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When Laura Fisher noticed striking similarities between research
papers submitted to RSC Advances, she grew suspicious. None of
the papers had authors or institutions in common, but their
charts and titles looked alarmingly similar, says Fisher, the
executive editor at the journal. “I was determined to try to get
to the bottom of what was going on.”
A year later, in January 2021, Fisher retracted 68 papers from
the journal, and editors at two other Royal Society of Chemistry
(RSC) titles retracted one each over similar suspicions; 15 are
still under investigation. Fisher had found what seemed to be
the products of paper mills: companies that churn out fake
scientific manuscripts to order. All the papers came from
authors at Chinese hospitals. The journals’ publisher, the RSC
in London, announced in a statement that it had been the victim
of what it believed to be “the systemic production of falsified
research”.
What was surprising about this was not the paper-mill activity
itself: research-integrity sleuths have repeatedly warned that
some scientists buy papers from third-party firms to help their
careers. Rather, it was extraordinary that a publisher had
publicly announced something that journals generally keep quiet
about. “We believe that it is a paper mill, so we want to be
open and transparent,” Fisher says.
The RSC wasn’t alone, its statement added: “We are one of a
number of publishers to have been affected by such activity.”
Since last January, journals have retracted at least 370 papers
that have been publicly linked to paper mills, an analysis by
Nature has found, and many more retractions are expected to
follow.
Much of this literature cleaning has come about because, last
year, outside sleuths publicly flagged papers that they think
came from paper mills owing to their suspiciously similar
features. Collectively, the lists of flagged papers total more
than 1,000 studies, the analysis shows. Editors are so concerned
by the issue that last September, the Committee on Publication
Ethics (COPE), a publisher-advisory body in London, held a forum
dedicated to discussing “systematic manipulation of the
publishing process via paper mills”. Their guest speaker was
Elisabeth Bik, a research-integrity analyst in California known
for her skill in spotting duplicated images in papers, and one
of the sleuths who posts their concerns about paper mills online.
Bik thinks there are thousands more of these papers in the
literature. The RSC’s announcement is significant for its
openness, she says. “It is pretty embarrassing that so many
papers are fake. Kudos to them to admit that they have been
fooled.”
At some journals that have had a spate of apparent paper-mill
submissions, editors have now revamped their review processes,
aiming not to be fooled again. Combating industrialized cheating
requires stricter review: telling editors to ask for raw data,
for instance, and hiring people specifically to check images.
Science publishing needs a “concerted, coordinated effort to
stamp out falsified research”, the RSC said.
Paper-mill detectives
In January 2020, Bik and other image detectives who work under
pseudonyms — Smut Clyde, Morty and Tiger BB8 — posted, on a blog
run by science journalist Leonid Schneider, a list of more than
400 published papers they said probably came from a paper mill.
Bik dubbed it the ‘tadpole’ paper mill, because of the shapes
that appeared in the papers’ western blot analyses, a type of
test used to detect proteins in biological samples. A spate of
media headlines followed. Throughout the year, the sleuths (not
always working together) posted spreadsheets of other suspect
papers — picking up on similar features across multiple studies.
By March 2021, they had collectively listed more than 1,300
articles, by Nature’s tally, as possibly coming from paper mills.
Journals started to look at the papers. According to Nature’s
analysis, around 26% of the articles that the sleuths alleged
came from paper mills have so far been retracted or labelled
with expressions of concern. Many others are still under
investigation. The Journal of Cellular Biochemistry (JCB), for
instance, announced in February1 that, last year, editors
investigated and retracted 23 of 137 papers alleged to contain
image manipulation.
Journals did not identify problems with all of the papers that
had been flagged. Chris Graf, director of research integrity at
Wiley, which publishes JCB, said in January that the publisher
had completed investigations into 73 papers identified by Bik
and others, and had found no reason to act on 11 of them. Seven
others required corrections and 55 have been retracted or will
be retracted.
Publishers almost never explicitly declare on retraction notices
that a particular study is fraudulent or was created by a
company to order, because it is difficult to prove. None of the
RSC’s retraction notices, for instance, mentions a paper mill —
despite the RSC’s announcement that it thinks the articles did
come from one. But Nature has tallied 370 articles retracted
since January 2020, all from authors at Chinese hospitals, that
either publishers or independent sleuths have alleged to come
from paper mills (see ‘Fraud allegations’). Most were published
in the past three years (see ‘Chinese hospital papers on the
rise’). Publishers have added expressions of concern to another
45 such articles.
