Introduction

Vaccination is considered one of the most important measures of preventing and controlling human and animal infectious diseases [1, 2]. A distinction is made between core and non-core vaccines in dogs. Core vaccines protect against infectious diseases that are common and have a severe outcome or zoonotic potential. They should be administered to all dogs. Non-core vaccines provide protection against specific infectious diseases and are given to dogs based on their risk of infection, which is influenced by factors, such as geographical location and lifestyle [3, 4].

According to the current World Small Animal Veterinary Association (WSAVA) vaccination guidelines, vaccines against canine distemper virus (CDV), canine adenovirus (CAV-1 and CAV-2) and canine parvovirus (CPV) are considered core vaccines in dogs. Rabies is a core vaccine in countries where it is endemic or required by law [4]. Since 2009, German guidelines have included vaccination against Leptospira spp. as a core component due to increase in prevalence in Germany and neighbouring countries and the zoonotic potential of the disease [5]. Due to zoonotic nature of leptospirosis [6], it is crucial to prevent humans from getting the infection through controlling the disease in dogs. Given that cases of hepatitis contagiosa canis (caused by CAV-1) only sporadically occur in Western Europe and that CAV-2 causes mild infection in dogs suffering from canine infectious respiratory disease complex (CIRDC), vaccination against CAV is a non-core vaccine.

To avoid epizootics, a population must reach a certain threshold of immunity, referred to as 'herd immunity', which describes how the ratio between the number of individuals immune to a particular infectious disease and the number of non-immune individuals influences the rate at which the infectious disease spreads. The equation to describe ‘herd immunity’ is (R0-1)/R0 [7]; the ‘basic reproduction number’ (R0) is defined as the average number of secondary cases caused by a single case within a susceptible population [8]. For example, the R0 for rabies in dogs in Machakos District, Kenya, represented 2.44 [9] and thus 59% of individuals within the dog population needed to be protected to avoid an epizootic. To the authors’ knowledge, there are no R0 values published for pathogens against which dogs are vaccinated, with the exception of rabies. Therefore, a vaccination coverage of ≥75% is generally recommended for all core vaccines [4]. Owner compliance with vaccination recommendations is crucial to achieve this level of vaccination coverage.

Diseases such as canine distemper and parvovirosis are still present in Northern and Western Europe [10, 11], although they are observed less frequently, but the exact number of clinical cases is unknown. Nevertheless, repeated outbreaks occur, mainly due to importation of dogs from Southern or Eastern European countries [12–14]. Therefore all dogs should have an up-to-date vaccination status. In human medicine, people are increasingly concerned about vaccine-associated adverse effects (VAAEs) and are unsure about using vaccines for themselves or for their children [15]. Similarly, many animal owners are hesitant about vaccinating their pets, they doubt the necessity of vaccinations [16] and are concerned about VAAEs [17, 18]. Several factors including waiting times at veterinary clinics have been shown to negatively affect owner compliance with cat vaccination in Germany [18]. The results of that study can be used to improve vaccination coverage in cats, and a similar study would be useful for the same purpose in dogs.

Currently, dog population in Germany is estimated to be 9.4 million and 20% of veterinary visits consist of preventive health care, including vaccinations [19]. However, there are no studies on dogs’ vaccination rates and owners’ attitudes to vaccination in Germany so far. Studies on compliance of dog owners across Europe are also scarce. In a 2019 survey (Animal Wellbeing Report) conducted in United Kingdom (UK), 78% of dogs received regular vaccination, but details on vaccination intervals and the vaccines used were not provided. Owners who were non-compliant stated that vaccination would be unnecessary and too expensive [20]. In a study done in Uganda on dog owners’ attitudes towards rabies vaccination, it was determined that 55.6% of owned dogs received rabies vaccination and poverty had a negative impact on vaccination rate [21]. However, the socio-demographic differences between Uganda and Germany likely indicate that the factors associated with owner compliance differ, and thus it is necessary to conduct a separate study focussing on dog owners in a European country.

The aim of the present study was to determine owner compliance with vaccination guidelines recommended for dogs. The status of dogs with regard to core vaccines and the factors associated with owner compliance were determined.

Methods

Results

Survey response

A total of 4,202 questionnaires were completed and those from participants who met exclusion criteria were left out: 3,881 questionnaires were evaluated. Table 1 shows the variables investigated in the logistic regression and selected by the model. The variables that were not selected and thus eliminated by the model are listed in S2–S5 Tables. Table 2 shows the vaccination history of the dogs and owner attitudes towards vaccination.

