Article

Nutritional and microbial analysis of bully sticks and survey of opinions about pet treats

Authors:
To read the full-text of this research, you can request a copy directly from the authors.

Abstract

The objectives of this study were to measure the caloric density of bully sticks, to analyze the bully sticks for bacterial contamination, and to assess owner opinions about these and other pet treat products. Mean caloric density was 15 kcal/inch (38 kcal/cm) [range: 9 to 22 kcal/inch (23 to 56 kcal/cm), 2.96 to 3.07 kcal/g]. Of 26 bully sticks that were tested for bacterial contamination 1 (4%) was contaminated with Clostridium difficile, 1 was contaminated with methicillin-resistant Staphylococcus aureus (MRSA), and 1 with a tetracycline resistant Escherichia coli.

No full-text available

Request Full-text Paper PDF

To read the full-text of this research,
you can request a copy directly from the authors.

... Even if the popularity of dog treats has been shown by many surveys (Bland, Guthrie-Jones, Taylor, & Hill, 2009;Courcier, Thomson, Mellor, & Yam, 2010;Heuberger & Wakshlag, 2011;Laflamme et al., 2008;Robertson, 2003;Rohlf, Toukhsati, Coleman, & Bennett, 2010;White, Ward, Pink, Craigon, & Millar, 2016), very little is known about these products. Only a few studies have considered dog treats, and especially their role in the spread of pathogens has been demonstrated, since most such studies focused on analyzing treat bacterial contamination (Clark et al., 2001;Freeman, Janecko, & Scott Weese, 2013;Galvão et al., 2015;White et al., 2003). Moreover, the assessment of many owners' feeding practices has shown that snack feeding can lead to the development of canine obesity (Bland et al., 2009;Courcier et al., 2010;Robertson, 2003). ...
... Moreover, the assessment of many owners' feeding practices has shown that snack feeding can lead to the development of canine obesity (Bland et al., 2009;Courcier et al., 2010;Robertson, 2003). The first survey on dog treats was part of a study by Freeman et al. (2013) in which not only the microbiological quality of one treat type (e.g., bully sticks) was tested, but caloric density was also evaluated and owners were asked opinions of this kind of product. Only one recent study (White et al., 2016) specifically investigated the motivations behind dog owner snack-feeding habits in the UK: although most owners did not consider treats to be an integral part of their dog's diet, the majority of the interviewed people stated to feed treats regularly, and a wide range of both positive and negative views were expressed, with some emphasizing the beneficial effects while others fearing the potential weight gain. ...
... Most of the respondents to our questionnaire were women, probably because they are the members of the household who usually handle the dog's diet (Rohlf et al., 2010). A high prevalence of women was also recorded in two other studies focused on dog treats, respectively 87% in that of Freeman et al. (2013) and 72% in that of White et al. (2016). In the latter study, the owners interviewed were recruited personally in outdoor locations and mostly aged 46 to 59 (41%), while in our study most of the people interviewed were from 20 to 30 years old. ...
Article
Commercially available dog treats have become very popular and a common part of the pet’s diet, yet very little is known about peoples’ opinions and feeding habits; therefore, a survey was shared on a popular social network. Most of the self-selected interviewed owners (n = 1833, 83%) use treats regularly, mainly to reward their dog’s behavior or during training-sports activities. Owners usually buy several types of treats, of which biscuits and dental care sticks are the most common, and usually hand out one to five pieces to their dogs every day. Most owners read the labels of the treats to seek the ingredients list and the claimed health benefits; contrarily, many owners look for non-nutritional values, such as flavor (n = 321, 18%), brand (n = 72, 4%) or shape (n = 46, 3%). Seventy-five percent of the owners (n = 1369) follow the feeding instructions provided by the producers on the label. Treat feeding is a common practice among dog owners and there is great variability among regimens (e.g., types and quantities provided). Understanding the owner’s attitudes could help veterinarians educate them to manage treats in the dog’s diet.
... In another study, Weese (2005) found the presence of S. aureus in one of the 25 tested raw foods (4%) at over 10 5 cfu/g. In turn, Freeman et al. (2013) examined 26 bully sticks and found one (4%) methicillin-resistant Staphylococcus aureus (MRSA). ...
... In this study, microbial contamination by Clostridium spp. was not found. However, Freeman et al. (2013) isolated C. difficile in one (4%) of 26 bully sticks. Manufacturers should take steps to reduce the possibility of contamination of products with pathogenic bacteria (Nemser et al. 2014). ...
Article
Full-text available
In addition to properly balancing nutritional value in accordance with the needs of a dog, estimating the microbiological quality of dog food is crucial in providing healthy and safe foods. The aim of this study was to examine the quality of dry food for adult dogs, with particular reference to: (1) evaluating the nutritional value and compliance with nutritional guidelines for dogs, (2) comparing the nutritional value of dog foods, with particular emphasis on the division into cereal and cereal-free foods, and (3) evaluating their microbiological safety. All thirty-six evaluated dry dog foods met the minimum European Pet Food Industry FEDIAF requirement for total protein and fat content. The total aerobic microbial count in the analyzed dry dog foods ranged from 2.7 × 10² to above 3.0 × 10⁷ cfu/g. In five (14%) dog foods the presence of staphylococci was detected; however, coagulase positive Staphylococcus (CPS) was not found. Mold presence was reported in one cereal-free dog food and in six cereal foods. In none of the analyzed foods Enterobacteriaceae were found, including coliforms, Escherichia coli and Salmonella spp. Bacteria of the genus Listeria and Clostridium as well as yeasts were also not detected. In conclusion, the evaluated dry dog foods had varied microbiological quality. The detected number of microorganisms may have some implications for long-term consumption of contaminated food. The lack of European Commission standards regarding the permissible amounts of microorganisms in pet food may result in insufficient quality control of these products.
... The majority of the owners who gave their animals kibble as single or additional component of the diet habitually fed their pet twice a day (48.4%, 700/1446); 22.1% (320/1446) preferred ad libitum feeding, 19.1% (276/1446) administered three meals per day, 5.4% (78/1446) more than three meals per day, and the remaining 5.0% (72/1446) a single daily meal. ...
