Abstract
1. Demonstrate how to render a vaccine ineffective; 2. Confer resistance to effective antibiotics or antiviral agents; 3. Enhance the virulence of pathogens or render nonpathogens virulent; 4. Increase transmissibility of a pathogen; 5. Alter the host range of a pathogen; 6. Enable the evasion of a diagnostic or detection modality; or 7. Enable the weaponization of a microbiological agent or toxin.
The H5N1 avian influenza experiments clearly meet the criteria of numbers 4 and 5. The public's outrage has not been helped by the mixed messages sent by the scientific community. The National Science Advisory Board for Biosecurity (NSABB) recommended that the controversial papers be published with parts of the study methodologies removed. The World Health Organization (WHO) subsequently convened a closed meeting that included research virologists and journal editors; they recommended that the papers be published in full. In the wake of this recommendation, the National Institutes of Health (NIH), which financed the research, wanted the NSABB to revisit their previous recommendation. 3 Contributing to the confusion, Ron Fouchier announced that the genetically altered virus he created was not as contagious or deadly as he had originally asserted.4,5
While the debate has focused primarily on whether or not to publish the papers, in part or in full, the larger issue, not being discussed, is the difference of opinion between the scientific and security communities. The scientific community largely defends the work, stating that it provides important information, while the security community asserts that the risks of the research outweigh the benefits.6,7
Can the divide between these 2 communities be bridged? Although the security community places great emphasis on the need to educate the scientific community about biosecurity, evidence suggests that the scientific community does not share this concern, even though national and international bodies recommend such actions. For example, in June 2007, the NSABB issued a report on a proposed framework for the oversight of dual-use life sciences research. The committee stated that one of the best ways to address concerns regarding dual-use research was to strengthen the culture of understanding and responsibility in the scientific community. Education is a vital component of this framework. According to the report, both the federal government and the research institutions have a responsibility to develop appropriate education and training materials for current and future life scientists. 8
In 2008, participants from more than 35 countries attended an inter-session meeting of the Biological Weapons Convention (BWC) addressing dual-use research of concern. The meeting objectives included exploring strategies for managing the oversight of dual-use research as well as fostering awareness at the international level on dual-use research issues. Individuals shared experiences about the education efforts taking place in their countries, including Brazil, the Philippines, Poland, and Uganda. In Brazil, for example, a biosecurity program was launched within the biosafety framework.9,10
The Commission on Prevention of Weapons of Mass Destruction Proliferation and Terrorism issued a report, World at Risk, that advocated for a culture of security and stressed the important role of education in preventing a future event. 11 In November 2009, the U.S. National Security Council released the “National Strategy for Countering Biological Threats,” which included the importance of norms of safe and responsible conduct. It noted that documenting, communicating, and reinforcing norms of conduct should be done during the initial education and throughout the career of life scientists in academia, industry, and government. 12
Although these high-level meetings and reports stress the importance of educating life scientists about biosecurity, studies have shown that few programs exist in this area. For example, in Europe, a Landau Network-Centro Volta (LNCV) and Bradford Disarmament Research Centre (BDRC) collaboration found only 3 out of 57 European universities surveyed offered some form of biosecurity module. Professors and course coordinators interviewed responded with a variety of reasons why there are so few biosecurity modules, including that the topics were not relevant, that the topics were possibly too upsetting for the students, or that biosecurity was too unfamiliar a subject to teach. 13 Another study in the UK found that few universities teach biosecurity and dual-use issues to students. 14 A Japanese study investigated 62 universities in 36 different regions and found 3 specific biosecurity modules and other instances of biosecurity teaching, but “dual use” was an uncommon term. 15 An Asia-Pacific study investigating biosecurity education in 58 universities across 10 countries, including Australia, India, and Taiwan, produced findings similar to those found in Europe, the UK, and Japan. Only 5 specific biosecurity cases in 3 countries were found. Bioethics was the most common subject: 93 cases in 10 countries. Biosafety was the next most common subject. 16 In Israel, education and training of biosecurity issues is mandated by law. 17 Yet, despite this mandate, a study of 6 research universities in Israel found no specific module on biosecurity. 18 In the U.S., the American Association for the Advancement of Science found only 16 programs that addressed the dual-use issue.19,20 These studies primarily focused on the presence or absence of biosecurity education modules offered in life sciences courses.
