# HUMAN-ANIMAL INTERACTION (HAI) RESEARCH: A DECADE OF PROGRESS

EDITED BY : Peggy D. McCardle, Sandra McCune and James A. Griffin PUBLISHED IN : Frontiers in Veterinary Science, Frontiers in Psychology, Frontiers in Public Health and Frontiers in Pediatrics

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# HUMAN-ANIMAL INTERACTION (HAI) RESEARCH: A DECADE OF PROGRESS

Topic Editors:

Peggy D. McCardle, Haskins Laboratories, New Haven, CT, United States Sandra McCune, Waltham Centre for Pet Nutrition, United Kingdom James A. Griffin, National Institutes of Health (NIH), United States

Human-Animal Interaction Research

Citation: McCardle, P. D., McCune, S., Griffin, J. A., eds. (2020). Human-Animal Interaction (HAI) Research: A Decade of Progress. Lausanne: Frontiers Media SA. doi: 10.3389/978-2-88963-601-3

# Table of Contents

Evan L. MacLean and Brian Hare

Tiffany Syzmanski, Rita J. Casey, Amy Johnson, Annmarie Cano, Dana Albright and Nicholas P. Seivert

## Editorial: Human-Animal Interaction (HAI) Research: A Decade of Progress

Sandra McCune1 \*, Peggy McCardle2,3, James A. Griffin4 , Layla Esposito4 , Karyl Hurley 5 , Regina Bures 4 and Katherine A. Kruger 6

*1 Waltham Centre for Pet Nutrition, Melton Mowbray, United Kingdom, 2 PM Consulting LLC, Tarpon Springs, FL, United States, 3 Haskins Laboratories, New Haven, CT, United States, 4 Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD), Bethesda, MD, United States, 5 Mars Inc, McLean, VA, United States, 6 School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA, United States*

Keywords: human-animal bond, human-animal interaction (HAI), human-animal relationships, child development, animal assisted intervention, animal assisted activities

**Editorial on the Research Topic**

**Human-Animal Interaction (HAI) Research: A Decade of Progress**

In 2008, the Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD), one of the 27 Institutes and Centers that make up the U.S. National Institutes of Health (NIH), and the WALTHAM R Centre for Pet Nutrition (WALTHAM R ), a division of Mars Inc., entered a public-private partnership (henceforth referred to as "the Partnership") to explore the science of human-animal interaction (HAI), specifically as it relates to children's health and overall development. To take stock of existing research and more fully understand research needs in this area, the partners convened a series of workshops, bringing together researchers and practitioners currently working in HAI as well as individuals with expertise in other relevant fields including ethology, developmental, cognitive, clinical and comparative (animal) psychology, pediatric and veterinary medicine, epidemiology, and public health. Based on the research needs identified, the NICHD established a new research program on HAI and child health and development (1).

Those initial meetings also led to the publication of two edited volumes to disseminate the information from the presentations and the rich discussions that took place. The first volume, Animals in Our Lives (2), provided information about HAI research design and methodology and studies of HAI in child development and human health. The second, How Animals Affect US (3), had a more applied focus, highlighting HAI in family, community, and therapeutic settings and emphasizing the need for evidence-based practice in this relatively young and rapidly growing research area.

Informed by the workshops, NICHD, joined by the NIH's National Institute of Nursing Research, issued the first in a series of Funding Opportunity Announcements (FOAs) (1) partially funded through a gift to the NICHD from Mars, Incorporated under the Partnership. The first FOAs focused on how children perceive, relate to, and think about animals; how pets in the home impact children's social and emotional development and health (e.g., allergies, asthma, mitigation of obesity); and whether and under what conditions therapeutic use of animals is safe and effective. Seven research grants were funded under the initial FOAs, and between 2008 and 2018 the NICHD has issued 8 FOAs and funded a total of 27 research grants in HAI (for current information on funded grants and current FOAs see https://www.nichd.nih.gov/about/org/der/branches/cdbb/ programs/psad/HAI).

#### Edited and reviewed by:

*Mary M. Christopher, University of California, Davis, United States*

\*Correspondence: *Sandra McCune<EMAIL_ADDRESS>
#### Specialty section:

*This article was submitted to Veterinary Humanities and Social Sciences, a section of the journal Frontiers in Veterinary Science*

Received: *11 December 2019* Accepted: *17 January 2020* Published: *18 February 2020*

#### Citation:

*McCune S, McCardle P, Griffin JA, Esposito L, Hurley K, Bures R and Kruger KA (2020) Editorial: Human-Animal Interaction (HAI) Research: A Decade of Progress. Front. Vet. Sci. 7:44. doi: 10.3389/fvets.2020.00044*

As the research investments began to bear fruit the Partnership continued to evolve and new Research Topics emerged involving a wider range of scientific fields. Researchers were documenting the relationship between the impact of HAI and child development, but little was known about the mechanisms underlying these effects. In 2011, a workshop was held on the social neuroscience of HAI, which formed the basis for another edited volume, The Social Neuroscience of Human-Animal Interaction (4), addressing the basic neurobiological mechanisms that underlie the effects observed in HAI. The Partnership also continued to disseminate information regarding new directions in HAI research (5) as well as how new research findings were relevant to clinical applications such as Animal-Assisted Therapy (6, 7) and HAI in school settings (8).

These Partnership workshops, research solicitations, and publications over the past 10 years have promoted the adoption and use of more rigorous designs and methods, raising the bar for the quality of research in HAI. As a result, the field has broadened the scope of studies undertaken, addressing not only correlational studies examining the association between interactions with pets and the subsequent social-emotional benefits generally, but also potential mechanisms for those quantifiable effects, including intervention studies employing randomized controlled trial designs.

In addition to promoting randomized controlled trials, the NICHD-Mars Partnership also has recognized the need to encourage and support more public health research through population representative studies. These efforts have included the development of survey questions/instruments and their inclusion in ongoing large-scale cross-sectional surveys and longitudinal studies that use population representative samples (5).

Embedding pet ownership questions in these studies informs our knowledge of the prevalence of pets and offers a costeffective way to collect data on the impact of pets on health and development for children, adults, and families for secondary analyses. Because data from these studies are publicly available, this also increases the research resources for the field of HAI. While cross-sectional data help describe the relationships between pet ownership and health and development, the Partnership's goal is, where possible, to encourage longitudinal data collection on the same individuals to allow for the study of changes in pet ownership over time and concomitant changes in owner physical and mental health status and overall well-being.

The Partnership also has fostered an increased focus on the health benefits of interaction with animals, including therapeutic and rehabilitative interventions for children and adults with intellectual, developmental, physical, and mental health-related disabilities and other disorders. These studies frequently examine the effects of HAI interventions on both the humans and the animals involved, exploring how the animals may benefit but also suffer stress as the result of their role in the intervention. Such studies are needed to identify appropriate selection, training, and monitoring protocols to ensure the well-being of the animal and the optimal conditions for the therapeutic interaction with the person receiving the intervention.

There is ample evidence that the field of HAI has grown and matured over the last decade (9), including the increased number of academic positions in research and education, the development of HAI Centers of expertise (e.g., Tufts' s Institute for HAI and Purdue's Center for the Human-Animal Bond), and funding and industry support through non-governmental organizations such as the Human-Animal Bond Research Institute (HABRI) and the Horses and Humans Research Foundation (HHRF). Likewise, journals dedicated to HAI research have expanded beyond Anthrozoos (a peerreviewed journal launched in 1987) to include the HAI Bulletin in 2013, which resulted from the establishment of the Human-Animal Interaction Section of Division 17 (Society of Counseling Psychology) by the American Psychological Association (APA) in 2012, as well as the creation of a special section devoted to HAI research in the journal Applied Developmental Science in 2016.

As recognition of the success of this decade-long collaborative effort, the Research Topic "Human-Animal Interaction: A Decade of Progress" highlights the research jointly funded by the Partnership. This thematic series of original research papers addresses a variety of topics within HAI research. Several papers address children's experiences and relationships with pets (Hart et al.; Hurley and Oakes; Kertes et al.; Meints et al.), one on teaching families to read the body language of dogs (Meints et al.), and an Opinion article highlighting potential health benefits of dog walking even when you are not the owner (Chen). There are reports on the social-emotional effects of pet ownership (Jacobson and Chang), and intervention studies of behavioral and biological effects of animal-assisted interventions on stress (Pendry et al.), including stress-reduction and adaptive behaviors in children with Autism Spectrum Disorder (ASD) (Gabriels et al.; Pan et al.), Attention Deficit Hyperactivity Disorder (ADHD) (Schuck et al.), and incarcerated youth (Syzmanski et al.). Three papers address new measures and methods (Guérin et al.; MacLean and Hare; Bures et al.). The final paper, by members of the NICHD-Mars Partnership (Griffin et al.) addresses what will be necessary to sustain and accelerate progress in HAI research over the coming decade. We note that this Research Topic does not reflect all of the research of all the investigators funded under the Partnership, as many have already published their findings and others are still in the data collection phase of their projects.

### AUTHOR CONTRIBUTIONS

All co-authors contributed to the design and writing of the paper. SM, PM, and JG served as Editors for the Research Topic. LE, KH, RB, and KK were not Topic Editors of this Research Topic but co-wrote the Editorial.

### ACKNOWLEDGMENTS

We wish to acknowledge some of the many individuals who supported us in establishing the Public-Private Partnership and developing the field of human-animal interaction research: From Mars, Inc., John Lunde, Megan Sibole Rottcher, Harold Schmitz, Cathie Wotecki, Susan Blount, and Kay O'Donnell; from the NIH, Duane O'Donnell; from the NIH, Duane Alexander, Lisa Freund, Alan Guttmacher, Yvonne Maddox, and Valerie Maholmes.

## REFERENCES

**Disclaimer:** The views expressed in this chapter are those of the authors and do not necessarily represent those of the National Institutes of Health, Eunice Kennedy Shriver National Institute of Child Health and Human Development, or the U.S. Department of Health and Human Services.

**Conflict of Interest:** SM and KH are employed by Mars Incorporated. KK was supported by a grant from Mars Inc. PM was employed by PM Consulting and as a science and ethics consultant by Mars Inc.

The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2020 McCune, McCardle, Griffin, Esposito, Hurley, Bures and Kruger. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

# Infants' Daily Experience With Pets and Their Scanning of Animal Faces

Karinna Hurley 1,2 and Lisa M. Oakes 1,3 \*

1 Center for Mind and Brain, University of California, Davis, Davis, CA, United States, 2 Human Development, University of California, Davis, Davis, CA, United States, 3 Department of Psychology, University of California, Davis, Davis, CA, United States

Very little is known about the effect of pet experience on cognitive development in infancy. In Experiment 1, we document in a large sample (N = 1270) that 63% of families with infants under 12 months have at least one household pet. The potential effect on development is significant as the first postnatal year is a critically important time for changes in the brain and cognition. Because research has revealed how experience shapes early development, it is likely that the presence of a companion dog or cat in the home influences infants' development. In Experiment 2, we assess differences between infants who do and do not have pets (N = 171) in one aspect of cognitive development: their processing of animal faces.  Although at the youngest ages infants with and without pets exhibited the same patterns of visual inspection of these animals faces, by 10 months infants with pets spent proportionately more time looking at the region of faces that contained the eyes than did infants without pets. Thus, exposure to pets contributes to how infants look at and learn about animal faces.

