The need for randomization in animal trials: An overview of systematic reviews

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Hirst, Jennifer A ^a   Howick, Jeremy ^a   Aronson, Jeffrey K ^a   Roberts, Nia ^b   Perera, Rafael ^a   Koshiaris, Constantinos ^a   Heneghan, Carl ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BONE CANCER; BRAIN HEMORRHAGE; EFFECT SIZE; EMERGENCY MEDICINE; EXPERIMENTAL STROKE; GLIOMA; META ANALYSIS (TOPIC); MULTIPLE SCLEROSIS; NONHUMAN; OUTCOME ASSESSMENT; PARKINSON DISEASE; RANDOMIZATION; REVIEW; SPINAL CORD DISEASE; SYSTEMATIC REVIEW (TOPIC); ANIMAL; ANIMAL EXPERIMENT; LITERATURE; METHODOLOGY; STATISTICAL BIAS;

ANIMAL EXPERIMENTATION; ANIMALS; BIAS (EPIDEMIOLOGY); RESEARCH DESIGN; REVIEW LITERATURE AS TOPIC;

EID: 84902597896     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0098856     Document Type: Review

References (71)

1. Sackett DL (1969) Clinical epidemiology. Am J Epidemiol 89: 125-128.
2. Sackett DL (1986) Rules of evidence and clinical recommendations on the use of antithrombotic agents. Chest 89: 2S-3S.
3. Sackett DL, Richardson WS, Rosenberg W, Haynes B (1997) Evidence-based medicine: How to Practice & Teach EBM. London: Churchill Livingstone.
4. Chalmers I (2007) The lethal consequences of failing to make full use of all relevant evidence about the effects of medical treatments: the importance of systematic reviews. In: Rothwell PM, editor. Treating individuals: from randomised trials to personalized medicine. London: The Lancet.
5. Howick J (2011) The Philosophy of Evidence-Based Medicine. Oxford: Wiley-Blackwell.
6. Juni P, Altman DG, Egger M (2001) Systematic reviews in health care: Assessing the quality of controlled clinical trials. BMJ 323: 42-46. (Pubitemid 32682008)
7. Farley SM, Libanati CR, Odvina CV, Smith L, Eliel L, et al. (1989) Efficacy of long-term fluoride and calcium therapy in correcting the deficit of spinal bone density in osteoporosis. J Clin Epidemiol 42: 1067-1074. (Pubitemid 19264334)
8. Knekt P, Reunanen A, Jarvinen R, Seppanen R, Heliovaara M, et al. (1994) Antioxidant vitamin intake and coronary mortality in a longitudinal population study. Am J Epidemiol 139: 1180-1189. (Pubitemid 24184411)
9. Decousus H, Leizorovicz A, Parent F, Page Y, Tardy B, et al. (1998) A clinical trial of vena caval filters in the prevention of pulmonary embolism in patients with proximal deep-vein thrombosis. Prevention du Risque d'Embolie Pulmonaire par Interruption Cave Study Group. N Engl J Med 338: 409-415. (Pubitemid 28135667)
10. Riggs BL, Hodgson SF, O'Fallon WM, Chao EY, Wahner HW, et al. (1990) Effect of fluoride treatment on the fracture rate in postmenopausal women with osteoporosis. N Engl J Med 322: 802-809. (Pubitemid 20094143)
11. Yusuf S, Dagenais G, Pogue J, Bosch J, Sleight P (2000) Vitamin E supplementation and cardiovascular events in high-risk patients. The Heart Outcomes Prevention Evaluation Study Investigators. N Engl J Med 342: 154-160. (Pubitemid 30051646)
12. Schulz KF, Chalmers I, Hayes RJ, Altman DG (1995) Empirical evidence of bias. Dimensions of methodological quality associated with estimates of treatment effects in controlled trials. JAMA 273: 408-412.
13. Odgaard-Jensen J, Vist GE, Timmer A, Kunz R, Akl EA, et al. (2011) Randomisation to protect against selection bias in healthcare trials. Cochrane database of systematic reviews: MR000012.