FRAUD ALLEGATIONS: barchart showing the number of published
papers potentially linked to companies that produce fraudulent
work.
Sources:
forbetterscience.com,
scienceintegritydigest.com and
Nature analysis
Nature has identified a further 197 retractions of papers from
authors at Chinese hospitals since the start of last year. These
are not ones that have made it onto lists of potential
publication-mill products, although some were flagged by sleuths
for image concerns, often on the post-publication peer-review
website PubPeer.
Industrialized cheating
The problem of organized fraud in publishing is not new, and not
confined to China, notes Catriona Fennell, who heads publishing
services at the world’s largest scientific publisher, Elsevier.
“We’ve seen evidence of industrialized cheating from several
other countries, including Iran and Russia,” she told Nature
last year. Others have also reported on Iranian and Russian
paper-mill activities.
In a statement this year to Nature, Elsevier said that its
journal editors detect and prevent the publication of thousands
of probable paper-mill submissions each year, although some do
get through.
China has long been known to have a problem with firms selling
papers to researchers, says Xiaotian Chen, a librarian at
Bradley University in Peoria, Illinois. As far back as 2010, a
team led by Shen Yang, a management-studies researcher then at
Wuhan University in China, warned of websites offering to
ghostwrite papers on fictional research, or to bypass peer-
review systems for payment. In 2013, Science reported on a
market for authorships on research papers in China. In 2017,
China’s Ministry of Science and Technology (MOST) said it would
crack down on misconduct after a scandal in which 107 papers
were retracted at the journal Tumor Biology; their peer reviews
had been fabricated and a MOST investigation concluded that some
had been produced by third-party companies.
Physicians in China are a particular target market because they
typically need to publish research articles to gain promotions,
but are so busy at hospitals that they might not have time to do
the science, says Chen. Last August, the Beijing municipal
health authority published a policy stipulating that an
attending physician wanting to be promoted to deputy chief
physician must have at least two first-author papers published
in professional journals; three first-author papers are required
to become a chief physician. These titles affect a physician’s
salary and authority, as well as the surgeries they are allowed
to perform, says Changqing Li, a former senior physician and
gastroenterology researcher at a Chinese hospital who now lives
in the United States.
“The effect is devastating,” says Li, about the impacts on
Chinese science. “The literature environment published in
Chinese is already ruined, since hardly anyone believes them or
references studies from them.”
“Now this plague has eroded into the international medical
journals,” he adds. The fact that people use paper mills also
affects China’s reputation globally, says Futao Huang, a Chinese
researcher working at Hiroshima University in Japan.
The prevalence of problem papers is leading some journal editors
to doubt the submissions they get from Chinese hospital
researchers. “The increasing volume of this ‘junk science’ is
wreaking havoc on the credibility of the research emanating out
of China and increasingly casting doubt upon legitimate science
from the region,” said a February 2021 editorial2 in the journal
Molecular Therapy.
Several other editors echo these concerns about the impact of
paper mills. “They are undermining our confidence in the other
manuscripts received from Chinese groups,” says Frank Redegeld,
editor in chief of the European Journal of Pharmacology,
published by Elsevier.
CHINESE HOSPITAL PAPERS ON THE RISE: chart showing the rise in
English language articles with authors from Chinese hospitals.
Source:
lens.org
China’s science and education ministries have taken steps to
curb problematic publication incentives. They published a notice
last February telling research institutions — including
hospitals — not to promote or recruit researchers solely on the
basis of the numbers of papers they publish, and also told them
to stop paying cash bonuses for papers. And in August, China
announced the introduction of measures to crack down on research
misconduct, including attempts to curb independent contractors
who fabricate data on others’ behalf. (MOST didn’t respond to
Nature’s request for comment on the scale of the problem or the
impact of its measures.)
Some Chinese researchers think these measures are beginning to
work. Li Tang, who researches science policy at Fudan University
in Shanghai, China, is hopeful that submissions from paper mills
in China will fall in the future — although she notes that the
issue isn’t confined to Chinese research.
Redegeld says he hasn’t yet seen a decrease in the number of
suspected paper-mill manuscripts his journal receives, which he
estimates to be around 15 a month.
