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Commercial influence and the content of
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Commercial influence and the content of medical journals
Joel Lexchin, Donald W Light
How confident should we be in the objectivity of medical journals? Do commercial biases play a partin determining what appears in print? Authors of articles in medical journals may be affected Reasons for non-disclosure were that disclosure is by commercial bias. Whether this same concern unnecessary, that editors do not have conflicts, and that applies to the editors and owners of journals has rarely been critically examined.1 2 Our article explores the An article about the benefits of escitalopram reasons for concern. We use information in the (Lexapro) over citalopram (Celexa) provides an exam- literature on three important questions. Do financial ple of apparent editorial conflict of interest. The article, conflicts of interest affect decisions made by journal by Jack M Gorman, was published in a special supple- editors? Do journals have policies on authors’ conflicts ment of CNS Spectrums, a neuropsychiatric journal that of interest, and how well do editors enforce those poli- he edits. The article, which was published at a time cies? Do financial considerations affect the content of when the patent for citalopram was expiring, medical journals? We end with a proposal for future concluded that escitalopram significantly improved research that would help to advance this debate.
primary endpoint efficacy scores in trial subjects “much sooner” than did citalopram and was “well- tolerated.” Dr Gorman was a paid consultant to Forest Sources of bias
(which marketed both drugs), and Forest paidMedworks Media, the publisher of CNS Spectrums, to Government organisations and societies of health pro- print the article,8 although Dr Gorman stated at the fessionals can also influence journal content. A former time the article was published that he was not paid per- editor of JAMA was fired by the American Medical sonally to write it.” A comparison of these two drugs Association because of political sensitivity over an published in Medical Letter, an independent drug bulle- article on oral sex that he published at the time of tin with no advertising, found no difference between President Clinton’s impeachment.3 An article in CMAJ on the information requested by pharmacists before Editors might not pursue aggressive conflict of dispensing postcoital contraception was changed after interest policies in their journals and may fail to complaints by the Canadian Pharmacists Association enforce existing policies. A 1999-2000 survey of the 24 about whether the research was ethical.4 However, we basic science journals and 24 clinical journals with the think that the greatest potential for bias comes from highest immediacy index rankings (how fast the commercial influences, hence the direction of ourarticle.
average article in a particular journal will be discoveredand cited) found that only 20 of the 47 that respondedreported having policies for the disclosure of conflictof interest.10 Definitions of conflict of interest varied Conflicts of interest
greatly, and disclosure of certain conflicts could be Because journal editors have a great deal of control avoided; for instance, 10 journals required disclosure over original scientific articles, commentaries, and edi- of income and equity interests, but only seven asked for torials, any commercial bias due to their own conflict of patent ownership to be reported, and only one interest would affect the content of their journals.5 required appearances of conflicts to be reported.
Only one systematic study has examined editors’ poli- Despite recent improvements in five leading medical cies on conflict of interest (financial and non-financial).
journals in the proportion of articles declaring conflict Nine of 30 peer reviewed general and internal medical of interest, 8% (13 of 163) original articles published journals, including the top four by impact factor (a from December 2003 to February 2004 in four major measure of frequency of citation), had an explicit journals failed to declare conflicts.11 12 Narrowly defining policy for dealing with editors’ financial conflicts of conflicts and not vigorously enforcing journal policies interest. Only eight of the remaining journals intended may result in editorial decisions that lead to the publica- to declare such conflicts in the next couple of years.
tion of articles with a commercial bias.
BMJ VOLUME 332 17 JUNE 2006
Revenue from advertisements in six major US medical associations and journals % of membership
Organisation
Annual ($m)
% of total
assessments
Journal of American College of Cardiology American Journal of Respiratory and Critical Commercial supplements
do not routinely report details of their sources ofrevenue, such as subscriptions, journal advertisements, Journal supplements are a good example of how financial considerations can influence the editorial Companies may refuse to advertise in journals that content of medical journals. Supplements are mostly publish articles that are critical of the drugs industry. In paid for by drug companies and usually contain 1992, the Annals of Internal Medicine published an articles about a single drug marketed by the company.
article that critically examined the scientific accuracy of These articles are usually based on papers presented at advertisements for drugs in 10 leading medical symposiums sponsored by drug companies. Because journals.16 Reviewers (doctors and pharmacists) judged the publisher is paid according to the number of that 34% should have been revised before publication, papers in each supplement, lax standards for these and 28% should not have been published. After publi- articles will generate more revenue than stricter stand- cation of this article, the decrease in drug advertise- ards.1 As a result, the scientific quality of most papers in ments in the Annals was greater than in four leading supplements is inferior to those published in the main general medical journals (figure).17 The journal lost an estimated $1-1.5 million in advertising revenue bypublishing the study.18 The editor said, “The episoderevealed the true colours of the pharmaceutical indus- Marketing reprints
try, which was willing to flex its considerable muscleswhen it felt its interests were threatened.”19 The poten- Most high profile, peer reviewed journals produce tial effects of articles on advertising revenue may con- press releases for newsworthy articles to generate sciously or subconsciously affect editors’ decisions media attention. Greater media attention leads to about publication or may influence which authors are more subscriptions, more advertising, and the sale of article reprints, all of which result in greater revenue.
