to October 2012. Faecal swab samples were collected and sent to the laboratory at the National Veterinary Institute (SVA) for isolation of Campylobacter, speciation and genotyping.

Results

Campylobacter spp. were isolated from 67 of the 180 sampled dogs which yields an overall prevalence of 37%. The most prevalent species of Campylobacter among the participating dogs was C. upsaliensis with 52 of the 67 identified isolates. A lower prevalence was observed for C. jejuni with seven identified isolates and one isolate was identified as C. helveticus. Multi-locus sequence typing (MLST) was carried out on the seven C. jejuni isolates and all sequence types that were found are also commonly found in humans. The dogs were divided into three age groups; 1) under 12 months, 2) 12 to 23 months and 3) 24 months and older. The highest prevalence was found in the two younger age groups. Dogs shedding C. jejuni were between 3–12 months of age while dogs shedding C. upsaliensis were found in all ages.

Conclusions

The present investigation finds that Campylobacter spp. known to cause campylobacteriosis in humans are present in Swedish dogs. The results suggest an age predisposition where dogs under 2 years of age are more likely to shed Campylobacter spp. than older dogs. The most commonly isolated species was C. upsaliensis followed by C. jejuni, which was only detected in dogs up to 12 months of age. All C. jejuni isolates identified in the present study were of the same MLST types that have previously been described both in humans and in animals. The awareness of the Campylobacter risk of healthy young dogs may be an important way to reduce the transmission from dogs to infants, young children and immunocompromised adults.

Background

Campylobacteriosis is the most commonly reported zoonotic disease and the most common cause of bacterial enteritis in humans in many countries throughout the world [1]. In 2013, there were 8114 notified human cases of campylobacteriosis in Sweden. Of these, 41% were considered to be domestically acquired [2]. Humans can be infected with Campylobacter by several routes and the bacteria are commonly found in a wide range of animals including cats and dogs. Especially in young dogs (<1 year), Campylobacter is often found in faecal samples and the dogs usually shed the bacteria without showing any clinical signs [3,4]. Several studies have reported the presence of Campylobacter spp. in both healthy dogs and dogs with diarrhoea, but Campylobacter is generally not considered to be pathogenic to dogs [5-8]. No association was found between presence of Campylobacter and diarrhoea in a Norwegian study on dogs [8] whereas a study in Canada found significant higher infection rate in diarrhoeic dogs compared with healthy dogs [5]. In an investigation of dogs in Ireland, diarrhoeic dogs were more likely to be Campylobacter positive than dogs without diarrhoea, but the dogs with diarrhoea also had concurrent gastrointestinal parasites, inflammatory bowel disease or diabetes [9]. A study of dogs in Barbados found no difference in clinical disease in dogs with and without presence of Campylobacter in the faeces, but indicated that co-infection with parvovirus and Campylobacter was common [10]. An association between occurrence of diarrhoea and Campylobacter infection was described in a previous Swedish investigation of dogs from 1979, and 63% of the dogs with diarrhoea also had antibodies to canine parvovirus [11]. The true role of Campylobacter in canine gastroenteritis is uncertain as the bacteria may be found in clinically healthy dogs or often as a co-infection or intestinal carriage in diseased dogs.

In most studies, the predominant Campylobacter species isolated from dogs is C. upsaliensis and dogs are regarded as an important reservoir for this species [3-6,9,12]. The second most common Campylobacter species isolated from dogs, in many populations, is C. jejuni [3,4,6,9,12], which is also responsible for the majority of human infections [13,14]. The reported prevalence of Campylobacter in dogs varies widely between studies, ranging from 22% to 100% and is reported to depend on factors such as the age, diet and housing of the dogs. Previous prevalence investigations of Campylobacter in dogs have also varied by study design and method of bacterial isolation.

Human campylobacteriosis is frequently attributed to contact with contaminated food (especially poultry meat) or water [15,16]. In several studies, direct contact with pet animals has also been identified as a possible source of human Campylobacter infection [15,17-19]. Presence of a puppy in the household has been identified as risk factor for campylobacteriosis, especially in young children [20,21]. In a study by Wolfs et al. [19] evidence was presented for transmission of C. jejuni from a dog to a 3-week old infant. However, a study by Studahl and Andersson [16] did not find a significant association between human campylobacteriosis and contact with dogs.

