Although it is necessary for the health and welfare of companion dogs, veterinary care has been associated with signs of stress and fear in some dogs. The authors of a recent review1 estimated that 10% to 78% of dogs display signs of fear in these circumstances. In an early study2 to assess the apparent willingness of dogs to enter a veterinary clinic, 279 of 462 (60%) dogs displayed signs of apprehension and had submissive postures, and 81 of 462 (18%) had fear-biting behaviors. A study3 of dogs in the waiting room of a veterinary clinic found that 24 of 45 (53%) dogs displayed ≥ 4 behavioral signs of fear. In another investigation,4 106 of 135 (79%) dogs were categorized as fearful across various components of a veterinary examination, with 67 (50%) appearing unwilling to enter the examination room and 105 (78%) displaying reduced posture (ie, standing with the head low; ears held sideways, down, or pinned back; and tail lowered or tucked between bent hind legs) when on an examination table.
Fear among dogs in a veterinary setting can impair patient welfare, place veterinary staff safety at risk,5,6 and lead to incomplete and inaccurate examinations and diagnostic testing.7–9 Results of a 2011 study10 of 2,188 US dog and cat owners suggest that concerns about fear and stress have contributed to a decline in veterinary visits, with 22% of responding dog owners indicating they would bring their dog to the veterinarian more often if the dog was less stressed. Fearful behavior among dogs in veterinary settings likely results from negative experiences during previous visits,4 handling in a manner that is unfamiliar or makes the dog uncomfortable, and exposure to various unfamiliar stimuli in the clinic environment. In addition, fear in dogs might arise from or be exacerbated by separation of the dog from its owner. Whereas routine examinations are generally conducted in an examination room with an owner present, it is common practice for animals to be moved to treatment areas for some procedures, including examinations, if warranted by patient behavior. Participants (including researchers and veterinarians with expertise in animal welfare) in a survey11 published in 2016 indicated that separation from owners was a key factor likely to impact animal welfare during veterinary visits.
Positive interactions between dogs and their owners have been associated with indicators of reduced stress levels, including the release of oxytocin and dopamine and reduced blood pressure.12 For example, dogs release oxytocin during social interactions that involve mutual gazing (prolonged eye contact) with their owners or familiar people13 and during reunions after time spent apart.14 Human-dog interactions have also been found to reduce behavioral and physiologic signs of fear in dogs during an aversive or stressful event. For instance, during exposure of dogs to a tone-shock sequence, petting has been found to reduce dogs’ heart rates, altering a previously established conditioned tachycardic response.15 Moreover, when introduced to a novel shelter environment, dogs had lower cortisol levels16–18 and reduced behavioral signs of stress (eg, vocalizing and panting)17,18 during interactions with people who petted them or engaged them in play. The potential buffering effects of dog owners in stressful situations are further supported by research that suggests owners act as a secure base for their dogs. During a modified Ainsworth Strange Situation Test, dogs in 1 study19 were more likely to display social play and exploration behavior in the presence (vs absence) of their owners, where there was more whining and orientation toward the door when left alone. Thus, previous research suggests that owner presence can alleviate signs of fear in dogs during common aversive situations.
Some dogs have separation-related behaviors when their owners are absent. Signs of separation distress commonly include inappropriate elimination, destructiveness, hypersalivation, and vocalization.20,21 Authors of a 2008 review article21 cited market research surveys suggesting that 14% to 17% of dogs in the United States have signs of separation anxiety, and in a report published in 2016, 17.2% of surveyed dog owners in Finland (with > 3,200 responses) reported their dog had separation anxiety.22 Furthermore, when dogs are separated from their owners in general, they can have physical signs of stress such as decreased surface temperature of the extremities.23 Thus, fear and stress in dogs might be increased by separation from their owners in the clinical setting, particularly for animals with preexisting separation-related issues.
The strength of the owner-dog relationship has the potential to impact the influence owners have on the fear their dogs can experience during a veterinary visit. For example, owners with greater emotional attachment to their dogs (as assessed by the veterinarian) were found to be more successful in calming their dogs than those considered to show less emotional attachment.24 Furthermore, during veterinary examination, dogs had a lower heart rate and made fewer escape attempts when the owner was present and able to make physical contact with them, compared with results when the owner was present but not interacting with the dog.25 Thus, owner interactions seem to reduce the signs of stress in dogs in this context; however, to the authors’ knowledge, no studies have been published that assess the influence of owner absence on stress-related variables during veterinary examination.
The objective of the study reported here was to investigate the effect of owner presence on behavioral and physiologic fear-related responses in dogs during a routine veterinary examination. We hypothesized that owner presence in the examination room would reduce behavioral and physiologic signs associated with fear in dogs during a routine veterinary examination.
Materials and Methods
Study recruitment and dogs
A convenience sample of owners (≥ 18 years of age) of privately owned companion dogs were invited to enroll their dogs in the randomized, controlled study. Recruitment was performed by emailing individuals who had previously consented to be contacted for future dog behavior studies. We explained to the owners that our objective was to examine whether dogs’ responses to a veterinary physical examination are influenced by owner presence and informed them that we would randomly assign them to a particular treatment group.
Owners were asked to complete a preliminary recruitment questionnaire to ensure eligibility. The form included a brief description of the study purpose, procedures that would be used, and information about confidentiality and the voluntary nature of participation. In addition to questions related to the dog's age, breed, and health status, owners were also asked to report whether their dog had previously displayed aggression at the veterinary clinic and to rank their dog's degree of fearfulness on a scale from 0 (no fear) to 4 (extreme fear) in the following situations: when the dog is approached directly in the examination room, when the dog is examined on the ground, and when the dog enters the examination room. Descriptive examples of fearful behaviors for each score on the 5-point scale were provided.