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Table 1. Variables investigated and selected by the logistic regression model (n = 3,881).

https://doi.org/10.1371/journal.pone.0238371.t001

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Table 2. Vaccination history of dogs and owner attitudes towards vaccination (n = 3,881).

https://doi.org/10.1371/journal.pone.0238371.t002

Vaccination records

Of all owners, 8.8% (n = 340/3,881) submitted the vaccination passports of their dogs. The descriptive evaluation of the passports and the survey results were similar (Table 3). Nearly 67.9% and 58.2% of the passports and the questionnaires showed that the dogs had an ‘up-to-date vaccination status’, respectively. The vaccination status reported on the questionnaires and vaccination passports did not match in 19.1% (n = 65/340) of the dogs; the kappa coefficient of 0.594 with a p-value of <0.001 indicated lack of agreement between the two assessments. A total of 4.7% (n = 16/340) of owners overestimated the vaccination status of their dog, and 14.4% (n = 49/340) of owners underestimated the status. In 80.9% (n = 275/340) of dogs, the vaccination status obtained from the questionnaire was consistent with the vaccination status of the vaccination passport. Around 53.5% (n = 182/340) of owners correctly stated that the dog had an ‘up-to-date vaccination status’ whilst 27.4% (n = 93/340) correctly stated that the dog did not have an ‘up-to-date vaccination status’.

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Table 3. Comparison of data from vaccination passports and survey responses (n = 340).

https://doi.org/10.1371/journal.pone.0238371.t003

Factors associated with status of canine vaccination in Germany

Twenty-seven factors were selected by the statistical model and thus associated with ‘up-to-date vaccination status’ reported by the owner. Dog’s age (16 weeks to 15 months) (OR: 3.08; 95% CI: 2.05–4.68), type (working dogs; OR: 2.06; 95% CI: 1.22–3.53) and travelling abroad within the previous 36 months (OR: 1.82; 95% CI: 1.12–2.96) were the factors having strongest ‘positive’ association with an ‘up-to-date vaccination status’ in relation to their respective reference categories (Table 4).

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Table 4. The 10 factors with the strongest ‘positive’ association with an 'up-to-date vaccination status' in relation to the respective reference categories (n = 3,881).

https://doi.org/10.1371/journal.pone.0238371.t004

Regarding veterinary recommendations on vaccinating dogs against infectious diseases, advice not to vaccinate against Leptospira spp. (OR: 0.08; 95% CI: 0.04–0.18), to vaccinate against CDV/CPV less frequently than every 3 years (OR: 0.21; 95% CI: 0.04–0.72) and owner’s ignorance of regular revaccination against leptospirosis (OR: 0.21; 95% CI: 0.16–0.28) had the strongest ‘negative’ association with ‘up-to-date vaccination status’ of a dog in relation to their respective reference categories (Table 5).

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Table 5. The 10 factors with the strongest ‘negative’ association with an ' up-to-date vaccination status' in relation to the respective reference categories (n = 3,881).

https://doi.org/10.1371/journal.pone.0238371.t005

Discussion

The goals of the present study were to investigate vaccination status of dogs in Germany and owner compliance with vaccination. The results showed that less than half of the dogs had an ‘up-to-date vaccination status’ according to current vaccination guidelines; especially the vaccination rate against Leptospira spp. was poor. Furthermore, vaccination recommendations made by the veterinarian had a strong association with the vaccination status.

An ‘up-to-date vaccination status meant in the present study that vaccinations were required a minimum of every 3 years for CDV, CPV and RV and annually for Leptospira spp. This vaccine schedule is in accordance with vaccination guidelines and recommendations for core vaccinations in dogs in Germany [3]. In contrast to international guidelines (e.g., WSAVA) [4], leptospirosis vaccine has been considered a core vaccine in Germany since 2009 [5] and in other countries including the UK [23]. The main reason for including leptospirosis as a core vaccine is to prevent disease in individual dogs and to reduce urinary shedding of leptospires [24] and thus to protect humans. Protection of other animals, such as livestock, is also important as infected dogs could inadvertently wander onto pastures and increase the risk of infection in cattle by shedding Leptospira spp. [25]. The rate of leptospirosis in dogs had markedly increased in several European countries including Switzerland in the last 10 years [26] as well as in countries outside Europe [27]. A similar increase has also been seen in human medicine [28, 29] with about 1 million new infections every year worldwide. Leptospirosis is therefore one of the most important zoonotic diseases in the world [30]. Climate change is considered responsible for further increases in prevalence of infections because higher temperatures, increased precipitation and flooding enhance the survival time and spread of Leptospira spp. Progressive urbanisation and reduction of animal habitat also lead to a higher risk of infection [31, 32], which confirms the importance of including the leptospirosis component in a core vaccine program.

