Open Access

Open access has evolved into one of the most contentious debates within the scientific community in recent years. During the past 18 months, the dialogue on how best to disseminate published research has been steadily gaining momentum.

Advocates of open access argue that the public should be able to access all online scientific literature for free. They maintain that the public has a right to access the results of federally funded research supported by their tax dollars. Opponents insist that the current subscription-based system does allow the public access to the literature, albeit not for free. They argue that subscriptions are needed to support the costs associated with journal publication and online archiving.

In October 2003, the Public Library of Science (PLoS) launched its first peer-reviewed, open-access journal, PLoS Biology. The new journal uses a publishing model in which authors, not subscribers, pay publication costs. While the journal's contents are freely available for anyone to view and use, authors must pay an article-submission fee of $1,500. PLoS has since launched PLoS Medicine and plans to launch three more open-access journals later this year: PLoS Genetics, PLoS Computational Biology, and PLoS Pathogens.

The National Institutes of Health heightened the open-access debate last year when it announced its draft open-access policy in September. During the review period, NIH received nearly 6,000 comments from publishers, researchers, and librarians, all stating their cases either for or against such a policy. Just last month, NIH revealed its final version of the policy after amending the draft based on the comments received. The policy strongly encourages--but does not require--scientists to submit peer-reviewed manuscripts resulting from NIH-funded research within 12 months to PubMed Central, the agency's free digital archive of biomedical research.

C&EN's third Point-Counterpoint brings together two of the voices in the open-access debate.

Richard J. Roberts, winner of the 1993 Nobel Prize in Physiology or Medicine, is the director of bioinformatics at New England Biolabs in Beverly, Mass. He is also a senior executive editor of Nucleic Acids Research, which is published by Oxford University Press. Roberts, along with 24 other Nobel Laureates, sent a letter to the members of Congress on Aug. 26, 2004, urging them to support free access to taxpayer-funded research.

Arguing the other side of the issue is Peter Banks, publisher for the American Diabetes Association. Banks is currently on the steering committee for patientINFORM, a project aimed at providing more biomedical research along with interpretation and context to patients. The project is set to debut this spring. Banks is also president of the Society of National Association Publications, composed of 300 nonprofit publishers.

ROBERTS POINT

Before the digital age, scientists published their findings in print journals, and libraries maintained collections of current and back issues of journals with ever-increasing space requirements. Smaller institutions have been unable to maintain large libraries because of cost, and as a result, their scientists have become seriously disadvantaged. In the early 1990s, many scientists and publishers realized that journal production and reader access could benefit from digital tools and that the digital content of the journals offered considerable advantages over print. Full-text searching became a possibility.

Now that digital publishing and dissemination are the norm, most readers work online and only print those few papers they need. This suggests that online publication, distribution, and archiving should be the standard mode of disseminating research results and that publication costs should reflect this. If librarians and archivists demand print for archival purposes, then those products should be priced independently and at cost.

It seems that scientists might benefit from this new technology, and full access to the scientific literature could be possible for everyone. No longer would poorer institutions be discriminated against because, in principle, everyone with a computer and Internet access could read the full scientific literature, not just scientists and university scholars, but teachers, high school students, and the general public. Diabetics wishing to find out more about the possibilities for curing their disease through stem cell research could go to the primary literature and avoid the free junk science that pervades the Internet. For this to happen, we need to revise the way we finance and disseminate the scientific literature. We all need "open access."

Open access means that once an article has been published it would be freely available to everyone. Central repositories such as PubMed Central could download (or be given) copies of all articles for inclusion in a central database that could function as an archive of the scientific literature, just as GenBank serves as an archive of DNA sequence information. The full text could be indexed and rendered searchable so that finally we would know just what is in the literature. No longer would we miss key experiments and facts because we hadn't seen the appropriate paper. Scientists in the developing world and the smaller U.S. institutions could have literature access that would equal that of the major universities. Ideally, such access would be immediate, but in the short term, the National Institutes of Health has proposed that a 12-month delay would be appropriate to alleviate the perceived negative impact on journal income.

