Vol 47, No 6 December 1997 Laboratory Animal Science Copyright 1997 by the American Association for Laboratory Animal Science Special Topic Overview Animal Well-Being I. General Considerations J. Derrell Clark,1,2 Dawn R. Rager,3* and Janet P. Calpin2† Abstract Recently, interest in and concern about animal well-being has been increasing because of changing views toward nonhuman animals, societal attitudes, legislation, and conduct of quality scientific research and testing. Animal well-being is a vague concept that can neither be viewed in a purely objective manner nor simply described, defined, or assessed. It is not a scientifically or technically precise state, but rather a multidimensional one. Factors such as animal needs and perspective, critical anthropomorphism, and human social and individual values are involved. There are limitations in determining the overall well-being of an animal and comparing well-being in disparate environments. Nevertheless, there is an extensive and evergrowing list of complex factors thought to affect homeostasis, sensitivity, interrelationships, and feedback control mechanisms. Research data from a variety of fields, such as animal biology and behavior, stress biology, and psychoneuroimmunology, increasingly support a holistic view of well-being. Existing data suggest an interactive system linking internal psychologic, neurologic, physiologic, immunologic, endocrine, and biochemical events with the external psychosocial and physical environment. An animal’s state of well-being or homeostasis is determined by a multitude of external (psychosocial and physical stimuli) and internal (mental and biological responses) factors and interacting variables and by other aspects such as ethology, genetics, individual variation, social milieu, experience, learning, perception, coping style, and intensity, duration, and frequency of stimuli. Objective This paper is the first in a series intended to provide a scientific overview of animal well-being. Although well-being is now a commonly used term, there is no consensus regarding its meaning, and a precise operational definition of animal well-being remains elusive. Consequently, factors that determine well-being are poorly understood, and means of assessing well-being have yet to be validated. This is especially true with regard to psychologic or mental well-being of nonhuman animals. Given that relatively few empirical studies addressing the psychological well-being in laboratory animals exist, it would appear that little objective information regarding this subject is available. However, farm animal scientists have advanced the understanding of animal well-being more so than any other scientific group. For the past four decades, those investigators have elucidated the factors affecting abnormal, Department of Medical Microbiology1 and Animal Resources,2 College of Veterinary Medicine, and Department of Psychology,3 College of Arts and Sciences, The University of Georgia, Athens, Georgia *Present address: St. John Fisher College, 3690 East Avenue, Rochester, NY 14618. †Address reprint requests to Janet Calpin, LATG, Animal Resources, College of Veterinary Medicine, The University of Georgia, Athens, GA 306027381. 564 appetitive, consummatory, and stereotypic behaviors; methods of measuring preferences, needs, and aversions; and the strengths and limitations of physiologic behaviors. Also, extensive literature has accumulated in related fields, such as basic animal biology, animal behavior, stress biology, and psychoneuroimmunology (PNI). Because much of this information is likely to be useful in developing an understanding of animal well-being, we reviewed these topics. However, exhaustive reviews proved to be impractical, given the diversity and breadth of these topics and the massive numbers of publications on the many individual facets that may relate to the concept of well-being. We have therefore chosen to focus on aspects of animal biology, behavior, stress, and PNI that we believe will be most useful in developing an understanding of the concept of animal well-being. It should be noted that, in addition to confusion regarding well-being per se, related concepts, such as stress and mind-body interactions (i.e., the focus of PNI), also are controversial. We view the current status of knowledge in these areas as rudimentary as it relates to animal well-being. The ideas presented in this series of articles are not intended to resolve existing controversies. Rather, our goal is to provide a scientific overview of animal well-being and related topics that will serve as a stimulus for empirical research in this area. This initial article of the series will discuss animal well-being from Special Topic Overview a philosophical and scientific perspective, address the difficult matter of defining animal well-being, and explain how the developing field of PNI may be especially relevant in understanding animal well-being. Background Concerns: Humans are keenly interested in their relationships with nonhuman animals, including use of them for food, fiber, research, teaching, entertainment, and companionship. One aspect of the issue deals with animal welfare or wellbeing. Well-being of animals used in laboratory settings is a major concern of the biomedical scientific community, regulatory agencies, and animal protectionists. For example, the stated purpose of