The statement not only signalled the urgent need for information as the epidemic kills thousands, but also flagged a behind-the-scenes conflict between academic publishers – such as Amsterdam-based Elsevier, and America’s Taylor & Francis Group – and scientists critical of publishing practices that lock leading research behind subscription paywalls.

While this isn’t a new argument, the Covid-19 pandemic is throwing a spotlight on how academic publishing works – an industry that some scientists say is based on a broken model and needs to be replaced.

Academic publishers have built highly profitable businesses by taking leading-edge scientific research, putting it to specialist review, and then selling it to companies, libraries and universities around the world.

It involved institutions like the University of California paying millions of dollars a year to get access to research that the author typically gives free to the publisher.

That element of the process has angered parts of academia for years, and the global coronavirus outbreak has reinvigorated the critics. Hundreds of scientists signed an online petition this month that prompted the publishers to unlock thousands of pages of coronavirus research from behind paywalls.

Under the existing system, a scientist submits a research paper, which is then peer reviewed in a process that can take months.

In most cases the authors do this without receiving a fee because getting the work published can pay off in the form of research grants and job opportunities. And more fundamentally it adds to scientific progress.

But this measured peer-review approach was upended by the coronavirus outbreak in the central Chinese city of Wuhan late in December, as fatalities mounted and the epidemic spread to other countries.

The cost of knowledge: when Chinese academics took on Elsevier

The Trust asked for signatories to support the effort and dozens did, from academic publishers themselves, including Elsevier; to medical institutions such as the US and Chinese disease control centres; and major drug makers like Japan’s Takeda Pharmaceutical.

Since the start of this year, more than 180 papers on the new coronavirus had been released on bioRxiv. Health sciences preprint server medRxiv, which started in 2019, saw 380 virus-related papers released in the past three months.

By comparison, the Zika epidemic that appeared in Brazil in 2015 prompted just 96 papers on bioRxiv up until 2016.

“Thousands of scientific studies about the coronavirus are locked behind subscription paywalls, blocking scientists from getting access to research needed to discover antiviral treatments and a vaccine to stop the virus,” said the petition, which had almost 2,000 signatures as of March 3.

Among those to put their name to the petition were Chris Bourg, the director of libraries at MIT, and Brooks Walsh, an emergency medicine doctor in Connecticut.

As coronavirus becomes pandemic, scientists ask if lines on the map hold the key to contagion’s spread

Four major scholarly publishers – Taylor & Francis, Wiley, Oxford University Press, and Springer – responded by making almost all of their coronavirus-related papers open access, according to a later notice on the petition.

However, as of March 3, Elsevier, the world’s biggest academic publisher by sales, still had thousands of papers on coronavirus research behind a paywall, according to the petition’s organiser, a US-based researcher who did not wish to be publicly identified, citing concern about possible legal ramifications.

The organiser said search engines owned by Elsevier, known as ScienceDirect and 1Science, held combined coronavirus research that totalled 7,945 papers. As of March 3, a total of 4,110 papers had been made freely available, but that left 3,800 papers requiring payment for access.

“That’s not how science works,” the petition organiser said. “Science works by learning from previous research, and putting everything together into a new understanding.”

However, Elsevier did then remove the paywall around the rest of the papers, saying in an email that since the Covid-19 outbreak escalated, it received more requests to do so.

“[This] led us to increase our commitment to open up more articles with Elsevier’s ScienceDirect and Elsevier’s 1Science Coronavirus Research Repository and unlocked nearly 20,000 research articles,” a company spokesman said on March 10 in an emailed response to questions.

He added that Elsevier would make the “research freely accessible for as long as the World Health Organisation considers the current and potential future situations a public health risk”. The company was committed to supporting the effort to contain and eradicate Covid-19, he said.

The petition organiser confirmed that Elsevier had unlocked more than 19,000 papers on coronavirus research by March 7, complying with the signatories’ requests.

