Written evidence submitted by the BMJ Group (PR 41)
This written evidence on behalf of BMJ Group examines the following aspects of the committee’s terms of reference, with particular focus on biomedical publication:
· the strengths and weaknesses of peer review as a quality control mechanism for scientists, publishers and the public
· measures to strengthen peer review
· the processes by which reviewers with the requisite skills and knowledge are identified, in particular as the volume of multi-disciplinary research increases
· the impact of IT and greater use of online resources on the peer review process
· possible alternatives to peer review.
1. Peer review and scientific norms. Peer review embodies all the so-called Mertonian norms of science.  Proposed by US sociologist Robert Merton, these comprise: Communalism (common ownership of scientific discoveries, where scientists give up intellectual property rights in exchange for recognition and esteem [Merton used the term Communism, but did not mean Marxism]), Universalism (claims to truth are evaluated in terms of universal or impersonal criteria and not on the basis of race, class, gender, religion, or nationality), Disinterestedness (scientists are rewarded for acting in apparently selfless ways), and organized Skepticism (all ideas must be tested and subjected to rigorous, structured community scrutiny).
2. Uses of peer review in science. Peer review provides scrutiny to support many elements of academic discovery: approval and funding of research studies; regulation and approval of new drugs and medical technologies; selection of research for presentation at conferences and for publication; and rating and funding of academic staff and departments.
3. Norms for peer review at biomedical journals. The International Committee of Medical Journal Editors (ICMJE) defines journal peer review as "unbiased, independent, critical assessment…by experts who are not part of the editorial staff" and deems it an intrinsic part of all scholarly work. In biomedical publishing several international organisations offer guidance to editors including the International Committee of Medical Journal Editors (ICMJE http://www.icmje.org), the World Association of Medical Editors (WAME http://www.wame.org/), the Council of Science Editors (CSE http://www.councilscienceeditors.org/), and the Committee on Publication Ethics (COPE http://publicationethics.org/). Each develops and promotes regularly updated policies and guidelines on fair, professional, and efficient editorial and peer review practices. Many biomedical editors are doctors or scientists with little relevant experience or training before taking on the role, so publishers and journal owners should point new editors to such guidance and support them while they learn.
4. Costs of peer review. Peer reviewers are rarely paid by publishers, and their work is often done out of hours. Nevertheless, in 2010 a report for JISC Collections, the organisation which supports the procurement of digital content for education and research in the UK, estimated that UK higher education institutions (HEIs) spend - in terms of staff time - between £110 million and £165 million per year on peer review and up to £30 million per year on the work of editors and editorial boards.  The authors of this report also cited a study est imating that, worldwide, peer review costs £1.9 bn annually and a ccounts for about a quarter of the overall costs of scholarly publishing and distribution.  Whether such expenditure represents good value for money is unclear, but the conduct and quality of peer review has been evaluated, and it is that evidence that we will focus on.
Biomedical grant review
5. Current status of grant review. A 2009/10 survey of 28 public and private organisations that give grants for biomedical research in 19 countries, and their reviewers, reported a growing workload of biomedical proposals that is getting harder to peer review.  Organisations reported these problems as frequent or very frequent: declined review requests, late reports, administrative burden, difficulty finding new reviewers, and reviewers not following guidelines. The administrative burden of the process had increased over the past 5 years. About half the responding organisations expressed interest in the development of uniform requirements for conducting grant review and for formatting grant proposals. In a sub-study 258 reviewers from 22 countries reported inadequate support for conducting grant review. Around half said their institutions encouraged grant review, yet only 7% got protected time and 74% received no academic recognition for this work. Reviewers rated these factors as extremely or very important in deciding to review proposals: desire to support external fairness, professional duty, relevance of the proposal’s topic, wanting to keep up to date, desire to avoid suppression of innovation. Most had not been trained in grant review and many wanted such training.
