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doi:10.1111/jgh.12500
HENRY L BOCKUS LECTURE 2013
Research misconduct: A grand global challenge for the 21st Century Michael J G Farthing University of Sussex, Brighton, UK
Key words prevention and detection of research misconduct, questionable research practices, research integrity, research misconduct. Accepted for publication 18 December 2013. Correspondence Michael J G Farthing, University of Sussex, Brighton BN1 9RH, UK. Email: [email protected] A summary of this lecture was published in World Gastroenterology News in December 2013. A related paper was presented previously as a keynote address at the 3rd World Congress on Research Integrity, Montreal 2013, and reported as a summary paper in the conference proceedings which is in press.
Abstract Research misconduct is now acknowledged to be an important global issue for both researchers and the wider community. Guidance on the responsible conduct of research is now widespread, but many are still concerned by the apparent rising tide of serious cases of research misconduct, and perhaps the more worrying widespread presence of questionable research practices. I would suggest that guidance and training, while essential, are not sufficient. Additional interventions, including enhanced monitoring of research outputs and random audit using the available technology should be considered, as should the desirability of having a register of “licensed researchers.” In addition, I would support a culture change in the research community in which researchers are encouraged to admit their mistakes; this should be accompanied by a spirit of forgiveness and programmed rehabilitation for the individual concerned. For multiple “premier league” offenders who are reluctant to face their misdemeanors, it is difficult to see how they could continue in the role of a researcher, and their “registration” should be revoked. Research is increasingly undertaken by researchers who cross national boundaries. The globalization of research demands greater collaboration between organizations that are responsible for ensuring standards of research integrity; the need for international standards and guidance has never been greater.
Introduction During the past 20–30 years, great progress has been made in defining the principles underpinning the responsible conduct of research (RCR) and in creating a culture of honesty and transparency in research environments.1 Guidance documents have been developed by many distinguished organizations around the world,2–4 and there is now an emerging consensus that the principles espoused in these documents reflect the aspirations of the research community for the future of global research. For those in the business of promoting the RCR, it might be argued that their work is done, and that it is the responsibility of others to ensure the adoption of these principles. It is quite clear, however, that the establishment of these high-level standards of best practice has almost certainly not led to a reduction in research misconduct, although it may have stemmed what appears to be a relentless rising tide.5 I suspect, however, that the converse may be true, as the number of high-profile cases appears to be on the increase with the emergence of a “premier league” of offenders
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with multiple instances of research misconduct now quantifiable quite simply by the number of retractions that have been made in their name.6,7 There is a general acceptance that the competitive pressure to engage in “shortcuts” to enhance publication outputs or win research grants has never been greater, although the introduction of cyclical national research assessment events, as has happened for example in the UK, Australia, and New Zealand, where the focus has been placed on a very limited number of high-quality outputs, may have gone some way to reduce the “quantitative” drive to enhance the personal research publication record. However, I would suggest that promoting the RCR alone may not be enough to prevent research misconduct; complementary strategies should be considered to deal with what appears to be a continuing rise in the number of reported cases of research misconduct.
What is research misconduct? Misconduct in the execution of research classically includes one or more of the triad of activities, namely fabrication, falsification, and
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plagiarism—the so-called FFP. These are serious offenses that are often referred to as “research fraud.”8 It is worth stating, however, that unlike other forms of fraud, notably financial fraud, which in most jurisdictions, if proven, warrants a custodial sentence, this is rarely ever imposed for research fraud. The reason sometimes given is that unlike financial fraud, research fraud is a victimless crime; an assertion I would suggest can be vigorously challenged. Serious research misconduct would also include the failure of duty of care to research participants, particularly patients involved in clinical trials. The situation may now be changing as several jurisdications have seriously considered changing the status of research fraud and making it a criminal offense, and at least one has awarded a custodial sentence for multiple instances of research fraud.9 There is another type of misconduct that is generally regarded as being “less serious” but quantitatively may have a similar or even greater impact on research outcomes and the research culture in general.10 These activities are known collectively as questionable research practices (QRP), and involve a broad spectrum of misdeameanors that include selectivity in data analysis and reporting, disputes about authorship, inadequate supervision, inappropriate image manipulation, and reporting errors. QRP will, in some instances, be viewed as misconduct and in less serious cases as poor research practice that could lead to misconduct. Either way, such conduct could never be regarded as good research practice.
