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Human interaction moderates plasma cortisol and behavioral responses of dogs to shelter housing
Physiology & Behavior 109 (2013) 75–79
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Human interaction moderates plasma cortisol and behavioral responses of dogs to shelter housing Matthew D. Shiverdecker, Patricia A. Schiml, Michael B. Hennessy ⁎ Department of Psychology, Wright State University, Dayton OH 45435, United States
H I G H L I G H T S ► ► ► ►
Brief (30-min) human interaction consistently reduced plasma cortisol levels and related behaviors in shelter dogs. Passive contact, petting and playing were equally effective. Initial cortisol concentrations were related to fear-related behavior during treatment. The results suggest practical means for improving welfare of shelter dogs.
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Article history: Received 15 October 2012 Accepted 3 December 2012 Keywords: Hypothalamic-pituitary-adrenal Cortisol Dog Shelter dog Human interaction Fear behavior Animal welfare
a b s t r a c t Housing in an animal shelter is a stressful experience for dogs. This study examined the effects of different forms of human interaction on concentrations of circulating cortisol and stress-related behaviors of dogs within 40 h of admittance to a county animal shelter. Blood samples were collected before and after 30-min sessions in a secluded area in which dogs received one of three forms of human interaction: exposure to a passive human, petting, or play. Controls were either exposed to the secluded area alone, or remained in the general housing area. There was a substantial and near uniform reduction in plasma cortisol concentrations from pretest to post-test in all three conditions receiving human interaction, but not in control conditions. Human interaction also reduced behavioral signs of excitation/social solicitation (vocalizing) and fear (panting). Finally, pretest cortisol levels were found to predict levels of panting and another fear-related behavior (tongue protrusions) that dogs exhibited during subsequent testing. The findings suggest practical means of reducing stress, and potentially of improving the welfare, of dogs in shelters. © 2012 Elsevier Inc. All rights reserved.
1. Intoduction The hypothalamic-pituitary-adrenal (HPA) axis is exquisitely sensitive to psychogenic stressors. Innumerable studies with laboratory animals and human volunteers have documented HPA responsiveness to events that are novel, unpredictable, uncontrollable, or violate positive expectancies (e.g., [1–4]). Some of the most potent stressors are social in nature, including the sudden absence of close social companions, or the introduction of an aggressive conspecific [5–7]. While studies of HPA responsiveness are often directed at translational issues, such as the antecedents of depression and anxiety [8–10], or are concerned with the adaptations of animals to their natural environments [11–13], one commonplace demonstration of the principles established in the laboratory is the experience of domestic dogs and cats upon admission to an animal shelter. By their nature, even progressive shelters confront these animals
⁎ Corresponding author at: Department of Psychology, 335 Fawcett Hall, Wright State University, 3640 Col. Glenn Hwy, Dayton OH 45435, United States. Tel.: +1 937 775 2391; fax: +1 937 775 3347. E-mail address: [email protected] (M.B. Hennessy). 0031-9384/$ – see front matter © 2012 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.physbeh.2012.12.002
with an array of psychogenic stressors that often include all those noted above. Indeed, dogs admitted to animal shelters exhibit protracted elevations of plasma and urinary cortisol levels [14–17], and extended shelter housing can enhance cortisol responsiveness to other stressors [18]. These effects are of concern not just for the immediate welfare (i.e., stressful state) of the dogs, but also because chronically stressful conditions may suppress immunological activity [19], potentially impacting health. Chronic stress can also disrupt behavior [20–22]. Behavior problems may prevent dogs from being adopted [23] and also are leading causes of unsuccessful adoptions [24–26]. Attempts to reduce the stress of shelter dogs, and HPA activity in particular, have largely focused on the ameliorative effect of human interaction. Forms of interaction involving comforting tactile contact with a soothing tone of voice have been found to diminish the impact on cortisol levels of additional stressors experienced in the shelter environment [18,27]. However, we and others have had little success reducing the actual HPA response to shelter housing itself. The one exception was a study by Coppola et al. [28], which found that dogs experiencing human interaction in the form of a temperament test on their second day in a shelter had lower salivary cortisol levels the following day. These results indicate
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that it is possible for human interaction to moderate the cortisol response to shelter-housing in recently admitted dogs, though several considerations raise questions about the degree of effectiveness and practicality of the procedure. First, although cortisol levels were lower the following day, no effect was observed on the day of the temperament test. Second, because the study employed between-subject comparisons with large sample sizes (45 and 48 dogs for the significant effect) the consistency with which dogs responded to the procedure could not be determined. Third, the length of the human interaction session varied between 30 and 90 min, so that the duration of interaction required for the effect was unclear. Finally, the temperament test involved a wide variety of forms of human interaction (e.g., play, physical contact, grooming) so that it was not possible to discern if or how the effectiveness of the procedure varied with the nature of human interaction. The goal of the present experiment was to attempt to identify a human-interaction procedure that would reduce the cortisol response to shelter housing in recently admitted dogs. To be practical for shelters to implement, we chose a 30-min procedure — the minimum length of interaction in the Coppola et al. [28] study. We focused on the immediate response to the interaction, using a within-subject (pretest/post-test) design that permitted examination of the consistency of the outcome across dogs. We also assessed the effect of the form of human interaction with three conditions in which the dogs experienced either the passive presence of a human, a soothing petting procedure, or active play and training. Finally, we examined the behavior of the dogs and the relation of behavior to cortisol levels. 