Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-08T08:18:18.571Z Has data issue: false hasContentIssue false
  • English
  • Français

Assessment of stress in non-human primates: application of the neutrophil activation test

Published online by Cambridge University Press:  11 January 2023

PE Honess ,
C Marin ,
AP Brown  and
SE Wolfensohn
PE Honess*
Affiliation:
Department of Veterinary Services, University of Oxford, Oxford OX1 3PT, UK
C Marin
Affiliation:
Department of Veterinary Services, University of Oxford, Oxford OX1 3PT, UK Department of Psychobiology, University Complutense Madrid, Madrid, Spain
AP Brown
Affiliation:
Harlan UK Ltd, Blackthorn, Bicester OX6 0TP, UK
SE Wolfensohn
Affiliation:
Department of Veterinary Services, University of Oxford, Oxford OX1 3PT, UK
*
* Contact for correspondence and requests for reprints: [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

A technique measuring leukocyte (neutrophil) activity was used to examine differences between stress levels in a breeding colony of rhesus macaques housed in either a traditional caging system or open-rooms. The leukocyte activation test measured the degree to which blood from the two treatment groups could launch a further neutrophil response (superoxide production) to an in vitro challenge. Animals housed in a traditional caging system produced a significantly lower leukocyte response than animals housed in open-rooms, indicating that there was a higher level of stress associated with caged housing than open-room housing. This was not influenced by whether animals were physically restrained or trained to stand for a sedating injection. No differences were found between treatment groups in leukocyte numbers or composition. This study validates the use of the leukocyte activation test to assess physiological stress levels in non-human primates and demonstrates the animal welfare benefits of open-room housing over traditional laboratory caging systems.

Keywords

animal welfarehousing refinementleukocyte activityMacaca mulattarhesus macaquesstress
Type
Research Article
Information
Animal Welfare , Volume 14 , Issue 4 , November 2005 , pp. 291 - 295
Copyright
© 2005 Universities Federation for Animal Welfare

