Animal Behavior for Shelter Veterinarians and Staff. Группа авторов

increased vomiting (Stella et al. 2013), decreased food intake, avoidance of elimination for 24 hours, and elimination outside the litterbox (Stella et al. 2011).

4.4 The Role of Stress

Nowhere else is the interplay between behavioral and physical health more apparent than when looking at the impact that stress plays on every aspect of health. Increasingly, science is uncovering the myriad of different ways in which stress affects living organisms at every stage of development. Much controversy exists about how to define stress, so for the purpose of this chapter, stress (or stressors) is defined as anything that disturbs or threatens homeostasis. These stressful forces may be physical, chemical, or emotional and typically result in physiological or behavioral responses as the organism attempts to restore homeostasis. The physiological events that occur during an acutely stressful event are intended to be adaptive, and, in most cases, they do succeed in helping an organism maintain homeostasis by adapting to the stressor. When stress is chronic and unremitting, or the individual cannot successfully act in such a way as to decrease the stressors, a variety of physiological events can conspire to damage the overall health and well‐being of the organism. Thus, in the long term, the stress response can be maladaptive.

      There are two primary components of the stress response, involving two different endocrine systems. The first is the sympathetic nervous system response. Within seconds of perceiving a stressor, the sympathetic nervous system begins secreting norepinephrine, and the adrenal medullae begin secreting epinephrine. This begins to prepare the body for “fight or flight.” The second system is the hypothalamic‐pituitary‐adrenal (HPA) axis, generally believed to be the body’s primary stress‐responsive physiological system (Hennessy 2013). When the HPA axis is triggered, the hypothalamus releases corticotrophin‐releasing factor that triggers the release of adrenocorticotropic hormone from the pituitary gland. This hormone then stimulates the release of glucocorticoids from the adrenal cortex. Several other hormones, including prolactin, glucagon, thyroid hormones, and vasopressin, are secreted from various other endocrine organs. The overall effect of these circulating hormones is to increase the immediate availability of energy, increase oxygen intake, decrease blood flow to areas not critical for movement, and inhibit digestion, growth, immune function, reproduction, and pain perception. In addition, memory and sensory functions are enhanced. Essentially, the goals of all of this physiological activity are to make more energy available for immediate use and to put on hold any and all processes that are not involved in immediate survival.

      Acute stress has been shown to enhance the memory of an event that is threatening (McEwen 2000). This is clearly adaptive if it allows the organism to form strong associations, enabling it to avoid dangerous things in the future. Knowing this should increase animal handlers’ awareness of the important and lasting impact that their behavior and actions can have on an animal. An unpleasant handling experience may have long‐term, negative effects on the animal’s behavior, ultimately making that animal less adoptable.

      If the stress response continues, for whatever reason, cardiovascular, metabolic, reproductive, digestive, immune, and anabolic processes can all be pathologically affected. The results can include myopathy, fatigue, hypertension, decreased growth rates, gastrointestinal distress, and suppressed immune functioning with subsequent impaired disease resistance. Chronic stress can even lead to structural and functional changes in the brain, and when extreme conditions persist, permanent damage can result (McEwen 2000). It is believed that when dealing with chronic stress, the HPA axis becomes dysregulated, and the various components of the system may no longer respond in the predicted fashion. For example, in some cases, chronic stress results in adrenal hypertrophy and elevated levels of glucocorticoids, while adrenocortical‐stimulating hormone (ACTH) levels remain unchanged. At this point, the dysregulation results in an HPA axis that is no longer able to respond appropriately to future stressful events, and measurements of glucocorticoid levels may become less meaningful (Hennessy 2013).

Stress can arise from a variety of different sources, both physiological and psychological. Physical stress can be caused by hunger, thirst, pain, exposure to extreme temperatures, disease, illness, and sleep deprivation. Psychological stress can result from exposure to novelty, unpredictable environments, social conflict, and constant exposure to fear‐ or anxiety‐provoking stimuli as well as any other situation that leads to chronic frustration or conflict. A lack or loss of control is another important psychological stressor. In fact, novelty, withholding of reward, and the anticipation of punishment (not the punishment itself) have been found to be the most potent of all psychological stressors (McEwen 2000).

      A variety of different means have been used in an attempt to measure physiological stress, including but not limited to measuring glucocorticoids and their metabolites in hair, urine, feces, blood, and saliva. Glucocorticoids in blood and saliva do appear to measure the condition of the animal at that moment, whereas glucocorticoids in urine, feces, and hair reflect the condition of the animal over a longer time frame (Hennessy 2013). ACTH and luteinizing hormone‐releasing hormone stimulation tests have also been used to measure adrenal and pituitary sensitivities, respectively, and one study demonstrated increased HPA responsiveness and reduced pituitary sensitivity occurring in the face of chronic stress (Carlstead et al. 1993). The altered responsiveness was suggestive of HPA dysfunction. A decrease in peripheral lymphocyte numbers and an increase in neutrophil numbers, along with an increased neutrophil:lymphocyte ratio, is another well‐documented response to glucocorticoid release and has been proposed as another reliable method for evaluating the stress an animal may be experiencing (Davis et al. 2008).

      Studies have shown that the average shelter dog does have higher levels of circulating cortisol than pet dogs that were sampled in their homes (Hennessy et al. 1997). Some studies of shelter dogs have found that circulating levels of cortisol return to normal within days to weeks, but others have found that HPA axis dysregulation develops in some dogs (Hennessy 2013).

Any single individual’s response to stress will vary as a result of several different factors such as genetics, temperament, experience, environment, and learning. For example, cats not socialized to people have been shown to be more likely to experience high levels of stress when exposed to people in a shelter setting (Kessler and Turner 1999a). Experiences during the first weeks of life have been shown to have profound effects on an animal’s ultimate ability to cope with stress (Foyer et al. 2013). The importance of the role of maternal stress on the developing offspring during the prenatal period is receiving an increasing amount of attention (Jensen 2014). Research in numerous species has demonstrated that when the gestating mother experiences stress, it can alter her behavior and affect the behavioral development of her young (Braastad et al. 1998; Chapillon et al. 2002; Champagne et al. 2006). Subsequently, her offspring often show a decreased ability to deal with stress: they may have some learning impairment and they may be more susceptible to the conditioning of fearful responses, especially to auditory stimuli (Ross et al. 2017). The individual’s perception of stress, which will also vary based on experience, is ultimately the most important factor that influences the effect of stress. Many potential stressors exist for the sheltered dog and cat. Table 4.1 provides a summary of common shelter stressors and behavioral signs of stress.

      4.4.1 Cats

      Several studies have evaluated the stressors impacting shelter and laboratory cats. Shelter cats exhibiting higher stress scores are at higher risk of developing upper respiratory tract infections (Tanaka et al. 2012). One study reported that feigned sleep may be a coping mechanism seen in stressed shelter cats (Dinnage 2006). An increased need for restorative sleep has been demonstrated in both humans and animals exposed to physiological or biological stress (Rampin et al. 1991; Rushen 2000). These data suggest that while cats may appear to be the most relaxed of animals, they may, in fact, suffer the highest levels of stress.

The stress level of most kenneled cats will decrease over the first few days to weeks. One study demonstrated that two‐thirds of cats will adjust well within the first two weeks (Kessler and Turner 1997). The same study demonstrated that about 4% of cats maintained a high level of stress for the entire study period, suggesting that