Journal of Veterinary Behavior 17 (2017) 44e49

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Journal of Veterinary Behavior

journal homepage: www.journalvetbehavior.com

Canine Research

Stress level evaluation in a dog during animal-assisted therapy

in pediatric surgery
Clara Palestrini a, *, Valeria Calcaterra b, c, Simona Cannas a, Zita Talamonti a,
Francesca Papotti a, Debra Buttram d, Gloria Pelizzo e, f
a
Dipartimento di Medicina Veterinaria, Università degli Studi di Milano, Milano, Italy
b
Pediatric Unit, Department of Mother and Child Health, Fondazione IRCCS Policlinico San Matteo, Pavia, Italy
c
Department of Internal Medicine, University of Pavia, Pavia, Italy
d
Associazione Natura Animale, Lambrugo, CO, Italy
e
Pediatric Surgery Unit, Department of Mother and Child Health, Fondazione IRCCS Policlinico San Matteo, Pavia, Italy
f
Department of Clinical-Surgical, Diagnostic and Pediatric Sciences, University of Pavia, Pavia, Italy

a r t i c l e i n f o a b s t r a c t

Article history: Animal-assisted interventions are associated with positive effects on human psychological and physio-
Received 13 June 2016 logical health. Although quality standards in animal-assisted interventions appear to be high, only few
Received in revised form investigations have focused on potential welfare implications in therapy dogs. In the present study, we
7 September 2016
monitored behavioral measures and heart rate in a therapy dog that participated in animal-assisted
Accepted 7 September 2016
Available online 15 September 2016
therapy during postoperative awakening in a pediatric surgery ward. Work-related activity, behavior,
response to human action, and heart rate were analyzed for more than 20 working sessions in an
experienced therapy dog. No physiological or behavioral indicators of stress, fatigue, or exhaustion were
Keywords:
animal-assisted therapy
present during animal-assisted therapy, suggesting that, with the limited generalizability of a case study,
animal welfare this activity did not negatively impact on the welfare of the dog. Further investigation into the effects of
behavior animal-assisted therapy on dogs’ physiological markers and behavior is warranted.
heart rate Ó 2016 Elsevier Inc. All rights reserved.
dog
stress

Introduction motivation to take part in health interventions, exercise, and social

interaction (Wilson and Barker, 2003; Glenk et al., 2014). The wide-
Animal-assisted interventions (AAIs) are achieving a certain level spread involvement of dogs in AAIs is grounded in the outstanding
of recognition worldwide, and this is accompanied by a growing body interspecific social ability of this species and in the dogs’ ease in
of research on the effect of these programs on human health and adapting to various human environments (Miklósi and Topál, 2013).
well-being (Bernabei et al., 2013; Marcus, 2013; Calcaterra et al., Although a growing body of evidence supports the rewards and
2015). AAIs, which use animals for human benefit, can be consid- benefits of human-animal interactions for humans, only few in-
ered animal-assisted therapy (AAT) when they involve the vestigations have focused on the potential welfare implications for
implementation of goal-directed, documented, and evaluated therapy dogs as a result of their performance in AAIs. Indeed, the
methodology in professional settings. In contrast, animal-assisted welfare of dogs involved in AAA and AAT has been questioned, as
activities (AAAs) are not centered on a specific goal or treatment social interactions have been described as among the most potent
outcome and can be carried out by nonprofessional volunteers too stressors a dog can endure (von Holst, 1998; McEwen and Wingfield,
(Kruger and Serpell, 2010). Animals are believed to be a source of 2003). This may be because social interactions can be unpredictable,
requiring the individual to constantly adapt physiologically and
behaviorally to maintain homeostasis (Karatsoreos and McEwen,
2011). Study of the physiological and behavioral effects of AAIs on
* Address for reprint requests and correspondence: Clara Palestrini, Dipartimento
registered dogs is needed to enhance our understanding of animal
di Medicina Veterinaria, Università degli Studi di Milano, Via Celoria 10, 20133,
Milano, Italy. Tel: þ39 0250318039; Fax: þ39 0250318030. welfare during these interventions, introduce evidence-based
E-mail address: [email protected] (C. Palestrini). guidelines for handlers, and establish rigorous methods for future