Between October 2004 and May 2005, Dando and Rappert conducted 25 seminars in life sciences departments, primarily in UK universities. These seminars were held to assist the June 2005 deliberations by States Parties at the Meeting of Experts and were conducted to raise awareness and encourage discussion and deliberation by scientists about the potential for misuse of life sciences research. The seminars primarily targeted scientists, but some included students. The main findings: few of the participants had given much consideration to the issue of biosecurity, and few regarded bioterrorism or bioweapons as a substantial threat or were aware of the debates and concerns about dual-use research. Twelve seminars conducted in the U.S. during 2006 found greater awareness and knowledge about biosecurity discussions than in Europe as well as an awareness of potential misuse policy initiatives and related bioweapons issues. The seminars conducted in the U.S. were set up through personal contacts by the researchers and limited in scope.21,22
One would hypothesize that, given the experience of the 2001 anthrax attacks and the subsequent multibillion dollar government investment in defense against bioterrorism, there would be widespread efforts to teach graduate students and postdoctoral fellows about biosecurity. 23 Is there biosecurity education and awareness among life sciences students and postdoctoral fellows in the U.S.? And if so, how does it compare to bioethics and biosafety? What are their attitudes toward these subjects? An informal survey was done to answer these questions.
An Informal Survey
From May to July 2011, an informal survey of 4 large public and 4 large private research universities in 7 states (Alabama, California, Georgia, Massachusetts, Missouri, Wisconsin, and Washington) was done to assess graduate students' and postdoctoral fellows' education experiences and attitudes regarding biosecurity in comparison to bioethics and biosafety. The 8 universities were chosen because they are among the top 30 recipients of NIH grant funding and are geographically spread around the country. 24 Students and postdoctoral fellows in the relevant fields of microbiology, molecular biology, infectious diseases, and immunology were targeted through their department chairs. The survey was done entirely online; Princeton University's Office of Research and Project Administration determined that the informal survey was exempt from Institutional Review Board review.
Of the total sample of approximately 1,852 graduate students and postdoctoral fellows, 220 (12%) answered all the questions. Of these respondents, 69% were graduate students, and 28% were postdoctoral fellows. Approximately 61% of the respondents were female. The response was very small, self-selected, and skewed (50%) from 1 institution, so the results should be viewed with caution. However, there were some intriguing findings.
Approximately 80% of the respondents had taken courses on bioethics and biosafety, but only 10% had taken a course on biosecurity, and of these, few remembered what the course covered or found it useful. Almost 100% and 97%, respectively, believed that biosafety and bioethics were very or somewhat important. In contrast, 88% believed that biosecurity was very or somewhat important.
Open-ended questions asking the respondents what they thought about biosecurity, bioethics, and biosafety yielded more confused answers about biosecurity than about bioethics or biosafety. For example, 18 respondents didn't know what the term “biosecurity” meant, and an additional 17 respondents confused biosecurity with other subjects by providing answers such as “hazmat, public health, or HIPAA.” In contrast, only 1 respondent was not familiar with the term “biosafety,” and no one was unfamiliar with the term “bioethics.”
Discussion
While this was an informal survey rather than a statistical sample, the responses suggest that graduate students and postdoctoral fellows in relevant areas of the life sciences are not being educated about biosecurity and are much more familiar with biosafety and bioethics. In an era in which tremendous resources have been invested in biodefense, it is unsettling that apparently so little has been done to educate the next generation of researchers about biosecurity. This is not just a U.S. phenomenon: Evidence suggests that it is global.
The U.S. government places great emphasis on bioethics and biosafety—why not biosecurity? For example, NIH has an ethics program with policies, procedures, and extensive training courses. Ethics concerns apply not only to NIH employees, but to all NIH grantees as well. 25
Similarly, biosafety is an important issue at NIH, the Centers for Disease Control and Prevention (CDC), and all institutions around the country. Institutional Biosafety Committees (IBCs) oversee biosafety activities. CDC offers publications, symposia, and training courses on biosafety.26,27
In the realm of biosecurity, CDC offers an online biosecurity course that is buried within biosafety. CDC's Select Agent and Toxin program focuses on proper storage and transfer of hazardous microbes and toxins. 28 Training programs emphasize public health preparedness rather than laboratory biosecurity. 29 Unlike bioethics and biosafety, there are no corresponding biosecurity education programs. Instead, NIH provides grant funding and guidelines for working on select agents, 30 even though the NSABB produces education materials. 31 These materials are not incorporated into the functioning of the NIH and extramural institutions the way bioethics and biosafety education materials are.
One reason for this lapse might be because biosecurity is a relatively recent concern compared to bioethics and biosafety. Ethical mandates were imposed on the life sciences community because of a history of past abuses such as the atrocities committed by Nazi physicians in World War II. The Nuremberg trials of Nazi physicians led to the Nuremberg Code, which set 10 conditions necessary for research involving human subjects. In 1964, the World Medical Association passed the Declaration of Helsinki: Recommendations Guiding Medical Doctors in Biomedical Research Involving Human Subjects. These guidelines were broader in scope than the Nuremberg Code.
