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

Pet ownership is common, with the majority of households in many developed countries owning pets [1–8]. A recent study estimated that 56% of Canadian homes have at least one dog or cat, with a minority owning fish (12%), birds (5%), rabbits or hamsters (each 2%), lizards, guinea pigs, snakes, frogs, turtles, ferrets, or gerbils (each 1%) [6]. Pet ownership has been shown to have mental and physical benefits [9], particularly among children, the elderly and immunocompromised individuals [10–16]. However, despite these benefits, there are also potential health hazards associated with pet ownership and contact.

A recent estimate suggests that 14% of all human illness caused by seven common enteric pathogen groups (i.e., Campylobacter spp, Cryptosporidium spp, Shiga toxin–producing Escherichia coli (STEC) O157, STEC non-O157, Listeria monocytogenes, nontyphoidal Salmonella spp., and Yersinia enterocolitica) are attributable to animal contact [17]. Although the proportion of human disease for which pets are specifically responsible is largely unknown, greater than 70 pathogens of companion animals are known to be transmissible to people [18] and pet contact has been clearly established as a risk factor for illness caused by various pathogens, including Campylobacter[19, 20], Salmonella[21], Pasteurella multocida[22] and Capnocytophaga canimorsus[23]. For some pet species, their role in human disease has been more clearly identified; reptiles and amphibians are estimated to be responsible for 6% of all sporadic Salmonella infections (11% among persons less than 21 yrs old) [24]. The emergence and dissemination of multidrug-resistant bacteria in both humans and companion animals has created additional concerns [25, 26].

People can acquire pet-associated zoonotic organisms through the skin and mucous membranes (via animal bites, scratches, or direct or indirect contact with animal saliva, urine and other body fluids or secretions), ingestion of animal fecal material, inhalation of infectious aerosols or droplets, and through arthropods or other invertebrate vectors [27]. Although any exposed person can become infected with a zoonotic pathogen, risks are particularly high for those with a compromised or incompletely developed immune system, such as the young (< 5 yrs), elderly (≥ 65 yrs), pregnant and those with immune function-reducing conditions or treatments (e.g., diabetes, cancer, infection with human immunodeficiency virus (HIV), chemotherapy) [27, 28].

Although incompletely understood, there are many factors that are involved in the occurrence of a zoonotic infection from a pet. Several of these factors likely have important roles in determining if an individual becomes infected, becomes symptomatic once infected, and the degree of illness that occurs. These include: 1) level and dose of exposure to the pathogen, 2) ability of the individual to suppress infection, with immunocompromised and extremes of age less able to successfully respond immunologically to pathogens, and 3) preventative veterinary care, husbandry and infection control practices that remove or reduce the level of the pathogen present and risk of transmission [27]. Existing recommendations stress that those at greatest risk for infectious disease should take the greatest precautions when interacting with pets, and be the most diligent in following infection prevention practices [29–35].

Despite the risk for pet-associated disease in people and role that appropriate infection control and husbandry practices may play in reducing disease risk, the area of household pet husbandry and infection practices has not been thoroughly investigated. The studies that have examined these topics, have noted the frequency of close contact between pets and people (e.g., licking of hands and sleeping in household member beds [36, 37]), general pet ownership patterns by individuals at higher risk of disease [15, 38–43], and general husbandry and infection control practices within pet-owning households (e.g., frequency of preventive veterinary care [40, 44], and occurrence of hand hygiene [36, 37] and husbandry practices [36, 45]). However, previous studies have not analyzed the associations between these factors, which would allow for a better understanding of how the factors may change with differing household disease risks or with prior receipt of zoonotic disease education. The objective of this study was therefore to characterize pet husbandry and infection control practices that relate to zoonotic disease risks in pet-owning households in Ontario, Canada. Additionally, the study aimed to integrate household demographics, including human disease risk status (i.e., extremes of age, immunocompromised) and prior receipt of zoonotic disease education to determine if these factors influenced household practices.

Six hundred forty one of the 853 individuals who were approached (75.1%) completed the general questionnaire [47]. Of these, 408 respondents (63.7%) reported having one or more household pets and 401 (98%) completed the supplemental pet-specific questionnaire. Ownership of dogs, cats, exotic companion animals (such as gerbils and rabbits), reptiles and birds were reported. In addition to having household pets, 16 (4.0%) of the respondents reported they lived on a farm where livestock, horses, or poultry were kept.

