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The influences of standard laboratory cages on rodents and the validity of research data

Published online by Cambridge University Press:  11 January 2023

CM Sherwin*
Affiliation:
Centre for Behavioural Biology, Department of Clinical Veterinary Science, University of Bristol, Langford House, Bristol B540 5DU, UK
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Abstract

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Standard cages for laboratory animals are often small, minimalist and barren. Such cages can compromise animal welfare, indicating that there are welfare-based reasons for improving their designs. However, a second issue, that is, whether animals from standard laboratory housing and husbandry conditions provide valid research data, also indicates that cage designs and husbandry methods need to be improved. This paper reviews various influences of standard laboratory cage design and husbandry. These include their effects on the repeatability of studies, models of neuro-degenerative disease, sensory development, physiology, and behaviour, the effects of standard social housing and standard handling, and the effects of maternal experience on the responses of offspring. These studies show that the development and responses of animals from standard laboratory housing and husbandry conditions are often unrepresentative and idiosyncratic, indicating that data are likely to have reduced external validity. An underlying question is whether animals from standard, barren laboratory cages are ‘abnormal’ and therefore might not provide valid baseline data. In terms of animal welfare, these studies indicate that standard laboratory housing may sometimes be associated both with reduced welfare and with reduced benefits gained from research. It is suggested that in a similar manner to the use of production measures when assessing cages for production animals, laboratory cages could be assessed in terms of their suitability to provide valid research data.

Type
Research Article
Copyright
© 2004 Universities Federation for Animal Welfare

References

Arnold, C E and Estep, D Q 1990 Effects of housing on social preference and behaviour in male golden hamsters (Mesocricetus auratus). Applied Animal Behaviour Science 27: 253261CrossRefGoogle Scholar
Callard, M D, Bursten, S N and Price, E O 2000 Repetitive backflipping behaviour in captive Roof rats (Rattus rattus) and the effects of cage enrichment. Animal Welfare 9: 139152Google Scholar
Carducci, J P and Jakob, E M 2000 Rearing environment affects behaviour of jumping spiders. Animal Behaviour 59: 3946CrossRefGoogle ScholarPubMed
Chamove, A S 1989 Cage design reduces emotionality in mice. Laboratory Animals 23: 215219CrossRefGoogle ScholarPubMed
Chapillon, P, Patin, V, Roy, V, Vincent, A and Caston, J 2002 Effects of pre- and postnatal stimulation on developmental, emotional, and cognitive aspects in rodents: a review. Developmental Psychobiology 41: 373387CrossRefGoogle ScholarPubMed
Chesler, E J, Wilson, S G, Lariviere, W R, Rodriguez-Zas, S L and Mogil, J S 2002 Influences of laboratory environment on behavior. Nature Neuroscience 5: 11011102CrossRefGoogle ScholarPubMed
Cook, M N, Williams, R W and Flaherty, L 2001 Anxiety-related behaviours in the elevated zero maze are affected by genetic factors and retinal degeneration. Behavioral Neuroscience 115: 468476CrossRefGoogle ScholarPubMed
Crabbe, J C and Wahlsten, D 2003 Of mice and their environments. Science 299: 13131314CrossRefGoogle ScholarPubMed