To be selected for participation, dogs were required to be healthy, up-to-date on vaccinations, and between 1 and 8 years of age; owners were allowed to enroll multiple dogs in the study. The age restriction was intended to prevent senior-related confounding factors.26 Dogs were not eligible to participate if owners indicated in the preliminary recruitment questionnaire that they had previously shown aggressive behavior or were extremely fearful (ie, a score of 4) in a veterinary clinic. These dogs were excluded to reduce the potential risk of bite injury to the investigators and possible adverse effects on the welfare of highly fearful dogs. The study was approved by the University of Guelph Animal Care Committee and conformed to all federal and provincial guidelines governing the use of animals in research (protocol No. 3780). The need for Institutional Review Board approval for owner participation was waived.
Procedures
Experiments were conducted in an examination room of Smith Lane Animal Hospital at the University of Guelph Ontario Veterinary College. This allowed study dogs to be exposed to the veterinary clinic environment and stimuli commonly encountered in the clinical setting. Testing was conducted by 1 author (ACS) and a dog-handling assistant; both were female and wore white laboratory coats throughout testing. All dogs underwent a standardized individual examination with or without their owner present during the procedure. The dogs were allocated to treatment groups (owner present or owner absent) in a randomized block design with sex and age of the dogs balanced between the 2 groups; randomization software was not used. Owner sex could not be balanced between groups owing to the nature of the recruitment methods. Duration of testing was approximately 15 minutes, and each test was video recorded for later analysis.
Owners arrived with their leashed dogs at the main reception area where the handling assistant explained the protocol to the dog owner. During this time, the assistant interacted with each dog by speaking softly, offering treats, and petting the dog when appropriate. After this initial introduction, the owner and the dog were taken to an examination room (3.56 × 2.97 m), the doors to the room were closed, and the owner was instructed to drop the leash. The dog was allowed to acclimate to the room for 1 minute, and during this time, the owner signed the consent form while the investigator and handler stood still and off to the side without interacting directly with the dog. After the acclimation period, the owner either remained in the room or was asked to leave, depending on the dog's treatment group assignment.
The 7-minute standardized physical examination was performed as described in further detail elsewhere.27 Duration of the examination was standardized by use of a timer. The standardized examination procedure allowed for direct and unbiased comparisons between treatments. The examination was performed with the dog standing on the examination room floor; it began when the dog placed all of its feet on a nonslip rubber mat (0.9 × 1.2 m). For the owner-present group, the owner was asked to walk the dog onto the mat, then to sit on a chair placed immediately beside the dog (with the edge of the chair 0.22 m away from the mat). Dogs in the owner-absent group were walked onto the mat by the investigator. The investigator conducted the examination in a predetermined and standardized order, examining the dog's eyes and ears and lifting the dog's lips to perform a modified mouth check (head examination), palpating the mandibular and prescapular lymph nodes (lymph node palpation), and palpating the abdomen before checking for abnormal masses and evaluating body condition by moving hands over the dog's body (body palpation). Physiologic variables were then assessed by the investigator while the handler minimally held the dog in place (regardless of owner presence or absence). This included measurement of axillary temperature with a digital thermometera for approximately 1 minute until the device made a beeping sound, followed by determination of heart rate by auscultation with a stethoscope (beats per minute; measured as count/15 s × 4). Respiratory rate was assessed last by visual inspection (breaths per minute; measured as count/15 s × 4). Axillary rather than rectal temperature was assessed to prevent potential stress associated with the latter procedure; this form of temperature assessment is commonly used for wellness examinations at the facility where the study was performed, and axillary temperature measures have been shown to be moderately correlated with rectal temperature in healthy dogs.28 If a dog showed signs of excessive discomfort or had aggressive behavior (eg, vigorous avoidance attempts or growling and baring the teeth), the examination was modified or terminated. Modifications to the examination procedure involved progressing through the steps more slowly and allowing the dog to assume the position that seemed to be preferred or most comfortable. Investigators offered occasional verbal encouragement to dogs but refrained from speaking to the owners.
During the examination for dogs in the owner-present group, dog owners were instructed to remain sitting on the chair while holding the end of the leash. They were asked to refrain from assisting with any handling and to withhold any comments or questions for the investigators until the end of the examination to maintain standardization and control of the examination. Owners remained positioned immediately beside their dog and were permitted to behave as naturally as possible by petting and talking to the dog as they normally would. The examination and evaluation period ended when the 7-minute timer sounded.
Data collection
All testing was video recorded using 2 video cameras,b with one positioned in front of the dog (1.1 m away from mat) and the other raised and pointed downward to image the caudal and dorsal aspects of the dog. An ethogram developed for a previous study27 was used to code each dog's posture, aversion behaviors, and other observable signs or behaviors. Posture was assessed as either neutral (with the head held high, ears forward, and tail high or positioned typically for the breed) or reduced (with the head low; ears held sideways, down, or pinned back; and tail lowered or tucked between bent hind legs, whether still or wagging). Aversion behaviors, when present, were categorized as avoidance (moving or manipulating the head or body away from the investigator or handler) or escape (stepping off the mat or attempting to step off the mat). Other behaviors or signs included shaking of the body (partial rotation of the head and body back and forth about the central axis with shaking of the fur), licking of the upper lip with the tongue, yawning, obvious trembling or shivering, and vocalizing (barking, growling, whining, or yelping). These measures have been widely cited as signs of fear and stress in dogs in previous literature.29–34
A third individual who was blinded to the study hypothesis performed behavior scoring by viewing the video-recorded examinations in a manually randomized order with specialized computer software.c All behaviors were scored during each phase of the examination (head examination, lymph node palpation, body palpation, temperature measurement, heart rate determination, and respiratory rate assessment), and the blinded individual annotated the start and end times for each of the examination phases for analysis purposes. Continuous sampling was used to score the frequency of aversion and other behaviors. Frequencies were used to report measures other than posture as rates (the number of behavior events observed per minute) during each phase of the examination. Neutral and reduced postures were scored as present or absent during each phase of the examination. To account for different postures being displayed during an examination phase, reduced posture was scored as present if it occurred at any time during the relevant phase. One of the investigators (ACS) scored video-recorded sessions for owner contact with the dog for the owner-present group. Owner contact included physical (owner-initiated contact by petting or touching the dog) and verbal (speaking directly to the dog) interactions and was assessed as present or absent at any time during the examination period.
