Assessment of the Welfare of Experimental Cattle and Pigs Using the Animal Welfare Assessment Grid
- The five needs (access to fresh water and a suitable diet that will keep them healthy; adequate shelter and somewhere comfortable to rest; access to veterinary treatment, but also steps taken to prevent pain, injury, or disease; company of other animals of their own kind with enough space and proper facilities so they can behave in a natural way, to be kept in conditions that mean they will not suffer; and to be treated in a way that does not frighten or distress them) .
- The five domains (nutrition, environment, health, behaviour and mental state) .
- Physical: This reflects an animal’s clinical state of health including factors such as body condition, clinical signs of disease and lameness.
- Behavioural/Psychological: This reflects an animal’s psychological condition, and includes factors such as abnormal/stereotypic behaviour, expression of natural behaviours and social structure.
- Environmental: This reflects the animal’s housing, including factors such as lighting, flooring, enclosure complexity and enrichment provision.
- Procedural: This assesses the challenge to the animal arising from experimental events and clinical/husbandry events, and includes factors such as blood sampling, clinical examination, vaccination and sedation .
2. Materials and Methods
2.1. Retrospective Studies Used for Analysis
2.2. Choosing Factors
- Food intake:
- Score 1—eating normally.
- Score 2—Food intake slightly lower than normal for one day or animal reported hungry for 1 day.
- Score 3—Food intake significantly lower than normal for one day or reported hungry for 2–3 days.
- Score 4—Food intake slightly lower than normal for 2 days (<80%) or reported hungry for 4–5 days.
- Score 5—Food intake significantly lower for 2 days (<50%) or reported hungry for 8–9 days.
- Score 6—Food intake slightly lower than normal for 3 days (<80%) or reported hungry for 8–9 days.
- Score 7—Food intake significantly lower than normal for 3 days (lower than 50%) or reported hungry for >9 days.
- Score 8—Not eaten for 1 day
- Score 9—Not eaten for 2 days
- Score 10—Not eaten for 3 days.
- Response to restraint:
- Score 1—Animal completely habituated, and restraint has no effect on animal’s behaviour.
- Score 2—Animals have minimal response to restraint and show no stress. Animals are well habituated.
- Score 3—Animals have moderate response to restraint but show no stress and are well habituated.
- Score 4—Noticeable change in animal’s behaviour in response to restraint. Mild signs of stress/fear.
- Score 5—Distinct change in animal’s behaviour. Moderate signs of stress/fear.
- Score 6—Animal is noticeably stressed/scared +/− mild aggression.
- Score 7—Animal shows elevated signs of stress/fear +/− moderate aggression.
- Score 8—Animal shows elevated signs of stress/fear with significant aggression.
- Score 9—Animal shows severe signs of stress/fear.
- Score 10—Animal extremely scared and/or aggressive in response to restraint, with potential to cause danger to themselves or the keepers.
2.3. Data Collection
2.4. Data Analysis
3.1. Ease of Scoring Factors with the Data Available from a Standard Approach to Monitoring in a Research Setting
3.2. Contingent Events and the Importance of Behaviour Assessment
3.3. Potential Application for Aiding the Decision of the Timing of Euthanasia
4.1. This Paper Demonstrates the Bias Often Seen in Research towards Assessment of Factors Relevant to the Study, as Opposed to Including All Those Relevant to Assessing Welfare
4.2. Clinical Factors Had the Most Significant Impact on Welfare. This Is Expected in Animals Being Used for Infectious Disease Studies, although Importance May Be Skewed by the Data Available
4.3. Housing Can Be Accurately Scored Using the AWAG and May Be Useful in Comparing the Quality of Different Housing Environments
4.4. Social Structure Was Difficult to Score Using the AWAG from the Data Available, and so Was Removed from the Results. It Could Be Argued Social Structure Is Not Essential for Welfare Assessment in Groups That Have Remained Stable for a Prolonged Period of Time
4.5. Further Research Is Needed in the Potential of the AWAG for Aiding the Decision of When Euthanasia May Be Appropriate
4.6. The AWAG Was Successfully Adapted for Experimental Cattle and Pigs
Institutional Review Board Statement
Data Availability Statement
Conflicts of Interest
|Humane End Points for Cattle Infected with Foot and Mouth Disease||Humane End Points for Pigs infected with African Swine Fever|
|Pyrexia—The animal will be euthanised if it has a fever above 40 °C at the beginning of the 4th consecutive day and has not responded to veterinary treatment.|
Lameness—The animal will be euthanised if not weight-bearing due to pain and inflammation from FMDV infection on one or more feet resulting in the affected animal showing reluctance to stand and/or if the lesions on the coronary band start to bleed at the beginning oft he 3rd consecutive day.
