Canine heartworm disease (CHD) incidence and geographic range is increasing in the United States (1, 2). From 2013 to 2016, Drake and Wiseman (1) estimated that the relative change in CHD was +15.3% in the US, with highest increases in the Southeast region. Heartworm disease is preventable with the use of prophylactic macrolide medications, which are safe and effective (3). Previous studies have estimated that adherence to the recommended 12-month use of heartworm preventative is low (24.4% for monthly HWD preventatives) (4, 5). One study found that use of heartworm preventatives was estimated to be approximately 74–79% of dogs presenting to a veterinary teaching hospital, however it was reduced to 50% in winter (5). Very few studies have evaluated what factors are associated with heartworm preventative use in dogs. Bir et al. (6) found greater heartworm preventative use among dogs with owners that were male, younger, lived in the South, and had higher socioeconomic status. Gates and Nolan (5) evaluated multiple factors included signalment, presenting complaint, and vaccination status and found that only month of presentation and neuter status were associated with heartworm preventative use. Due to the sparse research on this topic, there is a need to identify additional factors associated with heartworm preventative use, including lifestyle, the strength of the human-animal bond, the environment, and living conditions. Therefore, the objective of this study was to evaluate the association of multiple factors with heartworm preventative use utilizing data available from the Golden Retriever Lifetime Study, which is a large prospective study that aims to identify risk factors for disease in golden retrievers (7). Due to the large number of predictors evaluated, we utilized elastic net regression, which is a regularized regression method that reduces risk of overfitting and multicollinearity (8).

The Institutional Review Board at Lincoln Memorial University approved this study (1,068 V.0). All data cleaning and analyses were conducted in Stata version 17.0 (College Station, TX).

There are very few studies that have investigated what factors influence heartworm preventative use in dogs (5, 6). To address this knowledge gap, we examined multiple factors associated with heartworm preventative use in a large sample of golden retrievers from the Golden Retriever Lifetime Study (7). Due to the high number of predictors, we implemented a robust statistical analysis technique (bootstrapped elastic net regression) that can handle multicollinearity unlike traditional regression techniques. Regularization methods, also called penalized regression models, reduce risk of overfitting by constraining the estimated coefficients and decreasing out of sample error (13). We identified multiple variables associated with heartworm preventative use, including vaccine use, U.S. region, sex, height, other disease conditions, medication and supplementation history, and characteristics of the spaces where the dog spends time.

Overall, the prevalence of heartworm preventative use was 39.5%. This was much lower than an estimate from a sample of dogs presenting at the veterinary teaching hospital at the University of Pennsylvania, which reported that 79.8% of dogs were currently on preventatives at the time of their admittance (5). In our study, even among dogs located in the Southern U.S., which has the highest prevalence of heartworm preventative use and rate of heartworm disease, prevalence was only 45.9% (2, 6). Correspondingly, use of heartworm preventatives was lowest in the Pacific region which has some of the lowest rates of heartworm disease (2). Our estimates are similar to results reported in Bir et al., 2018 which found that 54% used heartworm prevention in a nationally representative sample. We also found that dogs in the highest quartile of height were less likely to be on heartworm preventative. Height is likely correlated with weight and cost could be prohibitive (14). However, weight did not make it into the final model, so the mechanism is unclear. It could be due to the distribution of the data and the quartile ranges may not correspond directly to the weight ranges of heartworm medications. We also found that sex was associated with heartworm preventative use. The “sex” variable was a combination of biological sex and spay/neuter status. While there were no differences between males versus females, intact males and females had lower rates of heartworm preventative use compared to their altered counterparts. Spay/neuter status likely represents owner investment in health and veterinary care. This corroborates other research from Gates and Nolan (5) who found that intact dogs were less likely to be on preventative compared to neutered dogs and that overall, there were no differences between males and females.