The duration of immunity (DOI) against RV varies from 1–3 years according to the vaccine manufacturer's specifications. In this study, however, the DOI was assumed to be 3 years regardless of the manufacturer's specifications because studies show that RV vaccination provides a DOI of at least 3 years [33]. Germany has been free of terrestrial rabies for many years. Rabies is currently still included in the core vaccines due to the national regulations [34]. Moreover, rabies is still present in large parts of the world [35, 36] and the majority of pet owners in Germany take their dog with them when travelling abroad (67%) [37], and rabies vaccination is required by law for crossing boarders in the European Union (EU) [34]. Rabies is a lethal zoonosis, and about 59,000 people die annually worldwide and a high number of cases go unreported [38]. In 99% of infections, the virus is transmitted to humans by a dog bite. Vaccination of dogs is therefore the most important measure to prevent human infections in endemic countries [39]. However, the core vaccine status of rabies vaccination might change in the future, as all EU countries will soon be declared ‘rabies-free’.

Vaccines against canine adenovirus (CAV-1 and CAV-2) are considered core vaccines according to some international guidelines [4]. However, CAV-1 causing infectious canine hepatitis has almost been eradicated from Western Europe [3, 40] and is no longer a core vaccine according to national guidelines [3]; CAV-2 only causes a very mild disease belonging to the CIRDC. Therefore, CAV vaccination was not considered part of an ‘up-to-date vaccination status’ in this study.

Based on the evaluation of the questionnaire and vaccination passports, owner compliance with vaccination guidelines was poor. Although this study is not necessarily representative of the whole dog population in Germany, it suggests that dogs might not be adequately protected. A comparison of information between the vaccination passports and owners’ responses revealed that owners had good knowledge on the vaccination status of their dogs. However, the number of dogs with an ‘up-to-date vaccination status’ was slightly higher in the group of participants who submitted vaccination passports than in the group that did not. This could have been because owners who sent in the vaccination passports of their dogs had a special interest in vaccination.

A study conducted in UK found that 78% of dogs had been vaccinated in the country, but information on used vaccines and vaccination intervals were missing, making comparison difficult [20]. Cat owner compliance with vaccination guidelines in Germany was shown to be considerably higher than dog owner compliance with 77.9% of cats having been currently vaccinated [18]. The most likely reason for the higher up-to-date vaccination status in cats is that all feline core vaccines provide a DOI of up to 3-year and thus vaccinations are commonly only performed every 3 years, while dogs need to be revaccinated annually for leptospirosis because of the short-term immunity afforded by this vaccine [3, 4]. In the present study, few owners stated that their dog had never been vaccinated, although it is possible that these participants were not aware of vaccinations the dog might have had before they became the owner.

Owner compliance with vaccination against Leptospira spp. was particularly poor, and only half of all dogs were up-to-date on this vaccine, which was concerning. Possible reasons for the poor compliance with vaccination against leptospirosis include scheduling issues and costs associated with annual vaccination and owner fear of VAAEs, especially in vaccines containing multiple serovars [41]. The German pharmacovigilance report showed increased VAAEs after leptospirosis vaccination that coincided with the market launch of multivalent vaccines against Leptospira spp. The VAAEs mainly manifested as an immunological hypersensitivity with oedema of the head, pruritus, vomiting and diarrhoea, as well as swelling and pain at the injection site. Approximately every 10th VAAE reported was an acute shock [42]. Another potential explanation for the low leptospirosis vaccination rate might have been that the dog owners were not aware of the seriousness of the disease in humans and in dogs. A Portuguese study found that dog owners lacked knowledge of the zoonotic potential of leptospirosis and its prevention [43]; this also likely applies to dog owners in Germany. In human medicine, inconsistent vaccination in children is associated with lack of parental knowledge of immunization [44], but vaccination rates can be increased by targeted educational measures [45, 46]. Sufficient consultation time and proper information from the veterinarian increases owner satisfaction and improves the client-veterinarian relationship, which can promote owner uptake of preventive measures [47–49]. A similar association was found in the present study; dogs belonging to owners who considered themselves poorly informed about vaccinations were less likely to be vaccinated than dogs of owners who considered themselves to be very well-informed.

