4.1. UB Demographic Data
Back in 1988, reporting on U.S. data, McKeown and Leuscher [42
] estimated that one in four dogs and cats were either euthanased or relinquished within 12 months of acquisition. Unfortunately, that situation does not seem to have changed. Dogs that died within the 1.0– < 2.0 age category had the highest odds (OR 3.71) of death attributed to an UB when compared to dogs in the < 1.0 age category. Owners who acquire a small, cute puppy are sometimes ill prepared for the challenges that emerge when the puppy approaches adulthood. Sexual maturity is reached by six to nine months, while social maturity commences at approximately 12 months and is generally complete by 36 months of age [15
]. During social maturity, significant changes in the brain manifest as changes in behaviour [17
]. Indeed, there is recent evidence that dogs may go through a rise in conflict behaviour as they approach puberty [43
]. It seems that while owners may be willing to excuse UBs in puppies, assuming that they will “grow out of it” or perhaps finding the behaviour more novel than undesirable, their tolerance of UBs is often finite. A dog’s behavioural responses, and especially those associated with aggression, are widely viewed as increasingly less plastic and more difficult to modify as the dog matures [17
]. This leaves a narrow window of opportunity to provide guidance and help to owners of young dogs displaying UBs [31
]. The current study showed only a six-month difference between the median age of first reported UB and age at euthanasia due to UB.
The median age of death due to a UB in the current study was 1.45 years, which is only 0.05 years lower than the equivalent age reported by the companion study in the UK [37
]. However, the current study found that the median age at which case dogs first displayed an instance of UB prior to death was 0.9 years, which is six months earlier than that reported by Boyd et al. [37
]. This suggests that Australian veterinarians may have an opportunity to assist owners of dogs exhibiting UBs that are younger, and possibly more malleable, than their UK counterparts. This is an opportunity, if pursued, that may save dogs’ lives and so merits close scrutiny.
Interestingly, whilst there was a higher proportion of female dogs dying of UB in Australia compared to the UK [37
], sex had no significant impact on the odds of death due to a UB in the Australian cohort. This is not consistent with previous studies that showed males to be at increased risk of death due to UB [5
]. That said, whilst female dogs had a lower prevalence of aggression, RTA, and other UBs, they had a higher prevalence of involvement in dog attacks than male dogs (Figure 1
). This finding is consistent with data reported by other studies where more aggression problems occur in males than females, particularly intermale and stranger-directed aggression, whilst higher rates of interfamilial aggression have been reported in females [44
]. It is normal for dogs from the same household to spend unsupervised time together and to share common resources in close proximity to each other, compared to time spent with unfamiliar dogs. Any conflict that arises, when there is no human around to intervene, has an increased risk of escalation to life-threatening injury. Further research to explore this difference could include: collecting data on domestic dog-keeping practices; the use of aversive stimuli in training [19
]; establishing whether the dogs involved in interdog aggression belong to the same household or are unfamiliar; exploring differences between same-sex aggression and male–female aggression; and assessing the role of competition for resources.
