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by the American Association for Laboratory Animal Science Animal Well-Being
III. An Overview of Assessment
J. Derrell Clark,1,2 Dawn R. Rager,3* and Janet P. Calpin2†
Abstract Assessment of animal well-being is a complex matter. It is difficult to establish a causal link
between stimuli and internal state because of numerous variables and the time interval between cause and
effect. Many studies document a correlation rather than a causal relationship among stimuli, responses, and
subsequent health, disease, or mental state. Research objectives are often vague, the choice of assessment
parameters is perplexing, and the results are difficult to interpret. In general, animal well-being cannot be
assessed directly. There are no standardized methods or specific endpoints that provide an objective determi-
nation. Overt changes in physical and psychological functions occur only after the animal has experienced a
prepathologic state. An animal’s response to general arousal, life’s events, and aversive stimuli depends on an
integrated activation of various neural and endocrine factors. A variety of physiologic, biochemical, and be-
havioral characteristics change when an animal is exposed to aversive situations and stimuli, although many
also change with the onset of positive general arousal, such as play, pleasant experiences, and sexual excite-
ment. There is a need to evaluate numerous criteria (e.g., performance, clinical state, neurochemistry, endo-
crinology, immunology, morphology, behavior, and ethology) to compile a complete mental and biological
profile of animals. The various systems, processes, and individual specific responses are interrelated and
interact in a well-structured manner. Given the complexity of the topic and the disparate disciplines in-
volved, developing a comprehensive understanding of animal well-being is not straightforward. Consequently,
observers should be cautious. Foremost in any determination of animal well-being is assurance that criteria
being used are relevant to well-being.
This is the third in a series of reports intended to provide a tion for animal care providers. Nevertheless, future research scientific overview of animal well-being. Here we provide an to evaluate well-being determinants should be directed to overview of means of assessing animal well-being. Specifi- applied animal care and use matters.
cally, assessment strategies, overview of assessment cri- Because well-being is complex and involves numerous so- teria, and precautionary factors to be considered are pre- matic and psychological aspects and interaction of body sys- tems, it is unlikely that investigators working alone or in onlyone area have sufficient expertise to derive the maximal in- Strategies for identifying assessment criteria
formation possible from collected data. A multidisciplinary Little objective research has focused specifically on the re- team approach of investigators, including veterinarians, be- lation of practical animal care and use issues, per se, to labo- haviorists, ethologists, immunologists, neurobiologists, psy- ratory animal well-being. However, basic research in such chologists, physiologists, pathologists, and epidemiologists, fields as animal biology and behavior, farm animal science, studying various systems and functions simultaneously is ethology, stress biology, and PNI has been extensive; the ex- more likely to be successful in assessing determinants of well- perimental paradigm involves physical or psychosocial fac- being and contributing to the improvement of animal care tors that are of concern in animal care and use. Thorough and use. Also, participation by sciences that have not tradi- review of this literature would likely provide useful informa- tionally been associated with investigation of animal issues,such as materials science, biomechanics, and industrial de-sign, may contribute relevant information that would not be Department of Medical Microbiology1 and Animal Resources,2 College ofVeterinary Medicine, and Department of Psychology,3 College of Arts and provided by traditional biomedical and behavioral approaches Sciences, The University of Georgia, Athens, Georgia *Present address: St. John Fisher College, 3690 East Avenue, Rochester, Some assume that captive or intensive conditions have a †Address reprint requests to Janet Calpin, LATG, Animal Resources, Col- negative influence on animals and that natural or exten- lege of Veterinary Medicine, The University of Georgia, Athens, GA 30602- sive conditions promote well-being. On the other hand, natural conditions have negative aspects, such as preda- be used with minimal disturbance to the animal because tion, starvation, natural disasters, disease, and death. Well- disturbance can induce confounding changes independent being of animals in captive conditions can be good. Domes- ticated animals have certain characteristics that facilitated Ultimately, well-being must be evaluated by objective their domestication (5). Domestic species and some animals comparisons between animals housed in different kinds of commonly maintained in captivity cope with and adapt and husbandry systems, as well as between laboratory animals habituate to life in captivity so that all aspects of life for and their wild counterparts (11). Specific environments their counterparts in a natural setting are neither neces- should be evaluated on the basis of an animal’s needs, from sary nor desirable in captivity. Research should be directed the animal’s perspective (12). Well-controlled experimen- toward determining the status of well-being in a captive tal protocols, quiescent conditions, and appropriate and environment and making appropriate adjustments rather consistent animal handling techniques are critical to suc- than simply attempting to simulate an animal’s natural cessful well-being studies. Attention to subtle procedural habitat and ecology (6). Simply providing naturalistic ma- details and stimuli not only adds to the understanding of terials and settings will not ensure natural behaviors or animal well-being but also reduces variability in data and facilitates comparison among closely related studies (3).
