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The New Physician September 2004
With the introduction of a new, free online peer-reviewed medical journal this fall, the controversial open-access publishing movement continues to grow.


Imagine having free, online access to the most prestigious medical journals. No subscriptions. No pay-per-view fees. No trips to the library. Keep dreaming. It’s starting to happen, but old habits in journal publishing are hard to break, which is why the 5-year-old open-access publishing movement might transform how peer-reviewed medical journals are published—or it might not.


Open-access journals—whose subject matter runs the gamut from bioinformatics to dermatology, from international health and human rights to pathology, from evolutionary biology to women’s health—break the centuries-old tradition of the “reader pays” model of publishing. Instead, it employs the “author pays” model, charging authors a fee that funds the peer-review, editing and electronic publication processes, and promises faster, cheaper and more widespread information sharing.


And similar to the beginning stages of any communications medium, open access is seen by some as experimental. Can it sustain itself financially and still maintain scientific quality?


Medical societies tend to be leery of it, including the American Medical Association (AMA), publisher of the Journal of the American Medical Association (JAMA), and the Massachusetts Medical Society, which produces the New England Journal of Medicine (NEJM). Skeptical, too, are the big commercial journal publishers like John Wiley & Sons Inc. and Reed Elsevier.


Meanwhile, young, just-getting-started physicians and scientists eager to publish their research like open access’ benefits but worry that having their papers appear in such unproven publications might lessen their chances for tenure, promotion and recognition.


IT BEGAN OVERSEAS


London-based, for-profit BioMed Central is the biggest open-access publisher of peer-reviewed scientific journals. It set up shop in 1999, making BioMed the first to dip its toes in the new publishing waters. Anyone can freely read, download, print and reuse the original research papers in its 100-plus publications.


For many of its journals, BioMed charges authors $525 for every original research article accepted for publication. Advertising helps pay publishing expenses, as do institutional memberships. If an author is affiliated with one of its 425 institutional members, the fee is waived. For example, the entire University of California system is a member of BioMed, so all of its researchers can publish in its journals at no extra cost.


Though smaller and newer, the nonprofit Public Library of Science (PLoS) is perhaps the best-known open-access publisher, because of its outspoken efforts to promote subscription-free publishing. PLoS was created in 2000 by three science heavy-hitters: Dr. Harold Varmus, a Nobel laureate for his research on cancer viruses, a former director of the National Institutes of Health (NIH) and the CEO and president of the Memorial Sloan-Kettering Cancer Center in New York; Dr. Patrick Brown, a Stanford University School of Medicine professor and genomics expert; and Michael Eisen, Ph.D., a computational and evolutionary biologist at the University of California, Berkeley.


Frustrated by the subscription barriers to the latest clinical information, the three scientists circulated an open letter in 2000 requesting scientific journal publishers make their content free online no later than six months after publication. Thirty thousand scientists signed onto the call and agreed to publish only in journals that complied. Their demand was greeted by silence. Most journals refused to change, and most of the scientists who signed the letter continue to publish in traditional subscription journals.


Refusing to give up, Varmus, Brown and Eisen expanded PLoS’ mission, transforming it into an open-access publishing house. According to the organization’s Web site, the scientists hoped “to catalyze a revolution in scientific publishing.” Their first journal—PLoS Biology—was launched in the fall of 2003 and competes against such prestigious journals as Nature and Science. This fall, they launch PLoS Medicine, which will compete against such top-tier tomes as the NEJM and JAMA. Authors pay $1,500 to publish their articles in PLoS journals. Acceptance rates for both so far hover a little above 20 percent, which is more than double the 10 percent rate for the NEJM and 8 percent for JAMA.


Supporters say open access is the ethical approach to take. Most biomedical research is largely funded by the approximately $50 billion per year granted through such government agencies as the NIH. “Taxpayers have already paid for it,” Varmus says. “It’s wrong to make us pay for it again with subscriptions.”


The PLoS co-founder believes such research should have the widest readership possible—thereby speeding scientific advances. The SARS virus genome, he points out, was sequenced in a short seven days, thanks partly to open sharing of data and results, something that’s not as easy when research is locked behind subscription-only barriers.


Unlike most traditional publishers, open-access journals generally let authors keep the copyrights to their articles—another often-cited advantage. Retaining the copyright means medical school faculty can freely share their papers with colleagues, journal clubs and students. They can post them on their Web sites and make photocopies without having to get permission from a publisher. Such articles can also be incorporated into databases and used in many ways, as long as the author is given proper attribution.


PLoS sees its primary targets as the thousands of peer-reviewed medical journals published by big, commercial publishing houses like Wiley and Elsevier. These two companies publish most of the 50,000 to 60,000 peer-reviewed research articles written each year. Reed Elsevier is perhaps the biggest—publishing around 1,700 science, technology and medicine journals that generate a 30 percent net profit, according to the Wall Street Journal.


These publishers are also the favorite targets of university librarians and some researchers, who believe they monopolize the medical publishing industry and are, therefore, able to keep raising journal prices to sustain high profit margins.