2. Methods 2.1. Animals Seventy nine dogs (44 males, 35 females) of various and mixed breeds admitted to the Montgomery County Animal Resource Center — a large, modern animal shelter serving the Dayton, Ohio region — were used in the study. The dogs were relinquished by their owners or brought in as strays. They were admitted to the shelter no more than 40 hours prior to testing. Both intact and gonadectomized males and females were included. Dogs that appeared ill, aggressive (e.g., growling or displaying canines), timid (e.g., tucking the tail or retreating to the back of the cage), or emaciated were excluded from the study. Puppies (identified by the presence of deciduous incisors) and lactating or pregnant females were excluded as well. Dogs were housed in a large noisy “intake” room which contained 75 permanent cages that were proportional to the size of the dog (most were 1.5 × 1.2 × 1.8 m) The cages were constructed of smooth brick on three sides with the fourth side made of metal mesh, which included a door. Illumination was provided during daylight hours by a combination of artificial and natural lighting. Most dogs were housed individually unless resource center personnel deemed it appropriate to house dogs in pairs. Two dogs used in the study had cage mates; the cage mates were excluded from the study. 2.2. Experimental design and testing procedures Dogs were assigned to one of five conditions: Passive Stranger, Pet, Play, Isolation, and Home Cage. Each day a list of recently admitted, eligible dogs was compiled. Initially, dogs selected from the list were randomly assigned to a condition. However, towards the end of the study, assignment was quasi-random to balance sex and mean weight across conditions. Final composition of the conditions by sex and mean weight was as follows: Passive Stranger — 8 males, 7 females, 17.0 kg; Pet — 8 males, 7 females, 17.3 kg; Play — 10 males, 6 females, 17.0 kg; Isolation — 9 males, 8 females, 17.3 kg; and Home Cage — 9 males, 7 females, 17.4 kg. All dogs underwent a single treatment between 1330 and 1630 h. The first blood sample (pre-test) was collected immediately after removing the dog from the home cage. For all conditions except Home
Cage, dogs were then taken on a 3-min walk to allow for elimination in a courtyard adjacent to the intake room, and led to a quiet, secluded room in the rear of the shelter building. There the dog was placed for 30 min in a chain-link enclosure (1.5 × 3.0 × 1.8 m) that contained a simple chair with a blanket or towel on the floor. In the Passive Stranger condition, an unfamiliar female sat silently in the chair with her hands on her lap, and did not engage the dog. If the dog jumped on her, she was instructed to gently move the dog off and say “no”. In the Pet condition, the unfamiliar woman encouraged the dog to lie down and then massaged the dog, focusing on the deep muscles of the lower neck and shoulders while speaking calmly to it [29]. In the Play condition, the unfamiliar woman engaged the dog in play (e.g., tossing a tennis ball or a squeaky toy) and training, while keeping physical contact to a minimum. Training consisted of teaching the dog basic commands for a food reward (maximum of 26 g dog treats) and praise. For all three conditions involving human interaction, the unfamiliar woman wore hospital scrubs to differentiate her from the observers who wore white laboratory coats. Dogs in the Isolation condition remained alone in the enclosure for 30 min. Immediately following the treatment period, a second (post-test) blood sample was collected. Dogs in the Home Cage condition had a “pretest” blood sample collected and were then returned to their cage until a second “post-test” sample was collected at the same interval as for dogs in the 4 groups exposed to the secluded room. All dogs were weighed before being returned to the home cage. All procedures were approved by the Wright State University Laboratory Animal Care and Use Committee. Two observers behind a one-way glass blind recorded behaviors. Vocalizations (whines and barks) were recorded as a measure of excitation/social solicitation. We also observed two behaviors exhibited by dogs in fearful situations: panting (duration) and non-directed tongue protrusions (frequency) [30,31]. The number of yawns was recorded as a possible displacement behavior, and the time spent lying down (dog's torso supported by the floor) was recorded as a measure of relaxed posture/calmness. 2.3. Blood sampling procedure and hormone assessment For blood sampling, one researcher held the dog and presented a front leg. A second researcher collected approximately 0.5 ml of blood from the cephalic vein with a heparinized, sterile syringe. Mean time for blood sample collection was 161 ± 9 s. Blood samples were then placed on ice until centrifugation (1,935 g for 20 min at 4 °C) at the laboratory where the separated plasma was frozen until assayed. Samples were assayed for cortisol using a standard radioimmunoassay procedure (cortisol Coat-a-Count, Siemens) as in previous work (e.g., [32]). Intra and inter-assay coefficients of variation were 8.3% and 12.9%, respectively. 2.4. Data analysis A 5 (Condition) × 2 (Sex) × 2 (Pre/Post) repeated measures Analysis of Variance (ANOVA) was used to assess cortisol levels as well as time required for blood sample collection. Tests for simple main effects [33] further analyzed any significant interaction. Due to heterogeneity of error variance, nonparametric tests (Kruskal–Wallis and Mann–Whitney U) were used for analysis of behavioral data. Because some behaviors could be affected directly by the nature of the human interaction in the Pet and Play conditions (e.g., panting due to exertion during play), Mann–Whitney U tests compared just the Isolation and Passive Stranger conditions for panting, tongue protrusions, yawning, and lying down. Preliminary Mann–Whitney U tests yielded no effect of sex for any of the observed behaviors; thus, males and females were pooled for all further analyses. Central tendency is represented by means and standard errors for cortisol and medians and percentiles for behavioral measures. Calculations were made with SPSS. A probability of pb 0.05 was considered significant.
