Artigo 4
Artigo 4
Artigo 4
PII: S0168-1591(17)30330-1
DOI: https://doi.org/10.1016/j.applanim.2017.11.014
Reference: APPLAN 4560
Please cite this article as: McCullough, Amy, Jenkins, Molly A., Ruehrdanz, Ashleigh,
Gilmer, Mary Jo, Olson, Janice, Pawar, Anjali, Holley, Leslie, Sierra-Rivera, Shirley,
Linder, Deborah E., Pichette, Danielle, Grossman, Neil J., Hellman, Cynthia, Guérin,
Noémie A., O’Haire, Marguerite E., Physiological and behavioral effects of animal-
assisted interventions on therapy dogs in pediatric oncology settings.Applied Animal
Behaviour Science https://doi.org/10.1016/j.applanim.2017.11.014
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Physiological and behavioral effects of animal-assisted interventions on therapy dogs in pediatric
oncology settings
Authors: McCullough, Amy (PhD)a, Jenkins, Molly A. (MSW)a, Ruehrdanz, Ashleigh (MPH)a, Gilmer,
Mary Jo (PhD, RN-BC, FAAN)b, Olson, Janice (MD)c, Pawar, Anjali (MD)d, Holley, Leslie (MS, CCLS)e,
Sierra-Rivera, Shirley (BSN, RN)e, Linder, Deborah E. (DVM, MS, DACVN)f, Pichette, Danielle (CCRP)g,
Grossman, Neil J. (MD)g, Hellman, Cynthia (MSW)a, Guérin, Noémie A. (MS)h, & O’Haire, Marguerite E.
(PhD)h
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Affiliation postal addresses:
a
American Humane/1400 16th Street NW, Suite 360/Washington, DC 20036 USA.
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b
Monroe Carell Jr. Children's Hospital at Vanderbilt/417 Godchaux Hall/461 21st Avenue South/Nashville,
TN 37240 USA.
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c
Randall Children’s Hospital at Legacy Emanuel/2801 N. Gantenbein Avenue, 3rd Floor/Portland, OR
97227 USA.
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d
UC Davis Comprehensive Cancer Center/4501 X Street, 2nd Floor/Sacramento, CA 95817 USA.
e
f
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St. Joseph’s Children’s Hospital/3001 W. Dr. Martin Luther King Jr. Boulevard/Tampa, FL 33607 USA.
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Cummings School of Veterinary Medicine at Tufts University/200 Westboro Road/North Grafton, MA
01536 USA.
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g
UMass Memorial Children’s Medical Center/55 Lake Avenue North/Worcester, MA 01655 USA.
h
Center for the Human-Animal Bond/Purdue University, College of Veterinary Medicine/725 Harrison
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Corresponding author:
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Phone: 303-588-6225
Fax: N/A
Email Address: [email protected]
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Highlights:
The responses of dogs to animal-assisted intervention sessions were investigated.
Dogs’ salivary cortisol did not increase during animal-assisted intervention sessions.
Dogs did not have increased stress-associated behaviors during AAI sessions.
Dogs who exhibited more stress behaviors also exhibited more affiliative behaviors.
Dogs who exhibited more stress behaviors also had increased salivary cortisol
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Abstract
Over the past two decades, animal-assisted interventions (AAIs), defined as the purposeful incorporation
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of specially trained animals in services to improve human health, have become increasingly popular in
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clinical settings. However, to date, there have been few rigorously-designed studies aimed at examining the
impact of AAIs on therapy animals, despite a notable potential for stress. The current study measured
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physiological and behavioral stress indicators in therapy dogs who participated in AAI sessions in pediatric
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oncology settings, while also examining the psychosocial effects for patients and their parents. This
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manuscript describes the study’s canine stress findings. A total of 26 therapy dog-handler teams were paired
with newly diagnosed children with cancer at five children’s hospitals in the United States. These teams
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provided regular AAI visits to the child and his/her parent(s) for a period of four months. The teams
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completed a demographic form, the Canine Behavioral Assessment & Research Questionnaire (C-BARQ),
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and a self-report survey to document the types of activities that occurred during each session. Canine saliva
was also collected at five baseline time points and 20 minutes after the start of study sessions for cortisol
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analysis, and all study sessions were video recorded to document the dog’s behavior via an ethogram
measure. Data showed no significant differences in salivary cortisol levels between baseline (0.51µg/dL)
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and AAI sessions (0.44µg/dL; p = 0.757). Higher salivary cortisol was significantly associated with a higher
number of stress behaviors per session (p = 0.039). There was a significant relationship between stress and
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affiliative session behaviors (p<0.0001), indicating that dogs who exhibited more stress behaviors also
exhibited more affiliative behaviors. The dog’s most commonly coded session behaviors were oral
behaviors, such as lip licking, and tail wagging. The only C-BARQ factor that was found to have a
significant association was stranger-directed fear; higher scores on this factor were significantly associated
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with the dog exhibiting fewer affiliative behaviors in sessions (b = 2.12, p = 0.042). Results show that
therapy dogs did not have significantly increased physiological stress responses, nor did they exhibit
significantly more stress-related behaviors than affiliative-related behaviors, while participating in AAIs in
pediatric oncology settings. There was a significant relationship between canine cortisol and behavior, thus
strengthening the argument for the use of cortisol in canine well-being research. This study discusses the
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importance of further investigation to confirm these findings, and to enhance therapy dog involvement in
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hospital settings.
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Keywords: animal-assisted intervention, therapy dog, stress, salivary cortisol, behavior, animal welfare
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1. Introduction
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Documented benefits of human-animal interactions have increasingly led to the integration of animal-
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assisted interventions (AAIs1) in services designed to improve human health, and to greater investment into
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exploring their effects (McCardle et al., 2011). When included as adjuncts to medical and mental health
treatment, interactions with therapy animals have been shown to distract from or alleviate anxiety; decrease
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pain perception; motivate therapeutic participation; normalize clinical environments and enhance therapist-
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client rapport; and provide social support (Braun et al., 2009; Fine, 2015; Nimer and Lundahl, 2007; Wu et
al., 2002). Dogs, because of their relative trainability, predictable behavior, and availability are commonly
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utilized as therapy animals in a variety of AAI applications and therapeutic settings (Glenk, 2017).
