Animal contact is a potential transmission route for campylobacteriosis, and both domestic household pet and petting zoo exposures have been identified as potential sources of exposure. Research has typically focussed on the prevalence, concentration, and transmission of zoonoses from farm animals to humans, yet there are gaps in our understanding of these factors among animals in contact with the public who don’t live on or visit farms. This study aims to quantify, through a systematic review and meta-analysis, the prevalence and concentration of Campylobacter carriage in household pets and petting zoo animals. Four databases were accessed for the systematic review (PubMed, CAB direct, ProQuest, and Web of Science) for papers published in English from 1992–2012, and studies were included if they examined the animal population of interest, assessed prevalence or concentration with fecal, hair coat, oral, or urine exposure routes (although only articles that examined fecal routes were found), and if the research was based in Canada, USA, Europe, Australia, and New Zealand. Studies were reviewed for qualitative synthesis and meta-analysis by two reviewers, compiled into a database, and relevant studies were used to create a weighted mean prevalence value. There were insufficient data to run a meta-analysis of concentration values, a noted study limitation. The mean prevalence of Campylobacter in petting zoo animals is 6.5% based on 7 studies, and in household pets the mean is 24.7% based on 34 studies. Our estimated concentration values were: 7.65x103cfu/g for petting zoo animals, and 2.9x105cfu/g for household pets. These results indicate that Campylobacter prevalence and concentration are lower in petting zoo animals compared with household pets and that both of these animal sources have a lower prevalence compared with farm animals that do not come into contact with the public. There is a lack of studies on Campylobacter in petting zoos and/or fair animals in Canada and abroad. Within this literature, knowledge gaps were identified, and include: a lack of concentration data reported in the literature for Campylobacter spp. in animal feces, a distinction between ill and diarrheic pets in the reported studies, noted differences in shedding and concentrations for various subtypes of Campylobacter, and consistent reporting between studies.
Citation: Pintar KDM, Christidis T, Thomas MK, Anderson M, Nesbitt A, Keithlin J, et al. (2015) A Systematic Review and Meta-Analysis of the Campylobacter spp. Prevalence and Concentration in Household Pets and Petting Zoo Animals for Use in Exposure Assessments. PLoS ONE 10(12): e0144976. https://doi.org/10.1371/journal.pone.0144976
Editor: Jan S. Suchodolski, GI Lab, UNITED STATES
Received: January 30, 2015; Accepted: November 25, 2015; Published: December 18, 2015
Copyright: © 2015 Pintar et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited
Data Availability: All relevant data are within the paper and its Supporting Information files.
Funding: The authors received no specific funding for this work.
Competing interests: The authors have declared that no competing interests exist.
Zoonoses can be transmitted from food [1–6], water [7,8], and animal contact [9–16]. Campylobacter is a zoonotic organism that contributes significantly to the burden of enteric illness globally and in Canada, as Campylobacteriosis is the leading cause of bacterial acute gastrointestinal disease [17,18]. Not all strains of Campylobacter are consistently attributed to human infections. Campylobacter upsaliensis is a frequently isolated strain in sick and healthy animals [19–22] but does not necessarily result in human illness [23–25]. It is thus worthwhile to consider Campylobacter transmission risks while excluding the prevalence and concentration of Campylobacter upsaliensis until we know more about its prevalence in human cases
Outbreaks of enteric diseases have been associated with petting zoos [26,27] and household pets [28–31], though many gaps in our understanding of the public health risks associated with these transmission routes remain, as most existing surveillance programs do not consider animals, and if they do, focus on the risks associated with farm animals and rural exposures [9–14,32,33]. Physicians may underestimate the importance of pet contact as a source of zoonotic disease, especially for immunocompromised or high-risk patients . As urban populations grow and interactions with farm animals become less frequent , the relative importance of zoonotic disease transmission from household pets and petting zoo animals thus increases [33,35].
Petting zoo animals and household pets are not captured in routine public health surveillance. There are many elements of petting zoo design and associated behaviours of the visiting public that can be quantified in greater detail to enhance operator and visitor education and operation guidelines to manage risks to the public . Likewise, households with pets produce numerous opportunities for pathogen exposure , and limited knowledge of the associated risks is a cause for concern and an opportunity for intervention .
It is valuable to review and synthesize the available literature to inform risk assessments, especially to bring greater awareness to the risks associated with petting zoo animal exposures and highlight where there are existing knowledge and data gaps. Quantifying a representative, weighted mean prevalence and concentration of Campylobacter in commonly contacted animals in Canada, the United States, Europe, Australia, and New Zealand has not yet been done. This study contributes to the body of evidence that is being gathered to inform our understanding of the multiple routes of exposure involved in the overall burden of campylobacteriosis. Efforts to systematically capture the available evidence are critical to inform public health risk management and decision-making, and prioritization of interventions.
The purpose of this study was to quantify the prevalence and concentration of Campylobacter carriage in animals to which the public are exposed: household pets and petting zoo animals. The question being addressed is: How often and how heavily are the feces, urine, hair coat or mouths of household pets and farm animals, with which the general public may come in contact, contaminated with Campylobacter? The results of this meta-analysis will be used to inform exposure models for animal contact to further inform source attribution studies of campylobacteriosis.
Materials and Methods
Systematic review and meta-analysis were used to estimate Campylobacter spp. prevalence in household pets and petting zoo animals and to identify data gaps.
Systematic review search strategy and selection criteria
Literature searches for published studies were conducted on February 16, 2012 of the following databases/data platforms (Table 1): PubMed, CAB direct, ProQuest, and Web of Science. Searches retrieved literature regarding enteropathogen prevalence and concentration in household pets and animals that are in contact with the public. All searches were for English language publications only. Publication types included journal articles and outbreak reports. No review protocol exists.
The search started as a scoping review of papers examining the prevalence and concentration of three enteropathogens in household pets and petting zoo animals. Two different searches were performed: Cryptosporidium, Giardia, and Campylobacter in petting zoo animals (S1 Table), and Cryptosporidium, Giardia, and Campylobacter in household pets (S2 Table). This search was restricted to Canada, USA, Europe, Australia, and New Zealand, the years 1992–2012, animal search terms (adapted from the literature [36,38]), and other search terms including fecal, hair coat, oral, or urinary exposure routes.
Inclusion was based on the following criteria: published in English, published between 1992 and 2012, reported naturally occurring disease/carriage, and investigated a relevant pathogen in animals in contact with the public (animals from petting zoos, fairs, or shows; production animals in public displays or open farms) or animals kept as a household pet.
Exclusion criteria specified that articles not include experimental infection/carriage, foodborne contamination from the species in question, or waterborne exposure without direct testing of animals/animal excretions. Articles were also excluded if they only investigated laboratory animals, feral animals, research colonies of dogs or cats from commercial facilities, or production animals: major farm species (cattle, swine, poultry, small ruminants), and purpose-bred animals with no contact with the general public (race horses, racing greyhounds). Finally, papers that were test validation studies or treatment evaluations studies were also excluded.
All search results were imported into Refworks reference software  for duplicate removal and further screening as per exclusion criteria. Attempts were then made to retrieve copies of all remaining references for review. Additional references were added via hand searches of the reference lists of the selected papers, searching through the papers that cited the selected articles (before 2012), and through branching by examining the reference lists of relevant reports, primary and review articles, and Google searches for the full text of some publications for sources that matched the original inclusion/exclusion study criteria. Reports that contained information pertinent to the research questions were then entered in the database. Some papers were removed in the final database because they could not be accessed by the reviewer, they were discovered to be additional duplicates or outside of the time frame of intent, citations were for book reviews, or they could not be retrieved electronically and hard copies were not received before the project deadline.