As pet-human contact frequently occurs and disease transmission is overall rarely reported [47], in most situations such contact should not pose a substantial health risk. However, there are practices that may increase pathogen exposure and individuals (< 5yrs, ≥ 65yrs, or immunocompromised) for whom these risks are known or presumed to be greater. Reported husbandry and infection control practices in this study indicated opportunities for exposure to pathogens. Respondents reported household children had close contact with pets (e.g., face licking, sleeping in beds, cleaning up pet fecal material). These findings are similar to a previous study in which dogs licked their owners’ face (50%) and dogs and cats slept in an adult’s bed (18%, 30%, respectively) [37]. The oral cavity of the dog and cat contain numerous potentially zoonotic opportunistic pathogens [49] and face licking can result in transmission of bacteria such as Pasteurella spp. and Capnocytophaga canimorsus[50], potentially resulting in life-threatening disease [22]. For these reasons, some discourage young children and immunocompromised individuals from regularly allowing face licking by pets [50]. The disease risk associated with dogs and cats sleeping in a child’s bed is largely unquantified, however sleeping with pets has been identified as a risk factor for several diseases, prompting some to discourage this practice by higher risk individuals [50].

Routine preventive veterinary care and husbandry practices are important techniques for reducing zoonotic disease transmission between pets and people [30, 35]. Consistent with previous studies [40, 44], most cat- and dog-owning households had these animals examined at least annually by a veterinarian, which allows for identification and education of potential disease concerns and facilitates implementation of an appropriate preventive medicine program. The differences observed between dog and cat preventative veterinary care, with cats having lesser veterinary contact, has been previously noted [40, 44]. Since cats have less contact with the veterinary healthcare system yet have close interactions with household members, educational approaches that reach beyond the veterinary clinic may be required.

Concerning husbandry practices were observed in all owned species. Feeding of raw meat or egg products are well-established risk factors for salmonellosis in dogs [45, 51] and presumably cats. Raw animal product treats (i.e. pig ears) have historically been a concern for Salmonella infections in pets and pet-owners, with outbreaks identified [52, 53]. Although feeding these items is discouraged, particularly in higher risk households [54], many households reported this practice. These risks are further compounded by feeding pets in the kitchen (frequently reported in this study) as documented in an outbreak investigation of salmonellosis in infants linked to Salmonella-contaminated pet food [55]. As several outbreaks of human salmonellosis have been associated with contaminated dry commercial pet food [55, 56], feeding pets in the kitchen should be discouraged, especially in higher risk households [29]. Concerning husbandry practices were frequently reported in reptile-owning homes (e.g., infrequent hand washing, permitting them to roam freely through a home or kitchen). Due to the high prevalence of Salmonella shedding by healthy reptiles [57] and the high incidence of human salmonellosis attributed to reptile contact [24], the reported practices are strongly discouraged [34, 58].

Hand hygiene serves a critical role in reducing the risk of zoonotic infections. Our results were similar to previous studies in which 96% of dog owners reported they usually or greater washed their hands after picking up feces [36] and 15% always washed their hands after touching the dog [37]. For lower risk circumstances, such as contact with a dog or cat, the level of hand hygiene documented in our study is likely adequate; however, in higher-risk situations, such as following contact with a reptile, hand washing should always occur.

Across all animal species that were owned, many households had an individual at higher risk of infections (< 5yrs, ≥ 65yrs, immunocompromised). Although pet ownership has previously been commonly reported in households with individuals who are immunocompromised [15, 38, 39] and of extremes of age [40–43], it was concerning to observe this trend with higher risk species such as reptiles, which are discouraged from being kept in higher risk households [29, 31–34, 58]. However, this finding was not surprising as a previous study involving this respondent group found households with higher risk individuals did not differ from the remaining households regarding their knowledge or perceived risk of pet-associated disease or recall of having received information regarding pet-associated disease risks [47]. Physicians and veterinarians are in an important position to offer guidance on proper pet selection. In order to tailor recommendations, physicians should obtain a history of contact with pets or other animals as part of every wellness evaluation, especially for individuals at higher risk of zoonotic disease, and veterinarians should utilize methods to encourage clients to divulge health information relevant to disease risk status for household members.