How common? Who does it? The most frequently asked question about research misconduct is: how common is it? The truthful answer is we just do not know, certainly with any precision. Reported cases. First, we only know about the misconduct that is reported, investigated and critically, when the outcome is finally placed in the public domain. Current evidence suggests that this represents a “tip of an iceberg.” These cases generally find their way into a variety of data repositories, such as that published annually by the Office of Research Integrity in the USA,11 and are now frequently picked up by the research and more general mass media. It has been estimated that these documented cases may occur in only 0.01% of reported research studies. Research surveys. Other methodologies have been used to estimate how large the pool of undiscovered cases might be; the most widely used technique has been to survey researchers and research students.12 Up to 6% of researchers will admit to being aware of undisclosed cases of possible research misconduct, and as many as 50% of students will admit on survey that they would be willing to fake research data. In summary, it has been estimated that between 0.3% and 0.8% of research studies include examples of serious research misconduct and 5–15% contain evidence of QRPs. I totally accept that these are estimates, and like all estimates almost certainly contain inaccuracies. However, what is clear is that we can no longer dismiss research misconduct and QRP as being rare phenomena and that we can just sit back and let science correct the record as has been proposed in the past. Retraction rates. A third possible indicator of the current status of research misconduct is the retraction rate of publications
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that are already in the public domain. Until research journals were digitized, it was extremely difficult to follow the trends in research paper retraction. In addition, the effectiveness of retractions in print journals was poor, with many retracted papers being cited for many years after the retraction notice, since there was no way of linking this to the print journals on library shelves that remained in their original form. However, there are now some compelling studies that confirm that there has been a major rise in retractions, which outstrips the increase in the number of annual publications. From about 1980, there has been an increase in retraction rate from less than 5/100 000 publications to about 35/100 000 publications in 2011.13 This increase had been most evident in the last 5 years. The website Retraction Watch now acts as an important repository of retracted papers and in addition provides a commentary on individual cases.14 The majority of these retractions are because of discovered misconduct, with only about 11% attributable to genuine errors.13 There has been an analysis of the relationship between journal impact factor and retraction index; there appears to be a fairly strong linear relationship between journal impact factor and retraction index with journals such as Cell, Lancet, Nature, New England Journal of Medicine, and Science having the highest retraction rates.13 This would suggest that research misconduct occurs across the research quality spectrum and might be particularly evident at the most competitive end. While researchers are the primary perpetrators of research misconduct, there are other players that may also breach the fundamental rules of good publication and research conduct. Editors and journal owners and publishers have been criticized for manipulating impact factors by encouraging submitting authors to add more references from the journal in their bibliography.15 It has been shown that there is a fairly close correlation between self-citation rate and impact factor. Editors have also been accused of sloppy review processes when competing for what they perceive to be groundbreaking papers.16 It has been suggested that this was a factor in some of the high-profile retractions in Nature and Science. Journals have also been criticized for being positively biased toward publishing major clinical trials sponsored by the pharmaceutical industry, which they know will attract a large number of purchased reprints. At the same time, there is a continuing concern that journals are biased against publishing negative studies, a practice that will inevitably skew the published literature. There is also a concern that further bias is introduced by authors and sponsors when they are selective about the data that are chosen to include in the publication. There is particular concern, for example, in the data selected when publishing the results of a clinical trial or metaanalyses to ensure a positive outcome.17 Clinical trial investigators often do not see the full analysis of the whole dataset, and the draft reports are usually written by a professional writer, leading to a further degree of separation of the investigators from the data. These are a few examples of where misconduct can exist beyond the direct reach of the researcher.
