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Italian Journal of Animal Science ISSN: (Print) 1828-051X (Online) Journal homepage: http://www.tandfonline.com/loi/tjas20 Animal-based measures for welfare assessment Agostino Sevi To cite this article: Agostino Sevi (2009) Animal-based measures for welfare assessment, Italian Journal of Animal Science, 8:sup2, 904-911 To link to this article: http://dx.doi.org/10.4081/ijas.2009.s2.904 Copyright 2009 Taylor & Francis Group LLC Published online: 07 Mar 2016 Submit your article to this journal Article views: 28 View related articles Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=tjas20 Download by: [80.82.77.83] Date: 02 March 2017, At: 03:35 Animal-based measures for welfare assessment Agostino Sevi Dipartimento di Scienze delle Produzioni e dell’Innovazione nei Sistemi Agro-alimentari Mediterranei (PrIME) Università di Foggia, Italy Corresponding author: Agostino Sevi Dipartimento di Scienze delle Produzioni e dell’Innovazione nei Sistemi Agro-alimentari Mediterranei (PrIME) Facoltà di Agraria, Università degli Studi di Foggia Via Napoli 25, 71100 Foggia, Italy – ����� Tel +39 ���� 0881 ������������ 589216 – ������� Fax: +39 ���� 0881 ��������������������� 589342 – Email: a.sevi@unifg.it ��������������� Abstract - Animal welfare assessment can’t be irrespective of measures taken on animals Indeed, housing parameters ��������������������������������������������������������������������������������� related to structures, design and micro-environment, even if reliable and easier to take, can only identify conditions which could be detrimental to animal welfare, but can’t predict poor welfare in animals per se Welfare assessment through animal-based measures is almost complex, given that animals’ responses to stressful conditions largely depend on the nature, length and intensity of challenges and on physiological status, age, genetic susceptibility and previous experience of animals welfare assessment requires a multi-disciplinary approach and the monitoring of productive, ethological, endocrine, immunological and pathological parameters to be exhaustive and reliable So many measures are needed, because stresses can act only on some of the mentioned parameters or on all of them but at different times and degree Under this point of view, the main aim of research is to find feasible and most responsive indicators of poor animal welfare In last decades, studies focused on the following parameters for animal welfare assessment: indexes of biological efficiency, responses to behavioral tests, cortisol secretion, neutrophil to lymphocyte ratio, lymphocyte proliferation, production of antigen specific IgG and cytokine release, somatic cell count and acute phase proteins Recently, a lot of studies have been addressed to reduce handling and constraint of animals for taking measures to be used in welfare assessment, since such procedures can induce stress in animals and undermined the reliability of measures taken for welfare assessment Range of animal-based measures for welfare assessment is much wider under experimental condition than at on-farm level In welfare monitoring on-farm the main aim is to find feasible measures of proved validity and reliability to be taken on a large number of animals in a reasonable time Human-animal interaction, body condition score, skin and hair conditions, lameness and injuries, cleanliness, and abnormal behaviors are regarded as the most reliable animal-based indicators for welfare assessment on-farm Key words: Behavior, Cortisol, Immunity, Cytokines Introduction - Welfare is strictly related to health and efficiency of production of farmed animals (Sevi, 2007) Indeed, exposure to stress activates a number of defence mechanisms which take off energy from production and, even if necessary to cope with emergency situations, can lead to pathology or increase animal susceptibility to disease, often by initiating immuno-suppression (Sevi et al., 2003b; Broom and Kirkden, 2004) The variety of mechanisms activated to face stress needs a multidisciplinary approach for welfare assessment and the use of productive, behavioral, physiological and pathological indicators Such a wide range of indicators is required because not all response mechanisms to stress are always or simultaneously activated Under experimental conditions animals can be subjected to a lot of testing procedures in order to assess their well-being status Social threat and stress conditions are associated with 904 09_895-912_09_Simposio_II.indd 904 Ital.J.Anim.Sci vol (Suppl 2), 904-911, 2009 22-05-2009 15:06:19 Proc 18th Nat Congr ASPA, Palermo, Italy increased production of pro-inflammatory cytokines and the activation of acute phase response which can give very early prediction of ongoing stress (Kemeny, 2009; Black, 2002) The wider the range of measures taken on the animals the stronger the stress the animals can undergo, because of the procedures used to take measures So several studies have been aimed to determine welfare indicators in biological fluids other than blood, such as cortisol in milk (Verkerk et al., 1998;), salivary cortisol (Fell et