Through nearly 35,000 years of domestication, dogs have become well-attuned to nuances in human
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emotions, behaviors, and attentional states (Albuquerque et al., 2016; Reid, 2009; Wang et al., 2016).
Studies (Handlin et al., 2011; Odendaal and Meintjes, 2003) show that people who interact with dogs
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experience elevated levels of the attachment hormone oxytocin, with recent research (Nagasawa et al.,
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AAI is to be defined as the purposeful incorporation of specially trained and qualified animals, most commonly
dogs, in services to improve human health (International Association of Human-Animal Interaction Organizations or
IAHAIO, 2014; Nimer and Lundahl, 2007).
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2015) demonstrating increased oxytocin for both humans and their pet dogs through mutual gazing. While
heightened sensitivity to the human condition is likely advantageous for connecting with AAI recipients, it
may also pose salient welfare risks to therapy dogs. For example, dogs have exhibited similar physiological
stress responses as humans after listening to infant crying (Yong and Ruffman, 2014). Because such
outward displays of human distress often occur in therapeutic settings, therapy dogs may be vulnerable to
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stress during AAI participation (Glenk, 2017). Additionally, as registered therapy dogs are trained to calmly
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tolerate interactions that they might otherwise find taxing (e.g., rushed head-petting by strangers), handlers
may find it difficult to notice distress in their dogs who may already be inclined to please (Glenk, 2017).
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To date, research regarding the experience of therapy dogs in AAIs has been informative, but remains
limited. Most measures of therapy dog welfare rely on physiological (cortisol), behavioral (stress-related)
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and/or observational (handler perspective) indicators, as it is problematic to assess canine stress by any one
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indicator alone. Without behavioral context, it is difficult to conclude whether elevated cortisol indicates
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distress or eustress (Edgar et al., 2012).
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While current research suggests minimal welfare concerns for therapy dogs, results have been mixed and
are difficult to generalize given a lack of practice fidelity. Likewise, organizations that register therapy dogs
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often differ in their health and safety policies, including inconsistent vetting and training procedures meant
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to limit canine stress (Linder et al., 2017). Recent research (Haubenhofer and Kirchengast, 2007, 2006)
found that therapy dogs experience higher levels of physiological stress on working days when compared
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to days at home. Salivary cortisol was also higher for dogs participating in shorter and more frequent AAI
sessions, possibly due to heightened intensity or fewer respite opportunities (Glenk, 2017; Haubenhofer
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and Kirchengast, 2007, 2006). King et al. (2011) reported indicators of canine physiological and behavioral
stress after 1-2 hours of AAI participation in hospital settings, including stress-related behaviors, increased
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salivary cortisol, and cortisol-stress behavior correlation. Additionally, a higher prevalence of behavioral
stress has been observed in therapy dogs during interactions with children younger than 12 years, whose
relatively erratic behavior may cause dogs discomfort (Marinelli et al., 2009).
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Environmental factors (e.g., strange stimuli/people) may also increase therapy dog stress. Recently,
researchers found that novel settings significantly increased salivary cortisol in therapy dogs when
compared to familiar locations, underlining the importance of allowing dogs to become accustomed to new
AAI environments (Ng et al., 2014). Likewise, handlers have reported such factors as high temperatures
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In contrast, other studies have found scant evidence indicative of canine distress during AAIs (Barstad,
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2014; Palestrini et al., 2017; Piva et al., 2008), including no differences in physiological stress between
working and non-working days (Glenk et al., 2014, 2013; Ng et al., 2014). In research examining cortisol
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and behavior, Glenk et al. (2014) found that therapy dog behavior did not significantly change over time,
and that salivary cortisol decreased in the final two sessions with adults undergoing substance abuse
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treatment.
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Simply put, AAI practice must be mutually beneficial to be considered both ethical and effective, and
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handlers must continually work to ensure the welfare needs and humane treatment of participating therapy
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animals (Serpell et al., 2010). Given the potential for canine stress during AAIs, as well as the current lack
of agreement regarding if and how AAIs affect animal welfare, additional research is essential to understand
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how to best support therapy dogs as their involvement in human health services broadens. To that end, this
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study measured the physiological and behavioral effects of regular AAI sessions for registered therapy dogs
in five U.S. pediatric oncology settings. This research also measured the effects of sessions on patients and
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their parents, with these findings reported elsewhere (McCullough et al., in press). In regard to canine
outcomes, we hypothesized that therapy dogs would exhibit minimal indicators of physiological and
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2. Methods
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All protocols and surveys were approved by the Institutional Animal Care and Use Committee and the
Institutional Review Board at American Humane, as well as at each participating hospital site. The
following five hospitals, located in the United States, participated in this research study: Monroe Carell Jr.
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Oregon; University of California Davis Children’s Hospital in Sacramento, California; St. Joseph’s
Children’s Hospital in Tampa, Florida; and Children's Medical Center at UMass Memorial Health Care, in
Massachusetts. Modifications to the protocol were made at two different time points, which impacted the
human participants’ enrollment and retention rates (e.g., broader inclusion criteria for children and a
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monetary incentive for control group patients). These changes were not related to any of the canine
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protocols.
2.1 Participants
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Eligible therapy dog-handler teams were identified by the hospital sites’ volunteer services coordinator,
study coordinator, and/or by other handlers through a referral process. Each participating team consisted of
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a therapy dog and his/her handler, who were registered by a national organization that requires rigorous
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training and evaluation policies. These teams volunteered to visit children, ages 3-17 years, who had been
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recently diagnosed with cancer, enrolled in the study at one of the study sites, and randomly assigned to the
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intervention group to receive regular (e.g., weekly) visits from a therapy dog-handler team for a period of
four months. Prior to participation, all handlers were required to complete the hospital volunteer services
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training and credentialing process, and to adhere to the rigorous health, safety, and privacy guidelines and
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policies in place at their respective hospital site. To support safe interactions, all therapy dog handlers had
completed extensive AAI training, and all therapy dogs had passed a behavioral and health evaluation, prior
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to enrollment. Dogs were required to be a minimum of one year old and have at least six months of AAI
Twenty-six teams participated in the study. Prior to consenting, each team attended a study-specific training
at their local hospital site. At this meeting, a detailed description of the study protocol, including how to
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collect their dog’s saliva and how to complete all other applicable instruments, was presented. Handlers
had the opportunity at this training to practice and demonstrate their ability to properly obtain a saliva
sample from their dog. All handlers received printed training materials to keep for their reference, as well
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Sample size was determined based on a power analysis for the human measures in the study, which yielded
a sample size of 100 patients to be enrolled. Approximately half of this group (n = 60) was randomly
assigned to receive AAI sessions with therapy dogs. To facilitate these sessions for 60 child participants
over a period of 33 months, 26 dogs participated in the canine assessment portion of the study.
