An analysis of the Bateson Review of research using nonhuman primates

References

• Hau J, Schapiro S. Non-human primates in biomedical research. Scand J Lab Anim Sci. 2006;33(1):9–12.
   Web of Science ®Google Scholar
• Carlsson HE, Schapiro SJ, Farah I, Hau J. Use of primates in research: a global overview. Am J Primatol. 2004;63(4):225–237.
   PubMed Web of Science ®Google Scholar
• Honess PE, Johnson PJ, Wolfensohn SE. A study of behavioural responses of non-human primates to air transport and re-housing. Lab Anim. 2004;38(2):119–132.
   Google Scholar
• Malik I. Consequences of export and trapping of monkeys. Primate Rep. 1992;34:5–12.
   Google Scholar
• Southwick C, Siddiqi M. Status, conservation and management of primates in India. In: Gupta AK, editor. Non-Human Primates of India, ENVIS Bulletin: Wildlife and Protected Areas. Vol 1(1). Dehradun: Wildl Inst India; 2001:81–91.
   Google Scholar
• Gad S. Preface. In: Gad S, editor. Animal Models in Toxicology. Boca Rotan: CRC Press; 2007:1–18.
   Google Scholar
• Thirlway H. US and UK primate imports. International Primate Protection League (IPPL) News. 2009;36(1):2009;14–16. Available from: http://www.ippl.org/newsletter/2000s/IPPL-News-May-2009.pdf. Accessed September 3, 2011.
   Google Scholar
• IPPL. US primate imports spike [web page on the Internet]. Summerville, SC: IPPL; 2007. Available from: https://secure.ippl.org/newsletter/2000s/101_v34_n1_2007-2004.pdf#page=8 (go to page 8). Accessed October 27, 2011.
   Google Scholar
• “Sharon.” US 2010 primate imports increase slightly over 2009 figures. [web page on the Internet]. Summerville, SC: IPPL; September 16, 2011. Available from: https://secure.ippl.org/gibbon-wp/u-s-2010-primate-imports-increase-slightly/. Accessed September 3, 2011.
   Google Scholar
• Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES). Experts concerned about level of trade in snake skins used in luxury products: long-tailed macaque used in biomedical research, sturgeons, seahorses and shark-fishing regulations also under review [press release]. Geneva: CITES; July 22, 2011. Available from: http://www.cites.org/eng/news/press/2011/20110722_AC25.php. Accessed August 30, 2011.
   Google Scholar
• Shanks N, Greek R. Animal Models in Light of Evolution. Boca Raton: Brown Walker; 2009.
   Google Scholar
• Shanks N, Greek R, Greek J. Are animal models predictive for humans? Philos Ethics Humanit Med. 2009;4(1):2.
   PubMedGoogle Scholar
• Scientific Committee on Health and Environmental Risks (SCHER). The Need for Non-Human Primates in Biomedical Research, Production and Testing of Products and Devices. Brussels: European Commission; 2009. Available from: http://ec.europa.eu/environment/chemicals/lab_animals/pdf/scher_o_110.pdf. Accessed August 30, 2011.
   Google Scholar
• Greek R, Greek J. Is the use of sentient animals in basic research justifiable? Philos Ethics Humanit Med. 2010;5:14.
   Google Scholar
• Greek R, Pound P. Animal studies and HIV research. BMJ. 2002; 324(7331):236–237.
   Google Scholar
• Greek R, Shanks N. FAQs About the Use of Animals in Science: A Handbook for the Scientifically Perplexed. New York: University Press of America; 2009.
   Google Scholar
• Shanks N, Greek R, Nobis N, Greek J. Animals and medicine: do animal experiments predict human response? Skeptic. 2007;13(3):44–51.
   Google Scholar
• Knight A. The poor contribution of chimpanzee experiments to biomedical progress. J Appl Anim Welf Sci. 2007;10(4):281–308.
   PubMed Web of Science ®Google Scholar
• Knight A. The beginning of the end for chimpanzee experiments? Philos Ethics Humanit Med. 2008;3:16.
   PubMedGoogle Scholar
• Knight A, Bailey J, Balcombe J. Animal carcinogenicity studies: 1. Poor human predictivity. Altern Lab Anim. 2006;34(1):19–27.
   PubMed Web of Science ®Google Scholar
• Bateson P. Review of Research Using Non-Human Primates. 2011. Available from: http://www.bbsrc.ac.uk/web/FILES/Reviews/review-research-using-nhps.pdf. Accessed October 21, 2011.
   Google Scholar
• Weatherall D. The Use of Nonhuman Primates in Research. London: Academy of Medical Sciences; 2006.
   Google Scholar
• The Cochrane Collaboration. Cochrane Handbook for Systematic Reviews of Interventions. Oxford: The Cochrane Collaboration; 2011. Available from: http://www.cochrane.org/training/cochrane-handbook. Accessed August 30, 2011.
   Google Scholar
• Van Buskirk NE. The review article in MEDLINE: ambiguity of definition and implications for online searchers. Bull Med Libr Assoc. 1984;72(4):349–352. Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC227511/pdf/mlab00064-0039.pdf. Accessed August 30, 2011.
   Google Scholar
• Leydesdorff L, Opthof T. Scopus’s source normalized impact per paper (SNIP) versus a journal impact factor based on fractional counting of citations. J Am Soc Inf Sci Technol. 2010;61(11):2365–2369.
