Systematic reviews of animal models: Methodology versus epistemology

International Journal of Medical Sciences

Volumn 10, Issue 3, 2013, Pages 206-221

  Greek, Ray ^a   Menache, Andre ^a  

^a Americans For Medical Advancement   (United States)

Author keywords

Animal models; Axiom; Biological complexity; Evolution; Systematic reviews

Indexed keywords

ABACAVIR; AZATHIOPRINE; CARBAMAZEPINE; CODEINE; ISONIAZID;

APPLIED RESEARCH; BIOAVAILABILITY; CONSENSUS DEVELOPMENT; DRUG DESIGN; DRUG HYPERSENSITIVITY; DRUG RESEARCH; DRUG RESPONSE; DRUG SAFETY; EMPIRICAL RESEARCH; EPISTEMOLOGY; EVALUATION RESEARCH; EVIDENCE BASED MEDICINE; EXPERIMENTAL ANIMAL; HUMAN; HUMAN VERSUS ANIMAL COMPARISON; MEDICAL LITERATURE; MEDICAL RESEARCH; METHODOLOGY; MOLECULAR EVOLUTION; NEUTROPENIA; NONHUMAN; OUTCOMES RESEARCH; PERIPHERAL NEUROPATHY; PREDICTIVE VALUE; QUALITY CONTROL; RESPIRATION DEPRESSION; REVIEW; SEDATION; SIDE EFFECT; STANDARDIZATION; STEVENS JOHNSON SYNDROME; SYSTEMATIC REVIEW; THEORETICAL STUDY;

ANIMAL MODELS.; AXIOM; BIOLOGICAL COMPLEXITY; EVOLUTION; SYSTEMATIC REVIEWS;

ANIMAL EXPERIMENTATION; ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; KNOWLEDGE; META-ANALYSIS AS TOPIC;

EID: 84873355257     PISSN: 14491907     EISSN: None     Source Type: Journal    
DOI: 10.7150/ijms.5529     Document Type: Review

References (224)

1. Van Buskirk NE. The Review Article in MEDLINE: Ambiguity of Definition and Implications for Online Searchers. Bull. Med. Libr. Assoc. 1984;72(4):349-52.
2. Greenhalgh T. How to read a paper: Papers that summarise other papers (systematic reviews and meta-analyses). BMJ. 1997; 315: 672-5. doi:10.1136/bmj.315.7109.672.
3. Shermer M. The Believing Brain: From Ghosts and Gods to Politics and Conspiracies---How We Construct Beliefs and Reinforce Them as Truths. New York: Times Books; 2011.
4. Green S, Higgins J, Alderson P, Clarke M, Mulrow C, Oxman A. Chapter 1: Introduction. In: Higgins J, Green S, editors. Cochrane Handbook for Systematic Reviews of Interventions Version 501. London: The Cochrane Collaboration; 2008.
5. The Cochrane Collaboration. Cochrane Handbook for Systematic Reviews of Interventions. London: The Cochrane Collaboration; 2011.
6. Sackett DL, Rosenberg WM, Gray JA, Haynes RB, Richardson WS. Evidence based medicine: what it is and what it isn't. BMJ. 1996; 312: 71-2.
7. Glass G. Primary, secondary and meta-analysis of research. Educational Researcher. 1976; 5: 3-8.
8. Barrett S. Be Wary of Acupuncture, Qigong, and "Chinese Medicine". Quackwatch. 2011.
9. Novella S. Acupuncture and Acoustic Waves. Neurologica. 2011.
10. Gorski D. NIH Director Francis Collins doesn't understand the problem with CAM. Science-Based Medicine. 2012.
11. Barret S. Quackwatch; Homeopathy: The Ultimate Fake. Quackwatch. 2009.
12. No author listed. Human albumin administration in critically ill patients: systematic review of randomised controlled trials. Cochrane Injuries Group Albumin Reviewers. BMJ. 1998; 317: 235-40.
13. Finfer S, Bellomo R, Boyce N, French J, Myburgh J, Norton R. A comparison of albumin and saline for fluid resuscitation in the intensive care unit. N Engl J Med. 2004; 350: 2247-56.
14. Hooijmans CR, Leenaars M, Ritskes-Hoitinga M. A gold standard publication checklist to improve the quality of animal studies, to fully integrate the Three Rs, and to make systematic reviews more feasible. Alternatives to laboratory animals: ATLA. 2010; 38: 167-82.
15. Nuffield Council on Bioethics. The ethics of research involving animals. London: Nuffield Council on Bioethics; 2005.
16. NC3Rs. Systematic Reviews of Animal Research. London: NC3Rs; 2011.
17. Macleod MR, O'Collins T, Howells DW, Donnan GA. Pooling of animal experimental data reveals influence of study design and publication bias. Stroke. 2004; 35: 1203-8.
18. Bracken M. Why animal studies are often poor predictors of human reactions to exposure. J R Soc Med. 2008; 101: 120-22.
19. Bracken MB. Why are so many epidemiology associations inflated or wrong? Does poorly conducted animal research suggest implausible hypotheses? Annals of epidemiology. 2009; 19: 220-4. doi:10.1016/j.annepidem.2008.11.006.