Problem signs
Image-integrity sleuths and journal editors have identified a
range of features in manuscripts that could be fingerprints of a
paper mill. “We’re wondering how we protect ourselves from
publishing this stuff,” says Jana Christopher, an image-
integrity analyst at the publisher FEBS Press in Heidelberg,
Germany, who screens incoming manuscripts for a number of
journals, and helped the RSC with its investigation.
Potential signs of trouble include papers from different authors
at different institutions sharing similar features: western
blots with identical-looking backgrounds and suspiciously smooth
outlines, titles that seem to be variations on a theme, bar
charts with identical layouts that supposedly represent
different experiments, or identical plots of flow cytometry
analyses, which are used in studying cells. It seems that these
manuscripts are produced from common templates, with words and
images slightly tweaked to make the papers look a little
different.
A particular problem is biomedical articles that claim to
investigate understudied genetic regions that might be involved
in cancers. Jennifer Byrne, a molecular oncology researcher at
the University of Sydney, Australia, specializes in exposing
flawed papers of this type, by spotting that their experimental
details sometimes list incorrect nucleotide sequences or
reagents, so that the experiments described cannot have taken
place. Many of these papers are probably doctored simply by
switching around the type of cancer or the genes involved in the
study, says Byrne, although it’s hard to prove they’re from
paper mills. “This problem of incorrect nucleotide sequences in
the literature is rampant,” she says.
At last September’s COPE forum, Bik rattled off other red flags
for editors to watch out for, including papers from Chinese
hospitals and manuscripts with e-mail addresses that don’t seem
to be linked to any of the author names. “Individually, these
factors may not be problematic, but taken together they raise
concerns and could be part of a pattern,” she said. Editors at
the forum also noted that a manuscript-processing system,
ScholarOne, can flag up unusual activity when it picks up on
submissions from the same computer. A ScholarOne alert was also
instrumental in the RSC’s investigation.
In February, Naunyn-Schmiedeberg’s Archives of Pharmacology said
it had been affected by paper mills. The journal published an
editorial3 listing important features of paper-mill articles.
These included non-academic e-mail addresses (which happen to be
common with Chinese scientists), authors’ inability to supply
raw data when asked, and poor English. The journal is retracting
10 studies, and it reports that around 5% of all its submissions
are from paper mills.
Publishers and others battling paper mills suspect they are only
seeing the tip of the iceberg in the published literature. In
part, that’s because similarities between images across studies
might become obvious only when many papers are compared. Sleuths
also know that features such as similar western blots and flawed
nucleotide sequences might be the most obvious signs of paper-
mill activity, says Bik. “There may be tonnes of other paper
mills that have done a better job of hiding it,” she says.
Editors at the COPE forum said they’d seen paper mills in areas
such as computer sciences, engineering, humanities and social
sciences, for instance.
The overall size of the paper-mill problem probably runs to
thousands or tens of thousands of papers, Bik, Byrne and others
think4. Graf, at Wiley, says it’s hard to estimate. “I don’t
think it should be understated, I can’t say how big it is,” he
says. “We have very little information about the people or
companies doing this. I am exasperated by the situation, and
that is being polite.”
“It’s detrimental to science as a whole because it makes science
and scientists look unreliable,” says Christopher. Byrne has
identified a different concern: she worries that by simply
appearing in journals, fake studies that link genes to
particular cancers can give the perception of activity in an
area where there is none, and might be included in meta-
analyses. “People die from cancer — it is not a game. It is
important that the literature describes the work that takes
place,” she adds.
Zombie papers
Journal editors know that if they reject manuscripts they
suspect to be fabricated, that might not kill the paper forever.
Fraudulent manuscripts can be submitted to multiple journals at
the same time: so even if an editor rejects it during peer
review, they might see it published elsewhere.
This has happened to Christopher, who 3 years ago saw alarming
similarities in a cluster of 13 research manuscripts submitted
to 2 journals published by FEBS Press, where she worked. Their
western blots seemed to be not only fabricated, but also
similar, as if they’d been created by tweaking a template. The
journals rejected the manuscripts on her advice. Christopher
published a 2018 paper5 warning of “systematic fabrication of
scientific images” and urged journals to invest in pre-
publication image screening. She also noted that she’d seen some
papers appear in other journals.