Young dogs are more likely to have an ‘up-to-date vaccination status’ presumably because owners are aware of the importance of the primary vaccination series in establishing immunity. This is also evident in human medicine where young children have higher vaccination coverage than adults [50]. A possible reason for not vaccinating older dogs might be owner assumption that primary immunization leads to lifelong immunity. In the case of CDV and CPV, this presumption might actually be valid because studies showed long-term immunity in some dogs; e.g., antibodies were present in dogs 14 years after the use of a modified live CDV vaccine [51, 52]. However, it cannot be assumed that long-term immunity occurs in all dogs.

The higher probability that working dogs, such as police or rescue dogs, had an ‘up-to-date vaccination status’ was presumably due to vaccination guidelines within the respective organizations. The financial input for training these types of dogs could have also played a role in owner compliaance with vaccination guidelines. The increased vaccination rate in dogs travelling abroad in the previous 36 months was likely because of rabies regulations within the EU. The veterinarians had probably recommended other core vaccines when these dogs were presented for RV vaccination.

Surprisingly, almost half of the dog owners reported that annual CDV and CPV vaccination was recommended by their respective veterinarians. Dogs of these owners were more likely to have an ‘up-to-date vaccination status’, which shows that owners trust veterinary advice even though this advice is outdated. Revaccination against CDV and CPV, which involves modified live vaccines, should generally not be carried out more frequently than every 3 years [53]. This is recommended by both the WSAVA and German guidelines [3, 4] and is based on numerous studies on the DOI of these vaccines [51, 52, 54–56]. Even if the manufacturers specify a shorter DOI, the veterinarian should follow the recommendations of the guidelines, which equates to off-label use, because dogs should not be vaccinated more often than necessary [4]. Outdated vaccination recommendations could be attributable to ignorance on the part of the veterinarian and the fear of lost revenue with less frequent vaccinations. Dogs owned by participants who were unsure about their veterinarian's recommendations for RV revaccination had a higher probability of an‘up-to-date vaccination status’, but the reasons for this association are unknown.

The higher vaccination rate in dogs staying in boarding kennels (future and past stays) compared with dogs staying at home, can be attributed to the requirement of an up-to-date vaccination status. The association between owners who had received a tetanus vaccination within the last 10 years and the vaccination status of their dogs was of interest and suggests a link between the vaccination habits of owners and the vaccination status of their dogs. A human health survey in Portugal investigated factors associated with tetanus vaccination in immigrants. Higher household income and older age were negatively associated with tetanus vaccination rates, while living in sparsely populated areas was positively associated [57]. This could be due to the fact that people in rural areas are involved in agricultural work and therefore have more contact with soil in which the tetanus-causing pathogen is usually located. However, in the present study, the status on other vaccines (pertussis, influenza), age and sociodemographic background of the owners were not selected by the model and thus not associated with the vaccination status of the dogs.

Veterinary recommendations to owners on revaccinating dogs less frequently than every 12 months for leptospirosis had a strong ‘negative’ association with the vaccination status of the dog, especially when the advice was not to vaccinate against Leptospira spp. Such recommendations for leptospirosis vaccination are concerning and require further studies. It is not known why veterinarians consider vaccination against Leptospira spp. unimportant, but perhaps the disease is underdiagnosed contributing to their lack of awareness. It is possible that vaccination against leptospirosis is viewed critically by some veterinarians because >300 serovars in 24 serogroups are known [58], and yet vaccines in Germany are licensed for serovars of a maximum of 4 serogroups (Canicola, Icterohaemorrhagiae, Australis and Grippotyphosa) [59] and cross-immunity is restricted to serovars within a serogroup. Thus, despite vaccination, infection with Leptospira spp. cannot always be prevented in dogs [60]. However, the currently available canine leptospirosis vaccines have demonstrated to significantly reduce the number of leptospirosis cases in dogs, as demonstrated in Switzerland [61] and the vaccines contain the serogroups of the most common serovars also found in infected people in Germany (serovars of the serogroups Icterohaemorrhagiae, Canicola and Grippotyphosa) [62]. The canine vaccines not only prevent disease but also shedding of Leptospira spp. [24] and therefore reduce the zoonotic risk.