20. UMC St Radboud. About systematic reviews. Bereikbaarheid: UMC St Radboud; 2012.
21. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG. Animal research: reporting in vivo experiments-The ARRIVE Guidelines. J Cereb Blood Flow Metab. 2011; 31: 991-3. doi:jcbfm2010220 [pii]10.1038/jcbfm.2010.220.
22. Crossley NA, Sena E, Goehler J, Horn J, van der Worp B, Bath PM, et al. Empirical evidence of bias in the design of experimental stroke studies: a metaepidemiologic approach. Stroke. 2008; 39: 929-34.
23. Amarasingh S, Macleod MR, Whittle IR. What is the translational efficacy of chemotherapeutic drug research in neuro-oncology? A systematic review and meta-analysis of the efficacy of BCNU and CCNU in animal models of glioma. Journal of neuro-oncology. 2009; 91: 117-25. doi:10.1007/s11060-008-9697-z.
24. Dirnagl U, Macleod MR. Stroke research at a road block: the streets from adversity should be paved with meta-analysis and good laboratory practice. British Journal of Pharmacology. 2009; 157: 1154-6.
25. Macleod M. Systematic Review and Meta-analysis of Experimental Stroke. International Journal of Neuroprotection and Neuroregeneration. 2004; 1: 9-12.
26. Macleod MR, Ebrahim S, Roberts I. Surveying the literature from animal experiments: systematic review and meta-analysis are important contributions. BMJ. 2005; 331: 110. doi:331/7508/110-b [pii]10.1136/bmj.331.7508.110-b.
27. O'Collins VE, Macleod MR, Cox SF, Van Raay L, Aleksoska E, Donnan GA, et al. Preclinical drug evaluation for combination therapy in acute stroke using systematic review, meta-analysis, and subsequent experimental testing. Journal of cerebral blood flow and metabolism: official journal of the International Society of Cerebral Blood Flow and Metabolism. 2011; 31: 962-75. doi:10.1038/jcbfm.2010.184.
28. Sena E, van der Worp HB, Howells D, Macleod M. How can we improve the pre-clinical development of drugs for stroke? Trends in neurosciences. 2007; 30: 433-9. doi:10.1016/j.tins.2007.06.009.
29. O'Collins VE, Macleod MR, Donnan GA, Horky LL, van der Worp BH, Howells DW. 1,026 experimental treatments in acute stroke. Ann Neurol. 2006; 59: 467-77. doi:10.1002/ana.20741.
30. Frantzias J, Sena ES, Macleod MR, Salman RA-S. Treatment of intracerebral hemorrhage in animal models: Meta-analysis. Annals of Neurology. 2011; 69: 389-99. doi:10.1002/ana.22243.
31. PAO-Heyendael. 1st International Symposium and Workshop on Systematic Reviews in Laboratory Animal Science. PAO-Heyendael. 2012.
32. Pound P, Ebrahim S, Sandercock P, Bracken MB, Roberts I. Where is the evidence that animal research benefits humans? BMJ. 2004; 328: 514-7. doi:10.1136/bmj.328.7438.514 [doi]328/7438/514 [pii].
33. Smith JA, Birke L, Sadler D. Reporting animal use in scientific papers. Laboratory animals. 1997; 31: 312-7.
34. Sniekers YH, Weinans H, Bierma-Zeinstra SM, van Leeuwen JP, van Osch GJ. Animal models for osteoarthritis: the effect of ovariectomy and estrogen treatment - a systematic approach. Osteoarthritis Cartilage. 2008; 16: 533-41. doi:10.1016/j.joca.2008.01.002.
35. Alfaro V. Specification of laboratory animal use in scientific articles: current low detail in the journals' instructions for authors and some proposals. Methods Find Exp Clin Pharmacol. 2005; 27: 495-502. doi:10.1358/mf.2005.27.7.921309.
36. Festing MF. Inbred strains should replace outbred stocks in toxicology, safety testing, and drug development. Toxicologic pathology. 2010; 38: 681-90. doi:10.1177/0192623310373776.
37. Macleod MR, Fisher M, O'Collins V, Sena ES, Dirnagl U, Bath PM, et al. Reprint: Good laboratory practice: preventing introduction of bias at the bench. Journal of cerebral blood flow and metabolism: official journal of the International Society of Cerebral Blood Flow and Metabolism. 2009; 29: 221-3. doi:10.1038/jcbfm.2008.101.
38. van der Worp HB, Howells DW, Sena ES, Porritt MJ, Rewell S, O'Collins V, et al. Can Animal Models of Disease Reliably Inform Human Studies? PLoS Med. 2010; 7: e1000245.
39. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG. Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol. 2010; 8: e1000412.
40. Greek R, Shanks N. FAQs About the Use of Animals in Science: A handbook for the scientifically perplexed. Lanham: University Press of America; 2009.
41. Greek R, Greek J. Is the use of sentient animals in basic research justifiable? Philos Ethics Humanit Med. 2010; 5: 14. doi:1747-5341-5-14 [pii]10.1186/1747-5341-5-14.