The present survey is part of an ongoing more comprehensive Campylobacter source attribution study in Sweden. Strains from human cases of campylobacteriosis were collected during the same time period as samples were taken from dogs, cattle, pigs, sheep, poultry and wild birds. Other relevant sources of human campylobacteriosis such as retail poultry meat, raw water and bathing water were also sampled during this period.

The aim of this study was to update our knowledge on the prevalence of Campylobacter spp. in young dogs in Sweden by collecting samples from healthy, young dogs throughout a year. The aim was also to identify the species of the Campylobacter isolates and to genotype the C. jejuni isolates by multi-locus sequence typing (MLST) to enable comparison between C. jejuni isolates from dogs and humans.

Methods

Study population and sampling

Selection of clinics to participate in the study

The sampling of dogs was performed at veterinary clinics throughout Sweden from October 2011 through October 2012. The geographical regions (counties) to be included in the survey were selected depending on the number of reported human cases of campylobacteriosis in recent years (based on data from the Public Health Agency of Sweden, www.folkhalsomyndigheten.se). The counties with the highest incidence of human campylobacteriosis were prioritised but the aim was also to cover a large part of the country. Requests for participation in the sampling process were sent to 53 veterinary clinics that had a previously established contact with the laboratory at Department of Bacteriology at the National Veterinary Institute (SVA, www.sva.se). A selection of 11 was made from the 18 veterinary clinics that had agreed upon participation in the study. One of them, located in the north of Sweden was included in the survey despite the lower incidence of human campylobacteriosis in favour of the better geographic coverage.

Sampling procedure

The requirements for dogs to be sampled were that they were under the age of two, weaned and healthy with no signs of diarrhoea. Young dogs were targeted because the prevalence of Campylobacter spp. is likely to be highest in young animals [4,6,22]. The aim was to collect a total of 200 samples in the study in order to obtain approximately 100 isolates. Based on a previous study in Sweden by Engvall et al. [4] an overall isolation rate of Campylobacter spp. of around 50% was expected. The clinics were instructed to sample one to two dogs per month. Each dog was sampled only once during the sampling period. Faecal samples were collected from freshly voided faeces and sent to SVA on swabs in Amies transport medium with charcoal (Amies agar gel swabs – with charcoal, Copan, Italy). The swab samples were sent to SVA by ordinary mail at the day of sampling for isolation of Campylobacter, species identification and genetic subtyping of C. jejuni isolates. Written consent of the animal owners was obtained for sampling along with details about the age of the dog and postal code of the owner.

Isolation and species identification of Campylobacter

Swab samples were cultured on modified charcoal, cefoperazone, desoxycholate agar (mCCDA), (Oxoid Inc, Basingstoke, Hampshire, UK) and incubated at 41. 5 ± 1.0°C for up to 5 days in a microaerobic atmosphere created by use of Campygen (Oxoid Inc) or Anoxomat (Advanced Instruments, Inc., Norwood, Massachusetts, USA). Preliminary identification of Campylobacter spp. was based on colony and microscopic morphology and the following phenotypic and biochemical characteristics and tests; motility, oxidase-, catalase-, hippurate and indoxyl acetate reactions. Strains confirmed as Campylobacter spp. were stored at −80°C until further identification. Identification of C. jejuni was mainly based on a positive hippurate test. The species identification of all hippurate-negative isolates was done by mass spectrometry, time of flight, Maldi-Tof [23]. All isolates that were identified as C. upsaliensis by Maldi-Tof were further tested by polymerase chain reaction (PCR) for confirmation [24,25].

Genotyping of C. jejuni

MLST was carried out as previously described by Dingle et al. [26] on the isolates identified as C. jejuni. Alleles, sequence type (ST) and clonal complex were assigned using the pubMLST database (http://pubmlst.org/campylobacter). Sequence types that shared four or more alleles were considered to belong to the same clonal complex. Because the present study is part of a larger comparative study of C. jejuni between various sources in Sweden, genotyping was restricted to this Campylobacter species.

Results

In total, 180 dogs were sampled from the 11 participating veterinary clinics. The sampling period was from October 2011 to October 2012; however, two samples received in November 2012 were also included in the study. For practical reasons, the number of samples received per month varied between the participating clinics. One clinic only sent in samples from one month. The location of the clinics and number of sampled and positive dogs per clinic is illustrated in Figure 1. One of the positive samples lacked information about clinic on the referral form. Most samples were received during the first seven months of the sampling period (October – April). The highest proportion of positive samples occurred in the winter months with a peak in March 2012 (57%). The number of samples per month and positive samples per month are shown in Figure 2.

