Hostname: page-component-8448b6f56d-m8qmq Total loading time: 0 Render date: 2024-04-16T13:09:10.745Z Has data issue: false hasContentIssue false
  • English
  • Français

Acute effects of cage cleaning at different frequencies on laboratory rat behaviour and welfare

Published online by Cambridge University Press:  11 January 2023

CC Burn ,
A Peters  and
GJ Mason
CC Burn*
Affiliation:
Department of Zoology, Oxford University, South Parks Road, Oxford OX1 3PS, UK
A Peters
Affiliation:
Department of Biomedical Sciences, University of Oxford, South Parks Road, Oxford OX1 3UD, UK
GJ Mason
Affiliation:
Department of Animal and Poultry Science, University of Guelph, Ontario N1G 2W1, Canada
*
* Contact for correspondence and requests for reprints: charlotte.burn@worcester.oxon.org
Get access Rights & Permissions [Opens in a new window]

Abstract

In rodents, cage cleaning increases cardiovascular and behavioural activity for several hours, which are commonly interpreted as stress responses. In mice, post-cleaning activity also includes aggression, which can cause serious injuries. This study was part of a long-term investigation into the effects of cage cleaning frequency on rat behaviour and welfare. Here we aimed to ascertain whether post-cleaning activity is stress- or aggression-related, thereby leading to recurrent acute reductions in welfare, or simply a result of non-aversive stimulation. Male Wistar (n = 160) and Sprague–Dawley (n = 160) rats, kept in four animal units, had their cages cleaned twice per week, once per week or once per fortnight, and were kept on one of two types of bedding. Behaviours were recorded in detail before and after cage cleaning for 20 weeks, as was the aversion-related Harderian gland secretion, chromodacryorrhoea (‘red tears‘). Cage cleaning caused decreased resting and increased feeding, walking, bedding manipulation and sheltering for at least 30 min after the disturbance. Skirmishing also increased markedly for 15 min after cleaning, but decreased thereafter to below baseline levels. Unlike in mice, all skirmishing was non-injurious and play-like. The frequency of cage cleaning did not affect the magnitude of this skirmishing peak, but rats that had their cages cleaned more frequently settled more quickly after cleaning. Surprisingly, chromodacryorrhoea decreased after cage cleaning; this could mean that rats find soiled cages stressful or alternatively, like many disturbances, cage cleaning might provoke frequent, curtailed bouts of grooming, thereby removing the secretion. Rats also manipulated aspen bedding more than paper bedding. Overall, we found no evidence that cage cleaning caused rats any acute decrease in welfare — a finding consistent with additional data we have obtained on the lack of preference by rats for soiled over clean cages, and a lack of long-term, behavioural and physiological responses to being cleaned frequently or infrequently.

Keywords

aggressionanimal welfarebehaviourhusbandryratsstress
Type
Research Article
Information
Animal Welfare , Volume 15 , Issue 2 , May 2006 , pp. 161 - 171
Copyright
© 2006 Universities Federation for Animal Welfare