Data extraction for qualitative synthesis
A database was created to include prevalence and concentration values along with other study information (S3 and S4 Tables). Additional extraction variables included: the animals studied; the different pathogens investigated; whether detection was quantitative or qualitative; whether detection was based on culture (for bacteria) or microscopy (for parasites) or molecular techniques (including PCR on DNA extracted from raw samples or antigen testing on samples); whether molecular (i.e. DNA-based/PCR) techniques were used to characterize strains/isolates detected by other means (e.g. culture/microscopy); whether samples were pooled (potentially from multiple animals) or collected from the environment (observed freshly passed feces from single animals were not considered environmental samples); whether carriage of pathogens was fecal, oral, urinary or found on the skin/haircoat; and whether the number of cases of human illness due to pathogens were included in the report, if any. Quality criteria recorded for studies included: location of the study (Canada, USA, Europe, Australia, or New Zealand); whether the pathogen detection technique (culture, microscopy or molecular) was either described, referenced or stated as “done according to manufacturer’s instructions (if the technique was only named with no further description or reference this was recorded as not described); whether pathogen detection (or characterization) was done at a government/state lab; whether the strains/species detected in animals were also detected in human cases who had been in contact with the animal, and if not, whether the strains/species detected in animals were reported to infect humans; and the source of animal samples. i.e. the population investigated.
Data extraction for meta-analysis
Data for Campylobacter prevalence and concentration were extracted from the studies identified through the systematic review of the literature and included in the study database independently by a single trained reviewer and validated by a second. The prevalence of fecal, oral, urinary or skin/haircoat Campylobacter in the animal studies was defined as the proportion of positive samples collected from the specific animal population. Data were extracted for animals of interest (S1 and S2 Tables) that were either household pets or animals that could come in contact with the public, such as at a fair/zoo/exhibit.
Among the household pet population, prevalence values for diarrheic animals were included, a potential source of bias. Studies in which the sample population size was not clearly reported and studies reporting farm-level proportions were excluded from data extraction. In studies reporting prevalence estimated from repeated measures, the most clinically significant results were extracted. Data were extracted for Campylobacter detected by culture and isolation techniques or by molecular (PCR) methodologies. In some cases, studies relied exclusively on culture-based detection for Campylobacter spp.—those studies were included. In other cases, studies relied on a combination of molecular and/or culture-based detection. Wherever possible, we extracted the prevalence estimates that were species specific, which was most often based on molecular methods. Data were extracted for the prevalence and concentration of total Campylobacter spp. but when specified, estimates of Campylobacter upsaliensis were excluded. Campylobacter upsaliensis was excluded when possible as it is a frequently isolated strain of Campylobacter in animals yet its public health significance is currently not well-understood [19–22] Including C. upsaliensis in the prevalence estimates could result in an overestimation of risk [23–25]. For this reason, two prevalence values were produced: one overall prevalence value (which excludes Campylobacter upsaliensis where possible) and a revised prevalence that includes studies where Campylobacter upsaliensis is identified but cannot be excluded because of a lack of available data.
The overall prevalence of Campylobacter in household pets and petting zoo species was estimated by meta-analysis as a weighted mean, and run a second time incorporating Campylobacter upsaliensis prevalence. The weighted mean prevalence was computed from the proportion of positive animals and the number of animals sampled in each study, allowing some data points to contribute more to the overall mean than others (based on sample size, in this case) . Study-specific effects are variations in study conditions that cannot be quantified or explicitly characterized, which may result in variations in effect size [41–43]. By calculating a weighted mean through a random effects model the study-specific variation in the effects between and within studies can be controlled [42,43]. Given the a priori assumption that the study populations would comprise significant differences, random effects models were constructed . Prevalence estimates for each study and the corresponding summary estimate were generated using the Metaprop command in Stata v12 (StataCorp LP, College Station, Texas). The model was fit to a DerSimonian-Laird random effects model that assumes heterogeneity between the studies and outcome values. The assumption behind random effects models is that there is between- and within-study variability in the results, whereas fixed effects models are fit to data where variance is unlikely and occurs only as a result of sampling error. It was hypothesized that the prevalence of Campylobacter in our populations of interest would vary widely thus a random effects model was used. In order to analyse model sensitivity the meta-analysis was run a second time substituting a random effects model for a fixed effects model. Variance was stabilized using the Freeman-Tukey arcsin transformation and confidence intervals were calculated with score (Wilson) methods. In addition, a measure of heterogeneity representing the proportion of total variation that was due to between study variation in the estimation of the weighted mean was reported (I2) . Potential sources of heterogeneity and selection bias were addressed with sub-models within the meta-analysis. The effect of nationality, animal species, and diarrheic populations were examined.
Pathogen concentration values were extracted when possible for the animal populations of interest. Limited data prevented the development of a meta-analysis of estimates for household pets and petting zoo animals.
Characteristics of the articles included in the systematic review
The searches resulted in the identification of 2464 studies that examined Campylobacter, Cryptosporidium, and Giardia of which 2038 duplicates were removed (Fig 1), resulting in 426 records. An additional 28 records were found through branching (from reference lists or citation lists). The abstracts of these 454 records were assessed when available, and 199 were retained and screened for eligibility, of which 56 were excluded. Full-text articles were sought for the remaining 143 records and of these 114 were selected for inclusion in the study database (S3 and S4 Tables). These studies were assessed for inclusion in the Campylobacter meta-analysis and 45 were initially selected. After further analysis of the studies, 4 were excluded and only 41 were selected.
A total of 114 papers were included based on the results of the systematic review, which are described in the appendix (S3 and S4 Tables). Of these, 50 of the papers were from the USA [19–22,45–64], 26 were from the UK [16,25,65–89], 19 were from other European countries [15,90–99], 15 were from Canada [100–119], two were from Australia [120,121], and one was from New Zealand  (S4 Table). The populations investigated were most frequently veterinary patients, of which there were 45 studies, and animals in contact with the public, which were the population of interest in 44 studies. Following these, 22 studies examined household pets, 15 examined shelter animals, and three studies each examined laboratory submissions, kennels, and breeding operations. The most frequently studied animals were household pets (dogs and cats), with dogs appearing in 55 of the studies and cats in 44 of the studies. The most frequently studied petting zoo animals were cattle, which were included in 28 of the studies, followed by 26 studies of equids, 24 studies of sheep, 22 studies of goats and 18 studies of pigs. The research was supported from a state or government lab in 21 of the papers. Forty-six of the papers studied Giardia, 45 studied Campylobacter, and 33 studied Cryptosporidium. Although the search was limited to these pathogens, many articles also examined other pathogens, such as pathogenic E. coli (Shiga toxin-producing E. coli [STEC] or Verocytotoxin-producing E. coli [VTEC]) in 36 of the papers and Salmonella in 28 of the papers.
All 114 selected papers examined fecal carriage of pathogens as the animal outcome of interest. Twenty-five of the studies examined human illness as an outcome and 27 used pooled environmental samples. The laboratory technique of culture/microscopy was used in 102 studies followed by molecular characterization in 57 studies, and molecular detection methods in 31 studies. Similar strains within the animals and humans studied were tested in two of the studies, but more commonly no zoonotic strains/species were identified in 42 studies.
Characteristics of the articles included in the meta-analysis
The 45 articles in the database that examined Campylobacter were considered for the meta-analysis. The research papers were most frequently from Europe (n = 22/45), the United States (n = 15/45), followed by Canada (n = 4/45) and the United Kingdom (n = 4/45). Four of these papers were excluded from the meta analysis for insufficient reporting of the sample size [70,85,92,123], resulting in 41 papers being considered for the meta-analysis. Of these, 7/41 examined petting zoo animals, and 34/41 considered household pets.
