Download Stress and coping in farm animals

Arch. Tierz., Dummerstorf 43 (2000) Sonderheft, 144-152
Institute of Animal Breeding and Husbandry with Velerinary Clinic, Martin-Luther-University Halle-Wittenberg6
Halle, Germany
'
E B E R H A R D von BORELL
Stress and coping in farm animals
Summary
Stress is a broad term which implies a threat to which the body needs to adjust. Stress may be classified as
physical, psychological, or interoeeptive in nature, but usually contains components of all three classifications
The adjustment to stress induces a broad ränge of neuroendoerine, physiological and behavioural changes to
allow for a rapid recovery or adaptation to the change. The hypothalamic-adrenal medullary system involves the
hypothalamus, p.tuitary gland, the sympathetic neural pathways to the adrenal medulla, and the release of
epinephnne by the adrenal gland. This short acting stress-response was originally proposed by Walter Cannon
and is refeued to as the Fight-Flight Syndrome (FFS). The hypothalamic-pituitary-adrenocortical (HPA) stressresponse system with the release of corticosteroids represents a longer-term, sustained response to Stressors and
was conceptualised by Hans Selye (General Adaptation Syndrome, GAS). These two classical stress response
Systems have been linked to different coping pattem in that FFS is primarily activated in situations of threat of
control, whereas the pituitary-adrenocortical system is activated in situations of loss of control. Several studies
have confirmed that unpredictable or uncontrollable Stimuli will activate the hippocampal pathway and the HPA
axis leading to depression of behaviour. The ability to adjust to some Stressors (controllability), however seems
to be under the control ofthe amygdala through activation ofthe sympathetic nervous system and prepares the
animal for fight and flight responses. In the past, housing Systems and handling procedures for farm animals
were mainly assessed by descriptive behavioural studies using indicators presumed to be related to stress (i.e
Stereotypie behaviours). Physiological indicators included endocrine changes on the pituitary-adrenal-axis by
measuring adrenocorticotropin (ACTH), corticosteroids and catecholamines. The neuroendoerine and immune
system has been studied in relation to stress effects at a cellular or neural level during the last decade. All these
studies were often conducted in an isolated manner without considering that the neuroendoerine and immune
system are communicating with each other and are ultimately influenced by the animals individual pereeption of
a Stressor. Psychological Stressors perceived as threats may be equally important as those ofa physical nature in
challenging coping mechanisms. Situations of uncertainty, social pressure and fear are potent Stressors with
relevance for the welfare of animals, leading to severe damage to specific target organs and tissues or even to
death in some species. Transportation is considered as a major Stressor for farm animals and might have
deletenous effects on the health, welfare, Performance and ultimately on product quality. Studies on the
assessment of stress during animal housing, management procedures and transportation require non-invasive
methods as classical approaches of data collection with direct human interference (i.e., for blood collection and
heart rate measurement) might directly alter the stress response. Telemetrie devices for measuring heart and
respiration rate, body temperature and blood pressure are useful tools to obtain undisturbed responses. Also, noninvasive measurements of stress indicating metabolites in saliva, faeces or urine has been recently developed and
validated. Parallel to behavioural observations, these physiological measurements provide valuable information
on coping strategies and the consequences for the welfare offarm animals.
Key words: stress, coping, behaviour, physiology, farm animal
Zusammenfassung
Titel der Arbeit: Stressbewältigung bei Nutztieren
Stress beschreibt einen Zustand des Organismus, der durch spezifische Anpassungsreaktionen auf
verschiedenartige Belastungsreize (Stressoren) gekennzeichnet ist. Die Empfindung und Verarbeitung von
Stressoren geschieht über eine Kaskade von biologischen Mechanismen mit dem Ziel der Schadensvermeidung
und dem Erreichen eines psychophysiologischen Gleichgewichtszustandes (Prinzip der Homöostase).