#### Edited by:

Peggy D. McCardle, Consultant, New Haven, CT, United States

#### Reviewed by:

Federica Pirrone, Università degli Studi di Milano, Italy Mitsuaki Ohta, Tokyo University of Agriculture, Japan

> \*Correspondence: Lisa M. Oakes<EMAIL_ADDRESS>
#### Specialty section:

This article was submitted to Veterinary Humanities and Social Sciences, a section of the journal Frontiers in Veterinary Science

> Received: 30 April 2018 Accepted: 18 June 2018 Published: 10 July 2018

#### Citation:

Hurley K and Oakes LM (2018) Infants' Daily Experience With Pets and Their Scanning of Animal Faces. Front. Vet. Sci. 5:152. doi: 10.3389/fvets.2018.00152 Keywords: infant development, pets, experience, cognitive development, human-animal interaction, face processing

### INTRODUCTION

Many families with children have pets (1–3), and there has been significant interest in the connection between experience with animals and development in childhood (4–8). However, few studies have considered the impact of exposure to pets on very young infants (9). Instead, the vast majority of work on how exposure to animals influences development has focused on older children and, often, in therapeutic settings (4, 10, 11). The lack of work on the period of infancy is surprising because it is a developmental period profoundly influenced by experience. For example, experience with particular sounds, faces, and objects contribute to infants' rapidly developing abilities in language (12), facial perception (13), and categorization (14). Why has the effect of pets on infants' development been so neglected? One possibility is that because households without children often have high levels of pet ownership (15, 16) people assume that most families with infants are unlikely to have pets, and thus there are few opportunities for infant development to be shaped by pets. Another possibility is that research on the effect of pet experience on development has not focused on typical cognitive development, as the examples given for the effect of languages, faces, and categorization.

Here we address both of these possibilities. First, we present data on the prevalence of pets in homes with infants between 4 and 12 months of age. These data provide an important context for why researchers should focus on the influence of pets on development during this age range. To preview our findings, we observe that families with infants have companion dogs and cats at similar rates as have been reported for families with older children (17). Thus, there is no reason to assume that infants have less exposure to pets than do children at other developmental stages.

Next, we examine the effect of pet exposure on one aspect of typical cognitive development in infancy, their learning of animal faces. Thus, our work will fit in the context of findings that infants' developing face processing is related to their experience with faces of a particular gender, race, or species. For example, infants have a processing advantage for female faces (18–20), perhaps because most infants have female primary caregivers (21), and therefore, in general, have more experience with female faces. By 3 months infants show preferences for ownrace faces over those from unfamiliar races (22–24), presumably reflecting, at least in part, their daily experience with faces of a particular (parents') race. In addition, experience shapes the development of infants' face processing. Although 3-month-old infants discriminate between individual faces from both their own (parents') racial group as well as from other less familiar racial groups, 9-month-old infants discriminate faces only from their own racial group (25). Similarly, whereas 6-month-old infants discriminate both individual human and monkey faces, 9-month-old infants discriminate only individual human faces and are unable to discriminate between individual monkey faces (26).

We extend this work to examine the effect of daily exposure to companion dogs and cats on infants' developing processing of animal faces. Providing infants with daily experience with monkey faces between 6 and 9 months helped them maintain the ability to discriminate monkey faces (27, 28), and this effect is particularly robust when that daily experience with each animal emphasized animals as an individuals [i.e., looking at pictures of named individuals (28)]. Exposure to a pet in the home, which emphasizes that pet as an individual (i.e., pets are named, they are talked to), may influence infants' perceptual processing of face stimuli similar to that pet. Thus, our results will allow us to generalize the effect of this artificial experimental manipulation to a naturalistic difference that occurs in infants' daily life. Family pets have the potential to have a profound effect on infants' development. Not only do infants with and without pets differ in their amount of exposure to animals, their experience with pets likely differs in other ways given the interactive social nature of domestic animals (29–33) and the fact that pets commonly are considered family members (34–38).

The work presented here builds on previous findings demonstrating that infants who live with indoor pets perceive and learn about images of dogs and cats in the lab differently than infants who do not live with indoor pets (39–43). For example, Kovack-Lesh et al. (41, 43) found that 4-monthold infants with pets responded differently in a categorization task than did infants without pets, at least if they engaged in high levels of looking back-and-forth between the two images during familiarization. Thus, observed differences in infants' responding during test trials appears to have been a function of their past experience. Other work points to differences in how infants actually approach stimuli as a function of their pet experience. Hurley et al. (39) observed that 6-monthold infants with pet experience engaged in more looking and comparison when viewing images of animals than did infants without pet experience, consistent with other findings that infants are more interested in stimuli relevant to their past experience (19, 44). Examinations of eye-movements of 4 month-old infants as they inspected individual images of cats and dogs revealed that infants with pets looked more at the informationally-rich head regions than did infants without pets (40, 42). Thus, experience with dogs and cats in the home appears to have translated into differences in attentional biases when infants processed images similar to that experience. Hurley and Oakes (40) further showed that infants with and without pets did not differ in their visual inspection of human faces and vehicles, suggesting that the effect of such animal experience was specific to images of animals that were similar to the animals common in the everyday experience of infants with pets.

The current work addressed several important unanswered questions. First, none of the previous studies of pet experience examined age-related changes in the effect of pet experience on infants' visual processing of animals. All of the existing work in this area has examined the relation between pet experience and visual processing of animal images in infants at a single age (39–43). We predict from the work on infants' processing of human faces, however, that pet experience will differentially influence how younger and older infants visually process images of animals, presumably as both the result of older infants having more experience—and that experience having more time to influence processing—than younger infants and the result of the effect of experience on development at early ages having a cascading effect on later developing skills and abilities. As described in more detail in the General Discussion section, we assume that daily experience with a pet helps to shape the attentional strategies infants adopt when looking at animal images. Thus, we anticipate that there will be differences in how older infants visually explore or scan images of animal faces as a function of pet experience, although there may be few, if any, differences in how younger infants visually explore or scan animal faces. We tested this prediction by observing separate groups of 4-, 6-, and 10 month-old infants' looking at animal faces. These are key ages in the work on changes in infants' processing of human faces.

A second question we addressed in this investigation is whether the effect of experience would be observed for infants' processing of animal faces. All the previous investigations of pet experience on infants' processing of dog and cat images have used representations of whole animals as stimuli. Although this work has shown that infants with pets have a stronger bias to look at the head and face region of these images (40, 42), we do not know whether differences will be observed for how infants process the faces of animals. Previous work suggests head regions are especially informative for infants' processing of animal images (45, 46), and Mareschal et al. (47) established that infants are sensitive to variations in the facial features of cats and dogs. Moreover, if the effects of experience on infants' processing of human faces reflect general processes, then we should see similar effects for the effect of experience on infants' processing of nonhuman faces. For these reasons, in the present investigation we presented infants with images of novel animal faces.

Finally, we asked how infants' pet experience extended to their processing of different types of animals. The previous work has focused on infants' visual cognitions of images of dogs and cats (39–43). Although (40) showed that the effect of pet experience did not extend to images of human faces and vehicles, we do not know how infants' pet experience influences their processing of other kinds of animals. Therefore, we presented infants with images of dogs and cats, that are likely highly familiar to infants (particularly infants who have pets at home) and images of animals monkeys and sheep, that are likely relatively unfamiliar to infants.

### EXPERIMENT 1

The goal of Experiment 1 was to document the prevalence of pet ownership in families with infants between 4 and 12 months of age. This Experiment will demonstrate that many infants are exposed to companion dogs and cats in their daily lives, and that there are significant opportunities for pets in the home to shape development in infancy.

Both Experiments 1 and 2 were carried out in accordance with the recommendations of the Institutional Review Board of the University of California, Davis. The protocols were approved by the Institutional Review Board of the University of California, Davis. All subjects gave written informed consent in accordance with the Declaration of Helsinki.

### Methods

### Participants

Between 12/13/2007 and 12/12/2014, we asked the parents of 1,270 infants between 106 and 320 days of age (M = 176.70, SD = 61.13) who were visiting our lab about the companion dog and cat animals who live in their homes. There were 648 boys and 622 girls. Infants were full healthy, typically developing fullterm infants recruited from the greater Sacramento Valley region of Central California.

Names of potential participants were initially obtained from the State Vital Records office. All parents who lived within a ∼30-min drive from the lab were sent informational packets describing our work and a general invitation to participate in studies, and parents who were interested in volunteering contacted us. Infants were recruited for this investigation solely based on age, and any infant in our pool who was born full term and who was healthy and typically developing was recruited to participate in this study via phone call or e-mail (depending on parental stated preference when they volunteered). Parents and infants received a certificate and a t-shirt, toy, or book as a thank-you for participation.

The parents of our sample were highly educated. Of the 1,256 mothers who reported their education, all but 17 completed high school, all but 70 had at least some college, and 847 had earned at least a bachelor's degree. Of the 1,196 parents who reported their infants' race, 852 reported their infant to be White, 36 reported their infant to be Black, 56 reported their infant to be Asian, 232 reported their infants to be of mixed race, and 20 reported their infants to be Native Hawaiian, American Indian, or other. Of the 1,196 parents who reported it, 323 indicated that their infant was Hispanic (165 White, 69 mixed race, 66 with no race reported, and the remaining were Black, Asian, Native Hawaiian, American Indian, or other race). Thus, our infants represented the diversity of the community.

### Procedure

When infants came to our lab to participate in a study of infant cognition, parents completed a questionnaire about family demographics (see Appendix). In this questionnaire, parents reported infant birthdate, due date, sex, race, and mother's education and the age of any older siblings. In addition, they reported on their infants' pet experiences by replying verbally to the following question: "Do you have pets?" If the answer was yes they were asked about the number and type as well as whether the pet(s) lived indoors with the family.

### Results and Discussion

To examine the likelihood of proportions, we conducted binomial probabilities of observing the number of occurrences or more given the sample size. We compared the difference in proportions between two groups (e.g., infants with and without siblings, Hispanic vs. non-Hispanic families) with z-ratios for the difference between two independent proportions. We used twotailed tests to evaluate these z-ratios. All binomial and z-tests were conducted using vassarstats.net. We compared group means on continuous variables (e.g., age, maternal education) using twotailed t-tests independent groups, performed using IBM SPSS Statistics for Mac (Armonk, NY: IBM Corp). Our critical p-value for significance was 0.05, except as noted to correct for multiple comparisons.

Of the 1,270 parents who completed our questionnaire, 804 (63.31%) reported having a pet dog or pet cat (or both), a proportion that was significantly different from chance, binomial probability (804 or more out of 1270), p < 0.001 (see **Table 1**). Of the 1,253 families who reported whether or not their pet lived indoors, 696 (55.55% of the sample) reported having an indoor pet, a proportion that was significantly different from chance, binomial probability (696 or more out of 1253), p < 0.001. The numbers of families who had dogs and cats or both are presented in **Table 1**. Clearly, in our sample more families had dogs than cats; 387 62%) of the 626 families who had only dogs or cats had only dogs, a proportion that is significantly different from chance, p < 0.001. Thus, most of the families in our sample had one or more pet, and more than half of the infants in our sample had exposure daily to a pet in the home.

To gain a clearer understanding of the frequency and type of pet ownership in this group, we provide in **Table 1** demographics for families who had any dog or cat (indoor or outdoor) and families without any pets. As is clear from this table, the two groups of infants looked very similar; they both had approximately equal proportion of boys and girls and the average age of the samples did not differ. For the infants who had information about siblings reported, the proportion of infants

without pets who had siblings was significantly greater than the proportion of infants with pets who had siblings, z = 2.23, p = 0.03.

Overall, maternal education did not differ for families who had pets compared to families who did not have pets, t(1254) = 1.25, p = 0.21, d = 0.07. Mother's education was higher for families who only had cats than families who had no pets, t(701) = 3.71, p < 0.001, d = 0.30, families who had only dogs, t(617) = 4.23, p < 0.001, d = 0.35, and families who had both dogs and cats, t(410) = 2.94, p = 0.003, d = 0.29. Mother's education did not differ between families without pets and families who had only dogs, t(842) = 0.63, p = 0.53, d = 0.04, or who had both dogs and cats, t(635) = 0.21, p = 0.84, d = 0.02. Similarly, maternal education did not differ between families who had only dogs and families who had both dogs and cats, t(551) = 0.70, p = 0.48, d = 0.06. We also evaluated these differences for families who reported having indoor pets, and the patterns were identical.

Next we examined how pet ownership varied according to infant race, which is a proxy for the family race (in our sample, all infants have the same race as their parents; if the parents are of different races, the infant is reported as mixed race). For the present purposes we divided the infants into three groups according to reported race: White and not Hispanic, infants who were rated as neither White nor Hispanic, and infants who were reported as Hispanic regardless of race. The proportion of families in each of these groups that had pets is presented in **Table 2**.