The acquisition source of dogs was recorded in only 12.5% of dogs that died with UB related reasons, but had comparable proportions to the data reported by Boyd et al. [37
]. This is surprising due to the disparity between purebred and crossbred status between the two study samples. One acquisition category in this study that was not captured by the UK study was online acquisition. However, this category contained only seven dogs (0.6%) in the current study. Previous research has shown the influence of acquisition source of a dog on levels of owner reported UB, with increased reports of unfriendliness, aggression, and excitability in dogs sourced from pet shops compared to those bred by the owner [21
4.2. Variables with a Genetic Basis
Crossbred dogs (OR 1.43) were significantly more likely to die from UB related causes than purebred dogs (Table 4
). They were proportionally more common in the current population than in the UK study [37
]. This is likely to reflect the true proportion of crossbred dogs in Australia as their continually rising popularity is estimated to comprise up to 46% of Australia’s total companion dog population, more than any single distinct breed of dog [1
]. Compared with crossbred dogs, purebred dogs in Australia are reported to have been more likely chosen for their temperament, they are less likely to have been desexed, and their owners have been found to be more likely to spend more money on their dogs and visit the veterinarian [1
]. Bennett and Rohlf (2007) [21
] postulated that the increased prevalence of UBs in crossbred compared to purebred dogs did not have a genetic basis, but rather reflected differences in the level of commitment between owner groups, and that owners who spend more on their dogs typically are more committed to their care and training [21
The “Crossbred” category in the current study contained dogs of a mixed heritage and “designer breeds” (e.g., cavoodles). The popularity of these first generation crosses in Australia has been growing this decade [1
]. Australian crossbred dogs have been identified as likely to comprise a mix of the popular purebred dogs, namely the kelpies, Maltese, Jack Russell terriers, Staffordshire bull terriers, and cattle dogs [1
]. Aside from the Maltese, these breeds also happen to be those identified by this study as at risk of dying due to a UB related cause (Table 5
). This may reflect the popularity of these breeds and the consequent prevalence of their crosses in Australia.
The breeds identified by the current study as being most at risk of dying due to UB (descending OR > 3, p
-value < 0.05) were as follows: Australian cattle dog; American Staffordshire terrier; miniature fox terrier; bull terrier; dachshund; shar-pei; and the Cavalier King Charles Spaniel. This is contrary to the study conducted at an Australian behaviour referral clinic in Queensland where Australian cattle dogs were at a significantly lower risk of aggression compared to other breeds, perhaps highlighting the effect of a wide range of dog-keeping practices that can be employed across different contexts [13
]. The Queensland study also used mixed breed dogs as their reference breed. The difference in breed popularity between the UK and Australia may explain the international differences in breeds found to be most at risk of dying due to a UB related cause, for example the Australian cattle dog in Australia, and the West Highland white terrier in the UK [37
]. The current study found that American Staffordshire terriers had a much higher risk of death due to a UB related cause (OR 4.69) than Staffordshire bull terriers (OR 2.68), despite similar proportional data regarding types of UB causing death (Figure 2
). This difference may further suggest that different dog keeping practices may influence behaviour, as both breeds are among the ten most popular breeds in Australia [1
], and are morphologically similar in both height and cephalic index [14
Risk of dying from a UB according to breed may also reflect the type of UB. A higher proportion of deaths due to RTA was seen in working breeds such as Australian kelpies, Labrador retrievers, and Australian cattle dogs. It may be that these dogs are at increased risk of RTA due to increased exposure to traffic and allowance of roaming behaviours. Terriers were originally bred to chase, so if this behaviour is transferred from prey to motor vehicles, it follows that they are exposed to increased risk of RTA. The location of the dogs may also play a part, as fencing will vary between suburban and rural locations.
Greyhounds were predisposed to aggression-related behaviours and dog attack among the UB categories for the cause of death. The clinical notes indicated that this was likely due to a high proportion dogs being kept as racers. This could mean that owner tolerance levels for interdog aggression was low as even non-life threatening dog attack injuries (so-called marring) risks ending a racing dog’s career, or that the dogs were frequently exposed to high arousal states whilst kept in groups, which inherently increases the risk of interdog conflict. It is important to note that this study was not designed to differentiate between predatory aggression and other types of aggression. Breed specific legislation also exists within several Australian states that stipulate that all pet and racing greyhounds are to be leashed whilst in public, which may explain the noticeable lack of greyhounds in the RTA category.