In some journals, marketing considerations seem Journals aggressively advertise reprint sales, as shown to be more important than editorial decisions. Despite by an advertisement on the web page of the BMJ: three good peer reviews, the editor of a leading neph- rology journal, Transplantation and Dialysis, rejected an exhibitions/seminars and sales support campaigns editorial questioning the value of epoetin in end stage and for mailing new product information to doctors renal disease. The editor admitted to the author of the (and for distribution) to conference delegates and visi- editorial, “I have been over-ruled by our marketing tors at exhibitions.”14 Companies may spend up to $1million (£0.53m; €0.77m) on purchasing reprints, andthe former editor of the BMJ, Richard Smith, thinks that this situation can create a conflict for journal edi-tors: “Publish a trial that will bring US$100 000 of profit or meet the end-of-year budget by firing aneditor.”1 2 Revenue from journal advertising
One study looked at the revenue from journal advertising as a proportion of the total income of six non-profit making doctors’ organisations that owned Decrease in number of drug advertisements July 1992 to December 1994 compared with journals.15 Five organisations obtained more than 10%of their gross income from advertising in theirjournals, and in four cases as much (or nearly as much) money was generated from advertising as from members’ fees and “other assessments” (table). The Changes in advertising revenue for five leading medical journals after authors concluded, “potential financial conflicts of Annals of Internal Medicine published an article that criticised interest arising from pharmaceutical advertisements in advertisements for drugs in medical journals medical journals may be substantial.” Of note, journals BMJ VOLUME 332 17 JUNE 2006
department with regard to publishing your editorial . . .
the publication of your editorial would, in fact, not be Summary points
accepted in some quarters . . . and apparently wentbeyond what our marketing department was willing to Most general and clinical medical journals do not have policies on conflicts of interest for their Without drug advertising, journals are economi- cally vulnerable. Only two general medical journalshave stopped advertising drugs, and one of these had to stop publication a little more than three years after supplements bring in substantial revenue for the Non-profit making doctors’ organisations may Recommendations for action
receive more revenue from advertising in journalsthan from members’ fees Commercial bias in medical journals owing to financialpressure or editors’ conflicts of interest would Journals do not seem to be able to survive without represent a fundamental threat to the credibility of journals and to science as a whole. The studies citedhere provide evidence for concern about commercial Articles in medical journals that criticise the drug influence. In this light, we recommend some easily industry can result in substantial loss of implemented measures to help alleviate these con- Journals should publish detailed information about Systematic research is needed to determine their sources of income, including the amount they get whether commercial interests influence the from the sale of reprints, supplements, and advertising; At a minimum, editors should follow the recom- mendations of the Committee on Publication Ethics(COPE), a forum for editors of peer reviewed journals Publishing medical journals is not a charitable ven- formed to discuss issues related to the integrity of the ture, even when the owners are non-profit making scientific record. Editors should disclose their own medical societies. Considerable financial resources are relevant conflicts of interest to readers and consider needed to publish high quality journals, and owners disclosing those of their editorial teams, editorial and editors are vulnerable to economic pressures that may threaten the intellectual integrity of their journals.
Journals should consider not allowing editors to The medical community should objectively and have any direct financial ties (for example, stock dispassionately investigate whether this concern is a ownership, speaker’s fees, advisory board participation) to any healthcare business that advertises in the journal Contributors and sources: JL has been conducting research into pharmaceutical policy for more than 20 years and has authored The International Committee of Medical Journal or coauthored more than 60 peer reviewed articles in this area, Editors (ICMJE) or a similar organisation such as the as well as serving as a consultant to various national World Association of Medical Editors should design a governments and the World Health Organization on pharma-ceutical matters. DL is a professor of comparative healthcare template for journals that would record the wide range policy, a contributor to the WHO observatory volume on Euro- of financial interactions that authors might have with pean pharmaceutical policy, and a member of the taskforce for commercial entities and journals should publish these the Gates Foundation on how best to make vaccines for global authors’ statements in full, either in print or electroni- diseases economically viable. DL had the initial idea for the article. JL did most of the literature searching and retrieval andwrote the various drafts. DL made intellectual contributions to Editors should consider publishing earlier versions the analysis of the literature and helped with revisions. Neither of manuscripts on the internet together with reviewers’ of the authors received any financial rewards for writing this and editors’ comments, so that readers can see how the tone and content of articles was changed. This information could help detect the origin of any bias.
All journals should be strongly encouraged to Smith R. Medical journals and pharmaceutical companies: uneasybedfellows. BMJ 2003;326:1202-5.
adopt these recommendations so that those that coop- Smith R. Medical journals are an extension of the marketing arm of erate will not suffer financially compared with those pharmaceutical companies. PLoS Med 2005;2:e138.
Hoey JCC, Elmslie T, Flegel KM, Joseph KS, Palepu A, Todkill AM.
