Over the last few years a number of studies have identified that large numbers of dogs are failing to cope with aspects of domestic life. For example, the PDSA Animal Wellbeing (PAW) Report (2015) related that owners considered that 19% of dogs were scared of visiting the veterinary practice; in addition, the report included visiting the groomers (7% showed signs of fear) and kennels as environments where dogs display fear. Blackwell et al (2008) suggested that owners considered that 30% of dogs show signs of anxiety when left alone while 80% could be suffering without their owners recognising their distress; that 47% are anxious when meeting other dogs and 15% can show anxiety around the dogs with whom they live. In addition, the same study suggested that 80% of dogs show an undesirable response to strangers and 13% to family members. Another study by Blackwell (2013) showed that 45% of dogs exhibited obvious signs of fear in response to fireworks and other loud noises. The same paper suggested that a dog exhibiting a distress response to one stressor is predisposed to stress in other contexts. Mills and Mills (2003) identified travelling and holidays as a source of distress for a considerable proportion of dogs (23%), and Pluijmakers et al (2010) wrote of the large proportion of under-habituated dogs, that having received inappropriate preparation for their domestic environment, display the generalised condition, neophobia (fear of anything new). When looking at these facts and figures, it is of particular concern that they are predominantly dependent on owner recognition of the stress-related conditions described, yet only approximately 50% of owners have been reported to recognise even the most obvious of stress indicators in their dogs (Mariti et al, 2012); hence, the actual incidence of these problems could be substantially higher.
More recently a British Veterinary Association (BVA) study (2016) found that almost every companion animal veterinary surgeon had been asked to euthanase a healthy dog, with 53% saying that this was not a rare occurrence, and 98% reporting that the most common reason given by owners for requesting euthanasia was a behaviour problem (Kernot, 2016). Of the behaviour problems reported, the majority were associated with aggression, particularly in dogs of less than 3 years of age (O'Neill et al, 2016). As the behaviour of these dogs is motivated by emotional systems that create a physiological and neurological stress response, it becomes imperative to the welfare of dogs that veterinary staff are able to recognise dogs that are experiencing stress. As a consequence of recognition, owners of stressed dogs can be identified and given support that can reduce the incidence of stress-related behaviours that may result in the breakdown of the pet–owner bond and the eventual relinquishment or euthanasia of the dog (Bower, 2002).
Preventing stress in dogs
A dog's natural response to a novel encounter with a stimulus (whatever it is) is one of preparatory arousal (Gray, 1987) — it is this initiation of a stress response that will enable an appropriate response of approach or avoidance. This arousal response involves the physical and neurological adaptations associated with stress (Notari, 2002). Although the average, mature, domestic dog is likely to have encountered a wide range of stimuli, it is the first exposure that dictates future responses. If this first encounter is associated with a state of complete relaxation, no emotional arousal or stress response will result and the dog will habituate to the stimulus, enabling it to remain emotionally neutral on subsequent encounters (Landsberg et al, 2013). Once a dog is in excess of approximately 8 weeks of age, habituation to a stimulus can be difficult to ensure, requiring carefully managed initial encounters. Consequently, it is reasonable to assume that novel stimuli (and those stimuli inappropriately introduced within the breeder's environment) that are met by the 8 week plus dog, both inside and outside the owner's home, will initiate stress through positive or negative emotional systems (Pluijmakers, 2010). These emotional motivations will drive behaviours associated with approach or avoidance — behaviours that once initiated will easily become the behaviours of choice for subsequent exposures to the stimulus (Mills et al, 2013).
Veterinary staff and owners are predominantly interested in behaviours that indicate that a dog is experiencing distress, enabling them to alleviate the dog's exposure to negative welfare conditions. However, it should not be overlooked that a dog's emotional arousal and behavioural motivation to gain access to resources that it considers to be beneficial (e.g. food, play, owners, safety) and that drive behaviours associated with eustress, positive arousal, (e.g. jumping, lunging, scavenging, attention seeking) can also drive behaviours that may be highly inconvenient for owners, members of the public and other animals (Overall, 2013). These behaviours can become particularly problematic if a dog's behavioural attempts to gain access to the resources are thwarted, resulting in frustration related behaviours that can invigorate the dog's initial attempts and that may ultimately result in aggression (Mills et al, 2013).
