Introduction

Dogs and cats, once barnyard livestock, have in recent years been brought into the house and treated increasingly as part of the family. One might surmise that this has dramatically reduced the amount of stress to which these animals are exposed. The environmental stress has most assuredly dwindled; however, stress has not been completely eliminated from their lives. Quite the opposite, in fact. In many cases, the change in how dogs and cats live has simply resulted in trading sources of stress from those they were readily adapted to combat, to sources they may not have well-developed defenses against.

Stress is a broad topic, which often includes fear, anxiety, and trauma. Much has been written about stress in the human psychology literature, and much has been published using mice and rats as models to elucidate the physiological mechanisms behind stress. However, this topic has not been explored as thoroughly in the dog or cat; especially stress from an emotional or psychological perspective. The prevailing assumption is that ‘stress triggers’ and stress effects for the companion animal do not differ from other mammals.

This may or may not be the case. The environment in which many dogs and cats are now living, coupled with their gregarious social natures, may make them unique among other animals, and more like their human owners.

What little research has been published regarding stress and its effects on the dog or cat has focused on more pathological responses that endanger pets and their relationships with people. Stress research is now gaining momentum with the discovery that certain medical conditions may have their origin in the response of the animal to acute or chronic stress. Therefore, we must ask some fundamental questions. First, do companion dogs and cats suffer from acute and/or chronic stress?

Secondly, if they do, what effect does this stress have on health and well-being? Finally, what solutions are available to resolve the stress response, and are any of these solutions diet-related?


Defining stress

Stress has been defined as ‘the sum of all nonspecific biological phenomena caused by adverse conditions or influences. It includes physical, chemical, and/or emotional factors to which an individual fails to make satisfactory adaptation and that cause physiological tensions that may contribute to disease’ (Campbell et
al., 2004). Therein lies the ‘stress’, the inability to escape or change the stimuli. This is especially poignant if one considers the inability of the house cat or the kenneled dog to extricate themselves from their ‘stressful’ habitat.

Stress can be divided into two distinct categories: psychological and physiological. The psychological stresses include fear, phobias, and anxiety. For the companion animal, psychological stress would include such things as visits to the veterinarian, boarding at a kennel, adding a new family member or new companion animal to the household, tight restraint, long term or tight confinement, inactivity and boredom, noise from guns, thunderstorms or vehicles, sleep deprivation, and numerous others. Physiological stress is the more commonly considered stress placed on animals; especially animals that were once in outdoor environments like dogs and cats. Physiological stress can come from normal processes (reproduction, exercise, work, etc), the environment (cold, heat, thirst, etc), injury and trauma, and others. In short, stress for companion animals can come in many forms and from many directions.


The neuroendocrine response to stress

To better determine how stress might affect companion animals, it is necessary to understand the generalized neuroendocrine response to stress. The ability to successfully cope with stress can have a strong genetic link, but is also an adaptive mechanism necessary for survival. It is rapid, long-lived, has memory and directs repair. In a generalized and simplistic overview, the response to stress can be divided into the autonomic nervous system response and the hypothalamic-pituitaryadrenal axis response (Casey, 2002). Each system/axis works separately, but congruently, to maintain homeostasis in whatever environment it is presented (Figure 1).




Figure 1. The autonomic nervous system and hypothalamic-pituitary-adrenal cortex axis.


The autonomic nervous system is composed of two segments, the sympathetic and parasympathetic systems.

