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Mechanisms of Peer Review

Inappropriate and Appropriate Selection of 'Peers' in Grant Review

(JAMA. 1994;272:114-116)

Stanton A. Glantz, PhD, Lisa A. Bero, PhD

Objective.--To assess the members of the California Tobacco Related Diseases Research Program Behavioral and Public Health Research on Tobacco Study Section and those of the Agency for Health Care Policy and Research (AHCPR) Dissemination Study Section as "peers" to review tobacco policy research. Both study sections reviewed a similar grant application on tobacco policy research written by one of us (S.A.G.).

Design.--Search of MEDLINE for 1989 through 1993 with the keyword tobacco for Tobacco Related Diseases Research Program and AHCPR reviewers. As a control, the National Institutes of Health Cardiovascular Study Section, which reviewed a ventricular function grant submitted by the same author with the keyword heart, was analyzed.

Setting.--Not applicable.

Patients or Other Participants.--Study section members.

Interventions.--None.

Main Outcome Measures.--Publications by study section members in areas germane to the proposal being reviewed.

Results.--Six (33%) of 18 Tobacco Related Diseases Research Program reviewers had no "tobacco" publications (median, two publications; interquartile range, zero to four). The members' "tobacco" publications concentrated on well-controlled experimental interventions on smoking cessation and prevention strategies, not tobacco policy. Only one member had primary expertise in tobacco policy research. None of the AHCPR reviewers had "tobacco" publications. All 31 (100%) of the National Institutes of Health reviewers had "heart" publications (median, nine publications; interquartile range, seven to 19). Five members had a primary interest in the subject of the National Heart, Lung, and Blood Institute application.

Conclusions.--Study section members' professional interests play a critical role in the level of interest and enthusiasm they will have for a proposal, which affects the priority score. In contrast to the study section that reviewed the heart grant, the study sections that reviewed the tobacco control grant were not "peers." The membership of these review committees has effectively precluded research on tobacco control policy.

(JAMA. 1994;272:114-116)


THERE IS A strong consensus among tobacco control professionals that public policy interventions hold great potential for reducing the burden of tobacco-induced disease and death.[1] As a result, both the State of California Tobacco Related Disease Research Program (TRDRP)[2] and the National Cancer Institute (NCI)[3] have solicited research on tobacco control policy. Despite this expressed interest, these organizations have not actually supported much research in this area.

Peer review is the centerpiece of the modern scientific review process, including decisions regarding grant funding. The cornerstone of the peer review process is that work is reviewed by peers. The dictionary definition of peer is "a person or thing of the same rank, value, quality, ability, etc.; equal; specifically, an equal before the law."[4] In scientific terms, a "peer" would be an individual with expertise and knowledge in the area in question that meets or exceeds that of the applicant. To function appropriately, the people selected as peers must not only have methodologic depth, but also a broad understanding of the field in question, particularly the questions that are important to address. Without this breadth, innovative work is often passed over purely on the basis of methodologic considerations.[5] Thus, the composition of the study section becomes the key issue in assessing whether a grant receives peer review. Review of the membership of the TRDRP Behavioral and Public Health Research on Tobacco Study Section demonstrates that, while suitable for reviewing experimental trials of smoking cessation, it does not represent a committee of peers for research in the area of tobacco control policy research. As a result, the study section applies inappropriate experimental standards to policy research and underrates its importance. A similar situation exists at the National Institutes of Health (NIH).

MATERIALS AND METHODS

Publications of Study Section Members

This report presents the results of the analysis of the peers selected to review three grants submitted by one of us (S.A.G.). Two of these proposals, one submitted to TRDRP and one submitted to the NCI, were in the area of tobacco policy research. The NCI proposal was referred to the Agency for Health Care Policy and Research (AHCPR) for review. One proposal, submitted to the National Heart, Lung, and Blood Institute, was in the area of basic studies of cardiac mechanics. None of these proposals initially received priority scores high enough to receive funding. (Both proposals were subsequently funded after revision and resubmission.)

