Survey of Heartworm Prevention Practices Among Members of a National Hunting Dog Club
Surveillance data indicate that failures have been reported for virtually all heartworm prevention product categories. Resistance of third and fourth stage larvae of Dirofilaria immitis to macrocyclic lactones, lack of compliance, other unknown factors, or a combination of these reasons may be the cause of failure. A survey of members of a national hunting dog club was conducted to identify practices used to prevent canine heartworm infections. Questionnaires were completed by 708 dog owners. Year-round administration of heartworm preventive medication was reported by 208 (88%) respondents residing north of the 37th parallel. Dosing was based on the estimated weight of the dog by 54 (7%) respondents, 389 (55%) did not record the date prophylaxis was administered, and 89 (13%) observed the dogs spit out pills. Heartworm testing at least once per year was done by 556 (79%) respondents and test dates were spread throughout the year. Only 448 (64%) respondents tested newly acquired dogs for heartworm. These findings suggest that veterinarians should place a greater emphasis on the frequency and timing of heartworm diagnostic tests, the importance of weighing dogs, duration of administration, recording the date monthly heartworm prophylaxis is given, and observing dogs to ensure that oral medication is retained.
Introduction
The U.S. Food and Drug Administration's Center for Veterinary Medicine (FDA/CVM) monitors adverse effects of approved products for heartworm prophylaxis.1 Currently, products that are licensed for prevention of heartworm in dogs are approved for 100% efficacy by the FDA/CVM; however, surveillance indicates that failures have been reported for virtually all heartworm prevention product categories.1 In a recent report the authors found that one of 14 dogs experimentally infected with L3 stage D. immitis larvae and given a single dose of a macrocyclic lactone preventive had a single live heartworm at necropsy 4 months post-treatment.2 In addition an in vitro assay for microfilaria has been developed in an effort to determine the susceptibility of D. immitis to the macrocyclic lactone class of preventives.3 In contrast to the previous finding, there are published studies that show macrocyclic lactones are 100% effective in preventing heartworm.4–9 When considering the proportion of D. immitis in refugia together with the specific stage in the life cycle that is targeted and a dosage that does not produce an adulticidal effect, it is unlikely that resistance to macrocyclic lactones by D. immitis will be selected.10 Most alleged prophylaxis failures have been reported in states endemic for heartworm. At this time, it is unclear if a true increase in complaints of ineffectiveness has occurred and, if so, whether this increase is due to an increase in reporting, lack of compliance, or failure of one or more products.1
In 2010, the American Heartworm Society (AHS) published guidelines for the prevention and management of heartworm infection in dogs.11 These guidelines are based on the latest information presented at the triennial symposium of the AHS, new research, additional clinical experience, and are revised from recommendations published in 2005.
The FDA/CVM has suggested that more comprehensive reporting in the future may provide evidence of patterns of emerging resistance to products used for heartworm prophylaxis, In turn, this will lead to updated labeling.1 In a previous study of records from 36 veterinary clinics, 48% of dogs were placed on the heartworm preventive program. Only 78% of the medication required to fully comply with the clinic's recommendations was administered.12
Currently, there are no other published studies that have evaluated the extent of compliance with recommendations for administration of heartworm prophylaxis and testing among dog owners. The purpose of this study is to compare current recommendations of the AHS and Companion Animal Parasite Council (CAPC) with practices for prevention of adult heartworm infection used by dog owners, kennel owners, and trainers, who are members of a national hunting dog club.11,13
Materials and Methods
Study Design
The study was conducted as an online survey and a mail-in questionnaire. The secretary for the national hunting dog club was contacted for permission to conduct an online survey of heartworm prevention practices used by club members. Permission to conduct the survey was granted by club officers and a request for club members to participate in the survey was placed on the club's website. In addition, dog owners attending one of eight club-sponsored events or field trials were made aware of the online questionnaire and were also given the opportunity to fill out and mail in a survey questionnaire identical to the online survey.
Study Subjects
Members of a national hunting dog club and visitors to the club's website were invited to participate in this study. In addition, attendees at events sponsored by the club that filled out an identical paper form of the questionnaire were eligible.
Procedures
A survey instrument was designed to identify the respondents' experience with dogs, location of housing, risk and duration of exposure of dogs to mosquitoes, how product(s) used for heartworm prophylaxis were chosen, duration of prophylaxis, method of administration, and frequency and timing of heartworm tests administered. In addition, respondents were asked if they ever had a dog test positive for heartworm after being on prophylaxis for >1 yr or >1 season (defined as failure of prophylaxis). If yes, the respondent was asked why they thought prophylaxis failed.