What can we do to prevent it? There is a key question I sometimes ask myself: is there a gap in our perception between initiatives to promote RCR and the
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apparent increase in proven cases of research misconduct? Is it enough to publish and promote guidance on good/best practice, or should there be additional measures to encourage researchers to apply the guidance in their everyday conduct? While heads of universities and research institutes may have confidence in their guidance documents on the RCR and have codes of conduct for the investigation of allegations of research misconduct, they may find it difficult to totally assure themselves and their governing bodies that all of the research conducted in their institution is compliant with this guidance. Many will trust and hope it is, but the monitoring of research practices and the audit of research processes and outcomes, I would suggest, are not currently sufficient to allow this to be stated with confidence. So what additional measures would be required to allow research leaders to be able to give that assurance to others about their research outputs? Commitment by researchers to follow guidance. I believe we need to do more to discourage and detect research misconduct. While the majority of research-intensive universities and research institutes have good guidance documents, they are not always widely read or assimilated. An increasing number of institutions are requiring researchers to confirm in writing that they have read these documents prior to taking up an appointment and that they will comply with their contents. There will always be a need to embed the principles of good practice not just in individuals but also in research groups to ensure a high-quality, honest and supportive culture. Enhanced monitoring and audit. In addition, I would suggest that there will also be a need for the introduction of measures to monitor research practice to enable institutions to be able to give assurance to their funders and governing bodies that the research is not only of high-quality but also of impeccable integrity. This will inevitably mean the promotion of even higher quality supervision and monitoring by the leaders of research groups and research disciplines, and a requirement that evidence should be provided that it has actually taken place. This monitoring process might be enhanced further by random spot audits of research projects and programs. This should be an internal but formal structured process, perhaps incorporating the use of digital technology to check for plagiarism, digital image analysis to determine whether unacceptable manipulation has taken place, and forensic examination of numeric datasets to confirm their validity. The recent major case of misconduct in social science research7 indicates that greater care will also be needed to assure the integrity of questionnaire-based research, both quantitative and qualitative. Registration of clinical trials and other major research studies. There has been a powerful movement during the past decade to demand that all clinical trials should be registered such that their progress can be tracked and the outcomes of those trials placed in the public domain.18 There has also been a call for patients to boycott studies in which they are invited to participate unless they have assurance that the trial will ultimately be published.19 The UK Health Technology Assessment Programme has an excellent record in registering and publishing 424
clinical trials, and the European Medicines Agency has agreed to publish all trial data by 2014.18 Thus, although progress is being made, there are still a large number of clinical trials that remain unpublished, leaving a hole in the literature and the risk that meta-analyses will be biased toward a positive outcome. There is also a powerful campaign to insist that the pharmaceutical industry places all of the information that it has about the drug in the public domain, a movement that is now supported by politicians and the new director of the National Institute for Clinical Excellence in the UK.20 The argument might be extended to include all major research studies, whether they are publicly or privately funded. It would follow that such an approach might go a long way to prevent the publication of large numbers of fabricated studies from an author as editors might be encouraged to ask why a major study that had been submitted to their journal had not been registered at its inception. Perhaps editors should be encouraged to expect a more detailed declaration about the funding of studies that are submitted to their journal. What would the serial offenders like Boldt,6 Stapel,7 and Melendez21 have said when asked about the funding of the multitude of studies that have subsequently been found to have been fabricated and/or falsified? These interventions might be the equivalent of “speed cameras” for the research community and enable the institutional research leaders to give the sort of assurance about the integrity of its research that will be required in the future. Despite the dislike by many motorists of these “watchful eyes” on their behavior, there is increasing evidence that they reduce speed, reduce the frequency of accidents, reduce serious injuries, and save lives! In the recently published Concordat for the support of research integrity in the UK, there are two important words in the last of the five key commitments: “monitor” and “assurance.”22 The monitoring of the conduct of research in my experience is variable in frequency and intensity. An assiduous research supervisor will do an excellent job with his/her doctoral