Often physical or psychological disorders and diseases In assessing prior studies of animal well-being or plan- do not develop suddenly, but days, months, or years may ning future studies to address the effect of biopsychosocial intervene between first exposure to an etiologic factor(s) factors, stimuli and responses that influence health and and full manifestation of illness or affective disorder. Dur- well-being should be considered. Also, factors other than ing pathogenesis a number of factors may be involved, and aversive stimuli may influence many responses. In inter- a number of changes may occur. Overt changes in physical preting data and comparing or contrasting situations, the and psychological functions occur only after the animal has consistency (or lack of it), controllability, and predictabil- experienced a state of vulnerability (i.e., a prepathologic ity should be considered. For a clear relationship between state). A prepathologic state does not necessarily imply that an aversive situation and well-being to be documented, the the pathologic state will follow, but it represents a threat aversive stimulus has to be identified, the physiologic and to well-being (8). Many stimuli may affect the physical and behavioral changes have to be clearly described, the re- psychological well-being of captive animals that would be sponses must be quantified, and damage to the physical unlikely to lead to a pathologic state, at least in the short and/or psychological well-being of the animal has to be evi- term. For example, atypical behaviors are not necessarily associated with reduced well-being. An animal may expressatypical behaviors as a homeostatic process of adapting to, Overview
coping with, and controlling a changing or potentially aver- General: Coping with and adapting to internal needs
sive situation. However, atypical behavior may be an indi- and external demands of the physical and psychosocial cator of a potentially aversive circumstance or event that environment by means of behavioral, neural, endocrino- may lead to maladaptive behavior, distress, and state of logic, metabolic, and other physiologic responses to main- nonwell-being (6). Pathologic states are not logical or hu- tain homeostasis is a general biological phenomenon in all mane measures of endpoints for assessing well-being (9).
animals. As discussed previously, reactions to life’s events An animal’s vulnerability increases as the duration and vary on the basis of a multitude of factors, and the responses magnitude of the prepathologic state intensifies, thus in- may be normal or abnormal, maladaptive, or an indication creasing the likelihood of a pathologic state (8). Therefore of an affective disorder. Conclusive diagnostic criteria to determination of early responses to aversive stimuli dur- differentiate between these states do not exist. Determin- ing the prepathologic state may potentially provide useful ing which physiologic and behavioral responses of animals indicators of threats to well-being.
are abnormal or extreme is a major factor in assessing well- Mench (10) has discussed some pros and cons regarding being. There are no true controls or baseline values and no attempts to identify measures for determining well-being.
single factor or set of criteria that are indicative of well- Understanding animal well-being involves study of under- being or nonwell-being. Assessing a single or a limited num- lying questions about animal emotions, sensations, needs, ber of responses is not likely to provide an objective overall motivations, and level of awareness. She concluded that view of the physical and psychological state of an individual the focus should not be on looking for and developing new subjected to potentially threatening situations. Even with measures of well-being, but on refining current measures known indicators, often there is no clear or natural delin- and determining how they are interrelated and related to eation between normal and abnormal values. When sub- jected to long-term, low-level, aversive stimuli, generally Neurobiology, endocrinology, immunology, behavior, mor- an animal’s response gradually moves from normal to ab- phology, and animal preference offer opportune areas of investigation for measures to assess well-being. In the past, To assess the impact of aversive stimuli, factors such as the autonomic nervous system and neuroendocrinologic re- the intensity, quality, frequency, duration, and rate of sponses have been studied most intensely. In assessing dif- change of the stimulus, and whether it is novel, incidental, ferent indicators of well-being, those most useful are reli- or routine must be considered. Stimuli may be of short term able in determining the state of animal well-being and can (phasic activation) or persist for a prolonged period (tonic Vol 47, No 6Laboratory Animal ScienceDecember 1997 activation) (14). In the past, most studies of stress have the median eminence of the hypothalamus before being used short-term, aversive stimuli. With longer-term stimuli, transported to the anterior pituitary gland. Stimulation of there may be a rapid change in response toward baseline this region excites many of these nerve endings and there- values as the animals adapt, cope, and habituate in an at- fore causes release of essentially all the hypothalamic fac- tempt to maintain homeostasis. Nevertheless, animals sub- tors, even though some may have little or no apparent role jected to tonic activation are not the same as activation- in maintaining homeostasis. Most neuroendocrine studies naive animals, and parameters do not necessarily return have focused principally on the responses of the pituitary to baseline, even after animals adapt, cope, or habituate.