14. Savovic J, Jones HE, Altman DG, Harris RJ, Juni P, et al. (2012) Influence of Reported Study Design Characteristics on Intervention Effect Estimates From Randomized, Controlled Trials. Annals of internal medicine.
15. Bath PM, Macleod MR, Green AR (2009) Emulating multicentre clinical stroke trials: a new paradigm for studying novel interventions in experimental models of stroke. International journal of stroke: official journal of the International Stroke Society 4: 471-479.
16. Bebarta V, Luyten D, Heard K (2003) Emergency medicine animal research: does use of randomization and blinding affect the results? Academic emergency medicine: official journal of the Society for Academic Emergency Medicine 10: 684-687.
17. Jerndal M, Forsberg K, Sena ES, Macleod MR, O'Collins VE, et al. (2010) A systematic review and meta-analysis of erythropoietin in experimental stroke. Journal of cerebral blood flow and metabolism: official journal of the International Society of Cerebral Blood Flow and Metabolism 30: 961-968.
18. Macleod MR, O'Collins T, Horky LL, Howells DW, Donnan GA (2005) Systematic review and metaanalysis of the efficacy of FK506 in experimental stroke. Journal of cerebral blood flow and metabolism: official journal of the International Society of Cerebral Blood Flow and Metabolism 25: 713-721.
19. Macleod MR, O'Collins T, Howells DW, Donnan GA (2004) Pooling of animal experimental data reveals influence of study design and publication bias. Stroke; a journal of cerebral circulation 35: 1203-1208. (Pubitemid 38543544)
20. Macleod MR, van der Worp HB, Sena ES, Howells DW, Dirnagl U, et al. (2008) Evidence for the efficacy of NXY-059 in experimental focal cerebral ischaemia is confounded by study quality. Stroke; a journal of cerebral circulation 39: 2824-2829.
21. Perel P, Roberts I, Sena E, Wheble P, Briscoe C, et al. (2007) Comparison of treatment effects between animal experiments and clinical trials: systematic review. BMJ 334: 197.
22. Sena E, Wheble P, Sandercock P, Macleod M (2007) Systematic review and meta-analysis of the efficacy of tirilazad in experimental stroke. Stroke 38: 388-394. (Pubitemid 46184311)
23. van der Worp HB, de Haan P, Morrema E, Kalkman CJ (2005) Methodological quality of animal studies on neuroprotection in focal cerebral ischaemia. Journal of neurology 252: 1108-1114. (Pubitemid 41355842)
24. van der Worp HB, Sena ES, Donnan GA, Howells DW, Macleod MR (2007) Hypothermia in animal models of acute ischaemic stroke: a systematic review and meta-analysis. Brain: a journal of neurology 130: 3063-3074.
25. Vesterinen HM, Egan K, Deister A, Schlattmann P, Macleod MR, et al. (2011) Systematic survey of the design, statistical analysis, and reporting of studies published in the 2008 volume of the Journal of Cerebral Blood Flow and Metabolism. Journal of cerebral blood flow and metabolism: official journal of the International Society of Cerebral Blood Flow and Metabolism 31: 1064-1072.
26. MacLeod M (2010) How to avoid bumping into the translational roadblock. Rodent Models of Stroke Neuromethods. 47: 7-15.
27. Ioannidis JP (2006) Evolution and translation of research findings: from bench to where? PLoS Clin Trials 1: e36.
28. Sena ES, Briscoe CL, Howells DW, Donnan GA, Sandercock PA, et al. (2010) Factors affecting the apparent efficacy and safety of tissue plasminogen activator in thrombotic occlusion models of stroke: systematic review and meta-analysis. Journal of cerebral blood flow and metabolism: official journal of the International Society of Cerebral Blood Flow and Metabolism 30: 1905-1913.
29. Macleod M (2011) CAMARADES. Edinburgh: CAMARADES.
30. Crossley NA, Sena E, Goehler J, Horn J, Van Der Worp B, et al. (2008) Empirical evidence of bias in the design of experimental stroke studies: A metaepidemiologic approach. Stroke 39: 929-934. (Pubitemid 351619572)
31. Macleod M, van der Worp HB (2010) Animal models of neurological disease: are there any babies in the bathwater? Practical neurology 10: 312-314.