As the biggest subscribers of biomedical journals, libraries could benefit the most financially should open access take off. Right now, they have to dig ever deeper into their pockets to pay for rising subscription costs. Journal prices in all scholarly fields have increased 210 percent between 1986 and 2001, according to the Association of Research Libraries (ARL). During the same time, faculty salaries have risen only 68 percent and the cost-of-living index only 62 percent.


Take the University of Minnesota (UM) Bio-Medical Library, for example. “In the past 10 years, we’ve cancelled 40 percent of our peer-reviewed journal subscriptions,” says UM reference librarian Kathy Robbins. “Our costs have stayed the same despite the cuts, because subscription costs for the journals we still get keep going up.” Subscription fees for libraries range between several hundred to several thousand dollars per year. Robbins says Minnesota’s subscription costs have risen 10 percent per year for the past 10 years.


UM’s story is repeated at every university biomedical library nationwide. The result: Between 1986 and 2001, libraries spent three times more on journals, but subscribed to 5 percent fewer titles, according to the ARL. During the same time, libraries needed to reduce their book purchases by 9 percent to offset the costs.


Meanwhile, more and more subscription journals are being published, resulting in steadily declining access to the body of biomedical research, Varmus argues. The “knowledge pipeline,” as he calls it, has production and distribution ends. “The distribution end of the pipeline powers the system, but it’s constricted by cost and access barriers,” he says.
Why, then, aren’t all researchers and publishers running to embrace it?


CAUTION: VESTED INTERESTS AT WORK


Open access threatens the status quo. Medical societies that publish journals rely on subscription revenues to not only cover production expenses—printing on paper costs much more than posting articles online—but also to help pay for scientific meetings, scholarships and staff salaries. The open-access model could hurt their organizations financially, and some might perish if they don’t publish the traditional way.


For the big houses like Wiley and Elsevier, open access endangers their profits. And if the subscription model has proven profitable, why change? Besides, they argue, most of their researchers are not demanding change. “We certainly haven’t heard an outcry from our editors to move to an open-access model,” says Eric Swanson, Wiley’s senior vice president of scientific, technology and medical publications. “Nor have we seen a decrease in submissions.”


Then there’s the fairness argument. Critics of open access say it’s not fair to make accepted authors pay the costs of reviewing and editing rejected articles, too. And what about small universities, independent researchers and those in developing countries who can’t afford the author fee? That lessens their access, critics say.


Not to worry, counters PLoS. If someone can’t afford the author fee, PLoS waives it. BioMed does, too. As for picking up the tab for processing rejected articles, PLoS says that $1,500 is a modest amount compared to the tens of thousands of dollars granted to fund the research.


Quality is another concern, traditional publishers and some researchers argue. Subscriptions pay for the peer review and technical editing necessary to produce a top-notch journal. Is a $1,500 author fee enough to cover these costs and still produce a high-quality publication? No, says JAMA’s editor-in-chief, Dr. Catherine DeAngelis. In a January 2004 JAMA editorial, she asserts that top-tier journals like JAMA and the NEJM would have an especially difficult time making ends meet should they switch to an author-pays model. When only 8 percent to 10 percent of submissions are accepted, where would the money come from to review and process the thousands of submissions that don’t get published?


“For us to jump on the open-access bandwagon would be extremely risky and irresponsible,” says Dr. Greg Curfman, executive editor of the NEJM. “We have a 200-year-old journal that plays an important role in medicine. We believe in our model. It’s been very well tested over time. A sophisticated review process is labor intensive and requires substantial resources we feel are best obtained through reader-pays subscriptions. We have real concerns about whether the open-access model would support our process.”


Still, Curfman, like other journal editors, welcomes the open-access model to the table—with some conditions. It may be appropriate for publishing the results of basic research, he says, but perhaps not for clinical medicine. “There’s no room for error [in clinical medicine]. People’s health and well-being may be at stake. You have to be scrutinizing,” he says.


DeAngelis worries that the need to generate revenue through author fees might motivate an open-access journal to publish more papers—perhaps of a lower quality—to remain profitable.


Varmus and other open-access supporters bristle at this suggestion. All peer-reviewed journals, they say, want to maintain quality, none more so than journals trying to prove themselves. “If we don’t maintain the quality,” he says, “we won’t attract established authors and readers.”


PLoS founders say theirs is the best model for peer-reviewed publishing, but they have not yet shown it can pay for itself long-term. Neither PLoS nor BioMed have broken even, which takes traditional journals about five to seven years to accomplish. Meanwhile, the British Medical Journal (BMJ), the first top-tier medical journal to adopt an open-access practice by offering its content free online, backed off from its 1995 venture, saying it will charge subscriptions for online access starting in January 2005. BMJ cites the need to maintain a source of revenue that would sustain its high-quality publishing practices.


Varmus admits it’s too early to tell if $1,500 author fees will be enough to sustain PLoS journals. For now, PLoS stays financially afloat primarily with a $9 million private foundation grant that expires in 2007. After that, Varmus says he hopes to obtain more grant money. PLoS will also rely on advertisements, just like a subscription journal. And it offers subscriptions for the print versions of the journals, generating some revenue that way. By 2007, PLoS wants to be publishing 50 to 100 specialty biomedical journals, all of them bringing in author fees. Varmus says PLoS is also counting on expanding its list of 85 institutional members.


