As I walked through the intake room of a large county animal shelter in Dayton, Ohio, evaluating dogs to enroll in the Behavior Modification and Enrichment Program (BMP), I stopped in front of a kennel and looked down at a young pit bull–type puppy, with a turned-up pink nose and floppy ears, sitting eagerly in his kennel. My heart dropped as I glanced at his paperwork. His name was Bingo, and the notation on the top of his paperwork said “Confiscate for Cruelty.” His appearance, strong and stocky, was remarkably similar to another dog that recently celebrated his first birthday just a few days before his last breath. With the memory still too fresh in my mind, I vowed that this young pup’s fate would not be that of the dog before him.

Animal shelters are truly a safe haven for millions of dogs that are lost, abandoned, mistreated, or neglected every year. However, even in those state-of-the-art shelters, the environment is very stressful. Shelters inadvertently expose animals to numerous stressors including the novelty of the shelter itself, a disruption from normal events such as feeding or walks for elimination, and a general loss of control over their environment. This is of concern not only in terms of the immediate welfare of the animal but also the long-term impact that this environment has on the behavior and health of the dog.

Stress and the shelter environment

Fig. 1. Plasma cortisol level of dogs during their first day in the shelter and dogs maintained as pets and sampled in their own home. Vertical bars represent standard errors of the means (adapted from Hennessy et al. 1997)

The hypothalamic-pituitary-adrenal (HPA) axis is generally regarded as the body’s primary stress response neuroendocrine systems, and responds to a multitude of stressors resulting in the secretion of glucocorticoids (primarily cortisol). Further, researchers have determined that psychological stressors, those that produce no physical insult, such as exposure to a novel environment, separation from an attachment figure, and unpredictability of events, will also activate the HPA axis. All of us experience psychological stress during our busy lives, and the physiological response that occurs during this immediate (acute) stress is actually adaptive—it helps us deal with the situation. But long-term (chronic) stress that last hours, days, or months becomes maladaptive, and this physiological response depletes our immune systems and causes a disruption in the brain region controlling the stress hormones. A disruption in this brain region increases the likelihood of psychiatric disorders such as post-traumatic stress disorder (PTSD), anxiety, and depression. In addition, dogs in animal shelters have a high rate of parasites and infectious disease; the elevated cortisol poses a threat for the spread of disease with a weakened immune system.

Researchers have demonstrated that a newly admitted shelter dog’s cortisol level is three times greater than a dog living in a home environment (Fig. 1).

Fig. 2 Mean plasma cortisol levels of dogs sampled at various days in the shelter. Vertical lines represent standard errors of the means (Hennessy et al. 1997)

Further, the cortisol level remains elevated for 3 days and then gradually decline (Fig. 2).

I observed the behavior of dogs experiencing psychological stress for those first days of their shelter stay. The dogs shut down; they burrowed their heads underneath their blankets, or hid in the corner of the kennel. They shook with fright, growled at the staff, and avoided eye contact at all costs. This was troubling because these dogs were expected to pass a SAFER test on their fourth day after being admitted to the shelter. It saddened me that many of the fearful dogs were never placed up for adoption, and were euthanized for behavior issues instead. Further, many of the dogs that displayed this behavior were surrendered to the shelter by their owners. For these dogs, entrance to the shelter may entail an assortment of stressors not experienced by strays, such as a loss of the attachment figure and an abrupt change in regular routines of feeding and walking. Researchers had previously found that owner-relinquished dogs showed a more elevated cortisol level following shelter admittance than did strays, suggesting that entrance to a shelter has a greater impact on dogs coming directly from a home (Fig. 3). It became apparent that we needed to look further into what we could do to help these dogs.

Fig. 3. Scatter diagram of slopes of regression for 26 dogs for C/C over day, plotted against C/C on day 1, showing past history category (adapted from Hiby et al. 2006).

Over a period of years, researchers attempted to inhibit the stress response of shelter dogs by providing repeated and prolonged human interaction inside the dog’s kennel and/or in their kennel area. This intervention continually failed to reduce the dog’s cortisol. However, one researcher removed the dog from the kennel area and provided a quiet room for human interaction, and she found that those dogs that spent time with a researcher in a quiet, secluded room had significantly lower cortisol. This was the key to stress reduction! Other studies followed, and researchers found similar results. In fact, our lab found that 30 minutes of petting, playing, training, or just the mere presence of a woman sitting in an enclosure with the dog in this quiet, secluded room significantly reduced cortisol (Fig. 4). These findings were very encouraging for the development of programs designed to reduce the stress of the dogs housed in shelters, suggesting that human interaction by volunteers or staff may be a practical way to reduce stress.

