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Financial Disclosures of Scientific Papers Presented at the 2003 RSNA Annual Meeting: Association with Reporting of Non–Food and Drug Administration–approved Uses of Industry Products¹

¹ From the Department of Radiology (S.D.B., J.C.D.) and Clinical Research Program (L.A.K., S.A.M.), Children's Hospital, 300 Longwood Ave, Boston, MA 02115. From the 2004 RSNA Annual Meeting. Received May 1, 2005; revision requested June 24; revision received August 2; final version accepted September 6. Address correspondence to S.D.B. (e-mail: Stephen.brown@childrens.harvard.edu).

	ABSTRACT

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Purpose: To retrospectively characterize the extent and nature of financial relationships with industry that are disclosed in the abstracts of scientific papers presented at the 2003 Radiological Society of North America (RSNA) Annual Meeting and to retrospectively assess whether the presence of relationships between researchers and industry was associated with a discussion on the use of products or devices that are not yet approved by the U.S. Food and Drug Administration (FDA).

Materials and Methods: Printed abstracts of scientific papers published in the 2003 Radiological Society of North America Scientific Assembly and Annual Meeting Program were classified according to the number and type of financial relationships disclosed. Also recorded was whether the abstracts discussed non–FDA-approved use of a product. Abstracts with and those without disclosures were then compared by using the Fisher exact test with respect to the percentage of abstracts that reported non–FDA-approved use.

Results: Of the 1549 published abstracts, 271 (17%) disclosed at least one author with financial ties to a company whose products or services were reported. The most common disclosures were for authors who were employees (39%), corporate grant recipients (34%), corporate consultants (23%), or shareholders (18%) of the corporation whose product was studied. A total of 87 (32%) of 271 abstracts with disclosed corporate relationships discussed non–FDA-approved use of a commercial product compared with 197 (15%) of 1278 abstracts with no disclosed tie to industry (P < .001).

Conclusion: RSNA abstracts in which authors disclosed corporate financial relationships were twice as likely as those without such disclosures to discuss non–FDA-approved use of a commercial product. This raises the possibility that corporate relationships may influence radiology research.

© RSNA, 2006

	INTRODUCTION

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Financial relationships between industry and medical academia are ubiquitous (1,2). They involve institutional arrangements that support clinical, research, and educational activities, as well as financial relationships between individual investigators and the companies that sponsor their research (2–4). There is a long-standing concern that biases due to personal financial ties with industry may influence the direction and outcome of research (4–8). This includes influence on the selection of research topics, although such influences may be more difficult to assess empirically than biases in methods and outcomes (7).

Findings reported in both the general media and academia suggest that drug and device manufacturers sometimes use financial incentives to steer investigators toward evaluating and promoting product applications that maximize commercial potential in lieu of more fundamental research (9–13). Some claim that such behavior has included the encouragement of research on products and applications that are not yet approved by the U.S. Food and Drug Administration (FDA) (14,15). Focus on non–FDA-approved applications may greatly broaden commercial opportunities, as illustrated by the observation that revenues for non–FDA-approved uses of certain prominent medications have far surpassed revenues for approved uses of these same medications (9,10,16–18).

This does not necessarily imply that pernicious motives are inherent in the conduct of such research. Investigating non–FDA-approved uses of medical products often represents innovative work. Any financial remuneration stemming from it may simply be an indication that industry (and ultimately society) rewards innovation. Indeed, some have observed that the indication-specific approval process mandated by the FDA creates an impediment to innovation (19). Furthermore, because background premarketing data are often required prior to the approval of a drug or device application, such research must first be performed in a non–FDA-approved setting and can be a natural part of the approval process.

On the other hand, commercial interests are often strongly inherent in the design of these preapproval studies (20). At times, the data from such studies have been used inappropriately by industry for promotional purposes (21). Of course, once a product is granted FDA approval for one indication, clinical uses for non–FDA-approved applications are less tightly regulated (19). In certain instances, companies and investigators may have deliberately chosen to conduct research on non–FDA-approved product applications rather than perform a long-term or complete analysis of the product for FDA-approved indications, an appropriate comparison against directly competing products, or an evaluation of unfavorable issues associated with approved uses, such as complications (1,14,15,20–23).

Critics maintain that such actions sometimes reflect an unhealthy conflation of clinical research design and marketing strategy in the course of medical product development (18,20,21). Over the past several years, a perceived link has emerged between the presentation of data on non–FDA-approved applications for medical products at scientific and educational forums and the intentional marketing of these products (9,10,12,16,17,24).