The finding that dogs were less likely to have an ‘up-to-date vaccination status’ when the veterinarian recommended a CDV/CPV revaccination interval of >3 years emphasizes the impact of veterinary recommendations on owners and the need to inform veterinarians of this issue. It is, however, possible that these dogs underwent testing for antibodies, which has been shown to be a useful tool for determining the necessity of revaccination [63, 64].

Occurrence of VAAEs in the past discouraged owners from having their dogs vaccinated and was ‘negatively’ associated with the vaccination status of the dog. Studies in cats and humans have shown that VAAEs have a negative effect on future vaccination decisions [18, 65]. Education about VAAEs appears to be important in allaying these concerns.

An association was found between the vaccination status of the dog and the owners' trust in the vaccination information provided by a homeopathic practitioner. This suggests that homeopathic practitioners, in contrast to veterinarians, are more likely to recommend alternative methods of disease prevention and discourage owners from having their dogs vaccinated, which is very concerning.

Compared with young dogs, an ‘up-to-date vaccination status’ occurred less frequently in older dogs, a finding that has also been reported in cats [18]. Owners of older animals might incorrectly assume that their pets are protected against infectious diseases because of long vaccination history or do not need vaccinations because infectious diseases do not occur in older cats and dogs. This assumption is supported by the finding that an ‘up-to-date vaccination status’ was more likely to be seen in dogs owned by participants who did not consider age as a very important factor in their decision on vaccination.

The association between the vaccination status of the dog and the residential area, the presence of children and the educational status of the owner was investigated, but the model did not select those variables. Interestingly, the model also did not select owner income or vaccination costs, which was in agreement with a study of cats in Germany [18]. These results indicate that pet owners in Germany are generally willing to pay for vaccination. This is in contrast to a cat study in the UK, where income and costs were selected by the model [2], although differences in the statistical model and vaccination guidelines used could have been the source of different findings. Many pets (57% dogs, 38% cats) have health insurance in the UK, but costs for vaccination are usually not covered [66]. Thus owners might not be accustomed or willing to pay for vaccination. In comparison, few cats (6%) and dogs (15%) are insured in Germany [67], and therefore owners are accustomed to paying for all veterinary costs. According to German veterinary fee regulations (GOT), the cost for vaccination of a dog (without including the cost of the vaccine) varies from 23.73 to 94.92 Euro, which is relatively inexpensive compared with treatment costs [68].

The limitations of the present study included validity of owners reporting an ‘up-to-date vaccination status’, which might not have always been correct. However, a sample of data on vaccination status reported by owners was checked by reviewing the vaccination passports and found to be in agreement. Nevertheless, it cannot be ruled out that owners, especially those who submitted vaccination passports, might have referred to this document while completing the survey, leading to an overestimation of owner knowledge on vaccination status. The definition of an 'up-to-date vaccination status' was based on RV revaccination every 3 years, although in Germany, RV vaccines with a shorter DOI (manufacturer’s specifications) are still available. However, it was assumed that most veterinarians follow the recommendation to vaccinate animals only as often as needed and therefore use vaccines with the longest possible DOI. Internet access was required for participation, which might have led to a certain bias, although the majority of the population in Germany (86%) uses the internet [69]. The survey was distributed via social media, and this might have attracted owners who were specifically interested in vaccination. However, a UK study showed that 78.6% of all pet owners use the internet as a source of information on health issues, especially social media and online forums [70]. A limitation of the statistical model was that post-selection inference is invalid and reference category selection can affect the results; classification into ‘positive’ or ‘negative’ depends directly on the choice of the reference category. Nevertheless, AIC is an established and common criterion for model selection as it balances goodness of fit with model complexity. Categorization into strongest ‘positive’ and ‘negative’ factors can result in strongly associated factors not being captured for discussion. However, all associated factors and their OR are listed in Table 1. Data similar to those reported in the present study do not exist in the current veterinary literature and therefore present an analysis that could serve as a model for further studies using causal inferences and binary variables.

Conclusion

This is the first study that provides information on vaccination status of dogs and dog owner attitudes and compliance relating to vaccination in Germany. The results suggest that the vaccination status of dogs does not meet guidelines for core vaccines. Protection against leptospirosis appears to be particularly poor, which is concerning from a veterinary and human medical standpoint and requires urgent improvement. The association between veterinary recommendations and owner compliance was strong, providing an opportunity for veterinarians to improve the vaccination status of dogs. Further research on owner compliance with vaccination and the vaccination status of dogs would be valuable to validate the results.

Supporting information

Acknowledgments

The authors would like to thank Anne-Claire Gehrig for her valuable input.