and postdoctoral students, and the work that emerges is usually exemplary. But this is not always the case, particularly as research groups grow in size and the supervisor builds an international reputation as a “flying professor.” The time spent scrutinizing raw data may diminish, although there is usually no relaxation of the pressure on researchers to produce. This is a potentially toxic vacuum that might be filled by using QRP or worse. Finally, the question remains as to who monitors the “boss”? Many of the high-profile, multiple retraction cases of research misconduct have been perpetrated by senior professors! Some research, however, is routinely audited in a formal way, notably the large multicenter clinical trials conducted by the pharmaceutical industry. It is now increasingly difficult for investigators to fabricate patients in such trials because of the requirement to match clinical records with the study report for each patient, and further assurances can be provided when the results are compared across centers to look for any outliers. Lead investigators know that this is the case, and I believe that it is a strong incentive for them to conduct the study honestly. This proposal to increase monitoring and audit will not be welcomed by some researchers or probably by their institutions. There will be claims of excessive interference and unnecessary bureaucracy. However, before we protest too much, research should be put into the wider context of activities that are
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undertaken by research-intensive universities and research institutes. Every university is required on an annual basis to have procedures in place for internal and external audit of its finances and its financial processes. This usually includes random, “deep dives” into areas in which the auditors might have concerns. In addition, in the UK, the Quality Assurance Agency (QAA) audits the teaching and learning in all UK universities on a regular basis. Again, the QAA has the freedom to inspect any area within the portfolio about which they might have concerns. Why is there no equivalent process for research which in the research-intensive universities can account for between 20–50% of total annual turnover? Schools and universities are increasingly using plagiarism detection software to discourage and detect; there is some evidence that this is already having a positive impact on the frequency of plagiarism.23 There has been an apparent upsurge in the frequency of image manipulation, particularly of gels and blots, although this began well before Photoshop became available to all! Many science journals are now requiring a full disclosure from authors about any changes they have made digitally to the original, but this sort of scrutiny should of course be conducted as a routine by the lead investigator of the research group.24 In addition, large numerical datasets can be assessed for their validity by wellestablished methodologies to determine, for example, whether they have been generated honestly in a biological system or whether they could have been constructed “on the desktop.”
Enhanced measures for detection of misconduct. While I believe that it is essential to introduce measures to actively discourage researchers from committing misconduct, there should also be enhanced approaches to the detection of misconduct when it has occurred. It is quite unacceptable for individuals to be able to publish large numbers of fraudulent papers (current record being 172 over a period of 23 years25), which is inevitably damaging to public confidence in science and research in general. Some of the preventive measures described above may go some way in addressing this challenge, but alone they will be insufficient. Those who express concerns about dubious research practices, the “whistle-blowers,” remain one of the most important components in the process to reveal misconduct. There has been a practice in the past to ignore complaints from anonymous “whistleblowers.” However, there has been an increasing trend to work sympathetically with these individuals to help them gain sufficient confidence to make a formal complaint and ultimately to reveal their identity. The emergence of websites that place concerns in the public domain14 and the use of the Internet to make contact with large numbers of individuals to express concerns about individual researchers and their institutions have progressed rapidly during the last 5 years. The use of digital media both to make allegations about research, notably image manipulation, and to broadcast this widely to the research community is unprecedented and probably unstoppable. Needless to say, this approach has had a mixed reception. In the UK, the University of Cardiff was subject to anonymous allegations of image manipulation on a grand scale. Initially, allegations were made about six published papers; these allegations were the subject of a formal internal investigation, but ultimately they were
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forced into extending the investigation by the anonymous “whistle-blower” to a total of 43. The final report, however, found deficiencies in four of these 43 papers examined.26 On the basis of this, the university has declared that it will no longer investigate complaints on an anonymous basis. This is not a view shared by all and has been criticized by the website Retraction Watch. Other organizations, such as Committee on Publication ethics and UK Research Integrity Office, have taken a more moderate stance, although clearly there has to be a balance, particularly if there is concern about the allegation being vexatious.