Christopher told Nature that she tried to privately raise the
alarm about the papers. In 2018, for instance, she and FEBS
Letters’ managing editor advised the journal Cellular Physiology
and Biochemistry that a paper it had published that year was
probably fabricated; it had been simultaneously submitted to
FEBS Letters, which had rejected it. But the journal’s publisher
at the time, Karger in Basel, Switzerland, did not hear of any
problem until 2020, when the paper was flagged up again in Bik
and others’ ‘tadpole paper mill’ collection, along with other
papers in the journal. Karger is now investigating all these
papers together with the journal’s current publisher, says
Christna Chap, Karger’s head of editorial development.
This year, Christopher again looked into the 13 manuscripts that
had been submitted to her journals. She found they had all been
published in other journals; so far, only three have been
retracted and one has an expression of concern.
Many journals have changed their editorial-review processes to
try to combat organized fraud. Some Elsevier journals, for
instance, have changed their scope to avoid subject areas that
seem to be a particular focus of paper mills, the publisher
says. And several publishers say many of their journals have
updated their policies to require that authors present the raw
data behind their western blots at the time of submission.
Asking for raw data is one of the main ways that publishers tell
editors to follow up when they think there might be something
wrong with a manuscript. But editors are aware that even raw
data can be faked, especially if paper-mill firms catch on that
such requests are being made.
“Asking for raw data is not an absolute guarantee, as you can
fake the data. It is a deterrent,” says Sabina Alam, director of
publishing integrity and ethics at Taylor and Francis. One of
its journals, Artificial Cells, Nanomedicine, and Biotechnology,
is investigating almost 100 published papers alleged to be from
paper mills.
Alam also says that once they started investigations, some
authors quickly asked to withdraw their papers. Some sent raw
data in unreadable formats or without labels. In all these
cases, journal editors say they’re not sure whether it’s correct
to withdraw such articles, or to do something else — and are
hoping for guidance on this from COPE. Bik has pointed out that
some journals have already allowed authors to withdraw papers
without stating the reason for retraction.
COPE says it will update its existing guidance on how journals
should deal with systematic manipulation of the publication
process, and is also creating a task force of editors from its
membership to determine how the organization can provide better
support on the issue.
Path forwards
Publishers say that they are limited in what they can do to
share information between journals because even titles within
the same stable are editorially independent of one another.
They’re wary of sharing information between titles or publishers
about an author that could be defamatory, and data-protection
rules hinder the sharing of authors’ personal data.
Once fraudsters know they can get a paper into a particular
title, they might continue to publish there, which could be why
some journals seem to be more affected than others. One journal,
the European Review for Medical and Pharmacological Sciences,
has retracted 186 articles since January 2020, most of them
flagged by Bik and Smut Clyde. “We were shocked by these
investigations,” says one of its editors in chief, Antonio
Gasbarrini.
Many journals are starting to employ analysts to try to spot
problems in manuscripts as they come in. Graf, for instance,
says that last year Wiley employed and trained 11 people to try
to spot manipulated images across 24 journals — focusing on the
papers most likely to be published. It hopes to expand the
programme to more titles.
Publishers would like to automate some of this screening
process. Many have teamed up with research groups to develop
software that could detect duplicated images across published
papers, and, last May, an industry group formed to try to set
standards for these checks. Software is improving but isn’t yet
capable of looking through many papers on a massive scale, says
IJsbrand Jan Aalbersberg, the head of research integrity at
Elsevier, who chairs the group. To do this would also require a
giant shared database of images that publishers could check for
duplication between papers. That will come when software can
handle it, Aalbersberg predicts.
Suzanne Farley, Springer Nature’s research-integrity director,
based in London, says she thinks that there will be a fall in
the proportion of paper-mill submissions. “The paper mills are
aware that publishers are getting better at detecting their
submissions, and potential paper-mill customers are aware that
there are now more serious consequences of using the services,”
she says. (Nature’s news team is editorially independent of its
publisher.) In the meantime, Farley says, there will be more
retractions and expressions of concern. “We are committed to
cleaning house,” she says.
But Christopher worries that an arms race could develop if
fraudsters get better at avoiding obvious mistakes. One preprint
posted to bioRxiv last year6, for instance, suggested that
artificial intelligence techniques could generate fake western
blots that were indistinguishable from real ones. “I’m really
worried about the sophistication going up,” she says.
Nature 591, 516-519 (2021)
doi:
https://doi.org/10.1038/d41586-021-00733-5
https://www.nature.com/articles/d41586-021-00733-5