From the household pet papers, dogs (n = 30/34) were studied more frequently than cats (n = 18/34) and among the petting zoo papers, the most frequently examined animal was cattle (n = 5/7) followed by equids (n = 3/7). All papers examined the fecal transmission of Campylobacter to measure prevalence and concentration and no other routes were considered in the papers. The population under investigation was most frequently veterinary patients (n = 26/41), followed by household pets (n = 11/41) and animals in contact with the public (n = 10/41).
Findings from the meta-analysis of prevalence values
For the petting zoos meta-analysis 20 prevalence values were extracted and included from the 7 papers (Fig 1; S3 Table). One of these prevalence values was from a population of diarrheic animals . The weighted mean prevalence of Campylobacter in petting zoo animal populations was estimated to be 6.5% (95% CI: 4.1–9.4) (Table 2; S5 Table). Subgroup meta-analyses were performed for animal species, country, and geographic region (Table 2; S1 Fig).
The household pets literature search resulted in the inclusion of 34 publications that reported on Campylobacter prevalence (S3 Table). From these 34 papers, 85 prevalence values were extracted. The resulting weighted mean prevalence of Campylobacter for household pets was 24.7% (95% CI: 19.8–29.9) (Table 3; S2 Fig). In cases where the studies differentiated between subtypes, Campylobacter upsaliensis was excluded, which is why sub-models with only one input may have valid prevalence and revised prevalence values. When Campylobacter upsaliensis prevalence was included, the prevalence was 34.0% (95% CI: 11.1–17.6) (Table 3; S3 Fig). Subgroup meta-analyses were performed using the prevalence value and the revised prevalence value (excluding Campylobacter upsaliensis) assessing subgroups of animal species, country, region, diarrheic status, and the source of the animals under investigation (Table 3; S2 and S3 Figs). A one-tailed paired t-test was performed on input values for prevalence and revised prevalence and a significant difference between these two groups of prevalence values was found (p < 0.001).
There are I2 values in the study that are high and some that are 0%. Although lower I2 values are preferable, a value of 0% heterogeneity is not ideal. These values are a reflection of having few study inputs and do not reflect a lack of variation between input values. Despite these results, a fixed effects model would be an inappropriate choice, as prevalence values are expected to vary. When fixed effects models were run, the weighted mean estimate for petting zoo animals did not change although the confidence interval narrowed (random effects: 0.07 (95% CI 0.04–0.09) fixed effects: 0.07 (95% CI 0.07–0.08). The weighted mean estimate for household pets was higher when a random effects model was used (0.25 (95% CI 0.20–0.30)) compared to the fixed effects model (0.11 (95% CI 0.11–0.12)). Further, some summary estimates produced I2 values that indicate high heterogeneity (I2 = 96.4% for household pets and 79.9% for petting zoo animals) suggesting that there is considerable heterogeneity in the study inputs. These high I2 values indicate that a random effects model was a better choice than a fixed effects model, as the random effects model is more appropriate for heterogeneous estimates.
Findings from the review of Campylobacter concentration values
The mean fecal concentration of Campylobacter in the petting zoo animals was based on one study which reported Campylobacter jejuni in cattle at a farm that is visited by the public .The values reported in this study were a range (3.0x102-1.5x104), so the value was estimated to be the average of the low and high values (7.65x103) (Table 4). Two studies reported three concentration values for fecal Campylobacter levels in household pets. One paper included two concentration values from 60 fecal samples: for Campylobacter jejuni (2.9x105 (range: 1.6x104–2.3x106) and Campylobacter upsaliensis (8.6x105 (range: 6.0x103–1.3x107)) . The other study reported a range (103–108) from 135 fecal samples, which included Campylobacter upsaliensis . The two values that included Campylobacter upsaliensis and were excluded, leaving only one study that reported the concentration of Campylobacter jejuni which was the value used to approximate Campylobacter spp. in household pets (Table 4).
In this study, a rigorous, comprehensive, and transparent approach was taken to identify publications reporting the prevalence and concentration of Campylobacter in household pet and petting zoo populations in Canada, the United States, Europe, Australia, and New Zealand. This study is a necessary step in identifying and quantifying the risk of Campylobacter exposure associated with household pets and petting zoos as well as identifying data gaps to encourage future research directions. Following an approach developed in Europe, a larger study was initiated to quantify the exposure of Ontarians to Campylobacter from 13 specific exposure routes of campylobacteriosis: foodborne (beef, pork, chicken, seafood/fish, vegetables, fruits), waterborne (drinking water, recreational water), and animal contact (household pets, petting zoos, visiting a farm, living on a farm) .
The results of the meta-analyses are an important first step in quantifying Campylobacter carriage in household pets and petting zoos, which is not measured as part of public health surveillance in Canada. Although the high heterogeneity associated with the summary estimates (I2 values of 96.4% and 79.9% for household pets and petting zoos respectively) introduces limitations into their interpretation and use, the summary estimate is a more representative estimate for Campylobacter prevalence in household pets and petting zoo animals compared to estimates from individual studies or the arithmetic mean of multiple studies. A sensitivity analysis of the results was performed by running inputs with a fixed effects model. The results of the fixed effects model were relatively similar to the random effects models for the petting zoos model and the revised household pets prevalence, but differed for the household pets prevalence. The fixed effects models resulted in 95% Confidence Intervals that were narrower than the random effects models.
The prevalence of Campylobacter estimated in petting zoo animals (approximately 6.5%) when compared to FoodNet Canada data from farms, is lower than swine, dairy cattle, beef cattle, and broiler chickens prevalence values (85%, 80%, 82%, 8.4% respectively using pooled manure samples) . However, the FoodNet Canada samples are collected from farm animals that are raised for food production, thus conditions that may influence Campylobacter carriage will be different than in petting zoo environments. A recent study from Quebec determined the prevalence of Campylobacter at dairy farms (72.5%) .
The prevalence of Campylobacter in household pets (approximately 24.7%) is higher than the petting zoo estimate and the prevalence reported by FoodNet Canada for broiler chickens, but lower than the prevalence reported for swine, dairy cattle, and beef cattle found by FoodNet Canada. Unlike the petting zoo estimate, the prevalence values used for the household pets estimate were adjusted to exclude Campylobacter upsaliensis. When this species was included, the prevalence of Campylobacter spp. in household pets was higher (34.0%).
Due to the high heterogeneity associated with the summary estimates for both pets and petting zoos, potential sources of heterogeneity were explored with subgroup meta-analysis The sub-models analysis also sheds light on potential sources of selection bias. Animal species are known to vary in prevalence and concentration of Campylobacter carriage [78,128]. Subgroup meta-analysis demonstrated that species may influence the heterogeneity observed in the summary measure. In particular, the studies containing multiple species suggest an increased prevalence of Campylobacter. However the limited number of studies prevents a full exploration of this observation, and is identified as an area of further research. The limited data available for other species (only one paper each for sheep, swine, goats, and llama) hindered a fulsome examination of the influence of different animal species on Campylobacter carriage and public health exposure risks. The literature is mixed on whether diarrheic animals differ by pathogenic carriage, making this a valuable comparison [77,129,130]. Our findings suggest that perhaps there is not a difference, however the high heterogeneity associated with both subgroup meta-analyses indicates a wide range of values is present in the literature and alternative sources of heterogeneity not identified in this study may be more influential. Campylobacter varies by geography and climate, [131,132] and our results found that the subgroup meta-analysis by the nationality of the study indicates that there may be some geographic differences in the prevalence of Campylobacter among pets and petting zoos species. Understanding the effect of geography is again limited in this study and additional research is needed to explore factors that influence within-country prevalence and could explain the heterogeneity observed in this analysis.
Limitations and data gaps
Limiting the search to select countries may have biased our results but these papers were most likely to reflect the animal population conditions experienced in North America. Subgroup meta-analyses were used whenever there was enough data to address potential selection bias based on the country of origin, animal species, and the inclusion of diarrheic animals however limited data and high heterogeneity in the subgroup meta-analysis indicates that factors affecting the range of prevalence values seen in the literature are yet to be identified. Publication bias may have impacted the results, as unfavourable research results are typically considered to be less worthwhile for publication. However, in the studies that were captured in the review, many reported a prevalence of zero, indicating that research with negative or inconclusive findings were published in the peer-reviewed literature.