How should we deal with it? Finally, there is a dilemma as to what is appropriate action when research misconduct is found after formal investigation. Are we sure that the punishment always fits the crime? Often, we do not know the outcome as the findings of an investigation remain confidential within an institution; in some situations, sanctions appear lenient, while in others they may seem harsh. I am uncertain as to whether we are doing enough to encourage a culture where mistakes can be acknowledged, and then followed by support and remediation. For example, UK doctors in clinical practice who have made a clinical error are now encouraged to declare this to their patients at the earliest opportunity and to make it clear what they intend to do to make amends. Perhaps we need to think about ways in which we could include such an approach in our guidance documents for researchers? In a move for greater transparency, Canadian researchers receiving public research funding must waive their right of privacy in cases of research misconduct. This might complement a move by employers to require all new research staff to make a declaration on appointment that they have no active investigations of alleged research misconduct in progress; they might also be expected to disclose whether there had been any allegations of misconduct in the past and their outcome. There has also been a recent call for the research community to be more sympathetic to younger researchers who, because of funding pressures for example, are allured to committing research misconduct. Brian Deer has spoken up in support of the British researcher Professor Peter Francis working in the USA, who fabricated a pilot study in a grant application.27 Deer is critical of the funding agency on the basis that “funders want the answer before they are willing to pay to ask the question”! Peter Francis has been allowed to continue to work as an investigator but under supervision for a period of 2 years.
Global challenges for the future? Enhanced case reporting. For the future, it will be important to collect and collate cases of research misconduct both nationally and internationally. This should be an important component of the assessment of any interventions to enhance the RCR, and to monitor progress of measures aimed at discouraging, detecting, and dealing with the research misconduct. This has proven to be difficult, except when an agency representing research integrity is nationally recognized, such as the ORI in the USA, and has authority to request that research institutions under its aegis should make annual returns on the cases that they have
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dealt with during the period. Nonetheless, this is a goal that we should strive to achieve in the future, and one that perhaps needs high-level governmental support and international collaboration to bring to fruition. This will go some way to provide data on the scope and scale of research misconduct globally, and support the evaluation of new interventions to reduce misconduct. Improved interinstitutional communication. There is also a need for there to be better communication between research institutions and in sharing their experiences of research misconduct. There appear to be major disincentives for institutions to place their reports on research misconduct cases into the public domain. In some cases, compromise agreements have constrained both the employer and the employee to make available a full declaration of what went wrong to the wider research community.28 Only when an external regulator is involved, such as the General Medical Council in the UK, will the outcome of the case be made public as a routine. Since the majority of university researchers are not subject to the rules of conduct of a professional body, their name will only routinely enter the public domain if a paper is formally retracted, and even then the reasons for the retraction are not always evident. The danger of this practice is that it can allow serial offenders to move from university to university largely unimpeded. Professor Anthony Segal at University College London (UCL) made this point recently when one of his postdoctoral researchers had been subject to allegations of research misconduct at two other leading universities before coming to UCL;29 his work with Professor Segal was eventually found to be wanting, and a high-profile paper was formally retracted from Nature. Ways must be found to allow institutions to exchange information of this nature without fear of litigation. A similar situation has occurred in the case of Professor Melendez, where investigation of