http://dx.doi.org/10.1016/j.jveb.2016.09.003
1558-7878/Ó 2016 Elsevier Inc. All rights reserved.
 C. Palestrini et al. / Journal of Veterinary Behavior 17 (2017) 44e49 45

research. Animal welfare has commonly been assessed by measuring participation in AAT, including documentation of the dog’s current
and analyzing stress-associated behavior and physiological in- vaccinations, controllability, and temperament. Twenty immuno-
dicators of stress in dogs (i.e., heart rate [HR]) (Vincent and Michell, competent children (15 males and 5 females), aged 3-17 years
1992; Beerda et al., 1999; Palestrini et al., 2005). Analysis of (mean  standard deviation, 8.59  3.70), undergoing surgical
behavior has also long been used as a research tool to assess stress procedures (including orchidopexy, inguinal or umbilical hernia
and welfare in animals. Stress-associated behavior in dogs, such as repair, circumcision, and varicocele treatment) were randomly
increased locomotor activity, lip licking, yawning, and circling, have assigned to the AAT session. In all subjects, surgery was performed
been observed to occur in response to acute stressors (Beerda et al., between 8.30 AM and 12 AM under general anesthesia, at the Pedi-
1997; Palestrini, 2009). Ferrara et al. (2004) reported the absence of atric Surgery Unit, Fondazione IRCCS Policlinico S. Matteo, Pavia.
stress behavior in dogs during AAA/AAT, whereas King et al. (2011) Parental permission was obtained by means of written and oral
observed multiple behavioral signs of stress (panting, yawning, informed consent. Written assent by the patient was also obtained
whining, and lip licking) in dogs after an AAT session. These dis- in children of 8 years and older before enrollment.
crepancies warrant clarification as to whether activity and therapy
sessions induce stress-associated behavior. Procedures and data collection
HR has a long history as a psychophysiological measure of ani-
mals’ affective and cognitive responses, and several studies have About 2 hours after surgery, during postoperative awakening,
investigated HR responses of dogs to different stimuli and environ- each child underwent a 20-minute session with the AAT dog. The
mental conditions (Beerda et al., 1997). HR represents an accessible, therapy dog was specially prepared and chosen for the interactions,
quantifiable, physiological measure underlying emotional responses which were evaluated as suitable and recorded together with the
in dogs, and the possibility of linking physiology and observable handler. During the sessions, the handler monitored the dog, ten-
behavior is of great importance in gaining a better understanding of ded to its needs, and supervised the dog-child interactions. Dog
the dog’s reactions to environmental changes (Kostarczyk, 1992; behavior was video recorded during the 20 experimental sessions.
Beerda et al., 1998; Casey, 2003). Both behavior and HR are consid- A video camera (Panasonic NV-GS330; Panasonic Italia, Milano,
ered useful indicators to evaluate stress reactions in dogs Italy) was installed in the room (5  4 m, with a constant room
(Kostarczyk, 1992) because of the interaction between the central temperature of 22  1 C) opposite the area where the child and
nervous system and the neuroendocrine system (Henry and Ely, dog-handler team remained during the session. HR was measured
1976; Beerda et al., 1998). The robustness of an animal welfare using a Polar Vantage NV Ó (Polar Electro, Kempele, Finland) sys-
assessment is thus improved when stress-associated behavior is tem (Vincent and Leahy, 1997) to allow comparison between HR
evaluated in conjunction with cardiac activity (Palestrini et al., 2005; and behavior. The Polar was fixed around the chest of the animal
Stiles et al., 2011). In this investigation, the objective was to measure with an elastic band. The monitor collected a reading of heart beats
and compare behavior and HR in an experienced therapy dog to per minute every 5 seconds throughout each 20-minute therapy
examine whether the dog exhibited behavioral or physiological session. The results were then downloaded to a computer using
signs of stress in AAT in a pediatric surgery setting. Polar ProTrainer 5 Ó (Polar Electro, Kempele, Finland) software.
Each session was transferred as separate file. The HR device was
Materials and methods activated at the start of each session and synchronized with the
video recording of behavior to have a perfect match between the
Participants behavioral and physiological data.