Some animals that are reported to be present in petting zoos (rabbits, donkeys, ponies, baby chicks, and llamas) [36,83,133] or household pets (rabbits)  were not identified in the literature that was found, and were not included in this study, representing an information gap. For animals that were included, in many cases (goats, llamas, sheep, and swine) there were not enough studies to analyse the species-level values. Investigating the level of risk in key sub-populations of animals would be worthwhile. The high degree of mixing of different species in an open farm/petting zoo setting may contribute to increased pathogen shedding among the animals [73,135,136] and young animals or clinically ill animals are often thought to be at higher risk for shedding certain pathogens [130,133,137,138].
The values for prevalence and concentration in this analysis are limited by a lack of data, which is a key finding of this study. Pathogen prevalence in animals used in public displays/exhibits is typically measured in the course of an outbreak investigation, as exhibits have already dispersed by the time the outbreak is detected. Many studies lacked a standardized reporting structure for prevalence values: the study locations, sample size (a clearly stated numerator and denominator), inclusion of diarrheic animals, and the study periods. The concentration values for both household pets and petting zoo animals could not be estimated with a meta-analysis and the estimations were each based on only one paper, representing an important information gap.
There are no available data regarding coat/skin, oral, or urinary carriage of Campylobacter in animals in contact with the public, which are potential routes even though carriage would likely be very low [46,93,94,139–142]. These behaviours can potentially be a significant source of pathogens via household pet contacts.
The proportion of Campylobacter species in each source, and the quantification of shedding are important for accurately estimating the risk to public health in a quantitative microbial risk assessment or exposure assessment ([2,143]. This study did not differentiate between subtypes of Campylobacter in part due to the diagnostic testing methods used in the studies included (e.g. enrichment culture, fecal antigen tests), and in part because the use of molecular subtyping of Campylobacter, such as MLST or CGF, is not widespread. With the increasing use of molecular detection techniques for primary detection, such as PCR, there needs to be an emphasis placed on the development of quantitative tests as well (i.e. quantitative PCR, semi-quantitative antigen tests) [144,145].
This review was not intended to be exhaustive but to provide the best available estimates for prevalence and concentration of Campylobacter in household pets and petting zoo animals. There are likely additional studies pertinent to the project objectives that were not retrieved through the database searches or secondary searches of study references. Nonetheless, this review provides a comprehensive, relatively broad cross-section of the available literature within the inclusion/exclusion criteria set at the beginning of the project and provides a foundational summary of the literature from which to build our evidence to inform public health strategies to reduce exposure risks.
The results of the meta-analysis were used to inform a comparative exposure assessment to determine how exposure to Campylobacter varies between expected sources, including household pets and petting zoos. The assessment was also used to prioritize the design and implementation of programs gathering information identified as important knowledge gaps, and to inform public health interventions. The prevalence and concentration values calculated as part of this literature review and subsequent meta-analysis are crucial for the approximation of risk associated with Campylobacter exposure from animal contact. It is estimated that roughly 16% of all cases of Campylobacter infection in Canada are attributed to animal contact , illustrating the importance in further understanding this route of exposure to reduce the burden of enteric illness. In this study, we have provided multiple areas of research required to improve understanding of the zoonotic transmission of Campylobacter. Future research should quantify the concentration of Campylobacter in petting zoo animal and household pet feces, as well as scenarios on how Campylobacter exposure occurs, how contact occurs between animals and humans, and whether contact and exposure varies by animal.
S1 Fig. Forest plot for meta-analysis of petting zoo animal prevalence values.
S2 Fig. Forest plot for meta-analysis of household pets prevalence values.
S3 Fig. Forest plot for meta-analysis of household pets revised prevalence values.
S1 Table. Petting Zoo Animals Search Strings.
S3 Table. Prevalence of Campylobacter in Petting Zoo Animals from Literature Review.
S4 Table. Prevalence of Campylobacter in Household Pets from Literature Review.
The authors would like to thank Janet Harris and Regan Murray from the Public Health Agency of Canada for their assistance with this work.
Conceived and designed the experiments: KP MKT AN BM FP. Performed the experiments: MA JK TC. Analyzed the data: KP TC JK. Contributed reagents/materials/analysis tools: KP. Wrote the paper: KP TC JK FP MKT BM MA AN.
- 1. Greig JD, Ravel A. Analysis of foodborne outbreak data reported internationally for source attribution. Int J Food Microbiol 2009;130(2):77–87. pmid:19178974
- 2. Pires SM, Vigre H, Makela P, Hald T. Using outbreak data for source attribution of human salmonellosis and campylobacteriosis in Europe. Foodborne Pathog Dis 2010;7(11):1351–1361. pmid:20586609
- 3. Ravel A, Greig J, Tinga C, Todd E, Campbell G, Cassidy M, et al. Exploring historical Canadian foodborne outbreak data sets for human illness attribution. J Food Protect 2009;72(9):1963–1976.
- 4. Eberhart-Phillips J, Walker N, Garrett N, Bell D, Sinclair D, Rainger W, et al. Campylobacteriosis in New Zealand: results of a case-control study. J Epidemiol Community Health 1997 Dec;51(6):686–691. pmid:9519133
- 5. Evans MR, Ribeiro CD, Salmon RL. Hazards of healthy living: bottled water and salad vegetables as risk factors for Campylobacter infection. Emerg Infect Dis 2003 Oct;9(10):1219–1225. pmid:14609455
- 6. Rind E, Pearce J. The spatial distribution of campylobacteriosis in New Zealand, 1997–2005. Epidemiol Infect 2010;138(10):1359–1371. pmid:20141648
- 7. Rosef O, Rettedal G, Lågeide L. Thermophilic campylobacters in surface water: a potential risk of campylobacteriosis. Int J Environ Health Res 2001;11(4):321–327. pmid:11798419
- 8. Kemp R, Leatherbarrow AJ, Williams NJ, Hart CA, Clough HE, Turner J, et al. Prevalence and genetic diversity of Campylobacter spp. in environmental water samples from a 100-square-kilometer predominantly dairy farming area. Appl Environ Microbiol 2005 Apr;71(4):1876–1882. pmid:15812015
- 9. Green CG, Krause DO, Wylie JL. Spatial analysis of campylobacter infection in the Canadian province of Manitoba. Int J Health Geogr 2006 Jan 16;5(2).
- 10. Arsenault J.. Épidémiologie spatiale de la campylobactériose au Québec. Québec, Canada: Université de Montréal; 2010.
- 11. Bessell PR, Matthews L, Smith-Palmer A, Rotariu O, Strachan NJC, Forbes KJ, et al. Geographic determinants of reported human Campylobacter infections in Scotland. BMC Public Health 2010;10(1):423.
- 12. Ethelberg S, Simonsen J, Gerner-Smidt P, Olsen KE, Molbak K. Spatial distribution and registry-based case-control analysis of Campylobacter infections in Denmark, 1991–2001. Am J Epidemiol 2005 Nov 15;162(10):1008–1015. pmid:16207804
- 13. Gabriel E, Wilson DJ, Leatherbarrow AJH, Cheesbrough J, Gee S, Bolton E, et al. Spatio-temporal epidemiology of Campylobacter jejuni enteritis, in an area of Northwest England, 2000–2002. Epidemiol Infect 2010;138(10):1384–1390. pmid:20202286
- 14. Jepsen MR, Simonsen J, Ethelberg S. Spatio-temporal cluster analysis of the incidence of Campylobacter cases and patients with general diarrhea in a Danish county, 1995–2004. International journal of health geographics 2009;8(1):11.