32. Janssen H, Bernhardt J, Collier JM, Sena ES, McElduff P, et al. (2010) An enriched environment improves sensorimotor function post-ischemic stroke. Neurorehabilitation and neural repair 24: 802-813.
33. Shea BJ, Bouter LM, Peterson J, Boers M, Andersson N, et al. (2007) External validation of a measurement tool to assess systematic reviews (AMSTAR). PLoS One 2: e1350.
34. DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Controlled Clinical Trials 7: 177-188. (Pubitemid 17189972)
35. Higgins JJ, Green S (2008) The Cochrane Handbook for Systematic Reviews of Interventions. Chichester: The Cochrane Collaboration.
36. Banwell V, Sena ES, Macleod MR (2009) Systematic review and stratified meta-analysis of the efficacy of interleukin-1 receptor antagonist in animal models of stroke. Journal of stroke and cerebrovascular diseases: the official journal of National Stroke Association 18: 269-276.
37. Bath PMW, Gray LJ, Bath AJG, Buchan A, Miyata T, et al. (2009) Effects of NXY-059 in experimental stroke: an individual animal meta-analysis. British Journal of Pharmacology 157: 1157-1171.
38. Egan KJ, Janssen H, Sena ES, Longley L, Speare S, et al. (2014) Exercise Reduces Infarct Volume and Facilitates Neurobehavioral Recovery: Results From a Systematic Review and Meta-analysis of Exercise in Experimental Models of Focal Ischemia. Neurorehabil Neural Repair.
39. Frantzias J, Sena ES, Macleod MR, Al-Shahi Salman R (2011) Treatment of intracerebral hemorrhage in animal models: meta-analysis. Annals of neurology 69: 389-399.
40. Gibson CL, Gray LJ, Murphy SP, Bath PM (2006) Estrogens and experimental ischemic stroke: a systematic review. J Cereb Blood Flow Metab 26: 1103-1113. (Pubitemid 44268172)
41. Horn J, De Haan RJ, Vermeulen M, Luiten PGM, Limburg M (2001) Nimodipine in animal model experiments of focal cerebral ischemia: A systematic review. Stroke 32: 2433-2438. (Pubitemid 32954819)
42. Lees JS, Sena ES, Egan KJ, Antonic A, Koblar SA, et al. (2012) Stem cell-based therapy for experimental stroke: a systematic review and meta-analysis. Int J Stroke 7: 582-588.
43. Macleod MR, O'Collins T, Horky LL, Howells DW, Donnan GA (2005) Systematic review and meta-analysis of the efficacy of melatonin in experimental stroke. Journal of pineal research 38: 35-41. (Pubitemid 40139308)
44. Pedder H, Vesterinen HM, Macleod MR, Wardlaw JM (2014) Systematic review and meta-analysis of interventions tested in animal models of lacunar stroke. Stroke 45: 563-570.
45. Sena E, van der Worp HB, Howells D, Macleod M (2007) How can we improve the pre-clinical development of drugs for stroke? Trends in neurosciences 30: 433-439. (Pubitemid 47374833)
46. Wheble PCR, Sena ES, Macleod MR (2008) A systematic review and meta-analysis of the efficacy of piracetam and piracetam-like compounds in experimental stroke. Cerebrovascular Diseases 25: 5-11. (Pubitemid 351280369)
47. Vesterinen HM, Currie GL, Carter S, Mee S, Watzlawick R, et al. (2013) Systematic review and stratified meta-analysis of the efficacy of RhoA and Rho kinase inhibitors in animal models of ischaemic stroke. Syst Rev 2: 33.
48. Antonic A, Sena ES, Lees JS, Wills TE, Skeers P, et al. (2013) Stem cell transplantation in traumatic spinal cord injury: a systematic review and meta-analysis of animal studies. PLoS Biol 11: e1001738.
49. Batchelor PE, Skeers P, Antonic A, Wills TE, Howells DW, et al. (2013) Systematic review and meta-analysis of therapeutic hypothermia in animal models of spinal cord injury. PLoS One 8: e71317.