Crabbe, J C, Wahlsten, D and Dudek, B C 1999 Genetics of mouse behavior: interactions with laboratory environment. Science 284: 16701671CrossRefGoogle ScholarPubMed
Denenberg, V H and Whimbey, A E 1963 Behavior of adult rats is modified by the experiences their mothers had as infants. Science 142: 11921193CrossRefGoogle ScholarPubMed
Fernandez-Teruel, A, Gimenez-Llort, L, Ascorihuela, R M, Gil, L, Aguilar, R, Steimer, T and Tobena, A 2002 Early-life handling stimulation and environmental enrichment. Are some of their effects mediated by similar neural mechanisms? Pharmacology, Biochemistry and Behavior 73: 233245CrossRefGoogle ScholarPubMed
Fleming, A S, Kraemer, G W, Gonzalez, A, Lovic, V, Rees, S and Melo, A 2002 Mothering begets mothering: the transmission of behavior and its neurobiology across generations. Pharmacology, Biochemistry and Behavior 73: 6175CrossRefGoogle Scholar
Garner, J P and Mason, G J 2002 Evidence for a relationship between cage stereotypies and behavioural disinhibition in laboratory rodents. Behavioural Brain Research 136: 8392CrossRefGoogle ScholarPubMed
Gartner, K 1990 A third component causing random variability beside environment and genotype. A reason for the limited success of a 30 year long effort to standardize laboratory animals? Laboratory Animals 24: 7177CrossRefGoogle ScholarPubMed
Hockly, E, Cordery, P M, Woodman, B, Mahal, A, van Dellen, A, Blakemore, C, Lewis, C M, Hannan, A J and Bates, G P 2002 Environmental enrichment slows disease progression in R6/2 Huntington's disease mice. Annals of Neurology 51: 235242CrossRefGoogle ScholarPubMed
Kessler, M R and Turner, D C 1999 Effects of density and cage size on stress in domestic cats (Felis silvestris catus) housed in animal shelters and boarding catteries. Animal Welfare 8: 259267Google Scholar
Kohl, Z, Kuhn, H G, Cooper-Kuhn, C M, Winkler, J, Aigner, L and Kempermann, G 2002 Preweaning enrichment has no lasting effects on adult hippocampal neurogenesis in four-month- old mice. Genes, Brain and Behavior 1: 4654CrossRefGoogle ScholarPubMed
Korz, V and Gattermann, R 1999 Housing conditions affect susceptibility to mercury in the golden hamster. Laboratory Animals 33: 228233CrossRefGoogle ScholarPubMed
Krohn, T C, Hansen, A K and Dragsted, N 2003 Telemetry as a method of measuring the impact of housing conditions on rats’ welfare. Animal Welfare 12: 5362Google Scholar
Kuhnen, G 1999 The effect of cage size and enrichment on core temperature and febrile response of the golden hamster. Laboratory Animals 33: 221227CrossRefGoogle ScholarPubMed
Larsson, F, Winblad, B and Mohammed, A H 2002 Psychological stress and environmental adaptation in enriched vs impoverished housed rats. Pharmacology, Biochemistry and Behavior 73: 193207CrossRefGoogle ScholarPubMed
Martinez-Cue, C, Baamonde, C, Lumbreras, M, Paz, J, Davisson, M T, Schmidt, C, Dierssen, M and Florez, J 2002 Differential effects of environmental enrichment on behaviour and learning of male and female Ts65Dn mice, a model for Down syndrome. Behavioural Brain Research 134: 185200CrossRefGoogle Scholar
Mason, G J, Cooper, J and Clarebrough, C 2001 Frustrations of fur-farmed mink. Nature 410: 3536CrossRefGoogle ScholarPubMed
Mering, S, Kaliste-Korhonen, E and Nevalainen, T 2001 Estimates of appropriate number of rats: interaction with housing environment. Laboratory Animals 35: 8090CrossRefGoogle ScholarPubMed
Morgan, M J 1973 Effects of post-weaning environment on learning in the rat. Animal Behaviour 21: 429442CrossRefGoogle Scholar
