Balancing animal research with animal well-being: Establishment of goals and harmonization of approaches

ILAR Journal

Volumn 46, Issue 2, 2005, Pages 118-128

  Weed, James L ^a   Raber, James M ^b  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b NATIONAL EYE INSTITUTE   (United States)

Author keywords

Animal research; Environmental enrichment; Experimental design; Harmonization; Research methods; Welfare; Well being

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL HOUSING; ANIMAL TESTING REDUCTION; ANIMAL USE; ANIMAL WELLBEING; ARTICLE; ENVIRONMENTAL ENRICHMENT; EXPERIMENTAL ANIMAL; INFORMATION PROCESSING; NONHUMAN; REPRODUCIBILITY; RESEARCH; SCIENCE; TEAMWORK; VALIDATION PROCESS; ANIMAL; ANIMAL EXPERIMENT; ANIMAL WELFARE; BIOMEDICAL AND BEHAVIORAL RESEARCH; CONSTRUCTION WORK AND ARCHITECTURAL PHENOMENA; METHODOLOGY; PATIENT CARE; PERSONNEL; REVIEW; SOCIAL ENVIRONMENT; STANDARD;

ANIMALIA;

BIOMEDICAL AND BEHAVIORAL RESEARCH;

ANIMAL EXPERIMENTATION; ANIMAL WELFARE; ANIMALS; ANIMALS, LABORATORY; FACILITY DESIGN AND CONSTRUCTION; HOUSING, ANIMAL; PATIENT CARE TEAM; REPRODUCIBILITY OF RESULTS; RESEARCH DESIGN; RESEARCH PERSONNEL; SOCIAL ENVIRONMENT;

EID: 17144389357     PISSN: 10842020     EISSN: None     Source Type: Journal    
DOI: 10.1093/ilar.46.2.118     Document Type: Article

References (88)