Despite evaluating over 50 practices consistent with existing recommendations for individuals at greater risk for infectious disease [29–35], few significant associations were identified. Most of those identified suggested a lower risk of practice occurrence in households with young children; the extent to which such decisions were purposefully implemented versus simply a consequence of young age is unknown. The finding that young children were at increased risk to be licked on the face by the household dog was expected due to their age and size, but nonetheless concerning because of reports of lick-associated infections in children [22, 50].

The limited use of husbandry and infection control practices by households with higher risk individuals was disappointing but not surprising. Previous research on this respondent group found pet owners were overall unconcerned about pet-associated zoonoses and a minority (36%) recalled previously receiving zoonotic disease education [47]. Most respondents were comfortable with their level of knowledge of, and methods to reduce, zoonotic disease risk [47]. While it is unclear whether participants had reasonable knowledge of those areas, their perceived competency could reduce the impetus to seek out further information.

General zoonotic disease counselling was previously associated with statistically higher zoonotic disease knowledge scores in this respondent group [47], yet no such difference was observed in husbandry or infection control practices in the present study. This discrepancy may have arisen due to the minimally defined nature of this variable (i.e. timing and quality of information provided were not assessed), but it is also possible that although education imparted improved knowledge of zoonotic disease risks, due to a lack of concern for pet-associated zoonoses or competing time commitments, infection control and husbandry practices were unaffected. It is also possible that education regarding diseases was not accompanied by adequate information about preventive measures.

This study identified numerous pet husbandry and infection control practices that may increase disease risk in pet-owning households. In order to determine the relative importance of these practices and educational efforts that should be employed, targeted observational studies are needed. While guidelines for infection-control practices in higher risk households are available, it appears that individuals in such households are no better educated on the topic of pet-associated zoonoses [47], nor do their husbandry or infection control practices differ from other households. Educational efforts are needed for households with individuals at higher risk of infections. Given the multifaceted nature of this topic, with communication barriers among physicians, veterinarians and the public [59–61], all members of the family healthcare team (i.e., physicians, veterinarians, public health) must work together to reach the common goal of reducing the public’s pet-associated disease risks.

Several biases may have been introduced into this study and affected the results. We acquired our data from a convenience sample from the waiting room of general practice physician offices from a limited geographic area. All Canadian residents receive medically necessary healthcare services at no charge [62], reducing the potential that variable access to physicians would result in a biased study population. As previously discussed [47], based on census data, our sample appeared to be representative of the region. Response bias cannot be excluded, however as blank and “don’t know” responses were uncommon (<20% for each question with the majority <10%), the magnitude of this bias is likely limited. As many questions addressed health-related actions taken by respondents for which they may have known what answers were ideal, respondents may have misclassified household practices. In these cases, information provided would suggest better husbandry and infection control practices than actually existed. This was perhaps most likely for questions surrounding hand washing [63]. As only a single individual from each household participated in the study, it is possible reported observations and perceptions may not have been representative of the household. Due to the nature of this study, small sample sizes were often encountered, which in some cases prohibited analysis and in others may have limited statistical power. Furthermore, small sample sizes prohibited multivariable analysis and the ability to investigate confounding. A large number of individual regression analyses were conducted and corrections were not made for this multiplicity of testing; estimates are likely to have an increased type I error and fewer significant associations may exist than reported.

This study characterized pet husbandry and infection control practices that relate to zoonotic disease risks in pet-owning households in Ontario, Canada, and identified deficiencies that could result in exposure to pathogens and human zoonotic infections. Individuals at higher risk of infections were frequently present in pet-owning households, regardless of species. With few exceptions, households with members at higher risk for infectious disease and those who recalled having received education on pet-associated disease risks followed similar practices to households without these individuals or education. Targeted educational efforts are indicated for households with individuals at higher risk of infections and those with high-risk species (e.g., reptiles). Healthcare team members, including veterinarians, physicians and public health practitioners, have the potential to serve as valuable resources in reducing pet-associated disease risks, however all must jointly work to address this area and devote more attention toward the public’s interaction with animals. Further research is needed to determine the reasoning behind household infection control and husbandry practices and the respective roles of education and perceptions in shaping these practices.