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As in previous studies (e.g., [18]), there was substantial variability in pre-test cortisol levels. We, therefore, asked whether differences in pretest cortisol predicted behavior in the secluded room. To do so, we used regression analyses with dummy-variables to control for condition. Licking and yawning violated the equal slopes assumption necessitating the use of simple linear regression for each condition individually. To control for an inflated alpha level in these post-hoc analyses, test-wise levels of significance of pb 0.01 (0.05/5 behavior tests) and pb 0.0125 (0.05/4 conditions) were used for the dummy variable regression and the simple linear regression, respectively. 3. Results 3.1. Cortisol Although pretest cortisol levels varied considerably, mean levels for all conditions were in the stress range observed in previous studies [15,27]. Despite the initial variation, all three human interaction conditions reduced cortisol levels. For Passive Stranger, Pet, and Play, all but one dog in each condition showed a reduction in cortisol concentration from pretest to posttest. The reductions ranged from 32% for the Passive Stranger condition to 49% for the Pet condition. ANOVA revealed a significant Condition × Pre-Post interaction F (4, 69) = 2.56, p b 0.05 (Fig. 1). Follow-up tests confirmed significant reductions from pretest to post-test for the Passive Stranger (pb 0.05), Pet (pb 0.001) and Play conditions (pb 0.001). In contrast, cortisol levels of dogs in the Isolation and Home Cage conditions did not significantly change from pretest to post-test. ANOVA of blood sample times showed that there were no differences across conditions or from pretest to post-test. 3.2. Behavior A Kruskal–Wallis test yielded a significant overall effect for vocalizations, p b 0.001. Mann–Whitney U follow-up tests indicated that dogs in the Isolation condition vocalized more than dogs in the Passive Stranger, p b 0.001, Pet, p b 0.001, and Play, p = 0.001, conditions (Fig. 2). There also was a significant effect for panting. Dogs in the Isolation condition panted more than did dogs in the Passive Stranger condition, p b 0.05. 3.3. Relation of cortisol to behavior Regression analysis indicated that the two measures of fearful behavior were associated with pretest cortisol levels. First, higher pre-test
Fig. 2. Number of vocalizations and sec panting by dogs in the secluded treatment area. Data are presented as medians, middle quartiles and 10th and 90th percentiles. Panting data for the Pet and Play condition are not included due to potential confounding. * pb 0.05 vs Passive Stranger; ** p≤0.001 vs each of the other conditions.
cortisol concentrations predicted longer duration of panting across conditions, F (1, 58)=7.24, pb 0.01 (Fig. 3, Panel A). Second, higher pretest cortisol levels were associated with a greater number of tongue protrusions in the Pet condition, R2 =.525, t (13)=4.06 p=0.001 (Fig. 3, Panel B). 4. Discussion
Fig. 1. Mean plasma cortisol levels of dogs prior to (pretest) and following (post-test) treatments. Home cage controls were returned to the home cage between samples. Vertical lines represent standard errors of the means. * p b 0.05 vs pretest; ** p b 0.001 vs pretest.
When a stray dog is admitted to an animal shelter, it often has been captured and confined during transport; for dogs relinquished by owners, all familiar social partners are gone. In any case, the new surroundings are extremely novel. With contagious as well as aggressive barking, the environment is loud and threatening. Events are no longer predictable and the dog loses control over environmental contingencies. Under these conditions, it is not surprising that the plasma cortisol concentrations of dogs during their first day in a shelter have been measured at about three-fold higher than those of pet dogs sampled at their homes (26.5 vs 9.6 ng/ml) [15]. Our earlier attempts to reduce HPA reactivity of shelter dogs had mixed results. Although responsiveness to additional stressors imposed in the shelter could be reduced with human interaction [18,27], the specific response to the shelter could not. That is, in several previous reports [15,18,27] and several recent unpublished experiments [Johnson et al., 2010;
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Fig. 3. Relation of pretest cortisol levels to sec panting and number of tongue protrusions. Pretest cortisol predicts levels of panting in all conditions in which behavior was observed (pb 0.01) and number of tongue protrusion in the Pet condition (pb 0.001).