42. Dombrowski D. Babies and Beasts: The Argument from Marginal Cases: University of Illinois Press. 1997.
43. Dombrowski DA. Is the argument from marginal cases obtuse? J Appl Philos. 2006; 23: 223-32.
44. NABR. The Human care and Treatment of Laboratory Animals. NABR. 1999.
45. Council for International Organizations of Medical Sciences (CIMOS). International ethical guidelines for biomedical research involving human subjects. Bull Med Ethics. 2002;: 17-23.
46. Festing S, Wilkinson R. The ethics of animal research. Talking Point on the use of animals in scientific research. EMBO reports. 2007; 8: 526-30.
47. Gad S. Preface. In: Gad S, editor. Animal Models in Toxicology. Boca Rotan: CRC Press; 2007;: 1-18.
48. CNN. Is animal testing necessary? CNN. 2009.
49. Marshall BioResources. Benefits of Animal Research. Marshall BioResources. 2010.
50. Buzoni-Gatel D, Decelle T, Hardy P, Montagutelli X, Louis J. Animal Models and Relevance/Predictivity: how to better leverage the knowledge of the veterinarian field. Fondation Mérieux. 2011.
51. Vassar R. Alzheimer's therapy: a BACE in the hand? Nat Med. 2011; 17: 932-3.
52. Devoy A, Bunton-Stasyshyn RKA, Tybulewicz VLJ, Smith AJH, Fisher EMC. Genomically humanized mice: technologies and promises. Nat Rev Genet. 2012; 13: 14-20.
53. Hau J. Animal Models. In: Hau J, van Hoosier Jr GK, editors. Handbook of Laboratory Animal Science Second Edition Animal Models. 2nd ed. Boca Rotan: CRC Press; 2003;: 1-9.
54. Giles J. Animal experiments under fire for poor design. Nature. 2006; 444: 981.
55. Gibson E. Q&A: Dr. Keith Cheng, researcher at Penn State's College of Medicine, shares views on using animals in scientific research. The Patriot-News. 2012.
56. Heywood R. Clinical Toxicity--Could it have been predicted? Post-marketing experience. In: CE Lumley, Walker S, editors. Animal Toxicity Studies: Their Relevance for Man. Lancaster: Quay; 1990;: 57-67.
57. Rudczynski AB. Letter. New Haven Register. New Haven. 2011.
58. Sisto A. Italian scientists convicted over earthquake warning. Chicago: Chicago Tribune. 2012.
59. Leshner A. Letter to Giorgio Napolitano. AAAS. 2012.
60. Hall SS. Scientists on trial: At fault? Nature. 2011; 477: 264-69. doi:10.1038/477264a.
61. Macleod M. Why animal research needs to improve. Nature. 2011; 477: 511. doi:10.1038/477511a.
62. Greek R, Hansen LA, Menache A. An analysis of the Bateson Review of research using nonhuman primates. Medicolegal and Bioethics 2011; 1: 3-22.
63. Greek R, Menache A, Rice MJ. Animal models in an age of personalized medicine. Personalized Medicine. 2012; 9: 47-64. doi:10.2217/pme.11.89.
64. Greek R, Shanks N, Rice MJ. The History and Implications of Testing Thalidomide on Animals. The Journal of Philosophy, Science & Law. 2011;: 11.
65. Shanks N, Greek R. Animal Models in Light of Evolution. Boca Raton: Brown Walker; 2009.
66. Shanks N, Greek R, Greek J. Are animal models predictive for humans? Philos Ethics Humanit Med. 2009; 4: 2. doi:1747-5341-4-2 [pii]10.1186/1747-5341-4-2.
67. Gamble LJ, Matthews QL. Current progress in the development of a prophylactic vaccine for HIV-1. Drug Des Devel Ther. 2010; 5: 9-26. doi:10.2147/DDDT.S6959.
68. Editorial. Cold shower for AIDS vaccines. Nat Med. 2007; 13: 1389-90.
69. van der Worp HB, Macleod MR. Preclinical studies of human disease: Time to take methodological quality seriously. Journal of molecular and cellular cardiology. 2011; 51: 449-50.
70. Dirnagl U, Lauritzen M. Improving the Quality of Biomedical Research: Guidelines for Reporting Experiments Involving Animals. J Cereb Blood Flow Metab. 2011; 31: 989-90.
71. Macleod M, van der Worp HB. Animal models of neurological disease: are there any babies in the bathwater? Practical Neurology. 2010; 10: 312-4. doi:10.1136/jnnp.2010.230524.
72. American Paraplegia Society. Symposium on spinal cord injury models. Presented at the 33rd annual meeting of the American Paraplegia Society. September 1987. J Am Paraplegia Soc. 1988; 11: 23-58.
73. Crowley WF, Jr. Translation of basic research into useful treatments: how often does it occur? Am J Med. 2003; 114: 503-5.
74. Enna SJ, Williams M. Defining the role of pharmacology in the emerging world of translational research. Advances in pharmacology. 2009; 57: 1-30. doi:10.1016/S1054-3589(08)57001-3.
75. Hackam DG, Redelmeier DA. Translation of research evidence from animals to humans. JAMA. 2006; 296: 1731-2.
76. Schnabel J. Neuroscience: Standard model. Nature. 2008; 454: 682-5.
77. Hurko O. Understanding the strategic importance of biomarkers for the discovery and early development phases. Drug Discovery World. 2006;: 63-74.