   Web of Science ®Google Scholar
• Honey RC, Bateson P. Stimulus comparison and perceptual learning: further evidence and evaluation from an imprinting procedure. Q J Exp Psychol B. 1996;49(3):259–269.
   Google Scholar
• Honey RC, Bateson P, Horn G. The role of stimulus comparison in perceptual learning: an investigation with the domestic chick. Q J Exp Psychol B. Feb 1994;47(1):83–103.
   Google Scholar
• McCabe BJ, Cipolla-Neto J, Horn G, Bateson P. Amnesic effects of bilateral lesions placed in the hyperstriatum ventrale of the chick after imprinting. Exp Brain Res. 1982;48(1):13–21.
   Web of Science ®Google Scholar
• McCabe BJ, Horn G, Bateson PP. Effects of restricted lesions of the chick forebrain on the acquisition of filial preferences during imprinting. Brain Res. 1981;205(1):29–37.
   Web of Science ®Google Scholar
• Bradley P, Horn G, Bateson P. Imprinting. An electron microscopic study of chick hyperstriatum ventrale. Exp Brain Res. 1981;41(2): 115–120.
   Web of Science ®Google Scholar
• Horn G, McCabe BJ, Bateson PP. An autoradiographic study of the chick brain after imprinting. Brain Res. 1979;168(2): 361–373.
   Web of Science ®Google Scholar
• Bateson PP, Horn G, McCabe BJ Imprinting: the effect of partial ablation of the medial hyperstriatum ventrale of the chick [proceedings]. J Physiol. 1978;285:23P.
   Web of Science ®Google Scholar
• Bateson PP, Horn G, McCabe BJ Imprinting and the incorporation of uracil in the chick brain: a radioautographic study [proceedings]. J Physiol. 1978;275:70P.
   Google Scholar
• Hambley JW, Haywood J, Rose SP, Bateson PP. Effects of imprinting on lysine uptake and incorporation into protein in chick brain. J Neurobiol. 1977;8(2):109–118.
   Google Scholar
• Haywood J, Rose SP, Bateson P. Changes in chick brain RNA polymerase associated with an imprinting procedure. Brain Res. 1975;92(2):227–235.
   Web of Science ®Google Scholar
• Bateson PP, Horn G, Rose SP. Imprinting: correlations between behaviour and incorporation of (14-C) uracil into chick brain. Brain Res. 1975;84(2):207–220.
   Web of Science ®Google Scholar
• Bateson PP, Rose SP, Horn G. Imprinting: lasting effects on uracil incorporation into chick brain. Science. 1973;181(99):576–578.
   Google Scholar
• Bateson PP, Horn G, Rose SP. Effects of early experience on regional incorporation of precursors into RNA and protein in the chick brain. Brain Res. 1972;39(2):449–465.
   Web of Science ®Google Scholar
• Horn G, Horn AL, Bateson PP, Rose SP. Effects of imprinting on uracil incorporation into brain RNA in the “split-brain” chick. Nature. 1971;229(5280):131–132.
   Web of Science ®Google Scholar
• Rushworth MF, Johansen-Berg H, Young SA. Parietal cortex and spatial-postural transformation during arm movements. J Neurophysiol. 1998;79(1):478–482.
   Web of Science ®Google Scholar
• Mellanby J, Johansen-Berg H, Leyland R, Milward AJ. The effects of tetanus toxin-induced limbic epilepsy on the exploratory response to novelty in the rat. Epilepsia. 1999;40(8):1058–1061.
   Web of Science ®Google Scholar
• Mars RB, Jbabdi S, Sallet J, et al. Diffusion-weighted imaging tractography-based parcellation of the human parietal cortex and comparison with human and macaque resting-state functional connectivity. J Neurosci. 2011;31(11):4087–4100.
   Web of Science ®Google Scholar
• Klein JC, Rushworth MF, Behrens TE, et al. Topography of connections between human prefrontal cortex and mediodorsal thalamus studied with diffusion tractography. Neuroimage. 2010;51(2):555–564.
   PubMed Web of Science ®Google Scholar
• Croxson PL, Johansen-Berg H, Behrens TE, et al. Quantitative investigation of connections of the prefrontal cortex in the human and macaque using probabilistic diffusion tractography. J Neurosci. 2005;25(39):8854–8866.
   PubMed Web of Science ®Google Scholar
• Freidlin RZ, Ozarslan E, Komlosh ME, et al. Parsimonious model selection for tissue segmentation and classification applications: a study using simulated and experimental DTI data. IEEE Trans Med Imaging. 2007;26(11):1576–1584.
   Web of Science ®Google Scholar
• Pomeroy IM, Jordan EK, Frank JA, Matthews PM, Esiri MM. Diffuse cortical atrophy in a marmoset model of multiple sclerosis. Neurosci Lett. 2008;437(2):121–124.
   Web of Science ®Google Scholar
• Pomeroy IM, Matthews PM, Frank JA, Jordan EK, Esiri MM. Demyelinated neocortical lesions in marmoset autoimmune encephalomyelitis mimic those in multiple sclerosis. Brain. 2005;128 (Pt 11):2713–2721.