al., 1985; Negrão et al., 2004); antigen ������������������������������������������������������� specific IgG����������������������������������� concentrations in milk (Caroprese et al., 2006a; 2006b), milk amyloid A (Winter et al., 2006) Of course, such alternative indicators must be as reliable as conventional ones and closely correlated to them A quite different approach is required for welfare assessment on-farm In this case, in fact, measures must be taken on a large number of animals and in short times by using indicators rapidly collected and often subjectively measured Behavioral indicators play a main role in this case, and so indicators visually collected and for which a close relationship was demonstrated with objective indicators of animal welfare, taken under experimental conditions In this paper main animal-based measures for welfare assessment, under experimental conditions and at on-farm level, will be reviewed Based on the latest experimental findings, the reliability of these parameters as welfare indicators will be discussed, and the impact on performance and health of animals which can be expected when such parameters shift from baseline values Behavioral responses - Animals firstly react to difficult situations by altered behavior Behavioral responses of animals are often correlated with both physiological and immune responses; as a consequence, behavioral indicators of stress can be utilized to predict the effects of stress on the biological functions of the animal (Rushen, 2000) Anyway, the interpretation of behavioral indicators is very difficult because of the complexity of the motivational system underlying behavior A very useful test to measure animals’ responses to stress is the open field test In lambs subjected to isolation in a novel environment withdrawal behaviors have been associated with increased stressful management practices (Napolitano et al., 2003; Sevi et al., 2003a) Another possibility to test the way an animal is trying to cope with a challenge is to ask it in a preference test or in an aversion test In the first case the animal is asked to choose between two or more situations, in the second case the time taken by an animal to approach an aversive situation or a place where an aversive treatment has took place is recorded (Cook et al., 2000) In addition, a deep knowledge of the behavioral repertoire of the animal can allow the recognition of stereotypies A stereotypy is a repeated, invariate sequence of movements without obvious purpose, which often occurs in situation when the animal lacks the control of its environment (Fraser and Broom, 1990) Stereotypies are clear indicators of poor welfare Danzter (1986) suggests that stereotypic behavior is a sign of brain function pathology It has been observed that ruminants show lower stereotypic behavior than other farm animals, probably because they perform rumination to fulfil a function similar to that of stereotypies (Houpt, 1987) Cortisol levels - The activation of the Hypothalamic-Pituitary-Adrenal (HPA) axis is one of the best known and consistent neuroendocrine adaptive response to stress Psychological, environmental and physiological stressors can determine the release by Ital.J.Anim.Sci vol 09_895-912_09_Simposio_II.indd 905 (Suppl 2), 904-911, 2009 905 22-05-2009 15:06:19 Proc 18th Nat Congr ASPA, Palermo, Italy the anterior hypothalamus of the corticotrophin-releasing factor, which stimulates the secretion of adrenocorticotropic hormone (ACTH) by the anterior pituitary gland The target organ of ACTH is the adrenal cortex, and the main action of ACTH is to increase the secretion of glucocorticoids Glucocorticoids play an important role in coping with stressful situation; however, the activation of the neuroendocrine systems can be different according to different type of stressors, as well as within and between different species of animals (Griffin, 1989) Glucocorticoids have a role in many body-regulating functions and their chronic elevation results in protein catabolism, hyperglycaemia, immune suppression, increased susceptibility to disease and depression It is worth noting that corticosteroids can exert different effects on the immune system depending on some variables such as their concentrations, and the host conditions (normal vs pathological conditions) As a consequence, cortisol could enhance immune functions at one concentration and inhibit the same functions at another Cortisol controls also cytokine production and action (Black, 2002) Cytokines and Acute phase protein - An increasing body of literature provides evidence of a crosstalk between the immune and nervous systems, which is involved in the animals’ response to stress The mediators of the interactions between the two biological systems are the cytokines Both physiological and psychological stressors can determine the secretion of pro-inflammatory cytokines, IL-1β, IL-6, and TNF-α (Caroprese et al., 2006a; Black, 2002) Cytokines can increase the productions of neutrophils, affect leukocyte adhesion and capillary permeability, induce fever and acute phase protein synthesis (Gregory, 2004) In addition, pro-inflammatory cytokines