Strengths and weaknesses of journal peer review as a quality control mechanism for scientists, publishers and the public
6. Strengths: journal review has an extensive evidence base. Appraisal of articles submitted to journals is probably the oldest form of formal peer review. It was used by Europe’s first scientific journals - the Journal des Sçavans (later renamed Journal des Savants) and the Philosophical Transactions of the Royal Society of London – when they launched in 1665. Journal peer review is also the most evaluated form; particularly in medical publishing. Many of these evaluations have been presented at the International Congresses on Peer Review and Biomedical Publication (held every four years since 1986) and have then been published in peer reviewed journals, and at the 2009 congress more than 100 studies on peer review were presented (http://www.ama-assn.org/public/peer/peerhome.htm). However, most of this evidence is about identifying the weaknesses of peer review and evaluating its different methods.
7. Strengths: peer review engenders trust. The Science and Technology Committee (Commons) concluded in 2004, when considering developments in open access publishing, that there were "at least three strong arguments, however, for keeping the system of peer review intact. Firstly, volume. .. academics are producing more research articles than ever before: output increases by approximately 3% per year… Secondly, peer review gives successful articles a mark of distinction that helps to provide a measure of the academic's and their department's level of achievement… Thirdly, peer review gives the lay reader an indication of the extent to which they can trust each article." [5, para 205] Peer review remains the best way to engender such trust in scholarly work.
8. Strengths: peer review improves manuscripts. Anecdotally, we know from authors and editors that peer review tends to make articles clearer and more accurate. And now that many journals - including BMJ Open ( bmjopen.bmj.com ) and some BMC journals (BioMed Central. BMC series journals: peer review processes. www.biomedcentral.com/info/authors/bmcseries) - post reviewers’ reports and previous manuscript versions on their websites alongside the published articles, readers can see how reviewers’ comments lead to revisions. The effects of peer review on manuscript quality have not, however, been much researched. Jefferson and colleagues’ 2008 Cochrane systematic review of 28 studies of editorial [journal] peer review, reported that it "appears to make papers more readable and improve the general quality of reporting (2 studies), but the evidence for this has very limited generalisability".  Moreover, they found only one small study testing the validity of peer review. They concluded that "little empirical evidence is available to support the use of editorial peer review as a mechanism to ensure quality of biomedical research. However, the methodological problems in studying peer review are many and complex … t he absence of evidence on efficacy and effectiveness cannot be interpreted as evidence of their absence. A large, well-funded programme of research on the effects of editorial peer review should be urgently launched." Editorial research continues but - as it is mostly conducted by editors interested in their own journals’ practices - it is haphazard, unfunded, and focused on processes rather than outcomes.
9. Weaknesses. We know from experience and evidence that journal peer review has many potential limitations.  Studies have shown peer review to be too slow; overly conservative; unreliable; [8-11] poor at detecting errors and misconduct; open to abuse; skewed towards research with positive results;  biased by conflicts of interest; and systematically biased against authors’ ideas, reputations, locations, and even gender. [13,14] Much submitted work is uncontentious, but controversial work within polarised debates often poses particular challenges to editors trying to find balanced reviews. However, many journals now have policies and practices aimed at overcoming such problems (see below), and those that conduct peer review research should, arguably, focus now on its impact on the quality of published content rather than the quality of their processes.
Measures to strengthen peer review
10. Choosing the right reviewers. For many journals online manuscript handling systems have greatly facilitated the search for and selection of reviewers, making reviewers’ and editors’ decisions quicker and easier to share. These systems usually have a single database that includes invited reviewers, volunteer reviewers, and everyone who has submitted an article via that journal’s online system. Indeed, a survey of more than 3000 academics in 2007 showed that more than 90% of authors were also reviewers.  From several blinded studies we know which type of reviewers tend to deliver the best opinions for medical journals: those who work in reputable institutions, understand statistics and epidemiology, and – perhaps counter-intuitively - are aged under 40 and are not yet in the most senior posts.  Asking authors to suggest reviewers helps to extend a journal’s pool of reviewers and is often invaluable. But editors should note evidence showing that author-selected reviewers - while producing reviews of similar quality –are more likely than editor-selected reviewers to recommend acceptance. 