... This survey provided evidence that the most common diet type used for both dogs and cats was kibble, which was fed either alone or in combination with canned food, and this finding is consistent with the latest official report drafted in Italy [16]. The percentage of owners who chose to feed a homemade diet (27.2%) has increased substantially compared to previous surveys conducted in Western countries [17][18][19][20]. The choice of a raw diet has become markedly popular in recent years, and almost equal numbers of RMBD-feeders and HCD-feeders were found in this study. ...
Article
Full-text available
Background: Pet food storage plays a crucial role in maintaining the nutritional and sensory properties of purchased products over time. Methods: An online survey was developed to collect data regarding owners' storage habits for both commercial and home-made diets. Results: The questionnaire was completed by 1545 dog owners and 676 cat owners. Pet and owner age played roles in the choice of the type of diet (commercial vs. home-cooked vs. raw meat-based) adopted. Kibble feeders (75.7%) usually bought one (50.1%) or two (24.6%) packages at a time, and most pets (64.4%) took a minimum four weeks to consume an entire bag. Almost half of the owners (43.5%) used a container to store pet food (plastic bins for 79.5%). Pet food was commonly stored in the kitchen (45.1%) and not exposed to direct light (94.5%); 23.6% of the kibble feeders said it might be exposed to high temperatures. Most commercial pet food feeders (67.3%) considered preservatives a potential health risk for pets. Among homemade diet feeders, 38.6% stored fish oil at room temperature. Conclusions: Pet owners should be educated in proper food storage management when receiving feeding instructions from veterinarians. More comprehensive information on the nature and importance of additives in pet food should be promoted by manufacturers.
... Incoming veterinary students' behaviors and beliefs toward pet nutrition paralleled those reported among pet owners in the general population. Prior studies have reported that clients consider veterinarians to be their principle and most trustworthy source of information regarding pet nutrition, [26][27][28] which is consistent with our results with incoming veterinary students. In our study, students who were cat owners were more likely to question conflicting information between veterinarians and other sources of information. ...
... Incoming veterinary students in this study and pet owners exhibited very similar information behaviors. Approximately 15%-17% of pet owners use online resources as a primary source of information for obtaining information on pet nutrition 5 , 26 -very similar to the 13% of incoming student veterinarians who use online resources as their primary source of information about pet nutrition. Incoming veterinary students are likely to be exposed to a wide range of companion animal nutrition information, similar to other consumers, some of which may be accurate and verified, and some that may be less accurate or opinion-based. ...
Article
Extant research shows veterinarians face increasing challenges in discussing nutrition with clients despite receiving professional nutrition education in the veterinary medical curriculum. This study's aim was to elicit student veterinarians' baseline nutrition-related perceptions and nutrition information-seeking behaviors at the time of entering veterinary school. Participants were newly enrolled veterinary students at the Ontario Veterinary College (n = 120). Focus group discussions (n = 19) informed the design of an online questionnaire capturing students' demographics and perceptions of their own and their pets' nutrition. Students reported being influenced by individual factors (e.g., time), social networks (e.g., family), and surrounding environment (e.g., cost, contradictory media messages). Overall, 58% of students considered themselves knowledgeable about pet nutrition when commencing veterinary school, with 71% prioritizing their pets' diets as much as their own. Students' confidence in finding pet nutrition information was correlated with perceived accessibility (r = .76, p = .001) and perceived quantity of information available on pet nutrition (r = .83, p = .001), but not quality of information (r = .13, p = .03). In general, students relied on and trusted veterinarians for nutrition advice. However, 94% of students mistrusted pet food companies' motivations. Our data supports that students entering veterinary school have their own perceptions on pet nutrition that impact nutrition education, suggesting this as an important consideration in the design and delivery of a veterinary nutrition curriculum. Veterinary medical faculty should be encouraged to discuss baseline nutrition information and address any misconceptions to prepare students for future consultations with clients.
... Previous studies performed on treats have assessed their microbiological quality with specific regard to the potential risk of bacterial contamination for dogs and human beings rather than evaluating their chemical composition. [3][4][5][6] Moreover, treats are not intended to contribute significantly to the daily ration, but they may be given in quantities that impact total energy intake. Therefore, feeding instructions should provide clear recommendations on how not to overfeed dogs as suggested by FEDIAF Nutritional Guidelines for Complete and Complementary Pet Food for Cats and Dogs. ...
... Most studies conducted on these products assessed whether any bacterial contamination poses risks to consumers and possibly to pet owners. [3][4][5][6] For example, Freeman and others 5 collected 26 bully stick treats for dogs, but beyond microbiological testing, only five were submitted to proximate analysis. Therefore, our study is the first that reports and compares the nutrient composition of different categories of treats. ...
Article
Forty-one dog treats were selected from the market with the aim of providing more insight into supplemental pet food composition. Thirty-two products (four biscuits, nine tender treats, two meat-based strips, ve rawhides, eight chewable sticks, four dental care sticks) were analysed for proximate nutrient composition and quantification of minerals, hydroxyproline (Hyp), starch, glucose, fructose and sucrose. Labelled ingredients were often expressed as non-specific categories. A treat supplied a mean of 332.0±39.2 kcal metabolisable energy (ME)/100 g, and the most energy-dense product was a tender treat (475.0 kcal ME/100 g). Small dogs receive the highest percentage of maintenance energy requirement when producers’ feeding instructions are followed. Treat categories revealed variability in dry matter, crude protein, ash, Hyp and starch. Rawhides showed the highest Hyp content. Simple sugars were identified in most treats, and sucrose was the most prevalent. Results of the study suggest treat labelling should include more information on the ingredients used, and the varying nutrient and caloric density of treats should be considered. Specific attention should be given to the use of treats in dogs with specific ingredient sensitivities or nutrient considerations.
... It has been shown that bacteria of the genus Clostridium can be responsible for the spoilage of vacuum-packed chilled beef, lamb and venison and cooked meat products, chilled dog rolls packed in an oxygen-impermeable plastic casing. In studies to analyze bacterial contamination of bully sticks, 4% were contaminated with Clostridium difficile, while one was found to be infected with methicillin-resistant Staphylococcus aureus (MRSA) and one with a tetracycline resistant Escherichia coli [42,43]. ...