allegations of research misconduct have been conducted at three universities: two in the UK, University of Liverpool and the University of Glasgow, and at the National University of Singapore. So far, these investigations have resulted in 12 retractions from leading journals, but it is reported that the universities felt unable to communicate freely about the investigations even though there must have been some overlap as Melendez had worked in all three institutions.22 Professor Segal has suggested that there should be a register for laboratory scientists and that maintenance of registration would be an indication of a researcher’s integrity.29 The concept of the “research passport” has already been entertained and might go some way to affirm the importance for a researcher to have a clean record with, say, a relevant professional body or learned society. For medical and dental researchers in the UK, for example, a finding of serious research misconduct could put their registration in jeopardy and could limit the right to work in the UK as a practitioner. Might it be reasonable to put similar stipulations on other researchers who currently escape this sanction by not being subject to the regulations of a professional regulator? More research. Finally, I would suggest that we need more research to understand better the motivations of those that commit misconduct and why they feel able to go against the high-level principles that are now accepted to be intrinsic to the integrity of 426
research across the disciplines. How important is the notion that research misconduct is worth the risk because the chances of getting caught appear to be slight? In a fascinating article in The New York Times Magazine (April 28, 2013) by Yudhijit Battacharjee, the story behind the 55 retractions by the Dutch social psychologist, Professor Diederik Stapel, is revealed in a face-to-face interview.7 Battacharjee writes: his lifelong obsession with elegance and order, Stapel says, led him to concoct sexy results that journals found attractive: “It was a quest for aesthetics, for beauty—instead of the truth.” I am not sure whether this alone is a compelling explanation, but there must be ways of detecting aberrant behaviors before they become a 10-year or a 23-year habit6,7,9! Research is increasingly undertaken by scholars who cross national boundaries either through direct collaborations or as research migrants. The globalization of research demands greater collaboration between organizations that are responsible for ensuring standards of research integrity; the need for international standards and guidance, such as the Singapore Statement,30 has never been greater.
References 1 Steneck NH. ORI introduction to the responsible conduct of research. The Office of Research Integrity. Cited 2004. Available from URL: http://ori.hhs.gov 2 Report Codes of Conduct. Cited 2009. Available from URL: http://www.UKRIO.org.uk/publications 3 Report Codes of Conduct. Cited 2011. Available from URL: http://www.ori.gov/general-resources-0 4 Report Codes of Conduct. Cited 2011. Available from URL: http://www.esf.org/publications 5 Macilwain C. Scientific misconduct: more cops, more robbers? Cell 2012; 149: 1417–9. 6 Wise J. Boldt: the great pretender. BMJ 2013; 346: 16–8. 7 Bhattacharjee Y. The New York Times 2013; 28 Apr; 44–52. 8 Report Codes of Conduct. Cited 2008. Available from URL: http://www.ukrio.org/Procedure-for-the-Investigation-of-misconduct -in-research 9 Interlandi J. An unwelcome discovery. Cited 2008. Available from URL: http://www.nytimes.com/2006/10/22/magazine/22sciencefraud 10 John LK, Loewenstein G, Prelec D. Measuring the prevalence of questionable research practices with incentives for truth telling. Psychol. Sci. 2012; 23: 524–32. 11 Report Codes of Conduct. Cited 2013. Available from URL: http://www.ori.gov 12 Fanelli D. How many scientists fabricate and falsify research? A systematic review and meta-analysis of survey data. PLoS ONE 2009; 4: e5738. 13 Grienensen ML, Zhang M. A comprehensive survey of retracted articles from the scholarly literature. PLoS ONE 2012; 7: e44118. 14 Oranksy A, Marons A. Retraction Watch. Cited 2010. Available from URL: http://www.retractionwatch.wordpress.com 15 Fassoulaki A, Papilas K, Paraskeva A, Patris K. Impact factor bias and proposed adjustments for its determination. Acta Anaesthesiol. Scand. 2002; 46: 902–5. 16 Adam D, Knight J. Publish, and be damned. Nature 2002; 419: 772–6. 17 O’Dowd A. NICE is urged to make drug companies supply all trial data. BMJ 2012; 345: e8294. 18 Chalmers I, Glasziou P, Godlee F. All trials must be registered and the results published. BMJ 2013; 346: 8.