   PubMed Web of Science ®Google Scholar
• Ramnani N, Behrens TE, Johansen-Berg H, et al. The evolution of prefrontal inputs to the cortico-pontine system: diffusion imaging evidence from Macaque monkeys and humans. Cereb Cortex. 2006;16(6):811–818.
   Web of Science ®Google Scholar
• Perrett DI, Smith PA, Mistlin AJ, et al. Visual analysis of body movements by neurones in the temporal cortex of the macaque monkey: a preliminary report. Behav Brain Res. 1985;16(2–3):153–170.
   Web of Science ®Google Scholar
• Perrett DI, Smith PA, Potter DD, et al. Visual cells in the temporal cortex sensitive to face view and gaze direction. Proc R Soc Lond B Biol Sci. 1985;223(1232):293–317.
   Web of Science ®Google Scholar
• Cranage M, Sharpe S, Herrera C, et al. Prevention of SIV rectal transmission and priming of T cell responses in macaques after local pre-exposure application of tenofovir gel. PLoS Med. 2008;5(8):e157; discussion e157.
   PubMed Web of Science ®Google Scholar
• Cranage MP, Fraser CA, Cope A, et al. Antibody responses after intravaginal immunisation with trimeric HIV-1 CN54 clade C gp140 in Carbopol gel are augmented by systemic priming or boosting with an adjuvanted formulation. Vaccine. 2011;29(7):1421–1430.
   Web of Science ®Google Scholar
• Curran RM, Donnelly L, Morrow RJ, et al. Vaginal delivery of the recombinant HIV-1 clade-C trimeric gp140 envelope protein CN54gp140 within novel rheologically structured vehicles elicits specific immune responses. Vaccine. 2009;27(48):6791–6798.
   Web of Science ®Google Scholar
• Veazey RS, Klasse PJ, Schader SM, et al. Protection of macaques from vaginal SHIV challenge by vaginally delivered inhibitors of virus-cell fusion. Nature. 2005;438(7064):99–102.
   Web of Science ®Google Scholar
• Wallace GS, Cheng-Mayer C, Schito ML, et al. Human immunodeficiency virus type 1 nucleocapsid inhibitors impede trans infection in cellular and explant models and protect nonhuman primates from infection. J Virol. 2009;83(18):9175–9182.
   Web of Science ®Google Scholar
• Wegmann F, Krashias G, Luhn K, et al. A novel strategy for inducing enhanced mucosal HIV-1 antibody responses in an anti-inflammatory environment. PLoS ONE. 2011;6(1):e15861.
   Web of Science ®Google Scholar
• Crano WD. Attitude strength and vested interest. In: Petty RE, Krosnick JA, editors. Attitude Strength: Antecedents and Consequences. Mahwah, NJ: Erlbaum; 1995:131–158.
   Google Scholar
• Biotechnology and Biological Sciences Research Council (BBSRC). Biomedical research funders respond to the Review of Research Using Non-Human Primates [web page on the Internet]. Swindon: BBSRC; July 27, 2011. Available from: http://www.bbsrc.ac.uk/news/policy/2011/110727-pr-response-review-research-using-nhps.aspx. Accessed August 31, 2011.
   Google Scholar
• politics.co.uk. RSPCA reaction to the review of using non-human primates. politics.co.uk; July 27, 2011. Available from: http://www.politics.co.uk/opinion-formers/rspca-royal-society-for-the-preventionof-cruelty-to-animals/article/rspca-reaction-to-the-review-of-usingnon-human-primates. Accessed October 27, 2011.
   Google Scholar
• Dr Hadwen Trust for Humane Research. Dr Hadwen Trust welcomes Bateson report but calls for annual review [press release]. Hitchin: Dr Hadwen Trust for Humane Research; July 29, 2011. Available from: http://www.drhadwentrust.org/downloads/press-releases/DHTpressrelease-responsetoBatesonnhpreview-29.07.11.pdf. Accessed August 31, 2011.
   Google Scholar
• Jha A. One in ten research projects using monkeys has no benefit, finds review. Guardian. July 27, 2011. Available from: http://www.guardian.co.uk/science/2011/jul/27/research-projects-monkeys-benefit. Accessed August 31, 2011.
   Google Scholar
• Callaway E. Primate research gets provisional thumbs-up in UK review. newsblog. July 27, 2011. Available from: http://blogs.nature.com/news/2011/07/primate_research_gets_provisio.html. Accessed August 31, 2011.
   Google Scholar
• Organisation for Economic Cooperation and Development (OECD). The Measurement of Scientific and Technical Activities: Proposed Standard Practice for Surveys of Research and Development. Paris: OECD; 1963.
   Google Scholar
• Carmichael M, Begley S. Desperately seeking cures. Newsweek. May 14, 2010. Available from: http://www.newsweek.com/id/238078?obref=obinsite. Accessed May 31, 2010.
   Google Scholar
• Editorial. Hope in translation. Nature. 2010;467(7315):499.
   Web of Science ®Google Scholar
• Rosenberg RN. Translating biomedical research to the bedside: a national crisis and a call to action. JAMA. 2003;289(10): 1305–1306.
   PubMed Web of Science ®Google Scholar
• Pound P, Ebrahim S, Sandercock P, Bracken MB, Roberts I. Where is the evidence that animal research benefits humans? BMJ. 2004;328(7438):514–517.