Figure 1
figure 1

Spatial distribution of veterinary clinics where dogs were sampled. The height of the bars represents the number of sampled dogs (red = positive samples, green = negative samples).

Figure 2
figure 2

Total number of samples and samples with Campylobacter species per month. Proportion positive samples is indicated by the red line.

The age distribution of the sampled dogs ranged from one month to 11 years. The aim was to sample dogs under the age of two, although 17 samples turned out to be from dogs between 2 and 11 years and 9 samples lacked information about age. The average and median age was 12 months. The dogs were divided into three age groups; 1) under 12 months, 2) 12 to 23 months and 3) 24 months and older. Number of samples and prevalence of Campylobacter in the different age groups are shown in Figure 3. Highest prevalence was found in the two younger age groups (37% and 40% for group 1 and 2, respectively) and the lowest in age group 3 (12%).

Figure 3
figure 3

Number of dogs in different age groups that tested positive or negative for Campylobacter species.

Campylobacter spp. were isolated from 67 of the 180 sampled dogs which yields an overall prevalence of 37% in this material. The most common species of Campylobacter isolated from the dogs was C. upsaliensis with 52 of the 67 identified isolates (78%). A lower occurrence of C. jejuni was observed, with 7 identified isolates (9%) and 1 isolate (1%) was identified as C. helveticus. All C. jejuni samples were found in dogs up to 12 months of age. In addition there were 7 isolates of Campylobacter species that did not survive the storage process, prior to the speciation. These isolates were all hippurate negative which indicates that they were most likely not C. jejuni, but could not be identified to species level by Maldi-Tof or PCR.

Results from the MLST are shown in Table 1. The dogs shedding C. jejuni were sampled at different locations except for two that were sampled in the same clinic. All seven isolates had different ST types. However, two dogs, sampled at different locations, were shedding C. jejuni of the same clonal complex, ST Clonal complex 21.

Table 1 Results from multi-locus sequence typing (MLST) of Campylobacter isolates from dogs

Discussion

In this study, 37% of the tested dogs were found to be positive for Campylobacter. This proportion is similar to the previous prevalence estimates of other studies [6,9,27]. However, as we targeted young dogs and the mean age of the sampled dogs was 12 months this estimated prevalence may not be representative for the entire Swedish dog population. Moreover, the study design was such that each dog was only sampled once and only one isolate per dog was analysed. In longitudinal studies with another type of study design where dogs were sampled at several occasions considerably higher prevalences of 73-100% have been reported [3,28]. The most common Campylobacter species among the tested dogs (52/180 dogs) was by far C. upsaliensis which is in agreement with many previous studies on dogs where relatively high prevalences of C. upsaliensis have been found in many different populations and countries [5,7,9,22,28]. The lower prevalence (4%) that was observed for C. jejuni (7/180 dogs) is similar to some studies [12,27,29,30], but lower than in a previous Swedish study by Engvall et al. [4] where 11% of the dogs were positive for C. jejuni. However, in the previous study all samples were cultured on three selective plates (two CAT and one Preston agar plate). This probably contributed to the higher isolation rate compared to the present study. A recent study in Switzerland by Amar et al. [30] found a low prevalence of C. jejuni (6.3%) and an even lower prevalence (5.9%) of C. upsaliensis in healthy dogs. A higher prevalence of C. jejuni has been reported in stray dogs [10,28], which may be due to a different exposure to environmental sources of Campylobacter than what household dogs are normally exposed to. In a study from Spain, 19% (20/105) of dogs under 2 years of age living in a household, were found to have C. jejuni [22]. In the present study, one sample was identified as C. helveticus which is not so often identified in samples from dogs, but has previously been associated with cats [29].