Physiologic changes that are widely known to occur during stress in mammals (increased temperature, respiratory rate, and heart rate)35,36 and have previously been associated with situations involving fear in dogs7,37,38 were assessed by the investigators during individual phases of the examination as described. Trembling or shivering were also recorded during the examination and noted as present or absent at any time during the examination period. This feature was assessed by the investigators at the time of the examination because the response could not be properly assessed from the video recordings.
Statistical analysis
For behavioral measures, generalized mixed models were used to assess the effects of owner presence, examination phase, sex of the dog, and age of the dog, with the dog as a random effect or repeated measure, depending on which resulted in the highest-quality model according to Akaike information criteria. Main effects in each model were identified through manual backward selection, with variables having a P value < 0.05 retained in the model. After main effects were finalized, all possible interactions were tested, and any main effect involved in a significant interaction was retained in the model, regardless of its significance level. For all statistical models, normality was assessed, and model assumptions were adequately met. Residuals were assessed to identify any outliers, which were removed if this improved the model fit. For lip licking, yawning, vocalizing, avoidance behavior, and escape behavior, Poisson distributions were used for analysis with the duration of each examination phase included as the offset. For posture, binary logistic distributions were used. Body shaking and trembling were not analyzed because of the small number of dogs that had the behavior or sign.
For physiologic measures (temperature, heart rate, and respiratory rate), the effect of examination phase could not be assessed because a single measurement was taken during the relevant phase. A general linear model was used to assess the effects of owner presence, sex of the dog, and age of the dog on these measures with the same model-building methods and model diagnostics as for the mixed models. For respiratory rate, the model was simplified to a Student t test on removal of nonsignificant variables.
Generalized mixed models were also used to assess the effects of owner contact (at levels of physical, verbal, both physical and verbal, no contact [when the owner was present], or not applicable [when the owner was absent]) with the dog as a random effect or repeated measure, depending on the Akaike information criterion as previously described. Pairwise comparisons were used to detect differences between the forms of contact. Owing to limited degrees of freedom, when analyzing the effects of owner contact on dog responses, we were only able to assess yawning and lip licking with Poisson distributions, posture with binary logistic distributions, and physiologic measures with general linear models.
All analyses were performed with statistical software.d Data were reported as mean ± SD with 95% CIs. Values of P < 0.05 were considered significant.
Results
Thirty-two dogs (16 in the owner-present group and 16 in the owner-absent group) with 28 dog owners completed the study. One dog that had initially been enrolled in the owner-present group was removed because of a high number of escape attempts that prevented completion of the examination. Four owners had multiple dogs participate in the study; 1 female owner with 3 dogs was present for the examination of 2 dogs, 2 female owners with 2 dogs each were present for the examination of 1 dog, and 1 male owner was present for the examination of 2 dogs. All dogs were examined in a standing position, except that 1 dog in the owner-present group assumed recumbency, and the examination was completed with the dog in that position.
The owner-absent group included 4 mixed-breed dogs, 2 Chihuahuas, 2 Pembroke Welsh Corgis, and 1 each of the following breeds: Shih Tzu, Labrador Retriever, Airedale Terrier, Löwchen, Australian Shepherd, Pug, Dachshund, and Bulldog. There were 10 males and 6 females (all neutered), with a median age of 5.5 years (range, 1 to 8 years); 8, 6, and 2 dogs were subjectively classified as small, medium, and large, respectively. One outlier was removed from heart rate analysis for this group because of potential errors in data recording and to improve model fit.
The owner-present group included 7 mixed-breed dogs, 2 Chihuahuas, 2 Novia Scotia Duck Tolling Retrievers, and 1 each of the following breeds: Collie, American Cocker Spaniel, Papillon, Labrador Retriever, and Doberman Pinscher. There were 9 males and 7 females (all neutered), with a median age of 5 years (range, 1 to 8 years). Three, 6, and 7 dogs in this group were subjectively classified as small, medium, and large, respectively. Owner contact was observed for 12 of 16 dogs in this group, which comprised touching the dog (n = 1), speaking to the dog (3), or both (8). One outlier was removed from yawning analysis for this group because of potential data-recording errors and to improve model fit.
Owner presence and contact with dogs
Behavioral signs of fear—When owners were present, the mean ± SD rate of vocalizations was significantly (P < 0.001) lower (0.11 ± 0.64 vocalizations/min; 95% CI, 0.03 to 0.39 vocalizations/min) than when owners were absent (1.84 ± 0.21 vocalizations/min; 95% CI, 1.2 to 2.8 vocalizations/min). In contrast, owner presence resulted in a higher rate of yawning (0.24 ± 0.51 yawns/min; 95% CI, 0.09 to 0.68 yawns/min) than did owner absence (0.046 ± 0.76 yawns/min; 95% CI, 0.01 to 0.21; P = 0.048). Owner presence was also associated with the rate of lip licking through an interaction with age (P = 0.017); the rate of lip licking was relatively stable across dog ages when the owner was absent, but when the owner was present, the rate of lip licking decreased as age increased (eg, the mean rate for 8-year-old dogs was 2.94 ± 0.24 [95% CI, 1.81 to 4.78], and the mean rate for 1-year-old dogs was 8.51 ± 0.18 [95% CI, 5.92 to 12.2]). The presence of reduced posture (P = 0.95), avoidance behavior (P = 0.17), and escape behavior (P = 0.07) did not differ significantly between treatment groups. Furthermore, owner contact (including physical contact, verbal contact, both, or none) with the dog during the examination was not significantly associated with the rate of lip licking (P = 0.5), rate of yawning (P = 0.083), or presence of reduced posture (P = 0.53).