McOwen et al., 2009; Tamborski et al., 2008] we found human interaction implemented in a variety of ways unable to moderate the cortisol response to shelter housing itself. In contrast in the present study, all but one dog in each of the human interaction conditions (95% in all) showed at least some reduction in plasma cortisol levels from pretest to post-test. Perhaps a critical difference between our earlier studies and the current one was the removal of the dog to a quiet, secluded room for the manipulation. Based on past experiments, exposing a dog to a novel room would be expected to increase HPA activity [18,34]. However, under the circumstances of our study, the secluded room was likely not perceived as more novel than the one from which the dog was taken, and probably was less stressful in other ways, notably in terms of noise and other dog-related stimuli. Further, in the one study from another laboratory in which the cortisol response to shelter housing was reduced, a portion of the human interaction manipulation occurred distant from the dog's home cage [28]. Our results say nothing about how long a reduction in cortisol levels might be expected to persist, though the work of Coppola et al. [28] indicates that, in theory, effects of 24 h might be expected from a single interaction episode. Of course, multiple sessions may produce more powerful or persistent effects, though this remains to be determined experimentally. The lack of discernable difference in the effectiveness of the three modes of human interaction was unexpected. In our earlier work, only a particular form of petting (focusing on deep tissue massage and a soothing tone of voice, as in the present experiment) was found to moderate the cortisol response of shelter dogs to a blood sampling procedure [27]. More-active petting was found to be ineffective. Yet, in the current study, either active play and training, or even the presence of an essentially immobile, non-interactive woman clearly reduced cortisol concentrations of newly admitted shelter dogs. Again, we suspect that the removal to the quiet, secluded room was key. In the absence of the incessant barking and other dog-related stimuli of the intake room, the mere presence a human social partner may have had a more-powerful calming influence. In this regard, it is interesting to note that Tuber et al. [34] found that the passive presence of a dog's owner significantly buffered the cortisol response to a novel though quiet environment, whereas the presence of the dog's long-standing kennel-mate did not.
Other work has suggested shelter dogs are about equally attracted to unfamiliar and familiar humans [35,36], and that women may be more attractive than men [37,38]. The current study, and many others, have relied on cortisol levels to indicate something about the internal “stressful” state of the animal. Indeed, elevated cortisol has been suggested to be the most valuable indicator of poor welfare for dogs [39]. Nonetheless, it is important to keep in mind that cortisol levels and stress should not be regarded as essentially synonymous. While it has long been recognized that a wide variety of aversive psychogenic and physical events reliably activate the HPA axis to produce elevated levels of glucocorticoids [4,40], under some circumstances, notably following chronic exposure to such events, glucocorticoid concentrations may not accurately register the stressful internal state of the individual. For instance, with prolonged exposure to stressors, sensitivity of the adrenal to ACTH may be reduced [41]. In the present context, these considerations caution against over-confidence in cortisol levels alone to assess the stressfulness of shelter housing, particularly during extended stays. Additional measures, such as heart rate variability [42] might be useful to confirm conclusions based on cortisol concentrations. The presence of a human also reduced the barking/whining and panting of the dogs, two behavioral measures we previously found to be lowered as a result of human interaction [15,32,43]. Moreover, we found that the substantial variability in pretest cortisol levels was related to two behavioral measures of fear — panting and tongue protrusions. Inspection of Fig. 3 suggests these relations were largely due to a small subset of dogs with especially high cortisol elevations. These effects are of interest for at least two reasons. For one, several previous studies have noted a general lack of association between cortisol and behavioral measures in shelter dogs [39,44–46]. Our results suggest that these relations might hold primarily for dogs that find shelter housing most aversive or threatening. These findings also might bear on the hypothesized relation between stress in the shelter and behavior problems after adoption [47]. Fear-related behaviors (e.g., defensive biting, extreme reactions to thunderstorms) are common sources of problems for dog owners. Here fear-related behaviors were not only associated with heightened cortisol levels, but the presence of a human reduced at least one of these measures. These findings afford some encouragement that intervention procedures in the shelter might positively affect processes underlying later problem behaviors. Previous findings that brief daily periods of human handling reduced destructive chewing and increased tail wagging in confined dogs also supports this notion [48,49]. We chose the 30-min duration of human interaction with the goal of identifying a procedure that would be practical for shelters to implement. Many animal shelters already have cohorts of volunteers who routinely spend time interacting with the resident animals. The present results suggest ways these interactions might be organized to mitigate physiological, as well as behavioral, stress responses of the dogs. Acknowledgments The authors would like to thank Josh Johnson, Nathan Stafford, Tang Watanasriyukul, Susan Vance, Aaron Fowler, Mary Bosworth, Jessica Finkeldey, Kate Foster, Caitlyn Kramer, Bobbie Richardson, Nicole Sapharas,Tiffany Horner, Amanda Vincent, Samantha Ward, Amanda West, and Jackie Floyd for assistance in data collection, Fran Linden for help in training students, Bev Grunden for statistical advice, and Mick Sagester, Mark Kumpf, and the staff of the Montgomery County Animal Resource Center for their continued and enthusiastic support. This work was supported as a “broader impact” of Grant IOS-1120932 from the National Science Foundation. References [1] Anisman H, Haley S, Kelly O, Borowski T, Merali Z. Psychogenic, neurogenic, and systemic stressor effects on plasma corticosterone and behavior: mouse strain-specific outcomes. Behav Neurosci 2001;115:443–54.