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19 Kmietowicz Z. Patients are urged to boycott trials that do not guarantee publication. BMJ 2013; 346: f106. 20 Hawkes N. Firms should release data for all licensed drug trials, say MPs. BMJ 2013; 346: 1. 21 Jump P. Tight-lipped over ethics inquiry. Times Higher Education 2012; 30 Aug: 9. 22 Report Codes of Conduct. Cited 11 Jul 2012. Available from URL: http://www.universitiesuk.ac.uk/concordat 23 Jump P. Turnitin is turning up fewer cases of plagiarism. Times Higher Education 2013; 4 Apr. 24 Gilbert N. Science Journals Crack Down on Image Manipulation. Cited 9 Oct 2009. Available from URL: http://www.nature.com/ news/2009/091009/full/news.2009.991
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25 Benderly B. Cited 9 Oct 2010. Available from URL: http://blogs.sciencemag.org/sciencecareers/2012/10/ 26 Dyer C. Cardiff dean is exonerated after claims that his team manipulated images in research papers. BMJ 2013; 346: f2356. 27 Akst J. Cited 3 Jul 2012. Available from URL: http://www.the -scientist.com/2012/07/03/anesthesiologist-fabricates-172-papers/ 28 Deer B. Doctor Who Admitted Research Fraud in the US Deserves Our Sympathy. Cited 19 Apr 2012. Available from URL: http://www.guardian.co.uk/science/blog/2012/apr19 29 Jump P. Faking it. Times Higher Education 2012; 23 Aug: 30–5. 30 Singapore statement on research integrity. 2010. Cited 22 Sept 2010. Available from URL: http://www.singaporestatement.org/
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doi:10.1111/jgh.12500
HENRY L BOCKUS LECTURE 2013
Research misconduct: A grand global challenge for the 21st Century Michael J G Farthing University of Sussex, Brighton, UK
Key words prevention and detection of research misconduct, questionable research practices, research integrity, research misconduct. Accepted for publication 18 December 2013. Correspondence Michael J G Farthing, University of Sussex, Brighton BN1 9RH, UK. Email: [email protected] A summary of this lecture was published in World Gastroenterology News in December 2013. A related paper was presented previously as a keynote address at the 3rd World Congress on Research Integrity, Montreal 2013, and reported as a summary paper in the conference proceedings which is in press.
Abstract Research misconduct is now acknowledged to be an important global issue for both researchers and the wider community. Guidance on the responsible conduct of research is now widespread, but many are still concerned by the apparent rising tide of serious cases of research misconduct, and perhaps the more worrying widespread presence of questionable research practices. I would suggest that guidance and training, while essential, are not sufficient. Additional interventions, including enhanced monitoring of research outputs and random audit using the available technology should be considered, as should the desirability of having a register of “licensed researchers.” In addition, I would support a culture change in the research community in which researchers are encouraged to admit their mistakes; this should be accompanied by a spirit of forgiveness and programmed rehabilitation for the individual concerned. For multiple “premier league” offenders who are reluctant to face their misdemeanors, it is difficult to see how they could continue in the role of a researcher, and their “registration” should be revoked. Research is increasingly undertaken by researchers who cross national boundaries. The globalization of research demands greater collaboration between organizations that are responsible for ensuring standards of research integrity; the need for international standards and guidance has never been greater.
