The following excerpt is reprinted with permission from The Trouble With Medical Journals (Taylor & Francis, 2000).
‘Redundant publication’ means republishing material that is closely related to material already published. There are many circumstances in which this is perfectly acceptable if the connections between the papers are made explicit. Often, however, researchers repeatedly publish closely related papers without making clear the connections. This might seem to be simply impolite and not a serious problem. Indeed, that’s how most academics view redundant publication, but I want to try and convince you that it’s an important problem —because it introduces a bias into medical evidence. The result may be that treatments seem more effective than they are, misleading doctors and patients. Bias also arises from failing to publish studies altogether, another common problem.
Academics, as I keep repeating, gain credit from publishing. The credit comes as much — and possibly more — from the quantity than from the quality of publication. There is thus a strong incentive to slice up studies into the smallest possible unit in order to maximize the number of publications that might result from any piece of research. This is known as ‘salami’ publication. You may also benefit from publishing the same material repeatedly.
You publish a case report of a patient with a new condition. Then you publish a series of three patients followed by another paper describing 20 patients. Next you might make a comparison with another group of patients or give an account of how the condition affects the kidneys, then the heart. Perhaps you participate in an international study of the patients. The Australian results are published in an Australian journal, the Brazilian results in a Brazilian journal, and so on for 15 countries. You, as a world authority and discoverer of the condition, are an author on all of the papers. You review all your studies, sometimes on your own initiative, sometimes at the invitation of editors. Very soon you can have dozens of publications, a professorship, an international reputation and invitations to international conferences in exotic places. (‘A successful scientist,’ a longstanding joke goes, ‘is one who converts data into airmiles.’) At each conference you give closely related papers that are published in supplements to journals.
When somebody attempts a systematic review of your work he or she will become very confused. Are the same patients being described repeatedly? What is new material and what is old material being recycled? The confusion is particularly profound if the author has obscured the links. The reviewer finds what he or she thinks is a new study but takes time to realize that it’s the same as a study reported in another journal. Worse, the studies are often not by one person but by several. Authors are trading authorship. Sometimes the same studies have the same authors, but often the authors appear in different combinations and different orders.
Medical evidence is in this way polluted. As I hope I’ve made clear in chapter 6, medical studies are hard to do and to interpret. Making sense of medical evidence — or as it’s pretentiously called, the medical literature — is hard if everything is optimal, but this pollution makes the job much harder.
I am perhaps being too cynical. A minority of researchers are wickedly and consciously inflating their publications through deception, but it requires both concentration and integrity to minimize rather than maximize the number of papers you publish from a given body of work. There is the ever present pressure — from your head of department, the university, your own insecurity — to publish more, and there are what sound like good reasons for publishing more rather than fewer papers. Too much material in one paper will make it indigestible for readers. You need to reach different audiences with papers with different emphases in different journals. It would be impolite to your charming host at that conference in Rome to refuse to write a paper. Your lecture in Beijing had enough new material to merit a paper, and the new material would not make sense if you didn’t include a considerable amount of the material you had already published.
Another group with an interest in material being republished is the pharmaceutical industry. Research and marketing have become intertwined, as I will discuss further in chapter 16, and the publication of a trial favourable to a company’s product in a major journal is worth hundreds of thousands of dollars spent on advertising. Furthermore, big trials cost millions of dollars to perform. Companies would thus like to see as many publications as possible coming out of trials. Many trials are conducted in several countries at once. As well as publishing the overall results in an international journal it might seem reasonable to publish the German results in a German journal, the French in a French journal, and so on. The German results will have an author who is an acknowledged leader in Germany, prompting German doctors to pay close attention to and trust the work. Sometimes the German and French results will be combined. Sometimes there will be yet another combination. It might so happen that emphasis will be given to the more favourable results. Favourable comments by leading doctors and researchers are invaluable, and they thus receive many invitations to speak at conferences, some of them huge, which are mostly funded by the industry. The industry also funds supplements to journals to report material presented at the conferences. These reports commonly include recycled material.
Editors and journals tend to see themselves on the side of the angels in this vexed issue of redundant publication, but that is to oversimplify. Although some journals are overwhelmed with material, many are not — and are by no means unwilling to publish material closely related to material already published. Many journals are keen to have the ‘top experts’ write for them and don’t worry too much if the ‘top expert’s’ paper is not much different from 50 he has already published. Supplements can be an important source of revenue and profit to journals and commonly contain recycled studies. The BMJ when I was editor was involved in republishing material. We had local editions of the BMJ in many countries and regions, including the United States, China and South Asia, and these reproduced material published in the weekly BMJ. We always, however, provided a reference to the original publication, and only the original publication is referenced in databases like Medline.
Editors and authors often tussle over whether papers are redundant or not. Editors see redundancy where authors see effective communication. Arguing over the degree of overlap and how much it matters can be fruitless, but what is important is transparency. Ideally, when submitting a study authors should send editors at the same time copies of any related material, published and unpublished. In addition, the manuscript should make clear any links to other material, particularly published material. And this should be done not with a reference half way through the discussion of a paper but with a clear statement at the beginning.
