The National Academies of Sciences, Engineering and Medicine (NASEM) publishes numerous reports each year that are received with high esteem by the scientific community and public policy makers. The NASEM has internal standards for selecting committee members that author its reports, mostly from academia, and vetting conflicts of interest. This study examines whether there were any financial conflicts of interest (COIs) among the twenty invited committee members who wrote the 2016 report on genetically engineered (GE) crops. Our results showed that six panel members had one or more reportable financial COIs, none of which were disclosed in the report. We also report on institutional COIs held by the NASEM related to the report. The difference between our findings and the NASEM reporting standards are discussed.

Competing interests: Sheldon Krimsky is a voluntary, unpaid board member of the non-profit public interest organization The Council for Responsible Genetics. Tim Schwab has no interest to declare other than his being an employee for Food and Water Watch, a non-profit public interest organization. This does not alter our adherence to PLOS ONE policies on sharing data and materials.

Funding: The authors acknowledge the Committee on Faculty Research Awards, Tufts University for their grant to fund the publication of this paper. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Copyright: © 2017 Krimsky, Schwab. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Introduction

During the mid-1980s, the first journals introduced requirements that authors disclose any financial interests they have on the subject matter of their submitted papers. By the early 1990s, the world’s leading science journals and the majority of medical journals had adopted conflict of interest (COI) policies for authors. Soon thereafter, COI policies were established by the National Science Foundation and the Public Health Service for their grant recipients.

Financial COI disclosures by individuals serving on scientific panels responsible for developing guidelines, such as clinical practice guidelines [1], or writing reports on behalf of professional organizations became another arena for transparency of financial COIs. After a study was published highlighting the undisclosed conflicts of interest of panel members who established guidelines in the Diagnostic and Statistical Manual of Mental Illness (DSM-IV), considerable media attention was directed at the American Psychiatric Association, publisher of the DSM volumes, calling for greater transparency [2]. In the next edition of the DSM (DSM-5), conflict of interest disclosures by DSM-5 panel members were cited in the volume.

Disclosure of conflicts of interest by individuals and institutions has become a widely accepted ethical norm and a legal requirement in science and medicine. Failure to disclose medical financial conflicts of interest has even been grounds for a lawsuit against a prominent university [3].

The growth of COI disclosure policies for university researchers was influenced by a body of social science research that discovered a new effect, termed the “funding effect” [4, 5]. This finding showed that studies funded by private companies, compared to independent non-profit and government sources as controls, tended to produce outcomes consistent with the financial interest of those companies [6,7]. The effect can be found in data collection and in the interpretation of results.

The “funding effect” has been reported across a number of fields, including pharmaceuticals [8], chemical toxicology [9], tobacco [10], surgery [11], mobile phones [12], nutrition [13], and biotechnology. Diels et al. (2011) examined research on genetically modified crops and found that “COIs through professional affiliations or direct research funding are likely to influence the final outcome of such studies in the commercial interest of the involved industry [14]. Another meta-analysis documented widespread conflicts of interest in published research about efficacy and durability of genetically engineered crops, and also found that the presence of conflicts was associated with favorable outcomes to agricultural biotechnology companies [15].

Federal advisory bodies The federal government had long established conflict of interest requirements for its employees and for members of Congress, but scientists and experts serving on federal advisory committees were not covered under those regulations prior to 1972 when the Federal Advisory Committee Act (FACA) was passed. Under FACA, scientists invited to serve on federal advisory committees are prohibited from holding substantial conflicts of interest on matters before the committee on which they serve. This applied to all federal agencies including the Food and Drug Administration, the National Institutes of Health and the Centers for Disease Control. The Federal Advisory Committee Act set certain principles for government agencies when setting up advisory committees. The act stipulated that balance, independence and transparency were requirements for establishing a federal advisory committee. The General Services Administration (GSA) was given the responsibility for developing regulations and guidance for federal agencies that establish advisory committees under FACA and the Office of Government Ethics (OGE) was responsible for issuing regulations on conflicts of interest for advisory committee members (see 18 U.S.C §208). In addition to the requirements of GSA and OGE, federal agency heads have responsibility for issuing guidelines and management procedures for addressing conflicts of interest on advisory committees they appoint. Members who serve on federal advisory committees are defined as special government employees, appointed by a government agency to perform certain temporary duties, with or without compensation [16].