Reizinformationen werden zunächst durch das sensorische System aufgenommen und über neurale Signale zu
den kognitiven bzw. nicht-kognitiven Zentren des Zentralen Nervensystems (ZNS) weitergeleitet, über die dann
wohl-koordinierte Anpassungsreaktionen gegenüber Belastungen eingeleitet werden. Das SympathoAdrenomedulläre-System umfasst den Hypothalamus, die Hypophyse und das Sympathische Nervensystem mit
Projektionen zum Nebennierenmark, über welches Adrenalin ausgeschüttet wird. Diese kurzfristige Reaktion auf
Belastungen wurde bereits zum Beginn des vergangenen Jahrhunderts durch Walter Cannon als Kampf- und
Flucht-Syndrom (engl.: Fight and Flight Syndrome, FFS) beschrieben. Die Aktivierung des Hypothalamo-
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Hypophysen-Nebennierenrinden-Systems (engl.: Hypothalamo-Pituitary-Adrenocortical [HPA]-Ax.s) stellt
dagegen eine längerfristige Anpassungsreaktion dar, bei der die Ausschüttung von Glukokortikosteroiden aus der
Nebennierenrinde durch Stimulation des Hypophysenhormons ACTH- (Adrenocorticotropes Hormon) im
Vordergrund steht. Dieses als Allgemeines-Anpassungs-Syndrom (AAS) bezeichnete System wurde durch H
Selve erstmalig beschrieben. Die beiden klassischen Belastungsreaktionen wurden vor etwa 25 Jahren mit
verschiedenen Bewältigungsstrategien in Verbindung gebracht. In bedrohlichen Notstandssituationen
(Bedrohung der Kontrolle) wird überwiegend das FFS aktiviert, während die HPA-Achse in Situationen des
Kontrollverlustes aktiviert wird. Neben diesen klassischen Anpassungsreaktionen sind auch andere Systeme,
einschließlich des Immunsystems, am Stressgeschehen beteiligt. Neuere Erkenntnisse zeigen dass das HormonImmun- und Zentrale Nervensystem gegenüber Stressoren wohlkoordiniert interag.erem Das Vorhandensein von
Hormonen Neuro- bzw. Immunotransmittem und gleichartigen Rezeptoren in allen drei Systemen unterstützt
die Hypothese, dass diese Systeme miteinander kommunizieren. Psychologische Belastungen werden in ähnlicher Weise wie physische Belastungen bewältigt. Konfliktsituationen, sozialer Stress und Angst sind Zustände
mit Relevanz ftlr das Wohlbefinden von Tieren, die längerfristig die Krankheitsanfälhgkeit erhöhen und zu
Leistungseinbußen, Organschädigungen und destruktiven bzw. depressiven Verhaltensweisen führen können.
Studien zu Belastungsreaktionen von Nutztieren basieren häufig auf der Beschreibung einzelner physiologischer
Parameter und Verhaltensänderungen, die in der Regel schwer zu interpretieren sind. Parallel zu
Verhaltensbeobachtungen erlauben neuere nicht invasive Methoden der Erfassung belastungsanzeigender
Metaboliten aus dem Speichel, Kot oder Urin sowie telemetrische Verfahren zur Messung der Herz- und
Respirationsrate,
Körpertemperatur
und des Blutdruckes eine störungsfreie
Beurteilung von
Managementmaßnahmen, Haltungs- und Transportsituationen bei Nutzeren, die Aufschlüsse über die
Bewältigungsmechanismen und deren Konsequenzen für das Wohlbefinden der Tiere geben können.
Schlüsselwörter: Stressbewältigung, Verhalten, Physiologie, Nutztier
History of stress research
Stress is defined as a condition in an animal that results from the action of one or more
Stressors that may be of either external or internal origin. The effort of the body to
maintain a stable internal environment to challenges from widely variable
environments was first described by Claude BERNARD (1878) and later referred to as
homeostasis (CANNON, 1932). The concept and the related definitions of stress were
given by Walter CANNON (1914) and Hans SELYE (1936). They discovered that
diverse detrimental Stimuli (Stressors) like pain, hunger, thirst, severe climatic
conditions or nocuous agents are causing physiological changes in the animal that
might lead to a pathological State in the long run. The non-specific response to
Stressors such as the release of adrenal hormones was defined as a State of stress. Some
ofthe long-term pathological consequences of stress are h y P ^ P ^ ^ * ^ ™ . 8 :
atrophy of the thymo-lymphatic system and stomach ulceration. CANNON (1914)
emphasized the emergency function of the adrenal medulla during stress. The
hypothalamic-adrenal medullary system involves the hypothalamus, pituttary gland,
the sympathetic neural pathways to the adrenal medulla, and the release of epinephnne
by the adrenal gland. This short acting stress-response was referred to as the MgntFlight Syndrome (FFS). The hypothalamic-pituitary-adrenocorttcal (HPA) stressresponse system represents a longer-term, sustained response to stressorsiand was
conceptualised by Hans Selye (General Adaptation Syndrome, GAS; SELYE, 1946).