The FDA, other federal agencies, and numerous professional organizations have sought to manage these and other perceived conflicts of interest by issuing guidelines and principles for disclosure and compliance (2,12,13,24–28). Scientific meetings, such as that of the Radiological Society of North America (RSNA), and well-respected journals, such as Radiology, have attempted in earnest to comply rigorously with the increasing demand for disclosure compliance. Those who present data at the RSNA Annual Meeting and in Radiology are required to make disclosures not only of any financial interests they have in the research they are conducting but also of whether they are discussing non–FDA-approved use of a product (29).

To the best of our knowledge, no studies have assessed the extent to which radiology researchers have personal financial relationships with industry or whether an association exists between the presence of financial interests and the investigation of non–FDA-approved product applications in radiology. Thus, the objectives of our study were to retrospectively characterize the extent and nature of financial relationships with industry that are disclosed in the abstracts of scientific papers presented at the 2003 RSNA Annual Meeting and to retrospectively assess whether the presence of relationships between researchers and industry was associated with a discussion on the use of products or devices that are not yet approved by the FDA.

	MATERIALS AND METHODS

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Data Recording
The RSNA asks that all authors of scientific abstracts published in the 2003 Radiological Society of North America Scientific Assembly and Annual Meeting Program disclose any "affiliation or financial relationship with companies or organizations about whose products or services they are reporting" (29). Disclosures are required at the time of submission and (if present) are listed at the end of each abstract. Two readers (S.D.B., J.C.D.) jointly reviewed authors' disclosures for the first 100 abstracts and created financial disclosure categories. One reader (J.C.D.) then applied these categories to all of the abstracts and conferred with the second reader (S.D.B.) on those disclosures for which questions arose about how best to categorize them. Also recorded was whether the authors disclosed reporting on the non–FDA-approved use of a product. The RSNA asks authors to report any discussion of "the unlabeled use of a commercial product, device, or pharmaceutical that has not been approved for such purpose by the FDA" (29).

Types of Relationships
We classified abstracts according to the types of relationships, as described by authors in their financial disclosures. Any disclosure by at least one author with a financial tie to a company whose products or services were reported was classified as a corporate relationship. We considered the following disclosures to represent corporate financial relationships: owner and/or chief executive officer, employee, shareholder, recipient of corporate grant, research support, honoraria, nonmonetary support, investigational agent provided by a company, educational sponsorship, patent license, member of an advisory board, beta site tester, paid speaker, research agreements, and corporate fellow. The following relationships were not considered to entail financial relationships with corporate entities ("noncorporate relationship"): noncorporate financial support, university grant, American College of Radiology grant, RSNA grant, National Institutes of Health grant, or other government grant.

Radiologic Subspecialties
We categorized radiologic subspecialties according to their designation in the program book and further subdivided them according to the nature of the subject matter (ie, clinical or nonclinical [informatics, health services, or physics]). Clinical subspecialties included breast imaging, cardiac imaging, chest radiology, gastrointestinal radiology, genitourinary radiology, musculoskeletal radiology, neuroradiology, nuclear medicine, pediatric radiology, radiation oncology and radiobiology, ultrasound, and vascular and interventional radiology. We included all ultrasound-related categories within the ultrasound specialty. These included gastrointestinal ultrasound, genitourinary ultrasound, and musculoskeletal ultrasound.

Statistical Analysis
Proportions were compared with the ² test or Fisher exact test. Two-sided P values are reported. Prevalence rate ratios comparing abstracts with versus those without corporate ties are reported with 95% confidence intervals. Homogeneity of rate ratios for different abstract categories was assessed by testing for interactions between corporate disclosures and abstract categories in a generalized linear model, with the logarithm of the proportion of abstracts reporting non–FDA-approved use as the outcome variable. All statistical analyses were performed with a commercially available software program (SAS, version 9.0; SAS Institute, Cary, NC).

	RESULTS

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Classification of Abstracts and Disclosures
A total of 1549 abstracts were published in the 2003 Radiological Society of North America Scientific Assembly and Annual Meeting Program. Overall, 271 (17%) of the 1549 abstracts disclosed at least one author with a corporate financial tie (Table 1).