In experimental studies using a prolonged stimulus, the Mason (18) has described two types of responses in rhesus question of whether the animals develop a successful cop- monkeys. Concentrations of some hormones (e.g., epineph- ing strategy or end up in a state comparable to learned rine, norepinephrine, corticosteroids, growth hormone, and helplessness needs to be considered (15). To some extent, thyroxine) increase during exposure to aversive stimuli and the activators and the responses are a continuum. All aver- return to baseline values after the stimuli are removed. These sive or potentially aversive stimuli cannot be simply cat- hormones have a predominantly catabolic function by mobi- egorized as phasic or tonic activators. Responses are inter- lizing energy reserves for a flight-or-fight response. Concen- related and cannot be separated on the basis of phasic or trations of other hormones, such as insulin, androgen, and tonic activation, but somewhat similar responses may oc- estrogens, decrease during aversive situations but increase cur with both. An animal’s responses to life’s events are after stimuli are removed. These hormones have anabolic func- extremely complex and dependent on many factors, and tions in metabolism. Therefore, prolonged aversive situations simple, straightforward conclusions about well-being will induce depression of thyroid activity, inhibition of body growth, not be readily available in the foreseeable future.
and suppression of sexual and reproductive behavior (19, 20).
This complexity makes it difficult to identify and address In simple terms, the body responds to prolonged aversive situ- all potential responses involved in an animal’s reactions to ations by conserving resources and reducing or stopping pro- aversive stimuli. Known responses may reflect only a por- cesses that detract from immediate energy mobilization (21).
tion of the body’s overall reaction. In general, responses Hypothalamus: The hypothalamus controls most of the can be categorized in broad terms (i.e., health status, clini- vegetative and endocrine functions of the body as well as many cal signs of disease, reproductive and productive perfor- aspects of emotional behavior (22). It has a vital role in ho- mance, longevity, neurochemistry, autonomic nervous sys- meostasis. In addition to stimulating release of catechola- tem reaction, endocrinology, immune function, morphology, mines, aversive stimuli initiate release of other hypothalamic behavior, and preference). The various systems, processes, hormones that in turn induce secretion of a number of ante- and individual specific responses do not function indepen- rior pituitary hormones, especially the gonadotropins and dently but are interrelated and interact in a well-struc- adrenocorticotrophic hormone (ACTH). Some of the spe- tured way. In addition to specific positive or negative re- cific hypothalamic hormones are corticotropin-releasing sponses to life’s events, counterresponses or feedback sys- hormone, serotonin, and prolactin-releasing factors, such tems affect an organism’s overall reaction and status and, as thyrotropin-releasing hormone, vasoactive intestinal therefore, its well-being. To improve our understanding of peptide, bombesin, cholecystokinin, neurotensin, endor- the perplexing question of homeostasis and well-being, phins, somatostatin, substance P, histamine, melatonin, these feedback patterns also must be considered.
Classic measures: Classic and practical criteria assess-
Anterior pituitary gland: In the anterior pituitary gland ing animal well-being include a combination of animal ap- is a closely related family of peptides derived from pro- pearance, performance, behavior, productivity, disability, opiomelanocortin (POMC), namely ACTH, -lipotropin injury, disease, longevity, mortality, and of the state of an ( -LPH), -endorphin (endogenous morphine), and animal’s environment. Morton (16) and Morton et al. (17) -melanotropin (23). Their secretion is under CNS control, discussed some of these assessment criteria as they apply via corticotropin-releasing hormone, which is thought to have a rapid effect on the synthesis and release of the Neurochemical and endocrine measures: Regulatory
POMC-derived peptides. Pro-opiomelanocortin is converted mechanisms and systems at several levels, namely the cen- to ACTH and -LPH. -Lipotropin is converted to -endor- tral nervous system (CNS; limbic system, midbrain, hypo- phin. Factors regulating the release of ACTH also control thalamus, and cerebrum), peripheral nervous system, pi- the secretion of -LPH and -endorphin. The gonadotro- tuitary gland, adrenal glands, kidneys, and pancreas, af- pins, luteinizing hormone and follicle-stimulating hormone, fect neural, biochemical, endocrinologic, immunologic, mor- and prolactin also are secreted from the anterior pituitary phologic, psychological, and behavioral responses associ- gland. A variety of aversive situations, similar to those in- ated with aversive stimuli. Many neurochemical and en- ducing ACTH secretion, stimulate prolactin secretion in docrine changes occur in response to arousing and stimu- lating events. The direct and indirect physiologic role of Posterior pituitary gland: Two octapeptide hormones, some of these neurotransmitters and hormones in response vasopressin and oxytocin, are formed in the hypothalamus to noxious stimuli is unknown or poorly understood; some and are stored in the posterior pituitary gland (neurohy- may be involved indirectly. For example, all or most of the pophysis). Both have a part in the stress response because hypothalamic hormones are secreted at nerve endings in they influence the release of ACTH. Vasopressin has been documented to enhance ACTH release in all species stud- dritic branching of neurons, and more synapses per neu- ied. However, oxytocin stimulates release of ACTH in the ron in the brain than do animals in a less enriched envi- rat but inhibits it in primates. Plasma concentrations of both hormones may be affected by aversive stimuli (29).