act on the brain causing a “sickness behavior”, characterized by increases in sleep and decreases in social, aggressive, explorative behaviors, together with reduced feeding (Kemeny, 2009) Cytokines are the major mediator of the synthesis of acute phase proteins (APPs) in the liver APPs are a group of proteins, as alpha 1-acid glycoprotein, caeruloplasmin, C-reactive protein, serum amyloid-P, haptoglobin and serum amyloid A, whose concentrations increase in blood of animals experiencing challenges as infections and stress Activation of the HPA by stress may be a signal for cytokine production, which enhances the APPs production in the liver, even though the mechanism of APPs synthesis in response to stress has not yet been clearly explained Inside this network the APPs play a key role in fighting disease, repairing tissue damage and restoration of the healthy state of animals (Murata et al., 2004) Immunological measures - The secretion of stress-induced corticosteroids causes leukocytosis until few hours after stimulation, especially neutrophilia and lymphopenia, thus causing the increase of the neutrophils to lymphocyte ratio (Jain, 1993) It has been found that parturition in sows (Damgaard et al., 2009) and emotional stress in calves (Hickey et al., 2003) can increase the neutrophils to lymphocyte ratio Physical, nutritional, psychological stresses can affect cell-mediated immunity by a reduction in lymphocyte proliferation in sheep (Sevi et al., 2003a; Caroprese et al., 2006a) As well, humoral immune responses, measured in terms of antigen specific IgG, can give an indication of relative stressfulness caused by both physical and emotional challenges (Napolitano et al., 2003; Sevi et al., 2003a; Caroprese et al., 2006a and 2009) 906 09_895-912_09_Simposio_II.indd 906 Ital.J.Anim.Sci vol (Suppl 2), 904-911, 2009 22-05-2009 15:06:20 Proc 18th Nat Congr ASPA, Palermo, Italy Concentration and type of leukocytes in milk can give an indication of the activation of mammary gland immune system in response to bacteria attack After penetrating the udder, bacteria interact with many cell types, especially macrophages These cells release chemoattractants that cause a rapid influx of polymorphonuclear neutrophil leukocytes (PMN) (Burvenich et al., 1994) So PMN increase in milk is a reliable indicator of on-going mastitis Evidence exists of a close relationship between poor welfare and increased susceptibility to mastitis Indeed, adequate immune functions are essential for defence against udder infections and mastitis occurs when natural defence mechanisms of the mammary gland can’t counterbalance the numbers and pathogenicity of the bacteria in contact with the udder A number of physiological (parturition, lactation), pathological (lameness, diarreha) and physical stresses (climatic extremes, inadequate housing, wrong management practices) have been recognized as factors predisposing dairy animals to mastitis Reducing animal handling - Animal-based measures of welfare assessment, apart from behavioral observations, are mainly represented by physiological and immunological evaluations in blood However, the assessment of perturbations in the levels of Figure Cortisol levels (ng/mL) in plasma (•) and saliva (n) before and after ACTH administration in calves (A) or machine milkin in cows (B) Values are means and standard errors of the mean (Negrão et al., 2004) Ital.J.Anim.Sci vol 09_895-912_09_Simposio_II.indd 907 (Suppl 2), 904-911, 2009 907 22-05-2009 15:06:20 Proc 18th Nat Congr ASPA, Palermo, Italy endocrine and immune indicators requires capture, handling, manipulations by stockmen and venipuncture of animals These procedures can be stressful for animals and their effects may confound the stressors to be tested Recent studies (Fell et al., 1985; Negrão et al., 2004) demonstrated that it is possible to estimate cortisol concentrations in the plasma of cattle and sheep directly from salivary cortisol concentration (Figure 1) In lactating animals milk collection is a routine procedure which creates minimal disturbance to the animal Milk cortisol in dairy cows can be considered a good indicator of stressors acting up to 2h before collection of milk samples (Verkerk et al., 1998) Indications of the welfare state of sheep also can be achieved by measuring immunological parameters in milk (Figure 2) such as antigen-specific IgG and serum amyloid A (Caroprese et al., 2006a and 2006b; Winter et al., 2006) Antibody titers to KLH (LS means ±SE) detected in blood samples and milk of Comisana ewes at d 21 and before parturition and at d 0, 3, 7, 14 and 35 after parturition (a, b, c: P < 0.05) (Caroprese et al., 2006a) IgG anti-KLH, mg/mL Figure Animal-based criteria in welfare assessment on-farm - Welfare assessment onfarm starts from the choice of proper welfare indicators: they should be simple to apply, easy to interpret Human-animal interaction, health status of the animals, management practices, in relation to cleanliness and animal handling, and abnormal behaviors, are the most used animal-based indicators for welfare assessment on-farm Human-animal interactions play a main role in sustaining the welfare