Although C. upsaliensis is not isolated very frequently from humans in routine investigations it is possible that available data underestimate the prevalence due to the methods that are used at the public health laboratories which are primarily developed to detect C. jejuni and C. coli. In Sweden and many countries in Europe, human clinical Campylobacter isolates are not identified to species level which might contribute to a lack of data regarding the prevalence of C. upsaliensis in humans [31]. The role of C. upsaliensis in human disease is not very well established but it has been shown that C. upsaliensis can be a cause of gastroenteritis in both adults and children [32,33]. Labarca et al. [34] found that C. upsaliensis was the second most frequently isolated species in humans after C. jejuni. The authors also found that three dogs living in the households of two human patients infected with C. upsaliensis had the same Campylobacter species isolated in their stool specimens, but were not from the same clonal complex [34]. A study in Belgium reported that an outbreak in four day care centres was caused by C. upsaliensis [35]. Damborg et al. [36] found that a cluster of human C. upsaliensis strains was unrelated to dog strains of C. upsaliensis examined in the study by AFLP fingerprinting. However, the human and dog samples were not collected in the same countries which makes it difficult to interpret the results with regard to host specificity.

The age of each dog at sample collection was recorded and the dogs were divided into three age categories for comparison of prevalences. The results were in agreement with many other studies that have reported higher prevalence of Campylobacter in younger dogs or puppies compared with adult dogs [6,9,12,22,27,37]. These results suggest an age predisposition where young dogs are more susceptible to colonisation, possibly due to the development of immunity with age. Senior dogs have also been found to be at risk for Campylobacter colonisation [27,28]. Wieland et al. [29] found a significant association with age and C. upsaliensis but no association between age and presence of C. jejuni. Dogs shedding C. jejuni in the present study were all young, between 3–12 months while dogs shedding C. upsaliensis were found in all age categories, which is similar to what was described by Hald et al. [3].

Seasonality that is observed in human campylobacteriosis with peaks during the summer months [31] was not observed in this material as the highest incidence was observed in the winter months with a peak in March. Due to the low number of samples per month it is not possible to draw any conclusions regarding seasonality based on our findings. Carbonero et al. [22] found a significantly higher prevalence of C. jejuni in dogs during spring compared to winter. They also reported a higher prevalence of C. upsaliensis during the summer. Hald et al. [3] did not find seasonal variation in carrier rates among dogs in a longitudinal study.

Molecular typing techniques enable comparison of sequence types (STs) between humans and the potential source of Campylobacter. In our study, seven C. jejuni samples were isolated and further subtyped by MLST. The results show high heterogeneity as all isolates were of different STs and only two isolates (from dogs sampled in different areas) belonged to the same clonal complex, ST-21. Since only 7 C. jejuni isolates were identified and typed, the true extent of the C. jejuni population diversity in Swedish dogs cannot be estimated from this material. Mughini Gras et al. [21] showed a high degree of overlap between human and pet (dog and cat) C. jejuni STs. They identified two cases where identical C. jejuni STs (ST45 and ST658) were isolated from dogs and their owners. Four of the STs identified in the present study (ST50, ST45, ST257 and ST122) belong to those more frequently found STs in pet owners in the study by Mughini Gras et al. [21]. Manning et al. [38] found that a majority of the identified C. jejuni ST-complexes overlap between human and various animal sources. When comparing to the Campylobacter MLST database of C. jejuni isolates (http://pubmlst.org/campylobacter) all seven STs that were found are common human STs. In the study by Amar et al. [30] the most frequent STs identified in dogs include ST45 and ST21 that was found also in the present study. Parsons et al. [28] also reported that ST45 was the most common complex in dogs at a rescue kennel. Many studies have identified ownership or close contact with dogs as a potential risk factor for human campylobacteriosis. However, despite the use of molecular information it is often difficult to know whether the bacteria is transferred from dog to human or human to dog or was acquired from the same common source.

In general, it is likely that dogs and humans are exposed to common sources of C. jejuni. The relatively low prevalence of C. jejuni in dogs in this study suggests that the importance of dogs for human infections compared with other sources such as food products may be low. However, dogs and in particular puppies are likely to have close contact with their owner and children in a family. Considering this it is important to note that all C. jejuni positive dogs were puppies or young dogs up to 12 months old. As the prevalence of C. upsaliensis in dogs under two years of age is relatively high there is a risk for transmission of zoonotic Campylobacter from dogs to humans and especially young children that are more susceptible for infection.