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Physiology & Behavior journal homepage: www.elsevier.com/locate/phb
Human interaction moderates plasma cortisol and behavioral responses of dogs to shelter housing Matthew D. Shiverdecker, Patricia A. Schiml, Michael B. Hennessy ⁎ Department of Psychology, Wright State University, Dayton OH 45435, United States
H I G H L I G H T S ► ► ► ►
Brief (30-min) human interaction consistently reduced plasma cortisol levels and related behaviors in shelter dogs. Passive contact, petting and playing were equally effective. Initial cortisol concentrations were related to fear-related behavior during treatment. The results suggest practical means for improving welfare of shelter dogs.
a r t i c l e
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Article history: Received 15 October 2012 Accepted 3 December 2012 Keywords: Hypothalamic-pituitary-adrenal Cortisol Dog Shelter dog Human interaction Fear behavior Animal welfare
a b s t r a c t Housing in an animal shelter is a stressful experience for dogs. This study examined the effects of different forms of human interaction on concentrations of circulating cortisol and stress-related behaviors of dogs within 40 h of admittance to a county animal shelter. Blood samples were collected before and after 30-min sessions in a secluded area in which dogs received one of three forms of human interaction: exposure to a passive human, petting, or play. Controls were either exposed to the secluded area alone, or remained in the general housing area. There was a substantial and near uniform reduction in plasma cortisol concentrations from pretest to post-test in all three conditions receiving human interaction, but not in control conditions. Human interaction also reduced behavioral signs of excitation/social solicitation (vocalizing) and fear (panting). Finally, pretest cortisol levels were found to predict levels of panting and another fear-related behavior (tongue protrusions) that dogs exhibited during subsequent testing. The findings suggest practical means of reducing stress, and potentially of improving the welfare, of dogs in shelters. © 2012 Elsevier Inc. All rights reserved.
1. Intoduction The hypothalamic-pituitary-adrenal (HPA) axis is exquisitely sensitive to psychogenic stressors. Innumerable studies with laboratory animals and human volunteers have documented HPA responsiveness to events that are novel, unpredictable, uncontrollable, or violate positive expectancies (e.g., [1–4]). Some of the most potent stressors are social in nature, including the sudden absence of close social companions, or the introduction of an aggressive conspecific [5–7]. While studies of HPA responsiveness are often directed at translational issues, such as the antecedents of depression and anxiety [8–10], or are concerned with the adaptations of animals to their natural environments [11–13], one commonplace demonstration of the principles established in the laboratory is the experience of domestic dogs and cats upon admission to an animal shelter. By their nature, even progressive shelters confront these animals
⁎ Corresponding author at: Department of Psychology, 335 Fawcett Hall, Wright State University, 3640 Col. Glenn Hwy, Dayton OH 45435, United States. Tel.: +1 937 775 2391; fax: +1 937 775 3347. E-mail address: [email protected] (M.B. Hennessy). 0031-9384/$ – see front matter © 2012 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.physbeh.2012.12.002
with an array of psychogenic stressors that often include all those noted above. Indeed, dogs admitted to animal shelters exhibit protracted elevations of plasma and urinary cortisol levels [14–17], and extended shelter housing can enhance cortisol responsiveness to other stressors [18]. These effects are of concern not just for the immediate welfare (i.e., stressful state) of the dogs, but also because chronically stressful conditions may suppress immunological activity [19], potentially impacting health. Chronic stress can also disrupt behavior [20–22]. Behavior problems may prevent dogs from being adopted [23] and also are leading causes of unsuccessful adoptions [24–26]. Attempts to reduce the stress of shelter dogs, and HPA activity in particular, have largely focused on the ameliorative effect of human interaction. Forms of interaction involving comforting tactile contact with a soothing tone of voice have been found to diminish the impact on cortisol levels of additional stressors experienced in the shelter environment [18,27]. However, we and others have had little success reducing the actual HPA response to shelter housing itself. The one exception was a study by Coppola et al. [28], which found that dogs experiencing human interaction in the form of a temperament test on their second day in a shelter had lower salivary cortisol levels the following day. These results indicate
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that it is possible for human interaction to moderate the cortisol response to shelter-housing in recently admitted dogs, though several considerations raise questions about the degree of effectiveness and practicality of the procedure. First, although cortisol levels were lower the following day, no effect was observed on the day of the temperament test. Second, because the study employed between-subject comparisons with large sample sizes (45 and 48 dogs for the significant effect) the consistency with which dogs responded to the procedure could not be determined. Third, the length of the human interaction session varied between 30 and 90 min, so that the duration of interaction required for the effect was unclear. Finally, the temperament test involved a wide variety of forms of human interaction (e.g., play, physical contact, grooming) so that it was not possible to discern if or how the effectiveness of the procedure varied with the nature of human interaction. The goal of the present experiment was to attempt to identify a human-interaction procedure that would reduce the cortisol response to shelter housing in recently admitted dogs. To be practical for shelters to implement, we chose a 30-min procedure — the minimum length of interaction in the Coppola et al. [28] study. We focused on the immediate response to the interaction, using a within-subject (pretest/post-test) design that permitted examination of the consistency of the outcome across dogs. We also assessed the effect of the form of human interaction with three conditions in which the dogs experienced either the passive presence of a human, a soothing petting procedure, or active play and training. Finally, we examined the behavior of the dogs and the relation of behavior to cortisol levels. 