A widely accepted, although imperfect, measure of scientific expertise is publication in the peer-reviewed scientific literature.[6] [7] To assess the qualifications of the members of the study sections as peers in the area of tobacco policy research, we searched the National Library of Medicine MEDLINE database for the period from January 1, 1989, through May 26, 1993, for members of the TRDRP Behavioral and Public Health Research on Tobacco Study Section and AHCPR Dissemination Study Section. This database contains 1,541,832 citations from medical and health sciences journals. The searches were performed by means of the Uni- versity of California Melvyl MEDLINE system with the following command: Find pa [personal author] StudySectionMember and kw [keyword] tobacco. Although this search was not exhaustive, it could be expected to give some indication of the areas related to tobacco in which members of the study section qualified as experts.

As a control concerning the qualifications of the members of these study section, we compared them with the NIH Cardiovascular Study Section, which reviews the applicant's NIH grant for basic research in ventricular function, substituting the term heart for tobacco in the search.

Nature of TRDRP Awarded Grants

To investigate whether biases inherent in the selection of study section membership influences the overall portfolio of grants awarded by TRDRP, we reviewed all grants awarded for three annual funding cycles (fiscal years 1990, 1991, and 1992) and categorized each one into one of the following mutually exclusive categories, by means of the published abstracts[8] [9] [10] of the grants: policy: grants that have direct impact on the formulation or measurement of tobacco control policies, such as studies of taxation or implementation of indoor air regulations; environmental tobacco smoke (ETS): grants that study the health effects or the physical distribution of ETS (these include basic science studies, clinical studies, and engineering studies); epidemiology: studies that use epidemiologic techniques (eg, case control, cohort studies) to examine the relationship between active smoking and disease or factors that contribute to smoking (studies of ETS epidemiology were categorized as ETS); prevention/cessation: evaluation of tobacco prevention or cessation programs, implementation of prevention or cessation programs, and studies that identify factors that contribute to the prevention or cessation of smoking (eg, a study of social factors among Asian Americans that contributed to the cessation of smoking); nicotine/addiction: grants that study the physiologic or pharmacologic actions of nicotine, including cellular pathways (eg, comparison of nicotine and caffeine and models of addiction; this category included basic science studies and clinical studies); and disease: all biomedical research on diseases that is related to tobacco, but that might not be directly linked to tobacco use (eg, general mechanisms of cancer genesis, but not necessarily lung cancer). This category is divided into two subcategories: clinical and basic science. Clinical research includes studies in humans that look at the effects of tobacco smoking on the pathophysiologic characteristics of certain diseases or the effect of pharmacologic interventions to treat disease. Basic science studies include animal, in vitro, cellular, or molecular studies that explore the mechanisms of action underlying some of the disease processes that have been related to smoking, such as seeking gene markers for atherosclerosis or cancer.

RESULTS

Publications of Study Section Members

Of the 18 members of the TRDRP Behavioral and Public Health Research on Tobacco Study Section, six (33%) had no publications indexed on tobacco, and two had only one citation. The median number of citations was two, and the interquartile range was zero to four. Examination of the publications of those members who had publications indexed with the term tobacco disclosed that these publications were concentrated in clinical and school-based smoking cessation and prevention and smokeless tobacco use. The primary focus was on well-controlled experimental interventions, such as randomized controlled trials of smoking cessation and prevention strategies. This expertise and publications in well-controlled experimental interventions are not particularly relevant for assessing the methods of a tobacco policy application. Only one member had primary expertise in tobacco policy research (two publications). During the same period, the applicant had seven publications indexed on the keyword tobacco; only one member of the study section had more than seven publications indexed on tobacco.

Of the 19 eligible members of the AHCPR Research Dissemination Study Section, none had citations indexed on the term tobacco.

Of the 31 members of the NIH Cardiovascular Study Section, all (100%) had publications related to the heart. The median number of citations was nine, with an interquartile range of seven to 19. Five members had a primary interest in the area of ventricular function, the subject of the applicant's National Heart, Lung, and Blood Institute application. During the same period, the applicant had 11 publications indexed on the keyword heart; 13 (42%) of the Cardiovascular Study Section members had more than 11 publications. Thus, all members of the study section had demonstrated expertise in heart research, with a number of publications similar to that of the applicant whose work they were reviewing. Nearly half of the members of the study section had more publications than the applicant. Five members had direct experience in the area of the application.