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. Human participants randomized to this study’s intervention group received their standard care offered at
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the hospital plus regular visits from a participating therapy dog-handler team. Children were enrolled for a
four-month period near the onset of their cancer treatment. Interactions with the therapy dog occurred
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approximately once per week, and coincided with the child’s treatment schedule and clinic visits.
Depending on existing hospital policies and procedures, children transferred to inpatient care could
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continue their visits with the therapy dog, while others could visit in the outpatient oncology clinic only.
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Children were matched, by the site coordinator, to a specific therapy dog-handler team who became their
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primary team for the study; back-up teams were used on an as-needed basis. Children were matched to their
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therapy dog team based on the child’s treatment schedule and the team’s volunteer availability.
All therapy dog sessions were prescribed to last approximately 20 minutes, with session length ultimately
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determined by the patient, parent, handler, site coordinator, or another medical staff member. AAI sessions
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were nonprescriptive in nature, allowing for flexibility in activities and physical intensity based upon the
child’s health status and the level of therapy dog and child engagement. However, all handlers were given
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a list of commonly used activities to choose from as a reference guide (e.g., pet the dog, brushed the dog,
practiced dog’s cues, etc.). These sessions took place in semi-private to private areas of the pediatric
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oncology clinic, depending upon the health status of the child and room availability.
2.3 Measures
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A variety of instruments were used to assess indicators of canine stress and well-being over the course of
the study.
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Demographic information was obtained from participating handlers using a self-report questionnaire. In
addition to factors such as age, race, gender, and canine breed, handlers reported information about the
length of time they had been volunteering with their therapy dog, with what populations, and in what types
of settings.
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After consenting to participate, therapy dog handlers completed the C-BARQ for their dog who would be
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participating in the study. This standardized 100-question instrument is completed online and asks dog
owners to indicate how their dog typically responds to common events and stimuli in their environment
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(Serpell, 2017). The C-BARQ is comprised of 14 behavioral factors: trainability, stranger-directed
aggression, owner-directed aggression, dog rivalry, stranger-directed fear, non-social fear, dog-directed
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aggression, dog-directed fear, touch sensitivity, separation-related behavior, excitability,
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attachment/attention-seeking, chasing, and energy. This instrument was utilized as a descriptor for the
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therapy dog population’s temperament and behavior.
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Salivary cortisol is a known bio-marker for stress and arousal in humans and other animals (Hekman et al.,
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2012; Kirschbaum and Hellhammer, 1994). Dog’s salivary cortisol levels lag plasma levels by 20 minutes,
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indicating that salivary cortisol peaks roughly 20 minutes after a stressful event, which is then maintained
for approximately 0.5 hours before declining (Hennessy et al., 1998; Vincent and Michell, 1992). In this
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study, therapy dog-handler teams collected their dog’s saliva at five different time points at the beginning
of the study to establish a baseline cortisol measurement. These five time points were as follows: 1. Upon
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their dog waking in the morning, prior to breakfast; 2. Mid-day/noon; 3. Evening, just prior to the dog’s
typical bedtime; 4. Approximately 20 minutes after the presence of an AAI-specific “trigger” – such as the
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introduction of his/her therapy vest/bandanna or visit bag; and 5. Approximately 20 minutes after arriving
Given the known salivary cortisol lag and peak times, as well as our flexible approach to session timing
described above, the study protocol specified that therapy dog handlers collect their canine’s saliva sample
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immediately following a session, except for in cases where sessions lasted fewer than 20 minutes. In
instances where sessions lasted less than 20 minutes, handlers were asked to wait in a quiet room for a short
period to allow for the saliva they collected to accurately represent their dog’s response to the session (e.g.,
if a session lasted five minutes, the handler waited in a quiet room for a period of 15 minutes and then began
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Saliva was collected by the therapy dog handler using recommended collection procedures (Dreschel and
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Granger, 2009). To collect saliva, the handler sat/kneeled on the floor or a chair, and placed an absorbent
125mm long Salimetrics (State College, PA, USA) SalivaBio Children’s Swab into the dog’s mouth. The
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handler would rub the swab around the dog’s cheek and gum area for approximately 90-300 seconds, until
the swab appeared to be saturated with saliva. Saturated swabs were then placed into a saliva collection
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tube pre-labeled with the Handler ID, Child ID (for post-session samples), and sample number. Handlers
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then hand-wrote the date and time of collection, and gave the saliva collection tube to the study coordinator
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to store and ship for analysis. All tubes were stored at -20° C in a medical grade freezer at each hospital to
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ensure sample viability. Approximately once every three months, a set of samples were shipped to
Salimetrics, in a Styrofoam cooler packed with dry ice, for testing. Each sample underwent
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Salimetrics Cortisol Enzyme Immunoassay Kit, which is a duplicate assay. The results of the assays were
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averaged to create one value for the study analyses, unless the saturation amount would not allow for
After each AAI session, handlers completed a self-report form to indicate the activities that occurred. They
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were provided with a list of common AAI activities to choose from, but could also indicate if any other
activities took place that were not pre-defined. This list of session activities was tracked for both the child
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and parent using one-zero sampling (i.e., activity occurred or did not occur). Handlers also used this form
to describe any environmental factors related to the session and their dogs’ behavior (e.g., “room was very
warm which affected dog's attention and behavior”, “[dog] intermittently distracted by noise in hallway”,
etc.). The site coordinator filled in who was present and participated in the activities, and indicated any
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observations of the child’s or dog’s behavior that they felt was pertinent (e.g., “had to meet with dog in
Each AAI session was recorded by two video cameras (Samsung HMX-F90BN HD Camcorder with 2.7"
LCD Screen) to ensure that the dog’s behavior was captured during the interaction. These recordings were
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then coded using a non-standardized behavior ethogram developed by the study’s researchers and informed
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by animal behaviorists and veterinarians. This ethogram included 26 behaviors divided into three
categories: affiliative indicators (leaning or resting body or head against a person or object; licking a
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person; pawing/paw lifting; play stance/bow; pushing snout; raising ears; rolling over; tail wagging;
walking towards a person), moderate stress indicators (body shaking or "shaking off"; escape; looking
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at/to handler; looking away; oral behaviors, such as lip licking, extending the tongue, or smacking the lips;
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panting - excessive or prolonged; restlessness; self-directed behaviors; yawning), and high-stress
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indicators (baring teeth; barking, yelping, yipping, whining, or whimpering; biting or attempting to bite;
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crouching; drooling--excessive or in copious amounts; ears plastered/pinned back; growling; stare gaze)
(See Table 2 for detailed ethogram information). All behaviors exhibited by the therapy dogs were tallied
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for their frequency. The total frequency of stress-related behaviors was summed to create one score (17
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Ethogram coders underwent several rounds of training on how to use the instrument, including viewing
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video clips of the potential behaviors that were to be coded. Intra-class correlation coefficients (ICC)were
calculated at various time points during the training process, and additional training sessions were
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conducted until a satisfactory level of inter-rater agreement and coder confidence was established. One
individual served as the primary coder, with two additional coders providing supplementary coding support.