- 15. 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 May;42(5):2003–2012. pmid:15131162
- 16. Acke E, Whyte P, Jones BR, McGill K, Collins JD, Fanning S. Prevalence of thermophilic Campylobacter species in cats and dogs in two animal shelters in Ireland. Vet Rec 2006;158(2):51–54. pmid:16415232
- 17. Public Health Agency of Canada. Canadian Notifiable Disease Surveillance System Count of Reported Cases of Disease Over Time in Canada (Campylobacter). 2014; Available: http://dsol-smed.phac-aspc.gc.ca/dsol-smed/ndis/charts.php?c=pl. Accessed 17 June 2014.
- 18. Thomas MK, Murray R, Flockhart L, Pintar K, Pollari F, Fazil A, et al. Estimates of the burden of foodborne illness in Canada for 30 specified pathogens and unspecified agents, circa 2006. Foodborne Pathog Dis 2013;10(7):639–648. pmid:23659355
- 19. Alelis KA, Borkowski PE, Fiorella P, Nasir J, Middaugh J, Blackmore C, et al. Outbreak of shiga toxin-producing Escherichia coli O157 infection associated with a day camp petting zoo-Pinellas County, Florida, May-June 2007. Morb Mortal Weekly Rep 2009;58(16):426–428.
- 20. Atwill ER, McDougald NK, Perea L. Cross‐sectional study of faecal shedding of Giardia duodenalis and Cryptosporidium parvum among packstock in the Sierra Nevada Range. Equine Vet J 2000;32(3):247–252. pmid:10836481
- 21. Blagburn BL, Lindsay DS, Vaughan JL, Rippey NS, Wright JC, Lynn RC, et al. Prevalence of canine parasites based on fecal flotation. The Compendium on continuing education for the practicing veterinarian (USA) 1996.
- 22. Ballweber LR, Panuska C, Huston CL, Vasilopulos R, Pharr GT, Mackin A. Prevalence of and risk factors associated with shedding of Cryptosporidium felis in domestic cats of Mississippi and Alabama. Vet Parasitol 2009;160(3):306–310.
- 23. Goossens H, Vlaes L, Butzler J, Adnet A, Hanicq P, N'Jufom S, et al. Campylobacter upsaliensis enteritis associated with canine infections. Lancet 1991 6/15;337(8755):1486–1487.
- 24. Sokolow SH, Rand C, Marks SL, Drazenovich NL, Kather EJ, Foley JE. Epidemiologic evaluation of diarrhea in dogs in an animal shelter. Am J Vet Res 2005;66(6):1018–1024. pmid:16008226
- 25. 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. Vet J 2010;184(1):66–70. pmid:19223212
- 26. LeJeune JT, Davis MA. Outbreaks of zoonotic enteric disease associated with animal exhibits. J Am Vet Med Assoc 2004;224(9):1440–1445. pmid:15124883
- 27. Steinmuller N, Demma L, Bender JB, Eidson M, Angulo FJ. Outbreaks of enteric disease associated with animal contact: not just a foodborne problem anymore. Clin Infect Dis 2006 Dec 15;43(12):1596–1602. pmid:17109295
- 28. Thompson R. The zoonotic significance and molecular epidemiology of Giardia and giardiasis. Vet Parasitol 2004;126(1):15–35.
- 29. Hale CR, Scallan E, Cronquist AB, Dunn J, Smith K, Robinson T, et al. Estimates of enteric illness attributable to contact with animals and their environments in the United States. Clin Infect Dis 2012 Jun;54 Suppl 5:S472–9. pmid:22572672
- 30. Weese JS, Greenwood SJ, Staempfli HR. Recurrent diarrhea associated with enterotoxigenic Clostridium perfringens in 2 dogs. Can Vet J 2001 Apr;42(4):292–294. pmid:11326633
- 31. Weese JS. Bacterial enteritis in dogs and cats: diagnosis, therapy, and zoonotic potential. Vet Clin N Am: Small Anim Pract 2011;41(2):287–309.
- 32. Galanis E, Mak S, Otterstatter M, Taylor M, Zubel M, Takaro T, et al. The association between campylobacteriosis, agriculture and drinking water: a case-case study in a region of British Columbia, Canada, 2005–2009. Epidemiol Infect 2014;142(10):1–10.
- 33. Smith A, Whitfield Y. Household Pets and Zoonoses, National Collaborating Centre for Environmental Health. 2012.
- 34. Stull JW, Brophy J, Weese JS. Reducing the risk of pet-associated zoonotic infections. Canadian Medical Association Journal 2015 April 20.
- 35. Whitfield Y, Mah V, Tataryn J, Belanger P, Leonard E, Finley R, et al. Enteric Zoonoses and Pet Food Public Health Survey. 2014.
- 36. Weese JS, McCarthy L, Mossop M, Martin H, Lefebvre S. Observation of practices at petting zoos and the potential impact on zoonotic disease transmission. Clin Infect Dis 2007 Jul 1;45(1):10–15. pmid:17554694
- 37. Stull J, Peregrine A, Sargeant J, Weese J. Pet husbandry and infection control practices related to zoonotic disease risks in Ontario, Canada. BMC Public Health 2013;13(1):520.
- 38. Centers for Disease Control and Prevention. Notes from the field: Escherichia coli O157:H7 gastroenteritis associated with a State Fair—North Carolina, 2011. MMWR Morb Mortal Wkly Rep 2012 Jan 6;60(51–52):1745–1746. pmid:22217625
- 39. Proquest LLC. Refworks. 2013.
- 40. Borenstein M, Hedges LV, Higgins JP, Rothstein HR. Introduction to meta-analysis.: John Wiley & Sons; 2009.
- 41. Higgins J, Thompson SG, Spiegelhalter DJ. A re‐evaluation of random‐effects meta‐analysis. Journal of the Royal Statistical Society: Series A (Statistics in Society) 2009;172(1):137–159.
- 42. Koricheva J, Gurevitch J, Mengersen K. Handbook of meta-analysis in ecology and evolution.: Princeton University Press; 2013.
- 43. de la Paz , Manuel Posada, Groft SC. Rare diseases epidemiology.: Springer Science & Business Media; 2010.
- 44. Keithlin J, Sargeant J, Thomas MK, Fazil A. Systematic review and meta-analysis of the proportion of Campylobacter cases that develop chronic sequelae. BMC Public Health 2014 09/30;14:1203. pmid:25416162
- 45. Bell JA. Parasites of domesticated pet ferrets. Comp Cont Educ Pract 1997;16:617–620.
- 46. Bender JB, Shulman SA, Averbeck GA, Pantlin GC, Stromberg BE. Epidemiologic features of Campylobacter infection among cats in the upper midwestern United States. J Am Vet Med Assoc 2005;226(4):544–547. pmid:15742694
- 47. Bybee SN, Scorza AV, Lappin MR. Effect of the probiotic Enterococcus faecium SF68 on presence of diarrhea in cats and dogs housed in an animal shelter. J Vet Intern Med 2011;25(4):856–860. pmid:21689152
- 48. Carlin EP, Bowman DD, Scarlett JM, Garrett J, Lorentzen L. Prevalence of Giardia in symptomatic dogs and cats throughout the United States as determined by the IDEXX SNAP Giardia test. Vet Ther 2006 Fall;7(3):199–206. pmid:17039442
- 49. Cave NJ, Marks SL, Kass PH, Melli AC, Brophy MA. Evaluation of a routine diagnostic fecal panel for dogs with diarrhea. J Am Vet Med Assoc 2002 Jul 1;221(1):52–59. pmid:12420824
- 50. Cho S, Diez-Gonzalez F, Fossler CP, Wells SJ, Hedberg CW, Kaneene JB, et al. Prevalence of shiga toxin-encoding bacteria and shiga toxin-producing Escherichia coli isolates from dairy farms and county fairs. Vet Microbiol 2006;118(3):289–298.