The current KC breed group analysis affords a broader examination of breeds that may be at risk of death due to UBs that may not be captured through individual breed analysis due to variations in popularity and availability of certain dog breeds. The breed group forms the larger umbrella under which the breed phenotype allocates both appearance and behaviour, and both qualities are reflected to an extent in the relevant breed standards. The terrier breed group showed the highest prevalence of dogs that had UB related deaths. Although the increased OR was not found to be significant in the current study, Boyd et al. [37
] reported similar results that were significant. Terriers may have a genetically based tendency to be less responsive to anthropogenic stimuli, a trait that may have been a by-product of selecting for dogs that had the ability to work independently in their traditional hunting roles [45
]. This may make them more difficult to manage when highly aroused.
The AKC breed groups at lowest risk of dying from UB were the gun dogs and utility dogs. These were also the AKC breed groups that contained the smallest number of individuals. It is difficult to categorise dogs belonging to the utility group because it is characterised chiefly by breeds that do not fit into the other groups. Views may vary on what does and does not constitute an UB among owners of disparate breed groups. For example, aggression towards strangers at the house can be highly desirable in a guarding breed, and therefore never reported to a primary care practitioner. The working dog group had decreased odds (OR 0.83) of having a UB ascribed as the cause of death compared to non-AKC dogs (Table 4
), despite containing dog breeds that are classically considered inappropriate for suburban life due to high drive and energy levels [46
]. However, working dogs that are in work usually receive high levels of training. Whilst there may be a basis for attributing UB in working dogs to frustration arising from inadequate mental and physical stimulation, the current results encourage a systematic and individualised approach when investigating UB in dogs as many can live comfortably outside of their breeds’ historical occupations.
Bodyweight is a phenotypic metric that varies predictably with breed [9
]. Dogs in the 10–19.9 kg weight category were found at the highest risk of a UB-related death (liberally significant at p
-value = 0.062). Dogs in the terrier breed group generally reach an expected bodyweight of 6–15 kg. In the current study, the prevalence of dogs dying due to a UB related cause decreased as the bodyweight rose (Table 1
), a trend reflective of previous studies that aligned breeds with certain behaviours [9
]. Owners of larger breeds may have less tolerance of UBs as they recognise the damage that a relatively large dog can inflict. In a survey of self-reporting dog bite victims, 70% of bites were by dogs considered medium or large [47
]. As a consequence, breeders of large breeds may practice routine training and socialisation of their dogs and select for temperament more than breeders of smaller breeds, and select for a similar awareness among those who may obtain puppies from them as part of optimising public perception of the breed.
Small dogs are more likely than large dogs to show UB [9
], possibly because their owners tolerate UBs for longer and fail to manage them appropriately. Owners of small dogs may also be more likely to underestimate the amount of exercise a small dog may need, and therefore allow the dog to accrue higher levels of frustration from unspent energy that manifests in hyperexcitability and anxiety-related UBs.
4.3. The Effect of Neutering
The current study showed that compared to entire dogs, neutered dogs had increased odds (OR 2.5) of an UB being ascribed as a cause of death. There are several possible explanations for this. Owners of intact animals may be, or may consider themselves to be, more experienced and able to manage the suite of behaviours exhibited by an entire dog, and are therefore also able to better manage other UBs. The increased level of care provided by owners who bring their animals to be surgically neutered compared to those who do not may come with a higher level of expectation regarding acceptable standards of behaviour [48
]. Additionally, some of the dogs that are euthanased as a result of UB may have had neutering alone administered in a weak attempt to resolve the UB, rather than comprehensive behavioural therapy.
