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Survey evaluation of dog owners’ feeding habits in a household setting and comparison of FDA hygiene protocols on dog bowl bacterial contamination as evaluated by total aerobic cell counts

In-home pet food handling and food dish hygiene practices can have adverse health impacts for both humans and pets. Safe food and dish handling guidelines are not easily evidenced for pet owners. The study was designed to investigate dog owners’ feeding habits and evaluate the impact of the Food and Drug Association (FDA) hygiene protocols on dog food dish contamination. Procedures and surveys were approved by NCSU-IACUC and -IRB. Pet feeding and food dish hygiene data were collected from 417 dog owner surveys and 68 food dish swabs. Total aerobic cell counts (TAC) were performed on 68 dishes and randomly assigned into Group A (FDA pet food handling and dish hygiene guidelines), Group B (FDA pet and human food handling and dish hygiene guidelines), or Group C (no guidelines). Hygiene protocols were instituted in-home for 1 week, followed by a second TAC and follow-up survey. Survey from dog owners-households indicated: 4.7% were aware of FDA pet food handling and dish hygiene guidelines; 36% have individuals ≤ 13 years old and/or immunocompromised; 43% store dog food 0-5 feet from human food; 34% wash their hands after feeding; and 33% prepare their dog food on human food preparation surfaces. The hygiene protocols followed by Groups A and B resulted in significant decreases in food dish TAC (P<0.001; 1.40; p=0.026; 0.604, respectively), as compared to Group C (p=0.373). Hot water (>160F) washing decreased TAC (p=0.005) over cold/lukewarm water. In the follow-up survey, 8% of Group A and B respondents reported likely to adhere to protocols long-term. This study suggests a need for pet food handling and dish hygiene guideline education to minimize bacterial contamination of dishes, especially in high-risk households.


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The Centers for Disease Control and Prevention (CDC) One Health initiative, which highlights the interconnection 49 between humans, animals and the environment, has been a prevalent focus in the scientific and lay literature of late.

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The aim of One Health is ultimately to achieve optimal health outcomes for all involved in these interactions (1).

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Food safety-related concerns are one aspect of One Health that span contamination of human and animal foodstuffs 52 as well as equipment and environment hygiene practices involved in food handling. Certainly, human food safety is 53 paramount to human wellness; correspondingly, emphasis on benefits of enhancing the human-animal bond invites 3 54 One Health concerns for pet food safety. The actual act of feeding a pet generally entails interplay between the pet, 55 the owner, and the food. This interaction creates the opportunity for mutual exchange of microbial contaminants 56 from food or water, dishes, and the food storage or preparation environment, which can cause health consequences 57 for both humans and pets. making it one of the second most contaminated sites of those sampled, ranking higher than surfaces commonly 67 considered to have high bacterial loads such as the toilet(4). More recently, a 2012 study also examining total 68 aerobic counts on household surfaces showed that pet water dishes had the third highest bacterial counts out of 26 69 surfaces studied. When categorized into areas of the household, the category of pet-related items (which comprised 70 the water dish and a pet toy) had the highest bacterial counts(5). These studies corroborate the concern of dog dishes 71 being a potential source of microbial contamination in a household setting.

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Despite the concern for contamination, few guidelines for pet dish hygiene exist and those guidelines are not easily 74 accessed or widely distributed. The Food and Drug Administration (FDA) has pet dish cleaning recommendations 75 available via their website in combination with general pet food handling guidelines(6), but in comparison to their 76 guidelines for human dishes in the FDA Food Code 2017(7), the pet information is sparse and vague. In addition, no 77 studies examining the effects of the FDA's recommendations on pet dish hygiene were found by the authors.

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Therefore, the goals of the study were to assess: dog owner's awareness of FDA pet food handling and feeding dish 79 hygiene guidelines; pet food and dish handling habits of pet owners; and evaluate the degree of dog bowl bacterial 80 contamination before and after the institution of the FDA pet food guidelines and FDA Food Code guidelines.    The impact of following specific food handling and food bowl hygiene protocols on food bowl contamination risk 100 was evaluated using a subset of the survey participants. From the survey participants, owners of 68 dogs (a total of 101 50 owners) were invited to complete a food bowl bacterial contamination study. To minimize bias, prior to survey 102 distribution to these 50 dog owners, a baseline food bowl swab was obtained, then owners were asked to complete 103 the Qualtrics survey. Participants were then randomly assigned to three treatment groups. Treatment group A 104 (n=27) were instructed to follow the FDA's Tips for Safe Handling of Pet Food and Treats(6) (last update 7/9/2019 105 at the time of study). Specifically, they were requested to: wash their hands before and after handling pet food, to not 106 use their dog food bowl as a food scooping utensil, wash the bowl and scooping utensils with soap and hot water 107 after each use, discard uneaten food in a designated manner and store dry pet food in its original bag. Treatment 5 108 group B (n=30) were given the FDA's Tips for Safe Handling of Pet Food and Treats and more stringent 109 instructions extrapolated from the FDA's Food Code 2017(7) to specify that handwashing should be at least 20 110 seconds and with warm water and soap, food dishes should be scraped of food prior to washing, that dishwashing 111 should be with water >160° F and soap for at least 30 seconds and dried thoroughly with a clean towel or put 112 through an NSF-certified dishwasher for a wash and dry cycle. Treatment group C (n=11) were given no specific

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A minority, less than 5%, of respondents were aware of the existence of FDA pet food handling guidelines.

