Why Current Publication Practices May Distort Science Neal S
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Essay Why Current Publication Practices May Distort Science Neal S. Young*, John P. A. Ioannidis, Omar Al-Ubaydli his essay makes the underlying Summary the more extreme, spectacular assumption that scientific results (the largest treatment The current system of publication information is an economic effects, the strongest associations, T in biomedical research provides commodity, and that scientific journals or the most unusually novel and a distorted view of the reality of are a medium for its dissemination exciting biological stories) may be scientific data that are generated in the and exchange. While this exchange preferentially published. Journals laboratory and clinic. This system can system differs from a conventional serve as intermediaries and may suffer be studied by applying principles from market in many senses, including minimal immediate consequences for the field of economics. The “winner’s the nature of payments, it shares the errors of over- or mis-estimation, but curse,” a more general statement of goal of transferring the commodity it is the consumers of these laboratory publication bias, suggests that the (knowledge) from its producers and clinical results (other expert small proportion of results chosen for (scientists) to its consumers (other scientists; trainees choosing fields publication are unrepresentative of scientists, administrators, physicians, of endeavour; physicians and their scientists’ repeated samplings of the real patients, and funding agencies). The patients; funding agencies; the media) world. The self-correcting mechanism function of this system has major who are “cursed” if these results are in science is retarded by the extreme consequences. Idealists may be severely exaggerated—overvalued imbalance between the abundance offended that research be compared to and unrepresentative of the true of supply (the output of basic science widgets, but realists will acknowledge outcomes of many similar experiments. laboratories and clinical investigations) that journals generate revenue; For example, initial clinical studies and the increasingly limited venues for publications are critical in drug are often unrepresentative and publication (journals with sufficiently development and marketing and to misleading. An empirical evaluation high impact). This system would be attract venture capital; and publishing of the 49 most-cited papers on the expected intrinsically to lead to the defines successful scientific careers. effectiveness of medical interventions, misallocation of resources. The scarcity Economic modelling of science may of available outlets is artificial, based on yield important insights (Table 1). the costs of printing in an electronic age Funding: The authors received no specific funding The Winner’s Curse and a belief that selectivity is equivalent for this article. to quality. Science is subject to great In auction theory, under certain Competing Interests: The authors have declared uncertainty: we cannot be confident conditions, the bidder who wins tends that no competing interests exist. now which efforts will ultimately yield to have overpaid. Consider oil firms worthwhile achievements. However, Citation: Young NS, Ioannidis JPA, Al-Ubaydli O bidding for drilling rights; companies (2008) Why current publication practices may distort the current system abdicates to a small estimate the size of the reserves, and science. PLoS Med 5(10): e201. doi:10.1371/journal. number of intermediates an authoritative pmed.0050201 estimates differ across firms. The prescience to anticipate a highly average of all the firms’ estimates would This is an open-access article distributed under the unpredictable future. In considering terms of the Creative Commons Public Domain usually approximate the true reserve society’s expectations and our own declaration, which stipulates that, once placed in the size. Since the firm with the highest public domain, this work may be freely reproduced, goals as scientists, we believe that there estimate bids the most, the auction distributed, transmitted, modified, built upon, or is a moral imperative to reconsider otherwise used by anyone for any lawful purpose. winner systematically overestimates, how scientific data are judged and sometimes so substantially as to lose Neal S. Young is with the Hematology Branch, disseminated. money in net terms [1]. When bidders National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, Maryland, United are cognizant of the statistical processes States of America. John P. A. Ioannidis is with the of estimates and bids, they correct for Department of Hygiene and Epidemiology, University of Ioannina School of Medicine, and the Biomedical the winner’s curse by shading their bids curse [5–8]. Indeed, the winner’s curse Research Institute, Foundation for Research and down. This is why experienced bidders was first proposed by oil operations Technology – Hellas, Ioannina, Greece; and the sometimes avoid the curse, as opposed researchers after they had recognised Department of Medicine, Tufts University School of Medicine, Boston, Massachusetts, United States of to inexperienced ones [1–4]. Yet in aberrant results in their own market. America. Omar Al-Ubaydli is with the Department of numerous studies, bidder behaviour An analogy can be applied to Economics and the Mercatus Center, George Mason appears consistent with the winner’s scientific publications. As with University, Fairfax, Virginia, United States of America. individual bidders in an auction, * To whom correspondence should be addressed. the average result from multiple E-mail: [email protected] The Essay section contains opinion pieces on topics studies yields a reasonable estimate of broad interest to a general medical audience. Provenance: Not commissioned; externally peer of a “true” relationship. However, reviewed PLoS Medicine | www.plosmedicine.org 1418 October 2008 | Volume 5 | Issue 10 | e201 Table 1. Economic Terms and Analogies in Scientific Publication Economic Term Meaning Analogy in Scientific Publication Winner’s curse The winner in an auction tends on average to have overpaid, Scientific studies try to find true relationships, but none are especially when no participant is sure exactly how valuable certain of what these relationships are exactly. Published the item is. articles, especially in very competitive journals, have on average exaggerated results. Oligopoly A market where a few traders have the major share and each Very few journals with limited publication slots (compared oligopolist has significant power to influence the market. with geometrically increasing scientific data that seek publication) determine highly visible science. Herding “Follow-the-leader” behaviour: the actions of the first or Scientists may uncritically follow paths of investigation dominant player supersede the individual information and that are popularised in prestigious publications, neglecting actions of all the players in a market. novel ideas and truly independent investigative paths. Artificial scarcity Restrictions on the provision of a commodity above that Print page limits are an obvious excuse for failure to expected from its production cost. accept articles, and further the small number of major “high-impact” journals have limited slots; extremely low acceptance rates provide status signals to successful publications and their authors. Uncertainty Situation where the real long-term value of a commodity is For much (most?) scientific work, it is difficult or impossible largely unpredictable. to immediately predict future value, extensions, and practical applications. Branding Marking a product as valuable; of key importance when it is Publishing in selective journals provides evidence of value difficult to determine a product’s value prior to consuming it. of a research result and its authors, independent of the manuscript’s content. doi:10.1371/journal.pmed.0050201.t001 published in highly visible journals in at conferences or among colleagues, considerations of experimental design, 1990–2004, showed that a quarter of but surface more publicly only when execution, or importance. Much data the randomised trials and five of six dominant paradigms are replaced. are never formally refuted in print, non-randomised studies had already Sometimes, negative data do appear but most promising preclinical work been contradicted or found to have in refutation of prominent claims. eventually fails to translate to clinical been exaggerated by 2005 [9]. The In the “Proteus phenomenon”, an benefit [22]. Worse, in the course of delay between the reporting of an extreme result reported in the first ongoing experimentation, apparently initial positive study and subsequent published study is followed by an negative studies are abandoned publication of concurrently performed extreme opposite result; this sequence prematurely as wasteful. but negative results is measured in may cast doubt on the significance, years [10,11]. An important role of meaning, or validity of any of the Oligopoly systematic reviews may be to correct results [18]. Several factors may predict Successful publication may be more the inflated effects present in the initial irreproducibility (small effects, small difficult at present than in the past. studies published in famous journals studies, “hot” fields, strong interests, The supply and demand of scientific [12], but this process may be similarly large databases, flexible statistics) [19], production have changed. Across the