Physiologic measures—Mean axillary temperature was lower in dogs with the owner present (37.2 ± 0.24°C [99 ± 0.43°F]; 95% CI, 36.7°C to 37.7°C [98.1°F to 99.9°F]) than in dogs with the owner absent (38.0 ± 0.24°C [100.4 ± 0.43°F]; 95% CI, 37.5°C to 38.5°C [99.5°F to 101.3°F]; P = 0.02). Owner presence also affected heart rate through an interaction with dog sex (P = 0.046); female dogs without their owners had a higher mean heart rate (112 ± 7.1 beats/min), compared with male dogs without their owners (85.2 ± 5.0 beats/min) and male (81.3 ± 5.3 beats/min) and female (83.4 ± 6.0 beats/min) dogs with their owners present. Male dogs maintained relatively consistent heart rates regardless of owner presence. There was no significant (P = 0.39) difference in mean respiratory rate between dogs with the owner present (54.3 ± 6.8 breaths/min; 95% CI, 40.4 to 68.1 breaths/min) and dogs with the owner absent (46 ± 6.8 breaths/min; 95% CI, 32.2 to 60 breaths/min). In addition, owner contact (including physical contact, verbal contact, both, or none) with the dog during the examination was not significantly associated with axillary temperature (P = 0.2), heart rate (P = 0.15), or respiratory rate (P = 0.6).
Dog age and sex
Age had a significant (P = 0.047) quadratic relationship with axillary temperature, with model estimates indicating 3-year-old dogs had the highest temperature (38.2°C [100.8°F]). Females had a higher mean temperature (38.1 ± 0.27°C [100.6 ± 0.49°F]; 95% CI, 37.5°C to 38.6°C [99.5°F to 101.5°F]), compared with males (37.2 ± 0.22°C [99 ± 0.4°F]; 95% CI, 36.7°C to 37.6°C [98.1°F to 99.7°F]; P = 0.016), when both treatment groups were combined. Females also had a higher mean rate of vocalizations (0.82 ± 0.36/min; 95% CI, 0.39 to 1.7/min), compared with males (0.24 ± 0.41/min; 95% CI, 0.1 to 0.55/min; P < 0.001) within the overall study sample.
Examination phase
The phase of examination was significantly associated with the rate of lip licking (P < 0.001), avoidance behavior (P < 0.001), and escape behavior (P < 0.001) and the presence of reduced posture (P = 0.005). Lip licking occurred at higher rates during examination of the head and body palpation (phases 1 and 3, respectively) than during other examination phases (Figure 1). Avoidance behavior was observed at higher rates during examination of the head and body palpation than during temperature, heart rate, and respiratory rate assessment (phases 4, 5, and 6, respectively), whereas reduced posture was more common during lymph node (phase 2) and body palpation than during temperature, heart rate, and respiratory rate assessment. However, the rate of escape behavior was higher during respiratory rate assessment than during all other phases except for examination of the head. There were greater odds of reduced posture during body palpation, compared with the odds of this behavior during the temperature assessment (OR, 3.06; 95% CI, 1.48 to 6.32; P = 0.003), heart rate assessment (OR, 2.69; 95% CI, 1.28 to 5.63; P = 0.009), and respiratory rate assessment (OR, 3.51; 95% CI, 1.57 to 7.88; P = 0.003) phases of the examination. Similarly, there were greater odds of reduced posture during lymph node palpation than during the temperature assessment (OR, 2.55; 95% CI, 1.25 to 5.20; P = 0.011), heart rate assessment (OR, 2.24; 95% CI, 1.04 to 4.81; P = 0.04), and respiratory rate assessment (OR, 2.92; 95% CI, 1.50 to 5.69; P = 0.002) phases of examination.
Results of regression analysis to evaluate associations between physical examination phase and behavioral signs of fear (lip licking [A], assuming a reduced posture [head low; ears held sideways, down, or pinned back; and tail lowered or tucked between bent hind legs; B], and aversion behavior [avoidance {white bars} and escape attempts {gray bars}; C]) in 32 client-owned dogs with the owner present (n = 16) or absent (16) during the procedure. All dogs underwent a standardized 6-phase physical examination as follows: phase 1, examination of the head; phase 2, lymph node palpation; phase 3, body palpation; phase 4, axillary temperature measurement; phase 5, auscultation of heart rate; and phase 6, visual assessment of respiratory rate. In all panels, observations for dogs in the owner-present and owner-absent groups were combined. Mean results are shown; error bars represent 95% CIs.a–c For a given behavior, values with different letters differed significantly (P < 0.05) between examination phases.
Citation: Journal of the American Veterinary Medical Association 257, 10; 10.2460/javma.2020.257.10.1031
Results of regression analysis to evaluate associations between physical examination phase and behavioral signs of fear (lip licking [A], assuming a reduced posture [head low; ears held sideways, down, or pinned back; and tail lowered or tucked between bent hind legs; B], and aversion behavior [avoidance {white bars} and escape attempts {gray bars}; C]) in 32 client-owned dogs with the owner present (n = 16) or absent (16) during the procedure. All dogs underwent a standardized 6-phase physical examination as follows: phase 1, examination of the head; phase 2, lymph node palpation; phase 3, body palpation; phase 4, axillary temperature measurement; phase 5, auscultation of heart rate; and phase 6, visual assessment of respiratory rate. In all panels, observations for dogs in the owner-present and owner-absent groups were combined. Mean results are shown; error bars represent 95% CIs.a–c For a given behavior, values with different letters differed significantly (P < 0.05) between examination phases.