78. Cressey D. Traditional drug-discovery model ripe for reform. Nature. 2011; 471: 17-8.
79. Hughes JP, Rees S, Kalindjian SB, Philpott KL. Principles of early drug discovery. British Journal of Pharmacology. 2011; 162: 1239-49.
80. Giri S, Bader A. Foundation review: Improved preclinical safety assessment using micro-BAL devices: the potential impact on human discovery and drug attrition. Drug Discovery Today. 2011; 16: 382-97.
81. Litchfield JT, Jr. Symposium on clinical drug evaluation and human pharmacology. XVI. Evaluation of the safety of new drugs by means of tests in animals. Clin Pharmacol Ther. 1962; 3: 665-72.
82. Suter K. What can be learned from case studies? The company approach. In: Lumley C, Walker S, editors. Animal Toxicity Studies: Their Relevance for Man. Lancaster: Quay. 1990;: 71-8.
83. Lumley C. Clinical toxicity: could it have been predicted? Premarketing experience. In: Lumley C, Walker S, editors. Animal Toxicity Studies: Their Relevance for Man. London: Quay. 1990;: 49-56.
84. Spriet-Pourra C, Auriche M. SCRIP Reports: PJB. 1994.
85. Eason CT, Bonner FW, Parke DV. The importance of pharmacokinetic and receptor studies in drug safety evaluation. Regul Toxicol Pharmacol. 1990; 11: 288-307.
86. Igarashi T. The duration of toxicity studies required to support repeated dosing in clinical investigation-A toxicologists opinion. In: C Parkinson NM, C Lumley, SR Walker, editor. CMR Workshop: The Timing of Toxicological Studies to Support Clinical Trials. Boston/UK: Kluwer; 1994;: 67-74.
87. Igarashi T, Nakane S, Kitagawa T. Predictability of clinical adverse reactions of drugs by general pharmacology studies. J Toxicol Sci. 1995; 20: 77-92.
88. Igarashi T, Yabe T, Noda K. Study design and statistical analysis of toxicokinetics: a report of JPMA investigation of case studies. J Toxicol Sci. 1996; 21: 497-504.
89. Weaver JL, Staten D, Swann J, Armstrong G, Bates M, Hastings KL. Detection of systemic hypersensitivity to drugs using standard guinea pig assays. Toxicology. 2003; 193: 203-17. doi:S0300483X03002671 [pii].
90. Willis RC. The Virtual Patient. Modern Drug Discovery. 2003; 6: 35-40.
91. Sankar U. The Delicate Toxicity Balance in Drug Discovery. The Scientist. 2005; 19: 32.
92. Fourches D, Barnes JC, Day NC, Bradley P, Reed JZ, Tropsha A. Cheminformatics analysis of assertions mined from literature that describe drug-induced liver injury in different species. Chem Res Toxicol. 2010; 23: 171-83.
93. Park BK, Boobis A, Clarke S, Goldring CEP, Jones D, Kenna JG, et al. Managing the challenge of chemically reactive metabolites in drug development. Nat Rev Drug Discov. 2011; 10: 292-306.
94. Lin JH. Species similarities and differences in pharmacokinetics. Drug Metab Dispos. 1995; 23: 1008-21.
95. Sietsema WK. The absolute oral bioavailability of selected drugs. Int J Clin Pharmacol Ther Toxicol. 1989; 27: 179-211.
96. Greek R. Animal Models and the Development of an HIV Vaccine. J AIDS Clinic Res. 2012; S8:001.
97. Greek R. Book Review. Zoobiquity: What Animals Can Teach Us About Health and the Science of Healing. Animals. 2012; 2: 559-63.
98. Horrobin DF. Modern biomedical research: an internally self-consistent universe with little contact with medical reality? Nat Rev Drug Discov. 2003; 2: 151-4.
99. Wall RJ, Shani M. Are animal models as good as we think? Theriogenology. 2008; 69: 2-9.
100. Zielinska E. Building a better mouse. The Scientist. 2010; 24: 34-8.
101. Miska D. Biotech's twentieth birthday blues. Nat Rev Drug Discov. 2003; 2: 231-3.
102. Ahn AC, Tewari M, Poon CS, Phillips RS. The limits of reductionism in medicine: could systems biology offer an alternative? PLoS Med. 2006; 3: e208.
103. Krakauer DC, Collins JP, Erwin D, Flack JC, Fontana W, Laubichler MD, et al. The challenges and scope of theoretical biology. J Theor Biol. 2011; 276: 269-76.
104. American Association for the Advancement of Science. Q & A on Evolution and Intelligent Design. Washington DC: American Association for the Advancement of Science. 2011.
105. Van Regenmortel MHV. Basic Research in HIV vaccinology is hampered by reductionist thinking. Frontiers in Immunology. 2012;:3. doi:10.3389/fimmu.2012.00194.
106. Jura J, Wegrzyn P, Koj A. Regulatory mechanisms of gene expression: complexity with elements of deterministic chaos. Acta Biochim Pol. 2006; 53: 1-10. doi:20061177 [pii].