Nature of TRDRP-Funded Grants

As shown in the Table, funds allocated to areas directly related to tobacco (policy, ETS, epidemiology, prevention/cessation, and nicotine/addiction) have steadily fallen from 54% of all funds in cycle 1 to 30% of all funds in cycle 3, with funding for general biomedical research increasing from 47% to 70% of funds. The decline in resources allocated to policy has been particularly precipitous, from 8% of funds to only 1%. Similar, although slightly less dramatic, changes have taken place when the analysis is based on the number of grants.

COMMENT

The differences between the study sections that reviewed the tobacco policy grants and the Cardiovascular Study Section are extremely important in ensuring a real peer review.[11] The professional interests of the members of a study section play a critical role in the level of interest and enthusiasm they will have for an investigation of a given question. These judgments affect how important the reviewers consider the questions to be investigated, and this judgment directly affects the priority score. By this standard, the NIH Cardiovascular Study Section members are "peers" for the reviews of basic investigations of ventricular mechanics. In contrast, TRDRP had the tobacco policy grant reviewed by a study section whose primary area of expertise was smoking cessation and prevention interventions with a strong experimental orientation; the presence of a single member whose primary interest was in tobacco control policy is not enough to overcome the biases intrinsic in this membership. It is interesting that in the first year, TRDRP had a separate study section devoted to tobacco policy grants; in that year a much higher portion of funds went to tobacco policy grants than in the second or third years.

A similar situation exists at the NIH, including the AHCPR study section that reviewed the grant for the NCI. Most tobacco grants go to the Behavioral Medicine Study Section. This study section is renowned as a graveyard for tobacco control research. (Because of this reputation, the applicant requested that the Behavioral Medicine Study Section not review the tobacco control grant.) According to the Division of Cancer Prevention and Control Board of Scientific Advisors, of the past 41 cancer prevention and control grant applications submitted to the Behavioral Medicine Study Section, not one has been funded.[12] The board found (written communication from M. Alfred Hayes, MD, chairman, Board of Scientific Counselors, Division of Cancer Prevention and Control, NCI, to Bernadine Healy, MD, director, NIH, June 19, 1993) that this problem extended beyond tobacco control policy research to prevention issues in general and concluded that

"at this time there is no true peer review of extramural applications for community-based cancer prevention and control research. This serious omission in the NIH peer review system is serving to bar an entire field of research from NIH funding, therefore retarding the advancement of knowledge in an area critical to improving the nation's health."

Although assignment of a grant proposal to a study section composed of peers is crucial for a quality review of the proposal, the selection of the study section by the Division of Research Grants at the NIH appears to be somewhat arbitrary. Both of us responded to the NCI program announcement seeking proposals on tobacco control policy research.[3] The application by one of us (S.A.G.) was to study the political activity of the tobacco industry in response to tobacco control efforts, particularly as they relate to clean indoor air legislation designed to reduce ETS exposure by the health community. The proposal by the other of us (L.A.B.) was to examine the quality and use of tobacco industry-sponsored research on ETS. Although the specific topics of the two proposals were different, they both focused on the activities of the tobacco industry to influence policy regarding ETS. It would have been appropriate for both grants to have been reviewed by similar peer reviewers. However, S.A.G.'s grant was assigned for review by the AHCPR Research Dissemination Study Section, and the Division of Research Grants declined to review L.A.B.'s grant. After a formal protest and a 6-month delay, the grant was assigned to the AHCPR Health Services Development Grant Study Section. Like the Research Dissemination Study Section, none of the 18 members of the Health Services Development Grant Study Section had any publications indexed on tobacco. The assignment of the two grants to different study sections, neither of which had expertise in tobacco policy research, suggests that the qualifications of the study section members as peers to review the proposals were not considered by the Division of Research Grants.