Article
Full-text available
Nowadays, dogs are usually equally treated with other family members. Due to the growing caregivers' awareness, the pet foods industry is changing dynamically. Pet foods are manufactured with a myriad of ingredients. Few authors of scientific papers deal with the topic of foods products' safety for pet animals, assessed from the perspective of their caregivers. Despite the many methods of producing foods of the highest quality, there are still cases of contamination of pet foods and treats. In the case of dried chews for dogs, bacteria of the genus Salmonella are the most common risk. In the case of both dry and wet foods, in addition to many species of bacteria, we often deal with mold fungi and their metabolites, mycotoxins. This article presents selected microbiological risks in dog foods and treats, and analyzes the Rapid Alert System for Food and Feed (RASFF) system (2017-2020) for pathogenic microorganisms in dried dog chews, treats and foods. In this period, pet food-related notifications were registered, which were categorized into different types. Analyzing the RASFF notifications over the period, it has been shown that there are still cases of bacterial contamination of dog foods and treats, while in terms of the overall mycotoxin content, these products may appear safe.
... Approximately 76% of the home-cooked diets were formulated by the owners themselves based on non-veterinarian advice, including Internet resources, a friend or colleague, breeder, and a book, as a primary source of information on pet nutrition. Similar to previous studies (12,15,16,21), more than a quarter of owners in this study used Internet resources as their primary source of home-cooked diet formulation. The findings indicate that, as in previous studies, owners who feed home-cooked or raw diets trust veterinarians less than other resources in determining what to feed their pets (13,16,22). ...
Article
A survey was designed to investigate the prevalence and characteristics of feeding, dietary supplement use, and rehabilitative management use in flyball dogs. The survey was completed by 394 respondents. There were 12.5% (n = 49/392) and 33.4% (n = 131/392) of owners who fed home-cooked and raw diets, respectively, to their dogs. About 77.7% (n = 306/394) and 56.6% (n = 223/394) of owners used dietary supplement and rehabilitative management, respectively, primarily joint supplements (89.8%, n = 275/306) and chiropractic (73.1%, n = 163/223). Owners were more likely to use supplements (P = 0.0002) and rehabilitative management (P = 0.0001) when their dogs were injured. Dogs with more than one reported injury received rehabilitative management (P < 0.0001) and used supplement (P = 0.0006) more often. Key clinical message: There is considerable demand for non-commercial food, supplements, and rehabilitative management among flyball dog owners, underscoring the importance for veterinarians to understand the motivation of dog owners' decisions as well as the risks and benefits of these practices to ensure optimal outcomes for their patients. Copyright and/or publishing rights held by the Canadian Veterinary Medical Association.
... Most of the respondents affirmed relying on information sources other than veterinarians and, according to other surveys [8][9][10], an important percentage of owners consult websites to learn how to feed pets nowadays. This is especially true for owners who do not feed commercial pet food owing to their distrust in the veterinarian's nutritional expertise [8,[11][12][13]. ...
Article
Full-text available
Background The popularity of raw meat-based diets (RMBDs) for pets has been increasing in recent years even if the reputed health benefits are mainly anecdotal. A web-based survey was developed to better understand the motivations and habits of owners who decided to feed their dogs RMBDs. Results The questionnaire was completed by 218 dog owners, 62 of whom were living with people whose immune system was impaired or weakened. Internet was the preferred source of information for more than half of the respondents, and feeding dogs a more natural and healthier diet was the main reason behind owners’ interest in RMBDs. About 80% of the participants completely abandoned commercial pet food and showed marked distrust especially towards the lack of clarity on the ingredients used (n = 169). The vast majority of owners interviewed (94%) believed RMBDs to be absolutely safe for dogs, and shinier coat, muscle mass gain, and cleaner teeth were the principal improvements seen on their pets. Controlling the composition and quality of the ingredients provided to their animals was the main advantage of RMBDs for 57% of the owners, while the main disadvantages were related to the purchase of some components (38%) and the time required (22%) for the preparation of the diet. Only 8% of the respondents relied on veterinarians for RMBD formulation, and a wide variety of feeding regimens and combinations of ingredients was observed. Conclusions As revealed by this study, most owners are unaware of the risks posed by the feeding of RMBDs for both animal and human health, and they often rely on questionable sources for advice on pet nutrition. Owners see RMBDs as a more natural and healthier alternative to commercial pet food even if the actual benefits remain unproven. Consulting veterinarians for proper information and board-certified nutritionists for the formulation of complete and balanced RMBDs should be promoted.
... Pet nutrition has been identified as a possible source of C. difficile, via pet treats (as bully sticks for dogs) and other raw or processed foods (Freeman et al. 2013;Rodriguez-Palacios et al. 2013). In a study conducted in France, C. difficile was not detected in any feline raw foods (n ¼ 20) purchased from 20 Paris stores (Bouttier et al. 2010). ...
Chapter
Zoonoses are infections or diseases that can be transmitted between animals and humans through direct contact, close proximity or the environment. Clostridium difficile is ubiquitous in the environment, and the bacterium is able to colonise the intestinal tract of both animals and humans. Since domestic and food animals frequently test positive for toxigenic C. difficile, even without showing any signs of disease, it seems plausible that C. difficile could be zoonotic. Therefore, animals could play an essential role as carriers of the bacterium. In addition, the presence of the spores in different meats, fish, fruits and vegetables suggests a risk of foodborne transmission. This review summarises the current available data on C. difficile in animals and foods, from when the bacterium was first described up to the present.
... However, it is important to mention that these data were collected prior to the pet food recall of 2007; thus, these percentages may differ if the survey were conducted today. In a study 14 that involved a survey conducted in 2011, 10.8% of 791 pet owners from 44 US states and 6 countries who responded fed a commercial or home-prepared RMBD as a major component of their pet' s diet, and 32.9% fed a homeprepared or commercial RMBD as some component of their pet' s diet. ...