Citation: Journal of the American Veterinary Medical Association 257, 10; 10.2460/javma.2020.257.10.1031
Results of regression analysis to evaluate associations between physical examination phase and behavioral signs of fear (lip licking [A], assuming a reduced posture [head low; ears held sideways, down, or pinned back; and tail lowered or tucked between bent hind legs; B], and aversion behavior [avoidance {white bars} and escape attempts {gray bars}; C]) in 32 client-owned dogs with the owner present (n = 16) or absent (16) during the procedure. All dogs underwent a standardized 6-phase physical examination as follows: phase 1, examination of the head; phase 2, lymph node palpation; phase 3, body palpation; phase 4, axillary temperature measurement; phase 5, auscultation of heart rate; and phase 6, visual assessment of respiratory rate. In all panels, observations for dogs in the owner-present and owner-absent groups were combined. Mean results are shown; error bars represent 95% CIs.a–c For a given behavior, values with different letters differed significantly (P < 0.05) between examination phases.
Citation: Journal of the American Veterinary Medical Association 257, 10; 10.2460/javma.2020.257.10.1031
Discussion
We hypothesized that owner presence in the examination room would reduce physiologic and behavioral signs of fear in dogs during routine physical examination, and some results of the present study supported this hypothesis. Multiple behavioral and physiologic measures of fear, including the rate of vocalizations, axillary temperature, and heart rate (in female dogs), were lower when owners were present than when owners were absent during an examination. In previous investigations, dogs have been found to whine and bark during anticipation of an aversive event,39 and vocalizations are a key diagnostic feature of separation anxiety in this species.20,40,41 Exposure to stressors is also widely known to activate the sympathetic nervous system, resulting in physiologic changes, including increases in body temperature and heart rate,42 and these responses have been confirmed in dogs. For example, increased heart rate and rectal temperature in dogs have been observed during conditioning with aversive stimuli.33 Thus, these inter-group differences in the present study suggested that owner presence during veterinary examinations can have a positive influence on the welfare of dogs. However, the frequencies of some other (generally more extreme) responses, such as the presence of reduced posture, avoidance behavior rate, and escape behavior rate, did not differ between treatment groups, suggesting that potential effects of owner presence on fear in dogs in this setting may be subtle.
We considered 2 possible explanations for the described associations between owner presence and dogs’ responses during examinations in the present study: first, owners might have reduced the degree of fear experienced by their dog during the examination through social buffering,19 and second, owners leaving the examination room might have elicited fear and separation-related behaviors in some dogs. Regardless of the reason, these results suggested that owner presence during the examination was beneficial.
The rate of yawning was higher for the owner-present group than for the owner-absent group in the study reported here. In a previous study,25 dogs had increased rates of yawning when owners were present and able to provide physical contact during an examination, compared with results for the same dogs when the owner was present but did not physically interact with the dog. Furthermore, shelter-housed dogs that were petted by a female study participant on removal from their cages yawned more, sought greater contact with the person, and adopted a more relaxed posture, compared with dogs that received no interaction.17 Similar results have also been observed during dog-dog interactions, in which yawning was observed more frequently when dogs encountered familiar dogs than when they encountered unfamiliar dogs.43 Thus, yawning might have been a social signal during interactions between a dog and its owner during the examination. Dogs have also been shown to yawn during exposure to stressful stimuli, such as forced physical restraint,39 and some authors have suggested that it is an appeasement signal to deescalate a threat.44 Further studies investigating the function of yawning are needed to fully understand this response.
Female dogs in the present study were found to have higher axillary temperatures and higher vocalization rates than male dogs within the study sample as a whole, and heart rate was also higher in female dogs with the owner absent than in females or males with the owner present and males with the owner absent. A previous study45 revealed that heart rate measured during examinations does not differ between neutered male and female dogs, and the authors are not aware of any other studies indicating that baseline measures for heart rate or vocalization are consistently higher in female dogs; this suggests that these differences in the present report were attributable to a greater degree of fear in female dogs in response to the examination. Investigations that assessed associations between the development of separation anxiety and the sex of dogs have shown variable results, with some suggesting no sex differences20,46–50 and others suggesting that male dogs are more commonly represented among dogs with this diagnosis.51–53 However, in studies39,54–57 that assessed signs of chronic and acute stress in response to environmental social and spatial changes, female dogs have generally been found to have more posture reductions and greater cortisol responses, suggesting females may have a greater fear response than males. Sample sizes for the present study were small, and sex differences were not detected for other measures, so further research is necessary to explore the potential for sex differences in this context.
Lip licking has been discussed as a sign of acute stress in response to unpredictable stimuli within a social setting30 and to an examination.7,58 Older dogs in our study had a lower rate of lip licking when owners were present, compared with younger dogs in the same group. This was not found for dogs in the owner-absent group, suggesting that older dogs were positively influenced by owner presence during examination in the clinic setting. Previous research to investigate attachment behavior in older dogs (≥ 7 years of age) found that they were more responsive during a strange situation test than younger dogs; for example, older dogs had greater salivary cortisol concentrations and showed less interest in a stranger when separated from their owners.59 Similar results were also found in a longitudinal study60 of 17 trained guide dogs, in which older dogs (adult vs juvenile) displayed less comfort-seeking behaviors toward a stranger in the absence of their owner and more contact-seeking behaviors toward their owners in a strange situation test. This differed from the results related to lip licking in the present study. It is possible that older dogs have a stronger bond that is established over time with an owner, but duration of ownership was not assessed, and this would not explain the increase in lip licking with the owner present versus absent. Therefore, our findings related to lip licking should be interpreted with caution, and further research examining the possible effects of age on dogs’ behavioral responses to veterinary care is warranted.