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adams, N and Boice, R 1983 A longitudinal study of dominance in an outdoor colony of domestic rats. Journal of Comparative Psychology 97: 24–33CrossRefGoogle Scholar
Barnett, SA, Fox, IA and Hocking, WE 1982 Some social postures of five species of Rattus. Australian Journal of Zoology 30: 581–601CrossRefGoogle Scholar
Bender, R and Lange, S 2001 Adjusting for multiple testing — when and how? Journal of Clinical Epidemiology 54: 343–349Google ScholarPubMed
Borrello, P, D'Amore, E, Di Virgilio, A, Panzini, G, Valeri, M and Lorenzini, RN 1998 The use of AGI as a method to measure microbial contamination in the cage microenvironment. Animal Technology 49: 81–85Google Scholar
Broderson, J, Lindsey, J and Crawford, J 1976 The role of environmental ammonia in respiratory mycoplasmosis of rats. American Journal of Pathology 85: 115–130Google ScholarPubMed
Buelke-Sam, J, Sullivan, PA, Kimmel, CA and Nelson, CJ 1984 Sex and strain differences in the developmental activity profile of the rat tested over clean vs home cage bedding. Developmental Psychobiology 17: 67–77Google ScholarPubMed
Bulla, G 1999 Fancy Rats: A Complete Pet Owner's Manual. Barrons Educational Series Inc: New York, USAGoogle Scholar
Burn, CC Unpublished Effects of Husbandry Manipulations and the Laboratory Environment on Rat Health and Welfare. DPhil Thesis, University of Oxford, Oxford, UKGoogle Scholar
Burn, CC, Day, MJ, Peters, A and Mason, GJ 2006 Long-term effects of cage-cleaning frequency and bedding type on laboratory rat health, welfare and handleability: a cross-laboratory study. Laboratory Animals: in pressGoogle Scholar
Carissimi, AS, Chaguri, LCAA, Teixeira, MA, Mori, CMC, Macchione, M, Sant' Anna, ETG, Saldiva, PHN, Souza, NL and Merusse, JBL 2000 Effects of two ventilation systems and bedding change frequency on cage environmental factors in rats (Rattus norvegicus). Animal Technology 51: 161–170Google Scholar
Clement, JG 1994 Chromodacryorrhea in rats — absence following soman poisoning. Toxicology and Applied Pharmacology 124: 52–58CrossRefGoogle ScholarPubMed
Dagg, AI, Bell, WL and Windsor, DE 1971 Urine marking of cages and visual isolation as possible sources of error in behavioural studies of small mammals. Laboratory Animals 5: 163–167CrossRefGoogle ScholarPubMed
De Villiers, C, Seier, JV and Bok, E 2004 Cage enrichment: the rats decide. Some preliminary observations. 9th FELASA Symposium: Internationalization and Harmonization in Laboratory Animal Care and Use Issues. 14–17 June 2004. Nantes, FranceGoogle Scholar
Doerning, B 1999 Effects of routine animal husbandry and experimental procedures on physiological parameters of rats. Workshop on Refinements in Toxicology Testing. 14 March 1999. Hosted by the Humane Society of the United States: New Orleans, USAGoogle Scholar
Duke, J, Zammit, T and Lawson, D 2001 The effects of routine cage-cleaning on cardiovascular and behavioural parameters in male Sprague–Dawley rats. Contemporary Topics in Laboratory Animal Science 40: 17–20Google Scholar
Foulkes, A 2004 Effects of Enrichment on Chromodaccryrhoea in Rats. MSc Thesis, University of Guelph, Ontario, CanadaGoogle Scholar
Fox, S 1997 The Guide to Owning a Rat. TFH Publications Inc: Neptune City, NJ, USAGoogle Scholar
Gattermann, R and Weinandy, R 1996 Time of day and stress response to different stressors in experimental animals. Part I: Golden hamster (Mesocricetus auratus Waterhouse, 1839). Journal of Experimental Animal Science 38: 66–76Google ScholarPubMed
Gray, S and Hurst, JL 1995 The effect of cage cleaning on aggression within groups of male laboratory mice. Animal Behaviour 49: 821–826CrossRefGoogle Scholar