The sympathetic neurons are organized from the spinal cord directly to target organs or through ganglia. The sympathetic nerve endings secrete norepinephrine and are described as adrenergic. The parasympathetic system has direct connection to the target organs through the vagus nerves. The terminal nerve endings of the parasympathetic system secrete acetylcholine and are therefore described as cholinergic. The hypothalamic-pituitary-adrenal (HPA) axis, on the other hand, is a predominately endocrine system. When signaled from higher centers in the brain, the hypothalamus releases corticotrophin releasing factor (CRF), which stimulates the release of adrenocorticotrophic hormone (ACTH) from the anterior pituitary into the circulation. ACTH then stimulates the release of cortisol (and aldosterone) from the adrenal cortex into the circulation. Most cells in the body have cortisol receptors, therefore effects can be far-reaching. Secretion of ACTH and/or cortisol stimulates the release of a myriad of other endocrine signals involved in homeostasis and response to the environment (e.g. ß-endorphins, serotonin (Takeda et al., 2004), growth hormone, insulin-like growth hormone-1 (Uhde et al., 1992), and others. Cortisol has anti-inflammatory effects both alone and in concert with the immune system. Cortisol levels are controlled by negative feedback mechanisms at the hypothalamus and anterior pituitary levels.

In general, the autonomic nervous system response is very rapid and targeted; whereas the HPA axis adjusts for more chronic changes and is broader in its reach. As an example, when stress occurs, the autonomic nervous system increases the sympathetic and decreases the parasympathetic response. This elicits a mass discharge of the neurons, norepinephrine is released, and heart rate, cardiac output, blood flow to visceral organs, and respiration rate increase. Conversely, gastrointestinal motility and blood flow decrease and reproductive functions are dampened. Norepinephrine also stimulates central nervous system activity and spatial learning, while a release of epinephrine stimulates glycolysis. On the other hand, the HPA axis is continually making adjustments to maintain homeostasis. When a change to the perceived environment is communicated from the higher centers of the brain to the hypothalamus, a cascade of endocrine signals is invoked that ultimately results in cortisol release into the circulation. Cortisol causes rapid mobilization of amino acids and fatty acids from body stores, stimulates gluconeogenesis in the liver, decreases the rate of glucose utilization by the cells, and ultimately increases circulating blood glucose. Cortisol invokes a higher sense of awareness in the brain, pain perception is decreased by ACTH-stimulated release of ß-endorphins and reproductive functions are dampened.

As a nutritionist, it is important to understand whether the responses to stress might have predisposing nutritional factors (i.e. conditional deficiency, imbalance, or toxicity). Further, to understand if supplementation of a given nutrient might play a supporting role or serve as a solution. The endocrine messengers, norepinephrine, acetylcholine, and cortisol, are synthesized de novo from tyrosine, choline and acetate, and cholesterol and acetate, respectively. Several of the key enzymes necessary for the synthesis of these endocrine messengers are dependent upon co-factors such as zinc, copper, and manganese. In addition, transmission of nervous signals is brought about by discharge of action potentials along the neuron and exchange of sodium, calcium and potassium ions across the synapse. It is understood that each of these elements is important for proper physiological communication of a stress response and that they are needed in the diet for normal neuroendocrine responses.

In a search of the literature, there are very few specific examples of the responses to stress reported for companion animals. That does not mean they do not exist; rather, the information has usually been described in terms of a pathological condition and in many cases must be extracted from the pharmacology literature. This makes the effort more difficult and complicated.

However, an emotional/behavioral component of stress in companion animals does exist. Long-term stress can lead to medical and compulsive disorders (Luescher, 2003). Issues such as feline lower urinary tract disease and feline idiopathic cystitis, irritable bowel disease, gastric dilatation volvulus (bloat), eating disorders such as obesity and anorexia, noise and storm phobias, and separation anxiety syndrome are prevalent in companion animals. Following is a brief glimpse into these disorders and the stress factors associated with them.