With such openness editors cannot accuse authors of misconduct. They may, however, decline to publish the paper submitted.
Often, however, authors are not open, and various studies have suggested that something like one-fifth of medical studies are redundant (177-180). In other words, redundant publication is common. It is the form of misconduct most commonly seen by the Committee on Publication Ethics. But does it matter? The world has tended to see it as sloppiness, a minor misdemeanour, but might it be more?
A group from Oxford have provided the most compelling evidence on how redundant publication can be misleading and potentially dangerous. They conducted a systematic review of the effectiveness of a drug called odanstetron in reducing the sickness that patients commonly experience after an operation (178). The group found 84 trials that included information on 11,980 patients. But when they looked closely they found that there were in reality only 70 trials and 8645 patients. In other words, 17% of the studies had been published more than once and the number of patients had been inflated by 28%. The Oxford group confirmed this duplication of results by going back to the original authors. The published papers did not make clear that trials had been published more than once. The duplication was covert.
The reviewers had to work hard to spot the duplication. One trial had been conducted in several centres, which is very common for trials of drugs. The results from the overall trial had been published, but then researchers from four centres had published their part of the trial. These papers all had different authors, adding to the difficulty of spotting that they were the same trial. It’s easy to understand the temptation of both the authors and the pharmaceutical company to publish in this way. The authors get a publication to themselves, and the companies have the benefits of their drug publicized four times — in different journals and probably different countries.
In addition, four pairs of identical trials, the Oxford group found, were published by completely different authors without any common authorship. This has to be misconduct. I discussed in chapter 9 how authorship carries both credit and accountability. Readers and editors need to know who did the work. Clearly in these reports important information is missing. The work reported is the same but the authorship is completely different. This is deception.
Equally worrying was the Oxford group’s finding that duplicate reports used different numbers of patients or patient characteristics from the original. In another trial the sex distribution was different in the two reports. We will all be inclined to think that this is sloppiness not misconduct, but such discrepancies are always worrying.
Thus far this study from Oxford had confirmed what we already knew — that redundant publication is common, that the redundant studies often don’t refer to each other, and that often the authorship is different. The group then went on to look at which studies were most likely to be duplicated, and — perhaps you’ve guessed already — it was the ones with the most positive results. The group presented the results as ‘number needed to treat’ — which means the number of patients you needed to treat in order to stop one patient from vomiting. (Clearly the lower the number the more effective the treatment. This is a measure that seems to be useful for both doctors and patients. Often dozens of patients need to be treated in order to prevent one death, heart attack, or whatever.) The number needed to treat for the trials that were not duplicated trials was 9.5, while it was 3.9 for the duplicated trials. In other words, the duplicated trials suggested that the drug was more than twice as effective. If all the trials were combined without duplication the number needed to treat was 6.4, whereas if reviewers had combined all the trials without spotting the duplication the apparent number needed to treat improved to 4.9. The effectiveness of the treatment was overestimated by one-quarter.
Authors of systematic reviews — which, as I’ve discussed, are widely regarded as the best evidence on which to base decisions about treating patients — do not usually go to the lengths of the Oxford group to exclude results that are published more than once. It was a major undertaking to do so, made much more complicated by the lack of cross references and the change in authorship. Systematic reviews may thus be routinely misleading patients and doctors because of redundant publication, which is why redundant publication is serious.
Perversely, I believe, some people see this as a problem not of redundant publication but of systematic reviews. It’s important to recognize, however, that systematic reviews simply do systematically what reviewers and doctors do more haphazardly — synthesize evidence. The problem lies not with the systematic review but with the underlying evidence. The Oxford group illustrated this in its review by showing how various experts and a textbook had cited duplicate publications without recognizing that they were duplicates.
How can we respond to the problem of redundant publication? Perhaps the first response should be to cease regarding it as simply impoliteness. It is more — and may be very much more. Prevention must be next, producing and promoting codes of good practice — as, for example, the Committee on Publication Ethics (COPE) has done. Authors should be actively encouraged to send editors any other papers related to their submissions. This can be done through guidance to authors (which are famously unread) and through specific reminders at the time of submission. Reviewers may sometimes spot duplicate publication, and the best reviewers will do a search for related papers. The electronic world may make it easier to spot redundant publication, although it may also make it easier to publish redundantly — as outlets proliferate and it becomes ever easier to copy and transmit words and data.
What about punishment? Editors like other groups divide into hawks and doves. Some see redundant publication as a dreadful sin (more sometimes because it wastes their resources rather than distorts and pollutes medical evidence) and want redundant publishers punished by their employers, publicly shamed, and perhaps banned from receiving further submissions to their journal for some period. Certainly if redundant publication is detected after publication then ‘notices of redundant publication’ should appear in both journals — to alert readers of both journals to the redundancy. The figures suggest, however, that such a notice appears for perhaps one in a thousand cases. Redundant publication seems to be like speeding, so common a ‘crime’ as to be normal. Nevertheless, when I was at the BMJ if we identified a case we tended to bring it to the attention of heads of departments, deans or employers — largely to raise consciousness of the problem and its consequences.