A carefully screened 7-year-old spayed female golden retriever Statistical analysis

was used as the therapy animal. She had previous experience in
AAIs and was already trained and prepared for this type of work. The videotaped sessions were analyzed by 2 trained observers, and
The dog was fully vaccinated, regularly groomed, screened for the dog’s behavior was recorded in 11 categories. Any interaction of the
enteric pathogens, and treated for internal and external parasites children with the dog, under the handler’s supervision, was also
on a monthly basis. The dog and handler met hospital policy for recorded. Table 1 shows the list of mutually exclusive categories and

Table 1
Behavioral categories and their definition

Behavioral category Definition

Duration
ExplorationdEX Motor activity directed toward physical aspects of the environment, including sniffing, and gentle oral examination such
as licking
Passive behaviordPA Lying down with the head on ground without any obvious orientation toward the physical or social environment
Oriented to the environmentdOE Sitting, standing, or lying down (the head does not rest on the ground) with obvious orientation toward the physical or
social environment, including sniffing, close visual inspection, distant visual inspection (vigilance or scanning)
Interaction with the childdIC Any behavior performed when interacting the child including active physical contact, sniffing, close visual inspection,
and gentle oral examination such as licking
Interaction with the handlerdIH Any behavior performed when interacting the handler, including active physical contact, sniffing, close visual inspection,
and gentle oral examination such as licking
Interaction with the peopledIP Any behavior performed when interacting with the people in the room (child’s parents, hospital staff), including active
physical contact, sniffing, close visual inspection, and gentle oral examination such as licking
WithdrawaldWT Avoiding interaction with the child by either moving away, very clearly turning away, or looking away
PantingdPT Rapid shallow breathing (mouth open)
Frequency
YawningdYA Yawning
Lip lickingdLL Part of tongue is shown and moved along the upper lip
GroomingdGR The action of cleaning the body surface by licking, nibbling, picking, rubbing, scratching, etc., directed toward the
animal’s body (self-grooming)
46 C. Palestrini et al. / Journal of Veterinary Behavior 17 (2017) 44e49

their definitions. All 20 recorded AAT sessions were included in the handler [IH], 8.61%  6.09%) than with the child (interaction with
behavior analysis. Videos were analyzed using the Solomon Coder the child [IC], 4.93%  3.80%) or other people (interaction with the
(version: beta 15.11.19; Ó2016 by András Péter). Interobserver and people [IP], 2.24%  3.03%). Exploration (EX, 3.48%  2.37%) was
intraobserver reliability were assessed by means of independent coding observed for very short periods especially during the early AAT
of a random sample of videotaped sessions (10%) using percentage sessions. Grooming (GR), lip licking (LL), and yawning (YA) were
agreement: percentage agreement was always more than 92%. observed, respectively, for 1.65  1.73, 5.65  3.82, and 1.25  0.97
A focal animal continuous recording method (Martin and (Figure 2). Children behaved differently with the dog, some never
Bateson, 1993) was used to describe the dog’s activity. Some of sought any interaction, whereas others interacted with the dog for
the dog behaviors (exploration, passive, orientation to environ- most of the time (Figure 3). No correlation was found between dog
ment, panting, interaction with the child/handler/people, and stresserelated behaviors (lip licking, yawning, grooming, panting,
withdrawal) were recorded in terms of duration of occurrence and avoidance) and children interactions.
(states), and other behaviors (licking lips, yawning, and grooming)
were recorded in terms of frequency (events). Children’s in- Heart rate
teractions with the dog were recorded in terms of duration of
occurrence (states). To describe duration and frequency for each HR was recorded every 5 seconds for only 10 therapy sessions.
behavior, a descriptive analysis was first performed. The dog’s HR levels always remained within a range of normal
Durations of states were calculated as percentage of total values (basal metabolic rate, 60-110) (Santilli and Perego, 2009) as
observation time, and events were expressed as frequencies. A reported in Table 2.
bivariate correlation was used to verify the relationship between
child-dog interactions and variables related to the dog’s stress be-
haviors (licking lips, yawning, grooming, and withdrawal). Discussion
Continuous recording of HRs was only available for 10 sessions. The
remaining sessions could not be considered in the analysis because It is well known that humans benefit from interaction with
the recorded signal was either absent or incomplete. Mean therapy dogs; therefore, the behavioral and physiological health of
(standard deviation) HR values were calculated. the animal should be carefully reflected on (Stetina and Glenk, 2011).
Dedicated research on animals in AAIs is limited and does not pro-
vide evidence on which standards can be issued regarding animal
Results welfare (Beck and Katcher, 2003). In dog-assisted therapy, there are
considerable differences between different programs with regard to
Behavior the procedures in dog training, the AAI working schedule, time span
between arrival at a facility and the start of the AAI, and quality
Analysis of dog behavior (Figure 1) on tape showed that she assessment and quality assurance (Stetina and Glenk, 2011).
spent most of her time exhibiting panting behavior (panting [PT], Consequently, it is crucial to increase knowledge of which measur-
28.35%  18.09%) as opposed to avoiding interactions with the child able variables reflect aspects of animal welfare and provide evidence
or other people in the room (withdrawal [WT], 0.06%  0.15%). Most on which standards should be achieved during AAT. This study
of her time she was oriented to the environment (OE, 23.22%  explored whether a prepared dog exhibited behavioral or physio-
14.37%) or showed passive behavior (passive [PA], 6.58%  7.54%). logical signs of stress during AAT in pediatric surgery setting. Of the
The dog interacted more with the handler (interaction with the behaviors recorded, panting was most often exhibited. In addition to