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2.4 Settings
Data collection for this study occurred in the handler’s place of residence and at the participating hospital
sites.
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Four out of the five baseline cortisol data points (morning, mid-day, evening, trigger) were obtained at the
therapy dog team’s place of primary residence. The morning collection occurred upon the dog waking, and
typically occurred between 05:19 and 10:30 (M = 07:47, SD = 01:13 hours:minutes). The mid-day
collection occurred between 07:00 and 21:15 (M = 12:40, SD = 2:41 hours:minutes). The evening collection
occurred between 10:40 and 23:00 (M = 19:57, SD = 3:16 hours:minutes). The trigger collection occurred
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approximately 20 minutes after giving the dog a signal that s/he would be going to work (e.g., therapy dog
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vest/bandanna). The trigger sample was collected between 07:05 and 23:00. (M = 11:11, SD = 3:12
hours:minutes).
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2.4.2 Hospital Setting
The final baseline saliva sample was collected 20 minutes after arriving at the hospital where the team
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participated in study sessions. This collection occurred between 08:15 and 16:45 (M = 12:16 SD = 2:08
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hours:minutes). The goal of collecting baseline samples at the dog’s home and at the hospital was to obtain
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a measure of the dog’s typical salivary cortisol levels on non-working days (without any interactions with
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unfamiliar individuals) to then compare to cortisol collected after each AAI session.
To allow for the therapy dog to have minimal distractions during the collection process, post-session saliva
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samples were collected at the hospital site in a quiet, semi-private to private area designated by the site
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coordinator and handler. This area was generally separate from where the AAI sessions took place.
Analyses were conducted to address two key goals: 1). to compare differences in salivary cortisol between
control/baseline and AAI conditions and 2). to examine factors affecting salivary cortisol and behavior
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during AAI sessions. Statistical analyses were conducted using mixed modeling procedures (Raudenbush
and Bryk, 2002). This hierarchical analysis technique accounted for the nested data design, with repeated
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measurements nested within individual dogs nested within hospital sites. Random factors in all models
Salivary cortisol data were positively skewed and not normally distributed. Therefore, raw values were log-
transformed for further analyses using linear mixed models. Means and graphs present back-transformed
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values for ease of interpretation. All models for salivary cortisol control for time of day as a fixed factor.
To compare the effect of study conditions on salivary cortisol, we conducted a linear mixed model with the
fixed effect of condition (morning, mid-day, evening, trigger, hospital, AAI session). To examine factors
affecting salivary cortisol, we conducted linear mixed models with additional fixed factors related to
demographics (age, gender, experience, breed), C-BARQ factor scores, or AAI session characteristics
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(duration, number of people present and participating, reported activities).
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Ethogram behavior data were analyzed using generalized linear mixed models appropriate for count data
with a Poisson distribution sampling method and a log-link function. To control for the differing video
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lengths, all ethogram behavior models controlled for the length of the video as a fixed factor. To examine
factors affecting behavior, we conducted linear mixed models for stress and affiliative behaviors with fixed
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factors related to demographics (age, gender, experience, breed), C-BARQ factor scores, or AAI session
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characteristics (number of people, reported activities). We also included the fixed factor of cortisol to
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examine the relationship between cortisol and behavior.
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Analyses were performed using the Statistical Package for the Social Sciences (SPSS) Version 24.0 (IBM
Corp., released 2016. IBM SPSS Statistics for Windows, Version 24.0. IBM Corp., Armonk, NY). All
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3. Results
The final dataset for analysis included 604 data points, or records, across 26 dogs. At the dog level (n = 26),
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data included demographic characteristics (n = 24 dogs) and C-BARQ surveys (n = 26 dogs). At the
repeated measures record level (n = 604), data included AAI Therapy Dog Handler and Study Coordinator
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Self-Reports (n = 445), ethogram behavioral data (n = 405), and valid salivary cortisol samples (n = 411).