Behaviour—The animal will be euthanised if it stays isolated, has a delayed response to stimuli, is slower in movement and lethargic, and/or presents an abnormal posture, e.g., back arched at the beginning of the 2nd consecutive day.
Anorexia—The animal will be euthanised if it is not eating at the beginning of the 3rd consecutive day or sooner if the animal has any swelling of the tongue, face or oral lesions that prevent it from eating or drinking.
The following signs are not typical of an uncomplicated case of FMD but could be seen with secondary infections or if aspiration pneumonia occurs due to the presence of oral lesions
Respiratory System—The animal will be euthanised immediately if it shows respiratory distress or has an arched back with accompanying signs of fluid present on the lungs after chest auscultation. If the animal develops a persistent cough it will be euthanised at the beginning of the 3rd consecutive day.
Digestive System—The animal will be euthanised if it has watery/haemorrhagic diarrhoea at the beginning of the 3rd consecutive day.
Any animal showing 3 or more of the above clinical signs combined on a single day will be euthanised on the same day even if the duration of individual endpoints has not been reached.
|Pyrexia—The animal will be euthanised if it has a fever above 40.5 °C and shows other clinical signs at the beginning of the third consecutive day. If the animal has no other clinical signs, apart from a raised temperature, it will be euthanised at the beginning of the fourth consecutive day of temperature. |
Behaviour—The animal will be euthanised if it has a tendency to stay isolated, shows a delayed response to stimuli (gets up slowly when touched), and/or presents an abnormal posture, e.g., head hung or back arched for two consecutive days.
Anorexia—The animal will be euthanised if it is not eating on a second consecutive day.
Digestive system—The animal will be euthanised if it has haemorrhagic diarrhoea.
Respiratory system—Any pig showing an increase in breathing rate at the beginning of the second day without improvement will be euthanised at the beginning of the second day.
Vomiting—The animal will be euthanised if vomiting is observed on the third day of pyrexia in association with one other of the above clinical signs.
Lameness—Animals showing non-weight bearing lameness will be euthanised 48 h after treatment if it does not show improvement. Animals showing non-weight bearing lameness will be euthanised at the beginning of the 5th consecutive day after treatment if lameness has not improved significantly. If there is a recurrence of the lameness, due to a regulated procedure, within 21 days from initial onset of lameness the animal will be euthanised on the same day. If the animal becomes lame due to a regulated procedure a third time, it will be euthanised on the same day.
Any animal showing three or more of the above clinical signs combined on a single day will be euthanised on the same day even if the duration of individual endpoints has not been reached. If in any individual case it is considered necessary to maintain animals beyond these severity limits the Home Office Inspector will be consulted.
- Wolfensohn, S.; Sharpe, S.; Hall, I.; Lawrence, S.; Kitchen, S.; Dennis, M. Refinement of welfare through development of a quantitative system for assessment of life-time experience. Anim. Welf. 2015, 24, 139–149. [Google Scholar] [CrossRef]
- European Parliament and Council Directive 2010/63/EU of the European Parliament and of the Council of 22 September 2010 on the Protection of Animals Used for Scientific Purposes. 2010. Available online: https://ec.europa.eu/environment/chemicals/lab_animals/legislation_en.htm (accessed on 26 November 2020).
