ALTEX preprint
published March 29, 2019
doi:10.14573/altex.1811061
1
Research Article
Opportunities for Refinement in Neuroscience:
Indicators of Wellness and Post-operative Pain in
Laboratory Macaques
1
Kris A. Descovich
1,2,3
, Susan E. Richmond
1,4
, Matthew C. Leach
5
, Hannah M. Buchanan-Smith
1
, Paul
Flecknell
6
, David A. H. Farningham
7
, Claire Witham
6,7
, M. Carolyn Gates
8
and Sarah-Jane Vick
1
1
Psychology, Faculty of Natural Sciences, University of Stirling, Stirling, United Kingdom;
2
Environmental and Animal Sciences, Unitec
Institute of Technology, Auckland, New Zealand;
3
Centre for Animal Welfare and Ethics, University of Queensland, Gatton, Australia;
4
Humane Slaughter Association. The Old School, Brewhouse Hill, Wheathampsted, United Kingdom;
5
School of Natural and
Environmental Science, Newcastle University, Newcastle upon Tyne, United Kingdom;
6
Comparative Biology Centre, Newcastle
University, Newcastle upon Tyne, United Kingdom;
7
Centre for Macaques, Medical Research Council, Salisbury, United Kingdom;
8
School of Veterinary Science, Massey University, Palmerston North, New Zealand
Abstract
Being able to assess pain in nonhuman primates undergoing biomedical procedures is important for preventing
and alleviating pain, and for developing better guidelines to minimise the impacts of research on welfare in line
with the 3Rs principle of Refinement. Nonhuman primates are routinely used biomedical models however it
remains challenging to recognise negative states, including pain, in these animals. This study aimed to identify
behavioural and facial changes that could be used as pain or general wellness indicators in the rhesus macaque
(Macaca mulatta). Thirty-six macaques scheduled for planned neuroscience procedures were opportunistically
monitored at four times: Pre-Operative (PreOp), Post-Operative (PostOp) once the effects of anaesthesia had
dissipated, Pre-Analgesia (PreAn) on the subsequent morning prior to repeating routine analgesic treatment, and
Post-Analgesia (PostAn) following administration of analgesia. Pain states were expected to be absent in PreOp,
moderate in PreAn, and mild or absent in PostOp and PostAn when analgesia had been administered. Three
potential pain indicators were identified: lip tightening and chewing, which were most likely to occur in PreAn, and
running which was least likely in PreAn. Arboreal behaviour indicated general wellness, while half-closed eyes,
leaning of the head or body shaking indicated the opposite. Despite considerable individual variation, behaviour
and facial expressions could offer important indicators of pain and wellness and should be routinely quantified,
and appropriate interventions applied to prevent or alleviate pain, and promote positive welfare.
1 Introduction
Animals are currently used as bioscience research models and although primate use is a small proportion of total animal
use, they are routinely subjected to procedures or conditions that directly and indirectly affect their welfare (e.g. Capitanio
et al., 1996; Balcombe et al., 2004; Carlsson et al., 2004; Rennie and Buchanan-Smith, 2006a, b, c; Olsson and Westlund,
2007; Wolfensohn and Lloyd, 2013). It is a societal expectation that animals used in bioscience experience good welfare,
which is characterised by an absence of unnecessary suffering (Lund et al., 2012; Leaman et al., 2014). Such
considerations are also important for scientific validity as poor animal welfare may confound experimental results and
affect the translation of scientific findings to human health benefits (Poole, 1997; Würbel, 2001; Tasker, 2012; Everds et
al., 2013; Hall et al., 2015; Sneddon, 2017). To address these issues, animal use is guided in legislation and policy by the
‘3Rs’ principles of Replacement, Reduction and Refinement, which aim to replace sentient animals with non-sentient
alternatives, reduce the number of affected animals, and minimise the impact of experimental procedures and promote
welfare when non-animal alternatives are not available, respectively (Russell et al., 1992; Osborne et al., 2009; Prescott et
al., 2010).
In the 3Rs framework, Refinement is defined as “any approach which avoids or minimises the actual or potential
pain, distress and other adverse effects experienced at any time during the life of the animals involved and which enhances
their well-being” (Buchanan-Smith et al., 2005 pp. 379–380). The relative impact of some experimental protocols is
species-dependent, for example social isolation (Dawkins, 2006a; Rennie and Buchanan-Smith, 2006b, c), however others,
such as the experience of pain, are widely relevant to all sentient species (Bateson, 1991; Carstens and Moberg, 2000;
1
Received November 6, 2018; Accepted January 24, 2019;
Epub March 29, 2019; © The Authors, 2019.
ALTEX 36(X), ###-###. doi:10.14573/altex.1811061
Correspondence: Kris Descovich, PhD;
Centre for Animal Welfare and Ethics,
University of Queensland, Gatton, Australia
(k.descovich1@uq.edu.au)