Science, sex and semantics: the firing of George Lundberg. CMAJ In addition, the influence of commercial interests Kassirer JP, Davidoff F, O’Hara K, Redelmeier DA. Editorial autonomy of on medical journals should be investigated systemati- cally. A respected and independent body, such as the Wilkes MS, Kravitz RL. Policies, practices, and attitudes of North Ameri-can medical journal editors. J Gen Intern Med 1995;10:443-50.
Institute of Medicine in the United States, should study Haivas I, Schroter S, Waechter F, Smith R. Editors’ declaration of their the past five years’ contents of a selection of leading own conflict of interest. CMAJ 2004;171:475-6.
medical journals and look for bias in articles that deal Schroter S. A survey of editors’ conflicts of interest. In: White C, ed. TheCOPE report 2003: annual report of the committee on publication ethics.
with specific drugs and pharmaceutical policy in general. Such a study would allow comparisons Petersen M. Madison Ave has growing role in the business of drugresearch. New York Times 2002 November 22; sect A: 1.
between journals and over time to detect trends in Escitalopram (Lexapro) for depression. Medical Letter 2002;44:83-4.
publications. The results should be reported to the 10 Van McCrary S, Anderson CB, Jakovljevic J, Khan T, McCullough LB, Wray NP, et al. A national survey of policies on disclosure of conflicts of interest in biomedical research. N Engl J Med 2000;343:1621-6.
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11 Hussain A, Smith R. Declaring financial competing interests: survey of 16 Wilkes MS, Doblin BH, Shapiro MF. Pharmaceutical advertisements in five general medical journals. BMJ 2001;323:263-4.
leading medical journals: experts’ assessments. Ann Intern Med 12 Goozner M. Unrevealed: non-disclosure of conflicts of interest in four leading medical and scientific journals. Washington DC, US: Centre for Science in 17 Landefeld C, Chren M, Siddique R. A 4-year study of the volume of drug the Public Interest, 2004. www.cspinet.org/new/pdf/unrevealed_final.pdf advertisements in leading medical journals. J Gen Intern Med 13 Cho M, Bero L. The quality of drug studies published in symposium pro- 18 Altman LK. Inside medical journals, a rising quest for profits. New York ceedings. Ann Intern Med 1996;124:485-9.
Times 1999 August 24; sect F: 7.
14 Ray J. Judging the judges: the role of journal editors. Q J Med 19 Fletcher RH. Adverts in medical journals: caveat lector. Lancet 15 Glassman PA, Hunter-Hayes J, Nakamura T. Pharmaceutical advertising 20 Dyer O. Journal rejects article after objections from marketing revenue and physician organizations: how much is too much? West J Med department. BMJ 2004;328:244.
The price of independence
Joe Collier
Career pressure and a focus on payment by results are making the critical and impartial thinker anendangered species. Society must take steps to protect this invaluable resource My professional life has been dominated by a drive to ensure that every opinion or piece of advice I give is independent and seen as such. Independence first became an issue for me in 1969 when I edited my first article for Drug and Therapeutics Bulletin.1 The then editor, Andrew Herxheimer, made my responsibilitiesclear: I was to scrutinise all the relevant published data, read and note all of the comments made by article reviewers, and use all this information to prepare the article for publication, ensuring clarity, reliability, andimpartiality. The published article must reflect the sci- entific knowledge available and distinguish what was known about the product from what was derived from conjecture, bias, or the uncritical position of the estab- lishment. Moreover, there would be no place for myown (preconceived) biases. Readers were to be giveninformation they could trust and be confident that theadvice given had no hidden agenda no ulterior motive.
Four decades on, and I am still discovering the full implications of these ideals. Their meaning becamemore pertinent when I was appointed the bulletin’sdeputy editor in 1972, then its editor in 1992, and a have conflicts of interest often find giving clear advice year later when it coined the strapline, “The independ- (or opinions) particularly difficult.
ent review for doctors.” Perhaps, more importantly, the Advice also needs to target the recipients’ needs ideals have taken on new dimensions as they have and respond to their concern or question, whether the shaped my career as teacher, researcher, physician, recipient is a patient, a government minister, a administrator, writer, broadcaster, and adviser.
committee, or one of millions of people listening to abroadcast or reading an article. How advice or opinion What is independence and does it
is couched and delivered will depend on the particular circumstances. Sometimes it will be signalled simply bythe act of raising your hand to vote at a meeting, some- In the context of this article, independence relates to times be spoken as part of the rapid deliberations of intellectual function, the way our minds process infor- the busy committee, sometimes be more measured (as mation to make decisions; ultimately, it is the way we when presenting a report), and sometimes argued in make up our minds and, as advisers, give our opinions.
detail (as in an article in a medical journal). Whatever What has emerged over the years is that my views the method, the responsibilities of the independent have needed to be much more than independent. To be of real value, they have needed to be delivered in away that the message was clear, pertinent, honest, and Sources of bias
unambiguous. Advice that can be misinterpreted orleaves room for misunderstanding is often unusable So what influences might undermine impartiality? In and may be dangerous. In my experience, people who advice relating to medicines, drug companies are BMJ VOLUME 332 17 JUNE 2006

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