A notice was placed on the opening screen of the national hunting dog club's website encouraging members to complete the online questionnaire and directing the respondents to a secure server at the University of Tennessee, College of Veterinary Medicine (UTCVM). In addition, an announcement was made by a volunteer club member at eight regional events sponsored by the club, asking for participation in the online survey. Paper copies of the survey were handed out at these events, together with preaddressed stamped envelopes addressed to the principal investigator.
The online questionnaire was converted to a Hypertext Markup Language format and placed on a secure web server at the UTCVM. Data were collected into a MySQL relational databasea for the duration of the survey (May 1, 2008 to Nov 15, 2008). The database was password-protected and configured as “write-only” to prevent accidental data loss. Upon completion of the survey, the database was deleted from the server.
Data from respondents who completed paper copies of the questionnaire were added to the database as they were received. At the termination of the data collection period, survey responses were downloaded from the server as an Excelb spreadsheet and imported into SASc format for statistical analysis.
Based on an adaptation of the Fortin/Slocombe model, using temperatures conducive to incubation of infective larvae, heartworm transmission in the continental U.S. is predicted to occur for ≤6 mo above the 37th parallel (i.e., the Virginia-North Carolina State line).14 Therefore, survey respondents were divided into two groups: those residing north of the 37th parallel (group A); and those residing south of the 37th parallel (group B). States included in group B were NC, TN, SC, GA, FL, AR, LA, OK, TX, NM, AZ, MS, and AL. All other states were included in group A. Data on current recommendations made by the AHS and CAPC for prevention of infection with adult heartworm in dogs and schedules for heartworm testing were obtained from their respective websites.11,13
Statistical Analysis
Denominators vary due to a respondent either overlooking or failing to respond to a specific question. Summary statistics for continuous variables were computed and expressed as mean ± 1 standard deviation unless data were nonnormally distributed. In this case data were summarized as median, 25th and 75th percentiles, and interquartile range (IQR). Categorical data are expressed as numerator, denominator, and percent. Comparison of categorical outcomes between respondents residing north and south of the 37th parallel was done with a χ2 test. Continuous outcomes were compared with a t-test or nonparametric two sample Wilcoxon test depending on whether the data were normally distributed. The Shapiro-Wilk test was used to assess the fit of continuous data to a normal distribution. A P value of <0.05 was used to determine statistical significance for all tests.
Results
A total of 708 responses were obtained, consisting of 39 mail-in and 669 online questionnaires. Distributions of heartworm and residences of respondents are shown in Figures 1 and 2. The majority of respondents identified themselves as dog owners and respondents had been caring for dogs a median of 19 yr (Table 1). The majority of all respondents was responsible for 2–5 dogs and resided south of the 37th parallel. The proportions of respondents that gave heartworm prophylaxis all year were similar among those residing north (88%) and south (86%) of the 37th parallel (Table 1). Among respondents that did not give heartworm prophylaxis all year, the average number of months the dogs received heartworm preventive for those residing north and south of the 37th parallel were similar(7.0 ± 1.6 mo and 7.2 ± 1.6 mo, respectively). Similar proportions of respondents, residing north (16%) and south (16%) of the 37th parallel reported mosquito activity during all months of the year. Mosquito activity was observed by 43% and 45% of residents north and south of the 37th parallel, respectively, prior to April 1. During Nov and Dec, 43% of respondents north and 44% of those residing south of the 37th parallel reported mosquito activity (Figure 3).
Citation: Journal of the American Animal Hospital Association 47, 3; 10.5326/JAAHA-MS-5643
Citation: Journal of the American Animal Hospital Association 47, 3; 10.5326/JAAHA-MS-5643
Citation: Journal of the American Animal Hospital Association 47, 3; 10.5326/JAAHA-MS-5643
Reported as median (interquartile range)
Application of topical repellents and bringing dogs indoors were the most common procedures used by respondents to reduce exposure of dogs to mosquitoes (Table 2). One or more risk factors for the presence of mosquitoes were present within 91.44 m of the house or kennel, as reported by 396 (56%) respondents. During the season of year when mosquitoes were reportedly present, 79% of respondents reported that dogs were outdoors at dusk, dawn, or after dark, a time of day when many mosquito vectors for D. immitis were actively feeding.15–17
Numerator not equal to 708 due to more than one risk factor listed by single respondent.