2. Methods 2.1. Animals Seventy nine dogs (44 males, 35 females) of various and mixed breeds admitted to the Montgomery County Animal Resource Center — a large, modern animal shelter serving the Dayton, Ohio region — were used in the study. The dogs were relinquished by their owners or brought in as strays. They were admitted to the shelter no more than 40 hours prior to testing. Both intact and gonadectomized males and females were included. Dogs that appeared ill, aggressive (e.g., growling or displaying canines), timid (e.g., tucking the tail or retreating to the back of the cage), or emaciated were excluded from the study. Puppies (identified by the presence of deciduous incisors) and lactating or pregnant females were excluded as well. Dogs were housed in a large noisy “intake” room which contained 75 permanent cages that were proportional to the size of the dog (most were 1.5 × 1.2 × 1.8 m) The cages were constructed of smooth brick on three sides with the fourth side made of metal mesh, which included a door. Illumination was provided during daylight hours by a combination of artificial and natural lighting. Most dogs were housed individually unless resource center personnel deemed it appropriate to house dogs in pairs. Two dogs used in the study had cage mates; the cage mates were excluded from the study. 2.2. Experimental design and testing procedures Dogs were assigned to one of five conditions: Passive Stranger, Pet, Play, Isolation, and Home Cage. Each day a list of recently admitted, eligible dogs was compiled. Initially, dogs selected from the list were randomly assigned to a condition. However, towards the end of the study, assignment was quasi-random to balance sex and mean weight across conditions. Final composition of the conditions by sex and mean weight was as follows: Passive Stranger — 8 males, 7 females, 17.0 kg; Pet — 8 males, 7 females, 17.3 kg; Play — 10 males, 6 females, 17.0 kg; Isolation — 9 males, 8 females, 17.3 kg; and Home Cage — 9 males, 7 females, 17.4 kg. All dogs underwent a single treatment between 1330 and 1630 h. The first blood sample (pre-test) was collected immediately after removing the dog from the home cage. For all conditions except Home
Cage, dogs were then taken on a 3-min walk to allow for elimination in a courtyard adjacent to the intake room, and led to a quiet, secluded room in the rear of the shelter building. There the dog was placed for 30 min in a chain-link enclosure (1.5 × 3.0 × 1.8 m) that contained a simple chair with a blanket or towel on the floor. In the Passive Stranger condition, an unfamiliar female sat silently in the chair with her hands on her lap, and did not engage the dog. If the dog jumped on her, she was instructed to gently move the dog off and say “no”. In the Pet condition, the unfamiliar woman encouraged the dog to lie down and then massaged the dog, focusing on the deep muscles of the lower neck and shoulders while speaking calmly to it [29]. In the Play condition, the unfamiliar woman engaged the dog in play (e.g., tossing a tennis ball or a squeaky toy) and training, while keeping physical contact to a minimum. Training consisted of teaching the dog basic commands for a food reward (maximum of 26 g dog treats) and praise. For all three conditions involving human interaction, the unfamiliar woman wore hospital scrubs to differentiate her from the observers who wore white laboratory coats. Dogs in the Isolation condition remained alone in the enclosure for 30 min. Immediately following the treatment period, a second (post-test) blood sample was collected. Dogs in the Home Cage condition had a “pretest” blood sample collected and were then returned to their cage until a second “post-test” sample was collected at the same interval as for dogs in the 4 groups exposed to the secluded room. All dogs were weighed before being returned to the home cage. All procedures were approved by the Wright State University Laboratory Animal Care and Use Committee. Two observers behind a one-way glass blind recorded behaviors. Vocalizations (whines and barks) were recorded as a measure of excitation/social solicitation. We also observed two behaviors exhibited by dogs in fearful situations: panting (duration) and non-directed tongue protrusions (frequency) [30,31]. The number of yawns was recorded as a possible displacement behavior, and the time spent lying down (dog's torso supported by the floor) was recorded as a measure of relaxed posture/calmness. 2.3. Blood sampling procedure and hormone assessment For blood sampling, one researcher held the dog and presented a front leg. A second researcher collected approximately 0.5 ml of blood from the cephalic vein with a heparinized, sterile syringe. Mean time for blood sample collection was 161 ± 9 s. Blood samples were then placed on ice until centrifugation (1,935 g for 20 min at 4 °C) at the laboratory where the separated plasma was frozen until assayed. Samples were assayed for cortisol using a standard radioimmunoassay procedure (cortisol Coat-a-Count, Siemens) as in previous work (e.g., [32]). Intra and inter-assay coefficients of variation were 8.3% and 12.9%, respectively. 2.4. Data analysis A 5 (Condition) × 2 (Sex) × 2 (Pre/Post) repeated measures Analysis of Variance (ANOVA) was used to assess cortisol levels as well as time required for blood sample collection. Tests for simple main effects [33] further analyzed any significant interaction. Due to heterogeneity of error variance, nonparametric tests (Kruskal–Wallis and Mann–Whitney U) were used for analysis of behavioral data. Because some behaviors could be affected directly by the nature of the human interaction in the Pet and Play conditions (e.g., panting due to exertion during play), Mann–Whitney U tests compared just the Isolation and Passive Stranger conditions for panting, tongue protrusions, yawning, and lying down. Preliminary Mann–Whitney U tests yielded no effect of sex for any of the observed behaviors; thus, males and females were pooled for all further analyses. Central tendency is represented by means and standard errors for cortisol and medians and percentiles for behavioral measures. Calculations were made with SPSS. A probability of pb 0.05 was considered significant.