- Van der Harst, J.E.; Spruijt, B.M. Tools to measure and improve animal welfare: Reward-related behaviour. Anim. Welf. 2007, 16, 67–73. [Google Scholar]
- Barugh, I.; Mellor, D.; Neumann, E.; Vink, D. A Tool for On-Farm Welfare Assessment of Pigs in New Zealand. J. Appl. Anim. Welf. Sci. 2009, 12, 145–146. [Google Scholar] [CrossRef]
- Fleming, T.; Stockman, C.; Wickham, S.; Collins, T.; Barnes, A.; Miller, D. Qualitative Behavioural Assessment (QBA) as an Integrated Measure of Welfare. Available online: https://www.researchgate.net/publication/283007956_Qualitative_behavioural_Assessment_QBA_as_an_integrated_measure_of_welfare (accessed on 26 November 2020).
- Yeates, J.W. Is ‘a life worth living’ a concept worth having? Anim. Welf. 2011, 20, 397–406. [Google Scholar]
- Farm Animal Welfare Council Press Statement. Available online: https://webarchive.nationalarchives.gov.uk/20121010012427/http://www.fawc.org.uk/freedoms.htm (accessed on 26 October 2020).
- Mellor, D.J. Affective states and the assessment of laboratory-induced animal welfare impacts. Altex. Proc. 2012, 1, 445–449. [Google Scholar]
- Mellor, D.J. Updating animal welfare thinking: Moving beyond the ‘five freedoms’ towards a ‘life worth living’. Animals 2016, 6, 215. [Google Scholar] [CrossRef] [PubMed]
- Boissy, A.; Manteuffel, G.; Jensen, M.B.; Moe, R.O.; Spruijt, B.; Keeling, L.J.; Winckler, C.; Forkman, B.; Dimitrov, I.; Langbein, J.; et al. Assessment of positive emotions in animals to improve their welfare. Physiol. Behav. 2007, 92, 375–397. [Google Scholar] [CrossRef] [PubMed]
- Boissy, A.; Lee, C. How assessing relationships between emotions and cognition can improve farm animal welfare. Rev. Sci. Tech. l’OIE 2014, 33, 103–110. [Google Scholar] [CrossRef] [PubMed]
- Farm Animal Welfare Council. Farm Animal Welfare in Great Britain: Past, Present and Future. 2009. Available online: https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/319292/Farm_Animal_Welfare_in_Great_Britain_-_Past__Present_and_Future.pdf (accessed on 2 December 2019).
- Yeates, J.W. How good? Ethical criteria for a ‘good life’ for farm animals. J. Agric. Environ. 2017, 30, 23–35. [Google Scholar] [CrossRef][Green Version]
- Honess, P.; Wolfensohn, S. The extended welfare assessment grid: A matrix for the assessment of welfare and cumulative suffering in experimental animals. Altern. Lab. Anim. 2010, 38, 205–212. [Google Scholar] [CrossRef]
- Wolfensohn, S.; Shotton, J.; Bowley, H.; Davies, S.; Thompson, S.; Justice, W.S.M. Assessment of Welfare in Zoo Animals: Towards Optimum Quality of Life. Animals 2018, 8, 110. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Russell, W.M.S.; Burch, R.L. The Principles of Humane Experimental Technique; Universities Federation for Animal Welfare: Wheathampstead, UK, 1992. [Google Scholar]
- FELASA Working Group on Farm Animals. Recommendations of best practices for the health management of ruminants and pigs used for scientific and educational purposes. Lab. Anim. 2020. [Google Scholar] [CrossRef]
- Home Office 2014 Code of Practice for the Housing and Care of Animals Bred, Supplied or Used for Scientific Purposes. Available online: https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/388535/CoPanimalsWeb.pdf (accessed on 26 October 2020).