107. Vicsek T. The bigger picture. Nature. 2002; 418: 131.
108. Goodman AF, Bellato CM, Khidr L. The Uncertain Future for Central Dogma. Uncertainty serves as a bridge from determinism and reductionism to a new picture of biology. The Scientist. 2005;: 19.
109. Van Regenmortel M. Reductionism and complexity in molecular biology. Scientists now have the tools to unravel biological complexity and overcome the limitations of reductionism. EMBO Rep. 2004; 5: 1016-20.
110. Csete ME, Doyle JC. Reverse engineering of biological complexity. Science. 2002; 295: 1664-9.
111. Sole R, Goodwin B. Signs of Life: How Complexity Pervades Biology: Basic Books. 2002.
112. Kitano H. Computational systems biology. Nature. 2002; 420: 206-10.
113. Kitano H. Systems biology: a brief overview. Science. 2002; 295: 1662-4.
114. Kauffman SA. The Origins of Order: Self-Organization and Selection in Evolution. Oxford University Press. 1993.
115. Ottino JM. Engineering complex systems. Nature. 2004; 427: 399.
116. Alm E, Arkin AP. Biological networks. Curr Opin Struct Biol. 2003; 13: 193-202.
117. Goodwin B. How the Leopard Changed Its Spots: The Evolution of Complexity. Princeton: Princeton University Press. 2001.
118. Van Regenmortel M. Reductionism and the search for structure-function relationships in antibody molecules. J Mol Recognit. 2002; 15: 240-7. doi:10.1002/jmr.584.
119. van Regenmortel M. Pitfalls of Reductionism in Immunology. In: van Regenmortel M, Hull DL, editors. Promises and Limits of Reductionism in the Biomedical Sciences. Chichester: John Wiley & Sons LTD; 2002;: 47-66.
120. van Regenmortel M. Biological complexity emerges from the ashes of genetic reductionism. Journal of Molecular Recognition. 2004; 17: 145-8.
121. Cairns-Smith AG. Seven Clues to the Origin of Life: A Scientific Detective Story. Cambridge: Cambridge University Press. 1986.
122. Monte J, Liu M, Sheya A, Kitami T. Definitions, Measures, and Models of Robustness in Gene Regulatory Network. Report of research work for CSSS05. 2005.
123. Morowitz HJ. The Emergence of Everything: How the World Became Complex. Oxford: Oxford University Press. 2002.
124. Novikoff AB. The Concept of Integrative Levels and Biology. Science. 1945; 101: 209-15.
125. Van Regenmortel MH, Hull DL. Promises and Limits of Reductionism in the Biomedical Sciences (Catalysts for Fine Chemical Synthesis). West Sussex: Wiley. 2002.
126. Woodger JH. Biological Principles. New York: Humanities Press; 1967.
127. Kastens KA, Manduca CA, Cervato C, Frodeman R, Goodwin C, Liben LS, et al. How Geoscientists Think and Learn. Eos Trans AGU. 2009;: 90. doi:10.1029/2009eo310001.
128. Greek R, Rice MJ. Animal models and conserved processes. Theoretical Biology and Medical Modelling. 2012;: 9. doi:10.1186/1742-4682-9-40.
129. LaFollette H, Shanks N. Animal models in biomedical research: some epistemological worries. Public Aff Q. 1993; 7: 113-30.
130. LaFollette H, Shanks N. Animal Experimentation: The Legacy of Claude Bernard. International Studies in the Philosophy of Science. 1994; 8: 195-210.
131. LaFollette H, Shanks N. Two Models of Models in Biomedical Research. Philosophical Quarterly 1995; 45: 141-60.
132. Mazzocchi F. Complexity and the reductionism-holism debate in systems biology. Wiley Interdiscip Rev Syst Biol Med. 2012; 4: 413-27. doi:10.1002/wsbm.1181.
133. Morange M. A successful form for reductionism. The Biochemist. 2001; 23: 37-9.
134. Pearson H. Surviving a knockout blow. Nature. 2002; 415: 8-9. doi:10.1038/415008a415008a [pii].
135. Willyard C. HIV gender clues emerge. Nat Med. 2009; 15: 830. doi:nm0809-830b [pii]10.1038/nm0809-830b.
136. Holden C. Sex and the suffering brain. Science. 2005; 308: 1574. doi:308/5728/1574 [pii]10.1126/science.308.5728.1574.
137. Kaiser J. Gender in the pharmacy: does it matter? Science. 2005; 308: 1572. doi:308/5728/1572 [pii]10.1126/science.308.5728.1572.
138. Simon V. Wanted: women in clinical trials. Science. 2005; 308: 1517. doi:308/5728/1517 [pii]10.1126/science.1115616.
139. Wald C, Wu C. Of Mice and Women: The Bias in Animal Models. Science. 2010; 327: 1571-2.
140. Klein S, Huber S. Sex differences in susceptibility to viral infection. In: Klein S, Roberts C, editors. Sex hormones and immunity to infection. Berlin: Springer-Verlag; 2010;: 93-122.
141. Cheung DS, Warman ML, Mulliken JB. Hemangioma in twins. Ann Plast Surg. 1997; 38: 269-74.
142. Gregor Z, Joffe L. Senile macular changes in the black African. Br J Ophthalmol. 1978; 62: 547-50.
143. Stamer UM, Stuber F. The pharmacogenetics of analgesia. Expert Opin Pharmacother. 2007; 8: 2235-45. doi:10.1517/14656566.8.14.2235.