In our sample, the proportion of White/non-Hispanic families with pets was greater than the proportion of non-White/non-Hispanic families with pets, z = 5.67, p < 0.001, and than Hispanic families, z = 2.96, p = 0.003. More Hispanic families had pets than did non-White/non-Hispanic families, z = 2.53, p = 0.01. This is not due to the fact that most Hispanic families were White; 165 (51%) of the infants who were reported to be Hispanic were also reported to be White. In addition 95 (58%) of the White/Hispanic families had pets and 100 (63%) of the non-White/Hispanic families had pets. Thus, the differences appear to be a lower rate of pet ownership by families who are non-White and non-Hispanic. However, this finding would need to replicated in a larger, more representative sample before strong conclusions could be drawn about racial differences in pet ownership by families with infants.

What is clear from these data is that many infants have opportunities to learn from household pets, and that this is a naturally occurring difference in experience that could yield different developmental outcomes. Interestingly, infants were not more likely to have a pet and a sibling; more families in our sample with pets had only one child. In addition, although there were no overall differences in maternal education and the presence of a pet, maternal education was highest for families who had only cats than for any other group. These data are the first to our knowledge to describe aspects of the home context of infants under 1 year who do and do not live with pets.

### EXPERIMENT 2

Experiment 1 revealed that ∼63% of the infants between the ages of 4 and 12 months living in our region have daily experience with pets. In Experiment 2, we asked how infants with this experience differed from infants without such experience in their processing of animal faces. Importantly, we examined the effect of animal experience across age, allowing us to determine whether infants with and without pets differed at all points in development, or whether the effect of such experience changed across this developmental period.

### Methods

#### Participants

The final sample included a total of 171 healthy, full-term infants with no known vision problem: 52 infants were 4 months old (M = 125.02 days, SD = 7.46 days; 24 girls and 28 boys), 57 infants were 6 months old (M = 184.91 days, SD = 7.92 days; 27 girls and 30 boys), and 62 infants were 10 months old (M = 304.11 days, SD = 7.89 days; 26 girls and 36 boys). The same self-report questionnaire was used here as in Experiment 1, probing the presence of pets and whether they lived indoors. These parental reports revealed that in our sample 64 infants did not have an indoor pet, 35 had only a cat or cats that lived indoors with the family, 52 had only a dog or dogs that lived indoors with the family, and 20 had both a cat or cats and a dog or dogs that lived indoors with the family; thus the proportion of infants in our sample with pets (63%) was similar to that in Experiment 1. Infants were recruited as described in Experiment 1. We tested 28 additional infants, but excluded their data from the final analyses due to fussiness or inattention (N = 8), equipment or experimenter error (N = 8), ambiguous pet status (i.e., an infant who had a dog for several months and then did not) (N = 1), or failure to provide useable data on the minimum number of trials (N = 11, see Data Processing section below).

In the final sample of 171 infants, 116 infants were reported to be White. The remaining infants were reported to be Asian (N = 4), Black or African American (N = 2), mixed race (N = 38), or other (N = 2); 9 parents did not report the race of their infant. Thirty-seven infants were reported to be Hispanic; of these infants 17 infants were White, 11 infants were mixed race, and 9 infants did not have their race reported. The sample was highly educated; of the 167 mothers who reported their educational background, all but one mother had completed high school, 47 had completed at least some college, and 113 had earned at least a bachelor's degree. Thus, the sample was demographically similar to that in Experiment 1.

#### Stimuli

Stimuli were digitized photographs of 12 different faces from each of four animal categories: cat, dog, monkey, and sheep (see **Figure 1**). Using these four types of images allowed us to compare infants' responding to both relatively familiar and relatively unfamiliar animal faces. Specifically, we selected cats and dogs because they are relatively familiar to infants (even infants who do not have a dog or cat as pet at home likely see one or both types of animals at the homes of friends and relatives, in the park, walking in their neighborhood, etc.), and we selected sheep and monkeys because they are relatively unfamiliar to infants. Thus, these four face types will allow us to determine how general any effect of pet experience is on infants' face scanning; if it extends only to familiar cats and dogs or even to unfamiliar sheep and monkeys. We selected monkeys and sheep specifically because they varied configurally, with the monkey faces being configurally more similar to cat faces (e.g., relatively large eyes, small noses) and sheep faces being configurally more similar to dog faces (e.g., smaller eyes at the top of the face, prominent snout with larger nose at the bottom of the face). Thus, this will allow us to determine if pet experience extends more to some configurations than to others. Finally, we selected sheep and monkeys faces because both species had been used in facial discrimination studies and thus good quality stimuli sets already existed.

Sheep faces came from a photograph stimuli set previously used to study facial discrimination in infants' and adults' (48) as well as in sheep (49). Monkey faces came from a photograph

stimuli set used to understand facial discrimination in monkeys (50, 51). Cat and dog photographs were gathered from breed books and cropped to match in size in Adobe Photoshop. All faces were front-oriented, symmetrical, and similar in breed (dogs were either Golden Labradors or Golden Retrievers) species (all monkeys were tufted capuchins), or coloring and marking (all sheep where white and all cats were brown tabbies). Using Adobe Photoshop, an oval mask was overlaid on the images to make the external contours of the images identical within face type and similar across faces, similar to the mask used in Chien et al. (52). Thus, differences in infants' looking or scanning would not reflect differences in face shape, protrusion of ears, etc., but rather would primarily reflect differences in internal features, such as the prominence of the nose, the top-heaviness, etc. Due to differences in the overall shape of the different faces we created two masks; one mask for the dog and cat faces and another for the sheep and monkey faces. The mask covered the ears of all animals (see **Figure 1**). Images were ∼38 cm × 25 cm in size, subtending ∼21.5 by 14.25 degrees visual angle.

#### Apparatus

A Dell computer was used to present the stimuli and control the experiment. Stimulus images were presented side-by-side in the center of a 37-inch LCD TV monitor (19:9 aspect ratio), and subtended ∼21.5 by 14.25◦ visual angle at a viewing distance of 100 cm. Eye gaze was recorded using an Applied Science Laboratory (ASL) pan/tilt R6 eye-tracker controlled by a second Dell computer. An eye-camera located at the bottom and center of the monitor focused on the infants' right eye; using the image from this camera, the eye-tracker calculated the location of infants' fixations from the reflections of an infrared light source of the cornea and pupil. A wide-angle camera was affixed to the eyecamera to provide an image of infants' heads and torsos. A sensor, attached to an infant-sized headband, was positioned above the right eye and was used to locate the infants' head in a magnetic field produced by a generator located directly behind the parents' chair. This position was communicated to the eye-tracker, which, if necessary, was used to adjust the camera to refocus the infants' eye (e.g., if the infant looked at the parent and then back at the screen). A white curtain separated the infants from the observers and equipment.

#### Procedure

Infants sat on their parents' lap in a dimly lit room ∼100 cm from the monitor and ∼75 cm from the eye-camera. Parents wore occluding glasses in order to reduce any bias their reaction to the stimuli could have on infants' looking. Sessions began with a five-point calibration protocol in which a looming circle was presented at each point: (1) 11.5◦ above and to the left of the central fixation point, (2) 11.5◦ above and to the right of the central fixation point, (3) at the central fixation point, (4) 11.5◦ below and to the left of the central fixation point, and (5) 11.5◦ below and to the right of the central fixation point. As infants fixated at each point an experimenter pressed a key on the computer to record the relative locations of the corneal and pupil reflections when the infant was fixating on that known location. This information was used to calculate the point-of-gaze (POG) for each data sample during the experiment.

Immediately after calibration the experimenter initiated the experimental paradigm. Each trial began with a geometric colored shape (e.g., a purple diamond, green triangle, yellow star) presented at the central fixation point; the shape continuously loomed for 800 ms (from 0◦ × 0 ◦ visual angle to ∼16◦ × 16◦ visual angle) and was accompanied by a randomly selected sound (e.g., buzz, beep, ding). When infants fixated this stimulus (as indicated by cross-hairs superimposed on the stimulus by the ASL eye-tracking system) the experimenter pressed a computer key to initiate the start of an experimental trial.

The experimental trials were 5 s in duration, and on each trial a pair of images from the same category was presented (e.g., two dogs, two cats, two sheep, or two monkeys). We presented two images on each trial, center-to-center distance was 22◦ (the center of each image was ∼11.5◦ to the left or right of midline). Each trial was initiated when infants looked at an attention getter at center of the monitor; thus when the stimuli were first presented, infants were fixating the center of the monitor and they had to move their eyes from fixation to look at either image. A bias to look at a particular region (e.g., eyes, nose) therefore could not reflect infants simply maintaining fixation in the location where the stimulus happened to be presented; rather any observed bias will reflect infants' selecting that region and maintaining their attention to it.

We created a custom program in Adobe Director to control stimulus presentation and randomly order image pairs in blocks of four trials. Each block contained one trial with a pair of dogs, one trial with a pair of cats, one trial with a pair of sheep, and one trial with a pair of monkeys. Thus, infants saw a pair of images from each animal category in each block of four trials. On each trial, a randomly selected clip of classical music (Bach, Beethoven Mozart, Pachelbel, Vivaldi, or Ravel) was played to aid in keeping infants' attention.

If the infant became uninterested in general and looked away from the monitor, the experimenter could present one of several stimuli to recapture their attention. These stimuli included sequences of randomly chosen clips of children's television shows (Teletubbies, Blues Clues, Sesame Street), a cartoon of animated animals singing, a series of pictures of babies accompanied by classical music, and the calibration stimuli. Key commands in the computer program were used to present the stimuli and allowed the experimenter to present any of the attention-getting stimuli between trials if infants' attention needed to be redirected to the center of the screen. There were a maximum of 264 experimental trials, and trials were presented

FIGURE 2 | An example of one possible pair of stimuli presented on a single (cat) trial. To illustrate how we evaluated infants' looking times, Areas of Interest (AOIs) corresponding to the top and bottom halves of the faces are superimposed on the images.

until infants showed signs of disinterest in looking at screen (e.g., fussing, looking at the parent, refusing to look at the screen).

### Results Data Processing

Data processing was similar to that reported in Hurley et al. (40). The point of gaze data was recorded at a rate of 60 Hz, using an online average of 4 samples (the current sample and the 3 previous samples) to minimize noise in the data. In addition, a blink filter was implemented in which pupil loss of fewer than 12 samples was considered a blink. The horizontal and vertical position of the gaze was recorded at each sample with a code to indicate which type of stimulus was presented on each trial. Data were first processed using the software program ASL Results to parse the datastream into trials. Next, we used custom a Matlab routine to determine how may samples fell into prespecified Areas of Interest (AOIs). We evaluated infants' looking in four AOIs: the top and bottom halves of each of the two stimuli presented side-by-side (see **Figure 2**). This approach allowed us to have the same AOIs across faces and species, while having one AOI contain the eye region, known to be important for face processing (53). This approach—of dividing the face into upper and lower halves—has been used in other studies of face processing (54).

The number of samples in each AOI was converted to duration for analysis. We included in the analyses any trial in which at least 200 ms of looking was recorded; across all infants at all ages the analyses are based on an average of 28.49 trials per infant (Range = 4–105, SD = 14.85). All infants who contributed at least one trial of each type (cat, dog, monkey, and sheep) that met this criterion were included in the final analyses (as described in the Participants section, 11 infants failed to meet this criterion).

### Analysis Plan

We tested our hypotheses by examining differences in infants' preferences for the top half of the faces. To examine how infants' scanning of these faces varied by age and pet status we calculated infants' preference for the top half of each type of face. If infants focus more on the eye-region on our faces, as is typical when young infants scan human faces (53), we should see a strong preference for the top half of the faces. If infants scan more broadly—a pattern exhibited by older infants when exhibiting human faces (55)—will should see a weaker top-half preference. To evaluate any effect of age, pet experience, or type of face on infants' top half preference, we conducted Analyses of Variance (ANOVAs) comparing the top half preferences. We conducted follow up comparisons for any significant effects using t-tests, adjusting our criterion of significance to control for multiple comparisons. We also examined infants' preference for the top half by comparing their preferences using one-sample t-tests and Bayes Factors.