As a consequence of the above, the first step in preventing stress in dogs is to ensure that it is minimised. An essential part of this process is adequate social and environmental referencing within the breeding environment (between approximately 3 and 8 weeks of age) (Pluijmakers, 2010). This habituation to social and environmental stimuli should continue in the puppy's new home, by identification of likely future stressors and gradual and systematic introduction to those stressors to enable relaxed encounters by 12–16 weeks of age (Bowen and Heath, 2015). From 8 weeks of age, when novel situations are encountered it is advisable to distance the dog to ensure relaxation and to then embark on a gradual habituation to increasing levels of exposure (carefully considering whether for example habituation to the sound of a stimulus may need to be established before the dog is exposed to the visual stimulus), to ensure that the dog has socially appropriate strategies that enable it to cope with future exposure to the stressor (Hunthausen, 2009). This routine will enable behaviours associated with relaxation as opposed to either active avoidance or overt attempts to gain proximity to the stimulus. Such preparation for life in a complex human environment must then be maintained by regular subsequent exposures to stimuli to prevent future stress following dishabituation (Mills et al, 2013).
Despite the above, puppies are not the only canines to find themselves in new homes that are far removed from their early, formative experiences. Clients adopting relinquished dogs will need guidance if they are to understand that:
Consequently, despite the many welfare improvements provided by a new home, such dogs can continue to experience distress in a wide range of circumstances (Neilson, 2009). Owners will require guidance to understand this concept and to initiate remedial habituation programmes to assist their new charges. An extension of this argument is to ask ourselves how this concept affects the welfare of dogs that some rescue centres are bringing in from outside the UK. Both prospective owners and rescue staff will benefit from access to veterinary staff who engage in pragmatic discussions regarding how moves from an environment in which the dog has developed some competency can be enhanced by ‘rescue’ to a different country and lifestyle. If originally strays, many of these dogs may benefit more from charities concentrating their finances and efforts on capture, neuter, vaccinate and release programmes.
Often under recognised is the distress experienced by dogs when left ‘home alone’ (Pluijmaker, 2010). As a social species the dog has an expectation of social companionship (Bowen and Heath, 2005). The puppy's mother reinforces the puppy's emotional ‘care needing’ circuitry through her attention. Many puppies are either removed from their mothers before adequate independence of this attachment figure has been developed, or, experience separation in a manner that is emotionally traumatic for the puppy (e.g. transportation for sale in puppy farms) (Pluijmaker, 2010). This can result in a puppy that has an enhanced need for a secure social base to assist its coping mechanisms. Trauma to older dogs can have the same effect and in these situations dogs can develop rapid and strong requirements for proximity to an individual (canine or human) that is accessible in its new environment (Horwitz, 2009). Separation from this secure base leaves the dog in an environment within which it has a reduced level of competency and an impeded concept of coping, leading to distress (Landsberg, 2013). The distress is initiated by activation of the emotional neural circuitry associated with the dog's panic/grief system (Merrill, 2001). This situation can arise purely due to the loss of access to a secure social base (even if they have only moved into an adjoining room), or the need for proximity to a secure social base may arise due to exposure to distress inducing incidents being associated with periods of owner absence (e.g. being exposed to novel, sudden or loud noises) (Pluijmaker, 2010). In addition, coping can fail during owner absence due to increased anxieties associated with old age or illness (Mills et al, 2013). Consequently, all dogs need early preparation and ongoing support for periods of social isolation. As it is inevitable that dogs will need to spend time alone, prevention of the delayed development of ‘home alone’ problems will be closely linked to the dog's level of habituation, and subsequent competence, with the environment in and around its home (Pluijmakers 2010).