Unfortunately, the Nuremberg Code and the Declaration of Helsinki were not enough to get U.S. legislators to mandate ethical research practices. It was the public outrage from the infamous Tuskegee syphilis experiments, conducted from 1932 to 1972 by the U.S. Public Health Service, that prompted Congress to pass the National Research Act of 1974. This act required the then–Department of Health, Education, and Welfare (HEW) to codify policies for the protection of human subjects into federal regulations. In 1979, the Belmont Report: Ethical Principles and Guidelines for the Protection of Human Subjects was published, establishing fundamental ethical principles relevant to all studies involving human subjects. In 1991, the current ethical policies for all federally funded research were updated in Title 45, Code of Federal Regulations, Part 46.32,33
Public outrage was not needed to implement biosafety policies, procedures, and practices. The life sciences community itself developed and implemented biosafety programs because of published reports of thousands of laboratory-acquired infections, including more than 100 deaths. 34 Numerous laboratory-acquired infections prompted the microbiological and biomedical communities to develop safety equipment, safe microbiological practices, and facility safeguards as a strategy to protect the laboratory workers, the public at large, and the environment. 34 This might explain why acceptance and support for biosafety in the life sciences community is so high.
For bioterrorism, there has not been enough outside pressure or inside buy-in to enact more meaningful education or practice changes, aside from placing more locks on doors. The anthrax attacks of 2001 did not culminate in the arrest and trial of the prime suspect, Dr. Bruce Ivins. Nor was there an investigation by an independent commission analogous to the 9/11 Commission. 35 There was public fear, but not enough public outrage to prompt Congress to mandate the biosecurity changes recommended in the 2004 Fink Report aside from the establishment of the NSABB.
In addition, one could argue that bioterrorism inherently places blame on life sciences research or on the researchers themselves, alleging that they might commit malevolent acts or aid others through their research findings. No profession wants to acknowledge that there might be bad actors in its midst or that its work might help others inflict public harm. This sentiment might explain why the life sciences community has been so reluctant to acknowledge the risks and educate the next generation about these issues; for them, the threat remains theoretical and remote.
How should the security community proceed? Does it have to wait for public outrage from another bioterrorist disaster before Congress passes mandatory biosecurity measures on the life sciences community? The life sciences community itself is unlikely to embrace meaningful biosecurity changes given its defense of the H5N1 avian influenza research.
There are strategies that could be implemented to embed biosecurity in the life science culture, but they would require the NIH's full commitment and cooperation. This is the institution that approved and funded the controversial H5N1 avian influenza research. Getting the NIH to implement these changes would likely require a directive from the highest levels of the executive branch of the U.S. government. Since the NIH also funds international research projects, such as the H5N1 avian influenza research in the Netherlands and Japan, these strategies would have an impact globally as well.
The first strategy would be for the NIH to develop policies and procedures requiring all grants officers to implement the Fink Report's biosecurity recommendations for project reviews. Grants officers must read, evaluate, and approve proposed life sciences research before the work can get funded. Once a grants officer decides to fund a project, all subsequent debate as to the risks versus the benefits, including whether or not it meets the criteria for the “7 experiments of concern,” becomes moot. An NIH grants officer evidently did not consider the fact that the H5N1 avian influenza research met 2 of the criteria before approving it. For many in the security community, the H5N1 avian influenza research should never have been approved or funded. The Fink Report recommended that questionable life sciences research proposals should undergo extensive review before being approved. 36 This recommendation should be implemented.
Second, the NIH should require all life sciences researchers in relevant fields such as microbiology, molecular biology, synthetic biology, genomics, immunology, and infectious diseases to take an online biosecurity course, analogous to the mandatory online bioethics course, before becoming eligible to participate in NIH-funded research studies. 37 The Fink Report's first recommendation was that the scientific community be educated on biosecurity issues. The online course would include a brief history of bioterrorism, the Biological Weapons Convention, and key findings and recommendations of the Fink Report. The online course would be easily accessible and free of charge. A certificate of completion, analogous to the certificate of completion for the NIH's mandatory bioethics course, would be issued once the researcher completed the course and successfully passed an online examination.
Once the life sciences community sees that the NIH is serious about implementing biosecurity, then perhaps it might take the issue more seriously as well. Until then, cases like the H5N1 avian influenza research controversy will likely continue. By the time controversial studies are under consideration for publication, it is too late; they have already been conducted. The NSABB reversed its initial decision and has recommended that the H5N1 avian influenza research be published in full. 38
The H5N1 avian influenza study represents a failure in the life sciences research oversight system. Without external pressure or internal buy-in by the life sciences community, the security community and the public should expect to see more controversial cases like it crop up. It would be far preferable to implement biosecurity measures such as educating grants officers and researchers and reviewing research proposals that meet the criteria of the 7 “experiments of concern” before an unmitigated microbiological disaster forces Congress to pass draconian biosecurity mandates, potentially altering the nature of scientific inquiry in the life sciences permanently.