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Industry representatives stated publicly that the TIRC was formed to fund independent scientific research to deter- mine whether there is a link between smoking and lung cancer. However, internal documents from Brown and Williamson Tobacco Company have shown that the TIRC was actually formed for public relations purposes, to con- vince the public that the hazards of smoking had not been proven.17
Research proposals to federal organizations or large foun- dations are typically reviewed by other researchers before funding is approved. Although the CTR had a Scientific Advisory Board consisting of well-respected researchers, not all of the research funded by CTR was peer-reviewed by this board. Beginning in 1966, tobacco industry lawyers became directly responsible for many of the funding decisions of CTR. From 1972 to 1991, CTR awarded at least $14.6 million in special project funding.26 Lawyers were not only involved in selecting projects for funding, but also in designing the research and disseminating the results of the selected projects.26
The research funded by CTR, although initially useful for public relations, became increasingly important for the tobacco industry’s activities in legislative and legal settings. This evolution is described in an April 4, 1978, memo from Ernest Pepples, Brown and Williamson’s Vice President and General Counsel, to J.E. Edens, the company’s Chairman and CEO:
Originally, CTR was organized as a public relations effort. . . . The research of CTR also discharged a legal respon- sibility. . . . There is another political need for research. Recently it has been suggested that CTR or industry re- search should enable us to give quick responses to new developments in the propaganda of the avid anti-smoking groups. . . . Finally, the industry research effort has in- cluded special projects designed to find scientists and medical doctors who might serve as industry witnesses in lawsuits or in a legislative forum.17
Center for Indoor Air Research. The Center for Indoor Air Research (CIAR) was formed by Philip Morris, R.J. Reynolds Tobacco Company, and Lorillard Corporation in 1988.28 The founding companies were joined by Svenska Tobaks A.B., a Swedish domestic tobacco company in 1994.28 The stated mission of CIAR was “to create a focal point organization of the highest caliber to sponsor and foster quality, objective research in indoor air issues including environmental to- bacco smoke, and to effectively communicate research find- ings to a broad scientific community.”29 CIAR’s mission state- ment was modified in 1992 to eliminate the reference to environmental tobacco smoke.30 The elimination of research on secondhand smoke from the mission statement was fol- lowed by a reduction in CIAR-funded research on health effects of secondhand smoke. Instead, CIAR emphasized research on other contaminants in indoor air, a shift in the research agenda of CIAR to prevent the answering of ques- tions about the health effects of secondhand smoke.
CIAR awarded funding for “peer-reviewed” projects after review by a Science Advisory Board and for “special-reviewed” projects after review by a Board of Directors consisting of tobacco company executives.28 From 1989 to 1993, CIAR
awarded $11,209,388 for peer-reviewed projects and $4,022,723 for special-reviewed projects.28 Seventy percent of the peer- reviewed projects funded by CIAR examined indoor air pol- lutants other than tobacco smoke, diverting attention from secondhand smoke as an indoor air pollutant.
In contrast, almost two-thirds of CIAR’s special-reviewed projects were related to secondhand smoke.28 In addition, most special-reviewed projects studied exposure rather than health effects. The tobacco industry may have been funding research through CIAR to develop data it could use to sup- port its frequent claim that levels of exposure to second- hand smoke are not sufficient to cause disease.31
Six CIAR-funded investigators testified at government hearings in the 1990’s. All of their statements supported the tobacco industry position that secondhand smoke exposure is not harmful to health. Data from two of CIAR’s special- reviewed projects were presented at hearings held in 1994 by the Occupational Safety and Health Administration re- garding its proposed indoor air quality regulation. Data from a third special-reviewed project was presented at a Congres- sional hearing in 1989 related to a proposed ban on smok- ing on commercial aircraft. One CIAR-funded study was investigated extensively by the Congressional Subcommittee on Health and the Environment after it was cited in testi- mony before numerous government agencies. The study concluded that, with good building ventilation, clean air could be maintained with moderate amounts of smoking32
and was used to support testimony that indoor smoking restrictions are not necessary. However, the Congressional Subcommittee found that data for this study had been al- tered and fabricated. An earlier CIAR-funded study by the same research organization was also severely compromised because the Tobacco Institute selected the sites where pas- sive smoking levels were measured for the study.28
The CIAR was disbanded as part of the Master Settle- ment Agreement in 1998. However, in 2000, Philip Morris created the Philip Morris External Research Program (PMERP) with a structure similar to that of CIAR. Grant applications were reviewed by a group of external peer re- viewers, a science advisory board, or an internal anonymous review and approval committee. Three of the six advisory board members had a previous affiliation with CIAR. The majority of the named reviewers also had previous affilia- tions with the tobacco industry.33
STRATEGY 2: PUBLISH RESEARCH THAT SUPPORTS THE INTEREST GROUP POSITION
Research has little impact unless it can be cited. The tobacco industry has realized that the funding of research that sup- ports its interests must be followed by the dissemination of this research in the scientific literature. The tobacco indus- try uses several vehicles to publish the findings of its spon- sored research, including symposium proceedings, books, journal articles, and letters to the editor in medical journals. To suggest that the research it funds meets scientific stan- dards and that there is substantial support for its position, the tobacco industry then cites its industry-funded, non- peer-reviewed publications in scientific and policy arenas.