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As in previous studies (e.g., [18]), there was substantial variability in pre-test cortisol levels. We, therefore, asked whether differences in pretest cortisol predicted behavior in the secluded room. To do so, we used regression analyses with dummy-variables to control for condition. Licking and yawning violated the equal slopes assumption necessitating the use of simple linear regression for each condition individually. To control for an inflated alpha level in these post-hoc analyses, test-wise levels of significance of pb 0.01 (0.05/5 behavior tests) and pb 0.0125 (0.05/4 conditions) were used for the dummy variable regression and the simple linear regression, respectively. 3. Results 3.1. Cortisol Although pretest cortisol levels varied considerably, mean levels for all conditions were in the stress range observed in previous studies [15,27]. Despite the initial variation, all three human interaction conditions reduced cortisol levels. For Passive Stranger, Pet, and Play, all but one dog in each condition showed a reduction in cortisol concentration from pretest to posttest. The reductions ranged from 32% for the Passive Stranger condition to 49% for the Pet condition. ANOVA revealed a significant Condition × Pre-Post interaction F (4, 69) = 2.56, p b 0.05 (Fig. 1). Follow-up tests confirmed significant reductions from pretest to post-test for the Passive Stranger (pb 0.05), Pet (pb 0.001) and Play conditions (pb 0.001). In contrast, cortisol levels of dogs in the Isolation and Home Cage conditions did not significantly change from pretest to post-test. ANOVA of blood sample times showed that there were no differences across conditions or from pretest to post-test. 3.2. Behavior A Kruskal–Wallis test yielded a significant overall effect for vocalizations, p b 0.001. Mann–Whitney U follow-up tests indicated that dogs in the Isolation condition vocalized more than dogs in the Passive Stranger, p b 0.001, Pet, p b 0.001, and Play, p = 0.001, conditions (Fig. 2). There also was a significant effect for panting. Dogs in the Isolation condition panted more than did dogs in the Passive Stranger condition, p b 0.05. 3.3. Relation of cortisol to behavior Regression analysis indicated that the two measures of fearful behavior were associated with pretest cortisol levels. First, higher pre-test
Fig. 2. Number of vocalizations and sec panting by dogs in the secluded treatment area. Data are presented as medians, middle quartiles and 10th and 90th percentiles. Panting data for the Pet and Play condition are not included due to potential confounding. * pb 0.05 vs Passive Stranger; ** p≤0.001 vs each of the other conditions.
cortisol concentrations predicted longer duration of panting across conditions, F (1, 58)=7.24, pb 0.01 (Fig. 3, Panel A). Second, higher pretest cortisol levels were associated with a greater number of tongue protrusions in the Pet condition, R2 =.525, t (13)=4.06 p=0.001 (Fig. 3, Panel B). 4. Discussion
Fig. 1. Mean plasma cortisol levels of dogs prior to (pretest) and following (post-test) treatments. Home cage controls were returned to the home cage between samples. Vertical lines represent standard errors of the means. * p b 0.05 vs pretest; ** p b 0.001 vs pretest.
When a stray dog is admitted to an animal shelter, it often has been captured and confined during transport; for dogs relinquished by owners, all familiar social partners are gone. In any case, the new surroundings are extremely novel. With contagious as well as aggressive barking, the environment is loud and threatening. Events are no longer predictable and the dog loses control over environmental contingencies. Under these conditions, it is not surprising that the plasma cortisol concentrations of dogs during their first day in a shelter have been measured at about three-fold higher than those of pet dogs sampled at their homes (26.5 vs 9.6 ng/ml) [15]. Our earlier attempts to reduce HPA reactivity of shelter dogs had mixed results. Although responsiveness to additional stressors imposed in the shelter could be reduced with human interaction [18,27], the specific response to the shelter could not. That is, in several previous reports [15,18,27] and several recent unpublished experiments [Johnson et al., 2010;
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Fig. 3. Relation of pretest cortisol levels to sec panting and number of tongue protrusions. Pretest cortisol predicts levels of panting in all conditions in which behavior was observed (pb 0.01) and number of tongue protrusion in the Pet condition (pb 0.001).