The membership of the Behavioral Medicine Study Section is similar to that of the TRDRP study section. The selection of reviewers for TRDRP and resulting biases in the peer review process have led to an important lost opportunity. We used a generous criterion for assessing expertise in tobacco, by using tobacco rather than tobacco policy as the criterion for evaluating publications of study section members. While every reviewer need not be an expert on tobacco, a reasonable number of members should have a broad understanding of the field in question, not just methodologic expertise. Even with this loose standard, few members of the TRDRP study section, and none of the AHCPR study section members, were "peers" in the area of tobacco-related research in general, much less tobacco control policy research in particular. The TRDRP is the only research program in the world devoted to tobacco. As such, it was in a unique position to nurture a strong research environment on tobacco-related problems. Instead, TRDRP has been evolving into simply one more place for biomedical scientists to seek funding for their work because tobacco causes so many diseases.

In spring 1993, the California legislature recognized the problems with the TRDRP and amended the authorizing legislation to require TRDRP to give high priority to research in tobacco control policy.[13] In response, TRDRP issued a request for proposals in tobacco policy research and convened a new study section with expertise in tobacco policy to review these applications. The governor vetoed this bill on September 25, 1993, saying that the program should be reevaluated in the context of all tobacco control programs funded by the California tobacco tax.

AFTERWORD

One of us (S.A.G.) revised and resubmitted both grants described in this article to the NIH. The ventricular mechanics grant, which initially received a 16th percentile priority score and was not funded, received an 11th percentile score and was subsequently funded. The tobacco control policy grant was resubmitted together with a letter making essentially the same arguments concerning problems with the peer review it received. The priority score of the original grant was 92nd percentile; the revised grant received a ninth percentile score and was funded. An appeal was filed with TRDRP making essentially the same arguments concerning problems with the peer review process; TRDRP rejected this appeal and did not grant reconsideration of the proposal.


From the Department of Medicine, Institute for Health Policy Studies (Drs Glantz and Bero), Cardiovascular Research Institute (Dr Glantz), and Division of Clinical Pharmacy (Dr Bero), University of California-San Francisco.

Presented in part at the Second International Congress on Peer Review in Biomedical Publication, Chicago, Ill, September 10, 1993.

This study was supported by funds provided by the Cigarette and Tobacco Surtax Fund of the State of California through the Tobacco-Related Disease Research Program of the University of California (awards IRT 520 and 2KT 072).

Reprint requests to Division of Cardiology, Department of Medicine, Box 0124, University of California, San Francisco, CA 94143-0124 (Dr Glantz).


References

1. Chapman S. Upgrading the academic respectability of advocacy studies. Tobacco Control. 1993;1:81-83.

2. University of California Tobacco Related Diseases Research Program, Call for Proposals. Oakland: University of California; 1992.

3. Division of Cancer Prevention and Control Research Program Announcement (PA-92-61). In: NIH Guide for Grants and Contracts. Bethesda, Md: National Institutes of Health; March 27, 1992.

4. Neufeldt V, Guralnik DB, eds. Webster's New World Dictionary. New York, NY: Webster's New World Dictionaries; 1986:996.

5. Horrobin DF. The philosophical basis of peer review and the suppression of innovation. JAMA. 1990;263:1438-1441.

6. Knoll E. The communities of scientists and journal peer review. JAMA. 1990;263:1330-1332.

7. Garfunkel JM, Lawson EE, Hamrick HJ, Ulshen MH. Effect of acceptance or rejection on the author's evaluation of peer review of medical manuscripts. JAMA. 1990;263:1376-1378.

8. Tobacco Related Diseases Research Program. Annual Report to the State of California Legislature, 1991. Oakland: University of California Office of Health Affairs; 1991.

9. Tobacco Related Diseases Research Program. Annual Report to the State of California Legislature, 1992. Oakland: University of California Office of Health Affairs; 1992.

10. Tobacco Related Diseases Research Program. Annual Report to the State of California Legislature, 1992. Oakland: University of California Office of Health Affairs; 1993.

11. Cohen J. Study sections: does a superb system need a tune-up? Science. 1993;261:1678-1679.

12. DCPC advisors to consider seeking prevention and control study section. Cancer Lett. 1993;19(20):5.

13. Senate Bill 1088, as amended, August 15, 1993.

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