Only 39 (3%) of 1549 abstracts provided any type of noncorporate disclosure. Three abstracts made two different noncorporate disclosures for a total of 42 different disclosures in 39 abstracts. These included two authors who described themselves as university employees, two who received university grants, three who received RSNA or American College of Radiology support, nine who received National Institutes of Health grants, and 13 who received government grants. A total of 13 authors described noncorporate financial support, without further specification.

Analysis of Abstracts with Corporate Disclosures
Among the 271 abstracts with corporate disclosures (Table 2), 100 (37%) had one author with a corporate disclosure, 74 (27%) had two authors with corporate disclosures, and 97 (36%) had three or more authors with corporate disclosures. Of the 97 abstracts that had three or more authors with corporate disclosures, 26 had three authors with corporate disclosures, 27 had four authors with corporate disclosures, 16 had five authors with corporate disclosures, 20 had six authors with corporate disclosures, three had seven authors with corporate disclosures, two had eight authors with corporate disclosures, one had nine authors with corporate disclosures, and two had 10 authors with corporate disclosures. Authors were not given a list of disclosure types to choose from and there was great variability in the reported types of disclosure, with more than 15 different types reported (Table 2). The most common disclosures were for authors who were employees (39%), corporate grant recipients (34%), corporate consultants (23%), or shareholders (18%) of the corporation whose product was studied. There were also other less common disclosures (Table 2).

	DISCUSSION

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Overall, 17% of abstracts had authors who disclosed personal financial relationships with the corporate sponsors of their research. This is consistent with more broadly focused reports in the literature on the prevalence of such relationships among academic faculty and authors who publish biomedical research (1,30). The most common corporate relationships disclosed were for authors who were employees, corporate grant recipients, corporate consultants, or shareholders of the corporation whose product was studied. However, categories were not mutually exclusive, and, as has been described in reports outside of Radiology, many abstracts had authors disclosing multiple relationships with corporate sponsors (2,30). A total of 15% of abstracts in clinical subcategories contained at least one author with a corporate financial interest, ranging from 8% for radiation oncology and radiobiology abstracts to 39% for chest radiology abstracts. This variation among clinical subcategories suggests that some fields of radiology have more prevalent ties to industry than others. Nearly one-third of abstracts in nonclinical subcategories had authors with corporate ties, which is primarily attributable to relationships disclosed in the physics and radiology informatics subcategories rather than in the health services, policy, and research subcategory.

The finding that radiology researchers with financial ties to industry focus to a greater degree (twice as often) on the evaluation of non–FDA-approved uses of medical products than do researchers without such ties is consistent with concerns that corporate financial relationships may influence the selection of research topics (7). Because we investigated only the association between commercial involvement and the evaluation of non–FDA-approved uses of drugs and devices, our study results do not provide direct evidence that industry ties influence or affect radiology research. Because we did not systematically analyze the content of each abstract for a potential commercial effect, we cannot confirm more specific assertions that researchers with corporate financial relationships are more likely to concentrate on studies that have commercial applicability (4,31), nor can we conclude definitively that financial incentives influenced investigators to perform clinical research designed specifically to evaluate non–FDA-approved applications of various products.

Investigators with an independent interest in non–FDA-approved uses may be more likely than those without such interests to seek funding from industry. Conversely, industry may pursue relationships with investigators whose work is already focused on non–FDA-approved or commercial product applications (32). In both cases, the a priori interests of the researchers and industry are well aligned and complementary; our data may simply reflect this dynamic.

Even so, less benign explanations for the association we have demonstrated also merit consideration. There are enormous potential market opportunities for non–FDA-approved product applications. The conduct of industry-sponsored research has considerable academic and financial rewards for faculty and institutions (32). A significant association has been observed between the level of industrial research support received by academic faculty in the life sciences and both the frequency of commercial outcomes and their stage of advancement (4). Numerous empirical analyses across a wide range of medical disciplines have demonstrated that industry funding may compromise investigator objectivity (1,12,22,33). Industry funding is acknowledged to compromise the impartiality of information that is discussed by speakers at medical education symposia (13,25).

In light of these issues, our findings portray the possibility that, in addition to more well-disposed intentions, the financial interest and corporate ties of individual investigators at the RSNA Annual Meeting may have provided motivation to test and discuss non–FDA-approved uses for radiologic devices, contrast agents, and other diagnostic and therapeutic products. Further exploration of potential incentives for radiology researchers who present data at major meetings will require a survey of the reasons why presenters select certain topics and the potential influence that commercial companies may have on their decision making.