McOwen et al., 2009; Tamborski et al., 2008] we found human interaction implemented in a variety of ways unable to moderate the cortisol response to shelter housing itself. In contrast in the present study, all but one dog in each of the human interaction conditions (95% in all) showed at least some reduction in plasma cortisol levels from pretest to post-test. Perhaps a critical difference between our earlier studies and the current one was the removal of the dog to a quiet, secluded room for the manipulation. Based on past experiments, exposing a dog to a novel room would be expected to increase HPA activity [18,34]. However, under the circumstances of our study, the secluded room was likely not perceived as more novel than the one from which the dog was taken, and probably was less stressful in other ways, notably in terms of noise and other dog-related stimuli. Further, in the one study from another laboratory in which the cortisol response to shelter housing was reduced, a portion of the human interaction manipulation occurred distant from the dog's home cage [28]. Our results say nothing about how long a reduction in cortisol levels might be expected to persist, though the work of Coppola et al. [28] indicates that, in theory, effects of 24 h might be expected from a single interaction episode. Of course, multiple sessions may produce more powerful or persistent effects, though this remains to be determined experimentally. The lack of discernable difference in the effectiveness of the three modes of human interaction was unexpected. In our earlier work, only a particular form of petting (focusing on deep tissue massage and a soothing tone of voice, as in the present experiment) was found to moderate the cortisol response of shelter dogs to a blood sampling procedure [27]. More-active petting was found to be ineffective. Yet, in the current study, either active play and training, or even the presence of an essentially immobile, non-interactive woman clearly reduced cortisol concentrations of newly admitted shelter dogs. Again, we suspect that the removal to the quiet, secluded room was key. In the absence of the incessant barking and other dog-related stimuli of the intake room, the mere presence a human social partner may have had a more-powerful calming influence. In this regard, it is interesting to note that Tuber et al. [34] found that the passive presence of a dog's owner significantly buffered the cortisol response to a novel though quiet environment, whereas the presence of the dog's long-standing kennel-mate did not.
Other work has suggested shelter dogs are about equally attracted to unfamiliar and familiar humans [35,36], and that women may be more attractive than men [37,38]. The current study, and many others, have relied on cortisol levels to indicate something about the internal “stressful” state of the animal. Indeed, elevated cortisol has been suggested to be the most valuable indicator of poor welfare for dogs [39]. Nonetheless, it is important to keep in mind that cortisol levels and stress should not be regarded as essentially synonymous. While it has long been recognized that a wide variety of aversive psychogenic and physical events reliably activate the HPA axis to produce elevated levels of glucocorticoids [4,40], under some circumstances, notably following chronic exposure to such events, glucocorticoid concentrations may not accurately register the stressful internal state of the individual. For instance, with prolonged exposure to stressors, sensitivity of the adrenal to ACTH may be reduced [41]. In the present context, these considerations caution against over-confidence in cortisol levels alone to assess the stressfulness of shelter housing, particularly during extended stays. Additional measures, such as heart rate variability [42] might be useful to confirm conclusions based on cortisol concentrations. The presence of a human also reduced the barking/whining and panting of the dogs, two behavioral measures we previously found to be lowered as a result of human interaction [15,32,43]. Moreover, we found that the substantial variability in pretest cortisol levels was related to two behavioral measures of fear — panting and tongue protrusions. Inspection of Fig. 3 suggests these relations were largely due to a small subset of dogs with especially high cortisol elevations. These effects are of interest for at least two reasons. For one, several previous studies have noted a general lack of association between cortisol and behavioral measures in shelter dogs [39,44–46]. Our results suggest that these relations might hold primarily for dogs that find shelter housing most aversive or threatening. These findings also might bear on the hypothesized relation between stress in the shelter and behavior problems after adoption [47]. Fear-related behaviors (e.g., defensive biting, extreme reactions to thunderstorms) are common sources of problems for dog owners. Here fear-related behaviors were not only associated with heightened cortisol levels, but the presence of a human reduced at least one of these measures. These findings afford some encouragement that intervention procedures in the shelter might positively affect processes underlying later problem behaviors. Previous findings that brief daily periods of human handling reduced destructive chewing and increased tail wagging in confined dogs also supports this notion [48,49]. We chose the 30-min duration of human interaction with the goal of identifying a procedure that would be practical for shelters to implement. Many animal shelters already have cohorts of volunteers who routinely spend time interacting with the resident animals. The present results suggest ways these interactions might be organized to mitigate physiological, as well as behavioral, stress responses of the dogs. Acknowledgments The authors would like to thank Josh Johnson, Nathan Stafford, Tang Watanasriyukul, Susan Vance, Aaron Fowler, Mary Bosworth, Jessica Finkeldey, Kate Foster, Caitlyn Kramer, Bobbie Richardson, Nicole Sapharas,Tiffany Horner, Amanda Vincent, Samantha Ward, Amanda West, and Jackie Floyd for assistance in data collection, Fran Linden for help in training students, Bev Grunden for statistical advice, and Mick Sagester, Mark Kumpf, and the staff of the Montgomery County Animal Resource Center for their continued and enthusiastic support. This work was supported as a “broader impact” of Grant IOS-1120932 from the National Science Foundation. References [1] Anisman H, Haley S, Kelly O, Borowski T, Merali Z. Psychogenic, neurogenic, and systemic stressor effects on plasma corticosterone and behavior: mouse strain-specific outcomes. Behav Neurosci 2001;115:443–54.
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