Stress-related disorders of companion animals


FELINE IDIOPATHIC CYSTITIS

Feline idiopathic cystitis (FIC) is just one of several feline lower urinary tract diseases. Unlike several of the other lower urinary tract diseases, an obvious cause for FIC is difficult to isolate. Affected cats present with hematuria, dysuria, frequent urination, inappropriate urination, and acidic urination. Middle-aged, overweight, inactive, litter-box accessible, indoor with little or no outdoor access, Persian, Himalayan, male, and feeding only dry food have been described as several of the predisposing factors to FIC. It has been suggested that stress should be added to this list as well. The results of a controlled case retrospective survey found that stress and/or anxiety played a role in FIC (Cameron et al., 2004). In this study, access to an indoor litter box, living with another cat(s), and conflicts with another cat were the leading predisposing factors to FIC. In dogs, conditioning to mild shock avoidance decreased urinary output, renal blood flow, and glomerular filtration (Koepke, 1985). This might provide a clue to the underlying neuroendocrine response to stress in FIC.

There is no standard therapy for this disease short of removing the cat from stress.


IRRITABLE BOWEL DISEASE

Irritable bowel syndrome/disease (IBD) is the cause for much pain and anguish in people with the disease. Thus, a great deal has been written on the topic, and a direct link to stress has been described. The disease manifests as a disorder in colonic motility; the gastrointestinal tract fails to ‘segment’ for the movement of its contents, all the while peristalsis is increased. Cramping, pain, and constipation are common complaints. The condition has been reported in dogs, but not cats. It represents a small proportion of the intestinal diseases (about 3%) and may be precipitated by stress in the dog (Simpson, 1998). In dogs exposed to restraint stress, intestinal motility increased in both the fed and fasted state (Muelas et al., 1993). This would be predicted based on the knowledge of vagal innervation of the parasympathetic nervous system. However, with vagal communication severed, stress increased motility during fasting, but decreased motility in the fed state. The vagus nerve is the primary highway for nervous transmission to the deep visceral organs in the parasympathetic system. Thus, only a portion of the signaling pathway and stress response in IBD can be explained by the parasympathetic system modification. The HPA axis and cortisol release may play a part in the condition; however, this has not been explored in the dog. Standard therapy is to treat with anti-inflammatory medications and corticosteroids.

One might surmise that similar to the provision of soluble fiber for other bowel diseases in dogs and cats, this therapy, along with supplementation of antiinflammatory intermediates like omega-3 fatty acids, might be worth considering for treatment of IBD.


GASTRIC DILATATION-VOLVULUS SYNDROME

Gastric dilatation-volvulus syndrome (GDV) in the dog is commonly called bloat. The term is descriptive of the condition in the stomach, namely that a large amount of gas is trapped and if not released can be terminal. In dogs, GDV is described as a mal-position of the stomach. The condition is thought to be precipitated by rapid and ravenous eating along with the ingestion of large amounts of air. It is more common in large and giant breed dogs, in dogs eating dry foods exclusively, dogs fed single daily meals, those ingesting large amounts of water and/or having vigorous exercise bouts at or near meal time. Anatomically, a longer heptogastric ligament has been implicated and may explain the association with dogs that have a narrow thorax and deep chest.

Glickman et al. (1997) reported that a stressful event, change in meal time, elevated intake, change in physical activity, and an underlying fearful temperament were risk factors for the development of GDV in a controlled retrospective case study. Stress (noise) has been shown to decrease gastric intestinal motility and gastric emptying in dogs (Gue et al., 1989).

Further, central administration of CRF (the HPA stress signal) blocked motilin (an endocrine signal for gut motility) release in dogs (Bueno et al., 1986). While stress is not likely the underlying cause of GDV, it may exacerbate the condition via its effects on the HPA axis and subsequent decrease in the movement of gut contents at a very critical time. Fatality rates for dogs can be high without immediate veterinary attention.

Prevention of GDV relies on food and animal management and includes feeding multiple meals daily, feeding some canned or wet foods, keeping food bowls at ground level (not elevated), and discouraging exercise just before and just after meal time.


EATING DISORDERS

Obesity and anorexia are at the two polar extremes of eating disorders. However, they may share a relationship with stress and its effects on nutrition and health. Obesity affects approximately 30% of domestic dogs and cats.