Article
Treats are commonly fed by most dog caregivers and can constitute a significant proportion of a dog's diet, potentially contributing to obesity. Feeding aspects related to treats specifically, remain underexplored. An e-survey was voluntarily completed by 716 dog caregivers predominantly from Canada and the USA to identify and describe caregivers' perceptions, motivations, and behaviours surrounding treats, and factors that influence decisions about feeding treats. Survey responses were analyzed using descriptive statistics, chi-square tests, Kruskal-Wallis one-way ANOVA, and Wilcoxon signed-rank tests. Multivariable logistic regression analyses were performed to analyze (1) measurement methods associated with monitoring treat intake, and (2) frequency of feeding different types of treats with perceiving dog as overweight/obese. Most caregivers considered the term 'treat' in a nutritional context, but respondents expressed mixed perceptions of how they consider treats in relation to their dog's primary diet. Alongside training and sports activities, aspects relating to the human-animal bond were highly reported to influence decisions surrounding treats. Most respondents were motivated to provide treats because it makes their pet happy, and to strengthen the bond with their dog, and nearly 40% of caregivers frequently feed treats to show love to their dog. Human food and table scraps were frequently fed by 30-40% of caregivers and feeding human food weekly was predictive of caregivers perceiving their dog to be overweight/obese (OR=2.24, p = 0.007). Caregivers estimated treats to account for a median of 15% of their dog's total diet, based on estimated quantity. Caregivers who reported using a measuring cup/scoop to measure their dog's treats were more likely to monitor their dog's treat intake (OR=3.38, p = 0.002). Most caregivers monitor their dog's body condition (60%) or consider their dog's recent activity level (43%) to decide on the amount of treats to feed; only 22% of caregivers reported veterinary advice to support their decisions on the amount of treats to feed. Findings from this research offer new insights to dog caregiver feeding habits and their perceptions of treats in relation to the canine diet. These results can be used to inform veterinary counselling strategies and caregiver education initiatives to promote animal health and well-being.
Article
The purpose of this study was to use routine morphologic-based staining techniques to examine the histology of commercially labeled rawhide and rawhide-free dog chew products and compare the results to the product labeling. Ten dog chew products were examined by light microscopy using hematoxylin and eosin and Masson’s trichrome stains. The products were labeled by the manufacturer as rawhide, beef hide, beef chew/rawhide free, and rawhide free. Four of the products were composed of two separate materials, a main chew roll and a second substance (filler) which was coated on or between the layers of the main chew roll. These materials were processed independently. Microscopically, a variety of tissues and materials were identified including collagen, skeletal muscle, fat, plant material, and starch. The products and their fillers were separated into four distinct groups based on microscopic appearance. The components identified in eight of the products appeared consistent with the product labeling. Two products labeled as rawhide free appeared similar to the dermis and this was inconsistent with product labeling. Masson’s trichrome stain was not helpful in distinguishing tissue types in the tested products and this may have been due to the heat processing the products underwent during manufacturing. Bacteria and/or fungi were identified by microscopy in the H&E stained sections in four rawhide-free products.
Preprint
Full-text available
Clostridioides difficile (CD) is a spore-forming bacterium that causes life-threatening intestinal infections in humans. Although formerly regarded as exclusively nosocomial, there is increasing genomic evidence that person-to-person transmission accounts for only <25% of cases, supporting the culture-based hypothesis that foods may be routine sources of CD-spore ingestion in humans. To synthesize the evidence on the risk of CD exposure via foods, we conducted a systematic review and meta-analysis of studies reporting the culture prevalence of CD in foods between January 1981 and November 2019. Meta-analyses, risk-ratio estimates, and meta-regression were used to estimate weighed-prevalence across studies and food types to identify laboratory and geographical sources of heterogeneity. In total, 21,886 food samples were tested for CD between 1981 and 2019 (232 food-sample-sets; 79 studies; 25 countries). Culture methodology, sample size and type, region, and latitude were significant sources of heterogeneity (p<0.05). Although non-strictly-anaerobic methods were reported in some studies, and we confirmed experimentally that improper anaerobiosis of media/sample-handling affects CD recovery in agar (Fisher, p<0.01), most studies (>72%) employed the same (one-of-six) culture strategy. Because the prevalence was also meta-analytically similar across six culture strategies reported, all studies were integrated using three meta-analytical methods. At the study level (n=79), the four-decade global cumulative-prevalence of CD in the human diet was 4.1% (95%CI=-3.71, 11.91). At the food-set level (n=232), the weighted prevalence ranged between 4.5% (95%CI=3-6%; all studies) and 8% (95%CI=7-8%; only CD-positive-studies). Risk-ratio ranking and meta-regression showed that milk was the least likely source of CD, while seafood, leafy green vegetables, pork, and poultry carried higher risks (p<0.05). Across regions, the risk of CD in foods for foodborne exposure reproducibly decreased with Earth latitude (p<0.001). In conclusion, CD in the human diet is a global nonrandom-source of foodborne exposure that occurs independently of laboratory culture methods, across regions, and at variable level depending on food type and latitude. The latitudinal trend (high CD-food-prevalence towards tropic) is inverse to the epidemiological observations of CD-infections (frequent in temperate regions). Findings suggests the plausible hypothesis that ecologically-richer microbiomes in the tropic might protect against intestinal CD colonization/infections despite CD ingestion.
Article
Full-text available
Background The practice of feeding of diets containing raw animal products (RAP) to pets (dogs and cats) is discouraged by veterinary organizations and governmental public health organizations. Nevertheless, the practice of feeding RAP to pets is increasing in popularity. Pet owner motivations for feeding RAP diets to pets have not been explored and the benefits of RAP diets remain largely anecdotal. We hypothesized that pet owners feeding RAP diets would not rely on veterinary advice in choosing their pet’s diet. We also hypothesized that these owners would have lower levels of trust in veterinary advice with respect to nutrition relative to pet owners not feeding RAP. Methods An anonymous web-based survey was developed to identify pet owner motivations for feeding RAP diets, and to characterize the veterinarian-client relationships of individuals feeding RAP diets. Results There were 2,337 respondents and 2,171 completed surveys. Of survey respondents, 804 reported feeding RAP at the time of the survey. While 20% of pet owners feeding RAP relied on online resources to determine what or how much RAP to feed, only 9% reported consulting with a veterinarian in making decisions about feeding RAP. Pet owners feeding RAP reported lower levels of trust in veterinary advice both ‘in general’ and ‘with respect to nutrition’ than pet owners not feeding RAP. Most pet owners reported that a discussion regarding their pet’s nutrition does not occur at every veterinary appointment. Discussion Pet owners feeding a RAP diet have lower trust in veterinary advice than pet owners not feeding a RAP diet. Owners feeding RAP are more reliant on online resources than their own veterinarian in deciding what and how much RAP to feed. Pet owners perceive that nutrition is not discussed at most veterinary appointments. Therefore, there is room for improvement in the veterinarian-client communication with regards to nutrition.