Only 29.7% of the total 4341 dogs captured by this study were neutered. This is much lower than the 81% quoted in the most recent Australian pet survey [1
]. The proportion of neutered dogs that died due to UB was found to be 42.2%. The UK study [37
] reported 76.5% of dogs whose death was attributed to UB were neutered, but neuter status was recorded in only one third of dogs within that study. Relatively low lifetime exposure to gonadal hormones has been shown to increase the frequency of aggression [49
] and anxiety-related behaviours, including territorialism, fear, and reactivity to visitors to the household [18
Preliminary investigations have shown that neutering used as a management method to decrease UBs achieved improvements in less than a third of aggression-related behaviour cases, and fewer than half of owners reported more than 90% improvement on roaming (which is linked to increased incidence of RTAs) [50
]. The current analysis showed that neutered dogs under one year of age had significantly higher odds of dying due to an UB related cause than dogs in the 1.0– < 2.0 and 2.0– ≤ 3.0 age categories (see Table 5
, ‘Combined’). Early age desexing in male dogs has been associated with increased risk of aggression towards family members [49
] and, in both sexes, increasing signs of separation anxiety-related disorders [10
]. However, there is some evidence that the younger the dog is neutered, the lower the reported incidence of the dog exhibiting escape behaviours, which may influence the prevalence of deaths due to RTA [49
Whilst the current study was not designed to follow the dogs that had been neutered as a response to a UB and subsequently survived, the association it has revealed between death due to UB and neuter status has been observed by others [10
]. Dogs neutered for UBs are more likely to have required prior treatment for those UBs [51
], and, in most cases, neutering has not been shown to increase trainability [52
]. Even if neutered animals were aggressive prior to neutering, the higher incidence of aggression in the current study, despite the sizeable proportion of neutered dogs in the sample, indicates that the procedure is not therapeutic for management of UB. This presents a paradox in which neutering on a population level decreases the number of unwanted dogs through indiscriminate breeding, yet may increase the likelihood of individual dogs exhibiting UBs, making them less desirable pets, which renders them just as unwanted [10
4.4. Types of UB and Interventions Offered
Aggression was the most common UB category related to death in dogs of three years of age or under. This is consistent with reports from behavioural clinics [13
], shelters [36
], and owner surveys [31
]. The threat of injury is often the most pressing concern for owners of aggressive dogs, and a repeat episode of aggressive behaviour is often the trigger for owners to euthanase the dog. Aggression and disobedience consistently feature among the top risk factors for owner dissatisfaction and subsequent abandonment or euthanasia [13
]. Whilst most UB categories are distinct, they are strongly correlated and comorbidities are common [54
], for example interpet and interfamily conflict types of UB may also manifest as canine aggression. Dog attacks have an actively aggressive component, for example in disputes over resources, but like many aggressive problems exhibited by dogs they can also be motivated by anxiety, fears, and/or phobias, rather than unprovoked aggression [5
]. Aggression associated with concurrent chronic disease and, most notably, chronic skin disease was also noted in the EPRs in the current study. Dogs with skin allergies have been previously associated with increased problem behaviours and lower trainability scores [55
]. A highly aroused dog can also be motivated to aggress if it enters a negative emotional state [56
Once a dog exceeds an emotional threshold, its owner may misinterpret its overstimulation as disobedience, and incorrectly assign blame for the motivation for the UB. Escape behaviour, destructiveness, and excessive vocalisation may be manifestations of frustration in dogs with unmet behavioural needs [13
], but may also arise in dogs with separation-related distress [28
]. Breed and limited time spent at home by the owner often influence the expression of these UB categories [13
]. Additionally, there may be causal interactions between an animal’s behaviour and its owner’s personality and level of attachment [2
], some of which predispose to inadequate socialisation and a tendency towards aggressive assertiveness towards their dog [57
]. The importance of both learning and genetic influences on behaviour cannot be overstated [18
], as reflected in both owner breed selection and subsequent steps taken to ensure adequate socialisation after acquisition of a new dog. Adequate socialisation is pivotal in ensuring a strong, positive human–animal relationship that is ultimately crucial for many companion animals’ survival [58
The proportion of mortality due to RTA was similar in both the UK (39.0%) [37
] and Australia (41.4%). Death due to RTAs was classified as UB mortalities, as RTAs may result from dogs showing poor recall, limited traffic training, and escape behaviours, which are all associated with UBs [46
]. The current overall high incidence of death due to RTA (Table 3
) has implications for better regulations of dog keeping, such as mandatory leashing of dogs when crossing thoroughfares with high traffic flow.