The national academies The NASEM, a private, non-profit institution chartered by Congress, has always functioned as an advisory body to federal agencies and Congress since it was established in 1863. It recruits scientists from academia, industry and non-profit organizations, who serve on an unpaid basis to author studies and provide technical consultation to the government. Nevertheless, the organization did not fall under the Federal Advisory Committee Act in 1972. The Academies receive hundreds of millions of dollars in annual contributions from private and public sources [17], and it has long maintained close ties to industry that have raised conflicts-of-interest allegations—at times directed at the committees of invited scientists that author its reports [18]. A 1970 committee examining the health effects of lead came under scrutiny because several committee members were employed by companies producing lead additives [19]. Shortly after, a committee examining food chemicals and cancer drew controversy because some members were consultants to the food industry, which was also providing funding to the committee [19]. In amendments made to FACA in 1997, specific COI requirements were laid out for committees of the NASEM, at that time called the National Academy of Sciences [20]. Congress noted that federal agencies could not utilize the scientific advice of the Academy unless the following instructions were heeded: no individual appointed to serve on the committee has a conflict of interest that is relevant to the functions to be performed, unless such conflict is promptly and publicly disclosed and the Academy determines that the conflict is unavoidable, the committee membership is fairly balanced as determined by the Academy to be appropriate for the functions to be performed [21]. The NASEM, noting its requirements under FACA, has developed its own conflicts-of-interest guidelines that define a conflict as “any financial or other interest which conflicts with the service of the individual because it (1) could significantly impair the individual’s objectivity or (2) could create an unfair competitive advantage for any person or organization” [22]. The interest in question must be closely related to the work of the committee. According to the NASEM, removing financial conflicts eliminates potentially compromising situations in which others “could reasonably question, and perhaps discount or dismiss, the work of the committee simply because of the existence of such conflicting interests” [22]. This language appears in line with a National Academies’ guidebook of best practices for scientists, “On Being a Scientist” (now in its third edition), which notes that “even the appearance of a financial conflict of interest can seriously harm a researcher’s reputation as well as public perceptions of science” [23]. Despite its attention to conflicts of interest, The Academies’ work continues to raise questions, stemming, in part, from the continued recruitment of scientists who have financial interests in the field studied by committees on which they serve [18]. By 1998, the year after FACA was amended to include The Academies, twenty-four percent of their committee members worked for industry [24]. A 2006 investigation by a public-interest group examined twenty-one NASEM committees, finding that nearly one in five committee members had financial ties to industry [25,26]. Under FACA, the NASEM may appoint scientists with financial COIs, but must make every effort to avoid doing so—and may only do so when it is an “unavoidable” conflict of interest. If the NASEM appoints a committee member with a financial COI, it is obligated to “promptly and publicly” disclose it. Critics have argued that the NASEM does not follow FACA guidelines by virtue of the number of panel members with financial COIs, often undisclosed. One area of the NASEM’s work that has repeatedly drawn criticism around conflicts of interests over the last two decades concerns agricultural biotechnology, as numerous media outlets have reported on a variety of alleged conflicts related to several reports [27–29]. In 2016, the NASEM issued one of its most comprehensive studies on GE agriculture, a topic that has drawn considerable public debate. Because of the importance of this study and the fact that the NASEM has long had a conflicts-of-interest policy in place, we chose to examine this report.