Article
Objectives: To evaluate owner experiences and adherence to home-cooked diet recipes for dogs. Methods: Clients of a veterinary teaching hospital clinical nutrition service who had a home-cooked diet recipe formulated for their dogs between March 2011 and December 2013 were given a survey by email, postal mail and telephone. Survey questions addressed motivations, positive and negative aspects of feeding home-cooked diets and current feeding practices. Responses were compared to animals' medical records to determine adherence. Results: Of the 93 owners who were contacted, 53 (57%) completed the survey. Of the 53 respondents, 43 owners (81%) reported that they were still feeding an home-cooked diet or had fed an home-cooked diet until the time of their dogs' deaths. The most common motivation for feeding a home-cooked diet was suitability for specific medical needs. Of the 30 surveys that included a complete diet history, only four (13%) demonstrated exact adherence to home-cooked diet recipes. Clinical significance: Most respondents liked and continued to feed a home-cooked diet, but few owners adhered to prescribed recipes and many dogs required recipe modifications. It is important to counsel dog owners about benefits and drawbacks of feeding home-cooked diets, importance of recipe adherence and necessity for follow-up after diet formulation with a board-certified veterinary nutritionist.
Article
Full-text available
Recent studies have identified Clostridium difficile in food animals and retail meat, and concern has been raised about the potential for food to act as a source of C. difficile infection in humans. Previous studies of retail meat have relied on enrichment culture alone, thereby preventing any assessment of the level of contamination in meat. This study evaluated the prevalence of C. difficile contamination of retail ground beef and ground pork in Canada. Ground beef and ground pork were purchased from retail outlets in four Canadian provinces. Quantitative and enrichment culture was performed. Clostridium difficile was isolated from 28/230 (12%) samples overall: 14/115 (12%) ground beef samples and 14/115 (12%) ground pork samples (P = 1.0). For ground beef, 10/14 samples (71%) were positive by enrichment culture only. Of the 4 ground beef samples that were positive by direct culture, 20 spores/g were present in 2 while 120 and 240 spores/g were present in 1 each. For ground pork, 10/14 (71%) samples were positive by enrichment culture only. Of the 4 ground pork samples that were positive by direct culture, 20 spores/g were present in 3 while 60 spores/g were present in 1. Ribotype 078 predominated, consistent with some previous studies of C. difficile in food animals. Ribotype 027/North American pulsotype 1 was also identified in both retail beef and pork. This study has identified relatively common contamination of retail ground beef and pork with C. difficile spores; however, the levels of contamination were very low.
Article
Full-text available
Three hundred and twenty isolates of Staphylococcus aureus were typed by DNA sequence analysis of the X region of the protein A gene (spa). spa typing was compared to both phenotypic and molecular techniques for the ability to differentiate and categorize S. aureus strains into groups that correlate with epidemiological information. Two previously characterized study populations were examined. A collection of 59 isolates (F. C. Tenover, R. Arbeit, G. Archer, J. Biddle, S. Byrne, R. Goering, G. Hancock, G. A. Hébert, B. Hill, R. Hollis, W. R. Jarvis, B. Kreiswirth, W. Eisner, J. Maslow, L. K. McDougal, J. M. Miller, M. Mulligan, and M. A. Pfaller, J. Clin. Microbiol. 32:407-415, 1994) from the Centers for Disease Control and Prevention (CDC) was used to test for the ability to discriminate outbreak from epidemiologically unrelated strains. A separate collection of 261 isolates form a multicenter study (R. B. Roberts, A. de Lencastre, W. Eisner, E. P. Severina, B. Shopsin, B. N. Kreiswirth, and A. Tomasz, J. Infect. Dis. 178:164-171, 1998) of methicillin-resistant S. aureus in New York City (NYC) was used to compare the ability of spa typing to group strains along clonal lines to that of the combination of pulsed-field gel electrophoresis and Southern hybridization. In the 320 isolates studied, spa typing identified 24 distinct repeat types and 33 different strain types. spa typing distinguished 27 of 29 related strains and did not provide a unique fingerprint for 4 unrelated strains from the four outbreaks of the CDC collection. In the NYC collection, spa typing provided a clonal assignment for 185 of 195 strains within the five major groups previously described. spa sequencing appears to be a highly effective rapid typing tool for S. aureus that, despite some expense of specificity, has significant advantages in terms of speed, ease of use, ease of interpretation, and standardization among laboratories.
Article
Full-text available
In the summer of 1999, the incidence of Salmonella enterica serotype Infantis infections in Alberta rose dramatically. Subsequent laboratory and epidemiological investigations established that an outbreak of human disease caused by this organism was occurring across Canada and was associated with pet treats for dogs produced from processed pig ears. Laboratory investigations using phage typing and pulsed-field gel electrophoresis (PFGE) established that isolates of Salmonella serotype Infantis from pig ear pet treats and humans exposed to pig ear pet treats comprised a well-defined subset of all isolates analyzed. Of the 53 subtypes of Salmonella serotype Infantis obtained around the time of the outbreak as defined by PFGE and phage typing, only 6 subtypes were associated with both human infection and isolation from pig ears. Together with information from epidemiological studies, these investigations established pig ear pet treats as the cause of the Salmonella serotype Infantis outbreak. The results are consistent with a model in which contaminated pig ear pet treats constitute a long-term, continuing vehicle for infection of the human population rather than causing temporally delimited point-source outbreaks. During the course of this outbreak, several other Salmonella serotypes were also isolated from pet treats, suggesting these products may be an important source of enteric infection in both humans and dogs. Though isolates of Salmonella serotypes other than Salmonella serotype Infantis from pet treats were also subjected to PFGE and phage typing, no link with human disease could be definitively established, and the contribution of pig ear pet treats to human disease remains unclear. Elimination of bacterial contamination from pet treats is required to reduce the risk of infection from these products.