Harkness, JE and Ridgway, MD 1980 Chromodacryorrhea in laboratory rats (Rattus norvegicus): etiologic considerations. Laboratory Animal Science 30: 841–844Google ScholarPubMed
Hepburn, MJ, Little, PJ, Gingras, J and Kuhn, CM 1997 Differential effects of naltrindole on morphine-induced tolerance and physical dependence in rats. Journal of Pharmacology and Experimental Therapeutics 281: 1350–1356Google ScholarPubMed
Home Office 1995 Code of Practice for the Housing and Care of Animals in Designated Breeding and Supplying Establishments. Animals (Scientific Procedures) Act 1986. HMSO: London, UKGoogle Scholar
Hugo, J, Krijt, J, Vokurka, M and Janousek, V 1987 Secretory response to light in rat Harderian gland: possible photoprotective role of Harderian porphyrin. General Physiology and Biophysics 6: 401–404Google ScholarPubMed
Ishii, T, Yoshida, K, Hasegawa, M, Mizuno, S, Okamoto, M, Tajima, M and Kurosawa, T 1998 Invention of a forced-air-ventilated micro-isolation cage and rack system. Environment within cages: temperature and ammonia concentration. Applied Animal Behaviour Science 59: 115–123CrossRefGoogle Scholar
Kerins, CA, Carlson, DS, McIntosh, JE and Bellinger, LL 2003 Meal pattern changes associated with temporomandibular joint inflammation/pain in rats; analgesic effects. Pharmacology Biochemistry and Behavior 75: 181–189CrossRefGoogle ScholarPubMed
Komorowska, J and Pisula, W 2003 Does changing levels of stress affect the characteristics of grooming behavior in rats? International Journal of Comparative Psychology 16: 237–246CrossRefGoogle Scholar
Lore, R and Flannelly, KJ 1978 Habitat selection and burrow construction by wild Rattus norvegicus in a landfill. Journal of Comparative and Physiological Psychology 92: 888–896CrossRefGoogle Scholar
Manser, CE, Broom, DM, Overend, P and Morris, TH 1998 Investigations into the preferences of laboratory rats for nest-boxes and nesting materials. Laboratory Animals 32: 23–35CrossRefGoogle ScholarPubMed
Mason, G, Wilson, D, Hampton, C and Wurbel, H 2004 Non-invasively assessing disturbance and stress in laboratory rats by scoring chromodacryorrhoea. Alternatives to Laboratory Animals 32: 153–159Google ScholarPubMed
Meany, MJ and Stewart, J 1981 A descriptive study of social development in the rat, Rattus norvegicus. Animal Behaviour 29: 34–45CrossRefGoogle Scholar
Mulder, JB 1975 Bedding preferences of pregnant laboratory-reared mice. Behavior Research Methods and Instrumentation 7: 21–22Google Scholar
Odynets, A, Simonova, O, Kozhuhov, A, Zaitsev, T, Verreva, A, Gnilomedova, L and Rudzish, R 1991 Beddings for laboratory animals: criteria of biological evaluation. Laboratornye Zhyvotnye 1: 70–76Google Scholar
Panksepp, J and Burgdorf, J 2000 50–kHz chirping (laughter?) in response to conditioned and unconditioned tickle-induced reward in rats: effects of social housing and genetic variables. Behavioural Brain Research 115: 25–38Google ScholarPubMed
Patterson Kane, EG 2003 Shelter enrichment for rats. Contemporary Topics in Laboratory Animal Science 42: 46–48Google ScholarPubMed
Pellis, SM and Pellis, VC 1987 Play-fighting differs from serious fighting in both target of attack and tactics of fighting in the laboratory rat Rattus norvegicus. Aggressive Behavior 13: 227–242Google Scholar
Pellis, SM and Pellis, VC 1992 Juvenilized play fighting in subordinate male rats. Aggressive Behavior 18: 449–4573.0.CO;2-T>CrossRefGoogle Scholar
Pellis, SM, Pellis, VC and McKenna, MM 1993 Some subordinates are more equal than others: play fighting amongst adult subordinate male rats. Aggressive Behavior 19: 385–3933.0.CO;2-#>CrossRefGoogle Scholar