the Guide for the Care and Use of Laboratory Animals (1) “is to assist institutions in caring for and using animals in ways judged to be scientifically, technically, and humanely appropriate,” and one of the purposes of the Animal Welfare Act (2) is to ensure that certain animals intended for use in research facilities are provided humane care and treatment. Anthropomorphism: In the evolution of the scientific community’s practices related to care of animals used in research, we have, perhaps out of necessity, determined what we think is best for animals principally from the human perspective based on human objectives (anthropocentrism). To some extent, this approach has been fueled by industrialized societies’ utilitarian concept toward animal use (3), an urge to control nature (4), and the need for reduced variables with scientific control. Because the final judgement of animal wellbeing ultimately rests with humans, a critical anthropomorphic perspective is necessary. Critical anthropomorphism has been defined as empathy tempered by objective knowledge of the particular species’ (or individual animal’s) life history, behavior, and physiology (5–7). Biomedical and behavioral scientists must strive to develop an acceptable definition and understanding of animal wellbeing and to implement valid and objective means of evaluating well-being in laboratory animals. From the physical wellbeing perspective, this has been at least partially accomplished. Much emphasis has been placed on physical factors, such as freedom from disease and contamination. This has led to strict veterinary care and disease-control practices, cleaning and sanitation protocols, guidelines for facility construction, and other managerial practices and programs that have focused on the standardization of animal care and use and reduction of variables to improve the quality of science. Until recently, there has been little interest in the psychological well-being of animals unless it overtly affected specific research activities and data interpretation. It has been taken for granted that animal caregivers know what is desirable or aversive for animals. Scientists and animal protectionists alike are guilty of uncritical anthropomorphism and subjectivism regarding the psychological well-being of animals. Science has compiled a voluminous amount of knowledge about animals on the basis of scientific and technologic advances, computer technology, and biotechnology, yet we know little about their mental well-being and what factors promote it. Relatively few empirical studies have addressed psychological well-being; thus, scientists find themselves in a tenuous position when faced with this issue. This situation was exacerbated in 1985 when the U.S. Congress legislated enrichment of animals’ environments by passing laws mandating exercise for dogs and consideration of psychological well-being of nonhuman primates. Ideally, legal judgments about housing, animal husbandry practices, and psychological needs of captive animals should be based on objective scientific information. However, the scientific community and U.S. Department of Agriculture officials readily admitted there was inadequate scientific information on which to objectively base these standards (8). Nevertheless, with the passage of this federal law, standards had to be written and implemented despite the lack of scientific knowledge in these areas. Similar circumstances could arise in the future. Often society, sometimes through governmental regulation, demands change before definitive scientific knowledge is available. Dilemmas: The issue of animal well-being is a scientific and ethical enigma and presents numerous dilemmas for science and society in general. Uncertainties and differences arise in the process of making value judgements, formulating concepts, selecting appropriate descriptive terms, developing assessment criteria, and interpreting available data related to the issue of well-being. Our views of well-being in animals have evolved from reliance on criteria that reflect humans’ goals and values, such as prevention and treatment of disease, reproduction, growth, and productivity. On the other hand, it is being argued that such criteria should reflect the animal’s perspective (i.e., the true needs of the animal), what matters to the animal (9), or, in the words of Russell and Burch, “what is right for the animal” (10). Health, reproduction, and growth are important to animals and contribute to well-being. It is our opinion that although humans cannot logically evaluate well-being from the animal’s perspective, a critical anthropomorphic perspective may be ethically preferable to an anthropocentric perspective. These perspectives need not be mutually exclusive, although they may be so. Much of the debate surrounding animal well-being arises from this concern for adopting an ethically appropriate perspective (9). Animal needs: An acceptable definition of well-being will almost certainly involve reference to an animal’s needs, and will require that such needs be determined from a critical anthropomorphic perspective. According to Curtis (11), application of Maslow’s ranking of human needs to the needs of animals could result in a hierarchical organization from highest to lowest priority: physical needs, safety needs, and psychological needs. The concept of physical and safety needs is generally