Article
Full-text available
The objectives of this study were to determine the potential risk of dog treats in transmitting Salmonella to humans in the USA, and to characterize genetic relatedness and antimicrobial resistance among the isolates. A total of 158 dog treats derived from pig ears and other animal parts were randomly collected nationwide and assayed for the presence of Salmonella. The Salmonella isolates were characterized using serotyping, pulsed-field gel electrophoresis (PFGE) and antimicrobial susceptibility testing. Forty-one percent (65/158) of samples were positive for Salmonella. Eighty-four Salmonella isolates, comprising 24 serotypes, were recovered from the 65 positive samples. Fourteen samples were contaminated with more than one Salmonella serotype. PFGE analysis of 78 Salmonella isolates yielded 64 patterns. S. Infantis with PFGE patterns indistinguishable from those of strains identified in Canadian outbreaks in 1999 were recovered in several dog treat products. The majority of Salmonella isolates were susceptible to the antimicrobials tested; however, resistance was observed to tetracycline (26%), streptomycin (23%), sulfamethoxazole (19%), chloramphenicol (8%) and ampicillin (8%). Twenty-eight (36%) Salmonella isolates were resistant to at least one antimicrobial and 10 (13%) isolates displayed resistance to four or more antimicrobials. Two isolates were identified as S. Typhimurium DT104 with the characteristic penta-resistance phenotype (ampicillin, chloramphenicol, streptomycin, sulfamethoxazole and tetracycline). One S. Brandenburg isolate was resistant to eight antimicrobials. Seven Salmonella isolates also contained class I integrons encoding resistance genes to aminoglycosides, beta-lactam and streptothricin antimicrobials. The study indicates that animal-derived dog treats in the USA could be a potential source of animal and human infections with Salmonella, including multidrug-resistant Salmonella strains.
Article
Full-text available
Resistance to the extended-spectrum cephalosporins can occur in Salmonella species via the production of extended-spectrum and AmpC β-lactamases. We describe human infections with Salmonella enterica serotype Newport phage type 14 strains resistant to ceftazidime (CAZ) and cefoxitin (FOX) related to the handling of pet treats containing dried beef. These strains were isolated from five patients in Calgary, Alberta, Canada, during 2002 and were compared to a strain cultured from a commercial pet treat present at the property of one of the patients. The strains were resistant to FOX, CAZ, cefpodoxime, ampicillin, and chloramphenicol; intermediate resistant to ceftriaxone and cefotaxime; and sensitive to the aminoglycosides, ciprofloxacin, cefepime, and imipenem. Isoelectric focusing, multiplex PCR, and sequencing of the amplicons showed that all strains produced the plasmid-encoded AmpC β-lactamase, CMY-2. Restriction analysis of plasmid DNA following transformation demonstrated that blaCMY-2 was encoded on an approximately 140-kb plasmid. Pulsed-field gel electrophoresis showed the human and pet treat Salmonella strains to be highly related. This study is the first to implicate the transfer of multidrug-resistant Salmonella species through the handling of commercial pet treats containing animal products. In addition to documenting the first cases of human infection caused by CMY-2-producing S. enterica serotype Newport strains in Canada, this study illustrates the necessity of rapid and accurate laboratory-based surveillance in the identification of novel types of antimicrobial resistance.
Article
Full-text available
A multiplex PCR toxigenic culture approach was designed for simultaneous identification and toxigenic type characterization of Clostridium difficile isolates. Three pairs of primers were designed for the amplification of (i) a species-specific internal fragment of the tpi (triose phosphate isomerase) gene, (ii) an internal fragment of the tcdB (toxin B) gene, and (iii) an internal fragment of the tcdA (toxin A) gene allowing distinction between toxin A-positive, toxin B-positive (A+B+) strains and toxin A-negative, toxin B-positive (A−B+) variant strains. The reliability of the multiplex PCR was established by using a panel of 72 C. difficile strains including A+B+, A−B−, and A−B+ toxigenic types and 11 other Clostridium species type strains. The multiplex PCR assay was then included in a toxigenic culture approach for the detection, identification, and toxigenic type characterization of C. difficile in 1,343 consecutive human and animal stool samples. Overall, 111 (15.4%) of 721 human samples were positive for C. difficile; 67 (60.4%) of these samples contained A+B+ toxigenic isolates, and none of them contained A−B+ variant strains. Fifty (8%) of 622 animal samples contained C. difficile strains, which were toxigenic in 27 (54%) cases, including 1 A−B+ variant isolate. Eighty of the 721 human stool samples (37 positive and 43 negative for C. difficile culture) were comparatively tested by Premier Toxins A&B (Meridian Bioscience) and Triage C. difficile Panel (Biosite) immunoassays, the results of which were found concordant with toxigenic culture for 82.5 and 92.5% of the samples, respectively. The multiplex PCR toxigenic culture scheme described here allows combined diagnosis and toxigenic type characterization for human and animal C. difficile intestinal infections.
Article
Full-text available
A total of 184 methicillin-resistant Staphylococcus aureus (MRSA) strains were collected from patients who sought treatment primarily for skin and soft tissue infections from January 1, 1999, to March 31, 2002, in east-central Saskatchewan, Canada. Molecular subtyping analysis using pulsed-field gel electrophoresis showed 2 major clusters. Cluster A (n = 55) was composed of a multidrug-resistant MRSA strain associated with a long-term care facility and was similar to the previously reported nosocomial Canadian epidemic strain labeled CMRSA-2. Cluster B (n = 125) was associated with cases identified at community health centers and was indistinguishable from a community-associated (CA)-MRSA strain identified previously in the United States (USA400). Cluster B remained susceptible to a number of classes of antimicrobial agents and harbored the lukF-PV and lukS-PV toxin genes. Over 50% of both clonal groups displayed high-level resistance to mupirocin. This is the first report of the USA400 strain harboring the lukF-PV and lukS-PV toxin genes in Canada.