The major adrenal cortical hormones are corticosteroids and aldosterone. Selye
distinguished three phases of the stress response which are described as (1) alarm
(Cannon's emergency concept), followed by (2) resistance (i.e. by release of
corticosteroids), which if unsuccessful results in (3) exhaustion ofthe response system
(pre-pathological State) and eventually death. The theory of non-speciftcity of Stressors
was later questioned by pychophysiologists like MASON (1971). The acttvatton ofthe
HPA-axis is mainly dependent on the emotional involvement of the animal, as
Stressors do not necessarily activate the HPA System when the animal does not
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perceive the Situation as stressful. Based on this research the new disciplines of
psychoneuroendocrinology and -immunology evolved two decades ago which were
substantially influenced by the work of Robert Ader. Numerous studies indicate that
psychosocml stress can have profound effects on the immune system (DANTZER and
KELLEY 1989, ADER et al., 1990). The term stress is used today in a much broader
sense. As for the defmition of animal welfare (BROOM, 1996a), stress could refer to
the coping ofthe animal with the environment, describing the animal's State when it is
challenged beyond its behavioural and physiological capacity to adapt to its
environment (TERLOUW et al., 1997).
Psychophysiological integration of stress
The response to Stressors requires a progression of events beginning with sensing and
signallmg the animal s various biological mechanisms that a threat exists These
events are followed by activation of neurophysiological mechanisms to mount a
biological effort to resist and prevent major damage. The various sensory detectors not
only receive the Information but transform that information into neural signals that are
ransmitted to either or both cognitive and non-cognitive centres ofthe nervous system
P M ^ e r a t I 3 . C °-° r d J i n a t e d r e s P ° n s e to the challenge. The central nervous system
(CNS), endocrme and immune system interact and respond to stressful Stimuli in a coordinated manner and influence the behaviour of an animal (see Fig. 1) The presence
of hormones, neurotransmitters and receptors common to all three Systems supports
the view that communication exists between these Systems (DE SOUZA, 1993).
Neurobiological Integration of Stress
Stressor
Behaviour.
Endocrine
System
Hormones
Immunotransmitter
Immune
System
Fig_ 1: Communication between CNS, endocrine and immune system (Kommunikation zwischen ZNS
Endokrinum und Immunsystem)
The parasympathetic nervous system maintains homeostasis through the release of
acetylcholine and is mainly responsible for energy conservation and relaxation during
stress. Parasympathetic activities are antagonized by sympathetic activities that
mobihze energy during stress. The secretion of catecholamines (adrenaline,
noradrenahne) from the adrenal medulla is characteristic for the FFS, preparing the
body for an active coping response to the Stressor (i.e., by increasing heart rate and
147
blood pressure). Studies on different individual coping strategies have shown that
proactive animals (removal themselves from the source of stress or removal of the
source itself) seemed to be predominated by the sympathetic nervous system, whereas
the reactive animals (aimed to reduce the emotional impact of stress) seemed to be
predominated by the parasympathetic nervous system (KOOLHAAS et al., 1999). The
ratio between sympathetic and parasympathetic activity determines whether an animal
is in a State of physical or. psychological arousal or relaxation.
Cognitive brain centres such as the cerebral cortex perceive external threats and act to
initiate response mechanisms via nervous signals that activate corticotropin-releasing
hormone (CRH) producing neurons, mainly in the paraventricular nucleus of the
hypothalamus. CRH is released from the median eminence, and transported by the
hypophyseal portal blood system to the anterior pituitary, where it increases the
synthesis and secretion of ACTH, ß-endorphin, ß-Lipotropin and a-MSH / aMelanotropin. CRH not only activates the HPA axis, it also has a neurotransmitter
function in the brain. For example, the intracerebroventricular administration of CRH
activates the sympathetic and adrenomedullary system, resulting in elevations of
plasma catecholamine concentrations and increases in arterial pressure and heart rate.
Increasing glucocorticoid concentrations in the blood may inhibit ACTH secretion
from the pituitary gland. However, the release of ACTH is dependent on the intensity
of the Stressor and modulated by a steady-state sensitive feedback mechanism. Mild
Stressors might therefore be gradually inhibited by a glucucocorticoid feedback,
whereas severe Stressors are not inhibited (AXELROD and REISINE, 1984).
CRH receptors have been identified in several brain regions including areas involved
in cognitive function as well as in limbic areas involved in emotion. This explains why
centrally administered CRH causes emotional responses in animals (JOHNSON et al.,
1994). The limbic system ofthe brain includes structures like the hypothalamus (the
endocrine control centre), thalamic nuclei, amygdala and hippocampus. HENRY and
STEPHENS (1977) hypothesized that the amygdala and hippocampus are involved in
two different coping processes which enable the animal to respond to threatening and
frustrating Stimuli (Coping / Predictability Concept). Several studies have confirmed
that unpredictable or uncontrollable Stimuli will activate the hippocampal pathway and
the HPA axis leading to depression of behaviour. The ability to adjust to some
Stressors (controllability), however, seems to be under the control of the amygdala
through activation ofthe sympathetic nervous system and prepares the animal for fight
and flight responses (see Fig. 2). The activation of one or the other system depends on
many factors such as genetic disposition, early experience and cognitive ability, and on
the Stressor quality and quantity (LADEWIG, 1994). Psychological Stressors perceived
as threats may be equally important as those of a physical nature in challenging coping
mechanisms. Situations of uncertainty, social pressure and fear are potent Stressors
with relevance for the well-being of animals, leading to severe damage to specific
target organs and tissues or even to death in some species.
