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Regulating Dual-Use Research in Europe THE EUROPEAN SOCIETY FOR VIROLOGY (ESV), which represents scientists active in basic, medical, veterinary, plant, and environmental aspects of virology, has been following with particular interest the debate on “gain-of-function” studies catalyzed by the

Letters to the Editor Letters (~300 words) discuss material published in Science in the past 3 months or matters of general interest. Letters are not acknowledged upon receipt. Whether published in full or in part, Letters are subject to editing for clarity and space. Letters submitted, published, or posted elsewhere, in print or online, will be disqualified. To submit a Letter, go to


QIUYAN LIAO* AND RICHARD FIELDING Division of Behavioural Health, School of Public Health, The University of Hong Kong, Pokfulam, Hong Kong SAR, China. *Corresponding author. E-mail: [email protected]

References 1. Government of Hong Kong Special Administrative Region, Press Releases, “LCQ2: Poultry slaughtering plant” (2006); 2. R. Fielding et al., Emerg. Infect. Dis. 11, 677 (2005). 3. R. Fielding et al., Emerg. Infect. Dis. 13, 1065 (2007). 4. Q. Liao, B. J. Cowling, W. T. Lam, R. Fielding, Emerg. Infect. Dis. 17, 2379 (2011).

H5N1 influenza virus transmission studies from the Dutch group led by Ron Fouchier and published by Science in June 2012 (1). The Dutch government insisted that Fouchier ask for official permission (an export permit) before publishing his research abroad, on the basis of European Council regulation EC 428/2009, which was issued in 2009 to prevent the spread of nuclear, chemical, and biological weapons. Although Fouchier complied before the Science paper was published, Erasmus MC Rotterdam sued the government over the requirement for an export permit, based on the fact that the Annex to Council regulation EC 428/2009 contains an exclusion clause for basic scientific research and information already in the public domain. The appeal was recently rejected by a district court, and the case is now being brought before Amsterdam’s Court of Appeal. The News of the Week story “Virologist

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IN THE NEWS & ANALYSIS STORY “TENSE VIGIL IN CHINA AS NASTY FLU virus stirs back to life” (C. Larson, 29 November 2013, p. 1031), George Gao, the deputy director-general of the Chinese Center for Disease Control and Prevention, is quoted as saying that “You cannot change culture,” suggesting that there is no point in trying to change the live poultry markets in China. Evidence contradicts this assumption. During the first A(H5N1) influenza outbreak in Hong Kong in 1997, prompt government action regarding live poultry markets and culling cut the epidemic short. After repeated reemergence of A(H5N1) in the first decade of the century, the Hong Kong government first proposed a central slaughterhouse to remove live poultry from wet markets, but trade and NIMBY residential opposition deferred that decision indefinitely (1). Our initial population surveys indicated that individuals were more willing to change their habits of buying if such changes were observed among others in the community (2). The population pragmatically realized that a change in the practice of poultry retail was needed.

The Hong Kong government subsequently initiated a policy of reducing live poultry availability through reduced imports and internal production, as well as buying back licenses from traders who sell live poultry for slaughter, so that today such stalls are a rarity. Instead, chilled poultry is widely available, with many former live poultry stalls now selling pre-killed and chilled poultry. Population exposure to live poultry from markets declined by 60% between 2004 and 2006 and by a further 21% between 2006 and 2010, attributable to reduced live poultry availability and public health education (3, 4). Thus, culture can be changed. We believe that cultural changes that promote public health principles of separating the agent, vector, and host are China’s only real long-term solution to repeated influenza emergence.

appeals decision on H5N1 export rules” (8 November 2013, p. 676) stated that the ESV has “sided with Fouchier.” Roughly 90 viruses and microorganisms that can cause disease in humans, animals, and plants are listed in the Annex to Council regulation EC 428/2009. ESV’s position stems from the concern that results from scientific work carried out in Europe on these organisms would require an export permit before they can be published in international scientific journals. This prospect raises a number of serious issues. Under what circumstances should this EC regulation be applied to biomedical research? Who is going to decide when the EC regulation does or does not apply? What should be considered “basic scientific research,” and who is going to judge this criterion? (This is not a trivial question, especially in the European Union context, where, in theory, there might be 28 different inter-

VOL 343 SCIENCE Published by AAAS


Flu Threat Spurs Culture Change

LETTERS pretations of the same regulation.) Does this create the potential for discrimination among scientists working in different European States and between European scientists and those in the rest of the world? Does this decision apply only when specific results are going to be published in journals outside Europe, or does it apply universally? It may be that controversial questions related to this issue were ignored for too long, allowing a precedent to be set prematurely. We are overdue for discussions on how to regulate the dissemination of “sensitive” data in a way that does not compromise biosecurity, while maintaining the principle that acquiring important and meaningful knowledge cannot simply be stopped. ESV believes that export control does not represent the best way to deal with this issue. Our intention is not to criticize or to disregard the work of jurisprudence experts. We believe that the European Commission should take steps to promote a common understanding of the current regulation by existing working groups or by a new advisory committee created to deal with the dual-use research in a harmonized and balanced way throughout

Europe. In the meantime, we have expressed our willingness to provide law officers with proper scientific advice, making available the expertise of our many European scientists. GIORGIO PALÙ President of the European Society for Virology, Department of Molecular Medicine, University of Padova, 35121, Italy. E-mail: [email protected]

Reference 1. S. Herfst et al., Science 336, 1534 (2012).