1. AWA [Animal Welfare Act]. 2002. Public Law (PL) 89-544, 1966, as amended (PL 91-579, PL 94-279, and PL 99-198). 7 USC 2131-2159, as amended (PL 107-171, May 2002).
2. AWR [Animal Welfare Regulations]. 2002. 9 CFR: 54 FR 36119, Aug. 31, 1989, as amended at 55 FR 12631, Apr. 5, 1990; 58 FR 39129, July 22, 1993; 62 FR 43275, Aug. 13, 1997; 63 FR 47148, Sept. 4, 1998; 63 FR 62926, Nov. 10, 1998; 65 FR 6314, Feb. 9, 2000, revised January 2002).
3. Bayne KAL, Beaver BV, Mench JA, Morton DB. 2002. Laboratory animal behavior. In: Fox JG, Anderson LC, Loew FM, Quimby FW, eds. Laboratory Animal Medicine. 2nd ed. San Diego: Academic Press. p 1229-1264.
4. Bayne KAL, Hurst JK, Dexter SL. 1992. Evaluation of the preference to and behavioral effects of an enriched environment on male rhesus monkeys. Lab Anim Sci 42:38-45.
5. Bazille PG, Walden SD, Koniar BL, Gunther R. 2001. Commercial cotton nesting material as a predisposing factor for conjunctivitis in athymic nude mice. Lab Anim 30:40-42.
6. Beach FA. 1955. The descent of instinct. Psych Rev 62:401-410.
7. Beaver BV. 1989. Environmental enrichment for laboratory animals. ILAR J 31:5-11.
8. Benaroya-Milshtein N, Hollander N, Apter A, Kukulansky T, Raz N, Wilf A, Yaniv I, Pick CG. 2004. Environmental enrichment in mice decreases anxiety, attenuates stress responses and enhances natural killer cell activity. Eur J Neurosci 20:1341-1347.
9. Benefiel AC, Greenough WT. 1998. Effect of experience and environment on the developing and mature brain: Implications for laboratory animal housing. ILAR J 39:5-11.
10. Beveridge WIB. 1957. The Art of Scientific Investigation. 3rd ed. New York: WW Norton.
11. BHAG [Behavior and Husbandry Advisory Group]. 1999. A scientific advisory group of the American Zoo and Aquarium Association Workshop at Disney's Animal Kingdom. Orlando FL.
12. Bohus B, Koolhass JM. 1991. Psychoimmunology of social factors in rodents and other subprimate vertebrates. In: Ader R, Felten DL, Cohen N, eds. Psychoneuroimmunology. New York: Academic Press. p 807-830.
13. Broom DM, Johnson KG. 1993. Stress and Animal Welfare. Dordrecht: Kluwer Academic Publishers.
14. Capitanio JP. 1998. Social experience and immune system measures in laboratory-housed macaques: Implications for management and research. ILAR J 39:12-20.
15. Capitanio JP, Lerche NW. 1998. Social separation, housing relocation, and survival in simian AIDS: A retrospective analysis. Psychosom Med 60:235-244.
16. Chamove AS. 1989. Environmental enrichment: A review. Anim Technol 40:155-178.
17. Chamove AS, Anderson JR, Morgan-Jones SC, Jones SP. 1982. Deep woodchip litter: Hygiene, feeding, and behavioral enrichment in eight primate species. Int J Study Anim Probl 3:308-318.
18. Clark JD. 1998. Introduction. ILAR J 39:3-4.
19. Clark JD, Rager DR, Calpin JP. 1997a. Animal well-being. I. General considerations. Lab Anim Sci 47:564-570.
20. Clark JD, Rager DR, Calpin JP. 1997b. Animal well-being. IV. Specific assessment criteria. Lab Anim Sci 47:586-597.
21. Clough G. 1982. Environmental effects on animals used in biomedical research. Bio Rev 57:487-523.
22. Coe JC. 2003. Steering the ark toward Eden: Design for animal well-being. J Am Vet Med Assoc 223:977-980.
23. Coq JO, Xerri C. 1998. Environmental enrichment alters organizational features of the forepaw representation in the primary somatosensory cortex of adult rats. Exp Brain Res 121:191-204.
24. Crabbe JC, Wahlsten D, Dudek BC. 1999. Genetics of mouse behavior: Interactions with laboratory environment. Science 284:1670-1672.
25. Crockett CM. Psychological well-being of captive nonhuman primates: Lessons from laboratory studies. In: Shepherdson DJ, Mellen JD, Hutchins M, eds. Second Nature. Washington DC: Smithsonian Institution Press. p 129-152.
26. Crockett CM, Bowers CL, Shimoji M, Leu M, Bowden DM, Sackett GP. 1995. Behavioral responses of longtailed macaques to different cage sizes and common laboratory practices. J Comp Psychol 109:368-383.
27. Crockett CM, Shimoji M, Bowden, DM. 2000. Behavior, appetite, and urinary cortisol responses by adult female pigtail macaques to cage size, cage level, room change, and ketamine sedation. Am J Primatol 52:63-80.
28. Curtis SE, Widowski TM. 1991. Enrichment of the environment. In: Ruys T, ed. Handbook of Facilities Planning. Vol 2. New York: Van Nostrand Reinhold. p 125-135.