Correlational evidence supports a direct link between stress and disease susceptibility.
Both physical and psychological Stressors have been demonstrated to suppress T-cell
and B-cell blastogenesis, natural killer cell activity and cytokine production
(interleukin-2 (IL-2) and interferon-g). Cytokines (i.e., IL-1, 11-6, tumor-necrosis
factor (TNF), and interferon (INF)) are considered as mediators of the immunological
and pathological responses to stress and infection. The cytokine IL-1 not only induces
148
fever and reduces food intake, it also stimulates the HPA axis and inhibits the
hypothalamic-pituitary-gonadal axis (DANTZER and KELLEY, 1989). The release of
stress hormones does, however, not only suppress immune competence
Glucocorticoids are known to increase the non-specific resistance towards Stressors
and infections (i.e., by its anti-inflammatory properties). This explains why animals
with an madequate functioning ofthe adrenal glands are more likely to die from stress
than others with intact glands.
Visual, tactile, olfactorial, auditorial
Stimulus
(Stressor)
Coping Pattern
Genetic Disposition
Early Experience
Threat of control
Loss of control
(Fight & Flight)
Amygdala
Behavioural activity
Threat of Status or territory
(Depression)
Hippocampus-Seprn m
Suppression of spatial
behaviour and social Status
Defense
of territory or social Status
Withdrawal Avoidance
reduced activity; Submission;
suppression of sexual &
maternal hehavimir
Activation ofthe sympathicoadreno-meduHarv svstt>rn
Catecholamines
Corticosteroids
Testosterone
^
«_>
+
Activation ofthe pituitaryadrenocortical svstem
Corticosteroids
Catecholamines
Testosterone
+
++
+
Fig. 2: Coping/Predictability Concept (modified after HENRY and STEPHENS, 1977) (Coping/Predictabilitv
Konzept)
'
Adaptation to stress in farm animals
Studies on stress responses in farm animals are often conducted on the basis of single
physiological alterations or irregulär behavioural phenomena that might be difficult to
interpret. In the past, most physiological studies on stress were solely based on the
analysis of glucocorticoids or catecholamines without considering that multiple
physiological Systems are altered during stress (DANTZER and MORMEDE, 1983;
EWING et al., 1999). These measurements of single parameters (i.e. cortisol) are of
little value when not considering the context in which the substance is released and not
knowing what consequences it has for the animal's welfare. (RUSHEN, 1991). A
major problem of applied stress research in livestock relates to the methodology of
stress assessment or to the non-speeificity of the selected parameter. The stress an
animal might experience during blood collection procedure might interfere with the
effect of housing or management procedure under investigation. Vocalization analysis
149
has been proven useful to obtain information on stressful procedures such as the
castration of piglets (HÖRN et al., 1999). Housing environments often do not allow
continuous blood sampling (i.e. in groups of free moving animals) which is usually a
prerequisite for consideration of the natural circadian and episodic release of
hormones. Remote controlled blood sampling devices (CARRAGHER et al, 1997) and
wireless heart rate monitors (HANSEN and VON BORELL, 1998) can help to
overcome some of these problems. Elevated hormone concentrations as well as an
increase in heart rate does not necessarily relate to a stressful Situation with negative
consequences for the well-being of the animal. Physical activities and presumably
pleasurable events such as sexual intercourse are also increasing these parameters.
Recent studies are utilizing a new parameter deriving from calculations of the R-R
heart beat intervals (heart rate variability) with which the relative ratio between
sympathetic and parasympathetic activity can be estimated. The method has been
recently used in pigs for the assessment of social stress in relation to housing
conditions (HANSEN, 2000). Measurements were only taken from resting animals in
order to avoid interfering effects from physical activities.
The impact of housing conditions and management procedures on physiological
parameters depends on the duration and intensity of the factor that acts on the animal.