While opposition was expected from commercial publishers, surprisingly, many scientific societies, including the American Chemical Society, and some disease-related foundations are against open access, even with a delayed release. They fear the negative impact on their finances, arguing that profits from journal subscriptions subsidize many worthy programs that societies frequently support. I have not yet heard a sound argument as to why library subscriptions to journals should bear the financial burden of these causes. Wouldn't a scientific society better serve its members' interests by supporting open access to the literature in its field? Why haven't the societies polled their members to find out what they really want?

A key feature of open access is that the scientific literature could be made freely available to anyone with a computer. One would not be limited to the search algorithms made available at a publisher's website nor would one be limited to online access of a subset of journals. Archives might spring up in many locations, just as GenBank is maintained by groups in the U.S., Europe, and Japan. Under the current system, publishers don't usually permit download of their archives, thereby preventing researcher-devised algorithms from mining their content. With open access, researchers would be free to browse the full text across many titles without the exorbitant fees charged today when encountering journals they don't subscribe to. This barrier discourages such browsing, and I read the literature much less often as a result of it. Open access would permit and encourage such browsing.

Currently, we have the paradoxical situation that much of the research entering the scientific literature has been paid for by taxpayer dollars or through charitable contributions to foundations, societies, and universities. Yet much of that literature is inaccessible without expensive subscriptions. Worse still, the content of a scientific paper is given to the journals for free, yet many publishers demand page charges, color charges, and other fees before they will publish the work. The editorial and review process is often done for little or no remuneration, yet still when I wish to read the article adjacent to my own in a journal, I have to pay a fee to do so. The publishers--whether commercial or scientific societies--are laughing all the way to the bank. We know there is enough money in the system to finance the production of the scientific literature because it exists now. The scientific literature should belong to the scientists who created it, not the publishers. It is imperative that we move as fast as possible to find alternative financial models that permit open access to the products of research: the scientific literature.

BANKS POINT

In 2004, the open-access movement in scholarly publishing discovered its most important ally: the U.S. taxpayer.

In their Aug. 26, 2004, open letter to Congress, Richard J. Roberts and 24 other Nobel Laureates made an impassioned appeal to taxpayers, the cornerstone of their case for a proposed NIH public repository of research results. Calling NIH's proposal a "taxpayer access policy" that will open up research currently "inaccessible to taxpayers," Roberts and his colleagues argued for an open-access policy to ensure "taxpayers get their money's worth."

What will the tax-paying public truly gain from open-access publishing as currently proposed by advocates such as Harold Varmus, and the founders of the Public Library of Science? Under the PLoS model, journals would be supported by authors' fees rather than subscriptions, with many authors' fees being passed on to federal granting agencies such as NIH. In effect, PLoS's "author pays" business model really amounts to a "taxpayer pays" model.

The first claim is dubious. For-profit and nonprofit publishers now routinely allow open archiving of postprints (pre-copyedited manuscripts accepted for publication), and more than 800,000 final manuscripts are freely available in full text at HighWire press. It is highly doubtful that access to research articles is a rate-limiting step in the advancement of science. Nor is the second argument more compelling. The costs of disseminating research are distinct from the costs of conducting it, just as the taxpayer-funded development of weapons systems has costs distinct from their deployment. If the taxpayer wishes to gain access to research, it will require federal support for the costs of distribution that are now largely borne by private parties.

The third argument of the Nobel Laureates merits special examination, because it is the promise of life-saving research that supposedly lies locked behind subscription barriers that has attracted the attention of members of Congress and the media.

The claim does not bear scrutiny. For example, a search of PubMed reveals that 7,756 papers on breast cancer were published in 2004. The vast majority are in basic or preclinical fields, many from obscure journals, and have no immediate applicability to patient care. In fact, only 208 (2.7%) of the articles represent the results of randomized controlled clinical trials, the standard for making informed decisions about treatment. Perhaps 10 of these papers address critical questions that breast cancer patients routinely have, such as choosing between established adjuvant treatment with tamoxifen and newer aromatase inhibitors.