But, the Covid-19 epidemic did not cause this rift between some scientists and publishers over access to research, only resurfaced and aggravated it.

Critics in the scientific community have long questioned this model of sharing research, which has made the academic publishing industry highly lucrative.

The Britain-based Relx Group, which owns Elsevier, had an operating income margin of 26.16 per cent compared to an average of 9.82 per cent among 17 publicly traded European publishing companies, according to the latest Bloomberg Intelligence data.

Relx’s operating income margin was the biggest on the list, and science, medical and technical publishing make up about 35 per cent of its revenue, or the largest.

Critics say such profit margins from practices that limit access to research are not in the best interests of science. While the traditional academic publishing system is far from being displaced, governments and universities around the world are pushing for more open sharing of research and data.

Test, test, test: Chinese doctors advise on containing the coronavirus

The University of California is one example. In 2019, the institution, which is spread across 10 campuses, held talks with Elsevier on renewing research subscriptions.

The university said it was already paying Elsevier US$11 million a year in subscription costs, but Elsevier refused to grant the open access option, proposing instead that the university pay an additional US$30 million over three years for that service, an increase of about 80 per cent. The University of California refused.

Meantime, preprint servers outside the control of the big academic publishers are seeing a surge in activity.

One preprint paper from a team at the Los Alamos National Laboratory in the US modelled the reproduction number of Covid-19 based on publicly available data.

The reproduction number – known as the R0 or R-naught – indicates how many people are at risk from an infected person, or the contagiousness of the disease. The information has important implications for strategies on how to control the virus, according to researcher Ruian Ke from the lab.

According to the preprint paper, the transmission rate of the disease might have fallen as much as 59 per cent after China introduced lockdown measures in the country near the end of January.

“I think the amount of attention paid to the preprint service is really unprecedented,” Ke said.

Nick Hengartner, group leader of theoretical biology and biophysics at the Los Alamos lab, said preprints were part of the democratisation of the scientific process.

Instead of having a few people review the work, many scientists could take part in this process, put the findings in context and in real-time alongside other information available, Hengartner said.

Malaysia in partial lockdown to limit coronavirus spread

Ke and Hengartner both acknowledged that some of the early findings released through preprints might be flawed, because of limited data during the outbreak’s initial stages.

Some preprints that stirred controversy included one from scientists in India that compared the new coronavirus to HIV. Another paper from researchers at South China University of Technology suggested the virus was leaked from the Wuhan Institute of Virology.

Both these papers were retracted, but not before spreading on social media, fuelling misinformation on the public health emergency.

To try to reduce such incidents and highlight the most valuable work, scientists and public health experts have started up an online research platform called Outbreak Science Rapid PREreview to offer structured and timely feedback to preprints, according to Daniela Saderi, one of the founders.

“During an outbreak, we just don’t have the time for a three to six-month process for traditional peer review. With the new and open-source platform, we can work together to quickly vet them and help others find the best science,” Saderi said.

The platform launched on January 1, coinciding with the emergence of Covid-19. While preprints can spread unproven science, that’s also a problem in traditional academic publishing, according to Saderi.

“There have been plenty of examples of research that have been technically vetted by two to three reviewers through the journal-organised peer-review system and have turned out to be incorrect,” she said.

Coronavirus: don’t bank on epidemic easing in the summer, scientists say

An example is a paper linking autism to vaccines published in the medical journal The Lancet in 1998, which helped support the anti-vaccination movement. It was retracted in 2010, after it was determined to be a medical hoax.

Elsevier, which publishes The Lancet, said it saw preprints as a complement to journal publication, and a way for the research community to share information ahead of the important process of peer review.

“At the same time, we caution that preprints have not benefited from the pivotal role of peer review, which validates and improves the quality of final published journal articles,” a company spokesman said.

Hengartner at Los Alamos doesn’t entirely agree: “I think publishers who ask exorbitant prices to share scientific knowledge are dinosaurs.”

Illustration: Lau Ka-kuen