Short stressful events (i.e. direct handling and transportation) are usually followed by
an increase in stress hormones, whereas chronic events (i.e. long acting heat stress or
restraint) might not effect the basal hormone concentration at all or even lower the
concentration in the blood (down-regulation). Chronic presumably stressful situations
such as permanent tethering of animals might only be visuatized by hormone profiles
that are continuously recorded (LADEWIG and SMIDT, 1989) or by testing the
function of the adrenal cortex via Stimulation with ACTH (VON BORELL and
LADEWIG, 1989, ACTH challenge test). The results from these studies are often
contradictory, presumably reflecting the differences in the quality, intensity and
duration of the impinging Stressor. For example, repeated Stressors of low intensity
such as a confrontation with a novel housing environment will eventually lead to a
decreased response intensity (desensitisation), whereas repeated painful Stimuli are
likely to increase the response (sensitisation). Therefore, animals might adapt to long
acting housing conditions that are presumed to be perceived as stressful (i.e. tether
housing) or might not respond with permanent alterations on the various stress
response Systems (LADEWIG, 2000). Some researchers even believe that chronic
stress might not exist. It could be hypothesized that animals under intensive housing
conditions are only exhibiting chronic-intermittent stress responses oecurring in
situations like standing up or lying down in inadequately designed cubicle or tether
Stalls. In a recent study on the effect of repeated social isolation in pigs, it was
demonstrated that ACTH and cortisol responses gradually diminished with repeated
Stressor exposure, whereas the adrenaline and heart rate responses remained
unchanged (SCHRADER and LADEWIG, 1999).
The response ofthe individual animal to a Stressor also depends on genetic factors and
early experiences. There is a debate among behavioural physiologists whether farm
animals develop distinet coping strategies as demonstrated in laboratory animals.
Recent studies in pigs support that idea (MENDL et al., 1992, RUIS et al., 2000).
The interaction between the CNS, endocrine and immune system has also been studied
in farm animals. Centrally administered CRH to pigs resulted in characteristic dose
150
dependent endocrinological, immunological and behavioural responses (JOHNSON et
al., 1994). More recent studies are concerned with the role of glucocorticoid and
mineralocorticoid receptors in the limbic system of pigs in relation to weaning and
restraint stress (KANITZ et al., 1998, ZANELLA, 1999).
Handling and transportation are considered as major Stressors for farm animals and
might have deleterious effects on the health, well-being, Performance and ultimately
on product quality (as reviewed by GRANDIN, 1997). Most studies on farm animals
were concerned with stress during animal handling and to a lesser degree on
transportation stress per se, although transportation stress is considered as a major
global problem. This has to do with the methodological difficulties to obtain
Information from animals in an environment where space and visibility is very limited.
These studies therefore require non-invasive methods as classical approaches of data
collection with direct human interference (i.e., for blood collection and heart rate
measurement) might directly alter the stress response. Telemetrie devices for
measuring heart and respiration rate, body temperature and blood pressure are useful
tools to obtain undisturbed responses. Recently, non-invasive measurements of stress
indicating metabolites in saliva, faeces or urine have been developed and validated
(BROOM, 1996b; SCHÖNREITER and ZANELLA, 2000). A new saliva collection
device (oral diffusion sink) which stays for a defined period of time (i.e. during
transportation) in the mouth of the animal provides information on stress hormones
that have passed a membrane into a tube from where the average hormone
concentration is analysed. A combination with detaiied behavioural observations (via
video recordings) is required for these physiological stress parameters in order to
facilitate interpretation of results for the specific Situation in which they occur.
Conclusions and imphcations
Recent stress research suggests that the endocrine, immune and central nervous
Systems interact and respond to stressful Stimuli in a co-ordinated manner. The
presence of hormones, neurotransmitters and receptors common to all three Systems
supports the view that communication exists between these Systems. Psychological
Stressors perceived as threats may be equally important as those ofa physical nature in
challenging coping mechanisms. Situations of uncertainty, social pressure and fear are
potent Stressors with relevance for the well-being of animals, leading to severe damage
to specific target organs and tissues or even to death in some species. Studies on stress
responses in farm animals are often conducted on the basis of single physiological
alterations or irregulär behavioural phenomena that might be difficult to interpret.
Non-invasive methods for measuring stress indicating parameters have been developed
in addition to classical descriptive behavioural observations, allowing an evaluation of
stress by multiple criteria under different housing conditions and management
procedures. These behavioural and physiological measurements provide valuable
information on how livestock housing, handling and transportation can be improved in
the near future.
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Author's address
Prof. Dr. EBERHARD von BORELL
Institute of Animal Breeding and Husbandry with Veterinary Clinic
Martin-Luther-University Halle-Wittenberg
Adam-Kuckhoff-Str. 35
D-06108 Halle/S, Germany
E-Mail: [email protected]