- 51. Cole DJ, Cohen ND, Snowden K, Smith R. Prevalence of and risk factors for fecal shedding of Cryptosporidium parvum oocysts in horses. J Am Vet Med Assoc 1998 Nov 1;213(9):1296–1302. pmid:9810386
- 52. Crump JA, Sulka AC, Langer AJ, Schaben C, Crielly AS, Gage R, et al. An outbreak of Escherichia coli O157: H7 infections among visitors to a dairy farm. N Engl J Med 2002;347(8):555–560. pmid:12192014
- 53. Davies M, Engel J, Griffin D, Ginzl D, Hopkins R, Blackmore C, et al. Outbreaks of Escherichia coli O157: H7 associated with petting Zoos-North Carolina, Florida, and Arizona, 2004 and 2005 (Reprinted from MMWR, vol 54, pg 1277–1280, 2005). JAMA-J Am Med Assoc 2006;295(4):378–380.
- 54. De Santis-Kerr AC, Raghavan M, Glickman NW, Caldanaro RJ, Moore GE, Lewis HB, et al. Prevalence and risk factors for Giardia and coccidia species of pet cats in 2003–2004. J Feline Med Surg 2006;8(5):292–301. pmid:16678461
- 55. DebRoy C, Roberts E. Screening petting zoo animals for the presence of potentially pathogenic Escherichia coli. J Vet Diagn Invest 2006 Nov;18(6):597–600. pmid:17121091
- 56. Derlet RW, Carlson JR. An analysis of human pathogens found in horse/mule manure along the John Muir Trail in Kings Canyon and Sequoia and Yosemite national parks. Wilderness Environ Med 2002;13(2):113–118. pmid:12092962
- 57. Forde KN, Swinker AM, Traub-Dargatz JL, Cheney JM. The prevalence of Cryptosporidium/Giardia in the trail horse population utilizing public lands in Colorado. Journal of Equine Veterinary Science 1998;18(1):38–40.
- 58. Frederick J, Giguère S, Sanchez LC. Infectious agents detected in the feces of diarrheic foals: a retrospective study of 233 cases (2003–2008). J Gen Intern Med 2009;23(6):1254–1260.
- 59. Friedman CR, Torigian C, Shillam PJ, Hoffman RE, Heltze D, Beebe JL, et al. An outbreak of salmonellosis among children attending a reptile exhibit at a zoo. J Pediatr 1998;132(5):802–807. pmid:9602189
- 60. Gates MC, Nolan TJ. Endoparasite prevalence and recurrence across different age groups of dogs and cats. Vet Parasitol 2009;166(1):153–158.
- 61. Gookin JL, Stebbins ME, Hunt E, Burlone K, Fulton M, Hochel R, et al. Prevalence of and risk factors for feline Tritrichomonas foetus and giardia infection. J Clin Microbiol 2004 Jun;42(6):2707–2710. pmid:15184456
- 62. Hackett T, Lappin MR. Prevalence of enteric pathogens in dogs of north-central Colorado. J Am Anim Hosp Assoc 2003 Jan-Feb;39(1):52–56. pmid:12549614
- 63. Hill SL, Cheney JM, Taton-Allen GF, Reif JS, Bruns C, Lappin MR. Prevalence of enteric zoonotic organisms in cats. J Am Vet Med Assoc 2000;216(5):687–692. pmid:10707683
- 64. Centers for Disease Control and Prevention. Outbreaks of Escherichia coli O157:H7 infections among children associated with farm visits—Pennsylvania and Washington, 2000. MMWR Morb Mortal Wkly Rep 2001 Apr 20;50(15):293–297.
- 65. Aktan I, La Ragione RM, Pritchard GC, Woodward MJ. Prevalence of attaching and effacing Escherichia coli serogroup O103 in orphan lambs on an open farm in eastern england. Vet Rec 2007;161:386–388. pmid:17873270
- 66. Anonymous. Two outbreaks of Vero cytotoxin producing Escherichia coli O157 infection associated with farms. Commun Dis Rep CDR Wkly 1997 Jul 25;7(30):263.
- 67. Batchelor DJ, Tzannes S, Graham PA, Wastling JM, Pinchbeck GL, German AJ. Detection of endoparasites with zoonotic potential in dogs with gastrointestinal disease in the UK. Transbound Emerg Dis 2008;55(2):99–104. pmid:18397497
- 68. Chapman PA, Cornell J, Green C. Infection with verocytotoxin-producing Escherichia coli O157 during a visit to an inner city open farm. Epidemiol Infect 2000;125(03):531–536.
- 69. Elwin K, Chalmers RM, Roberts R, Guy EC, Casemore DP. Modification of a rapid method for the identification of gene-specific polymorphisms in Cryptosporidium parvum and its application to clinical and epidemiological investigations. Appl Environ Microbiol 2001 Dec;67(12):5581–5584. pmid:11722909
- 70. Evans MR, Roberts RJ, Ribeiro CD, Gardner D, Kembrey D. A milk-borne Campylobacter outbreak following an educational farm visit. Epidemiol Infect 1996;117(03):457–462.
- 71. Pritchard G, Willshaw GA, Bailey JR, Carson T, Cheasty T. Verocytotoxin-producing Escherichia coli O157 on a farm open to the public: outbreak investigation and longitudinal bacteriological study. Vet Rec 2000 Sep 2;147(10):259–264. pmid:11030226
- 72. Pritchard G, Marshall JA, Giles M, Chalmers RM, Marshall RN. Cryptosporidium parvum infection in orphan lambs on a farm open to the public. Vet Rec 2007 Jul 7;161(1):11–14. pmid:17617539
- 73. Pritchard G, Smith R, Ellis-Iversen J, Cheasty T, Willshaw GA. Verocytotoxigenic Escherichia coli O157 in animals on public amenity premises in England and Wales, 1997 to 2007. Vet Rec 2009 May 2;164(18):545–549. pmid:19411683
- 74. Gow AG, Gow DJ, Hall EJ, Langton D, Clarke C, Papasouliotis K. Prevalence of potentially pathogenic enteric organisms in clinically healthy kittens in the UK. Journal of Feline Medicine & Surgery 2009;11(8):655–662.
- 75. Milne LM, Plom A, Strudley I, Pritchard GC, Crooks R, Hall M, et al. Escherichia coli O157 incident associated with a farm open to members of the public. Commun Dis Public Health 1999;2(1):22–26. pmid:10462890
- 76. Mueller-Doblies D, Giles M, Elwin K, Smith RP, Clifton-Hadley FA, Chalmers RM. Distribution of Cryptosporidium species in sheep in the UK. Vet Parasitol 2008;154(3):214–219.
- 77. Netherwood T, Wood JLN, Townsend HGG, Mumford JA, Chanter N. Foal diarrhoea between 1991 and 1994 in the United Kingdom associated with Clostridium perfringens, rotavirus, Strongyloides westeri and Cryptosporidium spp. Epidemiol Infect 1996;117(02):375–383.
- 78. Ogden ID, Dallas JF, MacRae M, Rotariu O, Reay KW, Leitch M, et al. Campylobacter excreted into the environment by animal sources: prevalence, concentration shed, and host association. Foodborne pathogens and disease 2009;6(10):1161–1170. pmid:19839759
- 79. Parry SM, Salmon RL, Willshaw GA, Cheasty T, Lund LJ, Wearden P, et al. Haemorrhagic colitis in child after visit to farm visitor centre. Lancet 1995;346(8974):572.