Figure 1. Proportional duration of behaviors of 20 animal-assisted therapyeworking sessions of a therapy dog. EX, exploration; PA, passive; OE, oriented to environment; IC,
interaction with the child; PT, panting; IP, interaction with the people; IH, interaction with the handler; WT, withdrawal.
 C. Palestrini et al. / Journal of Veterinary Behavior 17 (2017) 44e49 47

the contrary, may help to manage stress. Recently, Shiverdecker et al.

(2013) supported this assumption.
Not all dogs express stress-associated behavior in the same way
because temperament and personality are influenced by many
variables, including age, breed, and previous experience (Hiby et al.,
2006; Passalacqua et al., 2013). Different dogs often have different
responses and coping strategies to the same stimulus (Rooney et al.,
2007). The brain and body develop coordinated biologic mecha-
nisms in response to potent stressors to anticipate and recover from
them in the future in an effort to maintain homeostasis
(Karatsoreos and McEwen, 2011). Responses are also likely influ-
enced by the type of interaction as it has been speculated that dogs
may not exhibit stress-associated behavior in the context of
human-animal interactions (Kuhne et al., 2012) despite being
physiologically stressed (Ng et al., 2014). Therefore, it is necessary to
assess behavior in conjunction with physiological parameters such
Figure 2. Proportional frequency of behaviors of 20 animal-assisted therapyeworking as HR.
sessions of a therapy dog. GR, grooming; LL, lip licking; YA, yawning. In our study, the 20-minute AAT sessions did not result in an
increase in HR levels during the 10 AAT sessions for which heart-
beat was measured. HR levels in the activity setting were no
being a response to heat, panting can be associated with negative different from the normal range (basal metabolic rate, 60-110)
stress (Godbout et al., 2007; Palestrini et al., 2010a) or with positive (Santilli and Perego, 2009). HR responses were not related to
arousal, such as during anticipation of a desired reward (Ng et al., whether the dog interacted with the child during the session. This
2014). It must be noted, however, that the effect of room tempera- may have been because interaction during the activity was safe and
ture on panting was probably substantial in this study because the predictable. The inability to predict what will happen induces sig-
temperature is maintained relatively high (22  1) during post- nificant stress in humans (Henry and Stephens, 1977), and this
operative awakening and remained constant between evaluations. likely occurs in dogs as well. An AAT, dog-handler team typically
No prior activity or stimulation was performed that could have consists of a dog with a consistent, nonfearful, and nonaggressive
influenced panting in the dog. The dog did not show noticeable signs temperament and a handler who is trained to minimize in-
of distress: she spent most of her time oriented to the environment teractions that might be perceived as threatening by the dog (Ng
or being passive. She never showed any withdrawal behavior and et al., 2014). It must be noted that the therapy dog was specially
interacted both with the child and other people present in the room. prepared and chosen for the interactions, which were evaluated as
The dog explored the environment especially during the early AAT suitable and performed together with the handler. The handler
sessions. The dog did not show more lip licking, yawning, grooming, monitored the dog, tended to the dog’s needs, and supervised each
or avoidance behavior during sessions where children interacted dog-child interaction.
with the dog compared with sessions without any interaction. Lip AAT dogs are selected for this type of activity because of their
licking, yawning, and grooming have been associated with fear or temperament and are trained to remain calm and relaxed, even in
anxiety (Beerda et al., 1998; Frank et al., 2007; Cannas et al., 2010; stressful situations (Viau et al., 2010). Therefore, AAT dogs may not
Palestrini et al., 2010b) or as a possible displacement behavior exhibit stress-associated behaviors typically demonstrated by the
indicative of conflict (Cannas et al., 2014). Lip licking and yawning rest of the canine population when physiologically aroused. This
have also been suspected to precede situations of social conflict in underscores the importance of measuring behavior in conjunction
dogs (Voith and Borchelt, 1996). However, according to Rehn and with HR. Although single AAT sessions may not induce an acute
Keeling (2011), lip licking may be communicative cues in dogs, stress response, it is not known to what extent the duration or
which do not necessarily correspond to a stressful experience but, on frequency of AAT sessions may induce stress, which over time may