Preventing the development of a stress response on exposure to a stimulus (stressor) is not the sole responsibility of the dog's owner. When the dog is within the practice premises, it is also the responsibility of the practice staff to ensure that both owner and colleagues understand that every interaction (with animate or inanimate stimuli) within the building is a learning opportunity which will dictate the dog's future response on subsequent exposure (Hunthausen, 2009). Whenever possible, procedures should be carried out in a manner that enables habituation to the situation — whether the dog is entering for a first puppy vaccination or as a regular adult client; whether in the reception area or experiencing hospitalisation. Consequently, the practice's responsibility to enable habituation does not stop with an explanation of the socialisation process to a new puppy owner, but extends to all dogs joining the practice and throughout their period as practice clients (Bower 2002). When procedures cannot be carried out with sufficient sensitivity to create habituation, an immediate assessment should occur regarding how the team should proceed. This should determine whether a combination of heavily rewarded owner behavioural guidance and staff providing rewards will over-shadow the dog's likely distress. If this is deemed unlikely, chemical agents should be immediately used to ensure that a negative association is not made with the social or physical environment (Yin, 2009).
Alleviating stress in dogs
With 80% of dogs showing distress while alone or in the presence of strangers, and nearly 50% distressed in the presence of loud noises or other dogs (see above), it is clear to the reader that the majority of dogs do not receive adequate preparation for the environments in which they live, so the next stage in improving the welfare of the stressed dog is to identify the affected animal (Shepherd, 2009). To do so, veterinary staff require familiarity with the signs of canine stress. Once spotted, such signs should be pointed out to owners with considerable sensitivity — no owner will thank you for suggesting that their home and care has resulted in the depletion of their dog's welfare! But despite the potential pitfalls of this responsibility, it is just that, a professional and legal responsibility (Animal Welfare Act, 2006; WSAVA, 2015). Without such professional intervention, it is easy for owners to assume that, with repeated exposure to a stimulus, their dog will eventually ‘get used to it’. This is far from the case, as repeated exposure will increase sensitivity to the stimulus and may also lead to generalisation of the distress-related behavioural response to predictive stimuli (Palestrini, 2009). Such sensitisation will not only increase the number of environments in which the behaviour is expressed, but it will also enhance the level of behavioural expression (Bowen and Heath, 2005). Table 1 is intended to assist with the recognition of canine signals associated with distress in dogs (Hargrave, 2015).
| Well known signs of canine stress | More subtle signs of canine stress |
|---|---|
| Turning body away | Sitting close to owners |
| Walking away from stressor | Pawing of owners |
| Yawing | Turning head away from stressor |
| Blinking | Staring at an item (e.g. the second hand on a clock or a spot on a wall) |
| Nose licking | Raised fore leg |
| Staring | Lying down |
| Stiffening | Ears back and/or flattened |
| Tail lowered or tucked | Creeping — slow deliberate movement |
| Scratching body | Body arching away |
| Full body shake | Rolling over to expose undercarriage |
| Ignoring owner requests for co-operation or responding in a distracted manner | Sniffing ground or engaging in a seemingly meaningless displacement behaviour |
| Shaking as though following a bath or swim | Shedding hair |
| Showing the whites of eyes or closing eyes | Higher tail carriage, tail vibrating in short, sharp bursts |
| Raised hackles | Crouching |
| Scanning visual field by rapidly looking from side to side | Increased sensitivity to other stimuli |
| Muscle tension | Sweaty paws |
| Trembling | Moving in slow motion |
| Inappetence for treats or snatching treats | Panting |
| Involuntary urination or defecation | Excessive salivation |
| Mounting behaviour | Biting/chewing of lead or owner's hands/clothing |
| Lunging | Furrowed brow/raised eyebrows |
| Barking | Urine marking |
| Growling | Tightened muzzle |
| Snapping | Appearing sleepy/tired |
| Biting | Ducking, cowering or backing away to avoid contact from hands |
The dog exhibiting behaviours associated with eustress, driving behaviours that enhance access to a resource (such as jumping up at or pulling/lunging towards people, other dogs or items that the dog desires), however, is also exhibiting a degree of emotional arousal (Mills et al, 2013) and subsequent stress response, that interferes with the dog's capacity to pay attention to guidance from owners and veterinary staff. Although every dog deserves pleasure in its life, there are situations where it is important for the dog to remain calm, relaxed and biddable (Figure 1). Hence such dogs should also be identified and owners advised regarding habituation to environments, thereby enhancing owner control and patient competence. In addition to habituation, or if habituation is impossible, an alternative, yet socially appropriate behaviour should be taught that is initiated by proximity of the stimulus — this behaviour should then be associated with reward so that the dog's emotional drive is satisfied (Yin, 2009). This is particularly important in social environments as failure of these eustress driven behaviours will result in frustration that will either invigorate and enhance the dog's behaviour (further reducing the dog's capacity for compliance with owner or veterinary staff) or if frustration continues (or if the dog associates the situation with a prediction of failure) aggression may follow (Mills et al, 2013).