- 80. Payne CJ, Petrovic M, Roberts RJ, Paul A, Linnane E, Walker M, et al. Vero cytotoxin-producing Escherichia coli O157 gastroenteritis in farm visitors, North Wales. Emerg Infect Dis 2003 May;9(5):526–530. pmid:12737734
- 81. Rechel B, Mahgoub H, Pritchard GC, Willshaw G, Williams C, Rodrigues B, et al. Investigation of a spatiotemporal cluster of verotoxin-producing Escherichia coli O157 infections in eastern England in 2007. Euro Surveill 2011 Jul 14;16(28):1–7.
- 82. Shukla R, Slack R, George A, Cheasty T, Rowe B, Scutter J. Escherichia coli O157 infection associated with a farm visitor centre. Commun Dis Rep CDR Rev 1995 May 26;5(6):R86–90. pmid:7606276
- 83. Stirling J, Griffith M, Blair I, Cormican M, Dooley JSG, Goldsmith CE, et al. Prevalence of gastrointestinal bacterial pathogens in a population of zoo animals. Zoonoses Public Hlth 2008;55(3):166–172.
- 84. Trevena WB, Willshaw GA, Cheasty T, Domingue G, Wray C. Transmission of Vero cytotoxin producing Escherichia coli O157 infection from farm animals to humans in Cornwall and west Devon. Commun Dis Public Health 1999 Dec;2(4):263–268. pmid:10598383
- 85. Tzannes S, Batchelor DJ, Graham PA, Pinchbeck GL, Wastling J, German AJ. Prevalence of Cryptosporidium, Giardia and Isospora species infections in pet cats with clinical signs of gastrointestinal disease. J Feline Med Surg 2008 Feb;10(1):1–8. pmid:17706446
- 86. Willshaw GA, Evans J, Cheasty T, Cummins A, Pritchard GC. Verocytotoxin-producing Escherichia coli infection and private farm visits. Vet Rec 2003 Mar 22;152(12):365–366. pmid:12678261
- 87. Moreno G, Griffiths P, Connerton I, Park R. Occurrence of campylobacters in small domestic and laboratory animals. J Appl Bacteriol 1993;75(1):49–54. pmid:8365954
- 88. Guest C, Stephen J, Price C. Prevalence of Campylobacter and four endoparasites in dog populations associated with Hearing Dogs. J Small Anim Pract 2007;48(11):632–637. pmid:17617160
- 89. Stavisky J, Radford AD, Gaskell R, Dawson S, German A, Parsons B, et al. A case–control study of pathogen and lifestyle risk factors for diarrhoea in dogs. Prev Vet Med 2011;99(2):185–192.
- 90. Burnens AP, Nicolet J. Detection of Campylobacter upsaliensis in diarrheic dogs and cats, using a selective medium with cefoperazone. Am J Vet Res 1992 Jan;53(1):48–51. pmid:1539914
- 91. Epe C, Rehkter G, Schnieder T, Lorentzen L, Kreienbrock L. Giardia in symptomatic dogs and cats in Europe—Results of a European study. Vet Parasitol 2010;173(1):32–38.
- 92. Hald B, Madsen M. Healthy puppies and kittens as carriers of Campylobacter spp., with special reference to Campylobacter upsaliensis. J Clin Microbiol 1997 Dec;35(12):3351–3352. pmid:9399557
- 93. Heuvelink AE, van Heerwaarden C, Zwartkruis-Nahuis A, Tilburg JJHC, Bos MH, Heilmann FGC, et al. Two outbreaks of campylobacteriosis associated with the consumption of raw cows' milk. Int J Food Microbiol 2009;134(1):70–74.
- 94. Heuvelink AE, Valkenburgh SM, Tilburg JJHC, Van Heerwaarden C, Zwartkruis-Nahuis JTM, De Boer E. Public farms: hygiene and zoonotic agents. Epidemiol Infect 2007;135(7):1174–1183. pmid:17313696
- 95. Heuvelink AE, Van Heerwaarden C, Zwartkruis-Nahuis JTM, Van Oosterom R, Edink K, Van Duynhoven YTHP, et al. Escherichia coli O157 infection associated with a petting zoo. Epidemiol Infect 2002;129(02):295–302.
- 96. Majewska AC, Solarczyk P, Tamang L, Graczyk TK. Equine Cryptosporidium parvum infections in western Poland. Parasitol Res 2004;93(4):274–278. pmid:15156396
- 97. Richter B, Nedorost N, Maderner A, Weissenbock H. Detection of Cryptosporidium species in feces or gastric contents from snakes and lizards as determined by polymerase chain reaction analysis and partial sequencing of the 18S ribosomal RNA gene. J Vet Diagn Invest 2011 May;23(3):430–435. pmid:21908271
- 98. Schilling AK, Hotzel H, Methner U, Sprague LD, Schmoock G, El-Adawy H, et al. Zoonotic agents in small ruminants kept on city farms in southern Germany. Appl Environ Microbiol 2012 Jun;78(11):3785–3793. pmid:22447607
- 99. Sandberg M, Bergsjø B, Hofshagen M, Skjerve E, Kruse H. Risk factors for Campylobacter infection in Norwegian cats and dogs. Prev Vet Med 2002;55(4):241–253. pmid:12392875
- 100. Blagburn BL, Schenker R, Gagne F, Drake J. Prevalence of intestinal parasites in companion animals in Ontario and Quebec, Canada, during the winter months. Vet Ther 2008 Fall;9(3):169–175. pmid:19003777
- 101. Bryan HM, Darimont CT, Paquet PC, Ellis JA, Goji N, Gouix M, et al. Exposure to infectious agents in dogs in remote coastal British Columbia: Possible sentinels of diseases in wildlife and humans. Can J Vet Res 2011 Jan;75(1):11–17. pmid:21461190
- 102. 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 Mar 10;10:1–7.
- 103. David ST, MacDougall L, Louie K, McIntyre L, Paccagnella AM, Schleicher S, et al. Petting zoo-associated Escherichia coli 0157:h7—secondary transmission, asymptomatic infection, and prolonged shedding in the classroom. Can Commun Dis Rep 2004 Oct 15;30(20):173–180. pmid:15536809
- 104. Gaunt MC, Carr AP. A survey of intestinal parasites in dogs from Saskatoon, Saskatchewan. Can Vet J 2011 May;52(5):497–500. pmid:22043068
- 105. Himsworth CG, Skinner S, Chaban B, Jenkins E, Wagner BA, Harms NJ, et al. Multiple zoonotic pathogens identified in canine feces collected from a remote Canadian indigenous community. Am J Trop Med Hyg 2010 Aug;83(2):338–341. pmid:20682878
- 106. Jacobs SR, Forrester CP, Yang J. A survey of the prevalence of Giardia in dogs presented to Canadian veterinary practices. Can Vet J 2001 Jan;42(1):45–46. pmid:11195521
- 107. Lefebvre SL, Waltner-Toews D, Peregrine AS, Reid-Smith R, Hodge L, Arroyo LGl, et al. Prevalence of zoonotic agents in dogs visiting hospitalized people in Ontario: implications for infection control. J Hosp Infect 2006;62(4):458–466. pmid:16466831
- 108. 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. Epidemiol Infect 2011;139(10):1531–1541. pmid:21208515
- 109. McDowall RM, Peregrine AS, Leonard EK, Lacombe C, Lake M, Rebelo AR, et al. Evaluation of the zoonotic potential of Giardia duodenalis in fecal samples from dogs and cats in Ontario. Canadian Vet J 2011;52(12):1329.