clear. Providing for these needs forms the basic tenets of what has long been considered adequate animal care and includes such aspects as nutrition; physical environment (e.g., thermal, air, light, gases, particulate matter); veterinary care; humane practices; and protection from harmful environments, predation, and vandalism. Psychological needs, however, are more difficult to identify, especially without imparting a subjective bias. A similar hierarchy of needs can be identified in the concept of “Five Freedoms” (12). These freedoms are factors likely to influence the well-being of animals. Modified from various sources in applied ethology, these are: freedom from thirst, 565 Vol 47, No 6 Laboratory Animal Science December 1997 hunger, and malnutrition; freedom from discomfort; freedom from pain, injury, and disease; freedom to express normal behavior; and freedom from fear and distress. Hurnik (13) has defined needs as physiologic requirements of an organism necessary for normal development and maintenance of good health. These needs have been categorized as life-sustaining, health-sustaining, and comfort-sustaining. However, satisfaction of these needs is not necessarily identical with the satisfaction of animal desires (wants). Odendaal (4) has described basic needs as primary requirements for an animal to have an acceptable quality of life, whereas wants are secondary and not necessary for an acceptable quality of life. Presumably, basic needs must be met for an animal to maintain a state of physical and psychological balance or homeostasis. If circumstances do not permit such needs to be satisfied, the result may be somatic and/or psychological pathologic changes. Species-specific as well as individual needs vary considerably and, therefore, should be considered. As discussed later, interacting variables contribute to individual differences. Deficiencies: In providing animal care, needs are either met or not met. If the needs are not met, they are considered deficiencies and may be the result of cruelty, abuse, neglect, or deprivation (11, 14). Cruelty involves the willful infliction of pain and/or distress because of human indifference or enjoyment. Abuse is associated with misuse, such as improper or injurious use, but not with self-gratification or satisfaction. Neglect occurs when a confined animal is denied a physical or safety need (e.g., feed, water, health care, or shelter), either deliberately or by ignorance. In laboratory animal care and use, cruelty, abuse, and neglect rarely occur. Deprivation, on the other hand, involves the denial of certain often less obvious, albeit vital needs. Many of these needs are psychological, involving various psychosocial aspects of an animal’s environment, and are not generally known or even ascertained. It is the form of maltreatment most difficult to assess. Deprivation is manifested (often subtly) by boredom, loneliness, discomfort, arousal, anxiety, uncertainty, frustration, irritation, aggression, alarm, conflict, fear, and distress. Semantics Terms: Terms and definitions are important in consideration of animal well-being. The inappropriate or inconsistent use of key terms can be a deterrent to progress and effective communication of ideas. Tannenbaum (15) states that “veterinarians and animal scientists sometimes define terms such as pain, stress, distress, anxiety, apprehension, fear, suffering, and needs carelessly or with insufficient attention to what these terms mean in ordinary discourse.” Although these terms are well understood generally and colloquially, it is difficult to gain agreement about their strict scientific definitions. Helpful, but not necessarily definitive, basic descriptive schemes of classification for different types of adverse states have been provided (5, 16). Some terms have become firmly fixed in our vocabulary and federal laws. Even though they are well intentioned, these words and phrases often confuse rather than clarify matters. Examples of such terms are humane care, welfare, psychological well-being, and exercise. Humane care is an anthro- 566 pomorphic term and is based on human perspectives, virtues, and values because humaneness is characterized by compassion, kindness, and sympathy. In contrast to humaneness, animal well-being involves conditions that the animal actually experiences or perceives (i.e., the animal’s feelings and perspective). Well-being and welfare are conditions of faring well and being free of discomfort, distress, and pain. There is confusion regarding use of “welfare” versus “well-being.” Even though welfare is an appropriate word for describing animal care and use, its use has engendered some disfavor in the United States because it has been associated with animal protectionism. Animal well-being is the more widely used and accepted term in the United States, but welfare is widely used and accepted in Europe (17). Fox (18) suggests that the concept of animal “welfare” has become entwined in ethical arguments relating to the proper treatment of animals. Accordingly, some veterinarians and ethologists tend to “avoid the term and advocacy of animal welfare in favor of advocating animal health and well-being (the latter implying provision of an environment and standards of care and husbandry that cause minimal stress and distress and satisfy the animal’s basic behavioral and social requirement)” (18). One approach uses