### Analyses

We calculated preference for the top half of faces by dividing the looking to the top half of the face by the looking to the top and bottom half combined. We use infants' median top half preference across trials because the median is less influenced than the mean by extreme values. We entered each infants' median top half preference for each stimulus type (dog, cat, sheep, monkey) with pet group and age as the between-subjects variables. This analysis revealed a main effect of trial type, F(3, 495) = 14.64, p < 0.001, η 2 p = 0.08, and a trial type by age group interaction, F(6, 495) = 2.38, p = 0.03, η 2 p = 0.03. The means for this interaction are provided in **Figure 3**. It can be seen in this figure that, overall, there were few age differences in infants' preference for the top halves of cat, monkey, or sheep faces, but that in general older infants had a weaker preference for the top half of dog faces than did the younger infants.

To better understand the age by trial type interaction and how infants' preferences for the top halves of the different face types varied by age, we conducted separate ANOVAs on each age group. The analyses of the top half preferences by 4-month-old infants revealed only a main effect of trial type, F(3, 150) = 7.15, p < 0.001, η 2 p = 0.13. As is evident in **Figure 3**, 4-month-old infants (open bars) had a weaker top half preference for sheep faces than for the other faces. We confirmed this impression by conducting the mean preference scores for each of the face types, using p ≤ 0.008 as our cut-off for significance to control for multiple comparisons. The preference for top halves of sheep faces was significantly lower than that of cat faces, t(51) = 4.51, p < 0.001, d = 0.63, or monkey faces, t(51) = 3.34, p = 0.002, d = 0.46, and the difference between sheep faces and dog faces was marginal, t(51) = 2.68, p = 0.01, d = 0.37. To provide further insight into infants' top half preferences, we compared each preference score to chance (0.50); these comparisons would confirm whether infants looked at the top half of any of the face more than expected by chance.  Their preference for the top half of sheep faces did not differ from chance, t(51) = 1.12, p = 0.27, d = 0.16. Thus, in general, at the youngest age infants preferred the top half of all the faces except the sheep faces which were both relatively unfamiliar and, as can be seen in **Figure 1**, dominated by the nose in the bottom half of the face.

The ANOVA on the mean preference for the 6-monthold infants also revealed only a main effect of trial type, F(3,165) = 8.31, p < 0.001, η 2 p = 0.13, however as can be seen in **Figure 3** the pattern was somewhat different.  In general, 6 month-old infants seemed to have stronger preferences for the top halves of the faces that are configured with larger eyes toward the top than the faces with longer snouts and relatively large noses at the bottom.

Comparisons of the preference for the top halves to chance corroborated this conclusion. Six-month-old infants had clearly significant preferences for the top halves of cat faces, t(56) = 5.09, p < 0.001, d = 0.67, and monkey faces, t(56) = 5.10, p < 0.001, d = 0.68. They had non-significant preferences for the top halves of sheep faces, t(56) = 2.14, p = 0.04, d = 0.28, and dog faces, t(56) = 1.76, p = 0.08, d = 0.23. Bayes factor analyses confirmed that these preferences were ambiguous, at best. For the sheep faces, Bayes factor analyses with a scale r on effect size of 0.707, revealed a Scaled JZS Bayes Factor in favor of the Null of 0.85; the Scaled JZS Bayes Factor in favor of the alternative was 1.18. For the dog faces, Bayes factor analyses with a scale r on effect size of 0.707, revealed a Scaled JZS Bayes Factor in favor of the Null of 1.62; the Scaled JZS Bayes Factor in favor of the alternative was 0.62. Thus, neither the t-tests nor the Bayes Factor analyses provided strong support for the conclusion that 6-month-old infants preferred the top halves of dogs and sheep. In general, therefore, these 6-month-old infants preferred the top halves of faces with large eyes in the top halves, but not the top halves of faces that were dominated by long snouts.

The analysis of the top half preference by 10-monthold infants revealed significant main effects of trial type, F(3, 180) = 4.67, p = 0.004, η 2 p = 0.07, and pet group, F(1, 60) = 4.16, p = 0.046, η 2 p = 0.07. Comparisons of infants' preferences for the top halves of each type of face revealed that overall 10-month-old infants had weaker preferences for the top halves of dog faces than cat faces, t(61) = 3.25, p = 0.002, d = 0.41, and monkey faces, t(61) = 3.44, p = 0.001, d = 0.44; the difference between the preference for the top halves of dogs and sheep did not reach our adjusted criterion of significance, t(61) = 2.02, p = 0.047, d = 0.26. The pet group main effect reflects the fact that across face types, 10-month-old infants with pets had stronger preferences for the top halves of faces (M = 0.65, SD = 0.27) than did 10-month-old infants without pets (M = 0.50, SD = 0.28). Moreover, comparison of the average top half preference to chance revealed that only infants with pets differed significantly, t(39) = 3.52, p = 0.001, d = 0.56; the average top half preference of infants without pets was not different from chance, t(21) = 0.14, p = 0.89, d = 0.03.

Finally, to provide additional insight into the preferences of 10-month-old infants, we compared the preferences for the top halves of each type of face to chance separately for infants with and without pets (see **Figure 4**). The 10-month-old infants with pets significantly preferred the top halves of cat faces, t(39) = 3.75, p = 0.001, d = 0.59, monkey faces, t(39) = 3.55, p = 0.001, d = 0.56, and sheep faces, t(39) = 2.85, p = 0.007,

FIGURE 4 | Mean preference for the top half of each face type by age and pet status. The individual blue circles represent a single infant; the squares represent the mean of each group.

d = 0.45. Ten-month-old infants without pets did not have preferences for the top halves of any faces that significantly differed from chance; cat faces, t(21) = 0.753, p = 0.46, d = 0.16,

dog faces, t(21) = 1.38, p = 0.18, d = 0.29, monkey faces, t(21) = 0.54, p = 0.60, d = 0.11, and sheep faces, t(21) = 0.03, p = 0.98, d = 0.006. Bayes Factor analyses, with an r scale of 0.707, provided modest support for the null hypothesis that the preferences were equivalent to chance for cat faces, Scaled JZS Bayes Factor of 3.47, monkey faces, Scaled JZS Bayes Factor of 3.94, and sheep faces, Scaled JZS Bayes Factor of 4.48. The Bayes Factor analysis did not provide clear support for either the null or the alternative hypothesis for the dog faces. Over time, experience with pets seems to help maintain an infant's interest in the top halves of these animal faces, as 10-monthold infants without pets show a reduced top half preference compared to the other age groups. All of the analyses from the 10-month-old infants lead to the same conclusion: infants with and without pets visually scanned these animal faces differently.

### GENERAL DISCUSSION

The experiments presented here provide important insight into the role of companion cats and dogs on development in infancy. Experiment 1 revealed that more than half of the infants we sampled lived with one or more pet. Thus, pets have the opportunity to have an influence on development for many infants. Experiment 2 showed that between 4 and 10 months, exposure to a pet in the home was related to how infants visually inspected images of animal faces. Although young infants with and without pets responded in the same way to animal faces, by 10 months infants with and without pets exhibited different patterns of visual inspection when looking at these images. Clearly, therefore many infants have experience with pets, and that experience seems to influence at least one aspect of their development.

These findings contribute to two separate literatures. First, they address the literature focused on the role of animals on child development (4–6, 8, 9). As described earlier, little research has examined either the prevalence of pet experience during infancy, or the effect of pet exposure on infant development. The present work addresses both gaps in the literature. In Experiment 1, we show that in our sample, ∼63% of families with infants had household cats or dogs. Clearly our sample is not representative of all families, but does show that the rates of pet ownership in families with infants—at least middle-class families in the Sacramento Valley of California—are similar to those documented in other studies of pet ownership [As reported by the American Pet Products Association (56); http://www.americanpetproducts.org/press\_industrytrends.asp] including in families with children (17). These data confirm that many infants have opportunities to develop in the context of experience with pets, and that this is a real difference in experience between infants. Thus, it is important to understand more about how infants' development is shaped by exposure to and experience with pets.

In addition, the data presented here confirm previous reported findings that exposure to a household cat or dog seems to induce different strategies for learning about images of dogs and cats in laboratory tasks (39–43). That is, we not only documented the prevalence of pet ownership, we also showed how infants' visual investigation of animal faces varied as a function of pet ownership. These results converge with previous findings that infants as young as 4 months visually investigate images of cats and dogs differently as a function of pet ownership (39, 42, 43), and that infants at 4 months learn about images of cats and dogs differently as a function of pet ownership (41). The results we reported here extend this previous work in several ways. First, we showed that these differences a function of pet ownership hold even when infants are shown only animal faces. The previous work revealed differences when infants were shown images of full bodied animals. Thus, not only does this extend previous work showing that by 4 months infants show a bias to look at the heads of whole body animal images as a function of pet experience (39, 42), it shows that previously reported results about the effect of experience on developmental changes in infants' processing and scanning of human faces (21, 27, 57, 58) may extend to the role of experience on their processing of other kinds of faces. Just as previous work suggested a tuning of human face perception between 4 and 9 months based infants' experience with face of a particular race (24, 25, 52, 59, 60), here we show a shift in the specificity of infants' investigation of animal faces as a function of their experience with dogs or cats.

Moreover, the timing of the effects suggests that experience with pets is not a single, unified influence, but rather that exposure to pets may have different effects at different time points. Specifically, previous work showed that pet experience influences young infants' processing of whole body images of animals (39, 42). The current results show that pet experience has an influence on infants' processing of animal faces during the same developmental time period during which infants show shifts in their perception, discrimination, and visual investigation of human faces (24, 25, 52, 54, 59– 62).

Importantly, these results also show that pet experience influences not only infants' processing of familiar animals such as cats and dogs, but that daily experience with a companion animal also has an effect on infants' processing of relatively unfamiliar animals such as sheep and monkeys. Thus, the current investigation addresses the specificity of the effect of infants' pet experience on their face processing. Our results suggest that experience with a pet influences infants' inspection of animal faces beyond their specific pet experience, as at 10 months we observed a difference in how infants with and without pets scanned monkey faces. This effect may reflect a mechanism like that is responsible for the effect of pet experience on children's understanding of biology and living kinds (63, 64).

In summary, the results reported here add to both the literatures on the impact of animals in child development and on the effect of experience on infants' processing of visual stimuli. We showed here that pet experience is pervasive in infancy, and that this experience influences one aspect of infant development. Future research on animals and child development should not overlook the important developmental period of infancy.

### AUTHOR CONTRIBUTIONS

KH and LO both contributed to the design and implementation of the research, analysis of the results, and writing of the manuscript.

### ACKNOWLEDGMENTS

This work was made possible by grants R03HD070651 Awarded by the National Institutes of Child Health and Human Development and BCS 095158 awarded by the National Science Foundation to LO. We thank Karen Leung, Mielle Setoodehnia, Mirjam Harrison, and all the lab members at the Infant Cognition Lab at the UC Davis Center for Mind and Brain for their help in

### REFERENCES

collecting and coding these data. We also thank Jennifer Pokorny and Keith Kendrick for sharing their animal face stimuli. We are especially grateful to the families who participated and made this research possible. This research was submitted by KH as partial fulfillment of a doctoral dissertation for the University of California, Davis. A version of this article was presented at the International Conference on Infant Studies in Minneapolis in 2012.