Open access is therefore an extremely cost-inefficient way to deliver critical information to patients--and a strategy that may actually be detrimental, by providing an overwhelming volume of information that makes uncovering the few truly relevant clinical findings harder. Rather than open access, taxpaying breast cancer patients and their families would be better served by a targeted strategy of making the results of randomized clinical trials immediately available in a form patients can readily use.

In fact, such a resource already exists for breast cancer patients with the excellent Breast Cancer Trial Results webpage of the National Cancer Institute. Here, patients can get the latest clinical trial results, such as those from National Surgical Adjuvant Breast & Bowel Project clinical trials, along with the background, context, and interpretation patients need to make use of the results and discuss them with an oncologist. A similar resource for patients with breast cancer and other diseases is NIH's MedlinePlus. Publishers themselves have recently announced plans to launch patientINFORM, which will make recent clinically relevant papers available to patients, along with interpretative materials. If open-access advocates are serious about helping patients, they would do well to focus on further developing such patient-oriented sites rather than open access to research that is of little use to most patients.

In fact, there is a need for immediate and widespread exploration of the Internet as a tool to deliver scientific and medical information to researchers, clinicians, and the public. Taxpayers in all three groups deserve a robust public discussion about how best to use the Internet to support critical decisions about science and health. While open access will certainly be a part of the discussion, it is only one of many potential solutions, and likely not the most efficient or effective one for patient education and empowerment.

ROBERTS RESPONSE

Mr. Banks proposes that "there is little hard evidence for the advertised public benefits of open access." But how could there be when we don't have open access? Experience shows that when people have free access to information, they use it more. Once the subscription-based Medline was replaced with the free PubMed, usage rose approximately 100-fold within a few years. Should we not be encouraging the use of the scientific literature by all--both scientists and the public, which includes scholars, teachers, high school students, and patients? Banks supports erecting a fence around the literature to prevent its use. I strongly disagree. The current situation is that much health information is available on the Web, but almost all is tied to product advertising. The real McCoy, the peer-reviewed scientific literature, is still mostly only available by subscription. My colleagues around the world, as well as those in the less wealthy colleges in the U.S., are severely limited in their access to the scientific literature. It is difficult to work at the cutting edge if you do not know where it is.

Banks argues that open access is too expensive. However, publication is only a small part of the total costs of doing research, especially if online publication becomes the norm. Given that the research funders usually demand that the results be published, why should they not pay for it directly? For publicly funded research, I would be surprised if the public would favor restrictions on who might read the results, except perhaps for the publishers who are trying to make money through restricting access.

Banks offers the Public Library of Science journals as a financial model and complains that the "author" has to pay the full costs. However, many other models are possible. At Nucleic Acids Research, we are exploring a combination of subscriptions and modest author fees to support publication costs. Subscribers would receive a big discount in author fees. Journals such as Science and Nature depend heavily on advertising revenue to supplement subscription fees. Their publishers could easily make their scientific articles freely available, since most subscribers are primarily interested in the News & Views features of these journals, which need not be made open access. We need some creativity from the publishers to find financial models that will permit open access and allow the journals to continue to flourish. It is too easy for publishers to bury their heads in the sand and cry, "It won't work."

However, the real highlight of Banks's piece is that "open access is an extremely cost-inefficient way to deliver critical information to patients." This argument is quite disingenuous. No one is suggesting that open access would supplant other methods of disseminating information to patients. Rather, it is an adjunct that would permit transparency and would enable individuals, both professionals and the lay public, to have complete access to the primary literature. This access would facilitate, not hinder, the preparation of accurate synopses that could then be explored by patients should they so desire. Banks may be surprised at how quickly nonexperts who receive a diagnosis of some debilitating disease become practiced at reading and understanding the basic scientific literature. Is he really suggesting they would prefer not to have access to it? That smacks of the kind of ivory-towered arrogance that has landed many elite university professors in trouble.

I would encourage Banks to poll the members of the American Diabetes Association and ask if they would prefer to be blocked from free access to the primary literature. I would love to sit in the audience as he tries to justify such a position to diabetics and their families. I would much prefer to trust the general public to make wise decisions about what they read and how they interpret it, rather than permit the publishing houses and their representatives, like Banks, to censor this information for them.