Adrenal cortex: In response to the release of ACTH by Precautions and other considerations
the anterior pituitary gland, the adrenal cortex produces In attempting to assess animal well-being, a number of glucocorticoids, the most important being cortisol and cor- precautionary factors must be considered. Principal con- ticosterone. Glucocorticoids are central to many of the siderations in any assessment of well-being are recogni- physiologic responses to aversive situations. Although an tion and control of independent variables and interaction increase in glucocorticoid concentrations in response to of physical and psychological states (38). The multitude of aversive stimuli can represent a sensitive index of the in- responses to aversive situations complicates the assessment tensity of discomfort or distress experienced by animals, of well-being and limits the significance of any single mea- the adrenal cortex does not respond to all aversive stimuli sure. Thorough evaluation of well-being requires consider- (21). Thus, a simple determination of the plasma concen- ation of multiple measures and different approaches. Even tration of corticosteroids is not a definitive measurement then, only the physical and psychological responses that directly affect animal well-being should be used as indica- Other hormones: Other hormones, such as insulin, thy- tors (9, 38). Statistical significance is not necessarily clini- roxin, testosterone, estrogen, growth hormone, renin, and cal significance when considering well-being. A statistically angiotensin, have not traditionally been associated with significant change cannot be judged negative or positive response to aversive stimuli. Noxious stimuli can affect until an association between the variable and animal well- their secretion. During noxious situations, growth hormone is secreted in some species, (e.g., nonhuman primates), In assessing measures of animal well-being, maladap- whereas GH secretion is suppressed in rodents and is un- tive or undesirable states are not necessarily the result of affected in sheep. Consistency of response is even more la- change. Life’s events, various stimuli, and threats to ho- bile in the secretion of gonadotropins or thyroid-stimulat- meostasis may be potentially aversive, but are not invari- ably so. When identifying situations that are aversive, the Immune function: The neuroendocrine system affects
effects of interacting variables on individual variation immune responses. Subjecting animals to aversive stimuli should be considered. Responses to the release of hormones during prenatal and early life, varying social interactions and neurotransmitters may differ between individuals and among adult animals, and exposing them to environmen- change from time to time on the basis of such things as tal circumstances over which they have no control are circadian rhythm and interaction with other events (40).
among the psychosocial manipulations that induce neuroen- One set of stimuli may evoke marked responses in one ani- docrine changes implicated in the modulation of immune mal and little or no response in another (38). An individual responses. There are a number of stimulus-induced, may respond differently to the same stimulus on different adrenocortically mediated alterations of immune responses.
occasions. Stimuli evoking amusement or other pleasant Glucocorticoids, for example, are usually immunosuppres- sensations are nearly as potent as unpleasant ones in pro- sive. It is generally assumed, therefore, that an increase in voking an increase in some neurochemicals and hormones adrenocortical steroid concentrations is responsible for the (41). Many forms of emotional arousal, such as mating, frequently observed suppression of immunologic reactiv- anticipation of food, or minor procedures like handling, ity associated with these stimuli. Other stimulus-induced stimulate the release of glucocorticoids and other hormones.
alterations in immunologic reactivity are independent of Even activities considered normal, such as standing, exer- adrenocortical activation (30–32).
cise, and mental stimulation, may be associated with in- Behavior and animal preference: Animal behavior
can be useful in the assessment of animal well-being.