Dogs that received a Bordetella vaccine, rabies, or other vaccine had greater heartworm preventative use. This could be due to greater trust in veterinarian recommendations (15). Interestingly, supplements were associated with lower heartworm preventative use. Pet owners that use supplements may prefer a holistic, naturopathic approach to pet care. They may use supplements such as black walnut or home remedies such as brewer’s yeast or essential oils instead of heartworm preventatives (15, 16). Prior use of heartworm preventatives and current use of tick preventatives were strongly associated with current heartworm preventative use which is not surprising since some heartworm preventatives also protect against infections from ticks. Offering a combination drug may increase adherence to heartworm preventatives, especially if owners do not understand and perceive the risk of heartworm disease (17). Dogs that were diagnosed with an infectious disease system or an ear/nose/throat system disease were more likely to be on preventative. The infectious disease system includes gastrointestinal parasites; therefore, owners may be more likely to be on medications for parasite control after a diagnosis and many of these medications include heartworm control. The mechanism behind why an ear/nose/throat system diagnosis is associated with greater heartworm preventative use is unclear. One possible mechanism is that some of the symptoms of heartworm disease involve the ear/nose/throat system, such as coughing, so the dog may have been tested for heartworm disease and then subsequently put on preventative. In a survey among members of a hunting club, only 70% tested annually, which is expected to be lower in the general population (17). Some of the dogs that do not get tested annually may only be tested when ill and presenting with symptoms that could be attributed to heartworm disease.

Dogs that were exposed to the sun on concrete flooring were more likely to be on preventative. The other sun exposure flooring categories were grass and dirt but were not retained in the final model during the variable selection process. Concrete flooring may be significant as it may indicate a closer proximity of the dog to the house, whereas dogs kept on grass and dirt may include dogs that free roam and that receive poorer general care compared to confined dogs (18). Heartworm preventative use increased with the number of carpeted rooms in the house and was higher among dogs that spent time on hardwood floors. Both variables could be proxies for socioeconomic status. Owners of higher socioeconomic status may be more likely to spend money on heartworm preventative as they have more disposable income. However, Gates and Nolan (5) did not find that income was significantly associated with heartworm preventative use in multivariable analyses, although Evason et al. (15) reported that 33% of clients said cost was a barrier and downside to using heartworm preventatives. It is of note that variables that represent attachment and the human-animal bond were not significant in the final model. This is similar to results reported in Shore et al. (19) who did not find a clear trend between attachment levels and heartworm preventative use.

A major limitation of this study is the limited generalizability outside the study population. The study population consisted of all golden retrievers that were less than 6 years of old. The results of the study may not be generalizable to other breeds, older dogs, and to the general dog population. In addition, owners that participate in the GRLS may be inherently different than owners that do not participate. Owners that participate may be more invested in their dog therefore more likely to adopt veterinarian recommendations for heartworm prevention. However, this does not seem to be the case, as the prevalence of heartworm preventative use was low in our sample and was close to other national estimates (6). Another limitation is that we did not have owner demographic data. We were only able to infer socioeconomic status from some of the variables. Owner factors including gender, age, and socioeconomic status have been shown to be associated with heartworm preventative use (14). This study also had many strengths. We were able to leverage a large dataset representative of the U.S. that collected multiple variables in a standardized questionnaire. In addition, we were able to evaluate a number of factors that have not been tested for their relationship with heartworm preventative use prior to this study. Still, the findings of this study can be strengthened by conducting additional studies outside of the study population.

Overall, we found multiple factors associated with heartworm preventive use. Results of this study can be used to help veterinarians understand motivations and factors behind heartworm preventative use in dogs so that client communication can be improved. Results can also be used to identify populations at risk of low heartworm preventative use so that education and outreach efforts can be better targeted. Future studies can confirm the findings in a more diverse study population and use the results of this study to develop and test client communication and educational interventions.

The data analyzed in this study is subject to the following licenses/restrictions: Data can be requested through the Morris Animal Foundation Golden Retriever Lifetime Study RFP. Requests to access these datasets should be directed to https://www.morrisanimalfoundation.org/golden-retriever-lifetime-study-rfp.

The secondary data analysis conducted in this study was approved by the Lincoln Memorial University Institutional Review Board.

LW was involved in developing the project proposal, study design, data analysis, and writing the first draft of the manuscript. CF and VF were involved with study design and editing the manuscript. All authors contributed to the article and approved the submitted version.

This study was supported by the Golden Retriever Lifetime Study and this manuscript were made possible through financial support provided by the Morris Family Foundation, the Mark & Bette Morris Family Foundation, VCA, the V Foundation, Blue Buffalo Company, Petco Love, Zoetis, Antech Inc., Elanco, the Purina Institute, Orvis, the Golden Retriever Foundation, the Hadley and Marion Stuart Foundation, Mars Veterinary, generous private donors and the Flint Animal Cancer Center at Colorado State University. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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