11. Managing reviewers’ behaviour. The tenth report of the science and technology committee 2003-4 session, Scientific publications: free for all? (para206), cited measures used by four high-profile journals - Cell, The Lancet, Science and Nature - to ensure the integrity of the peer review process.  At these and many other journals (including those of the BMJ Group) authors these measures include not using reviewers with potential conflicts of interest (see para 13 below); having clear policies that reviewers should disqualify themselves on the basis of conflicts of interest; using several reviewers per article to allow for the moderation of opinions; editors’ tracking of reviews submitted by a particular reviewer to monitor consistency; editors’ evaluations and actions regarding claims of reviewer bias or misconduct; and having formal appeals procedures for authors of rejected articles.
12. Ensuring scientific transparency in authors’ articles and reviewers’ reports. The Committee on Publication Ethics (COPE) expects the editors of its more than 4000 journal members worldwide to provide detailed advice on conducting high quality peer review (http://publicationethics.org/files/u2/Best_Practice.pdf). For authors the EQUATOR website (Enhancing the QUAlity and Transparency Of health Research www.equator-network.org/) hosts a wide range of freely available guidance on writing research papers, called "reporting guidelines". Reporting guidelines specify the minimum sets of items required to give a clear and transparent account of the design, conduct, and findings for each type of study in biomedical research. At the BMJ we do not send research articles for external review until they have been reported in line with the appropriate reporting guideline, thus helping reviewers, editors, and readers to fully evaluate and understand the methods and results and any limitations and biases within the research.
13. Declaring conflicts of interest. The International Committee of Medical Journal Editors (ICMJE) Uniform Requirements for Manuscripts Submitted to Biomedical Journals require that all participants in the peer review and publication process must disclose all relationships that could be viewed as potential conflicts of interest, and recommend that journals publish authors’ statements of competing interests when these might affect the way the work is judged by readers. ICMJE now provides a single disclosure form that has been adopted by all of its 12 member journals, including the BMJ (www.icmje.org/coi_disclosure.pdf). It is important to also ask reviewers to declare conflicts of interest, and in journals such as BMJ Open - which post reviewers’ reports online next to the accepted articles - these declarations are visible to all. Some conflicts may be unavoidable and acceptable, but when reviewers’ declared interests conflict significantly with the content or authorship of particular articles they should either decline to review or should not be chosen by editors for that assignment.
14. Blinded peer review. Journals have tried several ways to minimise bias in peer review. Most keep reviewers’ identities secret from authors (single blind review), so that reviewers can freely express their views without fear or favour. To reduce the risk of reviewer bias against particular authors or institutions, some journals have also removed authors’ names and addresses from manuscripts (double-blind review). Few journals use such double blind review, however: it is hard to do well and, anyway, studies have shown that around a third of the time reviewers correctly guess authors’ identities. [18,19] Furthermore, Jefferson and colleagues’ Cochrane review found "no clear-cut evidence of effect of the well-researched practice of reviewer and/or author concealment on the outcome of the quality assessment process". 
15. Potential for open (signed) peer review. Another approach is to ask reviewers to sign their reports and to reveal the identities of reviewers, editors, and authors to each other. Responses to a 2009 survey of more than 4000 science reviewers suggest, however, that reviewers prefer anonymity: 76% favoured the double blind system where only the editor knows who the reviewers and authors are. [ 20 ] This built on a 2007 survey of around 3000 academics and editors around the world (of whom about 10% worked in UK HEIs and 18% were working in clinical medicine or nursing) which found relatively little support for open review as an alternative to single- or double-blinded review.  Respondents did, however, show considerable enthusiasm for trying different approaches including post-publication review, though mainly as a supplement to formal peer review.