The syndrome is one of too much food and too little activity. Quite possibly it has an underlying stress factor as well. In people, a common response to stress and depression is consumption of ‘comfort’ foods. There may be a biochemical basis for this appetite. Pecororo et al. (2004) demonstrated that in rats subjected to repeated restraint stress concurrent with an increase in caloric efficiency and a selection for ‘comfort’ food, circulating ACTH and corticosterone peak concentrations decreased. In other words, stress led to a choice of comfort food and this in turn reduced the activity of the HPA axis. Whether similar effects occur in dogs or cats has not been reported. However, the implications for animals provided ad libitum access to tasty food choices, coupled with underlying stress or anxiety, may alter food intake behavior and exacerbate weight control and obesity problems. Ways to reduce obesity in dogs and cats have garnered much attention in the current literature.

Most approaches have attempted to reduce caloric intake through dilution with fiber, high levels of grain and starch, and food management strategies. However, few have been successful. Quite possibly the behavior/stress component of the equation has been overlooked and should be considered as part of the solution. The concept of feedback/feed-forward mechanisms on food selection provides a clue to explain why certain elements in food may invoke the feeling of comfort or relief from the stress. These elements, should they be identified, may benefit the stressed-induced obese dog or cat by helping to relieve the sensation of stress while overcoming the issues with excessive caloric intake.

At the other end of the eating disorder spectrum, stress has been linked to anorexia or inappetence. This is often associated with illness. Anorexia is common in clinical settings after surgery or as a function of boarding.

Inappetence is a leading sign and complaint for dogs and cats taken to the veterinary clinic. Finicky cats, aged animals, surgical recovery, and certain overly nervous breeds may suffer from inappetence thus leading to caloric intake below their needs (Houpt, 1991). Many dietary deficiencies and toxicities are first recognized when intake declines or stops. Therefore, changes in the diet, feeding environment, or psychological state may be partly involved (Michel, 2001), but most often it is a secondary effect of other acute or chronic illnesses.


FEARS, ANXIETY, AND PHOBIAS

Stress can manifest as fear, anxiety, and phobias. Although each may seem the same, there are some distinct and meaningful differences. Fear and anxiety are emotional states caused by the perception of actual danger (fear state) or possible danger (anxiety state) that threaten the well-being of the individual (Appleby et al., 2003). Phobias occur when the fear is perceived but the factual danger no longer exists. Fears, anxiety, and phobias involve the autonomic nervous system and the HPA axis. Rugbjerg et al. (2003), in a survey of Danish pet owners, established that 6.1% of the 4,359 respondents’ pets experienced separation anxiety and 6.1% were afraid of shooting (noises). The owners with dogs experiencing shooting phobias were less inclined to seek help than those with dogs experiencing separation anxiety. Although they share many of the same outward signs, noise phobia and thunder phobia are different conditions (Overall et al., 2001) and may involve a different neuroendocrine response. Treatment by desensitizing or conditioning is difficult and time consuming and pharmacological treatment must be administered prior to the episodes and has side effects.

Pheromone therapy was shown to have some benefit with noise fearful dogs (Sheppard and Mills, 2003). Millions of dogs and cats are relinquished to shelters every year. The temperament of these animals has a profound effect on whether they will be adopted and how successful they will be in the adoptive home.

Unfortunately, shelter dogs and cats react to a great number of stresses. In a study reported by Hennessy et al. (2002a), behavior and reactivity decreased (pre- vs. post-assessment) in shelter dogs fed a nutrient dense diet containing animal-derived proteins. In a separate study, shelter dogs had lower circulating stress hormones (ACTH and cortisol) when fed a higher plane of nutrition coupled with a program of human interaction (Hennessy et al., 2002b). Fear, aggression, and biting are also a major issue with dogs. In a study with dogs that had previous aggressive and dominance issues, dogs fed low (17%) and medium (25%) protein diets had lower territorial aggression (mostly from fear, Dodman et al., 1996). However, dominance aggression and hyperactivity were not affected by protein level.