Spotting the dog that requires remedial support with periods of isolation from its owner can be tricky. When the panic/grief emotional system is activated, the associated behavioural responses associated with the accompanying distress seems to divide dogs into two groups — active and passive responders (Mills et al, 2013). Some dogs will initiate active behaviours intended to bring about their reuniting with their social base — vocalisation, digging, chewing (Mills et al, 2013) (and if contained in for example a crate, other active attempts at escape). Less active responders may pace and their distress may become sufficiently intense as to lead to house soiling (Landsberg, 2013). However, other, more passive individuals may simply curl up in a dog bed or alternative place of relative safety and become behaviourally inhibited (Pluijmakers, 2010) — behaviours that owners can easily misinterpret as relaxation and rest. Studies suggest that up to 30% of the domestic dog population could fall into the active responder category (Blackwell et al, 2008), while up to 80% of the canine population may be passive responders (Pluijmakers, 2010), statistics that place a huge responsibility on the veterinary profession regarding the education of owners to be more proactive about identifying and alleviating this form of emotional suffering.
First aid for stressed dogs
The necessary remedial habituation or desensitisation and counter-conditioning to stimuli that may be required in response to stress inducing stimuli, will take time to accomplish (Neilson, 2009). Consequently, owners, veterinary staff and dogs require immediate solutions to stress inducing situations.
Whether in the veterinary practice or in a domestic environment, the most immediate solution is to stop exposing the dog to the problem and enable the dog to remove itself (or arrange for the stimulus to be removed) to a distance at which the dog can relax (Yin, 2009). Physical signals of relaxation do not ensure that neurochemical homeostasis has been created, stress-related neurochemicals take many hours to degrade and the dog will remain chemically primed for arousal-related behaviours for some time (Mills et al, 2013). Consequently, it is not ‘safe’ to merely resume an activity once the dog ‘looks’ relaxed. In the veterinary practice, this will involve re-assessing the need for immediacy of the procedure. If, for example, a dog has an obvious site of pain, but a specific diagnosis of the exact point or cause is not immediately essential to the welfare of the dog, effective analgesia can be prescribed along with sedatives. This would enable the dog to return in a more relaxed state and at a quieter time, for a more thorough examination the following day (Yin, 2009). If the procedure is absolutely necessary, strategies that enable the dog to continue in comfort will need to be initiated. In or outside the home, owners need to remove the dog to a safe distance and once it can concentrate on an alternative activity, they can organise the environment to ensure that no further exposure occurs (e.g. the dog that has lunged at one dog will not be relaxed on a subsequent exposure to another dog later in a walk).
When explaining stress-reducing strategies to owners, it is important to ensure that owners understand how easily dogs can become increasingly sensitised to stimuli on subsequent exposures and hence, how behaviours can develop from the mildly avoidant to overt distance creation (Palestrini, 2009) that can become frightening for both owners and onlookers — with the accompanying danger of transgression of the Dangerous Dogs legislation. Along with such advice, practice staff should ensure that owners understand that it is therefore counter-productive to attempt to improve a dog's anti-social behaviour to other dogs by forcing it to encounter them in the confines of the training class environment.