### SUPPLEMENTARY MATERIAL

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fvets. 2018.00152/full#supplementary-material

the owner: a cross-sectional study in Italy. Dog Behav. (2015) 1:23–33. doi: 10.4454/db.v1i2.14

**Conflict of Interest Statement:** The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2018 Hurley and Oakes. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

# Long-Term Effect of Therapeutic Horseback Riding in Youth With Autism Spectrum Disorder: A Randomized Trial

Robin L. Gabriels 1,2,3 \*, Zhaoxing Pan1,3, Noémie A. Guérin4 , Briar Dechant 2,3 and Gary Mesibov 5

1 Department of Pediatrics, University of Colorado Anschutz Medical Campus, Aurora, CO, United States, 2 Department of Psychiatry, University of Colorado Anschutz Medical Campus, Aurora, CO, United States, 3 Children's Hospital Colorado, Aurora, CO, United States, 4 Department of Comparative Pathobiology, Center for the Human-Animal Bond, College of Veterinary Medicine, Purdue University, West Lafayette, IN, United States, 5 Frank Porter Graham Child Development Institute, University of North Carolina, Chapel Hill, NC, United States

#### Edited by:

Peggy D. McCardle, Consultant, New Haven, CT, United States

#### Reviewed by:

Sophie Hall, University of Lincoln, United Kingdom Mitsuaki Ohta, Tokyo University of Agriculture, Japan

\*Correspondence: Robin L. Gabriels<EMAIL_ADDRESS>
#### Specialty section:

This article was submitted to Veterinary Humanities and Social Sciences, a section of the journal Frontiers in Veterinary Science

> Received: 16 April 2018 Accepted: 20 June 2018 Published: 16 July 2018

#### Citation:

Gabriels RL, Pan Z, Guérin NA, Dechant B and Mesibov G (2018) Long-Term Effect of Therapeutic Horseback Riding in Youth With Autism Spectrum Disorder: A Randomized Trial. Front. Vet. Sci. 5:156. doi: 10.3389/fvets.2018.00156 This paper presents 6-month follow-up data of 44% (N = 64/116) of participants (ages 6–16 years) with a diagnosis of autism spectrum disorder, who participated in a previously-published randomized controlled trial of therapeutic horseback riding (THR) compared to a no-horse contact active control. The objective of this study was to examine whether significant improvements of irritability, hyperactivity, social, and communication behaviors observed in participants randomized to receive a 10-week manual-based THR intervention were sustained 6 months after the intervention conclusion. Participants' caregivers from both the THR (n = 36) and active control (n = 28) groups completed a measure of irritability and hyperactivity behaviors (primary outcome variables). Additionally, only the THR group participants completed the full battery of study outcomes assessments. Between group comparisons examining the extended interval from baseline (1-month pre-intervention assessment) to 6-months after the intervention revealed that the THR group maintained reductions in irritability behavior at a 0.1 level (effect size = 0.32, p = 0.07). (Effect size = 0.32, p = 0.07), which was 73% of efficacy preserved from the primary post-intervention endpoint (within 1-month post-intervention). Hyperactivity behaviors did not sustain this same trend. Comparisons from baseline and 6-months after the intervention revealed that the THR group sustained significant initial improvements made in social and communication behaviors, along with number of words and different words spoken during a standard language sample. This is the first known study to examine and demonstrate the longer-term effects of THR for individuals with ASD and warrants a more thorough evaluation of whether the effects of THR are maintained for at least 6-months after the intervention compared to a control.

Clinical Trial Registration Information: Trial of Therapeutic Horseback Riding in Children and Adolescents with Autism Spectrum Disorder; http://clinicaltrials.gov; NCT02301195.

Keywords: animal-assisted interventions, autism spectrum, therapeutic horseback riding, long-term outcomes, irritability

### INTRODUCTION

Along with the diagnostic social, communication, restricted, and repetitive behavior features of autism spectrum disorder (ASD) this population has particular difficulties with emotion regulation (1). Emotional dysregulation and related aberrant behavior responses (e.g., irritability and aggression) can detrimentally affect the daily social functioning of this population (2). Such issues can also contribute to an increase risk of exhibiting highly inappropriate and unsafe behaviors, the consequences of which can erode the quality of life (QoL) for the child with ASD and caregivers (3–5). The fact that there is no "one-size-fitsall" ASD intervention package (6) fuels a particular interest in seeking complementary and alternative ASD treatment options (7). One increasingly popular practice is the inclusion of animals in interventions to enhance human health, quality of life or wellbeing, known as animal-assisted intervention (AAI) (8). The use of AAI for individuals with ASD has been hypothesized to provide a unique social partnership experience with the animal, one that can reduce arousal levels (i.e., dampen stressed/anxious states) and can address the unique social, communication, and behavior challenges of individuals with ASD (9).

Emerging evidence for the benefits of animals on the health and well-being of individuals with ASD is highlighted by recent systematic literature reviews (10, 11). Research on AAI for ASD has increased in recent years, from only 14 studies meeting inclusion criteria for empirical research between 1989 and 2012, to 28 studies between 2012 and 2015. Early studies reported improvements in social and communication skills, decreases in ASD symptom severity, amelioration of behavior problems (e.g., aggression), reduced stress, and enhanced quality of life (10). However, a majority of these studies lacked methodological rigor, making these findings difficult to interpret or rely upon. Although diverse methods continue to be employed methodological quality of some of the more recent AAI studies have improved (11). In this more recent review of 22 out of 28 AAI studies, social interaction skills was identified as the most consistent outcome reported with additional outcome indications of improved communication skills, positive emotions, and reduced arousal levels (11). In this same review, equines were the most common animal species included in AAI (55% of studies) (11).

A systematic mapping review of equine-assisted activities and interventions (EAAT) studies with the ASD population revealed a wide variety of intervention methods ranging from equine assisted activities (EAA) (e.g., psychoeducational horseback riding, therapeutic riding) involving riding instructors, coaches or trainers, and equine-assisted therapies (EAT) (e.g., hippotherapy, simulated developmental horse-riding) involving therapists (e.g., occupational or physical therapists) and therapeutic riding instructors (12). In 31 of 33 studies reviewed, riding the horse was a key component, but EAA and EAT had different aims. Horsemanship, communication, and social skills were an emphasis of EAAs, with 13 out of 25 involving group sessions. Conversely, the eight EAT studies did not always specify group or individual session type, instead focused on the use of the horse's movement to target physical and sensorimotor functioning. Outcome improvement areas reported by EAA studies included social interactions, communications, sensory processing, movement control, ASD symptom severity, and QoL, whereas EAT studies reported outcome improvements in motor control and adaptive living skills (12).

Although THR appears to be a wide-spread practice that has become popular for individuals with ASD, few studies have systematically validated the effects of THR for individuals with ASD following recommended guidelines for ASD research of therapeutic interventions (13). Such a practice is necessary to guide consumers' AAI treatment choice making and third-party payers' interest in funding evidenced-based AAI. In response to this need, this research team conducted the first known largescale (N = 127) randomized controlled trial (RCT) of THR compared to a no-horse activity control with children ages 6– 16 years diagnosed with ASD (14). Results showed a significant medium effect size improvement in participants from the THR group (n = 58) compared to the control (n = 58) on measures of irritability, hyperactivity, social cognition, social communication, and total words and new words spoken during a standardized language sample.

There is a paucity of research examining the longer-term maintenance of AAI benefits for individuals with ASD beyond immediate outcomes. A recent follow-up study by Hall et al. (15) examined the maintenance of the immediate observed improvements in family functioning and stress made after families of children diagnosed with ASD either acquired a dog or did not (16, 17). This two-and-a-half-year followup revealed maintenance of family functioning gains in the subset of those who followed-up from the intervention group (n = 22) compared to the control (n = 15) (15). One study to date has attempted to prospectively examine residual effects of THR for children with ASD (18). That study conducted a repeated measure, interrupted treatment design to evaluate 21 participants with ASD before and after 10-weeks of THR. An unintentional 6-week break from treatment interrupted the study design. Participant outcome assessment following this initial 16 week-period indicated that participants showed improvements in sensory processing abilities and autism-related symptoms. However, none of these improvements remained when re-evaluating participants after discontinuing THR for 6 weeks. After re-introducing 6 weeks of THR, an immediate follow-up assessment revealed initial improvements resumed. However, of note, this study had several methodological limitations including only teacher-report that limited outcome evaluation to the school environment, lack of a control condition, and an unplanned 6-week break during the initial treatment phase (18). Examining the durability of AAI improvements is an important area of research needed in the growing effort to validate the efficacy of these interventions.

This article presents 6-month follow-up data from a subset of participants who were randomized as part of a previously published RCT to receive either 10-weeks of THR intervention or 10-weeks of a barn activity (BA) control group with no exposure to horses (14). In this study, we examined whether the behavioral, social, and communication improvements remained 6 months after the completion of the THR intervention.

### MATERIALS AND METHODS

The following summarizes the methods of our previously published RCT (14), which was conducted at a Première certified PATH international center follows industry guidelines to insure horse welfare. For additional details concerning participant consent/assent process, inclusion, and exclusion criteria, ASD study diagnostic confirmation, screening, randomization, measures, and interventions, please see the discussion in Gabriels et al. (14).

### Participants

At the onset of the RCT (14), all of the 127 participants ages 6–16 years with a study confirmed diagnosis of ASD were invited to engage in this 6-month follow-up assessment, approved by the Institutional Review Board (IRB) at the first author's institution. Specifically, participants and caregivers completed an informed consent/assent process, giving consent for three evaluation points: (1) baseline assessment, (2) postintervention assessment, and a (3) 6-month post-intervention follow-up assessment contingent on agreement to refrain from continuing participation in THR for 6-months after the initial intervention phase. The informed consent process included mention of monetary incentives offered for each assessment period of the study, including the 6-month follow-up. From the 127 participants enrolled in the RCT (14), only 116 participants were eligible to complete this third study phase because they had completed RCT baseline (pre-intervention) assessments. However, only a subset of these 116 participants, 96 were invited to be included in the follow-up assessment process, because they completed 1-month post-intervention follow-up assessments and chose to refrain from continued participation in THR until after the 6-month follow-up evaluation period. Six months after completing the intervention phase of the RCT (14), the study coordinator contacted these 96 participants. A subset of these 96 participants contacted (64/66.67%) responded (THR group n = 36; control group n = 28). Of the 32 participants who did not complete this third study phase, two were no longer living with the same caregivers, rather were living in community-based placements, and the remainder were otherwise unable to schedule and/or complete study forms. Participating families received compensation for travel to study visits and for completing and returning the study questionnaire.

### Study Design

Following institutional review board-approved informed consent/assent procedures for the RCT (14), participants were randomized in a 1:1 ratio to receive either a 10-week THR group or a no-horse barn activity (BA) control group based on a priori randomization list generated study statistician. This was stratified by participants' nonverbal intelligence quotient (NVIQ) standard score (85 or >85) measured by the Leiter-R (19). Weekly intervention and control group lessons lasted 45-min, consisted of two to four participants, were led by a THR instructor, followed a consistent routine, and were taught horsemanship skills via activities tailored to ASD learning styles outlined in the THR intervention manual (20). Specifically, the THR group participants each had one or multiple assigned volunteers (one horse leader and up to two side walkers) and the BA group participants each had one assigned volunteer. BA group participants had no contact with horses at the riding center, but were just able to view horses from a distance. There was a life-sized stuffed horse present in the BA group for hands-on learning related to the weekly horsemanship topic.

### Six-Month Outcome Measures

Six months following the completion of the intervention phase of the study, the same caregiver who completed baseline (preintervention) study forms for THR (n = 36) and control (n = 28) groups, completed the 6-month follow-up study measures. Only the THR group participants (n = 36) were scheduled to come into the study clinic site for a re-administration of all baseline assessment measures (i.e., language assessment and social-communication caregiver report form). The speech therapist, who had conducted the baseline and post-intervention evaluations as a blinded evaluator, was unblinded at the 6 month follow-up, because only THR participants received the 6-month follow-up language assessment. However, baseline and post-intervention assessments were not available to the speech therapist during the 6-month evaluation period.

The Irritability and Hyperactivity subscales of the Aberrant Behavior Checklist-Community (ABC-C) (21) were the primary outcome measures for the RCT (14). For this follow-up, the subset of caregivers from both groups (THR and BA) were asked to complete the ABC-C (21). The ABC-C is a 58 item symptom checklist that assesses problem behaviors /selfregulation in children and adults with developmental disabilities (22, 23) and is commonly used as a primary outcome measure in psychopharmacological studies with the ASD population (21). Caregivers received this questionnaire electronically or by mail and were asked to report on participants' current (within the past 4 weeks) observed irritability and hyperactivity behaviors.