Reported as median (interquartile range)
Most dogs (99%) belonging to respondents were given heartworm preventive medication. The brand of heartworm preventive used by respondents at the time of the study had been in use for a median of 5 yr (IQR, 2–10 yr). The majority (82%) of respondents selected a product for heartworm prophylaxis based on their veterinarian's recommendation (Table 3). Other factors considered in product selection (n=67) included cost (n=22), experience (n=14), personal research (n=17), ease of administration (n=2), additional effects against selected internal or external parasites (n=4), free samples (n=4), and tradition (n=4). For respondents not giving heartworm prophylaxis all year, administration was started after April 31 by 5/12 (42%) respondents residing north of the 37th parallel and 16/41 (39%) of those south of the 37th parallel. Administration was stopped prior to October 31 by 3/13 (23%) of those residing north of the 37th parallel and 6/34 (18%) respondents residing south of the 37th parallel. The decision to start and stop heartworm prophylaxis was made on the advice of a veterinarian (29%), observation of mosquito activity (28%), or as an annual routine (38%, Table 3).
Temperature (n=3), weather (n=2)
The majority (84%) of respondents weighed each dog separately and determined the dose of heartworm preventive medication based on advice from their veterinarian or from label directions (Table 4). Other methods (not specified) were used to calculate dose by 33 (4%) of the respondents. Heartworm preventive was given on the same day each month by 94% of respondents and 45% recorded the date of administration. Most (82%) respondents administered heartworm preventive directly into the mouth and 14% gave the medication with the dog's food. Other methods included topical application (4%) and injection (0.4%). The majority of respondents (93%) were responsible for the administration of heartworm prophylaxis, whereas 3% of respondents indicated that prophylaxis was administered by two or more people. Dogs were observed at one or more times in the past to spit out pills by 13% of the respondents.
Computer (n=12), calendar (n=6), other recurring events (n=13)
Injectable (n=3), topical (n=25)
Reported as median (interquartile range)
Testing for heartworm annually or semiannually was reported by 78% of respondents and 84% reported a test for heartworm in the past 12 mo. Testing for heartworm was performed throughout the year and was done prior to April 1 by 36% of respondents residing south of the 37th parallel (Figure 4). Only 64% of respondents reported testing an adult dog for heartworm either prior to or at the time of their introduction into the kennel or home. Only 21% of newly introduced dogs that were tested had a second test after their introduction (Table 5). Of the respondents performing a second test, 15 (25%) tested <3 mo after introducing a new dog and 13 (22%) tested >9 mo after introducing a new dog. The majority (77%) of respondents that reported testing for heartworm did not know whether a test for antigen, microfilaria, or both was performed.
Citation: Journal of the American Animal Hospital Association 47, 3; 10.5326/JAAHA-MS-5643
Median (interquartile range)
A total of 121 (17%) respondents reported having at least one dog that tested heartworm antigen positive in the past, despite administration of preventive medication for one or more seasons. During the 12 mo prior to filling out the questionnaire, 65 (9%) reported experiencing failure of heartworm prophylaxis. The annual incidence of prophylaxis failure was 65 of 3,832 dogs under respondents care (0.017%). Among 70 of the 121 (58%) respondents that ever reported failure of prophylaxis, reasons given were: resistance to product (53%); missed doses (26%); dose was too low (11%); test was not accurate (6%); failure of the dog to absorb the drug (4%); and prior infection (1%).
Discussion
These data suggest a need for veterinarians to place a greater emphasis on specific recommendations made to clients to increase compliance with AHS guidelines and improve the effectiveness of heartworm prevention in dogs. The AHS's most recent guidelines for prevention of heartworm in dogs state that dogs, regardless whether the dog resides north or south of the 37th parallel, should receive prophylaxis year-round to prevent heartworm disease increase compliance and control of pathogenic and/or zoonotic parasites.11 In this study, only 16% of respondents that resided north of the 37th parallel reported observing mosquito activity all year.
Heartworm transmission is thought to require a constant average 24 hr temperature of 18°C for approximately 1 mo.14,18,19 Therefore, if prevention of heartworm is the primary concern, additional research is needed to show that year-round administration of heartworm prophylaxis will improve compliance and reduce the risk of heartworm infection among dogs, particularly those residing north of the 37th parallel. Among the study population, almost identical proportions of respondents residing north (19%) and south (21%) of the 37th parallel did not administer heartworm prophylaxis all year.