Whether in the practice, being exercised or in the home, the distressed dog requires an enhanced concept of coping and safety (Mills et al, 2013). In the practice this may be achieved through flexible use of consultation times and areas to ensure that distressed dogs are not forced to encounter stressors in confined spaces — enhancing their concept of choice (Figure 2). When this is combined with sensitive handling techniques that avoid inadvertent social threats, it is often sufficient to enable a consultation to occur (Yin, 2009). When exercised, use of a loose lead or long line and ensuring access only to environments that avoid known stressors can enable both dog and owner to relax and enjoy time spent outside the home. Within the home, avoidance of inadvertent threats (e.g. accidentally cornering a dog in a room or chair, staring at or leaning over the dog), owner observation of the dog's social signalling and the provision of a ‘safe place’ can enable an owner to gently encourage a distressed dog to distance itself from stressors (Mills et al, 2013).
In both the practice, exercise and home environments, as long as a dog is used to taking guidance from its owner regarding co-operative behaviours, mildly distressed dogs can be encouraged to concentrate on reward-based behaviours while being moved away from stressors (Yin, 2009). For necessary but relatively quick veterinary procedures, this technique accompanied by high salary scale rewards, e.g. relatively soft, fish or liver-based treats (must be soft as anxiety/fear may reduce saliva production and need to be tasty to overcome the inappetance associated with fear/anxiety-related nausea), may be used to over-shadow negative events. In addition, opportunities to play with valued toys, a puzzle feeder or to engage in scent-based games may be useful. However, whether in the practice or not, safety considerations may require the use of appropriately introduced and designed muzzles (remembering that the dog will require to pant freely and take rewards) and aids such as leads for guiding dogs.
Sedation and anaesthesia is underused in veterinary practice as a way of ensuring that animals do not suffer distress during examinations and routine procedures (Yin, 2009). Yet every encounter that practice staff have with a distressed dog will inform the dog regarding the behaviours that it will need to use on subsequent exposure to the veterinary environment — even if the subsequent procedure is not physically aversive (Yin, 2009). Consequently, every time a colleague makes a decision to continue a procedure with a distressed dog without alleviating the dog's distress, that colleague dictates that manner in which the dog will respond to practice staff on future occasions. If in doubt, sedate or anaesthetise.
Canine patients can benefit from the use of a synthetic analogue of dog appeasing pheromone to reduce distress in the veterinary environment (Mills et al, 2006), and the same product can reduce the level of distress experienced in a variety of domestic circumstances (Shepherd and Mills, 2003). There are also a range of nutraceutical products available to support the distressed dog. Although it is helpful for veterinary staff to explain the role of such products; it is important that owners are not given the impression that use of such products will provide a ‘stand-alone’ cure for distress.
The above are, however, short-term quick fixes for use in emergencies. Ultimately, when stressors are identified, if an animal is mildly affected, then remedial habituation can be effective. However, in all other cases, families should be guided towards assistance in undertaking a structured and supported desensitisation and counter-conditioning programme to the problem stressors (Notari, 2002).
Conclusion
Kendal Shepherd's ‘Ladder of Aggression’ (2009), placing canine social signals in an order of likely escalation towards overt aggression, is a tool that is familiar to most veterinary staff. However, the dog shows a far wider range of subtle communication when indicating a state of stress but these signals are often under recognised (Yin, 2009). The ‘facts and figures’ quoted in the introduction to this article suggest that a substantial proportion of dogs suffer from daily encounters with stress. However, there are a large number of dogs that remain behaviourally inhibited while experiencing distress, entering a state of learned helplessness (Mills et al, 2013), yet their distress remains unrecognised by owners and many veterinary staff. These animals are often assumed to be relaxed and compliant, leading to levels of exposure to stressors that far exceed their capacity to cope and resulting in a severe, but unrecognised, depletion in welfare.
As exposure to stressors is an inevitable part of living in a complex human environment (Mills et al, 2013) and as studies have indicated that considerable proportions of the canine population exhibit obvious signs of distress in a wide range of environments, the prevention and alleviation of stress should form part of the holistic approach to canine welfare that is offered by every veterinary practice (Landsberg et al, 2013). The veterinary professional should consider it their duty to assume that measures are required to alleviate stress, rather than assuming that a dog in their care will cope.