- Department for Environment, Food and Rural Affairs. Code of Recommendations for the Welfare of Livestock: Cattle. 2003. Available online: https://www.gov.uk/government/publications/code-of-recommendations-for-the-welfare-of-livestock-cattle (accessed on 27 November 2020).
- Department for Environment, Food and Rural Affairs. Code of Recommendations for the Welfare of Pigs. Available online: https://www.gov.uk/government/publications/pigs-on-farm-welfare (accessed on 27 November 2020).
- Godyń, D.; Nowicki, J.; Herbut, P. Effects of Environmental Enrichment on Pig Welfare—A Review. Animals 2019, 9, 383. [Google Scholar] [CrossRef] [PubMed][Green Version]
- World Organisation for Animal Health. African Swine Fever. Available online: https://www.oie.int/en/animal-health-in-the-world/animal-diseases/african-swine-fever/ (accessed on 9 December 2019).
- World Organisation for Animal Health. Foot and Mouth Disease. Available online: https://www.oie.int/en/animal-health-in-the-world/animal-diseases/Foot-and-mouth-disease/ (accessed on 9 December 2019).
- Farm Animal Welfare Committee. Sustainable Agriculture and Farm Animal Welfare. 2016. Available online: https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/593479/Advice_about_sustainable_agriculture_and_farm_animal_welfare_-_final_2016.pdf (accessed on 14 February 2021).
- Grandin, T.; Shivley, C. How farm animals react and perceive stressful situations such as handling, restraint, and transport. Animals 2015, 5, 1233–1251. [Google Scholar] [CrossRef] [PubMed]
- Dupjan, S.; Puppe, B. Abnormal behaviour with a focus on stereotypies—Indicators of suffering and impaired welfare? Berl. Munch. Tierarztl. Wochenschr. 2016, 129, 93–102. [Google Scholar]
- Zulkifli, I. Review of human-animal interactions and their impact on animal productivity and welfare. J. Anim. Sci. Biotechnol. 2013, 4, 25. [Google Scholar] [CrossRef] [PubMed]
- Mota-Rojas, D.; Broom, D.; Orihuela, A.; Velarde, A.; Napolitano, F.; Alonso-Spilsbury, M. Effects of human-animal relationship on animal productivity and welfare. J. Anim. Behav. Biometeorol. 2020, 8, 196–205. [Google Scholar] [CrossRef]
- Bracke, M.; Hopster, H. Assessing the importance of natural behaviour for animal welfare. J. Agric. Environ. 2006, 19, 77–89. [Google Scholar]
- Mandel, R.; Whay, H.; Klement, E.; Nicol, C. Invited review: Environmental enrichment of dairy cows and calves in indoor housing. J. Dairy Sci. 2016, 99, 1695–1715. [Google Scholar] [CrossRef][Green Version]
- Bolt, S.L.; George, A.J. The use of environmental enrichment on farms benefits animal welfare and productivity. Livestock 2019, 24, 183–188. [Google Scholar] [CrossRef]
- Van de Weerd, H.; Ison, S. Providing effective environmental enrichment to pigs: How far have we come? Animals 2019, 9, 254. [Google Scholar] [CrossRef] [PubMed][Green Version]
- The Animals in Science Committee. Review of Harm Benefit Analysis in the Use of Animals Used in Research. Available online: https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/675002/Review_of_harm_benefit_analysis_in_use_of_animals_18Jan18.pdf (accessed on 12 April 2020).
- National Centre for the Replacement Refinement & Reduction of Animals in Research (NC3Rs). Welfare Assessment. Available online: https://www.nc3rs.org.uk/welfare-assessment (accessed on 29 November 2020).
- Berckmans, D. Automatic On-Line Monitoring of Animals by Precision Livestock Farming. Available online: https://lirias.kuleuven.be/1249819?limo=0 (accessed on 14 February 2021).