Fig. 4. Mean plasma cortisol levels of dogs prior to (pre-test) and following (post-test) treatments. Vertical lines represent standard errors of the means *p

Fig 5. Mean change in plasma cortisol levels from pretest to post-test for dogs in the four treatment groups of Experiment 2. Dogs either received human interaction in the form of petting for 15 or 30 min (Pet 15 or Pet 30) in a quiet room or remained in their home kennels for the 15- or 30-min periods (Home Kennel 15 or Home Kennel 30). Vertical lines indicate standard errors of the means. n = 16/condition, ** P < 0.01 vs Home Kennel, Newman-Keuls test (Willen et al. 2017).

During my work at the shelter, our lab examined the practicality of human interaction. We knew that volunteers and staff had limited time. Therefore we examined if we could reduce the time, from 30 minutes in previous studies to just 15 minutes, to determine how long this stress reduction would persist. We found 15 minutes was just as effective as 30. However, we also found that when the dogs were returned to the kennel environment, their cortisol levels went back up in just one hour (Fig 5). In another study that was conducted about the same time as my work, shelter dogs were petted 7 to 8 times over a 10-day period and the results showed a cortisol reduction on the tenth day that was comparable to that seen on the first. This demonstrates that petting could continue to effectively reduce the stress responses when applied on a daily or near-daily basis. Moreover, reducing the petting time from 30 to 15 minutes may create a more reasonable expectation in terms of the length of time we can expect a volunteer at a shelter to devote to a single dog.

In addition, we found that a thirty-minute petting procedure that effectively reduced the cortisol levels of the strays produced a nonsignificant reduction in the cortisol levels of the dogs released by their owners (Fig. 6). Although behavior was not systematically scored in this experiment, I was left with the strong impression that dogs released by their owners were, on average, more resistant than strays were to interactions with me. This led us to believe that it may require more than a single half hour of interaction to have a measureable effect on the cortisol levels of the owner-relinquished dogs (Fig.7). The results were puzzling, and I wondered if we could somehow evaluate the stress history of owner-relinquished dogs. To estimate effects of stressors two weeks prior to admission to the shelter, we evaluated hair cortisol values in both groups. We found that measurements of hair cortisol secreted by the strays and the owner-relinquished dogs over a two-week period prior to entering the shelter were comparable. This initially was surprising to us in that dogs coming from a home would seem likely to experience fewer threats and aversive circumstances than stray dogs. But, while the transition to the shelter may be more difficult for dogs coming from a home, the home environment prior to relinquishment may still be about as stressful as the environment experienced by a stray.

Fig 6. Mean change in plasma cortisol levels from pretest to post-test for owner-relinquished and stray dogs provided human interaction in the form of petting in Experiment 3. Vertical lines indicate standard errors of the means. n = 16/condition. Stray dogs, but not those relinquished by their owners, showed a reduction from pretest to post-test in plasma cortisol levels, ** P < 0.01, Newman-Keuls test (Willen et al. 2017)

Fig 7. Mean hair cortisol levels for dogs in the two conditions of Experiment 3. There was no difference between owner-relinquished and stray dogs. Healthy pet dogs living in a home and Cushing’s dogs are included for visual comparison. Vertical lines indicate standard errors of the means. Owner-relinquished, n = 10; Stray, n = 12; Pet dogs living in a home, n = 4; Cushing’s dogs, n = 3 (Willen et al. 2017).

A breakthrough with Bingo

As Bingo jumped up and down in excitement for me to remove him from his kennel, I noticed he was definitely not fearful, unlike many dogs that enter the shelter, but possibly overly stimulated with noises and smells in the loud intake room. I put the leash around his neck and he grabbed it and walked—or should I say ran—me to the outside courtyard! Here I proceeded to assess him. He would require a behavior modification plan first and foremost to reduce his energy, and to stop him from biting the leash and nipping at the fat on my arms! I thought of my poor little 90-pound volunteer; how in the world would she ever be able to work with him? However, with the strong group of volunteers in the BMP, I was sure we could turn this guy around.

I sat on the couch in the BMP room reviewing the files of the dogs that were enrolled in the program. I read the notes about Bingo written by the volunteers. I shook my head as I read the notes. The volunteer wrote, “He is very high energy. He is affectionate however used his teeth to show his affection. Nipped several volunteers’ chins while showing his affection.” I placed the protocols that were written up especially for Bingo in his file, and gathered my group of volunteers to work one on one with him. My protocols were based on applied animal research, specifically how we can use the way animals learn to teach them to modify their behavior. I focused on the elements of learning theory that were most relevant to Bingo’s behavior problems, such as classical and operant conditioning. Bingo’s behavior modification protocols were not unusual, in that every dog enrolled in the BMP received a file with personal protocols and a daily diary of the type of training and enrichment they received. Because Bingo was a court case dog, he received human interaction in the form of training, leash walking, and play on a daily basis. Other more fearful dogs received daily interaction with a volunteer who worked on establishing trust and reducing stress. Some dogs only required a few days of human interaction to show improvement; others needed a few weeks. In addition to human interaction, other scientifically proven stress reducing techniques beyond human interaction were used such as essential oils, pheromones, thunder shirts, and classical music. After each session, the dog was returned to its kennel to find enrichment—a blanket, toy, and treat inside.