144. Wilke RA, Dolan ME. Genetics and Variable Drug Response. JAMA: The Journal of the American Medical Association. 2011; 306: 306-7. doi:10.1001/jama.2011.998.
145. Kopp JB, Nelson GW, Sampath K, Johnson RC, Genovese G, An P, et al. APOL1 Genetic Variants in Focal Segmental Glomerulosclerosis and HIV-Associated Nephropathy. Journal of the American Society of Nephrology. 2011; 22: 2129-37. doi:10.1681/asn.2011040388.
146. Haiman CA, Stram DO, Wilkens LR, Pike MC, Kolonel LN, Henderson BE, et al. Ethnic and racial differences in the smoking-related risk of lung cancer. N Engl J Med. 2006; 354: 333-42. doi:354/4/333 [pii]10.1056/NEJMoa033250.
147. Spielman RS, Bastone LA, Burdick JT, Morley M, Ewens WJ, Cheung VG. Common genetic variants account for differences in gene expression among ethnic groups. Nat Genet. 2007; 39: 226-31. doi:ng1955 [pii]10.1038/ng1955.
148. Couzin J. Cancer research. Probing the roots of race and cancer. Science. 2007; 315: 592-4. doi:315/5812/592 [pii]10.1126/science.315.5812.592.
149. Kalow W. Interethnic variation of drug metabolism. Trends in Pharmacological Sciences. 1991; 12: 102-7.
150. Bruder CE, Piotrowski A, Gijsbers AA, Andersson R, Erickson S, de Stahl TD, et al. Phenotypically concordant and discordant monozygotic twins display different DNA copy-number-variation profiles. Am J Hum Genet. 2008; 82: 763-71. doi:S0002-9297(08)00102-X [pii]10.1016/j.ajhg.2007.12.011.
151. Javierre BM, Fernandez AF, Richter J, Al-Shahrour F, Martin-Subero JI, Rodriguez-Ubreva J, et al. Changes in the pattern of DNA methylation associate with twin discordance in systemic lupus erythematosus. Genome Research. 2010; 20: 170-9. doi:10.1101/gr.100289.109.
152. Wong AH, Gottesman II, Petronis A. Phenotypic differences in genetically identical organisms: the epigenetic perspective. Hum Mol Genet. 2005; 1: R11-8. doi:14/suppl_1/R11 [pii]10.1093/hmg/ddi116.
153. Dempster EL, Pidsley R, Schalkwyk LC, Owens S, Georgiades A, Kane F, et al. Disease-associated epigenetic changes in monozygotic twins discordant for schizophrenia and bipolar disorder. Human molecular genetics. 2011; 20: 4786-96. doi:10.1093/hmg/ddr416.
154. Fraga MF, Ballestar E, Paz MF, Ropero S, Setien F, Ballestar ML, et al. Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci U S A. 2005; 102: 10604-9. doi:0500398102 [pii]10.1073/pnas.0500398102.
155. Williams G. Chaos Theory Tamed. Washington, DC: Joseph Henry Press. 1997.
156. Bickel PJ, Buhlmann P. What is a linear process? Proceedings of the National Academy of Sciences of the United States of America. 1996; 93: 12128-31.
157. Lippman N, Stein KM, Lerman BB. Nonlinear forecasting and the dynamics of cardiac rhythm. J Electrocardiol. 1995; 28 Suppl: 65-70.
158. Rosen R. Essays on Life Itself. New York: Columbia University Press; 1998.
159. Koch C. Systems biology. Modular biological complexity. Science. 2012; 337: 531-2.
160. Pelak K, Need AC, Fellay J, Shianna KV, Feng S, Urban TJ, et al. Copy number variation of KIR genes influences HIV-1 control. PLoS biology. 2011; 9: e1001208.
161. Mittelstrass K, Ried JS, Yu Z, Krumsiek J, Gieger C, Prehn C, et al. Discovery of sexual dimorphisms in metabolic and genetic biomarkers. PLoS genetics. 2011; 7: e1002215.
162. Yucesoy B, Johnson VJ, Fluharty K, Kashon ML, Slaven JE, Wilson NW, et al. Influence of cytokine gene variations on immunization to childhood vaccines. Vaccine. 2009; 27: 6991-7.
163. King C. Personalised vaccines could protect all children. New Scientist. 2009;: 11.
164. Sivakumaran S, Agakov F, Theodoratou E, Prendergast JG, Zgaga L, Manolio T, et al. Abundant pleiotropy in human complex diseases and traits. American journal of human genetics. 2011; 89: 607-18.
165. Gustincich S, Sandelin A, Plessy C, Katayama S, Simone R, Lazarevic D, et al. The complexity of the mammalian transcriptome. J Physiol. 2006; 575: 321-32.
166. Burgess DJ. Evo-devo: Hidden rewiring comes to light. Nat Rev Genet. 2011; 12: 586-7.
167. Lowe CB, Kellis M, Siepel A, Raney BJ, Clamp M, Salama SR, et al. Three periods of regulatory innovation during vertebrate evolution. Science. 2011; 333: 1019-24.