Among study participants, 56% reported one or more habitats favorable to mosquitoes within 90.44 m of the kennel or house. Further, 28% of those did not use any of the common methods to reduce exposure of dogs to mosquitoes during the transmission season. In addition, 79% reported that dogs were outdoors at dusk, dawn, or after dark, when increased activity of many mosquito vector species would be expected to occur. In a previous study, keeping dogs indoors, particularly during the evening and night, was reported to be as effective as chemoprophylaxis.20 In states where heartworm is most prevalent (i.e., MS, LA, AL, and AR), it would seem prudent to take additional precautions, together with administration of heartworm prophylaxis, to reduce the risk of infection.21
Among respondents that did not administer heartworm prophylaxis all year, 25/90 (28%) started and stopped medication based on the presence of mosquito activity. Of these, 34 (38%) started and stopped on the same day each year. Peak plasma levels of the macrocyclic lactones ivermectin and milbemycin will be reduced by 97% in an average of 16.6 days and 8.1 days, respectively.22,23 If seasonal administration of heartworm prophylaxis is chosen, the AHS recommends beginning administration of heartworm prophylaxis within 1 mo of the anticipated start of transmission and giving the last dose 1 mo after transmission ceases, because macrocyclic lactones may not kill L3 stage heartworm larvae that have been introduced posttreatment. Dog owners may not recognize a low level of mosquito activity that occurs at the onset of the transmission season and, more importantly, they may stop medicating too early if they fail to recognize activity at the end of the season. AHS guidelines published in 2005 suggest starting heartworm prophylaxis by April 1 and continuing until Oct 31 for dogs residing north of the 37th parallel.24 Among respondents residing north of the 37th parallel, when heartworm prophylaxis was administered seasonally, it was not started until after April 31 by 5/12 (42%) of the respondents and was discontinued prior to Oct 31 by 3/13 (23%) of dog owners. If infection with L3 stage larvae occurs after the administration of the last dose of a macrocyclic lactone, these larvae may not be affected due to the relatively short half-life of the these drugs in plasma.22,23
The dose of heartworm preventive was based on an estimated body weight of dogs by 54 (7%) respondents. Underestimation of weight or failing to take into consideration weight gain by growing puppies may result in a dose of heartworm preventive that is too low to be effective. When administering monthly heartworm prophylaxis, 94% of respondents reported medicating dogs on the same day each month and only 46% of respondents recorded the date on which prophylaxis was administered. Of the 37 respondents that did not administer heartworm prophylaxis on the same day each month, 11 (30%) did not record the date of administration. By failing to record day of administration of heartworm preventive and relying on memory to give medication each month, the likelihood that one or more treatments may be delayed or missed altogether may be increased. In addition, 13% of respondents observed dogs spit out the pills postadministration. It is likely that this occurrence is underreported and may go unnoticed, further reducing effective owner compliance.
The AHS recommends testing for heartworm annually, 6–7 mo after the last date when heartworm transmission could have occurred. Among dog owners in this study sample, only 78% tested one or more times per year and 10% did not test at all. Among the 70 respondents that did not test, 62 (89%) gave heartworm preventive all year. The AHS recommends testing once yearly, regardless of whether the dog is on year-round prophylaxis. This practice will identify a dog that is infected due to lack of compliance, was infected prior to the start of prophylaxis, or may represent true failure of prophylaxis.
The AHS guidelines also recommend against indiscriminate testing at any time of the year, in an effort by the veterinarian to distribute the workload. For instance, indiscriminate testing may put the date of testing within the predetection period for determining if infection occurred the preceding season, thereby wasting the test. Although heartworm testing is being done during all months of the year, the majority of tests on the dogs in this study were performed between Feb and June. Nonetheless, 106/537 (18%) of all dogs were tested during the months of Jan and Feb and 26/537 (5%) of dogs were tested in Nov and Dec. When conducting heartworm tests without consideration of the timing from the last possible date of transmission, an infection occurring late in the previous year may be missed if the test is not done 6–7 mo after the last possible date of transmission. Alternatively, if the test is done later during the transmission season, a positive test may not distinguish whether an infection occurred during the previous or current year. These test results may lead to erroneous conclusions regarding failure of heartworm prophylaxis or, in some cases, attributing failure to the wrong product. Among dog owners residing south of the 37th parallel, 36% tested for heartworm prior to April 1. Thus, infections that occurred in Sept or later during the previous year may not be detected. This will complicate attempts to determine the cause, if failure of the product is suspected. When changing product after a negative heartworm test done prior to April 1, a positive test performed later, during the current transmission season, may not distinguish whether infection occurred prior to or after switching products.