and production of domestic animals (Hemsworth, 2003) Behavioral tests aiming to assess the quality of human-animal relationship are avoidance distance from the stockman in the home pen, avoidance distance at the manger and approach behavior (Waiblinger et al., 2003) Parameters like capture time for milking and animal behavior in the waiting area and in the milk parlour (kicking, defecation and urination during milking), easily detectable in field conditions, represent other reliable indexes to evaluate animal welfare In farmed animals 908 09_895-912_09_Simposio_II.indd 908 Ital.J.Anim.Sci vol (Suppl 2), 904-911, 2009 22-05-2009 15:06:20 Proc 18th Nat Congr ASPA, Palermo, Italy aggressive behaviors are often connected to stressful management procedures (Mellor et al., 2000) In sheep, wool-biting and slat-chewing are regarded as abnormal oral behaviors (Cooper and Jackson, 1996), and their detection can be considered as an indicator of stressful management procedures The health status of the flock can be evaluated by scoring the body condition (BCS), checking skin and hair conditions, and detecting lameness and injuries Apart from sickness, deviations from average body condition scores depend on inadequate feeding management, in terms of excessive or limited energy content of the diet and of unbalance between nutrient intake and requirements of the animal on a given physiological stage In order to sustain health status of the flock the farmer should clean the parts of the accommodation with which animals come into contact Housing boxes and pens should be disinfected every time they have been emptied and before new animals are brought in Dirtiness can predispose animals to injury and lameness (Busato et al., 2000) Similarly, the presence of dirty sides, and hind limbs in animals can be considered a reliable indicator of inadequate management practices and poor care of animals by stockmen Some of the management practices adopted by the shepherds can be stressful for livestock: regrouping and relocations are routinely used to obtain uniform groups of sheep, but can result in transient stress, altered cell-mediated immune responses and increased frequency of aggressive behaviors (Sevi et al., 2001) Conclusions - Animal welfare has to be pursued to sustain health and efficiency of production in farmed livestock Behavioral responses to open field tests, cortisol levels, immunological measures and release of cytokines and acute phase proteins are regarded as the most reliable indicators for welfare assessment Further investigations in the field are needed for: i) reducing animal handling when immunological and endocrine measures for welfare assessment are taken, because capture, manipulations and venipuncture can be stressful for animals and their effects may confound the stressors to be tested; 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The Biology of Animal Stress Cabi Publishing, Wallingford, UK, pp.23-42 Sevi, A., Taibi, L., Albenzio, M., Muscio, A., Dell’Aquila, S., Napolitano, F., 2001 Behavioural, adrenal, immune, and productive responses of lactating ewes to regrouping and relocation J Dairy Sci 79:1457-1465 Sevi, A., Caroprese, M., Annicchiarico, G., Albenzio, M., Taibi, L., Muscio A., 2003a The effect of a gradual separation from the mother on later behavioral, immune and endocrine alterations in artificially reared lambs Appl Anim Behav Sci 83:41-53 Sevi, A., Taibi, L., Albenzio, M., Annicchiarico, G., Marino, R., Caroprese, M., 2003 Influence of ventilation regimen on micro-environment and on ewe welfare and milk yield in summer It J Anim Sci 3:197-212 Sevi, A., 2007 Ewe welfare and ovine milk and cheese 910 09_895-912_09_Simposio_II.indd 910 Ital.J.Anim.Sci vol (Suppl 2), 904-911, 2009 22-05-2009 15:06:21 Proc 18th Nat Congr ASPA, Palermo, Italy quality It J Anim Sci (Suppl 1):521-526 Verkerk, G.A., Phipps, A.M., Carragher, J.F., matthews, L.R., Stelwagen, K., 1998 Characterization of milk cortisol concentrations as a measure of short-term stress responses in lactating dairy cows Anim Welfare 7:77-86 Waiblinger, S., Menke, C., Fölsch, D.W., 2003 Influences on the avoidance and approach behaviour of dairy cows towards humans on 35 farms Appl Anim Behav Sci 84:23-39 Winter, P., Miny, M., Fuchs, K., baumgartner, W., 2006 The potential of measuring serum amyloid A in individual ewe milk and in farm bulk milk for monitoring udder health on sheep dairy farms Res Vet Sci 81:321-326 Ital.J.Anim.Sci vol 09_895-912_09_Simposio_II.indd 911 (Suppl 2), 904-911, 2009 911 22-05-2009 15:06:21 ... could be detrimental to animal welfare, but can’t predict poor welfare in animals per se Welfare assessment through animal- based measures is almost complex, given that animals’ responses to stressful... constraint of animals for taking measures to be used in welfare assessment, since such procedures can induce stress in animals and undermined the reliability of measures taken for welfare assessment. .. and for which a close relationship was demonstrated with objective indicators of animal welfare, taken under experimental conditions In this paper main animal- based measures for welfare assessment,