Pet husbandry and infection control practices related to zoonotic disease risks in Ontario, Canada

The site chosen for this study was the region of Waterloo, located in southern Ontario, Canada. The Waterloo Region is composed of three urban and four rural municipalities. This region was selected as it includes both rural and urban settings and its population has similar demographics to the Province of Ontario and Canada as a whole [46]. As of 2006, this region had a population of approximately 478,000 people in 178,000 private households. The median age was 36.4 yrs, with 81% of the population greater than 14 yrs. Median household annual income was $65,000 CAD [46]. These statistics are similar to those for the Province of Ontario and all of Canada, with the exception of a higher household median annual income ($60,000 for Ontario, $54,000 for Canada) [46].

Medical clinic and participant enrolment was part of a previously reported study that addressed knowledge and attitudes related to pet contact and associated zoonoses. Detailed enrolment methods and inclusion criteria are available elsewhere [47]. In brief, a convenience sample of multi-doctor general practice physician offices located within the Waterloo region was approached to participate in the study. Two practices agreed to participate (clinic A in Kitchener, Ontario and clinic B in Cambridge, Ontario).

During October and November, 2010, adults present in the waiting areas of the participating clinics were individually approached and invited to take part in the study. Individuals were eligible to participate if they were at least 18 yrs of age, able to read and speak English, and no one from their household had previously taken part in the study. When more than one eligible adult for a given household was present in the waiting area, a single household volunteer was requested. Participants were asked to complete an anonymous, confidential, self-administered written general questionnaire. Individuals who currently had pets in their household were also given a self-administered written 5-minute supplemental pet-specific questionnaire (Additional file 1). Household pets were defined as those that were indoor only, outdoor only, and those that spent time both indoor and outdoor. No incentives were offered for participating in the study.

The 7-page supplemental pet-specific questionnaire for this study was developed with guidance from epidemiologists, veterinarians, physicians and zoonotic disease experts. The questionnaire was pre-tested on six members of the public with varying zoonotic disease backgrounds, and revised accordingly. The final questionnaire utilized closed-ended questions, primarily Yes/No or multiple choice (using an ordinal scale). It gathered household-level data on the number and species of pets, pet husbandry and preventive medicine practices, involvement of children less than 16 yrs of age in select husbandry and pet-contact practices, childrens’ utilization of infection control practices, and the household’s and childrens’ emotional attachment to pets. Given the complexity of capturing and assessing flea and endoparasite prevention programs for each household pet, respondents were asked if all household dogs/cats were on intestinal parasite and flea prevention programs, without further defining, verifying or assessing specific components of the programs. Individual supplemental questionnaires were linked by respondent to the general questionnaire [47], allowing select variables collected through the general questionnaire to be utilized for additional analysis in this study. The study was approved by the University of Guelph’s Research Ethics Board.

Data were entered into an Access database (Microsoft Corp., Redmond, WA, USA) and analyzed using Intercooled Stata version 10.1 (Stata Corp., College Station, TX, USA). Descriptive statistics were computed for all variables. Blank and “don’t know” responses were excluded from analyses. Household demographic and health data were extracted from the general questionnaire [47] to characterize households as higher risk [one or more individuals < 5 yrs, ≥ 65 yrs, or ever diagnosed with an immunocompromising condition (such as HIV/acquired immunodeficiency syndrome (AIDS), diabetes, cancer)] or not higher risk. Data regarding the respondents’ recall of having previously received pet-associated zoonotic disease education (i.e. having ever received information from any source about diseases that can be transmitted from pets or precautions to take with pets) were also extracted from the general questionnaire [47]. For statistical analysis, ordinal levels of each pet husbandry and infection control practice were collapsed to produce dichotomous outcome variables; decisions on how categories were collapsed were made a priori and based on existing recommendations for higher risk households and relevance of comparisons (Table 1) [29‐35]. Statistical associations were individually assessed between pet husbandry and infection control practices (outcomes) and 1) households with individuals at higher risk of infections [at least one individual < 5 yrs, ≥ 65 yrs, or immunocompromised (exposed) vs. no one fulfilling these criteria (unexposed)] and 2) receipt of zoonotic disease education [previous receipt of pet-associated zoonotic disease education (exposed) vs. no recollection of having received this information (unexposed)]; Table 1. For households with children under 16 yrs of age, statistical associations were individually assessed between child-specific husbandry and infection control practices (e.g., child’s involvement and precautions taken in cleaning pet’s cages or feces, level of contact with pets) and households with all children at higher risk of infectious disease [presence of all household children < 5 yrs (exposed) vs. presence of all household children ≥ 5 yrs (unexposed)]. Due to small sample sizes for many of the variables, associations were measured using univariate exact logistic regression with conditional maximum likelihood estimates (CMLEs). When CMLEs were computed to be infinite, median unbiased estimates were calculated [48]. Odds ratios (ORs) and 95% confidence intervals (CI) for ORs were used to estimate the strength of associations. Statistical significance was based on a P-value < 0.05.