   PubMed Web of Science ®Google Scholar
• Ioannidis JP. Materializing research promises: opportunities, priorities and conflicts in translational medicine. J Transl Med. 2004;2(1):5.
   PubMedGoogle Scholar
• Begley S. Coddling human guinea pigs. Newsweek. 2008;152 (7–8):14.
   Google Scholar
• Steinman R, Szalavitz M. Patients have been too patient with basic research. Cerebrum. 2002;4:4.
   Google Scholar
• Editorial. Cancer drugs: remedy required. Nat Med. 2011;17(3): 231–231.
   Web of Science ®Google Scholar
• Contopoulos-Ioannidis DG, Ntzani E, Ioannidis JP. Translation of highly promising basic science research into clinical applications. Am J Med. 2003;114(6):477–484.
   Web of Science ®Google Scholar
• Crowley WFJr. Translation of basic research into useful treatments: how often does it occur? Am J Med. 2003;114(6):503–505.
   Web of Science ®Google Scholar
• Butler D. Translational research: crossing the valley of death. Nature. 2008;453(7197):840–842.
   PubMed Web of Science ®Google Scholar
• Ledford H. Translational research: the full cycle. Nature. 2008;453(7197): 843–845.
   PubMed Web of Science ®Google Scholar
• Marincola FM. In support of descriptive studies; relevance to translational research. J Transl Med. 2007;5:21.
   PubMed Web of Science ®Google Scholar
• Duyk G. Attrition and translation. Science. 2003;302(5645):603–605.
   Web of Science ®Google Scholar
• Rothwell PM. Funding for practice-oriented clinical research. Lancet. 2006;368(9532):262–266.
   Web of Science ®Google Scholar
• Rothwell PM. Medical academia is failing patients and clinicians. BMJ. 2006;332(7546):863–864.
   Google Scholar
• Fenster A. A TRENDS guide to imaging technologies. Trends Biotechnol. 2002;20(8):S1–S2.
   Web of Science ®Google Scholar
• Fuchs VR, Sox HCJr. Physicians’ views of the relative importance of thirty medical innovations. Health Aff (Millwood). 2001;20(5): 30–42.
   Web of Science ®Google Scholar
• Grant J, Cottrell R, Cluzeau F, Fawcett G. Evaluating “payback” on biomedical research from papers cited in clinical guidelines: applied bibliometric study. BMJ. 2000;320(7242):1107–1111.
   Google Scholar
• Grant J, Green L, Mason B. From Bedside to Bench: Comroe and Dripps revisited. Health Economics Research Group research report. Middlesex: Brunel University; Aug 2003.
   Google Scholar
• Grant J, Green L, Mason B. Basic research and health: a reassessment of the scientific basis for the support of biomedical science. Res Eval. 2003;12(3):217–224.
   Web of Science ®Google Scholar
• Grant J, Hanney S, Buxton M. Academic medicine: time for reinvention: research needs researching. BMJ. 2004;328(7430):48; discussion 49.
   Google Scholar
• Comroe JHJr, Dripps RD. Scientific basis for the support of biomedical science. Science. 1976;192(4235):105–111.
   Web of Science ®Google Scholar
• Smith R. Comroe and Dripps revisited. Br Med J (Clin Res Ed). 1987;295(6610):1404–1407.
   Google Scholar
• Cushman DW, Ondetti MA. Design of angiotensin converting enzyme inhibitors. Nat Med. 1999;5(10):1110–1113.
   PubMed Web of Science ®Google Scholar
• Lindl T, Voelkel M, Kolar R. Animal experiments in biomedical research. An evaluation of the clinical relevance of approved animal experimental projects. ALTEX. 2005;22(3):143–151.
   Google Scholar
• Hackam DG, Redelmeier DA. Translation of research evidence from animals to humans. JAMA. 2006;296(14):1731–1732.
   PubMed Web of Science ®Google Scholar
• Kaste M. Use of animal models has not contributed to development of acute stroke therapies: pro. Stroke. 2005;36(10):2323–2324.
   Web of Science ®Google Scholar
• Johnston SC. Translation: case study in failure. Ann Neurol. 2006;59(3): 447–448.
   Web of Science ®Google Scholar
• Dennis C. Cancer: off by a whisker. Nature. 2006;442(7104): 739–741.
   Google Scholar
• Cimons M, Getlin J, Maugh THII. Cancer drugs face long road from mice to men. Los Angeles Times. May 6, 1998. Available from: http://articles.latimes.com/1998/may/06/news/mn-46795. Accessed November 8, 2010.
   Google Scholar
• Hanash S. Integrated global profiling of cancer. Nat Rev Cancer. 2004;4(8):638–644.
   Web of Science ®Google Scholar
• Editors. Nic Jones. Nat Rev Drug Discov. 2011;10(4):252–252.
   Web of Science ®Google Scholar
• Caponigro G, Sellers WR. Advances in the preclinical testing of cancer therapeutic hypotheses. Nat Rev Drug Discov. 2011;10(3):179–187.
   PubMed Web of Science ®Google Scholar
• Leaf C. Why we are losing the war on cancer. Fortune. March 9, 2004: 77–92.
   Google Scholar
• Zielinska E. Building a better mouse. Scientist. 2010;24(4):34–38.