168. Pai AA, Bell JT, Marioni JC, Pritchard JK, Gilad Y. A Genome-Wide Study of DNA Methylation Patterns and Gene Expression Levels in Multiple Human and Chimpanzee Tissues. PLoS Genet. 2011; 7: e1001316.
169. Morley M, Molony CM, Weber TM, Devlin JL, Ewens KG, Spielman RS, et al. Genetic analysis of genome-wide variation in human gene expression. Nature. 2004; 430: 743-7.
170. Rosenberg NA, Pritchard JK, Weber JL, Cann HM, Kidd KK, Zhivotovsky LA, et al. Genetic structure of human populations. Science. 2002; 298: 2381-5.
171. Storey JD, Madeoy J, Strout JL, Wurfel M, Ronald J, Akey JM. Gene-expression variation within and among human populations. Am J Hum Genet. 2007; 80: 502-9.
172. Zhang W, Duan S, Kistner EO, Bleibel WK, Huang RS, Clark TA, et al. Evaluation of genetic variation contributing to differences in gene expression between populations. Am J Hum Genet. 2008; 82: 631-40.
173. Pritchard C, Coil D, Hawley S, Hsu L, Nelson PS. The contributions of normal variation and genetic background to mammalian gene expression. Genome Biol. 2006; 7: R26.
174. Rifkin SA, Kim J, White KP. Evolution of gene expression in the Drosophila melanogaster subgroup. Nat Genet. 2003; 33: 138-44.
175. Sandberg R, Yasuda R, Pankratz DG, Carter TA, Del Rio JA, Wodicka L, et al. Regional and strain-specific gene expression mapping in the adult mouse brain. Proc Natl Acad Sci U S A. 2000; 97: 11038-43.
176. Suzuki Y, Nakayama M. Differential profiles of genes expressed in neonatal brain of 129X1/SvJ and C57BL/6J mice: A database to aid in analyzing DNA microarrays using nonisogenic gene-targeted mice. DNA Res. 2003; 10: 263-75.
177. Somel M, Liu X, Tang L, Yan Z, Hu H, Guo S, et al. MicroRNA-Driven Developmental Remodeling in the Brain Distinguishes Humans from Other Primates. PLoS Biol. 2011; 9: e1001214.
178. Puente XS, Velasco G, Gutierrez-Fernandez A, Bertranpetit J, King MC, Lopez-Otin C. Comparative analysis of cancer genes in the human and chimpanzee genomes. BMC Genomics. 2006; 7: 15.
179. Varki NM, Strobert E, Dick EJ, Benirschke K, Varki A. Biomedical Differences Between Human and Nonhuman Hominids: Potential Roles for Uniquely Human Aspects of Sialic Acid Biology. Annual Review of Pathology: Mechanisms of Disease. 2011; 6: 365-93.
180. Walker CM. Comparative features of hepatitis C virus infection in humans and chimpanzees. Springer Semin Immunopathol. 1997; 19: 85-98.
181. Gagneux P, Muchmore EA. The chimpanzee model: contributions and considerations for studies of hepatitis B virus. Methods in molecular medicine. 2004; 96: 289-318.
182. Bettauer RH. Chimpanzees in hepatitis C virus research: 1998-2007. Journal of Medical Primatology. 2010; 39: 9-23.
183. Caldwell J. Problems and opportunities in toxicity testing arising from species differences in xenobiotic metabolism. Toxicology letters. 1992;: 64-65.
184. Festing MF. Rat Genetics and Toxicology. In: National Research Council, editor. Microbial Status and Genetic Evaluation of Mice and Rats: Proceedings of the 1999 US/Japan Conference: ILAR. 2000;: 97.
185. Roses AD. Pharmacogenetics and the practice of medicine. Nature. 2000; 405: 857-65. doi:10.1038/35015728.
186. Willyard C. Blue's clues. Nat Med. 2007; 13: 1272-3.
187. Weinshilboum R. Inheritance and drug response. N Engl J Med. 2003; 348: 529-37.
188. Bates S. Progress towards personalized medicine. Drug Discovery Today. 2010; 15: 115-20.
189. Bhathena A, Spear BB. Pharmacogenetics: improving drug and dose selection. Curr Opin Pharmacol. 2008; 8: 639-46.
190. Blair E. Predictive tests and personalised medicine. Drug Discovery World. 2009;: 27-31.
191. Dolgin E. Big pharma moves from 'blockbusters' to 'niche busters'. Nat Med. 2010; 16: 837.
192. Flaherty KT, Puzanov I, Kim KB, Ribas A, McArthur GA, Sosman JA, et al. Inhibition of mutated, activated BRAF in metastatic melanoma. N Engl J Med. 2010; 363: 809-19. doi:10.1056/NEJMoa1002011.
193. Froehlich TE, Epstein JN, Nick TG, Melguizo Castro MS, Stein MA, Brinkman WB, et al. Pharmacogenetic Predictors of Methylphenidate Dose-Response in Attention-Deficit/Hyperactivity Disorder. Journal of the American Academy of Child and Adolescent Psychiatry. 2011; 50: 1129-39.e2.