Dogs were the most frequently reported owned species, with 68.3% [(274/401); 95% CI: 63.5, 72.9] of respondents reporting one or more household dogs. For those respondents listing the number of dogs in the household (n=254), there was a mean (SD) of 1.3 (0.6) dogs per household (range: 1–6). The location of the dog was provided by 239 households; 6 households (2.5 %) had 1 or more outdoor only dogs, 231 (96.7 %) had one or more indoor/outdoor dogs, and 2 (0.8%) had both outdoor only and indoor/outdoor dogs.

Household demographics, animal husbandry, attachment and infection control practices for dog-owning households are listed in Table 2. The majority (52%) of households surveyed had one or more higher risk individuals. Forty percent of the dog-owning respondents recalled having ever received information about pet-associated zoonotic diseases or precautions to reduce the risk of disease.

Most (76-80%) dog-owning households had all dogs on flea or endoparasite prevention programs, with 92% of respondents taking all dogs to a veterinarian at least annually. High risk feeding or drinking habits were observed in many households. Most households (65%) fed dogs in the kitchen and some (15%) reported dogs drank from the toilet. High-risk foods were fed to dogs in 28% of households with raw animal product treats (e.g. pig ears) fed most frequently (22%), followed by raw meat (4%), and raw eggs (3%).

Potential contact between household children (< 16 yrs) and fecal material was frequently reported, through their involvement in cleaning up fecal material (24%) or playing in the same area where the dog tended to defecate (52%; 58% of these respondents stated feces were removed weekly or less often). Close contact between dogs and children was often reported, as respondents stated the dog slept in a child’s bed (26%) or licked a child’s face (68%) sometimes or more frequently. Hand washing was reported after children picked up feces (96%), and sometimes or greater following contact with the dog (77%).

In most cases the presence of higher risk individuals in the household or recalled receipt of zoonotic disease education were not significantly associated with the use of different or additional husbandry or infection control practices compared to other households (Table 3). Households with all children less than 5 yrs of age were less likely to report children cleaned up the dog’s feces (OR: 0.05; 95% CI: 0–0.3), but more likely to report a dog ever licked a child’s face (OR: 4.1; 1.1-23.5), than households with all children ≥ 5 yrs.

One hundred ninety one respondents (47.6%; 95% CI: 42.7, 52.6) reported owning one or more household cats. For those respondents listing the number of cats in the household (n=178), there was a mean (SD) of 1.7 (1.4) cats per household (range: 1–11). The location of the cat was provided by 176 households; 7 households (4%) had one or more outdoor only cats, 114 (65%) had one or more indoor only cats, and 73 (41%) had one or more indoor/outdoor cats. However, 41 (56%) of households with indoor/outdoor cats kept cats restrained on a leash when outdoors.

Household demographics, animal husbandry, attachment and infection control practices for cat-owning households are listed in Table 2. The majority (53%) of households had one or more higher risk individuals. Forty-four percent of the cat-owning respondents recalled having ever received information about pet-associated zoonotic diseases or precautions to reduce the risk of disease.

Bites and scratches ever occurring by any of the current household cats were frequently reported (32% and 63%, respectively). Approximately half of responding households had all cats on flea (55%) or endoparasite (42%) prevention programs, with 66% of households taking all cats to a veterinarian at least annually. High risk feeding and drinking habits were frequently observed, with many households (57%) having fed cats in the kitchen. High-risk foods were fed to cats in 3% of households with raw meat (3%) and raw eggs (0.5%) reported.

Potential contact between children and fecal material was frequently reported, through their involvement in cleaning up fecal material (25%) or access to the litter box (66%). Twenty-one percent of respondents reported the litter box was cleaned weekly or less often; this percentage was similar for households with and without children. Close contact between cats and children was frequently reported, as 59% of households reported a cat slept in a child’s bed. Hand washing was reported after children picked up feces (100%) and sometimes or greater following contact with the cat (76%).

The presence of only children under 5 yrs of age in the household was significantly associated with the occurrence of several infection control practices compared to households with all children 5 yrs of age or older (Table 3). Households with all children less than 5 yrs were less likely to report children cleaned up the cat’s feces (OR: 0.07; 95% CI: 0–0.5), less likely to touch the cat (OR: 0.04; 95% CI: 0–0.3), less likely to have access to the litter box (OR: 0.1; 95% CI: 0.02-0.4), and more likely for the cat to never sleep in the child’s bed (OR: 12.9; 95% CI: 2.4-135.9), than households in which all children were ≥ 5 yrs.