50. Batchelor PE, Wills TE, Skeers P, Battistuzzo CR, Macleod MR, et al. (2013) Meta-analysis of pre-clinical studies of early decompression in acute spinal cord injury: a battle of time and pressure. PLoS One 8: e72659.
51. Watzlawick R, Sena ES, Dirnagl U, Brommer B, Kopp MA, et al. (2014) Effect and reporting bias of RhoA/ROCK-blockade intervention on locomotor recovery after spinal cord injury: a systematic review and meta-analysis. JAMA Neurol 71: 91-99.
52. Currie GL, Delaney A, Bennett MI, Dickenson AH, Egan KJ, et al. (2013) Animal models of bone cancer pain: systematic review and meta-analyses. Pain 154: 917-926.
53. Hirst TC, Vesterinen HM, Sena ES, Egan KJ, Macleod MR, et al. (2013) Systematic review and meta-analysis of temozolomide in animal models of glioma: was clinical efficacy predicted? Br J Cancer 108: 64-71.
54. Vesterinen HM, Sena ES, ffrench-Constant C, Williams A, Chandran S, et al. (2010) Improving the translational hit of experimental treatments in multiple sclerosis. Multiple sclerosis 16: 1044-1055.
55. Rooke ED, Vesterinen HM, Sena ES, Egan KJ, Macleod MR (2011) Dopamine agonists in animal models of Parkinson's disease: A systematic review and meta-analysis. Parkinsonism & related disorders 17: 313-320.
56. Lynch JJ, Fregin GF, Mackie JB, Monroe RR, Jr. (1974) Heart rate changes in the horse to human contact. Psychophysiology 11: 472-478.
57. Newton JE, Ehrlich W (1993) Coronary blood flow in dogs: effect of person. Integrative physiological and behavioral science: the official journal of the Pavlovian Society 28: 280-286.
58. Breuer K, Hemsworth PH, Barnett JL, Matthews LR, Coleman GJ (2000) Behavioural response to humans and the productivity of commercial dairy cows. Applied animal behaviour science 66: 273-288. (Pubitemid 30141928)
59. Liberati A, Himel HN, Chalmers TC (1986) A quality assessment of randomized control trials of primary treatment of breast cancer. Journal of clinical oncology: official journal of the American Society of Clinical Oncology 4: 942-951.
60. Simera I (2008) EQUATOR Network collates resources for good research. BMJ 337: a2471.
61. Landis SC, Amara SG, Asadullah K, Austin CP, Blumenstein R, et al. (2012) A call for transparent reporting to optimize the predictive value of preclinical research. Nature 490: 187-191.
62. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG (2010) Improving bioscience research reporting: The ARRIVE guidelines for reporting animal research. Journal of pharmacology & pharmacotherapeutics 1: 94-99.
63. Henderson VC, Kimmelman J, Fergusson D, Grimshaw JM, Hackam DG (2013) Threats to validity in the design and conduct of preclinical efficacy studies: a systematic review of guidelines for in vivo animal experiments. PLoS Med 10: e1001489.
64. Sena ES, van der Worp HB, Bath PM, Howells DW, Macleod MR (2010) Publication bias in reports of animal stroke studies leads to major overstatement of efficacy. PLoS biology 8: e1000344.
65. International Committee of Medical Journal Editors (2009) Uniform Requirements for Manuscripts Submitted to Biomedical Journals.
66. Kimmelman J, Anderson JA (2012) Should preclinical studies be registered? Nat Biotechnol 30: 488-489.
67. Beery AK, Zucker I (2011) Sex bias in neuroscience and biomedical research. Neurosci Biobehav Rev 35: 565-572.
68. FDA (2005) CFR 314.126: Applications for FDA Approval to Market a New Drug. United States Food and Drug Administration.
69. Medical Research Council (2013) The MRC and Clinical Trials. London: MRC.
70. Vilar J, Duley L (2003) The need for large and simple randomized trials in reproductive health. Geneva: The World Health Organization Library.
71. SABRE (2012) SABRE Research UK. In: SABRE, editor.