   Web of Science ®Google Scholar
• Enna SJ, Williams M. Defining the role of pharmacology in the emerging world of translational research. Adv Pharmacol. 2009;57:1–30.
   PubMedGoogle Scholar
• Editorial. Cold shower for AIDS vaccines. Nat Med. 2007;13(12): 1389–1390.
   Web of Science ®Google Scholar
• Bailey J. An assessment of the role of chimpanzees in AIDS vaccine research. Altern Lab Anim. 2008;36(4):381–428.
   Web of Science ®Google Scholar
• Geerts H. Of mice and men: bridging the translational disconnect in CNS drug discovery. CNS Drugs. 2009;23(11):915–926.
   PubMed Web of Science ®Google Scholar
• Munos B. Lessons from 60 years of pharmaceutical innovation. Nat Rev Drug Discov. 2009;8(12):959–968.
   PubMed Web of Science ®Google Scholar
• Giri S, Bader A. Improved preclinical safety assessment using micro-BAL devices: the potential impact on human discovery and drug attrition. Drug Discov Today. 2011;16(9/10):382–397.
   Web of Science ®Google Scholar
• Collins FS. Reengineering translational science: the time is right. Sci Transl Med. 2011;3(90):90cm17.
   Web of Science ®Google Scholar
• Committee on Applications of Toxicogenomics to Cross-Species Extrapolation, Committee on Emerging Issues and Data on Environmental Contaminants, National Research Council. Application of Toxicogenomics to Cross-Species Extrapolation: A Report of a Workshop. Washington, DC: National Academy of Sciences; 2005.
   Google Scholar
• Sarkar SK. Molecular imaging approaches. Drug Discov World. 2009;(Fall):33–38.
   Google Scholar
• Littman BH, Williams SA. The ultimate model organism: progress in experimental medicine. Nat Rev Drug Discov. 2005;4(8):631–638.
   Web of Science ®Google Scholar
• Chabner BA, Roberts TGJr. Timeline: Chemotherapy and the war on cancer. Nat Rev Cancer. 2005;5(1):65–72.
   PubMed Web of Science ®Google Scholar
• Editorial. The time is now. Nat Rev Drug Discov. 2005;4(8):613.
   Web of Science ®Google Scholar
• Chapman AR. Addressing the ethical challenges of first-in-human trials. J Clinic Res Bioeth. 2011;2(4):113.
   Google Scholar
• Palfreyman MG, Charles V, Blander J. The importance of using human-based models in gene and drug discovery. Drug Discov World. 2002;(Fall):33–40.
   Google Scholar
• Dixit R, Boelsterli U. Healthy animals and animal models of human disease(s) in safety assessment of human pharmaceuticals, including therapeutic antibodies. Drug Discov Today. 2007;12(7–8): 336–342.
   PubMed Web of Science ®Google Scholar
• Editors. In this issue. Nat Rev Drug Discov. 2011;10(4):239–239.
   Google Scholar
• Leslie M. Biomedical research. Immunology uncaged. Science. 2010;327(5973):1573.
   Web of Science ®Google Scholar
• Dorsey ER, de Roulet J, Thompson JP, et al. Funding of US biomedical research, 2003–2008. JAMA. 2010;303(2):137–143.
   PubMed Web of Science ®Google Scholar
• Boat TF. Insights from trends in biomedical research funding. JAMA. 2010;303(2):170–171.
   Web of Science ®Google Scholar
• Translational research: getting the message across. Nature. 2008; 453(7197):839.
   Web of Science ®Google Scholar
• Begley S. Financial obstacles help keep doctors from patient research. Wall St J. May 2, 2003.
   Google Scholar
• Begley S. Physician-researchers needed to get cures out of rat’s cage. Wall St J. April 25, 2003.
   Google Scholar
• Begley S. Why nonprofits fund for-profit researchers. Wall St J. January 26, 2007.
   Google Scholar
• LaFollette H, Shanks N. Animal experimentation: the legacy of Claude Bernard. Intl Studies Philosophy Sci. 1994;8(3):195–210.
   Google Scholar
• Bernard C. An Introduction to the Study of Experimental Medicine. New York: Dover; 1957 (1865). (Specifically see pp 15, 24, 33, 111, 117–126, 138–139, 146–148, 180.)
   Google Scholar
• Elliot P. Vivisection and the emergence of experimental medicine in nineteenth century France. In: Rupke N, editor. Vivisection in Historical Perspective. New York: Croom Helm; 1987:48–77.
   Google Scholar
• Ahn AC, Tewari M, Poon CS, Phillips RS. The limits of reductionism in medicine: could systems biology offer an alternative? PLoS Med. 2006;3(6):e208.
   PubMed Web of Science ®Google Scholar
• Jura J, Wegrzyn P, Koj A. Regulatory mechanisms of gene expression: complexity with elements of deterministic chaos. Acta Biochim Pol. 2006;53(1):1–10.
   Web of Science ®Google Scholar
• Van Regenmortel MHV Biological complexity emerges from the ashes of genetic reductionism. J Mol Recognit. 2004;17(3):145–148.
   Web of Science ®Google Scholar
• Van Regenmortel MHV Reductionism and complexity in molecular biology. Scientists now have the tools to unravel biological and overcome the limitations of reductionism. EMBO Rep. 2004;5(11): 1016–1020.