Fifty-three respondents (13.2%; 95% CI: 10.1, 16.9) reported one or more household fish (median 4 fish per household; range: 1–60). Household demographics, animal husbandry, attachment and infection control practices are listed in Table 4. The majority (53%) of households had one or more higher risk individuals. Thirty percent of the fish-owning respondents recalled having ever received information about pet-associated zoonotic diseases or precautions to reduce the risk of disease.

Forty-four percent of respondents stated they disposed of used aquarium water by pouring it into a location with direct human or food contact [i.e., kitchen sink (24%), bathroom sink (16%), bathtub/shower (6%)]. Those households with higher risk members were less likely to dispose of aquarium water in this manner than households without these members (OR: 0.2; 95% CI: 0.05-0.9; Table 3). When children were present in a household, they were frequently involved with cleaning the aquarium (30%) and touching the fish or water (40%). Over 90% of households reported that children washed their hands after cleaning, or washed their hands sometimes or greater after touching the fish or water. A large percentage (43-46%) of households reported the household and children (if present) were not very, or not at all, attached to the fish.

Twenty-two respondents (5.5%; 95% CI: 3.5, 8.2) reported one or more household birds (median one bird per household; range: 1–40). Household demographics, animal husbandry, attachment and infection control practices for bird-owning households are listed in Table 4. The majority (57%) of households had one or more higher risk individuals. Thirty-three percent of the bird-owning respondents recalled having ever received information about pet-associated zoonotic diseases or precautions to reduce the risk of disease. Households with higher risk individuals were more likely to be very attached to the birds than households without these individuals (OR: 11.5; 95% CI: 1.3-infinite; Table 3).

Twenty-nine respondents (7.2%; 95% CI: 4.9, 10.2) reported one or more household exotic mammals (median 1 per household; range: 1–13), consisting of hamsters (n=10), rabbits (6), guinea pigs (5), rats/mice (4) and hedgehogs, chinchillas and gerbils (2 each). Household demographics, animal husbandry, attachment and infection control practices for exotic mammal-owning households are listed in Table 5. Many (46%) households had one or more higher risk individuals. Three households (10%) had at least one child less than 5 yrs of age. Forty-one percent of the respondents recalled having ever received information about pet-associated zoonotic diseases or precautions to reduce the risk of disease.

When children were present in a household, they were frequently involved with cleaning the animal’s cage (63%) or touching the pet (100%). Most children reportedly washed their hands after cleaning the cage (92%) or washed their hands sometimes or greater after touching the pet (100%). A minority (42%) always washed their hands after touching the pet. Most respondents (> 90%) reported the household and children (if present) were very or somewhat attached to the pets. No statistically significant associations between husbandry/infection control practices and risk factors were detected.

Twenty-two respondents (5.5%; 95% CI: 3.5, 8.2) reported one or more household reptiles (median one per household; range: 1–11), consisting of lizards (n=9), snakes (5), and turtles (9). Household demographics, animal husbandry, attachment and infection control practices for reptile-owning households are listed in Table 5. Many households (55%) had one or more higher risk individuals, with a high proportion (47%) having been diagnosed with an immunocompromising condition. Two households (9%) had at least one child less than 5 yrs of age. Forty-one percent of the reptile-owning respondents recalled having ever received information about pet-associated zoonotic diseases or precautions to reduce the risk of disease.

Three respondents (14%) reported the pet reptile was allowed to roam through the house, kitchen or washed in the kitchen sink. When children were present in a household, they were often involved with cleaning the animal’s cage (40%) or touching the pet (78%). In one household in which children touched the reptile, all children (n=2) were less than 5 yrs. Most respondents reported the children washed their hands after cleaning the cage (75%) or washed their hands sometimes or greater after touching the pet (86%). However, only 57% always washed their hands after touching the reptile. Many respondents reported the household and children (if present) were not very, or not at all, attached to the reptile (33% and 40%, respectively). No statistically significant associations between husbandry/infection control practices and risk factors were detected.

Sixteen respondents (4.0% of those with household pets; 95% CI: 2.3, 6.4) reported they lived on a farm. Respondents most commonly listed horses (n=9), chickens (5), cattle and pigs (3 each) as the farm animals present. Fifty percent (7/14) of households for which the data were provided had one or more higher risk individuals. When children were present [6/16 (38%)], they were often involved in higher risk activities. Most [5/6 (83%)] of such households reported children helped feed and clean-up after the farm animals at least sometimes, and in most households [5/6 (83%)] children usually or always washed their hands after contact with the animals or their housing.