Conclusion

The present investigation finds that Campylobacter spp. known to cause campylobacteriosis in humans are present in Swedish dogs. The results suggest an age predisposition where dogs under 2 years of age are more likely to shed Campylobacter spp. than older dogs. The most commonly isolated species was C. upsaliensis followed by C. jejuni, which was only detected in dogs up to 12 months of age. All C. jejuni isolates identified in the present study were the same MLST types as had been previously described both in humans and in animals. Further investigation is necessary to determine the similarity between these dog C. jejuni MLST types and those found in humans in Sweden during the same period. The awareness of the Campylobacter risk of healthy young dogs may be an important way to reduce the transmission from dogs to infants, young children and immunocompromised adults.

References

  1. EFSA, ECDC. The European Union Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Food-borne Outbreaks in 2011. EFSA J. 2013;11(4):3129. doi:10.2903/j.efsa.2013.3129.

    Google Scholar 

  2. Folkhälsomyndigheten. http://folkhalsomyndigheten.se/amnesomraden/statistik-och-undersokningar/sjukdomsstatistik/campylobacterinfektion/. 2014.

  3. Hald B, Pedersen K, Waino M, Jorgensen JC, Madsen M. Longitudinal study of the excretion patterns of thermophilic Campylobacter spp. in young pet dogs in Denmark. J Clin Microbiol. 2004;42(5):2003–12.

    Article  PubMed Central  PubMed  Google Scholar 

  4. Engvall EO, Brandstrom B, Andersson L, Baverud V, Trowald-Wigh G, Englund L. Isolation and identification of thermophilic Campylobacter species in faecal samples from Swedish dogs. Scand J Infect Dis. 2003;35(10):713–8.

    Article  PubMed  Google Scholar 

  5. Chaban B, Ngeleka M, Hill JE. Detection and quantification of 14 Campylobacter species in pet dogs reveals an increase in species richness in feces of diarrheic animals. BMC Microbiol. 2010;10:73. doi:10.1186/1471-2180-10-73.

    Article  PubMed Central  PubMed  Google Scholar 

  6. Parsons BN, Porter CJ, Ryvar R, Stavisky J, Williams NJ, Pinchbeck GL, et al. Prevalence of Campylobacter spp. in a cross-sectional study of dogs attending veterinary practices in the UK and risk indicators associated with shedding. Veterinary J. 2010;184(1):66–70. doi:http://dx.doi.org/10.1016/j.tvjl.2009.01.009.

    Article  CAS  Google Scholar 

  7. Weese JS. Bacterial Enteritis in Dogs and Cats: Diagnosis, Therapy, and Zoonotic Potential. Vet Clin North Am Small Anim Pract. 2011;41(2):287–309.

    Article  PubMed  Google Scholar 

  8. Sandberg M, Bergsjo B, Hofshagen M, Skjerve E, Kruse H. Risk factors for Campylobacter infection in Norwegian cats and dogs. Prev Vet Med. 2002;55(4):241–53.

    Article  CAS  PubMed  Google Scholar 

  9. Acke E, McGill K, Golden O, Jones BR, Fanning S, Whyte P. Prevalence of thermophilic Campylobacter species in household cats and dogs in Ireland. Vet Rec. 2009;164(2):44–7.

    Article  CAS  PubMed  Google Scholar 

  10. Workman SN, Mathison GE, Lavoie MC. Pet dogs and chicken meat as reservoirs of Campylobacter spp. in Barbados. J Clin Microbiol. 2005;43(6):2642–50. doi:10.1128/JCM.43.6.2642-2650.2005.

    Article  PubMed Central  PubMed  Google Scholar 

  11. Sandstedt K, Wierup M. Concomitant occurrence of Campylobacter and parvoviruses in dogs with gastroenteritis. Vet Res Commun. 1981;4(4):271–3.

    CAS  PubMed  Google Scholar 

  12. Leonard EK, Pearl DL, Janecko N, Weese JS, Reid-Smith RJ, Peregrine AS, et al. Factors related to Campylobacter spp. carriage in client-owned dogs visiting veterinary clinics in a region of Ontario, Canada. Epidemiology & Infection. 2011;139(Special Issue 10):1531–41. doi:doi:10.1017/S0950268810002906.

    Article  CAS  Google Scholar 

  13. Man SM. The clinical importance of emerging Campylobacter species. Nat Rev Gastroenterol Hepatol. 2011;8(12):669–85.

    Article  CAS  PubMed  Google Scholar 

  14. Folkhälsomyndigheten. http://www.folkhalsomyndigheten.se/documents/statistik-uppfoljning/smittsamma-sjukdomar/2012/brucellos-epidemiologisk-arsrapport-2012-2013-101-8.pdf. 2013.