The random factors in the mixed models accounted for variance across dogs and hospital sites. The random
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factor of hospital site was not significant in any model (ICC ≤ 0.423, p ≥ 0.209), indicating that there were
no significant differences in outcomes across hospitals. The random factor of dog was significant in all
models (ICC ≥ 0.030, p ≤ 0.046), indicating that there were significant individual differences across dogs
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3.1 Participants
The sample of therapy dog-handler teams with demographic data (n = 24; two handlers declined to provide
this information) included dogs aged two to 13 years old, who were primarily female (58%) with 0.5 to
9.17 years of experience as a visiting therapy dog. A wide range of dog breeds of varying sizes was
represented, including Miniature Poodles, Newfoundlands, a Border Collie mix, a Dachshund, and a
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Wheaton Terrier, while the most common breeds were Golden Retrievers (17%), Labrador Retrievers
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(13%), or mixed breeds that included part Golden or Labrador Retriever (16%). Therapy dog handlers
identified as predominantly female (92%), 46 years or older (83%), and Caucasian/White (96%). Therapy
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dog-handler teams were largely registered through Pet Partners (75%). Dog handlers had between 0.5 and
10.42 years of experience as AAI handlers, with most of these teams (67%) having previous experience in
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hospital settings.
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3.2 Session Characteristics: Therapy Dog Handler and Study Coordinator Self-Reports
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The study included 445 AAI sessions recorded by Therapy Dog Handler and Site Coordinator Self-Reports.
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Sessions lasted between five and 180 minutes, with an average of 23.95 minutes per session (Median = 17;
Mode = 15; SD = 21.13). The categories of individuals at each session were noted and the number of people
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who were present and participated at each session (excluding the handler) ranged from one to eight. On
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average, 3.11 people were present and 2.27 people participated in session activities with the therapy dog.
The most common people present included the child (n = 445 sessions, 100%), mother (n = 377, 85%),
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father (n = 151, 34%), and nurse (n = 110, 25%). The most common people who participated in session
activities included the child (n = 417, 94%), mother (n = 306, 69%), and father (n = 113, 25%).
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The most common activities engaged in by the child included petting the dog (n = 409, 92%), talking to the
dog (n = 307, 69%), viewing the dog’s photos (n = 144, 32%), and brushing the dog (n = 106, 24%). The
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most common activities engaged in by the parent included petting the dog (n = 244, 55%), talking to the
dog (n = 212, 48%), taking a photo of the dog and/or child with the dog (n = 69, 16%), and viewing the
dog’s photos (n = 64, 14%). Across 445 recorded sessions, children participated in 1,446 activities, while
parents participated in 801 activities. See Table 1 for a complete list of session activity frequencies.
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3.3 Canine Behavior Ethogram
AAI sessions were video recorded to code canine behavior via a pre-defined ethogram. Inter-rater reliability
of ethogram behavior data was calculated using a two-way mixed effect ICC. Reliability between the
primary and secondary coder was good (ICC = 0.782, p < 0.0001). More than 30 unique ethogram samples
were used to calculate the ICC, and therefore it is suggested that ICC “values between 0.75 and 0.9 indicate
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good reliability” (Koo and Li, 2016, p. 158). An average of 9.69 (SD = 10.47) stress behaviors and 9.14
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(SD = 9.33) affiliative behaviors were recorded in each session. There were no significant differences
between the frequency of displayed stress versus affiliative behaviors, t(404) = 1.19, p = 0.236. The most
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common canine behaviors included oral behaviors, such as lip licking, and tail wagging. There were no
high-stress indicator behaviors coded for any dog across all study sessions. Descriptive statistics for
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ethogram behaviors are presented in Table 3. There was a significant association between stress and
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affiliative behaviors, β = 0.21, t(402) = 9.39, p < 0.0001. Dogs who displayed more stress behaviors in a
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given session also demonstrated more affiliative behaviors during that session.
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Salivary cortisol levels were relatively consistent across all conditions (Figure 1). There were no significant
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differences between the AAI sessions (n=299) and any baseline session, including morning (n = 24, β = -
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0.05, p = 0.398), mid-day (n = 23, β = 0.02, p = 0.680), evening (n = 22, β = 0.08, p = 0.295), trigger (n =
Canine cortisol levels did not increase over time of involvement in the study, and remained consistent with
The relationship between demographic characteristics and canine outcomes are presented in Table 4.
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Therapy dog gender was related to salivary cortisol (p = 0.002), with female dogs exhibiting significantly
lower salivary cortisol than males. Animal age was related to salivary cortisol (p = 0.004), stress behaviors
(p = <0.0001), and affiliative behaviors (p = 0.010). Older dogs showed lower salivary cortisol and
displayed more behaviors during AAI sessions, including both stress and affiliative behaviors. There were
14
no effects of handler years of experience on salivary cortisol or behavioral outcomes (p range = 0.197 -
0.421).
There was no relationship between most C-BARQ factors and canine outcomes (p range = 0.129 - 0.882).
The only factor with a significant effect was stranger-directed fear. Higher stranger-directed fear, as rated
by handlers, was associated with 2.12 fewer affiliative behaviors on average per session (p = 0.042).
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3.6 Relationship Between Session Characteristics, Salivary Cortisol, and Behavior
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The relationship between session characteristics and canine outcomes is presented in Table 5. Duration of
sessions was not significantly related to salivary cortisol (p = 0.481) or stress behaviors (p = 0.092). Session
SC
length was significantly associated with affiliative behaviors (p < 0.0001), but the effect was relatively
small; therapy dogs displayed 0.01 more affiliative behaviors for each minute longer a session lasted. There
U
were no significant effects of the number of people present (p ≥ 0.165) or participating (p ≥ 0.134) on
N
salivary cortisol or behavior. There were also no effects of the type of session activities on salivary cortisol
A
(p ≥ 0.105).
M
There were significant relationships between session activity type and behavior (Table 6). Dogs displayed
significantly fewer affiliative behaviors per session when the following activities took place: participant got
D
water for the dog; child played a game on the dog’s vest; child drew a picture of the dog; child used a
TE
stethoscope to listen to the dog’s heartbeat; child collected an AAI-related sticker or card from the handler;
participant used a lint roller during the session; participant brushed the dog; and participants discussed
EP
Dogs displayed significantly more affiliative behaviors per session when the following activities took place:
CC
participant played with the dog’s toy; participant talked to the dog; handler discussed dog breeds and
histories with the family; participants took the dog for a walk; participants viewed photos of the dog; and
A
Dogs exhibited significantly fewer stress behaviors per session when the following activities took place:
child facilitated a visit between the therapy dog and hospital staff; participants pet the dog; and participants
took a photo of the dog (p range = ≤ 0.001 - 0.041). Finally, dogs displayed significantly more stress
15
behaviors per session when the following activities took place: child put a bandanna on the dog and when
the handler and participants discussed dog breeds (p = 0.035 and p = 0.003, respectively).