well-being to refer to the state of the animal and welfare to refer to the broader concept of social and ethical issues (19). Mayer (20) has stated that animal welfare is a concept that is readily understood but cannot be defined with any exactitude, certainly not in a way that is satisfactory to the scientific world. Ewbank (21) has suggested replacing “welfare” with the words “health and well-being.” Psychology has had a prominent role in consideration of human well-being for many years. Because concern for the psychological aspects of well-being in animals is more recent, appropriate terminology for discussing this issue in animals is formative and evolving. Perhaps use of some terms well accepted in human literature may be worthy of consideration in animals if they are appropriately modified and defined. In human psychology, affective disorders comprise several clinical conditions pertaining to or arising from feeling or emotional reactions, which have in common depression or elation as a clinical feature (22). They are associated with psychophysiologic, psychiatric, cognitive, and social disturbances. The cause of these disorders is multifactorial, implicating genetic, biochemical, developmental, and psychosocial factors. An affective disorder is defined as a condition induced by the imbalance between environmental demands and the response capability of the individual to the demands that are perceived as threatening or overtaxing. Well-being: We believe that well-being is multifaceted, and factors that affect it are interactive and interrelated. An animal’s well-being or quality of life is its internal somatic and mental state that is affected by what it knows (cognition) or perceives, its feelings (affect) and motivational state, and the responses to internal and external stimuli or environments. Thus well-being involves a triad of stimuli, responses, and internal state. Stimuli or environments may or may not be aversive. Normal bodily adaptive, coping, and habituative responses function continually to maintain a homeostatic internal state (well-being). Ineffective responses may result in disorder, dysfunction, disability, disease, or death. Special Topic Overview Dualistic view: Well-being is often characterized as an internal state that is dualistic in nature (i.e., well-being is viewed as having physical and psychological aspects), a carryover of 17th-century Cartesian mind-body dualism (23). In the context of well-being, the terms physical, biological, physiological, and somatic are often used synonymously, as are the terms behavioral, social, mental, and psychological. Indeed, their precise definitions overlap, especially those for the first four terms. This is less true for the last four terms. Nevertheless, each term has a somewhat unique connotation despite overlap in explicit meanings. For example, the term physical implies bodily, corporeal, or more generally, material; biological refers to living organisms in general; physiological connotes normal; and somatic relates to the body. The remaining four terms are somewhat easier to distinguish, because behavioral is most often used to refer to overt responses or actions; social implies association with other organisms, especially conspecifics; mental denotes subjective processes related to mind; and psychological is currently viewed as encompassing behavioral and mental phenomena. Thus, in referring to the dualistic concept of well-being in animals, the terms physical and psychological seem most appropriate because, when taken together, these terms encompass somatic, mental, and behavioral facets of well-being. Environmental stimuli affect well-being and may be intrinsic or extrinsic. Intrinsic stimuli may be somatic or psychological in nature. Extrinsic stimuli include the physical or psychosocial environments (24). An animal’s responses to environmental stimuli ultimately determine its state of wellbeing. Choice of terms related to animal well-being should be determined by whether we are referring to the internal state (well-being), environment (intrinsic or extrinsic stimuli), or responses (e.g., neurobiological, endocrinologic, immunologic, morphologic, or behavioral). Holistic view: Although we acknowledge the popularity of the dualistic scientific and philosophical perspective of wellbeing, we do not support it. Historically, some scientists and clinicians have tried to categorize and simplify departures from homeostasis (disabilities, disorders, dysfunctions, and disease) by identifying a single cause and effect, the reductionist view. However, for a long time ethologists and comparative psychologists and physiologists studying motivation have recognized that there is no single cause and effect for most behavioral phenomena. As discussed later, physical and psychological disorders have multiple determinants, and in many instances the search for a single cause is overly simplistic. Taking a holistic view, evidence is increasing that physical and psychological phenomena are not separable, but that molecules, cells, organs, systems, the animal, the social group, and the entire environment are interactive (25). Specifically, we believe that mental state (psychological phenomena) can affect the physical (i.e., bodily, somatic) state, and conversely that physical events can alter psychological processes. That is, we support a monistic or holistic perspective. It has