Article
Full-text available
Clostridium difficile was isolated from 12 (20%) of 60 retail ground meat samples purchased over a 10-month period in 2005 in Canada. Eleven isolates were toxigenic, and 8 (67%) were classified as toxinotype III. The human health implications of this finding are unclear, but with the virulence of toxinotype III strains further studies are required.
Article
Three hundred and twenty isolates of Staphylococcus aureus were typed by DNA sequence analysis of the X region of the protein A gene (spa), spa typing was compared to both phenotypic and molecular techniques for the ability to differentiate and categorize S. aureus strains into groups that correlate with epidemiological information. Two previously characterized study populations mere examined, A collection of 59 isolates (F, C. Tenover, R, Arbeit, G. Archer, J. Piddle, S, Byrne, R, Goering, G. Hancock, G. A. Hebert, B, Hill, R. Hollis, W, R. Jarvis, B, Kreiswirth, W, Eisner, J. Maslow, L, K, McDougal, J, M. Miller, M, Mulligan, and M. A. Pfaller, J. Clin, Microbiol. 32:407-415, 1994) from the Centers fbr Disease Control and Prevention (CDC) was used to test for the ability to discriminate outbreak from epidemiologically unrelated strains. A separate collection of 261 isolates form a multicenter study (R, B. Roberts, A. de Lencastre, W, Eisner, E, P, Severina, B. Shopsin, B, N. Kreiswirth, and A. Tomasz, J. Infect. Dis. 178:164-171, 1998) of methicillin-resistant S. aureus in New York City (NYC) was used to compare the ability of spa typing to group strains along clonal lines to that of the combination of pulsed-field gel electrophoresis and Southern hybridization. In the 320 isolates studied, spa typing identified 24 distinct repeat types and 33 different strain types. spa typing distinguished 27 of 29 related strains and did not provide a unique fingerprint for 4 unrelated strains from the four outbreaks of the CDC collection. In the NYC collection, spa typing provided a clonal assignment for 185 of 195 strains within the five major groups previously described. spa sequencing appears to be a highly effective rapid typing tool for S. aureus that, despite some expense of specificity, has significant advantages in terms of speed, ease of use, ease of interpretation, and standardization among laboratories.
Article
In Canada, there have been reported outbreaks of human salmonellosis related to exposure to animal-derived pet treats, involving pig ear treats, beef steak patty dog treats and pet treats of seafood origin. As a follow-up to recommendations made to the pig ear treat industry in 1999, a total of 245 pig ear treats were purchased in two Canadian cities to provide evidence of adoption of the recommendations and to determine the current levels of Salmonella contamination of pig ear treats available at pet stores. An overall prevalence of 4% was observed, with isolates exhibiting resistance to up to seven anti-microbials. Serotypes recovered included S. Bovismorbificans, S. Give, S. Derby and S. Typhimurium var. Copenhagen. Although the prevalence observed during this study is lower than the prevalence observed in 1999, pig ear treats should still be considered as a possible source of Salmonella and anti-microbial resistant bacteria to humans and dogs in Canada.
Article
Recent reports indicate that a large proportion of community-acquired Clostridium difficile infections (CA-CDI) are not linked to recent antibiotic therapy, older age, significant comorbidity or previous hospitalization. Possible community sources for CA-CDI include animals and food, and therefore a surveillance study on the prevalence of C. difficile in meat was performed. Samples of different meat species were collected from the retail trade and analyzed for the presence of C. difficile using a method that included selective enrichment in C. difficile broth, subsequent alcohol shock-treatment and plating onto C. difficile selective medium. C. difficile isolates were tested for the presence of toxin genes and were typed using PCR ribotyping. Of 500 samples tested, 8 (1.6%) were positive for the presence of C. difficile: 1 from lamb (6.3%) and 7 from chicken meat (2.7%). The isolated strains belonged to PCR ribotypes different from those that are currently most frequently found in patients with CDI in the Netherlands, except for C. difficile PCR ribotype 001 which was found in one chicken meat sample. This observation suggests that other matrices than meat may serve as a source for CA-CDI.
Article
The objective of the study was to determine the prevalence of methicillin-resistant Staphylococcus aureus (MRSA) contamination of retail meat and to determine the level of contamination. Pork (pork chops and ground pork), ground beef and chicken (legs, wings and thighs) were purchased at retail outlets in four Canadian provinces and tested for the presence of methicillin-resistant Staph. aureus using qualitative and quantitative methods. MRSA was isolated from 9.6% of pork, 5.6% of beef and 1.2% of chicken samples (P = 0.0002). Low levels of MRSA were typically present, with 37% below the detection threshold for quantification and <100 CFU g(-1) present in most quantifiable samples. All isolates were classified as Canadian epidemic MRSA-2 (CMRSA-2) by pulsed field gel electrophoresis (PFGE), with two different PFGE subtypes, and were spa type 24/t242. MRSA contamination of retail meat is not uncommon. While CMRSA-2, a human epidemic clone, has been found in pigs in Canada, the lack of isolation of livestock-associated ST398 was surprising. The relevance of MRSA contamination of meat is unclear but investigation is required because of the potential for exposure from food handling. Sources of contamination require investigation because these results suggest that human or animal sources could be involved.
Article
Recently the isolation of methicillin-resistant Staphylococcus aureus (MRSA) strains from several food-producing animals has been reported. During slaughtering of MRSA-positive animals, contamination of carcasses with MRSA may occur and consequently the meat of these animals may get contaminated. The aim of this study was to estimate the prevalence of MRSA in raw meat samples from the retail trade. Samples of raw beef, pork, veal, lamb/mutton, chicken, turkey, fowl and game were collected from the retail trade. A detection method including a two-step enrichment in Mueller-Hinton broth+6.5% NaCl and phenol red mannitol broth containing ceftizoxime and aztreonam, followed by isolation on MRSA ID agar (bioMérieux) was evaluated and subsequently applied for the detection of MRSA in samples of raw meats. MRSA strains were isolated from 264 (11.9%) of 2217 samples analyzed. Isolation percentages for the meat species were: beef (10.6%), veal (15.2%), lamb and mutton (6.2%), pork (10.7%), chicken (16.0%), turkey (35.3%), fowl (3.4%) and game (2.2%). The majority (85%) of the isolated strains belonged to spa-types of pulsed-field gel electrophoresis (PFGE) non-typeable (NT)-MRSA, corresponding to the multilocus sequence type ST398, a type also recently isolated in the Netherlands from pigs. However, a smaller part of these strains were found to be of other ST's, possibly of human origin. Further studies are needed to elucidate transmission routes of MRSA in relation to meat and other foods and to provide the tools for preventing the spread of MRSA. At present the high prevalence of MRSA in meat has not been shown to contribute significantly to the dissemination of MRSA to humans and the possible health hazard for consumers of the presence of MRSA in foods should be further elucidated.