The final analysis model included salivary cortisol level as a fixed factor to examine its relationship with
stress and affiliative behaviors. When controlling for affiliative behaviors, higher salivary cortisol was
PT
significantly associated with an increased frequency of stress behaviors per session, β = 0.16, t(243) = 2.08,
RI
p = 0.039. When controlling for stress behaviors, higher salivary cortisol was significantly associated with
a reduced frequency of affiliative behaviors, β = -0.26, t(243) = -2.82, p = 0.005. Thus, lower levels of
SC
salivary cortisol were related to increased displays of affiliative behaviors during AAI sessions, while
higher levels of salivary cortisol were related to increased displays of stress behaviors.
U
4. Discussion
N
The current study measured physiological and behavioral indicators of stress in registered therapy dogs
A
who participated in AAI sessions with pediatric oncology patients and their parents. To our knowledge, this
M
is the largest randomized controlled trial to measure the impact of AAI for both humans and therapy dogs
to date, particularly across multiple hospitals where AAI is commonly practiced. As hypothesized, results
D
indicate that therapy dogs show minimal signs of distress during AAI sessions, regardless of hospital site.
TE
The geographical heterogeneity (across the U.S.) of participating sites has favorable implications for the
generalizability of these findings, particularly in healthcare facilities with rigorous therapy dog
EP
The lack of significant differences in canine salivary cortisol levels between AAI sessions and each of the
CC
five baseline conditions is an important finding that supports existing selected studies in this area (Glenk et
al., 2014, 2013; Ng et al., 2014). Cortisol concentration levels also remained relatively consistent over time,
A
which could indicate that participation in a greater number of AAI sessions is not a source of stress for
therapy dogs.
Additionally, there was a significant relationship between canine cortisol and behavior, with lower cortisol
levels associated with increased displays of affiliative behavior, and higher cortisol levels with increased
16
stress behaviors. Both of these relationships, but particularly the latter, suggest that cortisol may be a good
indicator of distress in therapy dogs. Notably, there were few significant relationships between handler-
rated canine temperament and canine outcomes, except for the C-BARQ stranger-directed fear factor; dogs
with a perceived higher degree of stranger-directed fear exhibited significantly fewer affiliative behaviors
on average per session. Much like with novel settings (Ng et al., 2014), therapy dogs who find interactions
PT
with strangers stressful may benefit from a prolonged introduction to unfamiliar recipients, possibly
RI
comprised of shorter initial visits where the dog can initiate contact and take breaks when needed. Further,
canine temperament measures like the C-BARQ may serve as effective tools for facilities when screening
SC
prospective therapy dog-handler teams, and determining their optimal placement.
In addition, while therapy dogs exhibited slightly more stress behaviors than affiliative behaviors per
U
session on average, the difference between the two was not significant and may have been due to more
N
stress behaviors listed on the ethogram for researchers to code. Dogs who displayed a high frequency of
A
affiliative behaviors tended to exhibit a similarly high frequency of stress behaviors, which could indicate
M
Interestingly, older dogs displayed significantly more stress and affiliative behaviors than their younger
D
counterparts, but also had significantly lower session cortisol. Potentially, some dogs may grow
TE
increasingly expressive in their behavior or adept at communicating behaviorally as they age. Further,
behaviors traditionally deemed as stress indicators – such as panting or yawning (Beerda et al., 1999, 1998)
EP
– could serve as a calming mechanism for dogs to manage their stress during worrisome situations, as Glenk
et al. (2014) propose. Thus, this could lead to a higher number of stress behaviors, but a lower physiological
CC
stress response, as we observed with older therapy dog participants. With that said, it is essential that
handlers be responsive to the changing health needs of their therapy dogs as they age, and retire dogs when
A
they are no longer able to engage comfortably with recipients (Serpell et al., 2010).
Years of handler experience in AAI was not significantly related to either their dog’s physiological or
behavioral outcomes; just as many canine stress indicators were present with more experienced handlers as
with those who were newer to the practice. For less seasoned handlers, fewer years of experience could
17
have been offset by a shorter time lapse since undergoing training. As AAI trainings often emphasize the
primary role of handlers as stewards of their dog’s safety and comfort (Pet Partners, 2017), new handlers
may have been more keenly attentive to canine behavior than those more accustomed to the practice. This
finding highlights the importance of regular handler training opportunities that emphasize how to
effectively monitor and alleviate canine stress during sessions. Nevertheless, it can be argued that handler
PT
participants overall were heedful of their dog’s needs, as evidenced by the significant relationship between
RI
longer sessions and an increased frequency of affiliative canine behaviors. Handlers who observed a
relatively high frequency of affiliative behaviors in their dogs may have continued or even prolonged AAI
SC
sessions due to the perceived low risk of canine stress. However, given the small effect size of this
relationship, and the large range of documented session duration, this interpretation remains speculative
U
and needs further exploration.
N
There were several limitations of this study that may serve to clarify areas of future inquiry. While our
A
canine sample size is the largest known to date in studies of therapy dog welfare (Glenk, 2017), we studied
M
less than 30 dogs. Subsequent research would benefit from a larger sampling of therapy dog participants.
However, the sample was strengthened by its heterogeneity and representation of the breed variability
D
There were also certain outside factors that could have impacted the level of stress experienced by therapy
dogs that we did not document, including their adoption experiences, trauma histories, or any record of
EP
serious health conditions or medication regimens (although all dogs received prior veterinary approval for
AAI participation). We also did not note characteristics of AAI visits that the dogs may have participated
CC
in between study sessions, such as length, number, frequency, and population served. Indeed, due to ethical
reasons, therapy dogs were not prohibited from visiting with other people that they encountered when on
A
hospital premises for study sessions, and we did not inquire about these interactions.