29. Dahlqvist P, Zhao L, Johansson IM, Mattsson B, Johansson BB, Seckl JR, Olsson T. 1999. Environmental enrichment alters nerve growth factor-induced gene A and gluocorticoid receptor messenger RNA expression after middle cerebral artery occlusion in rats. Neuroscience 93: 527-535.
30. Dawkins MS. 1997. D.G.M. Wood-Gush memorial lecture: Why has there not been more progress in animal welfare research? Appl Anim Behav Sci 53:59-73.
31. Dewsbury DA. 1978. Comparative Animal Behavior. New York: McGraw-Hill, Inc.
32. Duncan IJH, Fraser D. 1997. Understanding animal welfare. In: Appleby MC, Hughes BO, eds. Animal Welfare. Wallingford UK: CAB International. p 19-31.
33. Ewing S, Lay DC, von Borell E. 1999. Farm Animal Well-Being. Englewood Cliffs NJ: Prentice Hall.
34. Grandin T. 1987. Animal handling. Vet Clin N Am Food Anim Pract. Vol 3. p 323-338.
35. Grandin T. 1991. Livestock behavior and the design of livestock-handling facilities. In: Ruys T, ed. Handbook of Facilities Planning. Vol 2. New York: Van Nostrand Reinhold. p 96-125.
36. Grandin T. 1997. Assessment of stress during handling and transport. J Anim Sci 75:249-257.
37. Guither H.D. 1998. Animal Rights. Carbondale: Southern Illinois University Press.
38. Hahn NE, Lau D, Eckert K, Markowitz H. 2000. Environmental enrichment-related injury in a macaque (Macaca fascicularis): Intestinal linear foreign body. Comp Med 50:556-558.
39. Hetts S. 1991. Psychologic well-being: Conceptual issues, behavioral measures, and implications for dogs. Vet Clin N Am Small Anim Pract 21: 369-387.
40. Hewson CJ. 2003. What is animal welfare? Common definitions and their practical consequences. Can Vet J 44:496-499.
41. Hill LR, Ambrose GA. 2003. A simple, inexpensive method to minimize floor-drain obstructions while supporting environmental enrichment in primate facilities. Contemp Top Lab Anim Sci 42:42-45.
42. Jennings M, Batchelor GR, Brain PF, Dick A, Elliott H, Francis RJ, Hubrecht RC, Hurst JL, Morton DM, Peters AG, Raymond R, Sales GD, Sherwin CM, West C. 1998. Refining rodent husbandry: The mouse. Lab Anim 32:233-259.
43. Johannsson BB, Belichenko PV. 2002. Neuronal plasticity and dendritic spines: Effect of environmental enrichment on intact and postischemic rat brain. J Cereb Blood Flow Metab 22:89-96.
44. Jones TA, Greenough WT. 1996. Ultrastructural evidence for increased contact between astrocytes and synapses in rats reared in a complex environment. Neurobiol Learn Mem 65 48-56.
45. King L. 2003. Behavioral evaluation of the psychological welfare and environmental requirements of agricultural research animals: Theory, measurement, ethics, and practical implications. ILAR J 44:211-221.
46. Landi MD, Kreider JW, Lang CM, Bullock LP. 1982. Effects of shipping on the immune function in mice. Am J Vet Res 43:1654-1657.
47. Laule GE, Thurston RH, Alford PL, Bloomsmith MA. 1996. Training to reliably obtain blood and urine samples from a young diabetic chimpanzee (Pan troglodytes). Zoo Biol 15:587-591.
48. Marashi V, Barnekow A, Ossendorf E, Sachser N. 2003. Effects of different forms of environmental enrichment on behavioral, endocrinological, and immunological parameters in male mice. Horm Behav 43: 281-292.
49. Mätz-Rensing K, Floto A, Kaup F-J. 2004. Intraperitoneal foreign body disease in a baboon (Papio hamadryas). J Med Primatol 33:113-116.
50. Moberg GP. 1985. Biological response to stress: Key to assessment of animal well-being. In: Moberg GP, ed. Animal Stress. Bethesda: American Physiological Society. p 27-49.
51. Moncek F, Duncko R, Johansson BB, Jezova D. 2004. Effect of environmental enrichment on stress related systems in rats. J Neuroendocrinol 16:423-431.
52. Morrow-Tesch JL. 2001. Evaluating management practices for their impact on welfare. J Am Vet Med Assoc 219:1374-1376.
53. Murchison MA. 1993. Potential animal hazard with ring toys. Lab Prim Newsltr 32:7.
54. NRC [National Research Council]. 1996. Guide for the Care and Use of Laboratory Animals. 7th ed. Washington DC: National Academy Press.
55. NRC [National Research Council]. 1998. Psychological Well-Being of Nonhuman Primates. Washington DC: National Academy Press.
56. NRC [National Research Council]. 2003. Guidelines for the Care and Use of Mammals in Neuroscience and Behavioral Research. Washington DC: National Academy Press.
57. Newberry RC. 1995. Environmental enrichment: Increasing the biological relevance of captive environments. Appl Anim Behav Sci 44:229-243.
58. Novak MA, Petto AJ, eds. 1991. Through the Looking Glass. Washington DC: American Psychological Association.