There were more UB-related deaths attributed to a dog attack in the Australian study (16.8%) than in the UK study (5.9%) [37
], although the proportion of unassisted deaths due to a dog attack were identical (3.5%). It is not possible to state whether this reflects a difference in dog socialisation practices, different rates of euthanasia, or severity of injuries in each case requiring attention at a primary care practice. The authors acknowledge that the current study could not identify the other dog(s) involved in the recorded dog attacks, if it was more than 3 years of age, or whether it died from the attack. The increased prevalence of death due to RTA and a dog attack in Australia could be due to favourable weather patterns encouraging owners to exercise their dog outside, increasing exposure to road traffic and other dogs, whilst inclement weather in the UK predisposes companion dogs to less outdoor activity [59
]. Similarly, purebred dogs in the current study were overrepresented in deaths due to RTA compared to crossbreds (Figure 1
), possibly as a reflection of owners of purebred dogs being more likely to take their dog to public places, such as the beach or park [1
In the current study, an overwhelming majority of dogs that died due to UB(s) either did not have an intervention recorded in the clinical notes, or none was offered. The most popular interventions represent those that demand the least effort (surrendering the animal) as opposed to those requiring most time and money (pharmaceutical therapy and behavioural referral). It is encouraging to note that, proportionally, more behavioural and pharmacological interventions were provided to the current cohort than were reported by Boyd et al. [37
] five years ago. However, there is still scope for considerable improvement. For example, dogs recorded as difficult to handle were frequently reported in the clinical notes as being muzzled but rarely sedated. There is a high risk that the dog may learn from this negative experience to become more reactive at the next veterinary visit, especially without the liberal use of food rewards. The role of the veterinarian at the forefront of animal care is undermined if addressing behaviour is not considered an integral aspect of animal welfare [60
Whilst it is worth noting that these results suggest a higher proportion of overall deaths through euthanasia in Australia (79.6%) than in the UK (76.2%) [37
], no data are available to explain the reasons for this difference. Areas of further investigation could include the effect of cultural attitudes to euthanasia, how often euthanasia was chosen due to financial restraints, or how many owners elected the low-cost option of taking their dog to a shelter for euthanasia. UBs are a common cause of relinquishment to shelters in both countries [31
]. While Australia has a lower estimated dog population than the UK [1
], RSPCA Australia reported an intake of 33,863 dogs in the 2018–2019 financial year [30
] whereas RSPCA UK reported an intake of 10,564 dogs in 2019 [62
]. The higher euthanasia rates in Australia may also reflect factors that increase the frequency of relinquishment, including tolerance of UB, availability of treatment options (such as access to behavioural referral), variance in the average size of the dog or the ways dogs are kept.
For several reasons, the current study is likely to have underestimated the national scale of canine euthanasia due to UB. For example, it does not include data from the considerable number of animals surrendered to and subsequently euthanased at animal shelters due to UBs [36
], or the proportion of animals that are lost or abandoned for reasons related to UBs but never presented to a primary care veterinary clinic. Ten per cent of dogs aged three years or under in this study were confirmed as having been euthanased in the clinical notes without any further explanation as to why the procedure was being performed. Whilst this somewhat detached method of recording death of a companion animal may simply reflect a lack of detail in the clinical records, it may also represent a severed owner–animal bond resulting from a UB.
It is possible that the breed analysis may have been affected by some misclassification of dog breeds when the EPRs were being completed at their respective veterinary practices. Breed and/or pedigree certification is rarely required in order to register an animal as purebred within a veterinary clinic database. Consequently, there is no guarantee that misclassification of dog breed did not occur, be it a purebred dog that has been recorded as another morphologically similar but divergent breed, misclassified as a crossbred, or vice versa. Furthermore, this study did not define crossbred dogs as mixed-breeds because the necessary information was not available to distinguish mixed-breed from true first-generation crosses. This methodology may have diluted the individual breed analysis and affected the prevalence of breed-specific traits discussed. However, the primary aim of the study was to produce a comparable analysis to Boyd et al. [37
], so the authors were obliged to follow suit even though more granularity in the demographic may have been preferred. Again, following the methodology of Boyd et al. [37
], the current study relied on one researcher to manually open records to confirm cases as individual dogs.