Goals and methods of the study In our study we examine financial COIs among committee members of the NASEM publication issued in May 2016 titled Genetically Engineered Crops: Experiences and Prospects (hereafter the NASEM2016 report). One of the principal objectives of the NASEM2016 report was to assess the “basis of evidence for purported negative effects of GE crops and their accompanying technologies, such as poor yields, deleterious effects on human and animal health, increased use of pesticides and herbicides, the creation of ‘super-weeds,’ reduced genetic diversity, fewer seed choices for producers, and negative impacts on farmers in developing countries and on producers of non-GE crops, and others, as appropriate” [30]. In our study we sought to determine whether there were undisclosed financial COIsamong committee members in the NASEM2016 report. We compared our results on financial COIs with the NASEM’s guidelines and its recommendations on how conflicts of interest among members of its committees are handled. We restricted our analysis to financial COIs—and disregarded other conflicts such as conflicts of commitment or ideological and political positions held by committee members—because an analysis of financial COIs allowed us to draw on well-established criteria from the NASEM and a variety of other guidelines. We examined the conflicts of interest of twenty committee members who developed, wrote, and approved the analysis and made recommendations in the NASEM2016 report. We applied a multi-modal method of ascertaining whether panel members held a financial conflict of interest that involved examining funding sources, patents, company advisory boards and consulting [31]. The following criteria were used to determine the existence of a financial COI. If within three years prior to the start of the study in 2014, a panel member was found to have one or more of the following financial interests related to the subject matter of the report, such findings were recorded as a financial COI for that panel member: (1) holds a patent or patent application on a genetically modified crop or a process involved in producing genetically modified crops. (2) holds equity in a company with a financial interest in the success or failure of genetically engineered (GE) crops; (3) serves or served on an advisory committee of such a company; (4) received research funding, in-kind contributions, or research supplies (other than donated seeds) for work related to GE crops from such a company; (5) employed by such a company, or by a non-profit that is primarily funded by such a company; (6) consults for such a company. These six categories are found in the NASEM’s own definitions of financial COIs, however our criteria differs from the NASEM in two ways. First, the NASEM only considers financial investments, i.e. equity holdings, greater than $10,000 to represents a disclosable financial COI, whereas we placed no threshold on financial investments [22]. The U.S. Department of Health and Human Services, which oversees the National Institutes of Health, recently reduced its reporting threshold from $10,000 to $5,000 [32]. The National Academy of Medicine, in recommendations it issued for biomedical institutions in 2009, determined that no thresholds should be used in financial COI forms, and that all financial relationships should be disclosed for review [33]. It also noted that “Because bias is unintentional and not a matter of corruption, however, small gifts may still produce results and therefore should not be assumed to be benign.” Given the scientific literature showing that the size of a financial relationship may be irrelevant to whether it creates bias, we chose to put no threshold on the value of a committee member’s financial investments [34]. Second, our criteria may also differ from the NASEM’s in the scope of our financial COI review. The NASEM only examines committee members’ “current interests,” noting that it “does not apply to past interests that have expired, no longer exist, and cannot reasonably affect current behavior” [30]. This language is included in the instructions given to committee members on financial COI disclosure forms, who apparently must interpret for themselves whether any of their previous financial relationships could “reasonably affect current behavior” [35]. A number of contemporary guidelines recognize that previous financial relationships can reasonably affect judgment and sometimes require five years of financial COI reporting [36]. The International Committee of Medical Journal Editors (ICMJE) uses three years as the disclosure interval for authors submitting publications to journals [37]. The American Psychiatric Association requires disclosure covering a period of the last three calendar years and the current year [38]. The National Academy of Medicine in 2009 noted that scientific institutions typically review any financial COIs from the previous year, and sometimes review as many as five years of information [39]. We chose a three-year review period. Holding a patent or patent application that is active during one’s tenure on the NASEM2016 committee was sufficient to meet our criteria and also appears to meet the NASEM’s “current interests” standard. However, we cannot be confident that our 3-year reporting period for other categories of financial interests—such as previously having consulted for or received research funding from a company—is what the NASEM and committee members interpreted as a previous financial COI that could “reasonably affect” judgment. The NASEM2016 study began in late 2014, so we examined financial COIs of committee members starting in 2012. Each of the twenty listed committee members was evaluated for financial conflicts of interest from 2012–2016 through reviewing published studies in journals with COI disclosures, committee members’ online biographies or curriculum vitae, databases that list scientist-industry collaborations, news articles that highlight scientists’ company activities, and the United States Patent and Trademark Office’s patent database.