Nagy, T R, Krzywanski, D, Li, J, Meleth, S and Desmond, R 2002 Effect of group vs single housing on phenotypic variance in C57BL/6J mice. Obesity Research 10: 412415CrossRefGoogle ScholarPubMed
Nerem, R M, Levesque, M J and Cornhill, J F 1980 Social environment as a factor in diet-induced artherosclerosis. Science 208: 14751476CrossRefGoogle Scholar
Olsson, I A S and Dahlborn, K 2002 Improving housing conditions for laboratory mice: a review of ‘environmental enrichment’. Laboratory Animals 36: 243270CrossRefGoogle ScholarPubMed
Olsson, I A S, Nevison, C M, Patterson-Kane, E, Sherwin, C M, van de Weerd, H A and Würbel, H 2003 Understanding behaviour: the relevance of ethological approaches in laboratory animal science. Applied Animal Behaviour Science 81: 245264CrossRefGoogle Scholar
Passineau, M J, Green, E J and Dietrich, W D 2001 Therapeutic effects of environmental enrichment on cognitive function and tissue integrity following severe traumatic brain injury in rats. Experimental Neurology 168: 373384CrossRefGoogle ScholarPubMed
Perez, C, Canal, J R, Dominguez, E, Campillo, J E, Guillen, M and Torres, M D 1997 Individual housing influences certain biochemical parameters in the rat. Laboratory Animals 31: 357361CrossRefGoogle ScholarPubMed
Poole, T 1997 Happy animals make good science. Laboratory Animals 31: 116124CrossRefGoogle ScholarPubMed
Poon, A M S, Wu, B M, Poon, P W F, Cheung, E P W, Chan, F H Y and Lam, F K 1997 Effect of cage size on ultradian locomotor rhythms of laboratory mice. Physiology and Behavior 62: 12531258CrossRefGoogle ScholarPubMed
Powell, S B, Newman, H A, McDonald, T A, Bugenhagen, P and Lewis, M H 2000 Development of spontaneous stereotyped behavior in deer mice: effects of early and late exposure to a more complex environment. Developmental Psychobiology 37: 1001083.0.CO;2-6>CrossRefGoogle ScholarPubMed
Powell, S B, Newman, H A, Pendergast, J F and Lewis, M H 1999 A rodent model of spontaneous stereotypy: initial characterization of developmental, environmental, and neurobiological factors. Physiology and Behavior 66: 355363CrossRefGoogle ScholarPubMed
Prior, H and Sachser, N 1995 Effects of enriched housing environment on the behaviour of young male and female mice in four exploratory tasks. Journal of Experimental Animal Science 37: 5768Google Scholar
Prusky, G T, Reidel, C and Douglas, R M 2000 Environmental enrichment from birth enhances visual acuity but not place learning in mice. Behavioural Brain Research 114: 1115CrossRefGoogle Scholar
Puurunen, K and Sivenius, J 2002 !nfluence of enriched environment on spatial learning following cerebral insult. Reviews in the Neurosciences 13: 347364CrossRefGoogle Scholar
Roy, V, Belzung, C, Delarue, C and Chapillon, P 2001 Environmental enrichment in BALB/c mice. Effects in classical tests of anxiety and exposure to a predatory odor. Physiology and Behavior 74: 313320CrossRefGoogle ScholarPubMed
Saito, T R, Moyumura, N, Taniguchi, K, Hokao, R, Arkin, A, Takahashi, K W and Sato, N L 1996 Effect of cage size on sexual behaviour pattern in male rats. Contemporary Topics in Laboratory Animal Science 35: 8082Google ScholarPubMed
Schapiro, S J 2002 Effects of social manipulations and environmental enrichment on behavior and cell-mediated immune responses in rhesus macaques. Pharmacology, Biochemistry and Behavior 73: 271278CrossRefGoogle ScholarPubMed
Schrijver, N C A, Bahr, N I, Weiss, I C and Würbel, H 2002 Dissociable effects of isolation rearing and environmental enrichment on exploration, spatial learning and HPA activity in adult rats. Pharmacology, Biochemistry and Behavior 73: 209224CrossRefGoogle ScholarPubMed