been suggested that the term biopsychosocial is more comprehensive and appropriate and less ambiguous than psychosomatic or holistic (26). Concept: On the basis of this holistic view, we have developed a conceptional model of well-being (Figure 1). Much is known about the causes and predisposing factors (precursors) associated with threats to physical well-being. Correspondingly much less is known about factors that affect psychologic well-being. Conceptually, the same mechanisms function in physical and psychologic well-being. Briefly, certain input or stimuli (intrinsic or extrinsic in origin) may cause departures from homeostasis. If such departures from homeostasis are severe and/or prolonged, they may lead to physical or psychological pathologic changes. A departure from physical or psychological homeostasis that has not yet resulted in disease or disorder (but if continued may do so) could be considered a prepathologic state (27). Thus, as a protective mechanism, departures from homeostasis generally elicit responses (e.g., adaptation and coping) designed to return the organism to its normal state of balance or equilibrium. These responses (outputs, symptoms, signs) can be influenced by a number of interacting variables—intrinsic or extrinsic factors that may either enhance, facilitate, attenuate, reduce, or prevent the action of the causative stimuli at the response, precursor, or disorder/disease stage (27, 28). Interacting variables are inherent (phylogenetic) or acquired (ontogenic) factors, such as individual vulnerabilities (e.g., age; sex; physiologic, mental, and health status); genetics; ethology; prior experience and learning; perception (controllability and predictability); motivational state; nature, intensity, duration, timing, frequency, and degree of novelty of stimuli; drugs; and enrichments (28–30). Some examples of internal and external environmental stimuli are provided. Somatic stimuli include cardiovascular collapse, loss of blood, hypoxia, exercise, trauma, malnutrition, dehydration, chemical injury, diseases, anesthesia, and surgery. Psychological stimuli include novelty, change, threats, conflict, and uncertain, uncontrollable, and unpredictable events. External physical and chemical stimuli are factors perceived by the senses, often associated with facilities and environment. These include habitat, temperature, food and water, gases, light, sound, odors, particulate matter, radiation, motion, pressure, and electricity. Psychosocial stimuli include such factors as conspecific relationships, isolation and separation in social species, and enrichments and interactions with people. However, on the basis of the holistic view of well-being, we emphasize that many stimuli are multifactorial and cannot be simply and distinctly categorized. Definition: Most definitions, in general, agree that wellbeing involves the relationship between an animal and its environment. However, arriving at a universally acceptable definition of animal well-being is probably impossible because the way people define quality of nonhuman animal life depends on their personal experiences, views, and values (31). Because different individuals and societies have differing opinions regarding what specifically constitutes animal wellbeing, value arguments are essentially unresolvable (32, 33). It is important that personal and cultural biases of humans be minimized, and that definitions be clear enough to be communicated readily and reliably. Well-being is a complex dynamic internal state that varies on a continuum and in its manifestations. It implies 567 Vol 47, No 6 Laboratory Animal Science December 1997 Figure 1. A schematic representation of well-being. Well-being and factors that affect it are interactive and interrelated. An animal’s well-being is an internal state involving quality of life that is affected by the responses to internal and external stimuli. Stimuli may or may not be aversive. As a protective mechanism, departures from homeostasis generally elicit normal adaptive and coping responses designed to return the animal to its normal state of balance or equilibrium. Ineffective responses may result in prepathology, disorder, dysfunction, disability, disease, or death. Responses can be influenced by a number of interacting variables–intrinsic or extrinsic factors that may either facilitate, attenuate, reduce, or prevent the action of the causative stimuli at the response, precursor, or disability/disease state. successful biological function, positive experiences, and freedom from adverse conditions. It can differ greatly among individuals as well as in the same individual from time to time (11, 19). An individual’s needs, goals, motivations, preferences, and homeostatic circumstances change: at different periods of life as it grows, develops, and matures; on the basis of rhythms (e.g., circadian, seasonal, and light); and according to internal and external environmental stimuli. Some of these changes are orderly or predictable events; others are not rigidly fixed (34). It is unrealistic to expect that animals will (or perhaps even should) be in an optimal state of well-being at all times. Although managing animals to optimize their well-being is a common goal of animal welfare advocates and animal care providers, the ideal artificial environment has not yet been described for any animal (11). On the other hand, the natural environment is not always optimal for animals, either. There are many threats, such as predation, starvation, natural disasters, and disease. 