Misleading Results: Translational Challenges WE AGREE COMPLETELY WITH THE NEWS FOCUS story “When mice mislead” (J. CouzinFrankel, 22 November 2013, p. 922). Many of the issues identified in this article, such as investigator bias, blinding, randomization, and inclusion and exclusion criteria, were clearly identified in the Stroke Therapy Academic Industry Round Table publication in 1999 (1) and discussed further by others (2). Tightening the standards for animal experimentation, especially for those experiments that test drugs for their neuroprotective


effects, is critical as we try to translate these drugs into human stroke therapy. There have been hundreds of drugs tested for neuroprotective effects and many, if not most, have positive effects, in animal models. If a mouse or rat had a stroke, we would know exactly how to treat it. Unfortunately, none of these drugs has shown success in humans. It is unlikely that poor methods used in animal studies account for all the negative clinical trials that have been performed based on preclinical studies. After all, some investigators do perform appropriate experiments, and even those studies rarely lead to positive clinical trials. One important issue not mentioned in the News Focus piece could also account for the lack of positive clinical trials: Most researchers in the stroke field work with normal, young, healthy animals. Humans who participate in neuroprotective drug clinical trials are most often not normal, young, or healthy. They have a variety of comorbid diseases such as hypertension, diabetes, obesity, and vascular disease, which could alter the way in which drugs work in humans. We suggest that in future animal experiments, drugs be tested in

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LETTERS animals that are aged, with comorbid diseases. Such studies may help to identify potentially effective drugs in an animal model that mimics more closely a human with stroke. RICHARD J. TRAYSTMAN1* AND PACO S. HERSON2 1

Departments of Pharmacology, Anesthesiology, Emergency Medicine, and Neurology, Anschutz Medical Campus, University of Colorado Denver, Aurora, CO 80045, USA. 2 Departments of Neuroscience and Anesthesiology, Neuronal Injury Program, Anschutz Medical Campus, University of Colorado Denver, Aurora, CO 80045, USA. *To whom correspondence should be addressed. E-mail: [email protected]

References 1. Stroke Therapy Academic Industry Round Table, Stroke 30, 2752 (1999). 2. M. M. Macleod et al., J. Cerebral Blood Flow Met. 29, 221 (2009).

Misleading Results: Don’t Blame the Mice IN THE NEWS FOCUS STORY “WHEN MICE MISlead” (22 November 2013, p. 922), J. CouzinFrankel raises concerns about practices that give rise to misleading scientific findings. The case studies cited demonstrate procedural

errors that can occur in the design or execution of experiments. These unfortunate mistakes can happen in any area of research and are not the exclusive domain of mice or animal models; clinical research is certainly not immune to error. Even well-executed studies can give rise to misleading results for reasons that are insidious and hard to control (1). With regard to mice, the first “risk of bias question” that a reviewer should ask is, “Was the result replicated in more than one genetic background?” Idiosyncrasies of particular mouse strains can be misleading (2). Ignoring the effect of genetic background is the most pervasive source of bias in animal studies. To reduce the problem of false or irreproducible scientific findings, we need to address two root causes. Science today is driven by an incentive system that often rewards precedence and impact over quality of the work. Statistical training of scientists often emphasizes analytical techniques over experimental design and quantitative reasoning. These are systemic problems that will not change without substantial effort. However, the message in this News Focus story does suggest some simple advice that

can redress many of the pitfalls of experimental studies: Be wise, randomize. GARY A. CHURCHILL The Jackson Laboratory, Bar Harbor, ME 04609, USA. E-mail: [email protected]

References 1. J. P. A. Ioannidis, PLOS Med. 2, e124 (2005). 2. V. Kumar et al., Science 342, 1508 (2013).

CORRECTIONS AND CLARIFICATIONS Table of Contents: (3 January, p. 3). The artist’s name was misspelled in the cover caption credit line. The correct spelling is Aurore Simonnet. Additionally, the Review Summary by M. Dalziel et al. was mislabeled as a Research Article Summary, and the URL for the full text was incorrect. The correct URL is The HTML and PDF versions online are correct. The title of the Perspective by Y. E. Türkmen and V. K. Aggarwal was also incorrect. It should be “A Simpler Route for Making Nitrogen-Alkene Rings.” The HTML version is correct online, and the PDF version has been corrected. Editorial: “No windfall for U.S. science” by M. McNutt (3 January, p. 6). In the second paragraph, the U.S. Senate budget mark is $1,058B, not $1.058B. The HTML and PDF versions online have been corrected. Essay: “Science & SciLifeLab Prize” (6 December 2013, p. 1185). Finalists have been reclassified as Second Runners-Up. The HTML and PDF versions online have been corrected.

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VOL 343 SCIENCE Published by AAAS

Flu threat spurs culture change.

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