Additionally, handler participants, while anecdotally representative, were not demographically diverse
enough to explore the potential effects of handler race, gender, or age on therapy dog well-being. Future
research and practice efforts should focus on the potential impact of handler demographics on canine and
18
human recipient outcomes, as well as how this population may be diversified to ensure culturally competent
AAI practices. Furthermore, handler adherence to certain study protocols, such as the timing of baseline
saliva collection, was not consistent, and could have impacted the interpretation of those data.
Further, in order to study the canine effects of AAI sessions as they are currently practiced, this study did
not prescribe a structured protocol of activities. Rather, the flow and type of session activities occurred at
PT
the discretion of patients, parents, handlers, and/or medical staff, and were largely dependent on child health
RI
status and/or the response of the child or dog to the interaction. Activities were documented, including how
SC
While there were no significant effects of session activities on canine salivary cortisol, there were
significant relationships between certain activities and the frequency of affiliative and stress behaviors. For
U
example, sessions where the therapy dog was brushed may have been more stressful for the dog, as
N
evidenced by the presence of less affiliative behaviors. Likewise, dogs displayed more affiliative behaviors,
A
and potentially less stress, in sessions where they were taken for a walk. However, at present, it is not sound
M
to infer a direct causal relationship between any particular activity and the dogs’ response. Additionally,
the direction of the activity and associated canine behavior is not clear (i.e., did the dog show more
D
affiliative behaviors when walked or was the dog walked because he/she showed more affiliative
TE
behaviors?). These research questions should be explored further, as they may help to refine prescribed
Finally, there may have been potential issues regarding the behavior ethogram used in this study. Because
a validated instrument for assessing therapy dog behavior during AAI sessions does not currently exist,
CC
piloting and utilizing our own measure was necessary. In developing our ethogram, it was important to refer
to previous canine behavioral measures (i.e., Beerda et al., 1998), consult with animal behaviorists and
A
veterinarians, and provide further context through the inclusion of both stress and affiliative behaviors.
Nevertheless, the development of a validated measure which re-evaluates the nature of currently recognized
behavioral indicators of therapy dog stress and affiliation in an AAI context is important to confirm this
19
4.1 Conclusions
The increasing prevalence of therapy dog programs in today’s pediatric hospitals (Chubak and Hawkes,
2016) and other services merits further investigation regarding the well-being of dogs who work in these
settings. AAIs have traditionally been positioned as services to improve human health, but the welfare needs
of therapy animals must be elevated if their participation in this pursuit is to advance. While further research
PT
is needed to verify these results, this study provides valuable and rigorous evidence that AAI participation
RI
in pediatric hospitals does not appear to place registered therapy dogs at significant risk of stress.
SC
Funding: This work was supported by Zoetis; Morris Animal Foundation exclusively from a partnership
with the Human-Animal Bond Research Institute (D14HA-012, 2014); Newman’s Own Foundation; and
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the Nora Roberts Foundation. The above funding sources did not have a role in the study design; in the
N
collection, analysis, and interpretation of data; in the writing of the report; or in the decision to submit the
A
article for publication.
M
Acknowledgments: The authors wish to thank all the children, families, therapy dogs, handlers, hospitals,
and partners who participated in this study and made this research possible.
D
20
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Figure 1 Back-transformed salivary cortisol concentrations across collection times
0.400
0.350
Mean Cortisol (µg/dL)
0.300
PT
0.250
0.200
RI
0.150
SC
0.100
0.050
U
0.000
N
Hospital
Evening
Session
Mid-Day
Trigger
Morning
A
M
Baseline AAI
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TE
EP
CC
A
24
Table 1 Number, percentage, and types of activities that children and parents participated in during animal-assisted intervention
(AAI) sessions (n=445)
PT
Dog 307 69 212 48
View Dog’s
Photos 144 32 64 14
Brush the
RI
Dog 106 24 16 4
Practice the
Dog’s Cues 99 22 29 7
SC
Discuss Dog
Breeds 62 14 55 12
Discuss
Therapy
U
Dogs 56 13 48 11
Walk the
Dog 53 12 10 2
Take Photo
of the Dog 43 10
N 69 16
A
Play with
Dog’s Toy 42 9 15 3
M
Facilitate
Dog’s Visit
with Staff 24 5 16 4
Collect a
D
Sticker from
Handler 22 5 2 0
TE
Use Lint
Roller 18 4 4 1
Listen to
Dog’s Heart
EP
Beat 13 3 3 1
Teach Dog
New Trick 10 2 5 1
Color a
CC
Picture 8 2 0 0
Put Bandana
on the Dog 8 2 3 1
Get the Dog
Water 6 1 0 0
A
Draw a
Picture of or
for the Dog 6 1 0 0
Read to the
Dog 4 1 3 1
Play a Game 3 1 1 0
Play on
Dog’s Vest 3 1 2 0
25
Table 2 Canine Behavior Ethogram
PT
Licking a person Passing the tongue over any part of the Count each period of licking, i.e. if
person's body multiple licks over and over, just count
once. Then if dog stops licking and
starts again, count again.
RI
Pawing/paw lifting Forearm lifted to a 45 degree angle; Count each time paw is lifted. If dog
paw extended or “waved”; sometimes puts paw down and then lifts again,
paw touches the person count again. Dog is seeking attention.
SC
Play stance/bow Excited and alert affect; bottom raised; Count each time the dog bows.
tail raised and wagging; front of body
lowered; front knees bent; tongue out;
head forward and erect; ears perked up;
eyes wide and bright; dog may jump
U
around and vocalize in anticipation
Pushing snout/Seeking pet Pushing, investigating, or eliciting This is typically a dog nosing a person's
N
contact with the snout at any body part
of the person; "goosing," shoving, or
hand for petting. Count once for each
time the dog "asks" for more petting.
A
poking a person (usually the handler or
someone familiar to the dog)
Raising ears (breed-specific) Ears noticeably raise or perk up This could be in response to seeing a
M
Tail wagging Tail moves repeatedly side to side or up Count once for each period of tail
and down wagging. If tail stops wagging but then
resumes, count again.
Walking/Approach Walking forward; walking towards a Count once for each time the dog
CC
off" involuntarily OR "shaking off" close contact. Count once for each
voluntarily (like when wet or dirty) shaking episode.