Figure 3. Proportional duration of children’s interactions with the dog during 20 animal-assisted therapy sessions. The symbol * refers to sessions with corresponding heart rate
measurements, as indicated in Table 2.
48 C. Palestrini et al. / Journal of Veterinary Behavior 17 (2017) 44e49

Table 2 investigations on animal welfare in AAT. It proposes a straightfor-

Mean  SD and minimum and maximum HR values for each recorded session ward and widely applicable approach to data collection that allows
Sessions HR (mean  SD) Minimum HR Maximum HR the synchronous recording of behavioral and HR data, which could
1 91  15 70 121
be used to standardize exploration of the effects of different types
4 140  8 88 126 of AAT on animal well-being. To provide consistent high quality in
6 75  3 71 138 AAIs, it is essential to monitor and interpret physiological and
7 93  12 78 119 behavioral parameters that are related to animal welfare. Future
11 86  8 75 134
studies could be aimed at ascertaining the effects of different
14 100  6 94 115
15 95  18 77 132 working conditions and environments by manipulating the therapy
16 85  10 72 111 sessions and at validating the experimental methodology used in
19 84  10 69 127 our study.
20 104  5 95 116

SD, standard deviation; HR, heart rate.

Ethics statement

result in a disruption of homeostatic mechanisms and chronic The study was performed according to the Declaration of Hel-
stress (Karatsoreos and McEwen, 2011). Further studies are needed sinki. The ethics committee of the Fondazione IRCCS Policlinico S.
to investigate this limit. Although the dog in this study did not Matteo and Department of Internal Medicine, University of Pavia,
appear to be negatively affected by this particular AAT work, the approved the study protocol on April 11, 2013. AAT was also
welfare of AAT dogs should be continuously monitored. Until a gold approved on April 11, 2013, by the ethics committee of the Fonda-
standard measure of stress or distress is clearly established, zione IRCCS Policlinico S. Matteo. No invasive intervention or drug
behavioral observation remains a principal and practical method of experimentation on the dog was performed; therefore, the appli-
evaluating stress and welfare in animals (Hekman, 2012). The cation of Decreto Legislativo 116/92, European Directives 86/609/EE
handler must be rigorously trained on the prevention, recognition, for the protection of animals used in scientific and experimental
and management of stress-associated behavior in his or her dog. It studies and 2010-63UE was not required. The dog owner provided
is particularly important that the handler understands normal dog consent for its use in the study. Participants were recruited between
behavior in the home environment to be able to recognize behav- September 1, 2013 and April 1, 2014. The study was registered at
ioral signs of stress when they occur (Ng et al., 2014). ClinicalTrials.gov (identifier: NCT02284100) after enrollment was
The physical environment plays a role in dogs’ stress response. initiated because AAT was considered a complementary treatment.
An appropriately trained handler can influence the dog’s perception The authors confirm that all ongoing and related trials for this drug/
of the environment and minimize the stress response by facilitating intervention are registered.
controlled and predictable interactions. Continuing education of
AAT dogs, monitoring for behavioral signs of stress, and intervening Conflict of interest
with mental stimulation (training obedience commands or taking a
break with a short time out from patient care areas) would be The authors declare no conflict of interest. All authors have
helpful. An optimal work shift achieved by monitoring behavioral approved the final article for submission.
signs of stress is mandatory to promote healthy interactions be-
tween the dogs and the people they serve. To date, there is no single
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