I doubt, however, that we will make much progress while redundant publication is seen as a trivial issue. We will probably make even slower progress with a common sin of omission — simply not writing up and publishing studies. Iain Chalmers, one of the founders of the Oxford Cochrane Collaboration, has argued this is a form of misconduct, and slowly but surely he is being taken seriously (181). Again the problem is that medical evidence is biased, because ‘negative studies’ (studies that find that an intervention doesn’t work) usually are not published and the evidence is consistently biased towards making treatments seem more effective than they actually are (182, 183).
It is well established that negative studies are less likely to be published, and it’s becoming steadily clearer that this is not so much because journals reject them (as has been commonly supposed) but because authors don’t write them up and submit them. People have looked at research protocols approved by ethics committees, doctoral dissertations and abstracts presented at scientific meetings, and followed them up to see if they resulted in publications. Consistently, negative studies are less likely to be published (182-184).
These studies also show that authors are more likely to write up and submit positive studies. Now a large study from JAMA has shown that it is just as likely to publish negative as positive studies (185). This was a study in just one journal and only on particular sorts of trials, but it fits with other evidence suggesting that the problem lies more with authors than editors.
Perplexingly, academics want nothing more than to be published. So paradoxically they may not be writing up and submitting studies because they don’t think that they will be able to get them published, even though that seems not to be the case.
Pharmaceutical companies, in contrast, might prefer not to have negative studies published, and some three-quarters of trials published in four of the major general journals (Annals of Internal Medicine, JAMA, Lancet and New England Journal of Medicine) are funded by the industry (186). (Interestingly it’s only one-third of those published in the BMJ.) The industry thus has a chance to be highly influential. I think it unlikely that big companies are actively suppressing negative studies, but they may well be less energetic in encouraging their writing up and submission. Many studies have shown that published papers sponsored by pharmaceutical studies are more likely to be positive than studies they have not been sponsored (187, 188). This could be because editors are preferentially selecting positive papers by pharmaceutical companies, but this seems highly unlikely.
As many as one-half of trials reported in summary form are never published in full, and the bias introduced into medical evidence may be huge. Nobody can know the extent of this bias, but there are stories. lain Chalmers quotes the work of RJ Simes, who found that published trials showed that a combination of drugs was better than a single drug for treating patients with advanced ovarian cancer. If unpublished trials were included then the combination was no longer better (181).
Chalmers also tells how failure to publish a study on how best to look after women about to give birth to twins led to an unnecessary delay in moving to the best management (181). Obstetricians were split 50:50 on whether these mothers should be routinely admitted to rest in bed before delivery. A study conducted in Zimbabwe in 1977 showed that the practice actually led to a worse outcome for mothers and babies. But the study wasn’t published until visitors to Zambia learnt about the study years later. Once published in the Lancet the study helped to lead to a change in policy across the world (189).
One response to this failing of people to publish is to raise awareness of the problem, and this has happened to some extent. I used to think of publication bias as a small, almost technical problem, but I’ve increasingly come to think of it as a serious problem — although I’m not sure exactly how serious.
In the late 1990s around 100 journals joined together to publicize an amnesty for unpublished trials (190). We urged people who had conducted trials and never published them to register that the trial had been conducted. Anybody doing a systematic review on the subject could then contact the authors for data. Many dozens of trials were registered, but they must constitute only a tiny fraction of all unpublished trials. This was more a publicity stunt to raise awareness of the problem rather than a solution to the problem.
A much more serious response is the creation of registers of trials underway. The hope is that eventually every trial that begins anywhere will be registered. There are now many registers and a register of registers. American law requires the registration of trials, and the International Committee of Medical Journal Editors now requires trials submitted to journals that follow its guidance to include a registration number (191).
These registers should allow the identification of trials that had been started but never published — and so counteract publication bias. They will also make it easier for doctors to encourage patients with problems where the best treatment is not clear to enter trials.
Those who conduct systematic reviews are well aware of the problem of publication bias, and various statistical techniques have been developed to try and identify missing studies. To identify what is not there is clearly a difficult problem, and no technique can be foolproof. It is even more difficult to try and adjust results to compensate for the missing evidence. Many would say it can’t really be done at all.
I hope that I have convinced readers that publishing studies more than once and failing to publish are both potentially serious problems, not simply minor misdemeanours. The combination of the two — with positive results being published more than once and negative studies not being published at all — may be particularly dangerous. The result can be patients being given toxic and expensive treatments that are thought to work but which in reality don’t.
More From The Trouble With Medical Journals
- Introduction: Medical Journals Are Probably a Force for Good but Need Considerable Reform
- Why Bother With Medical Journals and Whether They Are Honest?
- What and Who Are Medical Journals For?
- Can Medical Journals Lead or Must They Follow?
- What Are and What Should Be the Values of Medical Journals?
- The Complexities and Confusions of Medical Science
- The Death of the Author and the Birth of the Contributor
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