A more rigorous analysis of these data, including blinded review of the content of each abstract for issues such as whether the abstract reported on a product, might yield more definitive results. The authors of some abstracts may not have reported on products at all, rendering the distinction between FDA-approved and non–FDA-approved use irrelevant. However, several important limitations to the available data are intrinsic to the present analysis.

First, the RSNA itself does not categorize disclosures; the types of relationships detailed in this study were not standardized and reflect those provided by the authors. We do not know which relationships were short term and involved a relatively small amount of money and which were more complex. Stratification of the level and nature of support may help define problematic relationships more succinctly (26). Occasionally, because of a lack of uniformity in how the types of relationships were described by abstract authors, subjective judgments had to be made during classification. A more standardized mechanism for reporting disclosures, with specific coding options and categories of support, might enable a more objective and systematic analysis.

Second, while there is no reason to suspect underreporting of corporate financial relationships in the authors' disclosures, we cannot verify the frequency of undisclosed relationships. Steinbrook (25) has suggested that the disclosure of commercial relationships by the faculty and providers of continuing medical education has at times not been in accordance with expectations. It is possible that authors who are investigating non–FDA-approved uses of products are more diligent in reporting their commercial relationships. Abstract writers who recognize that a conflict may exist may merely be indicating their relationships more often.

Similarly, it is difficult to confirm whether the number of noncorporate relationships was reported accurately. Other analyses of financial relationships in academic medicine suggest that the percentage of researchers with funding from nonprofit agencies substantially exceeds the 2.5% of abstracts with such funding found in this study (30). In cases of nonprofit funding, the recipient gains no direct financial benefit, and the funding agency has no profit motive. Thus, the low rate of reporting of nonprofit funding may reflect a perception that such funding does not constitute, or poses less of a risk for, a conflict of interest. While this view seems reasonable, it may be appropriate for the RSNA to consider revising its conflict of interest policy to clarify whether such funding should be reported. Because of the small number of these disclosures in our study, we could not analyze whether government or other noncorporate relationships were associated with the reporting of research on non–FDA-approved product applications.

Another potential source of bias in this analysis is that the disclosure information was collected from the Radiological Society of North America Scientific Assembly and Annual Meeting Program alone and not from the oral presentations. Gathering such information would have been logistically onerous but leaves open the possibility that a certain number of disclosures were not made in the program but were made during the oral presentations themselves.

In addition, it is difficult to verify the appropriateness of the application of non–FDA-approved designations by various abstracts. In some instances, it may have been underreported. For example, none of the abstracts in which authors discussed the use of an intraarticular injection of gadolinium-based contrast agent for magnetic resonance arthrography disclosed that this is a non–FDA-approved use of this contrast agent. Alternatively, some abstracts may have applied the specification unnecessarily. Further, because many forms of information technology do not require FDA approval, the presence of such abstracts in the analysis could bias our measured association, depending on the proportion with financial disclosures.

Finally, the small clinical and nonclinical subcategory sample sizes limit our ability to detect significant variation in the association between corporate ties and the reporting on non–FDA-approved product use.

In conclusion, we found that abstracts of scientific papers presented at the 2003 RSNA Annual Meeting in which authors disclosed financial relationships with a corporate entity whose products were studied were significantly more likely to discuss non–FDA-approved uses of a product than abstracts without such disclosures. This raises the possibility that financial interests of individual investigators and sponsoring companies may influence what products are tested and for what indications.

	ADVANCES IN KNOWLEDGE

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• Financial ties to industry are present among authors of scientific abstracts presented orally at the RSNA Annual Meeting.
  
• Those abstracts with authors who have financial ties to industry are significantly more likely than those without to discuss the non–FDA-approved use of a medical product.
  

	ACKNOWLEDGMENTS

 
The authors thank N. Thorne Griscom, MD, and Sara R. Brown, MPH, for their editorial assistance and Rhonda K. Johnson, BA, for her assistance in manuscript preparation.

	FOOTNOTES

 

Abbreviations: FDA = Food and Drug Administration • RSNA = Radiological Society of North America

Authors stated no financial relationship to disclose.

See also the editorial by Becker in this issue.

Author contributions: Guarantors of integrity of entire study, S.D.B., J.C.D.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, S.D.B., J.C.D.; statistical analysis, J.C.D., L.A.K., S.A.M.; and manuscript editing, all authors

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