Some dog breeds recorded in the Australian EPR did not fall within the breeds as outlined in Boyd et al. [37
], and were categorised as crossbred in the purebred/crossbred analysis. This also subsequently altered the KC breed groupings. The breed categorisation guide used by this study can be viewed in File S2
Bodyweight categories were assigned by recording the last available weight for each dog through evaluation of EPR. However, this value may not always correlate with the final adult weight range of the animal. Dogs that were significantly underweight, obese, or their weight inconsistently recorded may have been inadvertently assigned to an upper or lower weight category.
Finally, whilst the current methodology aimed to replicate that of Boyd et al. [37
], there were two points at which it deviated. Firstly, Boyd et al. [37
] surveyed clinical notes, which spanned a five-year period, whereas data for the current study were only available for just over a four-and-a-half-year period. This temporal shortfall may have been offset by the larger sample population of confirmed patient deaths in this study, 4341 compared to 1574 [37
]. Secondly, data included in Boyd et al.’s [37
] univariable logistic regression included all three categories of dogs that were confirmed as deceased at three years of age or younger (n
= 1574): UB related; non-UB related; and reason for death not specified. The final multivariable logistic regression analysis excluded dogs from the final category where the cause of death was not specified. In contrast, the current study performed both the binary and final multivariable analysis on all three categories.
4.6. Implications for the Future
In keeping with a One Welfare approach [63
], preventative action ultimately seeks to improve not only canine welfare but also the welfare of any involved humans. Identifying risk factors helps to prevent problems from occurring. This is desirable not only because it means less harm comes to the dog and those around it, but behavioural modification takes time and often requires the owners to make lifestyle changes, which can be difficult to implement and sustain [64
]. Preventative action can be taken on every level. Breeders who base selection of breeding stock on behavioural and physical traits should be encouraged. Socialisation of dogs may begin much earlier than the socialisation window reported to commence at 3 weeks of age so arguably, best practice should begin prenatally by ensuring a stress-free birthing environment for the bitch, and, following birth, should involve provision of regular gentling of the newborns [65
]. Previous studies have demonstrated the effectiveness of giving veterinary behaviourists’ advice to puppy owners as a means of reducing UB [66
]. Liberal employment of services such as doggy daycare and dog walkers can normalise dog behaviour and advance dog welfare when the urban dog owner spends most of their time away from home.
Previous surveys have identified that veterinarians fail to adequately address UB concerns raised by owners [67
], which may be reflected in their lack of detailed clinical notes addressing routine behaviour. From the perspective of a veterinary practice, the time spent on behavioural consultations do not currently reap a proportional amount of revenue [68
]. However, veterinary practices are appearing to place increasing emphasis on behaviour, with accreditation programs for minimal stress handling gaining in popularity. Many practices now run puppy behaviour classes or have a close association with a reward-based trainer. There is an increasing awareness that veterinarians should be a trusted resource for assistance with behaviour problems. This requires that veterinary clinical staff feel confident to deal with UBs and are allocated the time needed to thoroughly address the problem. Ensuring graduate veterinarians acquire a basic knowledge of behaviour and learning theory will aid in the prevention of stress and subsequent escalation of UBs in dogs for multiple scenarios [69
]. The latter is even more pertinent now that UBs in dogs have been shown as a covert way of exhibiting pain [70
], further supporting the need for detailed scrutiny of UB reports on a case-by-case basis. Indeed, such studies may help to clarify some of the causal links that are absent from the current report.