194. Hudson KL. Genomics, Health Care, and Society. New England Journal of Medicine. 2011; 365: 1033-41.
195. Hughes AR, Spreen WR, Mosteller M, Warren LL, Lai EH, Brothers CH, et al. Pharmacogenetics of hypersensitivity to abacavir: from PGx hypothesis toconfirmation to clinical utility. Pharmacogenomics J. 2008; 8: 365-74. doi:tpj20083 [pii]10.1038/tpj.2008.3.
196. Serrano D, Lazzeroni M, Zambon CF, Macis D, Maisonneuve P, Johansson H, et al. Efficacy of tamoxifen based on cytochrome P450 2D6, CYP2C19 and SULT1A1 genotype in the Italian Tamoxifen Prevention Trial. Pharmacogenomics J. 2011; 11: 100-7.
197. Wang D, Guo Y, Wrighton SA, Cooke GE, Sadee W. Intronic polymorphism in CYP3A4 affects hepatic expression and response to statin drugs. Pharmacogenomics J. 2011; 11: 274-86.
198. Canto JG, Rogers WJ, Goldberg RJ, Peterson ED, Wenger NK, Vaccarino V, et al. Association of Age and Sex With Myocardial Infarction Symptom Presentation and In-Hospital Mortality. JAMA: The Journal of the American Medical Association. 2012; 307: 813-22.
199. Darlison MG, Pahal I, Thode C. Consequences of the evolution of the GABA(A) receptor gene family. Cell Mol Neurobiol. 2005; 25: 607-24. doi:10.1007/s10571-005-4004-4.
200. Geerts H. Of mice and men: bridging the translational disconnect in CNS drug discovery. CNS Drugs. 2009; 23: 915-26.
201. Jankovic J, Noebels JL. Genetic mouse models of essential tremor: are they essential? J Clin Invest. 2005; 115: 584-6.
202. Kieburtz K, Olanow CW. Translational experimental therapeutics: The translation of laboratory-based discovery into disease-related therapy. Mt Sinai J Med. 2007; 74: 7-14.
203. Liu Z, Maas K, Aune TM. Comparison of differentially expressed genes in T lymphocytes between human autoimmune disease and murine models of autoimmune disease. Clin Immunol. 2004; 112: 225-30.
204. Miklos GLG. The human cancer genome project--one more misstep in the war on cancer. Nat Biotechnol. 2005; 23: 535-7.
205. PMC. Personalized Medicine. Personalized Medicine Coalition. 2006.
206. Personalized Medicine Coalition. The Case for Personalized Medicine. Personalized Medicine Coalition 2011.
207. Jørgensen JT. A challenging drug development process in the era of personalized medicine. Drug Discovery Today. 2011; 16: 891-7.
208. Pirmohamed M. Pharmacogenetics: past, present and future. Drug Discovery Today. 2011; 16: 852-61.
209. Stamer UM, Stuber F. Genetic factors in pain and its treatment. Current opinion in anaesthesiology. 2007; 20: 478-84. doi:10.1097/ACO.0b013e3282ef6b2c.
210. Gura T. Cancer Models: Systems for identifying new drugs are often faulty. Science. 1997; 278: 1041-2.
211. Editorial. The time is now. Nat Rev Drug Discov. 2005; 4: 613.
212. Ellis LM, Fidler IJ. Finding the tumor copycat. Therapy fails, patients don't. Nat Med. 2010; 16: 974-5. doi:nm0910-974 [pii]10.1038/nm0910-974.
213. Fliri AF, Loging WT, Thadeio PF, Volkmann RA. Biological spectra analysis: Linking biological activity profiles to molecular structure. Proc Natl Acad Sci U S A. 2005; 102: 261-6.
214. Marshall E. Gene therapy on trial. Science. 2000; 288: 951-7.
215. Collins FS. Reengineering Translational Science: The Time Is Right. Science Translational Medicine. 2011; 3: 90cm17.
216. Reuters. US to develop chip that tests if a drug is toxic. Reuters. 2011.
217. Neuzil P, Giselbrecht S, Lange K, Huang TJ, Manz A. Revisiting lab-on-a-chip technology for drug discovery. Nature Reviews Drug Discovery. 2012; 11: 620-32.
218. Johnson JI, Decker S, Zaharevitz D, Rubinstein LV, Venditti JM, Schepartz S, et al. Relationships between drug activity in NCI preclinical in vitro and in vivo models and early clinical trials. Br J Cancer. 2001; 84: 1424-31.
219. Suggitt M, Bibby MC. 50 years of preclinical anticancer drug screening: empirical to target-driven approaches. Clinical cancer research: an official journal of the American Association for Cancer Research. 2005; 11: 971-81.
220. Cook N, Jodrell DI, Tuveson DA. Predictive in vivo animal models and translation to clinical trials. Drug Discovery Today. 2012; 17: 253-60.
221. Seidle T. Opportunities and Barriers to the Replacement of Animals in Acute Systemic Toxicity Testing. AltTox.org. 2007.
222. NC3Rs. News: Challenging the requirement for acute toxicity studies - workshop report published. 2007.
223. Chapman K, Robinson S. Challenging the requirement for acute toxicity studies in the development of new medicines. London: NC3Rs; 2007.
224. Sharp PA, Langer R. Promoting Convergence in Biomedical Science. Science. 2011; 333: 527.