Previous studies2,4,61 have established that dogs display signs of fear during physical examinations, and recent results suggest that dogs have fear responses of various degrees during specific phases of an examination. An investigation27 of dogs’ responses to the presence (vs absence) of background noises (various sounds played back at decibel levels commonly recorded in veterinary practices) during veterinary examinations revealed that background noise was associated with increased respiratory rate only, but dogs had greater frequencies of lip licking, avoidance behavior, and reduced posture during examination phases that involved more physical contact and handling by the investigator (head examination, lymph node palpation, and body palpation), similar to findings in the present study. In the present study, most of the escape attempts took place during respiratory rate assessment, with no dogs showing avoidance during this phase; this result was logical and therefore may not have been a clear indicator of fear in this phase when dogs had minimum handling and no equipment in place to avoid or prevent escape. However, the order of examination phases was consistent across the previous study27 and the present study, and further research is necessary to determine whether changes in behavior are attributable to the overall progression of the examination or procedures taking place in each phase. Importantly, the variability in fear responses across examination phases demonstrated that dogs were not experiencing high fear levels, so there was the potential for an increase in response during separation. This suggested ceiling effects were not a major concern for the present study.
Owners were instructed to behave as they normally would during the examination, without partaking in handling, and as such, they did not routinely or consistently pet their dogs. Although 1 study25 found that physical and verbal interactions with the dog were important in reducing stress-related behaviors during an examination, fear measures in the present study were not influenced by how the owner interacted with their dog (physical contact, verbal contact, or both). However, the number of dogs that received each type of owner contact was small, so there was likely insufficient power to detect differences.
Dogs that were 1 to 8 years of age were recruited for the study reported here. Whereas excluding dogs > 8 years of age reduced the generalizability of our results for senior dogs, the decision to exclude these dogs was important to help avoid enrollment of dogs likely to have physical (eg, chronic pain) or mental (eg, cognitive dysfunction) impairments that could confound responses to the examination. Also, dogs with a fear score of 4 (extreme fear) on the preenrollment survey were excluded for ethical and safety reasons. However, as these dogs would have likely shown a maximal level of fear in the clinical setting, it was considered unlikely that a treatment effect would have been detected. In addition, it was not possible to balance breed and body size across treatment groups owing to the voluntary nature of the recruitment method used. Although physiologic variables such as heart rate can be influenced by body size, the control and treatment groups had fairly well-distributed representations of various breeds and sizes, and it was unlikely that this had an important impact on the results reported.
In contrast to other studies that detected changes in the respiratory rates of dogs in response to a clinic environment23 and to background noise during an examination,27 respiratory rate was not associated with owner's presence during examination in the present study. This might have been explained, in part, by some dogs panting during assessment of this variable. While this could have been prevented by closing the dog's mouth during assessment, we chose not to do this, considering that the action could cause additional stress. In addition, physiologic variables were only assessed at 1 time point during the examination. These measures likely varied across phases of the examination; therefore, they represented the response to that particular activity and were not likely to be representative of the same measures throughout the examination.
Owner gender is thought to influence dog behavior,62–64 and only 3 male owners participated in our study; thus, our results may not be generalizable to dogs whose male owners accompany them during an examination. Also, 4 owners each had > 1 dog in the study. For 2 of these owners, random assignment resulted in enrollment of 1 dog to each treatment group, but in 1 situation it resulted in an owner present during the examination of both dogs, and in another situation, an owner was present in the room during examination of 2 dogs and absent during examination of a third dog. A small number of owners had multiple dogs, and it was unlikely that household effects or owner behavior would have influenced our results.
Our results suggested that owner presence during a routine examination has positive effects on some behavioral and physiologic measures of fear in companion dogs. However, it is important to acknowledge that owner presence also has the potential to negatively influence dogs’ experience or behavior in some situations. It has been suggested that dogs can become more fearful when their owner is nervous, either directly through social referencing65 or because of physiologic or behavioral changes associated with human emotional states that impact dog anxiety.66 Thus, our results suggested that owners should be encouraged to remain with their dog during routine veterinary examinations or procedures whenever possible, but further research is needed to examine the influence of owner anxiety in this context, and in-clinic decisions should be made on an individual patient basis, taking this into consideration. Despite the finding that owner presence was associated with reduced frequency of some signs of fear in dogs, evidence of examination-related fear was still observed in both the presence and absence of owners in the study reported here. Further research is necessary to determine whether examination methods can be developed that further reduce signs of fear and whether early socialization to relevant veterinary stimuli and other training methods can be employed that reduce fearful responses among dogs in veterinary clinic settings.
Acknowledgments
This study was performed at the Hill's Pet Nutrition Primary Healthcare Centre (Smith Lane Animal Hospital) at the University of Guelph, Ontario, Canada.
Funded by the Natural Sciences and Engineering Research Council of Canada.
The authors confirm that there are no known conflicts of interest associated with this publication, and there has been no financial support that could have influenced its outcome.
The authors thank William Sears for assistance with statistical analysis, Hailey Hoffman for assistance with examinations, and Siobhan Mellors for video analysis.
Footnotes
American Diagnostic Corp, Onbo Electronic (Shenzhen) Co Ltd, Shenzhen, China.
Handycam HDR-CX330, Sony, Japan.
Observer XT, Noldus Information Technology Inc, Wageningen, Netherlands.
SAS, version 9.3, SAS Institute Inc, Cary, NC.
References
1. Edwards PT, Smith BP, McArthur ML, et al. Fearful Fido: investigating dog experience in the veterinary context in an effort to reduce distress. Appl Anim Behav Sci 2019;213:14–25.
2. Stanford TL. Behavior of dogs entering a veterinary clinic. Appl Anim Behav Sci 1981;7:271–279.
3. Mariti C, Raspanti E, Zilocchi M, et al. The assessment of dog welfare in the waiting room of a veterinary clinic. Anim Welfare 2015;24:299–305.