References

Buchanan-Smith, HM, Prescott, MJ and Cross, NJ 2004 What factors should determine cage sizes for primates in the laboratory? Animal Welfare 13, Suppl: S197-S201Google Scholar
Carlstead, K and Sherpherdson, D 1994 Effects of environmental enrichment on reproduction. Zoo Biology 13: 447–458CrossRefGoogle Scholar
Crockett, C, Shimoji, M and Bowden, D 2000 Behaviour, appetite and urinary cortisol responses by adult female pigtailed macaques to cage size, cage level, room changes, and ketamine sedation. American Journal of Primatology 52: 63–803.0.CO;2-K>CrossRefGoogle ScholarPubMed
Davys, JS 1995 The development of a forage diet for a breeding colony of rhesus monkeys. Animal Technology 46: 63–66Google Scholar
Dhabhar, F, Miller, A, McEwen, B and Spencer, R 1995 Effect of stress on immune cell distribution — dynamics and hormonal mechanisms. Journal of Immunology 154: 5511–5527Google ScholarPubMed
Draper, WA and Bernstein, IS 1963 Stereotyped behaviour and cage size. Perceptual and Motor Skills 16: 231–234CrossRefGoogle Scholar
Ellard, D, Castle, P and Mian, R 2001 The effect of a short-term mental stressor on neutrophil activation. International Journal of Psychophysiology 41: 93–100CrossRefGoogle ScholarPubMed
Goebel, M and Mills, P 2000 Acute psychological stress and exercise and changes in peripheral leukocyte adhesion molecule expression and density. Psychosomatic Medicine 62: 664–670CrossRefGoogle ScholarPubMed
Graham, NMH, Douglas, RM and Ryan, P 1986 Stress and acute respiratory infection. American Journal of Epidemiology 124: 389–401CrossRefGoogle ScholarPubMed
Ha, J, Robinette, R and Davis, A 2000 Survival and reproduction in the first two years following a large-scale primate colony move and social reorganisation. American Journal of Primatology 50: 131–1383.0.CO;2-D>CrossRefGoogle Scholar
Haigh, JC, Stookey, JM, Bowman, P and Waltz, C 1997 A comparison of weaning techniques in farmed wapiti. Animal Welfare 6: 255–264Google Scholar
Halliwell, B and Gutteridge, J 2000 Free Radicals in Biology and Medicine. Oxford University Press: Oxford, UKGoogle Scholar
Home Office 1995 Code of Practice for the Housing and Care of Animals in Designated Breeding and Supplying Establishments. HMSO: London, UKGoogle Scholar
Honess, P and Marin, C 2005 Behavioural and physiological aspects of stress and aggression in nonhuman primates. Neuroscience and Biobehavioural Reviews. Available online 2 August 2005. doi: 10.1016/j.neubiorev.2005.04.003CrossRefGoogle Scholar
Hu, T, Bei, L, Qian, Z and Shen, X 1999 Intracellular free calcium regulates the onset of the respiratory burst of human neutrophils activated by phorbol myristate acetate. Cell Signal 11: 355–360CrossRefGoogle ScholarPubMed
Kang, D, Coe, C and McCarthy, D 1996 Academic examinations significantly impact immune responses, but not lung function, in healthy and well managed asthmatic adolescents. Brain, Behavior and Immunity 10: 164–181CrossRefGoogle Scholar
Koolhaas, JM, Korte, SM, De Boer, SF, Van Der Vegt, BJ, Van Reenen, CG, Hopster, H, De Jong, IC, Ruis, MAW and Blokhuis, HJ 1999 Coping styles in animals: current status in behaviour and stress-physiology. Neuroscience and Biobehavioral Reviews 23: 925–935CrossRefGoogle ScholarPubMed
Line, S, Morgan, K, Markowitz, H and Strong, S 1989a Heart rate and activity of rhesus monkeys in response to routine events. Laboratory Primate Newsletter 28(2): 11–14Google Scholar
Line, S, Morgan, K, Markowitz, H and Strong, S 1989b Influence of cage size on heart rate and behaviour in rhesus monkeys. American Journal of Veterinary Research 50(9): 1523–1526Google ScholarPubMed
Maes, M, Van Der Planken, M, Van Gastel, A, Bruyland, K, Van Hunsel, F, Neels, H, Hendriks, D, Wauters, A, Demedts, P, Janca, A and Scharpe, S 1998 Influence of academic examination stress on haematological measurements in subjectively healthy volunteers. Psychiatry Research 80: 201–212CrossRefGoogle ScholarPubMed
Maule, A and VanderKooi, S 1999 Stress induced immune-endocrine interaction. In: Balm, PHM (ed) Stress Physiology in Animals pp 205–245. Sheffield Academic Press: Sheffield, UKGoogle Scholar
McLaren, G, Macdonald, D, Georgiou, C, Mathews, F, Newman, C and Mian, R 2003 Leukocyte coping capacity: a novel technique for measuring the stress response in vertebrates. Experimental Physiology 88: 541–546CrossRefGoogle ScholarPubMed