The open-access publisher likens this revenue mix to public radio, but the NEJM’s Curfman thinks relying on private funding sources is risky. “Funding sources come and go,” Curfman says. “Some have an agenda or an ax to grind. Editors need to be free.”


CRITICAL MASS


To be financially sustainable, open-access journals must attract enough established authors to generate a critical mass of readers. Varmus says PLoS’ biggest challenge is convincing established researchers to “come on in—the water’s fine.” The problem: Researchers want the prestige, tenure and promotions that come with publishing in high-profile subscription journals.


Generating a critical mass to legitimize open access is well underway, according to Varmus. “A lot of prominent researchers are already published in open-access journals, including people who admit they never thought they would,” he says, and adds that PLoS submissions continue to increase in number and quality. Submissions to BioMed Central have risen as well, tripling since PLoS began banging the open-access drum.


As open-access journals attract more top-tier authors, prestige and awareness will come as well, supporters say. Other researchers and the media will cite the journals, further generating a growing snowball of interest. As this happens, libraries can cancel more journal subscriptions, and in order to compete, traditional journals may make more of their content free.


Dr. David Levitt believes in open access. The UM biomedical researcher has published more than 100 peer-reviewed articles during the past 40 years, mostly in traditional subscription publications. Now he prefers open-access journals, publishing six articles with BioMed in the past two years.


“Free distribution of scientific publications to everyone with access to the Internet, including the Third World, has to rank as one of the most important advances in the history of science,” he says. Levitt also likes how open access eliminates limitations on a manuscript’s length, and number and color of figures. “Removing these limits is a great help in describing results and making the article more readable.”


In response to critics who charge the journals publish lower-quality papers: “The manuscript review process is among the most thorough and careful of any that I have received,” he says.


Open-access publishers must also convince young biomedical researchers that open access can help, rather than hurt, their careers. Prominent researchers like Varmus and Levitt could publish on paper towels and still be read. Not true for young researchers trying to get tenures, promotions or build reputations in their fields. Even Varmus sometimes publishes in traditional subscription journals, “for the sake of the careers of my trainees,” he says.


With each accepted article, PLoS provides a signed endorsement explaining the importance of the published work and how it satisfies rigorous criteria for publication. “The letter can be used to support grant and job applications,” Varmus says.


Another part of building a critical mass is convincing subscription journals to switch to open access. That’s unlikely to happen with big commercial publishers, but Varmus hopes nonprofit medical society publications will take a different view. To encourage this, PLoS provides business planning and technical expertise to any journal interested in converting to open access. Declining to name names, Varmus says, “We’ve had quite a few journals declare their interest, including one especially prominent British journal.”


Another way to create a critical mass is to include money to pay author fees in research grants. “You have to consider publication as the final step in the research process,” Varmus says. For example, the Howard Hughes Medical Institute in Chevy Chase, Maryland, pays the open-access fees for all its researchers. So does the United Kingdom’s Wellcome Trust, an independent research-funding charity. Open access fees are now built into most research grants in the United Kingdom.


Institutional memberships are another way to streamline author payment. And some universities, according to Varmus, are considering creating funds to pay open-access fees for their researchers. Theoretically, institutional members and government funding agencies could require their researchers to publish in open-access journals.


In fact, Congress’ House Appropriations Committee suggested in a July report that the NIH make the articles of NIH-funded research available for free online no later than six months after publication. The language accompanies its spending recommendations for the Departments of Labor, Education, and Health and Human Services and is not part of the appropriations bill, on which the House had yet to vote when it had adjourned for the summer. Committee staffers say they doubt the suggestion will make it into the final bill.


Getting more universities to pick up the open-access ball and run with it is not going to be a slam-dunk either. Doubts lurk as to whether open access would really save them money. “Research-intensive institutions are likely to pay more under the open-access model,” says Ann Okerson, a Yale University librarian who researched the matter. To run the numbers, she examined how many journal articles Yale faculty publish in an average year, then assumed a $1,000 fee for each. Yale’s annual subscription journal budget is $4 million. A pure open-access model, at least based on author fees, not institutional memberships, would cost the university $4.4 million.


Duke University reached the same conclusion based on an author fee calculation, according to its librarian Rick Peterson. “The cost just shifts,” he says. “If we were to transition exclusively to open access for the 4,500 articles published each year by Duke authors, the costs would equal or exceed Duke’s current journal budget.”


“We don’t know if open access will save us money,” says UM’s Robbins. “At any rate, traditional journals aren’t going away in the foreseeable future even if the slow increase in open-access journals continues.” That could compound rather than relieve university budget pressures, because open-access journals will be an addition to, rather than a replacement for, traditional journals. Universities will get stuck paying for both.


Some open-access journals may one day be equals to the most prestigious subscription journals, but traditional journals are not going away. Over time, however, open access’ place in publishing will likely grow, especially if young researchers create a demand for it.
Howard Bell is a contributing editor with The New Physician and lives in Onalaska, Wisconsin. Direct comments about this article to tnp@www.amsa.org.