4. Döring D, Roscher A, Scheipl F, et al. Fear-related behaviour of dogs in veterinary practice. Vet J 2009;182:38–43.
5. Dobratz, K.J., Smith G. Evaluation of risk factors for bite wounds inflicted on caregivers by dogs and cats in a veterinary teaching hospital. J Am Vet Med Assoc 2003;223:312–316.
6. Jeyaretnam J, Jones H, Phillips M. Disease and injury among veterinarians. Aust Vet J 2000;78:625–629.
7. Bragg RF, Bennett JS, Cummings A, et al. Evaluation of the effects of hospital visit stress on physiologic variables in dogs. J Am Vet Med Assoc 2015;246:212–215.
8. Glardon OJ, Hartnack S, Horisberger L. Analysis of dogs and cats behavior during the physical examination in veterinary practice [in French]. Schweiz Arch Tierheilkd 2010;152:69–75.
9. van Vonderen IK, Kooistra HS, Rijnberk A. Influence of veterinary care on the urinary corticoid: creatinine ratio in dogs. J Vet Intern Med 1998;12:431–435.
10. Volk JO, Felsted KE, Thomas JG, et al. Executive summary of the Bayer veterinary care usage study. J Am Vet Med Assoc 2011;238:1275–1282.
11. Dawson LC, Dewey CE, Stone EA, et al. A survey of animal welfare experts and practicing veterinarians to identify and explore key factors thought to influence canine and feline welfare in relation to veterinary care. Anim Welf 2016;25:125–134.
12. Odendaal JS, Meintjes RA. Neurophysiological correlates of affiliative behaviour between humans and dogs. Vet J 2003;165:296–301.
13. Nagasawa M, Mitsui S, En S, et al. Social evolution. Oxytocingaze positive loop and the coevolution of human-dog bonds. Science 2015;348:333–336.
14. Rehn T, Handlin L, Uvnäs-Moberg K, et al. Dogs’ endocrine and behavioral responses at reunion are affected by how the human initiates contact. Physiol Behav 2014;124:45–53.
15. Lynch JJ, McCarthy JF. The effect of petting on a classically conditioned emotional response. Behav Res Ther 1967;5:55–62.
16. Coppola CL, Grandin T, Enns RM. Human interaction and cortisol: can human contact reduce stress for shelter dogs? Physiol Behav 2006;87:537–541.
17. Henessy MB, Williams MT, Miller DD, et al. Influence of male and female petters on plasma cortisol and behaviour: can human interaction reduce the stress of dogs in a public animal shelter? Appl Anim Behav Sci 1998;61:63–77.
18. Shiverdecker MD, Schiml PA, Hennessy MB. Human interaction moderates plasma cortisol and behavioral responses of dogs to shelter housing. Physiol Behav 2013;109:75–79.
19. Mariti C, Ricci E, Zilocchi M, et al. Owners as a secure base for their dogs. Behaviour 2013;150:1275–1294.
20. Overall KL, Dunham AE, Frank D. Frequency of nonspecific clinical signs in dogs with separation anxiety, thunderstorm phobia, and noise phobia, alone or in combination. J Am Vet Med Assoc 2001;219:467–473.
21. Sherman BL, Mills DS. Canine anxieties and phobias: an update on separation anxiety and noise aversions. Vet Clin North Am Small Anim Pract 2008;38:1081–1106.
22. Tiira K, Sulkama S, Lohi H. Prevalence, comorbidity, and behavioral variation in canine anxiety. J Vet Behav 2016;16:36–44.
23. Riemer S, Assis L, Pike TW, et al. Dynamic changes in ear temperature in relation to separation distress in dogs. Physiol Behav 2016;167:86–91.
24. Lind A-K, Hydbring-Sandberg E, Forkman B, et al. Assessing stress in dogs during a visit to the veterinary clinic: correlations between dog behavior in standardized tests and assessments by veterinary staff and owners. J Vet Behav 2017;17:24–31.
25. Csoltova E, Martineau M, Boissy A, et al. Behavioral and physiological reactions in dogs to a veterinary examination: owner-dog interactions improve canine well-being. Physiol Behav 2017;177:270–281.
26. Epstein M, Kuehn NF, Landsberg G, et al. AAHA senior care guidelines for dogs and cats. J Am Anim Hosp Assoc 2005;41:81–91.
27. Stellato A, Hoffman H, Gowland S, et al. Effect of high levels of background noise on dog responses to a routine physical examination in a veterinary setting. Appl Anim Behav Sci 2019;214:64–71.
28. Gomart SB, Allerton FJ, Gommeren K. Accuracy of different temperature reading techniques and associated stress response in hospitalized dogs. J Vet Emerg Crit Care (San Antonio) 2014;24:279–285.
29. Araujo JA, de Rivera C, Landsberg GM, et al. Development and validation of a novel laboratory model of sound-induced fear and anxiety in Beagle dogs. J Vet Behav 2013;8:204–212.
30. Beerda B, Schilder MBH, van Hooff JARAM, et al. Behavioural, saliva cortisol and heart rate responses to different types of stimuli in dogs. Appl Anim Behav Sci 1998;58:365–381.
31. Blackwell EJ, Bradshaw JWS, Casey RA. Fear responses to noises in domestic dogs: prevalence, risk factors and cooccurrence with other fear related behaviour. Appl Anim Behav Sci 2013;145:15–25.
32. Levine ED, Ramos D, Mills DS. A prospective study of two self-help CD based desensitization and counter-conditioning programmes with the use of dog appeasing pheromone for the treatment of firework fears in dogs (Canis familiaris). Appl Anim Behav Sci 2007;105:311–329.
33. Ogata N, Kikusui T, Takeuchi Y, et al. Objective measurement of fear-associated learning in dogs. J Vet Behav 2006;1:55–61.
34. Tami G, Barone A, Diverio S. Relationship between management factors and dog behavior in a sample of Argentine Dogos in Italy. J Vet Behav 2008;3:59–73.