The persistence of the previously-reported (14) improvements in social communication and social-cognition behaviors observed in the THR group, were again measured using the Social Responsiveness Scale (SRS) (24) completed by the subset of caregivers from the participants who completed the THR intervention. The SRS has high internal consistency and retest temporal stability in males and females with ASD (25).

To evaluate the persistence of word fluency improvements made in the THR group compared to the control from baseline to post-intervention (14), the subset of participants from the THR group were again administered the Systematic Analysis of Language Transcripts (SALT) (26) 6-months postthe THR intervention. The SALT (26) consists of a 5 min standardized language sample that includes software to structure the collection, transcription, and analysis of language samples obtained from individuals, including those with ASD.

TABLE 1 | Demographics for participants with follow-up at 6 months' post-treatment and those without follow-up.

ap-value for comparisons between THR and Barn group among participants with 6-month follow-up.

bp-values for comparisons between participants with 6-month follow-up and those without respectively for THR and Barn participants.

\*\*p < 0.05; \*p < 0.1 (Significant p-values are in bold).

### Statistical Analysis

SAS 9.4 was used for all the analyses (SAS Institute Inc.,)1 . Participant characteristics and outcome data were compared between the THR and BA groups using two-sample t-test or chi square test as appropriate. The outcome analysis used a linear mixed effects model (LMM). For irritability and hyperactivity, the fixed effects of LMM included the classification variables of evaluation time (i.e., baseline, post-THR, and 6-month followup) and group indicator (THR or BA) as well as their interaction. Statistical test of the interaction of group by time was used to examine the significance of efficacy. Cohen's D effect size for efficacy is estimated based on this interaction test using 2 times t value divided by degree of freedom. Other outcome variables collected only for THR participants were also analyzed by LMM. Compound symmetry was the covariance structure used for all LMM analyses.

### RESULTS

### Patient Demographics and Baseline Clinical Data

Summary statistics of demographic and baseline clinical characteristics for the 64 participants who chose to followup 6-months post the initial THR intervention (n = 64) and those participants (n = 52) who did not follow-up are listed in **Table 1**. There were no statistically significant differences between these two groups with respect to demographic and clinical data collected, except for the fact that those participants who did not chose to follow-up tended to travel from farther distances to the riding center (see **Table 1**).

### Between Group Efficacy Maintenance at Six-Month Follow-Up

For the subgroup of participants from the RCT (14) who completed the 6-month follow up assessment (THR group, N = 36; BA group, N = 28), the THR group experienced significantly more improvements (effect size = 0.44, p = 0.016) on the ABC-C (21) Irritability subscale between pre-intervention and within 1-month post-intervention as compared to the BA group (**Table 2** and **Figure 1**). This efficacy is consistent with the larger RCT study results (14). Examining the extended interval from baseline to 6-months after intervention, showed significance at the 0.1 level (effect size = 0.32, p = 0.07) results favoring the THR group for the ABC-C (21) Irritability subscale. The observed effect size at 6 months are 73% of that at postintervention in this sample and 64% of that observed in the larger RCT study. For the ABC-C (21) Hyperactivity subscale, the THR group showed a greater (non-significant) improvement compared to the BA group from pre-intervention to within 1

1 SAS Institute Inc. "SAS" (Cary, NC).

month post-intervention (effect size = 0.32, p = 0.08), in contrast to the significant finding in the original RCT study (14). There was no significant difference; however, when examining the extended interval from baseline to 6 months after intervention for the hyperactivity subscale (effect size = 0.09, p = 0.61), indicating efficacy of THR on hyperactivity was not sustained.

### Six-Month Follow-Up of the THR Group

Consistent with the original RCT study (14), significant improvements were observed in the THR group participants who completed the 6-month follow-up data collection using the SRS (24) Social Communication and Social Cognition subscales along with number of words and different words spoken during the SALT (26) from baseline (within 1-month pre-intervention) to 1-month post-intervention (each p < 0.01). These post-intervention changes sustained from 1-month postintervention to the 6-month follow-up period (see **Figure 2**). Specifically, there was significant improvement for each outcome (p < 0.01) between baseline and 6 months' post-intervention, while there was not a significant difference between 1-month post-intervention and 6 months' post-intervention.

### DISCUSSION

This report presents follow-up data from a subset of participants (n = 64) in a previously published RCT (14) study of the effects of a 10-week THR group intervention on children and adolescents with an ASD compared to a no-horse contact activity control group. Results from this follow-up study show that in the subset of THR participants measured, they retained some of their initial improvements made in irritability compared to the BA control. Additionally, an exploratory analysis of only the THR group revealed that they sustained their significant initial improvements made in social and communication behaviors, along with number of words and different words spoken during a standard language sample for at least 6 months following the completion of the THR intervention.

For reference, the previously published results of that RCT reported that after 10 weeks of intervention (THR or BA control), participants in the THR group showed significantly more improvements on the in irritability and hyperactivity behaviors compared to the BA control (14). The THR group also showed significant improvements on the SRS (24) subscales of social cognition and communication and used a greater number of different words as measured by the SALT (26), while the control group did not show similar improvements (14). The significant irritability and hyperactivity effects began by the fifth week of the THR intervention. Although the BA control showed significant within-group improvements in irritability and hyperactivity behaviors at end of intervention and 6 months after intervention, such improvements could be due to a variety of factors other than the BA group (e.g., placebo response). It would be misleading to make conclusions about the effects of this active (BA) control intervention due to the absence of a nonintervention control for comparison, a necessary element to test treatment effects as discussed in the literature [e.g., (29, 30)].

bCohen's D Effect size for efficacy at EoT or 6 months, estimated by 2 times t value divided by sqrt (DF).

\*\*p < 0.05; \*p < 0.1 (Significant p-values are in bold).

These results suggest that THR may be an effective complementary intervention to enhance social and verbal core symptoms of ASD, and to reduce irritability behaviors. Given the results of this study, particularly the lingering effects on irritability behaviors, we hypothesize that our THR manualbased approach may induce a reduction in arousal states, dampening stress/anxiety, in youth with ASD. Therefore, an important next step might be to examine the physiological regulation mechanisms involved in THR may explain (at least partially) improved outcomes in youth with ASD. Additionally, this study's finding of the long-term sustained improvements in irritability behaviors have clinical practice implications for youth with ASD that can add to the current standard of practice of administering anti-psychotic medications (i.e., Risperidone and

FIGURE 1 | Profile of irritability (IRR) and hyperactivity (HYP) over three assessment periods. Note, the typical clinical threshold for the ABC-C irritability subscale is >14–16 in psychopharmacology clinical trials for the ASD population [e.g., (27, 28)].

aripiprazole) to reduce symptoms of irritability in this population (ages 5–16 years and 6–17 years) (31–33). For example, it has been proposed that THR might be a safe adjunct intervention to facilitate lowering medication dosages in this population (34). Finally, this study expands the AAI research base by prospectively examining the residual effects of THR for children with ASD.

The limitations of this study include its small sample size due to the high dropout rate 6 months following the initial intervention phase. This limits the validity of the results, as findings may not represent the greater population of youth with ASD. Another limitation is the fact that for those participants who did not chose to follow-up, attrition might be because they lived farther away from the study site. This also presents a possible selection bias. Even though we only included participants who refrained from engaging in THR for 6-months following the initial intervention, we did not specifically assess what other, if any, contact with horses was made during that time, which is a limitation. Another limitation is the fact that this study did not assess the efficacy of THR compared to the BA control group on all outcome measures employed in the previously published RCT (14). This limits the validity of these study results and warrants a more thorough evaluation of whether the positive effects of THR can be maintained for at least 6-months after the THR intervention compared to a control.

Despite these limitations, this study provides useful preliminary data to both support and extend the significant findings from our previously published pilot study and RCT (14, 35). This study also provides suggestions for future investigations of the longer-term benefits of THR in children and adolescents with ASD. For example, future investigations should consider the addition of incentives to lower follow-up attrition rates such as conducting outcome evaluations in closer proximity to participants' residence and providing increased monetary

incentives for completing follow-up assessments. Future THR studies may consider collecting follow-up outcome assessments at several time points post-intervention to elucidate information regarding the lingering time course of outcome improvements. Finally, additional long-term outcome research will help to establish empirical evidence for THR as a valid intervention for youth with ASD, one that leads to the acquisition and long-term maintenance of behaviors skills that may enhance the quality of life for individuals with ASD and their caregivers.

### AUTHOR CONTRIBUTIONS

RG was the principal investigator of this study and contributed to writing the majority of this manuscript. ZP served as the statistical expert for this study and wrote the result section of this manuscript. GM served as a consultant for this study and provided editorial edits to this manuscript. BD served as the clinical coordinator for this study and provided editorial edits to this manuscript. NG assisted in writing the introduction of this manuscript.

### REFERENCES

### ACKNOWLEDGMENTS

Portions of the research described in this study have been previously presented at the International Meeting for Autism Research in May 2012 (Toronto, CA) and the Society for Research in Child Development in April 2013 (Seattle, WA). This research was supported by the NIH/National Institutes of Nursing Research grant NR012736-01. Luitpold Pharmaceuticals donated Adequan R medication for the horses in the study in collaboration with the riding center's veterinarian. The authors would like thank the families and children who participated in this study as well as our colleagues who assisted with this project: John Agnew, Natalie Brim, Laurie Burnside, Tina Farrell, Oren Gordon, Syd Martin, Shana Holderness, Amy Shoffner and the staff of the Colorado Therapeutic Riding Center, particularly Carol Heiden, Jody Howard, Heather McLaughlin, Mary Mitten, Penelope Powell and Sharon Van Boven. We also thank PATH International for supporting this study as well as Stephanie Luallin and James Heathers for their technical assistance formatting sections of this manuscript.

**Conflict of Interest Statement:** RG is a co-author of the book, Growing Up with Autism: Working with School-aged Children and Adolescents (Guilford Press) and the book, Autism from Research to Individualized Practice (Jessica Kingsley Publishers), from which she receives royalties. Current grant funding for RG provided by Simons and Lurie Foundations and The Human-Animal Bond Research Institute (HABRI) Foundation.

The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2018 Gabriels, Pan, Guérin, Dechant and Mesibov. This is an openaccess article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

# Children's Relationship With Their Pet Dogs and OXTR Genotype Predict Child–Pet Interaction in an Experimental Setting

#### Darlene A. Kertes1,2 \*, Nathan Hall3 and Samarth S. Bhatt1

1 Department of Psychology, University of Florida, Gainesville, FL, United States, 2 Genetics Institute, University of Florida, Gainesville, FL, United States, 3 Department of Animal and Food Sciences, Texas Tech University, Lubbock, TX, United States

Human–animal interaction (HAI) research has increasingly documented the important role of pet dogs in children's lives. The quality of interaction between children and their pet dogs, however, is likely influenced by individual differences among children as well as their perceived relationship with their pet dog. Ninety-seven children aged 7–12 years and their pet dogs participated in a laboratory protocol during which the child solicited interaction with their dog, from which time petting and gazing were recorded. Children reported on their perceived relationship with the pet dog via interview. Children provided saliva samples, from which a polymorphism in the oxytocin receptor, OXTR rs53576, which has long been implicated in social behavior, was genotyped. The results showed that OXTR genotype and children's perceived antagonism with the pet dog predicted the amount of petting, but not gazing, between children and their pet dogs. This research adds to the growing body of HAI research by documenting individual differences that may influence children's interactions with animals, which is key to research related to pet ownership and understanding factors that may impact therapeutic interventions involving HAI.

Keywords: human–animal interaction, relationships, child, petting, dogs, OXTR, oxytocin receptor gene, oxytocin

### INTRODUCTION

Human–animal interaction (HAI) research has increasingly documented the important role of pet dogs in providing social support to children (e.g., Friedmann et al., 1983; Kotrschal and Ortbauer, 2003; Anderson and Olson, 2006). However, the bulk of this research has been descriptive or correlational in nature, with long-standing concerns about methodological rigor (Griffin et al., 2011) and few well-controlled laboratory experiments that afford greater confidence to the validity of results (Wilson and Barker, 2003). Our group has previously reported that children randomly assigned to experience a standard laboratory stressor accompanied by their pet dog for social support reported feeling less stressed compared to children who completed the stressor with their parent present or with no social support (Kertes et al., 2017).