Only 64% of respondents reported conducting a heartworm test either prior to or at the time of introducing a new dog to the kennel or household. Of the respondents that reported testing either prior to or at the time of introducing a new dog to the kennel or household, only 13% of those tested the dog a second time after introduction. AHS guidelines state that to most effectively evaluate the efficacy of the original or a new product, the dog should be tested for antigen prior to starting or changing products again in 3–4 mo (for monthly products and diethlycarbamazine) or 4 mo (for 6 mo injectable products) and again in 5 mo (i.e., 8–9 mo after starting or changing products). A second heartworm test was performed ≤3mo after introducing a new dog as reported by 15 (25%) of the respondents that tested prior to or at the time of introduction. Testing before a predetection period of 3–4 mo may fail to detect a pre-existing infection. A second heartworm test was done >9 mo after introducing a new dog by 13 (22%) of respondents. When a second test is done >9 mo after introduction, a positive test may represent either a pre-existing infection or an infection that occurred after introduction. Both of these practices may result in an infection being attributed to failure of heartworm prophylaxis when, in fact, the infection was due to inadequate testing and failure to identify a pre-existing infection prior to initiation of prophylaxis.
The strength of this study is that data were obtained directly from dog owners; therefore, results represent practices that are being conducted, rather than those practices veterinarians are recommending. In addition, the distribution of respondents appears to be representative of the distribution of heartworm in the United States; therefore, these data are more likely to be representative of heartworm prevention practices nationally. The study sample may be biased toward dog owners who have a greater knowledge base and motivation to comply with recommendations for heartworm prevention compared with the average dog owner. Membership in the hunting dog club provides access to educational material with information on the prevention of heartworm. In addition, 669/708 (94%) of the surveys were completed online, suggesting that the respondents may be more affluent and have greater access to information on prevention of heartworm from the internet. Respondents had a median of 19 yr experience in caring for dogs. They may also have a greater motivation to comply with recommendations for preventing heartworm based on their membership in the club and greater potential investment in their dog(s), which are purchased and trained for hunting. Therefore, the reported compliance with current recommendations for heartworm prevention may be greater than that expected to be found with the average pet dog owner.
Among respondents, 65/708 (9%) reported a failure of prophylaxis in the past year. It has been estimated that 55% of 77.5 million (42,625,000) dogs in the United States are on heartworm preventive.25 A total of 5,794 reports of failure of prophylaxis were documented by the FDA/CVM in a report published in 2005; however, the time period during which reports were collected was not specified.26 There are two reports in which the authors estimate the failure of preventatives to prevent heartworm infection in dogs to be <0.0001% and <0.1%.3,27 In the current study, respondents experienced an annual incidence of 65 failures among 3,832 dogs under their care (1.7%). The higher than expected incidence of failure among study participants may be due to an increased motivation of dog owners that experienced failure of prophylaxis to participate in the study, increased exposure to mosquitoes due to more time spent outdoors by dogs used for hunting, or a true increase in the rate of failure of heartworm prophylaxis.
Conclusion
This study was not designed to address the possibility that L3-L4 stage larvae of D. immitis have developed resistance to macrocyclic lactones (this question will be addressed when the results of ongoing studies are made public). In the meantime, departures from recommendations by the AHS and CAPC for prevention of adult heartworm infection were identified. The low estimated incidence of prophylaxis failures cited in the literature and relatively high frequency of inappropriate administration of prophylaxis and timing of heartworm tests suggest that these factors may play a major role in reports of suspected failure. These data suggest that, when communicating with clients, veterinarians should place a greater emphasis on the frequency and timing of heartworm diagnostic tests and that year round treatment with heartworm prevention medication does not eliminate the need for annual testing. In addition, the importance of weighing dogs to calculate dose of heartworm preventive medication, recording the date when monthly heartworm prophylaxis is given and observing dogs after heartworm medication is administered to identify dogs that spit pills out should be stressed.
Distribution of heartworm 2007, American Heartworm Society (with permissionfrom Wallace Graham, DVM Secretary/Treasurer of the American Heartworm Society).
Distribution of respondents to a national survey of heartworm control practices by dog owners.
Months that first and last mosquito activity was observed by respondents to a national survey of heartworm control practices residing either north or south of the 37th parallel.
Month that heartworm test was performed for respondents to a national survey of heartworm control practices residing either north or south of the 37th parallel.
Contributor Notes