   PubMed Web of Science ®Google Scholar
• Schadt EE, Sachs A, Friend S. Embracing complexity, inching closer to reality. Sci STKE. 2005;2005(295):pe40.
   PubMedGoogle Scholar
• Hayden EC. Human genome at ten: life is complicated. Nature. 2010; 464(7289):664–667.
   Web of Science ®Google Scholar
• Ottino JM. Engineering complex systems. Nature. 2004; 427(6973):399.
   Web of Science ®Google Scholar
• Vicsek T. The bigger picture. Nature. 2002;418(6894):131.
   Web of Science ®Google Scholar
• 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. Available from: http://citeseerx.ist.psu.edu/view-doc/download?doi=10.1.1.89.1604&rep=rep1&type=pdf. Accessed October 27, 2011.
   Google Scholar
• Grove AS. Efficiency in the health care industries: a view from the outside. JAMA. 2005;294(4):490–492.
   Web of Science ®Google Scholar
• Fell D. Understanding the Control of Metabolism. Volume 1. 1st ed. London: Portland Press; 1996.
   Google Scholar
• Mayr M. Metabolomics. Circ Cardiovasc Genet. 2008;1(1):58–65.
   Google Scholar
• Herzig M, Christofori G. Recent advances in cancer research: mouse models of tumorigenesis. Biochim Biophys Acta. 2002; 1602(2):97–113.
   Web of Science ®Google Scholar
• Carroll SB. Whatever doesn’t kill some animals can make them deadly. New York Times. December 21, 2009. Available from: http://www.nytimes.com/2009/12/22/science/22creature.html?emc=eta1&pagewanted=print. Accessed August 2, 2011.
   Google Scholar
• Horrobin DF. Modern biomedical research: an internally self-consistent universe with little contact with medical reality? Nat Rev Drug Discov. 2003;2(2):151–154.
   Web of Science ®Google Scholar
• Hunter K, Welch DR, Liu ET. Genetic background is an important determinant of metastatic potential. Nat Genet. 2003;34(1):23–24; author reply 25.
   Web of Science ®Google Scholar
• Hunter KW, Broman KW, Voyer TL, et al. Predisposition to effi-cient mammary tumor metastatic progression is linked to the breast cancer metastasis suppressor gene Brms1. Cancer Res. 2001;61(24):8866–8872.
   Web of Science ®Google Scholar
• Ingram DK, Jucker M. Developing mouse models of aging: a consideration of strain differences in age-related behavioral and neural parameters. Neurobiol Aging. 1999;20(2):137–145.
   Web of Science ®Google Scholar
• Lifsted T, Le Voyer T, Williams M, et al. Identification of inbred mouse strains harboring genetic modifiers of mammary tumor age of onset and metastatic progression. Int J Cancer. 1998;77(4): 640–644.
   PubMed Web of Science ®Google Scholar
• Miklos GLG. The human cancer genome project – one more misstep in the war on cancer. Nat Biotechnol. 2005;23(5):535–537.
   Web of Science ®Google Scholar
• Ioannidis JP. An epidemic of false claims. Competition and conflicts of interest distort too many medical findings. Sci Am. 2011;304(6):16.
   PubMed Web of Science ®Google Scholar
• Nijhout HF. The importance of context in genetics. Sci Am. 2003; 91(5):416–423.
   Google Scholar
• Pearson H. Surviving a knockout blow. Nature. 2002;415(6867):8–9.
   Web of Science ®Google Scholar
• Raineri I, Carlson EJ, Gacayan R, et al. Strain-dependent high-level expression of a transgene for manganese superoxide dismutase is associated with growth retardation and decreased fertility. Free Radic Biol Med. 2001;31(8):1018–1030.
   PubMed Web of Science ®Google Scholar
• Regenberg A, Mathews DJ, Blass DM, et al. The role of animal models in evaluating reasonable safety and efficacy for human trials of cell-based interventions for neurologic conditions. J Cereb Blood Flow Metab. 2009;29(1):1–9.
   PubMed Web of Science ®Google Scholar
• Rohan RM, Fernandez A, Udagawa T, Yuan J, D’Amato RJ Genetic heterogeneity of angiogenesis in mice. FASEB J. 2000;14(7):871–876.
   PubMed Web of Science ®Google Scholar
• Threadgill DW, Dlugosz AA, Hansen LA, et al. Targeted disruption of mouse EGF receptor: effect of genetic background on mutant phenotype. Science. 1995;269(5221):230–234.
   PubMed Web of Science ®Google Scholar
• Viluksela M, Duong TV, Stahl BU, Li X, Tuomisto J, Rozman KK. Toxicokinetics of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in two substrains of male Long-Evans rats after intravenous injection. Fundam Appl Toxicol. 1996;31(2):184–191.
   Google Scholar
• Jones GL, Sang E, Goddard C, et al. A functional analysis of mouse models of cardiac disease through metabolic profiling. J Biol Chem. 2005;280(9):7530–7539.
   Web of Science ®Google Scholar
• Bendall JK, Heymes C, Wright TJ, et al. Strain-dependent variation in vascular responses to nitric oxide in the isolated murine heart. J Mol Cell Cardiol. 2002;34(10):1325–1333.