#### Edited by:

Peggy D. McCardle, Peggy McCardle Consulting, LLC and Haskins Laboratories, United States

#### Reviewed by:

Sabrina E. B. Schuck, University of California, Irvine, United States Kristine Ann Kovack-Lesh, Ripon College, United States

> \*Correspondence: Darlene A. Kertes<EMAIL_ADDRESS>
#### Specialty section:

This article was submitted to Developmental Psychology, a section of the journal Frontiers in Psychology

Received: 24 May 2018 Accepted: 26 July 2018 Published: 05 September 2018

#### Citation:

Kertes DA, Hall N and Bhatt SS (2018) Children's Relationship With Their Pet Dogs and OXTR Genotype Predict Child–Pet Interaction in an Experimental Setting. Front. Psychol. 9:1472. doi: 10.3389/fpsyg.2018.01472

Indeed, petting, and to a lesser extent gazing, have been suggested as potential mechanisms by which HAI impact humans by altering their emotional and physiological state (e.g., Odendaal and Meintjes, 2003; Shiloh et al., 2003). Among adults, petting is associated with reduced perceived stress or anxiety (Shiloh et al., 2003; Barker et al., 2005), increased immunoglobulin A (Charnetski et al., 2004), lower heart rate or blood pressure (Jenkins, 1986; Vormbrock and Grossberg, 1988; Demello, 1999; Handlin et al., 2011), and changes in β-endorphins, prolactin, β-phenylethylamine, oxytocin, cortisol, and dopamine (Odendaal, 2000; Barker et al., 2005). Adult owner-pet gazing has been linked with increased oxytocin levels (Nagasawa et al., 2009, 2015). Among children, petting during child–dog interaction has been associated with lowered cortisol stress response (Kertes et al., 2017) and positive affect (Kerns et al., 2018). The vast majority of research on HAI with children has focused on dog presence, which has been linked with reduced blood pressure (Friedmann et al., 1983) perceived stress (Kertes et al., 2017), enhanced emotional stability in the classroom (Anderson and Olson, 2006), increase social interaction, and decrease aggression and hyperactivity (Kotrschal and Ortbauer, 2003), and reduced distress to a routine medical procedure (Vagnoli et al., 2015).

Its potential benefits notwithstanding, the degree to which children's interactions with their pet dogs spontaneously include petting and gazing may be influenced by individual differences in children's perceived relationship with their pet dog. To date, the majority of research on pet owners' feelings toward their pets have centered on positive emotions (Johnson et al., 1992; Cromer and Barlow, 2013). This area of research has shown that children and adults alike report strong positive feelings toward their pet dogs (Serpell, 1996; Daly and Morton, 2006; Kurdek, 2008). Noticeably absent from most HAI studies is the role of perceived negative aspects of the child–pet relationship, such as feeling annoyed with or hassled by interactions with the pet. A more complete evaluation of effects of children's feelings toward their pet necessarily involves inclusion of both positive and negative components to children's perceived relationships (e.g., DeRosier and Kupersmidt, 1991; Furman and Buhrmester, 1992; Shantz and Hartup, 1992; Van Horn and Cunegatto, 2000; Moilanen and Raffaelli, 2010).

Another factor that may contribute to individual differences in children's interactions with their pet is variability within the oxytocinergic system. Oxytocin is a hormone and neuromodulator shown to be involved in a variety of social behaviors (Carter, 2014). Oxytocin is linked with affiliative behavior (Insel, 1992), formation of social bonds (Lim and Young, 2006), and responses to stressful social situations (Neumann et al., 2000; Kirsch et al., 2005).

Endogenous circulating oxytocin effects are influenced by actions at the oxytocin receptor. This receptor is encoded by the gene OXTR, which is variably expressed across individuals. Among the most commonly studied genetic polymorphisms at OXTR is rs53576, involving a guanine (G) to adenine (A) substitution. Genetic variation at this locus has been associated with both prosocial and negative behaviors. For example, A carriers, (i.e., individuals with the AA or AG genotype), compared to those with the GG genotype, have demonstrated lower levels of interpersonal empathy (Rodrigues et al., 2009; Smith et al., 2014), trust (Krueger et al., 2012), as well as lower self-esteem (Saphire-Bernstein et al., 2011), and higher negative affect and loneliness (Lucht et al., 2009). Among adolescents, A-carriers are reported to be less responsive to parental support (Smearman et al., 2016). Consistent with the differential susceptibility hypothesis (Belsky et al., 2009), it has been suggested that OXTR rs53576 may be one of a set of susceptibility loci in the genome, whereby genetic variation influences an individual's sensitivity to the social environment (Kim et al., 2010).

Notably, the extensive literature examining OXTR rs53576 in relation to social behavior has focused exclusively on human social interaction. To date, there are no published studies examining OXTR genotype with respect to children's interaction with animals. This is notable because interaction with and ownership of lay or trained therapy dogs is increasingly becoming a mainstay of clinical interventions for children with anxiety disorders, autism spectrum diagnoses, or a history of maltreatment, on the assumption that interacting with animals is particularly beneficial for individuals for whom social interactions are challenging (Nimer and Lundahl, 2007). The present report is the first to assess whether the OXTR genotype among children is related to HAI.

This study focused on typically developing children in middle childhood (aged 7–12 years). During this developmental period, the amount of time children spend with parents declines dramatically compared to earlier ages (Lam et al., 2012). Although parents continue to be important social partners, in middle childhood, children begin to rely on a broader network of social support figures compared to earlier ages, including pets (Bryant, 1985).

The purpose of the present study was to test whether children's perceived relationships (including both positive emotional support and negative interactions) along with child genotype at the OXTR rs53576 polymorphism predict directly observable child–pet interaction. To achieve this aim, we assessed two essential elements of child–pet interaction, petting, and gazing, via direct behavioral observation in the context of a controlled laboratory environment with minimal distractions. Based on the extant literature linking OXTR rs53576 genotype to social behavior, we expected that children who are A-carriers would differ from those with the GG genotype with respect to the amount of time spent petting and gazing with their pet dogs. Because of the complex associations of the OXTR genotype with respect to social behavior, and the fact that this is the first study to examine the rs53576 polymorphism with respect to HAI rather than human social interactions, we did not specify a priori directional predictions for the OXTR genotype. With respect to children's relationships, we anticipated that children's perceived relationship with their pet dogs, as reflected in higher levels of perceived support and lower levels of perceived negative interactions, would be associated with higher levels of petting and gazing with their pet dogs. Children were also asked about their perceived relationship with the mother, which was included on conceptual grounds for their key role in social emotional development, and to evaluate whether child–parent relationships were related to child–pet interactions.

### MATERIALS AND METHODS

fpsyg-09-01472 September 4, 2018 Time: 9:43 # 3

### Participants

Participants were 97 children (49 boys; 48 girls) accompanied by a parent (81% mother) and pet dog. Participating families were recruited through locally distributed mailings, flyers, and radio and TV advertisements. Interested families contacted the research lab and were screened for eligibility. To be eligible for the study, children could not have any diagnosed physical or behavioral health conditions, and the pet dog must have lived with the family for at least 6 months and have no history of aggression. If multiple dogs resided in the home that met inclusion criteria, the family selected one dog based on the child–pet relationship to accompany the child to the research lab.

Child age ranged from 7 to 12 years (M = 10.3 years, SD = 1.32) Child ethnicity was reported by parents as follows: 11% Hispanic; 89% non-Hispanic. The majority of the sample was White (84%), with the remainder reporting their race as follows: 7% two or more races; 3% Latino; 2% Native American; 2% African American, and 2% Asian.

### Procedure

Procedures were approved by the University of Florida Institutional Review Board and the Institutional Animal Care and Use Committee. All procedures took place in three adjacent rooms – a waiting room, interview room, and experimental testing room – at the research laboratory at the University of Florida. Children were aware of their parent's and dog's location at all times. All rooms were temperature controlled and water was available for the dog.

At the start of the study visit, parents provided written informed consent in the waiting room. The study was also explained to children verbally for purposes of oral assent.  Then, the child accompanied an experimenter to the interview room, decorated in child-friendly décor while the dog remained with the parent in the waiting room.

In the waiting room, parents completed questionnaires providing basic demographic information on their child, family, and pet dog. Parents also provided information about the breed of the dog, which was subsequently classified into breed groups. Children's pets included lap/toy dogs (n = 31), sporting breeds (n = 20), herders (n = 18), terriers/ratters (n = 12), bully/fighting breeds (n = 11), and unknown mixes (n = 5). A research assistant was present throughout to answer any parent questions.

### Children's Perceived Relationships

In the interview room, children completed an experimenterassisted questionnaire about their relationships with their mother and their pet dog using the Network of Relationships Inventory (NRI) (Furman and Burmheister, 1985). The original NRI, comprised of 21 items, was designed and has been validated for assessing relationship qualities across a broad variety of social relationships, including but not limited to parents, teachers, and peers. An example item from this measure is, "How often do you tell this person everything that you are going through?" The measure contains 10 subscales typically collapsed into two broader scales, termed Support and Negative Interactions. We have previously evaluated the NRI among children owning pet dogs to determine the relevance of items for assessing child–pet relationships. With the exception of two subscales, Instrumental Aid and Conflict, the remaining subscales were retained as applicable to child–pet relationships (Hall et al., 2016).

The NRI items tapping relationship with the mother was scored as recommended by the scale developers (Furman and Burmheister, 1985). Then, the overarching dimension of Support was created by computing the mean of the items on the subscales Companionship, Intimate Disclosure, Nurturance, Affection, Admiration, Reliable Alliance, and Instrumental Aid. The dimension of Negative Interactions was computed as the mean of the scores on Conflict and Antagonism.

The NRI pet items were subjected to a principal component analysis (PCA) to determine whether a two-dimension solution was appropriate with the more limited set of subscales assessed for child–pet relationships. As described in the Section "Results," a two-dimension solution was deemed appropriate for the data, and therefore the subscale means were computed and averaged into the two broad dimensions as follows: Support (Companionship, Intimate Disclosure, Nurturance, Affection, Admiration, Reliable Alliance) and Negative Interactions (Antagonism).

### Behavioral Assessment of Child–Pet Interaction

The child and pet dog were brought to the experimental testing room for behavioral assessment of interaction between the child and pet. Specifically, this assessment measured the proportion of time the child and dog spent interacting while the child was sitting quietly in a room (4.5 m by 3 m) that contained a chair, desk, and lamp for 10 min. This task was based on components of past sociability tests (e.g., Barrera et al., 2010; Jakovcevic et al., 2012), but were simplified such that the child could implement the protocol with brief instruction. The child sat in a chair in the center of a 1 m radius semi-circle marked with tape on the floor. The dog handler brought the dog to the opposite end of the room, where the dog was able to greet a second observer for approximately 1 min before beginning the task. The child was asked to direct attention to the dog, and call the dog over twice while remaining seated, once at the beginning of the 10 min session and again after the first 5 min. The child was asked to otherwise remain neutral unless the dog entered the semi-circle. If the dog entered the circle the child was told to interact with it as if they were at home, to capture natural variability in child– pet interaction. During the assessment, the handler and observer stood along the wall opposite of where the child was seated for an unobstructed view of the child–pet interaction.

The handler and the observer, both trained in coding dog behaviors, scored each session live on two dimensions: gazing and petting. Each behavior was scored using partial-interval recording by breaking the 10 min session into 120 5 s. epochs. If a target behavior occurred during that epoch, the interval was scored. The percentage of epochs during which a target behavior occurred was averaged across the scorers. Gazing was defined as the percentage of intervals in which the dog and child were facing each other. Petting was defined as the percentage of intervals in which the child made contact with the dog with their hand. Interclass correlations among the two coders was 0.85 for gazing and 0.99 for petting.