Applied animal behavior is a very new concept in a shelter environment. Many shelters do not have the time or opportunity to access the work of applied behaviorists, let alone decide how to apply it in their day-to-day shelter operations. Although this shelter invited graduate students from a local university to conduct applied studies for over two decades, it was difficult to implement their results due to lack of resources. However, this was a very mutualistic relationship. Not only did the shelter provide the psychology students with access to a group of subjects (shelter dogs) who are under acute and chronic stress, but the students provide scientifically tested data to the shelter about the welfare of their animals: a win-win situation.

The Behavior Modification Program (BMP) began with me, a single behaviorist. I worked with fearful dogs in a small room the shelter used for storage. I sat on the floor with a blanket, treats, and toys and attempted to do what I knew best, establish a relationship with the fearful dog. I volunteered for roughly twenty hours a week. I recall the day I proposed the BMP to the shelter manager. I had just completed a fourth study with the shelter’s dogs, and I sat across from him explaining my results. I recall how excited I was as I explained how we could reduce the petting time from thirty minutes to just fifteen. In addition, I raised my concern that dogs relinquished by their owners became more stressed during their stay in the shelter, unlike the strays that seemed to flourish from human interaction. I described how straightforward the stress-reducing technique we used in each study was, and how simple these techniques could be to implement with a group of volunteers. I stressed the importance of working with newly admitted dogs as they were in their critical state. However, I knew this was a big endeavor for the shelter to allow me to continue my work with shelter dogs now as a volunteer…not a researcher!

Today, three years later, I sit in the shelter garage, which has been made up to look like a living room, having graduated from the small storage room. The room is furnished from the thrift store, with a deep freezer full of chicken and hot dogs that I use to establish trust with the fearful dogs, a comfortable area rug for the dogs to play on, and toys scattered on the floor. The success of this program has surpassed my expectations. We have successfully worked with over 300 dogs and have an 85 percent success rate of adoption. We’ve successfully modified the behavior of fearful dogs, modified unwanted behaviors such as food aggression, dog reactivity, sensitivity to touch, provided enrichment for court case dogs, and witnessed a significant reduction in diseases due to stress reduction. This success rate has not come without its share of heartaches and tears, however, as I’ve said goodbye to those dogs that didn’t make it.

My volunteers have come and gone, and today I have a single dedicated volunteer. I would have never predicted this BMP would have caused sleepless nights of worry and distress: Some days we had endless dogs needing our care, and we volunteered a long 40-hour week. I am reminded of why we do this day after day every time I flip through our records, and smile as I remember each and every dog. But one case stands out in my memory and will most likely be there for a long time: Bingo, the floppy eared pup who grew up in the shelter finally found his forever home. Bingo, who never knew the feeling of grass on his feet, now has a big back yard to run and play. As I read the updates from the wonderful man who adopted him, tears roll down my face. “He is the most well-mannered dog. I take him everywhere and I receive so many compliments. He loves everyone: kids, cats, and other dogs!” he writes.

I put the folder aside, recalling how he was deemed hopeless by the staff, and pull my research folder out. Here I am again, as a researcher, studying the impact this program has on the behavior of the dogs. My hypothesis is that the enrichment program involving human interaction will increase the chances of fearful dogs passing the SAFER test. Although the study is still underway, we found that significantly more enrichment dogs (77 percent) than controls (33 percent) reached the criteria for passing the SAFER test. These findings suggest that enrichment with human interaction has meaningful effects on behavior and can determine the fate of the dogs in the shelter. As a researcher, I am cautious of drawing conclusions from the results prematurely, but as someone who has put their heart and soul into a program, I am celebrating.

Bingo enjoying his enrichment in his baby pool, playing with his jolly ball and cleaning out the peanut butter jar, and of course spending time with his favorite volunteers.

Bingo enjoying his enrichment in his baby pool, playing with his jolly ball and cleaning out the peanut butter jar, and of course spending time with his favorite volunteers. We attempted to find Bingo a friend at the shelter, but often times he was so strong and pushy that dogs would run away. But we happen to find a guy that could tolerate him, a court case dog as well. So they spent time with supervised much-needed play time.

Bingo living happy and comfy in his forever home. Look at that smile!

Regina Willen, MS, CDBC, ACAAB, is a researcher in Dayton, OH.  She holds a Master’s degree in Neuroscience, Physiology, and Cell Biology and is the director of Helping Animals Lost and Orphaned (HALO) a non-profit organization assisting the local community and local animal shelters with behavior modification and the overall care of the animals (assistance with veterinarian services, rehoming a pet, dog food assistance, etc). Regina is the process of opening a state-of-the-art behavior facility, where she will work one-on-one with the animals in need of behavior modification and their owners.  In addition, Regina will be attending Miami University Oxford OH in the fall to pursue her Ph.D. in Biology, continuing her research with shelter animals.