Institutional conflict of interest at the academies Though much of the literature and discussion surrounding the funding effect concerns individual researchers, there is now a growing appreciation of the potential bias introduced through institutional conflicts of interest (institutional COIs). The National Academy of Medicine notes that an institutional COI exists when an “institution’s own financial interests or those of its senior officials pose risks of undue influence on decisions involving the institution’s primary interests” [40]. The Association of American Medical Colleges and American Association of Universities have issued guidelines for human-subject research that enumerate sources of potential institutional COIs, which include “substantial gifts (including gifts in kind) from a potential commercial sponsor” [41]. These guidelines also recommend that institutional leaders establish an organizational culture around conflicts of interest, “demonstrat[ing] to the academic community and to the public that compliance with these policies, including full disclosure of financial conflicts of interest, is an imperative reflecting core institutional values.” The American Association of Universities makes the very broad, unqualified recommendation around institutional COIs to “disclose always” [42]. The NASEM’s conflicts-of-interest policy does not address institutional COIs, and it is not known if or how The Academies addresses this issue. Nevertheless, because the NASEM is a private institution, which receives funding from private entities that may have a financial interest in the NASEM’s work, we examined the role that private entities play in the NASEM’s operations to determine whether institutional COIs exist and if or how they were disclosed.

Findings The NASEM 2016 report discusses its finding that no committee members had financial conflicts of interest. “Every Academies committee is provisional until the appointed members have had an opportunity to discuss as a group their points of view and any potential conflicts of interest related to the statement of task. They also determine whether the committee is missing expertise that may be necessary to answer questions in the statement of task. As part of their discussion, committee members consider comments submitted by the public about the committee’s composition. The discussion takes place in the first in-person meeting of the committee. The committee is no longer provisional when it has determined that no one with an avoidable conflict of interest is serving on the committee and that its membership has the necessary expertise to address the statement of task” [30]. The report stated, without qualification, that the NASEM “did not identify” any conflicts of interest among the twenty panel members. “The Committee on Genetically Engineered Crops did not identify any conflicts of interest among its members. However, in light of comments received from the public before its first meeting and because of two resignations around the time of the first meeting, one new member with experience in molecular biology and two new members with international experience and expertise in sociology were added to the committee. Those appointments brought the committee’s membership to 20. That is a large committee for the Academies, but it ensured that diverse perspectives were represented in committee discussions and in the final report” [30]. By contrast, our inquiry found that six out of twenty committee members had financial COIs (Table 1). Five individuals received research funding from for-profit companies related to the subject matter of the report and five had patents or patent applications on the subject matter of GE crops. Four panel members had two financial COIs. In total there were ten financial COIs among the six committee members, and it would appear that most of these conflicts meet the NASEM’s own standards for financial COIs. PPT PowerPoint slide

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larger image TIFF original image Download: Table 1. Financial Conflicts of Interest of NASEM Panel Members: Committee on Genetically Engineered Crops: Past Experience and Future Prospects. https://doi.org/10.1371/journal.pone.0172317.t001 Five of the six committee members with financial COIs had patents or industry research funding during the time that they served on the NASEM2016 study, which would appear to meet the NASEM’s standard for “current” financial COIs. The only committee member who may not fall under the NASEM’s disclosure criteria was Carol Mallory-Smith, who reported receiving industry research funding in a 2012 journal article. This funding falls within our three-year window, but did not occur while Mallory-Smith served on the NASEM2016 committee and may or may not have met the NASEM’s criteria for a financial COIs. In all cases, the financial COIs concerned private interests that have a financial interest in the promotion of genetic engineering, not in opposition to it. Table 1 shows the range of financial COIs found for the panel members and their sources and Table 2 provides the documentation for the financial COI determination. PPT PowerPoint slide

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larger image TIFF original image Download: Table 2. Sources of Financial COIs of NASEM Committee Members. https://doi.org/10.1371/journal.pone.0172317.t002