35. Adolphs R. Biology of fear. Curr Biol 2013;23:R79–R93.
36. Adriaan Bouwknecht J, Olivier B, Paylor RE. The stress-induced hyperthermia paradigm as a physiological animal model for anxiety: a review of pharmacological and genetic studies in the mouse. Neurosci Biobehav Rev 2007;31:41–59.
37. Beerda B, Schilder MBH, van Hooff JARAM, et al. Manifestations of chronic and acute stress in dogs. Appl Anim Behav Sci 1997;52:307–319.
38. Riemer S, Assis L, Pike TW, et al. Dynamic changes in ear temperature in relation to separation distress in dogs. Physiol Behav 2016;167:86–91.
39. Solomon RL, Wynne LC. Traumatic avoidance learning: acquisition in normal dogs. Psychol Monogr 1953;67:1–19.
40. McCrave EA. Diagnostic criteria for separation anxiety in the dog. Vet Clin North Am Small Anim Pract 1991;21:247–255.
41. Sherman BL. Understanding behavior: separation anxiety in dogs. Compend Contin Educ Vet 2008;30:27–32, 42.
42. Stewart M, Webster JR, Schaefer AL, et al. Infrared thermography as a non-invasive tool to study animal welfare. Anim Welf 2005;14:319–325.
43. Mariti C, Falaschi C, Zilocchi M, et al. Analysis of the intra-specific visual communication in the domestic dog (Canis familiaris): a pilot study on the case of calming signals. J Vet Behav 2017;18:49–55.
44. Rugaas T. On talking terms with dogs: calming signals. Wenatchee, Wash: Dogwise Publishing, 2006.
45. Ferasin L, Ferasin H, Little CJ. Lack of correlation between canine heart rate and body size in veterinary clinical practice. J Small Anim Pract 2010;51:412–418.
46. Voith VL, Borchelt PL. Separation anxiety in dogs. In: Readings in companion animal behavior. Trenton, NJ: Veterinary Learning Systems, 1996;124–139.
47. Wright JC, Nesselrote MS. Classification of behavior problems in dogs: distributions of age, breed, sex and reproductive status. Appl Anim Behav Sci 1987;19:169–178.
48. Flannigan G, Dodman NH. Risk factors and behaviors associated with separation anxiety in dogs. J Am Vet Med Assoc 2001;219:460–466.
49. Gaultier E, Bonnafous L, Bougrat L, et al. Comparison of the efficacy of a synthetic dog-appeasing pheromone with clomipramine for the treatment of separation-related disorders in dogs. Vet Rec 2005;156:533–538.
50. Simpson BS, Landsberg GM, Reisner IR, et al. Effects of Reconcile (fluoxetine) chewable tablets plus behavior management for canine separation anxiety. Vet Ther 2007;8:18–31.
51. King JN, Simpson BS, Overall KL, et al. Treatment of separation anxiety in dogs with clomipramine: results from a prospective, randomized, double-blind, placebo-controlled, parallel-group, multicenter clinical trial. Appl Anim Behav Sci 2000;67:255–275.
52. Takeuchi Y, Houpt KA, Scarlett JM. Evaluation of treatments for separation anxiety in dogs. J Am Vet Med Assoc 2000;217:342–345.
53. Podberscek AL, Hsu Y, Serpell JA. Evaluation of clomipramine as an adjunct to behavioural therapy in the treatment of separation-related problems in dogs. Vet Rec 1999;145:365–369.
54. Beerda B, Schilder MB, van Hooff JA, et al. Chronic stress in dogs subjected to social and spatial restriction. I. Behavioral responses. Physiol Behav 1999;66:233–242.
55. Beerda B, Schilder MB, Bernadina W, et al. Chronic stress in dogs subjected to social and spatial restriction. II. Hormonal and immunological responses. Physiol Behav 1999;66:243–254.
56. Beerda B, Schilder MBH, van Hooff JARAM, et al. Behavioral and hormonal indicators of enduring environmental stress in dogs. Anim Welf 2000;9:49–62.
57. Garnier F, Benoit E, Virat M, et al. Adrenal cortical responses in clinically normal dogs before and after adaption to a housing environment. Lab Anim 1990;24:40–43.
58. Döring D, Haberland BE, Ossig A, et al. Behavior of laboratory Beagles towards humans: assessment in an encounter test and a simulation of experimental situations. J Vet Behav 2014;9:295–303.
59. Mongillo P, Piterri, E, Carnier P, et al. Does the attachment system towards owners change in aged dogs? Physiol Behav 2013;120:64–69.
60. Valsecchi P, Previde EP, Accorsi PA, et al. Development of the attachment bond in guide dogs. Appl Anim Behav Sci 2010;123:43–50.
61. Godbout M, Palestrini C, Beauchamp G, et al. Puppy behavior at the veterinary clinic: a pilot study. J Vet Behav 2007;2:126–135.
62. Bennett PC, Rohlf VI. Owner-companion dog interactions: relationships between demographic variables, potentially problematic behaviours, training engagement and shared activities. Appl Anim Behav Sci 2007;102:65–84.
63. Kubinyi E, Turcsán B, Miklósi A. Dog and owner demographic characteristics and dog personality trait associations. Behav Processes 2009;81:392–401.
64. Dodman NH, Brown DC, Serpell JA. Associations between owner personality and psychological status and the prevalence of canine behavior problems. PLoS One 2018;13:e0192846.
65. Merola I, Prato-Previde E, Marshall-Pescini S. Dogs’ social referencing towards owners and strangers. PLoS One 2012;7:e47653.
66. D'Aniello B, Semin GR, Alterisio A, et al. Interspecies transmission of emotional information via chemosignals: from humans to dogs (Canis lupus familiaris). Anim Cogn 2018;21:67–78.