#### Genotype Assessment

fpsyg-09-01472 September 4, 2018 Time: 9:43 # 4

Children were asked to provide a 4 mL saliva sample by passive drool into Oragene-DNA (OGR-500) saliva collection tube (DNA Genotek, Kanata, ON, Canada), which was stored at room temperature until the DNA extraction step. DNA extraction was performed using our lab's standardized protocol. Briefly, 750 µl of the content from OGR-500 tube was incubated at 50◦C in a GeneMate dry bath (Bioexpress, Kaysville, UT, United States) for 2 h, followed by incubation on ice for 10 min and centrifugation at 21,100 × g for 10 min. The DNA was precipitated by transferring the supernatant to a tube containing 750 µl of ethanol, mixing the content gently, incubating at room temperature for 10 min, and centrifuging at 16,000 × g for 3 min. The DNA pellet was washed using 70% ethanol, dried at room temperature, dissolved in 100 µl TE buffer and stored at −80◦C. The DNA quality and quantity was measured using NanoDrop 2000 spectrophotometer (Thermo Fisher Scientific, Wilmington, DE, United States). Genotyping was performed using TaqMan Genotyping Master Mix (Applied Biosystems, Foster City, CA, United States), TaqMan SNP Genotyping assay (Applied Biosystems, Foster City, CA, United States) for OXTR (rs53576), with the StepOnePlus real time PCR system (Applied Biosystems, Frederick, MD, United States), according to the manufacturer's instructions. PCR was performed using 10:l reaction mix with 1.5 ng DNA and the following cycling conditions: 60◦C for 30 s, 95◦C for 10 min, 40 cycles of 95◦C for 15 s and 60◦C for 1 min, 60◦C for 30 s. Allelic discrimination was performed using StepOne v.2.1 (Applied Biosystems, Frederick, MD, United States).

### Statistical Analysis

Statistical analyses were conducted in R version 3.3.2 (R Core Team, 2016). A hierarchical regression framework with backward selection was utilized to test for significant predictors of two dimensions of child–pet interaction, with predictors of petting and gazing tested in separate models. Tested predictors included demographics, relationship qualities, and child genotype.

### RESULTS

### Evaluating the NRI to Assess the Child–Dog Relationship

We first calculated the mean scores for each subscale for the child–dog relationship. We then conducted Principal Component Analysis on the scaled scores of each subscale. Two components explained 71% of the variance (55 and 16% respectively). The loadings of each component are shown in **Table 1**. Inspection of the loadings suggests a two-factor solution identical to Support and Negative Interactions used for computing summary scores for the child–mother relationship. This suggested that these two summary scores can be computed similarly for the child–dog relationship.

### Descriptives

Descriptive statistics of child-reported relationship qualities and behavioral observation of child–pet interaction are shown in **Table 2**. Genotype assessment of rs53576 yielded the following genotypes: 41% GG, 53% AG, and 6% AA. These proportions are comparable to other U.S.-based studies (see for review Luo and Han, 2014). As is common in analysis of rs53576, the AG, and AA genotypes were combined into one genotype group, termed A-carriers, yielding two genotype groups for analysis, GG homozygotes, (41%) and A-carriers (59%).

### Analysis of Petting

Predictors of child–dog petting during the child–pet interaction task were determined via regression analyses using backward selection to obtain a reduced model with the strongest predictors. An initial model included all predictors (demographic covariates, child self-reported relationship qualities, and child genotype). The initial model suggested that petting was associated with child age [F(1,84) = 4.18, p = 0.044], OXTR rs53576 genotype [F(1,84) = 6.15, p = 0.015], and Negative Interactions with the dog [F(1,84) = 6.31, p = 0.014]. Specifically, more petting was observed with older child age, OXTR rs53576 A-carrier status, and lower child-reported Negative Interactions with the pet dog (see **Figure 1**). Petting was not associated with child sex [F(1,84) = 0.37,

TABLE 1 | Principal component analysis (PCA) loadings of dog NRI subscales.

Loading absolute values >0.4 are in bold.

TABLE 2 | Descriptive statistics for child self report relationship qualities and behavioral observation.

FIGURE 1 | The proportion of time spent petting during a child–dog interaction task was independently predicted by child age, child genotype, and children's self-reported relationship with the pet dog. (A) Higher levels of child-reported negative relationships with the pet dog was associated with less petting. The relationship effect is shown averaged across child genotype and illustrates the overall main effect for the child–pet relationship. The regression line shows the final model prediction with the shaded area indicated standard error of the mean. (B) Older child age is associated with more time spent petting. Lines shows reduced model prediction for each genotype and shading indicates standard error of the mean. (C) Children who are A-carriers at the OXTR rs53576 genetic polymorphism, compared to GG homozygotes, engaged in more petting during the child–pet interaction.

TABLE 3 | Akaike's information criterion (AIC) for each step in the regression predicting petting using backward regression.

Values are shown for each variable successively dropped from the model to achieve the best fitting results.

p = 0.54], dog breed group [F(5,84) = 1.47, p = 0.21], childreported Support from dog [F(1,84) = 1.09, p = 0.300], or either of the two child-reported measures of relationship quality with the mother [F(1,84) = 0.53–1.21, p = 0.27–0.47]. To obtain the most parsimonious model for our dataset, the model was subjected to backward selection using the Step routine, which identifies the most parsimonious model based on Akaike's information criterion (AIC; see **Table 3** for AIC values at each regression step). All three significant predictors – child age, child genotype, and the Negative Interactions dimension of the child-reported relationship measure – were retained in the final model, as shown in **Table 4**.

### Analysis of Gazing

A comparable regression model was created for gazing during the child–pet interaction. The initial model including all predictors revealed that none of the demographic, genotype, or relationship quality variables was significantly associated with gazing (F's = 0.01–2.14, p's > 0.15). The backward selection procedure was implemented to yield the most parsimonious

TABLE 4 | Final regression model of significant predictors of child–dog petting during behavioral observation.

model. The final model of gazing during the child–pet interaction task included only child age as a predictor, however, the association was not statistically significant (F = 2.28, p = 0.13; see **Table 5**).

### DISCUSSION

The present study was the first to test whether the OXTR genotype and children's perceived relationships with their pet dogs are related to HAI, specifically, petting and gazing. The research design simulated a common, naturally occurring HAI, in which human owners call over their pets, within the context of a controlled laboratory experiment with minimal distractions. On average across children, the total time spent petting was approximately 50% of the 10 min interaction period. The results showed that variation at the OXTR polymorphism rs53576 was associated with the proportion of time spent petting during child–pet interactions. Specifically, A-carriers engaged in more petting than children with the GG genotype. This observation is noteworthy given that OXTR rs53576 has previously been suggested as a genetic locus associated with sensitivity to the social environment. Prior research with typically developing children has demonstrated that A-carrier youth are less responsive to parental support (Smearman et al., 2016) and to social consequences of peer relational aggression (Kushner et al., 2017), and show lower levels of interpersonal empathy (Rodrigues et al., 2009; Smith et al., 2014), trust (Krueger et al., 2012), and self-esteem (Saphire-Bernstein et al., 2011). This may be relevant to growing trend of incorporating HAI into behavioral therapy with children for whom human social interactions are challenging (Nimer and Lundahl, 2007; Silva et al., 2018). Although little empirical research has been conducted in this area, there is preliminary evidence that dogs may be preferred social partners for such children. Children with autism, a neurodevelopmental disorder in which social deficits are common, prefer to interact with a dog over another person or toy (Prothmann et al., 2009). Children with anxiety disorders tend to spend long durations interacting with a pet dog but tend to engage in fewer interactions with another person compared to children with other behavioral health problems (Prothmann et al., 2005). Although highly speculative, our results contribute to emerging evidence that pet dogs may be an important source of social interaction for children that have difficulty in other social environments.

The results of this study also demonstrated that children's selfreported negative interactions in the context of their relationship with their pet was related to the proportion of time spent petting the dog. Specifically, higher levels of antagonism, reflecting children's reports that they and their dog hassle each other, annoy each other, and "get on each others' nerves," spent less time engaged with petting. Children's perceptions of support, reflecting items tapping aspects of affection, companionship, and other positive features, were not associated with the proportion of time spent petting. Of note, this was the first study that simultaneously assessed both positive and negative components of children's relationships with their pet dog. Psychometric data from the principal components analysis demonstrated that children's responses about positive and negative relationship qualities were distinct measurable aspects of the child–dog relationship that paralleled the relationship dimensions measured for the child–parent relationship. The observation that negative interactions, and not support, was associated with petting speaks to the need to incorporate both positive and negative aspects of relationships in HAI research.

We also observed that older child age was associated with more time spent petting. This observation was of interest in light of the broad consensus in the developmental literature that, beginning in middle childhood, children spend proportionally less of their social time with parents and more time with other social partners (Lam et al., 2012). Research with 7–10 year old children has shown that with age, children broaden their network of social support figures, including pets (Bryant, 1985). With age, intimate disclosure also declines to parents whereas it rises with other social partners such as peers (Buhrmester and Furman, 1987). Although we did not assess peer relationships in this study, the age effected observed is consistent with the notion that

Values are shown for each variable successively dropped from the model.

non-parental sources of social interaction and support gain in importance during the course of middle childhood, and highlight the role that pets may play in this important developmental transition.

There was no evidence in this study that either genotype or relationship quality was associated with gazing. There are at least two possible explanations for this finding. First, the literature on owner-dog gazing has to date been restricted to research with adults, and there may be unknown differences in childrens' interactions with their pet dogs compared to adult owners. In the absence of any studies comparing adult to child owner's interactions with pets, this possibility cannot be ruled out. Second, in contrast to some studies with adults (e.g., Nagasawa et al., 2015), we did not attempt to manipulate owner-dog gazing, but rather quantified the degree to which such behavior naturally occurred in the context of the child soliciting interaction with the dog. It may be that the amount of naturally occurring gazing (approximately 20% of the total interaction time) was too low in our behavioral paradigm to detect association with children's individual differences.

The present results should be considered in light of several considerations. First, participants were primarily from non-Hispanic White families and thus the generalizability to a more diverse population warrants further study. Second, the participants in this study were typically developing children prescreened for known health conditions. Whether these findings generalize to clinical populations is unknown; however, the present results may serve as foundational research for application to clinical populations. Third, we did not genotype the pet dogs for variation at the OXTR gene. There is some evidence to suggest that dogs' human-directed behavior is associated with genetic polymorphisms at OXTR (Kubinyi et al., 2017; Oláh et al., 2017) or OXTR methylation (Cimarelli et al., 2017). Genotyping OXTR in both children and the pet dogs may reveal more nuanced associations of OXTR genotype within the context of HAIs. Fourth, this study focused on families who already owned a pet dog. This was intentional to avoid the inherent challenge of interpreting child–dog interaction among a mixed group of dog owners vs. non-owners. Finally, the study was conducted in a research laboratory. It is possible that child– dog interaction in a laboratory environment may not be the same as in more naturalistic environments. This limitation is

### REFERENCES

offset, however, by the benefits of the tightly controlled context of a laboratory, with standardized environmental and testing conditions for maximizing the validity of the observed results and reducing distractions and confounding variables. Moreover, the direct behavioral observation of child–pet interaction lends higher confidence in the validity of the observed empirical associations compared to descriptive or self-report studies.

This study adds to the growing body of literature on HAI by documenting two key factors that predict natural variation in children's interactions with their pet dogs. This knowledge is critical as the field as a whole strives to maximize the potential therapeutic benefits of HAI for clinical populations. A greater understanding of the individual differences that influence children's interactions with familiar animals will also aid in the broader research goal of determining the potential benefits and challenges of pet ownership for children.

### AUTHOR CONTRIBUTIONS

DK developed the study, oversaw its execution, analyzed the data, and wrote the manuscript. NH collected the data, conducted the behavioral coding, and analyzed the data. SB conducted the genotyping and analyzed the data. All authors contributed to the writing of the manuscript and approved the final manuscript.

### FUNDING

This research was supported by the National Institutes of Health grant HD071288 to DK. The content is solely the responsibility of the authors and does not necessarily represent the official views of the funders.

### ACKNOWLEDGMENTS

We would like to thank Clive Wynne, Jingwen Liu, and Natalie Hadad for their contributions to the research from which this study was developed. We gratefully acknowledge the families who participated in this study, without whom this research would not have been possible.