BANKS RESPONSE

No one could question Roberts' dedication to the advancement of science, which now finds expression in his support for taxpayer-funded open access to scientific information. Unfortunately, Roberts' arguments contribute little toward the goal publishers and open-access advocates share: wider access to information that can speed research, improve clinical care, and enhance public understanding.

Like other open-access advocates, Roberts offers sound bites rather than sound analysis, risking further polarization of the debate. In distressing ways, the open-access debate has begun to parallel the U.S's 60-year debate over universal health coverage. A majority of Americans have favored universal coverage since President Harry S. Truman proposed it in 1945; yet the two sides of the issue so misrepresent each other's positions that Americans remain unable to make the hard choices needed to expand coverage. The result: In 2003, 45 million people in the U.S. lacked health coverage, up 5.2 million since 2000.

In both health care and information, we are presented with two unappealing choices: known quality with limited access or universal access with unknown quality. Surely, there are better options.

To find better options in information requires an honest accounting of the situation. Unfortunately, Roberts relies on the glib arguments of extremists--especially propositions that taxpayers have a right to read research they have already paid for and that publishers get "laughing all the way to the bank" profits from material they receive and peer review for free. Taxpayers have, of course, paid only for the conduct of research, not for its peer review or dissemination. It would be honest to argue that the costs of preparing research for publication should be an integral part of government funding and to advocate for taxpayer-funded open access. It is misleading to pretend that the costs of disseminating research have already been covered and to deploy populist rhetoric to convince the public they should have access to information at no additional cost.

Nor is it true that publishers exploit free labor from authors and reviewers. Scholarly publishing is a costly enterprise that involves configuring and maintaining robust online systems for manuscript submission and peer review, paying salary and office support for editors at major universities, conducting copy editing, and covering the costs of online posting. One could honestly argue that we need to find more efficient systems of peer review, perhaps even to abandon traditional peer review in some cases for the postpublication peer review practiced in the physics community. It is misleading, however, to pretend that peer review costs nothing or to expect that some improbable leap in efficiency will make its costs largely evaporate.

Given Roberts' lifelong dedication to the truth, it is hard to explain his reliance on politically expedient arguments that are so demonstrably false. Most likely, it arises from his frustration that the Internet's potential has been imperfectly realized. Maximizing that potential, however, requires validating strategies for using the Internet to empower critical decision-making, not assuming a priori that taxpayer-funded open access is the panacea.

For one thing, relying on open access to empower patients ignores this country's health literacy crisis. According to a 2004 Institute of Medicine report, 90 million people in the U.S. have trouble understanding and acting on health information.¹ The primary biomedical literature will do little for this huge population, which may require low-literacy or visually based online health information.

We need more evidence about how even literate patients can be empowered by the Internet. Sue Ziebland, senior research fellow in Oxford University's department of primary health care, and colleagues found that cancer patients used the Internet to find second opinions, seek support from other patients, interpret symptoms and understand tests and treatments, identify questions for doctors, and gain competence in health care encounters.² More such research is needed on what types of online information support these patients' behaviors.

We also need more data on how online information can improve clinical practice. Improving clinical care requires educational interventions in the care delivery setting, more frequent feedback on quality of care, and multidisciplinary and disease management programs. These educational interventions could be delivered through the Internet--but it appears critical that they be interactive and not merely the passive delivery that open access entails.

With knowledge about how best to disseminate information to speed research and improve medical care, we can find cost-effective and efficient ways to use the Internet. These are unlikely to resemble either traditional publishing models or radical taxpayer-pays open-access models. Instead, we can probably expect a public-private partnership in which governmental and nongovernmental funding agencies direct users to an increasing body of independently supported free-access research reports. The best solution isn't yet clear. What is clear, however, is the need to reject posturing and polarization, and to partner to deliver information in ways that more fully realize the power of the Internet to improve human health.

1. Institute of Medicine. "Health Literacy: A Prescription To End Confusion." Washington, D.C.: National Academies Press, 2004.

2. Ziebland, Sue, et al., "How the Internet affects patients' experience of cancer: A qualitative study," Br. Med. J. 328, No. 7439 (2004): 564.