An animal’s responses to aversive situations are highly Behavior can be observed directly and noninvasively. A organized strategies and processes that have evolved over knowledge of species-specific behaviors and the normal time from dealing with life’s events. At times they are criti- behavior of individual animals is critical in using this as cal to survival, particularly for animals in their natural an indication of well-being. Animal preference is also state. It is only when the responses are a real threat to the used by some to assist in determining animal well-be- animal’s homeostasis or compromise the intended use of the animal that its well-being may be jeopardized. There Morphologic changes: Aversive conditions, especially
is reason to believe that when a stimulus produces fear, longer term, can cause morphologic and pathologic pain, or other unpleasant states, assessment may be use- changes in some tissues. Examples of morphologic ful in corroborating and quantifying the animal’s reactions changes caused by aversive stimuli include fatty acid deposits in walls of blood vessels, arteriosclerosis in kid- With passage of time, there has been a major shift in the neys, gastric ulceration, decrease in size of some organs perceived relationship between physiologic measures and of the immune system, and adrenal hypertrophy. On the well-being. Selye’s ideas led people to think that all man- other hand, animals in an enriched environment have ner of unpleasant psychologic states and challenges to bio- heavier and thicker visual cortex, more extensive den- logical functioning could be detected on the basis of in- Vol 47, No 6Laboratory Animal ScienceDecember 1997 creased activation of the hypothalamic-pituitary-adreno- density; age and sex of animals; effects of adaptation, cortical system. However, much of the earlier work with conditioning, and training; and biological interactions physical stimuli failed to consider psychosocial variables (37). Mason (44) pointed out that much of the early research Additionally, the organization of the endocrine system as a into stress, especially that involving exposure of animals whole is based on a hierarchy of closed-loop systems. The se- to a variety of aversive physical stimuli, shared one impor- cretion of most hormones is regulated by feedback mecha- tant characteristic: a novel, strange, or unfamiliar envi- nisms of these systems. There are two types of mechanisms: ronment. Thus, the common thread that may have ex- negative feedback and positive feedback. Negative feedback plained these animals’ responses was the psychological and is the most common control mechanism regulating endocrine psychosocial relevance of the stimulus rather than the par- secretion; in its simplest form, hormone A stimulates the pro- ticular physical stimulus to which they were exposed. Con- duction of hormone B, which in turn acts on the cells produc- versely, studies of psychological well-being must also con- ing hormone A to decrease its rate of secretion. In the less common positive feedback mechanisms, hormone B further Assessment of general health, production, reproduction, stimulates the production of more hormone A rather than di- longevity, and behavior has a vital role in determining well- minishing it. These feedback systems can indirectly affect being of animals. These should be used as an initial and other measures of assessing well-being.
general set of criteria, and some are useful for persons with Preference testing, as a measure of well-being, has in- limited training, experience, and/or diagnostic resources.
herent weaknesses. One major shortcoming is that it does However, productivity measures must be used with cau- not indicate the degree of importance that the animal at- tion. When these measures are used to assess animal well- taches to the preferred option (43). An animal’s choice may being, the focus should be on individual animal performance be based on something other than the experimental vari- rather than statistical data based on a large population, as ables. The animal’s choice may not be a true indicator of is commonly done in intensive production systems. Overt its preference of the available alternatives because it is disease and failure to grow or reproduce indicate poor well- possible that the animal may like or object to all available being. However, the reverse is not necessarily true. Ani- alternatives. Experience of animals is also a factor. Ani- mals may not have overt disease and may be growing and mals are reluctant to choose alternatives with which they reproducing. However, the growth and reproduction may have no experience (48). Animals may choose a desirable come at a physical and psychologic cost. Such animals may item or alternative to suit a short-term need, but these may be in a prepathologic state and thus be more vulnerable to not be the best choices for satisfying long-term needs or disease or psychological disorders (9). Differences in be- more basic necessities (49, 50). Animals may choose differ- havior that can be seen when animals are kept in various ently under different conditions, and individual animals environments may indicate that the environments are in- may have different preferences. Therefore, preference stud- ducing different levels of distress response in the animals ies should be well controlled and interpreted conservatively.
(13). Distressed animals in their natural habitats often Other, more stringent methods for assessing needs (as op- appear to limit behavioral responses, perhaps to avoid at- posed to preferences) have been developed on the basis of tracting the attention of predators (45). Nevertheless, be- operant conditioning/aversion testing methods (51).
havior alone is not an all-inclusive indicator of well-being.
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