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However, when asked where they expected to find this information, 8% replied the FDA, 41% the food label, 28% 153 their veterinarian, 11% the store of purchase, 6% the USDA and 6% various websites. Table 1 summarizes the dog 154 owner compliance in our study. Higher levels of compliance (>75%) were found for: inspecting packaging for 155 visible damage, avoiding use of the food bowl as a scooping utensil, tightly covering leftover pet food, discarding 156 food in a way a pet cannot access, and avoiding raw food. Lower levels of compliance (>25%) were found for: 157 washing hands as recommended prior to handling pet food, washing the food dish as recommended after each use, 158 and washing the food scoop as recommended after each use.

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The majority of respondents (22%) reported washing their dish, on average once weekly. However, there was a wide 167 distribution of responses with 12% washing their dish at least once daily to 18% reporting they wash their dish either 168 less than every 3 months or not at all.

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When respondents did wash their bowl, it was most often with soap and warm water (defined as 100-159°F, 36%) 171 followed by the dishwasher (33%), soap with hot water (>160°F, 17%), rinsing with water only (6%), soap with cool 172 water (5%) with the remainder (<3%) reporting undefined average protocols. Most reported allowing their dish to air 173 dry (44%), followed by hand-drying with a towel (32%), heated dry in a dishwasher (22%) and a smaller percentage 174 used a non-heated dry in a dishwasher (<3%). When washing their pet food bowl, 43% washed the food dish in a 175 sink/dishwasher alongside human dishes, 49% washed in the same sink/dishwasher used for human dishes but at a 176 separate time, and 8% reported washing it in a different sink/dishwasher than used for human dishes (

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Respondents were asked about the percentages of the food type placed in their dog bowl during an average 24-hour 189 period (Fig 1).

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and raw non-commercial food 1.54 (<1% and 3%, TAC and overall, respectively). Within the 3% of the overall 193 group who reported raw non-commercial food, 25% noted they fed raw meat or eggs, 49% raw vegetables, 15% raw 194 fruit, and 3% raw dairy. The bowl material for each group was also comparable (Fig 2) with the majority of each Bacterial Contamination Evaluation-10 208 As is common with total aerobic counts (TAC), there was a wide range in values, therefore data was examined on a 209 log10 scale. Differences were found within groups A and B for TAC between the pre-and post-treatments. Group C 210 showed no significant change in TAC from the initial to the final bowl swab for TAC. (Fig 3).

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The follow up survey was completed by 90% of TAC participants. Only 8% of Group A and B respondents reported

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A statistical model fitted to enable the prediction of the log-change, which included the last wash and last dry as 240 predictors, indicated that a significant difference, reflective of TAC, was observed between cold/lukewarm wash and 241 FDA recommended methods (dishwasher or hot water wash). The difference was a decrease of 1.52 units on the log 242 scale (p=0.005) for TAC following a hot water wash or dishwasher as compared to a cold/lukewarm water wash.

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No significant effect of the drying method was found within or across any treatment group (p=0.234).

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However, the risk of contamination of the household can be mitigated. We concluded that bacterial contamination is 268 impacted by dish washing protocols due to the significant decrease in TAC for both Groups A and B, but not in

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Group C. Although this study did not differentiate between pathogenic and non-pathogenic bacterial species, TAC

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The majority of respondents reported storing their pet food against FDA and most manufacturers' recommendations, 287 which may have implications as far as increased microbial risk(16), nutritional degradation(17) and palatability. In 288 addition, some respondents were engaging in behaviors that may increase risk of bacterial contamination that were 289 not addressed in FDA guidelines such as the location of food preparation and storage. It is noted that the FDA has 290 added more specific recommendations to their website regarding pet food storage and pet food recalls (website 13 291 updated 4/14/2020); however, it is not comprehensive in addressing pet owners' food preparation choices.

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Additionally, because survey respondents indicated low levels of awareness that the FDA was a source of such dog 293 feeding hygiene recommendations, the expected sources of this information including the pet food label, 294 veterinarians and pet food retailers, should consider prominently featuring these public health recommendations for 295 their consumers. Further, it was noted Group C showed no significant change in TAC, despite the survey and the 296 knowledge of the upcoming sample collection serving as potential introducers of bias. This suggests that education 297 beyond awareness is needed to institute effective hygiene changes.

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Sample size was a limitation to this study, in particular for subgroups such as raw diets. Future studies should further 300 examine contamination with specific pathogenic bacterial species and consider the contamination risk of other