Sherwin, C M 2002 Comfortable quarters for mice. In: Reinhardt, V and Reinhardt, K (eds) Comfortable Quarters for Laboratory Animals pp 617. Animal Welfare Institute: Washington, USAGoogle Scholar
Sherwin, C M and Glenn, E Cage colour preferences and effects of home-cage colour on anxiety in laboratory mice. Animal Behaviour (in press).Google Scholar
Sherwin, C M and Olsson, I A S 2004 Housing conditions affect self-administration of anxiolytic by laboratory mice. Animal Welfare 13: 3338Google Scholar
Skolnick, N J, Ackerman, S H, Hofer, M A and Weiner, H 1980 Vertical transmission of acquired ulcer susceptibility in the rat. Science 208: 16611663CrossRefGoogle ScholarPubMed
Spani, D, Arras, M, Konig, B and Rulicke, T 2003 Higher heart rate of laboratory mice housed individually vs in pairs. Laboratory Animals 37: 5462CrossRefGoogle ScholarPubMed
Steyermark, A C and Mueller, P J 2002 Cage size affects feeding and energetics of captive rodents. Physiological and Biochemical Zoology 75: 209213CrossRefGoogle ScholarPubMed
Syme, L A and Hughes, R N 1972 Social isolation in young rats: effects of cage size on open-field behavior. Psychonomic Science 29: 2526CrossRefGoogle Scholar
Tsai, P P, Pachowsky, U, Stelzer, H D and Hackbarth, H 2002 Impact of environmental enrichment in mice. I: Effect of housing conditions on body weight, organ weights and haematology in different strains. Laboratory Animals 36: 411419CrossRefGoogle ScholarPubMed
van Dellen, A, Blakemore, C, Deacon, R, York, D and Hannan, A J 2000 Delaying the onset of Huntington's in mice. Nature 404: 721722CrossRefGoogle ScholarPubMed
Van Loo, P L P, Kruitwagen, C L J J, Koolhaas, J M, Van de Weerd, H A, Van Zutphen, L F M and Baumans, V 2002 Influence of cage enrichment on aggressive behaviour and physiological parameters in male mice. Applied Animal Behaviour Science 76: 6581CrossRefGoogle Scholar
van Praag, H, Kempermann, G and Gage, F H 2000 Neural consequences of environmental enrichment. Nature Reviews Neuroscience 1: 191198CrossRefGoogle ScholarPubMed
Wagner, A K, Kline, A E, Sokoloski, J, Zafonte, R D, Capulong, E and Dixon, C E 2002 Intervention with environmental enrichment after experimental brain trauma enhances cognitive recovery in male but not female rats. Neuroscience Letters 334: 165168CrossRefGoogle Scholar
Wahlsten, D 2001 Standardizing tests of mouse behavior: reasons, recommendations, and reality. Physiology and Behavior 73: 695704CrossRefGoogle Scholar
Wahlsten, D, Metten, P, Phillips, T J, Boehm, S L, Burkhart-Kasch, S, Dorow, J, Doerksen, S, Downing, C, Fogarty, J, Rodd-Henricks, K, Hen, R, McKinnon, C S, Merrill, C M, Nolte, C, Schalomon, M, Schlumbohm, J P, Sibert, J R, Wenger, C D, Dudek, B C and Crabbe, J C 2003 Different data from different labs: lessons from studies of gene-environment interaction. Journal of Neurobiology 54: 283311CrossRefGoogle ScholarPubMed
Ward, H E, Johnson, E A, Salm, A and Birkle, D L 2000 Effects of prenatal stress on defensive withdrawal behavior and corticotropin releasing factor systems in rat brain. Physiology and Behavior 70: 359366CrossRefGoogle ScholarPubMed
Würbel, H 2001 Ideal homes? Housing effects on rodent brain and behaviour. Trends in Neurosciences 24: 207211CrossRefGoogle ScholarPubMed
Würbel, H 2002 Behavioral phenotyping enhanced — beyond (environmental) standardization. Genes, Brain and Behavior 1: 38CrossRefGoogle ScholarPubMed
Würbel, H, Chapman, R and Rutland, C 1998 Effect of feed and environmental enrichment on development of stereotypic wire-gnawing in laboratory mice. Applied Animal Behaviour Science 60: 6981CrossRefGoogle Scholar