   Web of Science ®Google Scholar
• Paigen B, Morrow A, Brandon C, Mitchell D, Holmes P. Variation in susceptibility to atherosclerosis among inbred strains of mice. Atherosclerosis. 1985;57(1):65–73.
   PubMed Web of Science ®Google Scholar
• Linder CC. The influence of genetic background on spontaneous and genetically engineered mouse models of complex diseases. Lab Anim (NY). 2001;30(5):34–39.
   Web of Science ®Google Scholar
• von Herrath M, Nepom GT. Remodeling rodent models to mimic human type 1 diabetes. Eur J Immunol. 2009;39(8):2049–2054.
   PubMed Web of Science ®Google Scholar
• Dowell RD, Ryan O, Jansen A, et al. Genotype to phenotype: a complex problem. Science. 2010;328(5977):469.
   Web of Science ®Google Scholar
• Agarwal S, Moorchung N. Modifier genes and oligogenic disease. J Nippon Med Sch. 2005;72(6):326–334.
   Google Scholar
• Gerhart J, Kirschner M. The theory of facilitated variation. In: Avise JC, Ayala FJ, editors. In the Light of Evolution: Volume 1. Adaptation and Complex Design. Washington, DC: National Academy of Sciences; 2007:45–64.
   Google Scholar
• Kirschner MW, Gerhart JC. The Plausibility of Life. New Haven: Yale University Press; 2006.
   Google Scholar
• 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(2):e1001316.
   PubMed Web of Science ®Google Scholar
• Ptashne M, Gann A. Genes and Signals. NewYork: Cold Spring Harbor Laboratory Press; 2002.
   Google Scholar
• Pennisi E. Searching for the genome’s second code. Science. 2004;306(5696):632–635.
   Web of Science ®Google Scholar
• Morley M, Molony CM, Weber TM, et al. Genetic analysis of genome-wide variation in human gene expression. Nature. 2004;430(7001):743–747.
   PubMed Web of Science ®Google Scholar
• Rosenberg NA, Pritchard JK, Weber JL, et al. Genetic structure of human populations. Science. 2002;298(5602):2381–2385.
   PubMed Web of Science ®Google Scholar
• 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(3):502–509.
   Web of Science ®Google Scholar
• Zhang W, Duan S, Kistner EO, et al. Evaluation of genetic variation contributing to differences in gene expression between populations. Am J Hum Genet. 2008;82(3):631–640.
   Web of Science ®Google Scholar
• 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(3):R26.
   Web of Science ®Google Scholar
• Rifkin SA, Kim J, White KP. Evolution of gene expression in the Drosophila melanogaster subgroup. Nat Genet. 2003;33(2):138–144.
   Web of Science ®Google Scholar
• Sandberg R,Yasuda R, Pankratz DG, et al. Regional and strain-specific gene expression mapping in the adult mouse brain. Proc Natl Acad Sci U S A. 2000;97(20):11038–11043.
   Web of Science ®Google Scholar
• 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(6):263–275.
   Web of Science ®Google Scholar
• Marvanova M, Menager J, Bezard E, Bontrop RE, Pradier L, Wong G. Microarray analysis of nonhuman primates: validation of experimental models in neurological disorders. FASEB J. May 2003;17(8):929–931.
   Google Scholar
• Kehrer-Sawatzki H, Cooper DN. Understanding the recent evolution of the human genome: insights from human-chimpanzee genome comparisons. Hum Mutat. 2007;28(2):99–130.
   Web of Science ®Google Scholar
• Khaitovich P, Muetzel B, She X, et al. Regional patterns of gene expression in human and chimpanzee brains. Genome Res. 2004;14(8):1462–1473.
   Web of Science ®Google Scholar
• LaFollette H, Shanks N. Brute Science: Dilemmas of Animal Experi-Mentation. London and New York: Routledge; 1996.
   Google Scholar
• Giles J. Animal experiments under fire for poor design. Nature. 2006;444(7122):981.
   Web of Science ®Google Scholar
• 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; 1990:71–78.
   Google Scholar
• Thomas C, Moridani M. Interindividual variations in the efficacy and toxicity of vaccines. Toxicology. 2010;278(2):204–210.
   Web of Science ®Google Scholar
• Letvin NL. Virology. Moving forward in HIV vaccine development. Science. 2009;326(5957):1196–1198.
   Web of Science ®Google Scholar
• Morrow MP, Weiner DB. DNA drugs come of age. Sci Am. Jul 2010: 49–53.
   Web of Science ®Google Scholar
• Thomas C. Roadblocks in HIV research: five questions. Nat Med. 2009;15(8):855–859.
   PubMed Web of Science ®Google Scholar
• Heywood R. Clinical toxicity – could it have been predicted? Post-marketing experience. In: Lumley CE, Walker S, editors. AnimalToxicity Studies: Their Relevance for Man. Lancaster: Quay; 1990:57–67.
   Google Scholar
• Spriet-Pourra C, Auriche M, editors. SCRIP Reports. New York: PJB; 1994.
   Google Scholar
• Marwick C. Promising vaccine treatment for Alzheimer disease found. JAMA. 2000;284(12):1503–1505.