Article
Toxigenic strains of Clostridium difficile have been reported to produce both toxins A and B nearly always, and nontoxigenic strains have been reported to produce neither of these toxins. Recent studies indicate that it is not always true. We established a PCR assay to differentiate toxin A-negative, toxin B-positive (toxin A-, toxin B+) strains from both toxin-positive (toxin A+, toxin B+) strains and both toxin-negative (toxin A-, toxin B-) strains as an alternative to cell culture assay and enzyme-linked immunosorbent assay (ELISA). By using the PCR primer set NK11 and NK9 derived from the repeating sequences of the toxin A gene, a shorter segment (ca. 700 bp) was amplified from toxin A-, toxin B+ strains compared to the size of the segment amplified from toxin A+, toxin B+ strains (ca. 1,200 bp), and no product was amplified from toxin A-, toxin B-strains. We examined a total of 421 C. difficile isolates by PCR. Of these, 48 strains showed a shorter segment by the PCR, were negative by ELISAs for the detection of toxin A, and were positive by cell culture assay. Although the cytotoxin produced by the toxin A-, toxin B+ strains was neutralized by anti-toxin B serum, the appearance of the cytotoxic effects on Vero cell monolayers was distinguishable from that of toxin A+, toxin B+ strains. By immunoblotting, the 44 toxin A-, toxin B+ strains were typed to serogroup F and the remaining four strains were serogroup X. Pulsed-field gel electrophoresis separated the 48 strains into 19 types. The PCR assay for the detection of the repeating sequences combined with PCR amplification of the nonrepeating sequences of either the toxin A or the toxin B gene is indicated to be useful for differentiating toxin A-, toxin B+ strains from toxin A+, toxin B+ and toxin A-, toxin B- strains and will contribute to elucidation of the precise role of toxin A-, toxin B+ strains in intestinal diseases.
Article
PCR-ribotying, a typing method based on polymorphism in the 16S-23S intergenic spacer region, has been recently used to investigate outbreaks due to Clostridium difficile. However, this method generates bands of high and close molecular masses which are difficult to separate on agarose gel electrophoresis. To improve reading of banding patterns of PCR-ribotyping applied to C. difficile, a partial sequencing of the rRNA genes (16S and 23S) and intergenic spacer region has been performed, then a new set of primers located closer to the intergenic spacer region has been defined. The new PCR gave reproducible patterns of bands easy to separate on agarose gel electrophoresis. Each of the 10 serogroups and 11 subgroups of serogroup A produced a different pattern. This typing method has evidenced major qualities such as easiness, rapidity and reproducibility. However, its discriminatory power has to be evaluated to validate its importance as a typing tool for C. difficile.
Article
In addition to the two large clostridial cytotoxins (TcdA and TcdB) certain strains of Clostridium difficile produce an actin-specific ADP-ribosyltransferase, or binary toxin. PCR reactions were developed to detect genes encoding the enzymatic (cdtA) and binding (cdtB) components of the binary toxin and 170 representative strains were tested to assess the prevalence of the toxin. Positive PCR results (n=59) were confirmed by immunoblotting and ADP-ribosyltransferase assay. PCR ribotype and toxinotype (restriction fragment length polymorphism analysis of genes for TcdA and TcdB) correlated with possession of binary toxin genes. All strains with cdtA and cdtB belonged to toxin-variable toxinotypes and five toxin-producing groups of strains have been described according to the presence or absence of TcdA, TcdB and binary toxin. Result indicate that ca. 6.4% of toxigenic isolates of C. difficile referred to the Anaerobe Reference Unit from UK hospitals have cdtA and cdtB genes.
Article
Methicillin-resistant Staphylococcus aureus (MRSA) is a highly pathogenic multiple-drug resistant (MDR) microorganism that has recently become more prevalent in the community. It has been found that MRSA strains can also contain genes that encode the panton valentine leukocidin toxin (PVL). The PVL toxin has been shown to be responsible for many of the severe clinical symptoms of infection with MRSA, such as furunculosis, severe necrotizing pneumonia, and necrotic lesions of the skin and soft tissues. The aim of this study was to determine the presence of the S. aureus PVL toxin genes (lukS-PV and lukF-PV) in MRSA strains isolated from companion animals. Eleven MRSA isolates, from a total of 23 tested, were shown to possess the mecA gene and the PVL toxin genes. Pulsed-field gel electrophoresis showed that the 11 PVL toxin positive MRSA strains were highly clonal.
Article
Clostridium difficile has received much attention in recent years because of the increased incidence and severity of nosocomial disease caused by this organism, but C. difficile-associated disease has also been reported in the community, and C. difficile is an emerging pathogen in animals. Early typing comparisons did not identify animals as an important source for human infection, but recent reports have shown a marked overlap between isolates from calves and humans, including two of the predominant outbreak types, 027 and 017. C. difficile has also been found in retail meat samples, suggesting that food could be involved in the transmission of C. difficile from animals to humans.
Canadian Integrated Program for Antimicrobial Resistance Surveillance (CIPARS) -Preliminary Report. Public Health Agency of Canada
  • Canada Government Of
Government of Canada, 2009. Canadian Integrated Program for Antimicrobial Resistance Surveillance (CIPARS) -Preliminary Report. Public Health Agency of Canada, Guelph, Ontario.
Food and Drug Administration
Food and Drug Administration, 2010. National Antimicrobial Resistance Monitoring System -Enteric Bacteria (NARMS): 2007