568 Numerous writers have attempted to define animal wellbeing or welfare (12, 35–42). The philosophical and ethical aspects of animal welfare and well-being have been addressed, and numerous definitions of animal welfare have been reviewed (15). According to Tannenbaum (15), these definitions are significantly different. He concludes that to prevent “the foreclosing of valuable ethical and scientific work, welfare investigators should avoid trying to give purportedly complete and exhaustive definitions of welfare.” Animal scientists should not be dismayed, because defining human health and disease also is controversial and not simple (43, 44). Burchfield (45) defines well-being as a state in which an animal is appropriately using and conserving its bodily resources and effectively coping and adapting to internal needs and environmental demands to maintain homeostasis. Homeostasis is a key aspect of well-being and is defined as the coordinated physiologic reactions that maintain the steady state of the body via the complex interaction of a wide range of organs (46). Some definitions of homeostasis also specifi- Special Topic Overview cally include psychological aspects (e.g., homeostasis is described as the steady harmonious state of mind and body) (47). Psychoneuroimmunology The notion that psychologic factors precipitate or cause disease go back to antiquity. However, current thinking has been heavily influenced by the observations of Alexander (48), who related psychological factors to seven specific disease entities. Dunbar (49) proposed that psychological conflicts are not specific, but rather that a definable personality type is the important etiologic factor, and she described disease-related personality profiles. In the 1959 book The Principles of Humane Experimental Technique (10), in which the principles of replacement, reduction, and refinement were first proposed, Russell and Burch addressed the concept of “psychosomatics” and animals. They stated that “the mind-body dichotomy is an entirely pathological fantasy...there can be no doubt that for lower animals, psychosomatics is just as important a relationship as it is for ourselves.” During the last 20 to 25 years, renewed interest in the mindbody relationship has led to the rapid development of PNI as an interdisciplinary field of study that focuses on the relationship between psychological state and physical health. The term “psychoimmunology” was first introduced in 1964, when Solomon and Moos published a report entitled “Emotions, Immunity, and Disease: A Speculative Theoretical Integration” (50). They reviewed evidence suggestive of interactions between psychosocial factors and disease, and speculated about possible mechanisms by which psychosocial factors might influence disease processes. They attempted “... a speculative theoretical integration of the relation of stress, emotion, immunological dysfunction (especially autoimmunity), and physical and mental disease...tentatively for heuristic aims to begin a meaningful synthesis of new basic medical concepts with observations from behavioral science.” Later, Ader and Cohen (51) documented that immune responses can be learned or classically conditioned, and thus provided convincing empirical support for the concept of nervous systemimmune system interactions. Skepticism toward the notion that psychological states may influence physical health subsequently began to diminish as research in the emerging field of PNI rapidly progressed. Recent research in the field of PNI has indicated that the nervous, endocrine, and immune systems influence each other through an elaborate system of chemical messengers that include neurotransmitters, hormones, and cytokines, and that interactions among these three systems may have important implications for various forms of physical and psychological pathologic changes in humans and animals. Although various strategies or paradigms have been used in PNI research, stress studies have proven particularly valuable in discovering how the nervous, endocrine, and immune systems respond to changing environments and influence each other in the intact organisms. Some have suggested that PNI is an outgrowth or extension of stress research (52). Because freedom from physical and psychological pathologic changes is an essential component of animal well-being, advances in the field of PNI are likely to be relevant to the issue of animal well-being. Much information, based on clinical and experimental studies of man and animals, already exists in PNI literature and in related areas, such as biopsychosocial medicine. The importance of life circumstances or change in altering susceptibility to disease in animals has been documented by experimental psychologists and appears in psychology journals (53). Thus, until additional data can be gathered regarding well-being in laboratory animals, it may be advantageous to rely on research conducted in related fields, such as PNI. Research needs The Council on Research of the American Veterinary Medical Association (AVMA) (36) and the Association of American Veterinary Medical Colleges (54) have identified animal wellbeing as one of several research priorities. 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