Elsevier

Physiology & Behavior

Volume 168, 1 January 2017, Pages 122-127
Physiology & Behavior

Reduced heart rate variability in pet dogs affected by anxiety-related behaviour problems

https://doi.org/10.1016/j.physbeh.2016.11.003Get rights and content

Highlights

  • Link between canine behaviour problems and HRV discovered.

  • Aimed to test if HRV was related to a range of anxiety-related behaviour problems.

  • Pet dogs either affected or unaffected by behaviour problems were recruited.

  • Affected dogs had reduced measures of HRV compared to unaffected.

  • Effect of behaviour problems on HRV not explained by reactivity or cortisol.

Abstract

We present here the first evidence of correlation between canine anxiety-related behavioural problems and heart rate variability (HRV). HRV is known to be related to a range of mental disorders in humans; however this has not been explored in dogs. Behavioural problems in dogs can result in suffering, property destruction and human injury. Dog behaviour problems were assessed by owner questionnaire and the extreme high and low scoring dogs were recruited into either affected (n = 10) or unaffected (n = 20) groups. HRV was assessed in dogs at their homes, while being held in lateral recumbency for 5 min using manual restraint. Salivary cortisol samples were taken before and after HRV testing. Dogs were assessed as either being reactive to the procedure (barking, growling, struggling or shaking) or unreactive. There was no effect of reactivity or behaviour problems on salivary cortisol levels at baseline or in response to the treatment. There was a significant effect of reactivity on HR (F1,26 = 5.54; P = 0.026), and no effect of behaviour problems (F1,26 = 1.07; P = 0.311). There was no effect of reactivity on any of the HRV measures. The presence of behaviour problems had a significant effect on a range of measures of HRV, with unaffected dogs having higher standard deviation of RR intervals (F1,26 = 6.39; P = 0.018), higher high frequency spectrum (F1,26 = 5.23; P = 0.031) and higher low frequency spectrum (F1,26 = 9.25; P = 0.005) power. There was no effect of behaviour problems on very low frequency spectrum power (F1,26 = 1.40; P = 0.248). Together these results provide evidence for a fundamental physiological difference between dogs affected or unaffected with behaviour problems. This study provides evidence for further investigation into the role of HRV in the pathophysiology of canine anxiety-related behaviour problems.

Introduction

There are a range of serious anxiety-related behaviour problems that exist in dogs, including noise phobias, separation anxiety and aggression [28]. These behaviour problems can each lead to a range of serious consequences and multiple diagnoses often exist concurrently in affected dogs [3]. The effect of these problems on society can be devastating. For example, dog bites are a common cause of injury to people and other dogs [30], [44], while separation anxiety and noise phobias can cause extensive damage to property and the dog itself [7], [35]. Behaviour problems can also disrupt the human-animal bond and so are a common cause of abandonment at shelters [26]. Unfortunately, canine behaviour problems are also a common cause of euthanasia at animal shelters [32]. Importantly, many canine behaviour problems are a sign of suffering in the dog itself due to fear and anxiety [28]. Diagnosis of anxiety-related behaviour problems in dogs can be achieved by referral to a veterinary behaviourist [28], which relies heavily on owner reported behaviours. Alternatively, owner questionnaires have been validated as an accurate method of assessing the severity of behaviour problems in a dog [17]. Without the information provided by the owner, temperament testing of dogs can assess behavioural reactions in specific situations however this does not have a high degree of accuracy of predicting behaviour problems [4], [9]. Moreover, owner perception of their own dogs' behaviour is not perfect, as even between members of the same household there can be significant disagreement on behavioural questionnaires [19]. Due to the inability to question dogs on their own feelings directly, as would be performed for human patients [1], alternative objective measures are lacking. An easily measurable physiological correlate to behaviour problems in dogs does not exist, yet could have many uses for diagnosis, breeding or further research into this field.

One potential correlate between dog behavioural problems and their physiology is the heart rate variability (HRV). The HRV of an animal is linked to its ability to regulate emotion, and is determined by the ability of the autonomic nervous system to dynamically adjust its parasympathetic and sympathetic response to the environment [2], [41]. The regulation of emotion is important for appropriate responses to stressors, and is believed to be disrupted in people with anxiety disorders such as panic disorder and depression [22], [27], [39]. In each case, correlations between the heart rate variability and the disorder are negative, with higher variability in the unaffected individuals as would be expected with superior regulation of emotion. For example, human depression is associated with a reduction in high-frequency HRV, with a greater reduction in more severely affected individuals [22]. Given the differences in HRV between people with and without these disorders, we hypothesised that dogs with or without behaviour problems would demonstrate similar differences.

Heart rate variability has been used as a measure of stress and welfare in a range of animal species, however its use for measuring welfare specifically in dogs has not been validated [38]. The use of HRV to investigate the effect of a schedule of human interaction on shelter dogs discovered small differences between dogs that did or did not receive this enrichment [6]. A study by Gácsi et al. [14] found that a direct threatening approach by an unfamiliar person elicited an increase in HR and a decrease in HRV in behaviourally reactive dogs in the absence of their owner [14]. The context of the measurement of these behaviours is also of significance. The two studies mentioned above show that HRV may be reduced during some stressful situations and in reactive dogs during a fear-eliciting context [14], [38]. While both these studies have explored the direct correlation between current behaviour and HRV, only one study (to our knowledge) has compared HRV with the reported behaviour of the dog in an alternative context [42]. We determined this association by measuring the HRV of greyhounds during blood donation, which we found to be correlated to aggressive behaviour in a subsequent assessment [42]. The current study aimed to build on this finding, by correlating HRV and a range of behaviour problems in pet dogs. A difference in context between the measurement of HRV and the reported behaviour problems is important as it suggests that the HRV may be related to a trait within the dog rather than a visceral reaction occurring only in the presence of the triggering stimulus.

Section snippets

Subjects

The subjects were 34 Australian owned pet dogs that were recruited as past participants from a previous (currently unpublished) study performed by these authors. They were selected from a pool of 161 dog owners, who had previously been screened by email as having dogs that might fit into the “affected” or “unaffected” groups mentioned below. All dogs were aged between 1.5 and 9 years old, male and female neutered, and from a range of breeds within the United Kennel Club “Gun Dog”, “Companion”

Results

Three dogs were excluded (two unaffected, one affected) due to excessive movement during the manual restraint leading to poor quality HRV readings with over 20% artefact. One dog (affected) was excluded because it displayed excessive struggling during the manual restraint which led to the procedure being aborted after 30 s. The remaining 30 dogs (20 unaffected, 10 affected) with valid measurements were used for this study. Analysis of the signalment of the two groups (Table 1) did not find any

Discussion

The present study has found that dogs affected by anxiety-related behaviour problems have reduced HRV during manual restraint when compared to unaffected dogs. This finding occurs despite the procedure being insufficiently stressful to increase salivary cortisol levels in either group of dogs. Furthermore, the differences in HRV cannot be explained by the degree of stress that the procedure placed on the dogs as it did not relate to behavioural reactivity. This is an important finding, as it

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