Perkins, SE and Lipman, NS 1995 Characterization and quantification of microenvironmental contaminants in isolator cages with a variety of contact beddings. Contemporary Topics in Laboratory Animal Science 34: 93–98Google ScholarPubMed
Ras, T, van de Ven, M, Patterson-Kane, E and Nelson, K 2002 Rats' preferences for corn versus wood-based bedding and nesting materials. Laboratory Animals 36: 420–426CrossRefGoogle ScholarPubMed
Richardson, R and Campbell, BA 1988 Effects of home nest odors on black-white preference in the developing rat: implications for developmental learning research. Behavioral and Neural Biology 50: 361–366CrossRefGoogle ScholarPubMed
Rohde, DS and Basbaum, AI 1998 Activation of coeruleospinal noradrenergic inhibitory controls during withdrawal from morphine in the rat. Journal of Neuroscience 18: 4393–4402CrossRefGoogle ScholarPubMed
Saibaba, P, Sales, GD, Stodulski, G and Hau, J 1996 Behaviour of rats in their home cages: daytime variations and effects of routine husbandry procedures analysed by time sampling techniques. Laboratory Animals 30: 13–21CrossRefGoogle ScholarPubMed
Schnecko, A, Witte, K and Lemmer, B 1998 Effects of routine procedures on cardiovascular parameters of Sprague–Dawley rats in periods of activity and rest. Journal of Experimental Animal Science 38: 181–190Google Scholar
Schultz, D 1972 The effects of novelty on laboratory rat digging behavior. Psychonomic Science 29: 303–304CrossRefGoogle Scholar
Sharp, J, Zammit, T and Lawson, D 2002a Stress-like responses to common procedures in rats: effect of the estrous cycle. Contemporary Topics in Laboratory Animal Science 41: 15–22Google ScholarPubMed
Sharp, JL, Zammit, TG, Azar, TA and Lawson, DM 2002b Stress-like responses to common procedures in male rats housed alone or with other rats. Contemporary Topics in Laboratory Animal Science 41: 8–14Google ScholarPubMed
Sharp, J, Zammit, T, Azar, T and Lawson, D 2003 Are ‘bystander’ female Sprague–Dawley rats affected by experimental procedures? Contemporary Topics in Laboratory Animal Science 42: 19–27Google ScholarPubMed
Sherwin, CM 1996 Preferences of laboratory mice for characteristics of soiling sites. Animal Welfare 5: 283–288CrossRefGoogle Scholar
Singh, A, Einstein, R and Lavidis, N 2001 Effects of restraint stress on responsiveness of atria and vas deferens in Sprague–Dawley rats. Journal of Autonomic Pharmacology 21: 255–261Google ScholarPubMed
Smith, LK, Fantella, SLN and Pellis, SM 1999 Playful defensive responses in adult male rats depend on the status of the unfamiliar opponent. Aggressive Behavior 25: 141–152Google Scholar
Takahashi, LK and Lore, RK 1983 Play fighting and the development of agonistic behavior in male and female rats. Aggressive Behavior 9: 217–227Google Scholar
Toates, F 1995 Stress: Conceptual and Biological Aspects. Wiley: Chichester, UKGoogle Scholar
Townsend, P 1997 Use of in-cage shelters by laboratory rats. Animal Welfare 6: 95–103Google Scholar
Van Loo, PLP, Kruitwagen, CLJJ, Van Zutphen, LFM, Koolhaas, JM and Baumans, V 2000 Modulation of aggression in male mice: influence of cage cleaning regime and scent marks. Animal Welfare 9: 281–295CrossRefGoogle Scholar
Van Loo, PLP, Van der Meer, E, Kruitwagen, CLJJ, Koolhaas, JM, Van Zutphen, LFM and Baumans, V 2003 Strain-specific aggressive behavior of male mice submitted to different husbandry procedures. Aggressive Behavior 29: 69–80CrossRefGoogle Scholar
Weinandy, R and Gattermann, R 1997 Time of day and stress response to different stressors in experimental animals. Part II: Mongolian gerbil (Meriones unguiculatus, Milne Edwards, 1867). Journal of Experimental Animal Science 38: 109–122Google Scholar