Escape Efforts to get away from the eliciting May signal the dog is done visiting -
stimulus by pulling on leash, backing tries to get off the bed and/or walks
up, hiding behind handler, digging, etc. away from client (e.g., away from
client, toward the door). Count once
each time dog initiates the motion.
1
Looking at/to handler Frequent looking at/to handler during Dog seems unsure of what s/he is
interaction with client/patient; gazing at supposed to do - looks to the handler for
handler during interaction guidance or direction. Count once for
each time the dog looks up/at the
handler.
Looking away Head turning away from the person; Dog purposefully turns away from
averting eyes/gaze from the person client who may be trying to get close to
dog's face. Count once each time the
dog turns his/her head.
Oral Behaviors/Lip Licking Tongue out; tongue briefly extended; Count once when you see dog's tongue
PT
lip licking; snout/nose licking; floor extend from his/her mouth. Count as a
licking; swallowing; lip smacking licking period - not each individual
lick. For each period of 5 licks or more,
count as one period of licking.
RI
Panting - excessive or Breathing quickly or in a labored Count once for each panting period. If
prolonged fashion; tongue usually out; abdomen dog stops and resumes, count again.
may noticeably move up and down
SC
Restlessness Frequent changes in posture or Seems dog needs to readjust position -
position; frequent “changes in the state may be physically uncomfortable.
of locomotion”; circling; difficulty Could be coupled with trying to leave
sitting or lying still the bed/room and move toward the
U
door. Count once each time the motion
occurs.
Self-directed behaviors
chewing N
Grooming; scratching; licking; biting; Dog interrupts visiting with client to
chew/scratch on self. Count once for
each chewing/licking/scratching
A
episode.
Yawning Open mouth; inhalation of breath/air Count once each time you see the dog
M
Baring teeth Pulling the upper lips up and back so Typically paired with growling,
D
the teeth are visible (lip "curling"); looking as if dog will bite.
snarling
TE
Barking, yelping, yipping, Relatively brief vocalizations of Not 'talking' on command or vocalizing
whining, or whimpering varying pitch without growly for attention - aggressive or
undertones stressed/unhappy vocalizations.
Biting or attempting to bite Mouth open; teeth exposed; head Different than mouthing during play -
EP
Crouching Body crouched low; legs bent; bottom Dog is/looks backed into a corner and
and head lowered; back arched; tail does not want a person to approach.
may be between hind legs; cowering
Drooling--excessive or in Increased salivation or moisture around Not food-induced - unusual or
A
2
Stare gaze An intense, fixed, and direct gaze into Part of a prey instinct -dog looks as if
the eyes of the person; eyes may be s/he is hunting.
dilated or the whites of the eyes may be
clearly visible
PT
RI
SC
U
N
A
M
D
TE
EP
CC
A
3
Table 3 Frequency of recorded animal behaviors during animal-assisted intervention (AAI) sessions (n=405)
PT
Licking 2.31 3.46 0.15 0.21
Tail Wagging 1.98 3.25 0.13 0.23
Yawning 1.39 1.84 0.09 0.11
RI
Raising Ears 1.24 3.89 0.07 0.21
Panting 1.17 1.36 0.08 0.10
SC
Snout (Pushing snout,
seeking pet) 1.09 1.67 0.07 0.12
Leaning (On the client) 0.97 1.71 0.06 0.10
Lifting Paw 0.97 2.13 0.06 0.14
U
Looking at Handler 0.79 1.32 0.05 0.09
Shaking (Shaking off
body, like when wet)
Walking
0.79
0.46
1.21
0.81
N 0.05
0.03
0.08
0.06
A
Restlessness (Frequent
posture changes) 0.29 1.25 0.02 0.07
M
Looking Away
(Intentionally looking
away from client) 0.26 1.16 0.02 0.07
Self-Directed Behaviors
D
(Grooming, chewing,
etc.) 0.25 0.78 0.02 0.05
TE
Escape (Attempting to
get away from
client/session) 0.21 0.82 0.01 0.04
Rolling Over 0.09 0.42 0.01 0.04
EP
4
Table 4 Relationship between demographic characteristics and canine salivary cortisol and behaviors (N = 406 samples, 23 dogs)
Dog Gender (Female vs. Male) -0.28** 0.09 -0.16 0.17 0.05 0.25
Dog Age (Years) -0.05* 0.02 0.15** 0.03 0.14** 0.04
Handler Experience (Years) -0.01 0.01 -0.04 0.03 0.06 0.04
PT
Breed (Lab/Golden vs. Other) 0.25* 0.09 -0.22 0.17 0.70** 0.25
Note: *p ≤ 0.05, **p ≤ 0.01, b = beta, regression coefficient, SE = standard error.
RI
SC
U
N
A
M
D
TE
EP
CC
A
5
Table 5 Relationship between session characteristics and salivary cortisol (N = 254 samples, 23 dogs) and ethogram stress and
affiliative behaviors (N = 368 samples, 25 dogs)
Stress Affiliative
Cortisol
Behaviors Behaviors
Session Characteristic B SE B SE B SE
0.0 0.0 0.0
Length of Session 0.00 0 0.00 0 0.01** 0
0.0 0.0 0.0
PT
Number of people present -0.03 2 -0.02 2 0.04 2
Number of people 0.0 0.0 0.0
participating 0.03 2 -0.01 2 0.03 2
Note: *p ≤ 0.05, **p ≤ 0.01, b = beta, regression coefficient, SE = standard error.
RI
SC
U
N
A
M
D
TE
EP
CC
A
6
Table 6 Relationship between session activities and coded ethogram stress and affiliative behaviors (N =368 samples, 25 dogs)
Talked to the dog (b = 0.26; p < .0001) Discussed dog breeds and histories (b = 0.15; p =
PT
.002)
RI
Viewed photos of the dog (b= 0.13; p = .006).
SC
Practiced the dog’s known cues (b = 0.11; p= .033).
U
Brushed the dog (b = 0.15; p = .003) Facilitated visit between dog and staff (b = 0.45; p
0.004)
TE
0.043)
EP
0.001)
CC