  15. Neimann J, Engberg J, Molbak K, Wegener HC. A case–control study of risk factors for sporadic campylobacter infections in Denmark. Epidemiol Infect. 2003;130(3):353–66.

    PubMed Central  CAS  PubMed  Google Scholar 

  16. Studahl A, Andersson Y. Risk factors for indigenous campylobacter infection: a Swedish case–control study. Epidemiol Infect. 2000;125(2):269–75.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  17. Carrique-Mas J, Andersson Y, Hjertqvist M, Svensson A, Torner A, Giesecke J. Risk factors for domestic sporadic campylobacteriosis among young children in Sweden. Scand J Infect Dis. 2005;37(2):101–10. doi:10.1080/00365540510027165.

    Article  PubMed  Google Scholar 

  18. Damborg P, Olsen KE, Moller Nielsen E, Guardabassi L. Occurrence of Campylobacter jejuni in pets living with human patients infected with C. jejuni. J Clin Microbiol. 2004;42(3):1363–4.

    Article  PubMed Central  PubMed  Google Scholar 

  19. Wolfs TF, Duim B, Geelen SP, Rigter A, Thomson-Carter F, Fleer A, et al. Neonatal sepsis by Campylobacter jejuni: genetically proven transmission from a household puppy. Clin Infect Dis. 2001;32(5):E97–9. doi:10.1086/319224.

    Article  CAS  PubMed  Google Scholar 

  20. Tenkate TD, Stafford RJ. Risk factors for campylobacter infection in infants and young children: a matched case–control study. Epidemiol Infect. 2001;127(3):399–404.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  21. Gras LM, Smid JH, Wagenaar JA, Koene MG, Havelaar AH, Friesema IH et al. Increased risk for Campylobacter jejuni and C. coli infection of pet origin in dog owners and evidence for genetic association between strains causing infection in humans and their pets. Epidemiol Infect. 2013:1–10. doi:10.1017/S0950268813000356.

  22. Carbonero A, Torralbo A, Borge C, Garcia-Bocanegra I, Arenas A, Perea A. 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. 2012;35(6):505–12. doi:10.1016/j.cimid.2012.05.002.

    Article  CAS  PubMed  Google Scholar 

  23. Bessede E, Solecki O, Sifre E, Labadi L, Megraud F. Identification of Campylobacter species and related organisms by matrix assisted laser desorption ionization-time of flight (MALDI-TOF) mass spectrometry. Clin Microbiol Infect. 2011;17(11):1735–9. doi:10.1111/j.1469-0691.2011.03468.x.

    Article  CAS  PubMed  Google Scholar 

  24. Lawson AJ, Linton D, Stanley J, Owen RJ. Polymerase chain reaction detection and speciation of Campylobacter upsaliensis and C. helveticus in human faeces and comparison with culture techniques. J Appl Microbiol. 1997;83(3):375–80.

    Article  CAS  PubMed  Google Scholar 

  25. Denis M, Soumet C, Rivoal K, Ermel G, Blivet D, Salvat G, et al. Development of a m-PCR assay for simultaneous identification of Campylobacter jejuni and C. coli. Lett Appl Microbiol. 1999;29(6):406–10.

    Article  CAS  PubMed  Google Scholar 

  26. Dingle KE, Colles FM, Wareing DR, Ure R, Fox AJ, Bolton FE, et al. Multilocus sequence typing system for Campylobacter jejuni. J Clin Microbiol. 2001;39(1):14–23. doi:10.1128/JCM. 39.1.14-23.2001.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  27. Procter TD, Pearl DL, Finley RL, Leonard EK, Janecko N, Reid-Smith RJ, et al. A Cross-Sectional study examining Campylobacter and other zoonotic enteric pathogens in dogs that frequent dog parks in three cities in South-Western Ontario and risk factors for shedding of Campylobacter spp. Zoonoses Public Health. 2013. doi:10.1111/zph.12062.

  28. Parsons BN, Williams NJ, Pinchbeck GL, Christley RM, Hart CA, Gaskell RM, et al. Prevalence and shedding patterns of Campylobacter spp. in longitudinal studies of kennelled dogs. Vet J. 2011;190(2):249–54. doi:10.1016/j.tvjl.2010.10.006.