- National Centre for the Replacement Refinement and Reduction of Animals in Research (NC3Rs). Approaches to Evaluating Environmental Enrichment. Available online: https://nc3rs.org.uk/news/approaches-evaluating-environmental-enrichment (accessed on 29 November 2020).
- Landsberg, G.; Denenberg, S. Social Behaviour of Swine. Available online: https://www.msdvetmanual.com/behavior/normal-social-behavior-and-behavioral-problems-of-domestic-animals/social-behavior-of-swine (accessed on 12 April 2020).
- Landsberg, G.; Denenberg, S. Social Behaviour of Cattle. Available online: https://www.msdvetmanual.com/behavior/normal-social-behavior-and-behavioral-problems-of-domestic-animals/social-behavior-of-cattle (accessed on 12 April 2020).
- Wolfensohn, S. Too Cute to Kill? The Need for Objective Measurements of Quality of Life. Animals 2020, 10, 1054. [Google Scholar] [CrossRef] [PubMed]
- Justice, W.S.M.; O’Brien, M.F.; Szyszka, O.; Shotton, J.; Gilmour, J.E.M.; Riordan, P.; Wolfensohn, S. Adaptation of the animal welfare assessment grid (AWAG) for monitoring animal welfare in zoological collections. Vet. Rec. 2017, 181, 143. [Google Scholar] [CrossRef] [PubMed]
|Body Condition score||Body condition scoring is a key measure of health and welfare state [19,20]. Weight loss is also a clinical sign of Foot and Mouth Disease (FMD) and African Swine Fever (ASF) [22,23].|
|Lameness score||Lameness in any animal is a sign that they are in pain, and a sign of ill-health and discomfort [19,20]. These are negative affective states and so need to be scored when assessing quality of life. Lameness is also a clinical sign of FMD and ASF [22,23]|
|Observable clinical signs (e.g., salivation, lethargy, pyrexia, diarrhoea, nasal discharge, etc.)||Maintenance of good health is the most basic requirement affecting welfare of cattle and pigs [19,20]. These animals are experimental and so are being subjected to infectious diseases. The physical effects of these must be assessed in order to determine the affect these diseases are having on physical health, and therefore welfare.|
|Presence of injury (not as a result of any procedure carried out by the study, e.g., kick injuries from other animals)||Contingent events (those that occur not as a direct result of the scientific study) must be factored into assessing welfare and quality of life . Injuries causing pain and discomfort are classed as negative affective states and so will affect overall quality of life .|
|Impact of study procedures (including blood sampling, vaccine administration with sedation, rectal temperature and foot examination).||These animals are experimental and will be experiencing procedures carried out by the studies involved. Scientific procedures have the potential to cause pain, suffering, distress or harm and as a result the effect of these must be evaluated to assess quality of life .|
|Response to restraint for each of the above procedures.||In order for the above procedures to take place, some form of restraint is usually required. The response to this depends on how each particular animal perceives it, for example ‘one animal may be well habituated to restraint for examination and find restraint a positive experience with food treats, whilst another animal may be highly fearful and actively resist being restrained’. These animals will experience vastly different levels of fear-stress . As a result, response to restraint will have a varying impact on each animal’s lifetime experience, and therefore needs to be assessed.|
|Display of abnormal/stereotypic behaviours||Abnormal behaviour is a ‘potential indicator of pain, suffering and injury’. Stereotypies, in particular, can be observed as a consequence of inadequate environmental conditions and impaired welfare .|
|Response to human activity (e.g., human presence during feeding/cleaning/routine daily inspection)||Human-animal interaction can have a profound impact on the welfare of farm animals. These interactions may be neutral, positive or negative in nature . A good human-animal relationship is fundamental to farm animal welfare , and therefore needs to be included when assessing quality of life.|
|Use of enrichment provided||The benefits of providing enrichment will not be seen if the enrichment provided is not appropriate or is not being used. It is therefore important to assess use of enrichment as opposed to just the presence of enrichment.|