Dominance aggression was highest in dogs fed a high protein (30%) diet without supplementation of tryptophan (DeNapoli et al., 2000). A low protein (18%) diet supplemented with tryptophan had lower territorial aggression scores. Tryptophan is a precursor to serotonin, which is associated with feelings of wellbeing and calm.


SEPARATION ANXIETY SYNDROME

Separation anxiety syndrome (SAS) makes up a significant caseload for behavioral specialists. It occurs in both cats and dogs, but is far more prevalent and dramatic in dogs. Numerous behaviors have been noted with this disorder and they can be conveniently put into three categories: inappropriate elimination, vocalization, and destructiveness. In extreme cases, self-mutilation may be noted as well (Schwartz, 2003). At the owner’s departure, the animal may display depression, agitation, and anxiety. Hyper-attachment, boarding, moving, and time spent in a shelter have been implicated as conditions that may predispose animals to SAS. Separation anxiety has also been reported to result from zinc toxicity (Goicoa et al., 2002). In a controlled study, Flannigan and Dodman (2001) surveyed owners of SAS dogs and owners of ‘control’ dogs with ‘other behavior problems’.

Owners of dogs diagnosed with SAS overwhelmingly identified behaviors of destruction, elimination, and vocalization versus owners of the control dogs. More importantly in this study, factors associated with the aberrant behaviors were dogs with single owners, dogs obtained from shelters, addition of family members or other pets, and noises. Factors that were not associated with SAS in these dogs were sex of the dog, age when acquired, other pre-existing pets in the home, gender of the owner, spoiling activities, and acquisition from a pet shop. In other words, stress was a predisposing factor in SAS. Current approaches to resolution of SAS involve changes to owner routines, changes to interaction between the pet and owner, removal of fear and phobic elements, changing sleeping, eating and exercise habits, pheromone therapy, and removal of punishment. In extreme circumstances, pharmacologic support may be used in an effort to mentally distance the anxiety initiators from the memory.


Concluding remarks

Clearly the response to stress is manifested in numerous behaviors and pathologies in the dog and cat. There are a number of food/nutritional, environmental, and psychological factors that can influence the perception of stress by dogs and cats. Recognizing that these are real factors in the lives of companion animals and that they can have an impact on animal health and wellbeing will likely be of great benefit. Further, gaining a better understanding of the interactions among various stress factors is just now in its infancy. Research in the future will likely provide valuable clues on how these systems are integrated and how better to balance the inputs.

Our current approach to dealing with stress responses in companion animals is to: 1) identify and remove or eliminate the stress, 2) treat the animal with a compound that blocks, blunts, or destroys the reflex response, and 3) develop a re-training behavior-modification regime to manage through the stress response. In the future, nutritional intervention may provide one more tool to aid in reducing or treating stress responses in affected companion animals. As a hypothetical example, nutritional support with soluble fiber, essential (conditionally) fatty acids, and probiotics/prebiotics may prove beneficial for IBD. Balance/supplementation with trace minerals like zinc, selenium, and chromium may benefit FIC and SAS. Peptides, nucleotides, and monosaccharides may be the ‘comfort’ food ingredients that alleviate the stress component of obesity. Protein levels and type of protein may benefit dogs with noise fear or fear/aggression. These and many more behavioral-nutrition approaches will find value in our ability to better understand and manage stress and stress responses in companion animals.

It has been shown that dogs and cats live with a variable degrees of stress. In some animals, stress precipitates a number of chronic behavioral and pathological conditions. Nutrition may play a supporting role in reducing the magnitude of stress, and in the future, a few of the stress conditions may actually be resolved by meeting nutritional deficiencies, imbalances, toxicities, or nutritional-endocrine interactions.


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Author: GREG ALDRICH
Pet Food & Ingredient Technology, Inc., Topeka, Kansas, USA