16. Evidence on open (signed) peer review. The surveys reported above support the common view that peer reviewers will either refuse to take part in open review or will provide only bland and uncritical comments, because they fear reprisals for criticising other researchers’ work openly. But in a randomised controlled trial, where reviewers invited in the usual way to review for the BMJ were allocated randomly to single blind review or to open (signed) review, signing did not reduce the extent or quality of reviewers’ reports and it improved their tone.  Another randomised trial, at the British Journal of Psychiatry, showed that such open review was feasible even in a specialist field - where professional rivalries might be stronger than in general medicine.  On the basis of its trial the BMJ mandated signed open review, and the journal has used this for more than decade with no significant problems. PLoS Medicine, however, tried and then discontinued this practice in late 2007 citing reviewers’ reluctance to sign their reports – perhaps because at that time it was publishing a lot of laboratory-based research, which is arguably more competitive than clinical research.
17. Evidence on open review with reviewers’ signed reports posted online alongside published articles. At the BMJ we have evaluated an extended kind of open review: making reviewers’ reports (with their consent) available to readers as part of an online pre-publication history alongside each research paper.  We aim to roll this out in late 2011, and have already done so in our new sister journal BMJ Open (bmjopen.bmj.com ). Meanwhile the medical journals in the BMC series published by BioMed Central have been using this approach for many years.
Impact of IT and greater use of online resources on the peer review process
18. Evidence on online community open review. In other experiments the Medical Journal of Australia  and Nature  made articles openly available online during, rather than after, the peer review process and invited free comments from readers. But responses from their communities were limited and both journals concluded that this was no substitute for formal, traditional peer review by experts. In the Nature trial, which ran for four months in 2006, papers that survived initial editorial assessment were hosted on an open server for moderated public comment as well as simultaneous standard peer review. During the study only 5% of authors agreed to take part and, of the 71 displayed papers only half received comments.
19. Sharing and reviewing raw data. The Wellcome Trust and other major international funders have called for public health researchers to make studies’ raw data available.  Annals of Internal Medicine , the BMJ , BMJ Open, the PloS journals and several BMC journals – among others –actively encourage authors to share data in online repositories with necessary safeguards to protect patient confidentiality . As yet, there has been no real debate on whether or how such datasets should be peer reviewe d.
Possible alternatives to peer review
20. Invited moderation rather than peer review. PLoS Currents: Influenza (http://knol.google.com/k/plos/plos-currents-influenza) is an open access online journal that uses the application Google knol (http://knol.google.com/k) to post informal articles or knols ("units of knowledge") that readers can rate and comment on. The journal describes itself as "a website for rapid and open sharing of useful new scientific data, analyses, and ideas in all aspects of influenza research [where]… all content is moderated by an expert group of influenza researchers, but in the interest of timeliness, does not undergo in-depth peer review."
21. Spontaneous post-publication comment. Many online journals encourage continuing discussion of their content. The BMJ’s Rapid Responses or eletters, posted daily, provide a voluminous, lively, and often scholarly discourse and constitute an important source of ongoing peer review (http://www.bmj.com/letters). Twitter has also entered the fray: although their <140 characters allow only the briefest comment, tweets are facilitating rapid and widespread sharing of links to articles and other online content and can, it seems, quickly expose failings in peer review. 
22. Post-publication measures of quality and impact. The web continues to bring other ways for rating and commenting on research articles and other scholarly publications. These include journal-specific measures of articles’ usage and reach eg the article-level metrics provided by PLoS journals (http://article-level-metrics.plos.org/) and the annual audit conducted by the BMJ (http://resources.bmj.com/bmj/authors/bmj-papers-audit-1); the independent rating of articles by services such as Faculty of 1000 (http://f1000.com/) and McMaster/BMJ EvidenceUpdates (http://plus.mcmaster.ca/EvidenceUpdates/); and - yet to come – the Impact Assessment for research within the new UK Research Excellence Framework (http://hefce.ac.uk/research/ref/).
Peer review is an art rather than a science. It can improve the trustworthiness and clarity of scholarly publications, and its known limitations can be minimised. While there are many ways to conduct and improve peer review, evidence shows it can be an open and transparent endeavour without compromising the quality of the process.
Trish Groves, deputy editor BMJ,
on behalf of BMJ Group
9 March 2011
Competing interests: Trish Groves is the senior research editor at the BMJ and is responsible for running the journal’s peer review processes. She is also Editor-in-Chief of BMJ Open.
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9 March 2011
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