59. Novak MA, Suomi SJ. 1988. Psychological well-being of primates in captivity. Am Psychol 43:765-773.
60. Novak MA, Suomi SJ. 1991. Social interaction in nonhuman primates: An underlying theme for primate research. Lab Anim Sci 41:308-314.
61. PHS [Public Health Service]. 2002. Public Health Service Policy on Humane Care and Use of Laboratory Animals. Washington DC: US Department of Health and Human Services, National Institutes of Health, Office of Extramural Research, Office of Laboratory Animal Welfare.
62. PL [Public Law] 85-765. 1958. Humane Slaughter Act of 1958. 7 U.S.C. 1901 et seq. Washington DC: GPO.
63. Priest GM. 1991. Training a diabetic drill (Mandrillus leucophaeus) to accept insulin injections and venipuncture. Lab Prim Newsltr 30:1-4.
64. Radley JJ, Sisti HM, Hao J, Rocher AB, McCall T, Hof PR, McEwen BS, Morrison JH. 2004. Chronic behavioral stress induces apical dendritic reorganization in pyramidal neurons of the medial prefrontal cortex. Neuroscience 125:1-6.
65. Reinhardt V. 1997. Training nonhuman primates to cooperate during blood collection: A review. Lab Prim Newsltr 36:1-4.
66. Reinhardt V, Cowley D. 1992. In-home cage blood collection from conscious stump-tailed macaques. Anim Welfare 1:249-255.
67. Reinhardt V, Liss C, Stevens C. 1995. Restraint methods of laboratory non-human primates: A critical review. Anim Welfare 4:221-238.
68. Riley V. 1981. Psychoneuroendocrine influences on immunocompetence and neoplasia. Science 212:1110-1109.
69. Rushen J. 1986. Some problems with the physiological concept of "stress." Aust Vet J 63:359-361.
70. Rushen J. 2003. Changing concepts of farm animal welfare: Bridging the gap between applied and basic research. Appl Anim Behav Sci 81:199-214.
71. Russell WMS, Burch RL. 1959. The principles of humane experimental technique. London: Methuen & Company Ltd.
72. Ruys T. 1991. Understanding animals as they affect the animal research environment. In: Ruys T, ed. Handbook of Facilities Planning. Vol 2. New York: Van Nostrand Reinhold. p 93-96.
73. Sanhouri AA, Jones RS, Dobson H. 1989. The effects of different types of transportation on plasma cortisol and testosterone concentrations in male goats. Br Vet J 145:446-450.
74. Schapiro SJ. 2002. Effects of social manipulations and environmental enrichment on behavior and cell-mediated immune responses in rhesus macaques. Pharmacol Biochem Behav 73:271-278.
75. Schapiro SJ, Nehete PN, Perlman JE, Jagannadha Sastry K. 2000. A comparison of cell-mediated immune responses in rhesus macaques housed singly, in pairs, or in groups. Appl Anim Behav Sci 68:67-84.
76. Schapiro SJ, Perlman JE, Boudreau BA. 2001. Manipulating the affiliative interactions of group-housed rhesus macaques using positive reinforcement training techniques. Am J Primatol 55:137-149.
77. Segal EF, ed. 1989. Housing, Care and Psychological Wellbeing of Captive and Laboratory Primates. Park Ridge NJ: Noyes Publications.
78. Shepherdson DJ. 1998. Tracing the path of environmental enrichment in zoos. In: Shepherdson DJ, Mellen JD, Hutchins M, eds. Second Nature. Washington DC: Smithsonian Institution Press. p 1-12.
79. Shomer NH, Piekert S, Terwilliger G. 2001. Enrichment toy-trauma in a New Zealand white rabbit. Contemp Top Lab Anim Sci 40:31-32.
80. Stewart KL, Bayne K. 2004. Environmental enrichment for laboratory animals. In: Reuter JD, Suckow MA, eds. Laboratory Animal Medicine and Management. Ithaca: International Veterinary Information Service (www.ivis.org); document no. B2520.0404.
81. Tuli JS, Smith JA, Morton DB. 1995. Stress measurements in mice after transportation. Lab Anim 29:132-138.
82. von Uexküll J. 1934. A stroll through the world of animals and men: A picture book of invisible worlds. Berlin: Springer. (1957 Translation. In: Schiller CH, ed. Instinctive Behavior: The Development of a Modern Concept. New York: International Universities Press.)
83. Wallace AR. 1869. The Malay Archipelago. (1962 Reprint. The Malay Archipelago. New York: Dover Publications.)
84. Wallace AR. 1900. Studies scientific and social. Vol 1. London: Macmillan and Company Ltd.
85. Webster AJF. 1998. What is science to animal welfare? Naturwissenschaften 85:262-269.
86. Williams LE, Abee CR, Barnes SR, Ricker RB. 1988. Cage design and configuration for an arboreal species of primate. Lab Anim Sci 38:289-291.
87. Yerkes RM. 1916. Provision for the study of monkeys and apes. Science 43:231-234.
88. Young RJ. 2003. Environmental Enrichment for Captive Animals. Oxford: Blackwell Science Ltd.