Mendoza, S, Capitanio, J and Mason, W 2000 Chronic social stress: studies in non-human primates. In: Moberg, G and Mench, J (eds) The Biology of Animal Stress: Basic Principles and Implications for Animal Welfare pp 23–42. CABI Publishing: Wallingford, UKGoogle Scholar
Mian, R and Marshall, J 1993 Effect of acute systemic hypoxia on vascular permeability and leucocyte adherence in the anaesthetised rat. Cardiovascular Research 27(8): 1531–1537CrossRefGoogle ScholarPubMed
Mian, R, McLaren, G and Macdonald, DW 2005 Of stress mice and men: a radical approach to old problems. In: Oxington KV (ed) Stress and Health: New Research. Nova Science Publications: New York, USA. In press. ISBN: 1-59454-244-9Google Scholar
Mian, R, Shelton-Rayner, G, Harkin, B and Williams, P 2003 Observing a fictitious stressful event: haematological changes, including circulating leucocyte activation. Stress 6(1): 41–47CrossRefGoogle Scholar
Moberg, G 1985 Biological responses to stress. In: Moberg, G (ed) Animal Stress pp 27–49. American Physiological Society: Bethesda, Maryland, USACrossRefGoogle Scholar
Moberg, G 2000 Biological responses to stress: implications for animal welfare. In: Moberg, G and Mench, J (eds) The Biology of Animal Stress: Basic Principles and Implications for Animal Welfare pp 23–42. CABI Publishing: Wallingford, UKCrossRefGoogle Scholar
Montane, K, Marco, I, Lopes-Olvera, J, Manteca, X and Lavin, S 2002 Transport stress in roe deer: effect of a short-acting antipsychotic. Animal Welfare 11: 405–417Google Scholar
Montes, I, McLaren, GW, Macdonald, DW and Mian, R 2004 The effect of transport stress on neutrophils activation in wild badgers (Meles meles). Animal Welfare 13: 355–359Google Scholar
Murata, H 1989 Suppression of lymphocyte blastogenesis by sera from calves transported by road. British Veterinary Journal 145(3): 257–262CrossRefGoogle Scholar
Paulk, H, Dienskeh, H, Dienski, H and Ribbens, G 1977 Abnormal behaviour in relation to cage size in rhesus monkeys. Journal of Abnormal Psychology 86(1): 87–92CrossRefGoogle Scholar
Porges, S 1985 Spontaneous oscillations in heart-rate: potential index of stress. In: Moberg, G (ed) Animal Stress pp 97–111. American Physiological Society: Bethesda, Maryland, USACrossRefGoogle Scholar
Pottinger, TG 1999 The impact of stress on animal reproduction activities. In: Balm, PHM (ed) Stress Physiology in Animals pp 130–177. Sheffield Academic Press: Sheffield, UKGoogle Scholar
Raberg, L, Grahn, M, Hasselquist, D and Svensson, E 1998 On the adaptive significance of stress-induced immunosuppression. Proceedings of the Royal Society of London, Series B, Biological Science 265: 1637–1641CrossRefGoogle ScholarPubMed
Reinhardt, V 1996 Space requirement stipulations for caged non-human primates in the United States: a critical review. Animal Welfare 5: 361–372Google Scholar
Röder, EL and Timmermans, PJA 2002 Housing and care of monkeys and apes in laboratories: adaptations allowing essential species-specific behaviour. Laboratory Animals 36: 221–242CrossRefGoogle ScholarPubMed
Sapolsky, R 1996 Why stress is bad for your brain. Science 273: 749–750CrossRefGoogle ScholarPubMed
Sapolsky, R 2003 Taming stress. Scientific American 289(3): 66–75CrossRefGoogle ScholarPubMed
Sousa, M and Ziegler, T 1998 Diurnal variation on the excretion patterns of fecal steroids in common marmoset (Callithrix jacchus) females. American Journal of Primatology 46: 105–1173.0.CO;2-#>CrossRefGoogle ScholarPubMed
Theorell, T 2003 Biological stress markers and misconceptions about them. Stress and Health 19: 59–60CrossRefGoogle Scholar
Uno, H, Tarara, R, Else, J, Suleman, M and Sapolsky, R 1989 Hippocampal damage associated with prolonged and fatal stress in primates. The Journal of Neuroscience 9(5): 1705–1711CrossRefGoogle ScholarPubMed
Veterinary Surgeons Act 1966 Chapter 36. http://www.rcvs.org.uk/Templates/Internal.asp?NodeID=89679, accessed 4 October 2005Google Scholar
Willard, MD, Tvedten, H and Turnwald, GH 1989 Small Animal Clinical Diagnosis by Laboratory Methods pp 64–66. WB Saunders: Philadelphia, USAGoogle Scholar
Wolfensohn, SE 2004 Social housing of large primates: methodology for refinement of husbandry and management. ATLA 32, Suppl 1: 149–151Google Scholar
Wolfensohn, SE and Honess, PE 2005 Handbook of Primate Husbandry and Welfare. Blackwell Publishing: Oxford, UKCrossRefGoogle Scholar