|Display of natural behaviours (species specific, e.g., various modes of locomotion, wallowing, ruminating, etc.)||Natural behaviours are behaviours that animals tend to exhibit under natural conditions, ‘because these behaviours are pleasurable and promote biological functioning’. Animals have a need to exercise certain natural behaviours, such as nest-building in pigs. All needs (not just physiological, such as the need for shelter, food and water) need to be taken into account in order to assess overall welfare .|
|Social structure (e.g., presence or absence of aggression/bullying/submissive behaviour)||Forming new groups can be stressful for farm animals. Regrouping destabilises the social dynamic which increases physical competition . It is fair to assume bullying within the group will cause a negative emotional state in pigs and cattle. As a result, social structure and the relationships within a group should be assessed.|
|Housing (e.g., space provision, lighting, flooring, substrate, etc.)||The more limited the space that cattle and pigs have in a housing system, the less choice the animal has to avoid unfavourable conditions [19,20]. Indoor housing may compromise choice for the animal and restrict its freedom to express normal behaviour, e.g., zero outdoor grazing for cattle, and no access to wallows for swine . This will have a negative impact on their welfare and so needs to be assessed.|
|Enclosure complexity (e.g., planting, water bodies, food, shelter, hiding places, ability to get away from other members of the group)||Accommodation should provide shelter and enough room to move around and interact with other individuals. This should include enough space for a subordinate animal to move away from a dominant one [19,20]. Enclosure complexity can contribute to negative and positive affective states, and so need to be factored into assessment.|
|Enrichment provision (species specific based on the DEFRA code of practice recommendations for each species)||Enrichment is a key aspect of animal welfare and reduces abnormal behaviours commonly seen in production animals .|
The welfare of farmed pigs can be improved by modifying their environment with bedding, substrates or objects so they can perform more of their natural behaviours. Enrichment can also help manage undesirable and damaging behaviours such as tail biting, which if present will reduce quality of life .
Enrichment can also improve biological functioning, help animals cope with stressful surroundings, increase the fulfilment of behavioural needs and therefore promote more positive affective states . Enrichment therefore has a significant impact on quality of life and provision needs to be assessed to ensure it is present and appropriate.
|Group size||Group size in these herd animals affects social behaviour as well as stocking density and can therefore have a direct impact on welfare .|
|Factors That Could Be Scored Accurately from the Available Retrospective Data.||Factors That Could Not Be Scored Accurately without Enhanced Data Collection during the Research Process.|
|Clinical signs (physical)||Natural behaviours (behavioural)|
|Food Intake (physical)||Response to catching event & human interaction (behavioural)|
|General Condition Score (physical)||Social structure (behavioural)|
|Lameness (physical)||Stereotypic behaviour (behavioural)|
|Presence of Injury (physical)||Interaction with enrichment (environmental)|
|Housing (environmental)||The effect of veterinary/husbandry procedures on welfare (procedural)|
|Group size (environmental)||The effect of restraint for regulated procedures on welfare (procedural)|
|Enclosure complexity (environmental)|
|Study procedures (procedural)|
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Ryan, M.; Waters, R.; Wolfensohn, S. Assessment of the Welfare of Experimental Cattle and Pigs Using the Animal Welfare Assessment Grid. Animals 2021, 11, 999. https://doi.org/10.3390/ani11040999
Ryan M, Waters R, Wolfensohn S. Assessment of the Welfare of Experimental Cattle and Pigs Using the Animal Welfare Assessment Grid. Animals. 2021; 11(4):999. https://doi.org/10.3390/ani11040999Chicago/Turabian Style
Ryan, Molly, Ryan Waters, and Sarah Wolfensohn. 2021. "Assessment of the Welfare of Experimental Cattle and Pigs Using the Animal Welfare Assessment Grid" Animals 11, no. 4: 999. https://doi.org/10.3390/ani11040999