- 110. Olson ME, Leonard NJ, Strout J. Prevalence and diagnosis of Giardia infection in dogs and cats using a fecal antigen test and fecal smear. Can Vet J 2010 Jun;51(6):640–642. pmid:20808578
- 111. Shukla R, Giraldo P, Kraliz A, Finnigan M, Sanchez AL. Cryptosporidium spp. and other zoonotic enteric parasites in a sample of domestic dogs and cats in the Niagara region of Ontario. Can Vet J 2006 Dec;47(12):1179–1184. pmid:17217087
- 112. Sockett PN, Rodgers FG. Enteric and foodborne disease in children: A review of the influence of food- and environment-related risk factors. Paediatr Child Health 2001 Apr;6(4):203–209. pmid:20084237
- 113. Warshawsky B, Gutmanis I, Henry B, Dow J, Reffle J, Pollett G, et al. Outbreak of Escherichia coli 0157:H7 related to animal contact at a petting zoo. Can J Infect Dis 2002 May;13(3):175–181. pmid:18159389
- 114. Engvall EO, Brändström B, Andersson L, Båverud 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):713–718. pmid:14606609
- 115. Moser I, Rieksneuwohner B, Lentzsch P, Schwerk P, Wieler LH. Genomic heterogeneity and O-antigenic diversity of Campylobacter upsaliensis and Campylobacter helveticus strains isolated from dogs and cats in Germany. J Clin Microbiol 2001 Jul;39(7):2548–2557. pmid:11427567
- 116. Rossi M, Hänninen M, Revez J, Hannula M, Zanoni R. Occurrence and species level diagnostics of Campylobacter spp., enteric Helicobacter spp. and Anaerobiospirillum spp. in healthy and diarrheic dogs and cats. Vet Microbiol 2008;129(3):304–314.
- 117. Moyaert H, Ceelen L, Dewulf J, Haesebrouck F, Pasmans F. PCR detection of Campylobacter species in feces from dogs. Vlaams Diergeneeskundig Tijdscrift 2008;78:92–96.
- 118. Carbonero A, Torralbo A, Borge C, García-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):505–512. pmid:22640550
- 119. 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 Oct 31;165(18):526–530. pmid:19880860
- 120. McGlade TR, Robertson ID, Elliot AD, Thompson RCA. High Prevalence of Giardia detected in cats by PCR. Vet Parasitol 2003;110(3):197–205.
- 121. Baker J, Barton MD, Lanser J. Campylobacter species in cats and dogs in South Australia. Aust Vet J 1999;77(10):662–666. pmid:10590795
- 122. Kingsbury DD, Marks SL, Cave NJ, Grahn RA. Identification of Tritrichomonas foetus and Giardia spp. infection in pedigree show cats in New Zealand. N Z Vet J 2010;58(1):6–10. pmid:20200569
- 123. 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 Jun 1;34(11):E59–60. pmid:12015708
- 124. Evers E, Van Der Fels-Klerx H, Nauta M, Schijven J. Campylobacter source attribution by exposure assessment. Int J Risk Assess Manag 2008;8(1):174–190.
- 125. Pintar K, Ravel A, Thomas MK, Christidis T, Otten A, Nesbitt A, et al. A comparative exposure assessment of Campylobacter in Ontario, Canada.
- 126. Public Health Agency of Canada. 2012 Short Report FoodNet Canada: Canada's National Integrated Enteric Pathogen Surveillance System. 2014;HP37-17/1-2012E-PDF.
- 127. Guévremont E, Lamoureux L, Loubier CB, Villeneuve S, Dubuc J. Detection and Characterization of Campylobacter spp. from 40 Dairy Cattle Herds in Quebec, Canada. Foodborne Pathog Dis 2014;11(5):388–394. pmid:24617502
- 128. Lee MK, Billington SJ, Joens LA. Potential virulence and antimicrobial susceptibility of Campylobacter jejuni isolates from food and companion animals. Foodborne Pathog Dis 2004;1(4):223–230. pmid:15992284
- 129. Spain CV, Scarlett JM, Wade SE, McDonough P. Prevalence of enteric zoonotic agents in cats less than 1 year old in central New York State. J Vet Intern Med 2001;15(1):33–38. pmid:11215908
- 130. Queen EV, Marks SL, Farver TB. Prevalence of selected bacterial and parasitic agents in feces from diarrheic and healthy control cats from Northern California. J Vet Intern Med 2012;26(1):54–60. pmid:22182203
- 131. Kovats RS, Edwards SJ, Charron D, Cowden J, D’Souza RM, Ebi KL, et al. Climate variability and campylobacter infection: an international study. Int J Biometeorol 2005;49(4):207–214. pmid:15565278
- 132. Nylen G, Dunstan F, Palmer S, Andersson Y, Bager F, Cowden J, et al. The seasonal distribution of campylobacter infection in nine European countries and New Zealand. Epidemiol Infect 2002;128(03):383–390.
- 133. Centers for Disease Control and Prevention. Compendium of Measures to Prevent Disease Associated with Animals in Public Settings, 2011. MMWR Morb Mortal Wkly Rep 2011;60(4).
- 134. Hemsworth S, Pizer B. Pet ownership in immunocompromised children—A review of the literature and survey of existing guidelines. Eur J Oncol Nurs 2006 4;10(2):117–127. pmid:16581294
- 135. Keen JE, Wittum TE, Dunn JR, Bono JL, Durso LM. Shiga-toxigenic Escherichia coli O157 in agricultural fair livestock, United States. Emerging Infect Dis 2006;12(5):780–786. pmid:16704838
- 136. Small A, Reid C-, Avery SM, Karabasil N, Crowley C, Buncic S. Potential for the Spread of Escherichia coli O157, Salmonella, and Campylobacter in the Lairage Environment at Abattoirs. J Food Prot 2002;65(6):931–936. pmid:12092725
- 137. Paiba GA, Wilesmith JW, Evans SJ, Pascoe SJ, Smith RP, Kidd SA, et al. Prevalence of faecal excretion of verocytotoxigenic Escherichia coli O157 in cattle in England and Wales. Vet Rec 2003 09;153(12):347–353. pmid:14533765
- 138. Atwill ER, Johnson E, Klingborg DJ, Veserat GM, Markegard G, Jensen WA, et al. Age, geographic, and temporal distribution of fecal shedding of Cryptosporidium parvum oocysts in cow-calf herds. Am J Vet Res 1999 Apr;60(4):420–425. pmid:10211683
- 139. Line J, Hiett K, Conlan A. Comparison of Challenge Models for Determining the Colonization Dose of Campylobacter jejuni in Broiler Chicks. Poultry Sci 2008 September 01;87(9):1700–1706.
- 140. Wells DL. Comparison of two treatments for preventing dogs eating their own faeces. Vet Rec 2003 07;153(2):51–53. pmid:12885213
- 141. Gonzalez AE, Lopez-Urbina T, Tsang B, Gavidia C, Garcia HH, Silva ME, et al. Transmission dynamics of Taenia solium and potential for pig-to-pig transmission. Parasitol Int 2006;55:S131–135. pmid:16352459
- 142. Kiang KM, Scheftel JM, Leano FT, Taylor CM, Belle-Isle PA, Cebelinski EA, et al. Recurrent outbreaks of cryptosporidiosis associated with calves among students at an educational farm programme, Minnesota, 2003. Epidemiol Infect 2006;134(04):878–886.
- 143. Stanley K, Jones K. Cattle and sheep farms as reservoirs of Campylobacter. J Appl Microbiol 2003;94:104–113.
- 144. Inglis GD, Kalischuk LD. Direct quantification of Campylobacter jejuni and Campylobacter lanienae in feces of cattle by real-time quantitative PCR. Appl Environ Microbiol 2004 Apr;70(4):2296–2306. pmid:15066825
- 145. Asensio L, González I, García T, Martin R. Determination of food authenticity by enzyme-linked immunosorbent assay (ELISA). Food Control 2008;19(1):1–8.
- 146. Butler AJ, Thomas MK, Pintar KD. Expert elicitation as a means to attribute 28 enteric pathogens to foodborne, waterborne, animal contact, and person-to-person transmission routes in canada. Foodborne pathogens and disease. 2015;12: 335–344. pmid:25835810