   Web of Science ®Google Scholar
• Manson JM. Biological considerations for risk assessment in developmental toxicology. In: McLachlan JA, Pratt RM, Markert CL, editors. Developmental Toxicology: Mechanisms and Risks. Banbury Report 26. Cold Spring Harbor Laboratory Press; 1987:307–322.
   Google Scholar
• Shepard T, Lemire R. Catalog of Teratogenic Agents. 11th ed. Baltimore: Johns Hopkins; 2004.
   Google Scholar
• Holmes B. Monkey genome springs surprise for human origins. New Sci. April 21, 2007.
   Web of Science ®Google Scholar
• Rhesus Macaque Genome Sequencing and Analysis Consortium, Gibbs RA, Rogers J, et al. Evolutionary and biomedical insights from the rhesus macaque genome. Science. 2007;316(5822):222–234.
   Web of Science ®Google Scholar
• Beniashvili DS. Experimental Tumors in Monkeys. Boca Raton, FL: CRC Press; 1994.
   Google Scholar
• Wald C, Wu C. Of mice and women: the bias in animal models. Science. 2010;327(5973):1571–1572.
   Web of Science ®Google Scholar
• Willyard C. HIV gender clues emerge. Nat Med. 2009;15(8):830.
   Web of Science ®Google Scholar
• Holden C. Sex and the suffering brain. Science. 2005;308(5728):1574.
   Web of Science ®Google Scholar
• Simon V. Wanted: women in clinical trials. Science. 2005;308(5728):1517.
   PubMed Web of Science ®Google Scholar
• Couzin J. Human genetics. In Asians and whites, gene expression varies by race. Science. 2007;315(5809):173–174.
   Web of Science ®Google Scholar
• Couzin J. Cancer research. Probing the roots of race and cancer. Science. 2007;315(5812):592–594.
   Web of Science ®Google Scholar
• Gregor Z, Joffe L. Senile macular changes in the black African. Br J Ophthalmol. 1978;62(8):547–550.
   Web of Science ®Google Scholar
• Willyard C. Blue’s clues. Nat Med. 2007;13(11):1272–1273.
   Web of Science ®Google Scholar
• Cheung DS, Warman ML, Mulliken JB. Hemangioma in twins. Ann Plast Surg. Mar 1997;38(3):269–274.
   Web of Science ®Google Scholar
• 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(2): 226–231.
   Web of Science ®Google Scholar
• Risch N. Dissecting racial and ethnic differences. N Engl J Med. 2006;354(4):408–411.
   Web of Science ®Google Scholar
• Haiman CA, Stram DO, Wilkens LR, et al. Ethnic and racial differences in the smoking-related risk of lung cancer. N Engl J Med. 2006;354(4):333–342.
   PubMed Web of Science ®Google Scholar
• Bachmanov AA, Reed DR, Beauchamp GK, Tordoff MG. Food intake, water intake, and drinking spout side preference of 28 mouse strains. Behav Genet. 2002;32(6):435–443.
   PubMed Web of Science ®Google Scholar
• Durrant C, Tayem H, Yalcin B, et al. Collaborative Cross mice and their power to map host susceptibility to Aspergillus fumigatus infection. Genome Res. 2011;21(8):1239–1248.
   Google Scholar
• Holmes AM, Solari R, Holgate ST. Animal models of asthma: value, limitations and opportunities for alternative approaches. Drug Discov Today. 2011;16(15/16):659–670.
   Web of Science ®Google Scholar
• Morris JA, Royall JJ, Bertagnolli D, et al. Divergent and nonuniform gene expression patterns in mouse brain. Proc Natl Acad Sci U S A. 2010;107(44):19049–19054.
   Web of Science ®Google Scholar
• Bruder CE, Piotrowski A, Gijsbers AA, et al. Phenotypically concordant and discordant monozygotic twins display different DNA copy-number-variation profiles. Am J Hum Genet. 2008;82(3): 763–771.
   PubMed Web of Science ®Google Scholar
• Fraga MF, Ballestar E, Paz MF, et al. Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci U S A. 2005;102(30):10604–10609.
   PubMed Web of Science ®Google Scholar
• Javierre BM, Fernandez AF, Richter J, et al. Changes in the pattern of DNA methylation associate with twin discordance in systemic lupus erythematosus. Genome Res. 2010;20(2):170–179.
   PubMed Web of Science ®Google Scholar
• US Food and Drug Administration (FDA). FDA announces new boxed warning on Plavix: alerts patients, health care professionals to potential for reduced effectiveness [press release]. Silver Spring, MD: FDA; March 12, 2010 [updated December 3]. Available from: http://www.fda.gov/NewsEvents/Newsroom/PressAnnouncements/ucm204253.htm. Accessed March 12, 2010.
   Google Scholar
• Weiss ST, McLeod HL, Flockhart DA, et al. Creating and evaluating genetic tests predictive of drug response. Nat Rev Drug Discov. 2008;7(7):568–574.
   Web of Science ®Google Scholar
• Americans for Medical Advancement (AFMA). FAQs about AFMA [web page on the Internet]. Goleta, CA: AFMA; 2010. Available from: http://www.afma-curedisease.org/faq.html. Accessed October 27, 2011.
   Google Scholar
• AFMA: Advocates For Science-Based Medical Research [homepage on the Internet]. Goleta, CA: AFMA; 2010. http://www.afmacuredisease.org. Accessed October 27, 2011.
   Google Scholar