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Symposium proceedings The tobacco industry has sponsored numerous symposia on secondhand smoke34 and paid for scientific consultants to organize and attend these meetings.19,21,35 From 1965 to 1993, the proceedings of 11 symposia on secondhand smoke were published. Six were published as special issues of medical journals, while five were published independently as books. None of these publications were peer-reviewed. Six of the symposia were sponsored by the tobacco industry or its affiliates such as CIAR, the Tobacco Institute, or Fabriques de Tabac Reunies, Neuchatel, Switzerland. Two of the six indus- try-sponsored symposia did not explicitly acknowledge in- dustry sponsorship. The tobacco industry has sometimes sponsored conferences through independent organizations so that its sponsorship would be hidden.26,34
The symposia on secondhand smoke were held across the world, including Europe, the United States, Canada, Japan, and Argentina. The proceedings of one symposium were published in Spanish. CTR special projects funds were often used to support scientists to prepare talks for confer- ences and to send scientists to conferences.17
On the surface, symposium presentations often look like peer-reviewed journal articles. To test the hypothesis that symposium articles on secondhand smoke differ in content from those appearing in scientific journals, two colleagues and I34 compared the articles from symposia on secondhand smoke to a random sample of articles on passive smoking from the scientific literature and to two consensus reports on the health effects of passive smoking.36,37 Of the sympo- sium articles, 41% (122/297) were reviews, compared with 10% (10/100) of journal articles. Symposium articles were significantly more likely to agree with the tobacco industry position that tobacco is not harmful (46% vs. 20%), less likely to assess the health effects of passive smoking (22% vs. 49%), less likely to disclose their source of funding (22% vs. 60%), and more likely to be written by tobacco industry– affiliated authors (35% vs.6%) than journal articles. Sympo- sium authors published a lower proportion of articles that were peer-reviewed (71% vs. 81%) and were more likely to be affiliated with the tobacco industry (50% vs. 0%) than the consensus report authors.34 Symposium proceedings can potentially have a disproportionate influence on policy be- cause they are often cited as if they are peer-reviewed articles, as if they are balanced reviews of the scientific literature, and with no disclosure of their industry sponsorship. For example, research presented at tobacco industry–sponsored symposia on secondhand smoke has been used to attempt to refute both peer-reviewed journal articles and risk assess- ments.38–40 Symposia have been cited in tobacco industry public relations materials and the lay press.31 Positions taken by symposium presenters were described as the consensus of a gathering “of leading experts from around the world”41
who disagreed with the published literature on secondhand smoke.
Quality of tobacco industry–funded symposium publications When policy makers, judges, lawyers, journalists, and scien- tists are presented with tobacco industry–sponsored sympo- sium articles, they must decide whether to incorporate these publications into their deliberations. Although the lack of
balance and lack of peer review suggest that tobacco industry– sponsored literature is not scientifically rigorous, the asso- ciation of peer review and study quality is a contentious subject. Therefore, we assessed the methodological quality of the research presented in symposia. Articles from pharma- ceutical industry–sponsored symposia have been found to be poor in quality.42,43 Barnes and I hypothesized that articles from tobacco industry–sponsored symposia would be poorer in quality than peer-reviewed journal articles.24 We evaluated characteristics of articles that we hypothesized might be as- sociated with quality, such as the disclosure of the source of research sponsorship, article conclusion, article topic, and study design.
We compared original research articles on the health effects of secondhand smoke published in peer-reviewed journals to those published in non-peer-reviewed sympo- sium proceedings from 1980 to 1994.24 Peer-reviewed ar- ticles were of better quality than symposium articles inde- pendent of their source of funding, the conclusion drawn about the health effects of secondhand smoke, or the type of study design.24 Peer-reviewed articles received higher scores than symposium articles for most of the criteria evaluated by our quality assessment instrument.
Quality of tobacco industry–sponsored review articles Review articles are often relied upon by policy makers and clinicians to provide accurate and up-to-date overviews on a topic of interest.44 Furthermore, reviews on the health ef- fects of secondhand smoke comprise a large proportion of tobacco industry-sponsored symposium articles34 and are fre- quently cited in response to government requests for infor- mation on tobacco regulations.38,40,45 Therefore, it is some- what disconcerting that published review articles often differ in the conclusions they reach about the adverse health ef- fects of secondhand smoke.
Barnes and I evaluated review articles on the health ef- fects of secondhand smoke to determine whether their con- clusions were primarily associated with their quality or other article characteristics.23 Our a priori hypotheses were that review articles concluding that passive smoking is not harm- ful would tend to be poor in quality, published in non-peer- reviewed symposium proceedings, and written by investiga- tors with tobacco industry affiliations. We also examined the topic of the review and the year of publication as potential confounding factors.
In our sample of 106 review articles, the only factor asso- ciated with concluding that passive smoking is not harmful was whether the author of the review article was affiliated with the tobacco industry.23 Tobacco industry–funded re- views were about 90 times as likely as reviews funded by any other source to conclude that passive smoking was not harm- ful. Thus, sponsorship of review articles by the tobacco in- dustry appears to influence the conclusions of these articles independent of methodological quality.
The tobacco industry has argued that independent re- views of secondhand smoke are flawed because studies with statistically significant results are more likely to be published than studies with statistically nonsignificant results.46 The industry argues that publication bias—the tendency to pub- lish work with statistically significant results—prevents the identification of all relevant studies for reviews of health