    Article  CAS  PubMed  Google Scholar 

  29. Wieland B, Regula G, Danuser J, Wittwer M, Burnens AP, Wassenaar TM, et al. Campylobacter spp. in dogs and cats in Switzerland: Risk factor analysis and molecular characterization with AFLP. J Vet Med Ser B-Infect Dis Vet Public Health. 2005;52(4):183–9. doi:10.1111/j.1439-0450.2005.00843.x.

    Article  CAS  Google Scholar 

  30. Amar C, Kittl S, Spreng D, Thomann A, Korczak BM, Burnens AP, et al. Genotypes and antibiotic resistance of canine Campylobacter jejuni isolates. Vet Microbiol. 2014;168(1):124–30.

    Article  CAS  PubMed  Google Scholar 

  31. ECDC, Annual Epidemiological Report 2012. Reporting on 2010 surveillance data and 2011 epidemic intelligence data. Stockholm: ECDC; 2013.

    Google Scholar 

  32. Patton CM, Shaffer N, Edmonds P, Barrett TJ, Lambert MA, Baker C, et al. Human disease associated with “Campylobacter upsaliensis” (catalase-negative or weakly positive Campylobacter species) in the United States. J Clin Microbiol. 1989;27(1):66–73.

    PubMed Central  CAS  PubMed  Google Scholar 

  33. Taylor DE, Hiratsuka K, Mueller L. Isolation and characterization of catalase-negative and catalase-weak strains of Campylobacter species, including "Campylobacter upsaliensis," from humans with gastroenteritis. J Clin Microbiol. 1989;27(9):2042–5.

    PubMed Central  CAS  PubMed  Google Scholar 

  34. Labarca JA, Sturgeon J, Borenstein L, Salem N, Harvey SM, Lehnkering E, et al. Campylobacter upsaliensis: Another pathogen for consideration in the United States. Clin Infect Dis. 2002;34(11):E59–60. doi:10.1086/340266.

    Article  PubMed  Google Scholar 

  35. Goossens H, Giesendorf BA, Vandamme P, Vlaes L, Van den Borre C, Koeken A, et al. Investigation of an outbreak of Campylobacter upsaliensis in day care centers in Brussels: analysis of relationships among isolates by phenotypic and genotypic typing methods. J Infect Dis. 1995;172(5):1298–305.

    Article  CAS  PubMed  Google Scholar 

  36. Damborg P, Guardabassi L, Pedersen K, Kokotovic B. Comparative analysis of human and canine Campylobacter upsaliensis isolates by amplified fragment length polymorphism. J Clin Microbiol. 2008;46(4):1504–6. doi:10.1128/JCM. 00079-08.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  37. Westgarth C, Porter CJ, Nicolson L, Birtles RJ, Williams NJ, Hart CA, et al. Risk factors for the carriage of Campylobacter upsaliensis by dogs in a community in Cheshire. Vet Rec. 2009;165(18):526–30.

    Article  CAS  PubMed  Google Scholar 

  38. Manning G, Dowson CG, Bagnall MC, Ahmed IH, West M, Newell DG. Multilocus sequence typing for comparison of veterinary and human isolates of Campylobacter jejuni. Appl Environ Microbiol. 2003;69(11):6370–9.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful to all dog owners who let their dogs be part of the study, we also gratefully acknowledge the veterinary clinics for their collaboration in the project. We would like to thank Mattias Myrenås, Boel Harbom and Ninni Pudas for their work in the lab with MLST, PCR and Maldi-tof. We would also like to thank the personnel at the Department of Bacteriology at the National Veterinary Institute for their work with analysing all the samples for presence of Campylobacter. This study was funded by the Swedish research council Formas.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mia Holmberg.

Additional information

Competing interests

The authors declare that they have no competing interests.

Authors’ contributions

AL designed and coordinated the study, EE participated in the design of the study and coordinated the laboratory work, AO was responsible for selection of clinics and the sampling process, MH was the main author of the manuscript and performed the data analysis, TR participated in the data analysis and the preparation and editing of the manuscript. All authors have read and approved the final manuscript.

Rights and permissions

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Holmberg, M., Rosendal, T., Engvall, E.O. et al. Prevalence of thermophilic Campylobacter species in Swedish dogs and characterization of C. jejuni isolates. Acta Vet Scand 57, 19 (2015). https://doi.org/10.1186/s13028-015-0108-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s13028-015-0108-0

Keywords