Introduction During the past 20–30 years, great progress has been made in defining the principles underpinning the responsible conduct of research (RCR) and in creating a culture of honesty and transparency in research environments.1 Guidance documents have been developed by many distinguished organizations around the world,2–4 and there is now an emerging consensus that the principles espoused in these documents reflect the aspirations of the research community for the future of global research. For those in the business of promoting the RCR, it might be argued that their work is done, and that it is the responsibility of others to ensure the adoption of these principles. It is quite clear, however, that the establishment of these high-level standards of best practice has almost certainly not led to a reduction in research misconduct, although it may have stemmed what appears to be a relentless rising tide.5 I suspect, however, that the converse may be true, as the number of high-profile cases appears to be on the increase with the emergence of a “premier league” of offenders
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with multiple instances of research misconduct now quantifiable quite simply by the number of retractions that have been made in their name.6,7 There is a general acceptance that the competitive pressure to engage in “shortcuts” to enhance publication outputs or win research grants has never been greater, although the introduction of cyclical national research assessment events, as has happened for example in the UK, Australia, and New Zealand, where the focus has been placed on a very limited number of high-quality outputs, may have gone some way to reduce the “quantitative” drive to enhance the personal research publication record. However, I would suggest that promoting the RCR alone may not be enough to prevent research misconduct; complementary strategies should be considered to deal with what appears to be a continuing rise in the number of reported cases of research misconduct.
What is research misconduct? Misconduct in the execution of research classically includes one or more of the triad of activities, namely fabrication, falsification, and
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plagiarism—the so-called FFP. These are serious offenses that are often referred to as “research fraud.”8 It is worth stating, however, that unlike other forms of fraud, notably financial fraud, which in most jurisdictions, if proven, warrants a custodial sentence, this is rarely ever imposed for research fraud. The reason sometimes given is that unlike financial fraud, research fraud is a victimless crime; an assertion I would suggest can be vigorously challenged. Serious research misconduct would also include the failure of duty of care to research participants, particularly patients involved in clinical trials. The situation may now be changing as several jurisdications have seriously considered changing the status of research fraud and making it a criminal offense, and at least one has awarded a custodial sentence for multiple instances of research fraud.9 There is another type of misconduct that is generally regarded as being “less serious” but quantitatively may have a similar or even greater impact on research outcomes and the research culture in general.10 These activities are known collectively as questionable research practices (QRP), and involve a broad spectrum of misdeameanors that include selectivity in data analysis and reporting, disputes about authorship, inadequate supervision, inappropriate image manipulation, and reporting errors. QRP will, in some instances, be viewed as misconduct and in less serious cases as poor research practice that could lead to misconduct. Either way, such conduct could never be regarded as good research practice.
How common? Who does it? The most frequently asked question about research misconduct is: how common is it? The truthful answer is we just do not know, certainly with any precision. Reported cases. First, we only know about the misconduct that is reported, investigated and critically, when the outcome is finally placed in the public domain. Current evidence suggests that this represents a “tip of an iceberg.” These cases generally find their way into a variety of data repositories, such as that published annually by the Office of Research Integrity in the USA,11 and are now frequently picked up by the research and more general mass media. It has been estimated that these documented cases may occur in only 0.01% of reported research studies. Research surveys. Other methodologies have been used to estimate how large the pool of undiscovered cases might be; the most widely used technique has been to survey researchers and research students.12 Up to 6% of researchers will admit to being aware of undisclosed cases of possible research misconduct, and as many as 50% of students will admit on survey that they would be willing to fake research data. In summary, it has been estimated that between 0.3% and 0.8% of research studies include examples of serious research misconduct and 5–15% contain evidence of QRPs. I totally accept that these are estimates, and like all estimates almost certainly contain inaccuracies. However, what is clear is that we can no longer dismiss research misconduct and QRP as being rare phenomena and that we can just sit back and let science correct the record as has been proposed in the past. Retraction rates. A third possible indicator of the current status of research misconduct is the retraction rate of publications
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that are already in the public domain. Until research journals were digitized, it was extremely difficult to follow the trends in research paper retraction. In addition, the effectiveness of retractions in print journals was poor, with many retracted papers being cited for many years after the retraction notice, since there was no way of linking this to the print journals on library shelves that remained in their original form. However, there are now some compelling studies that confirm that there has been a major rise in retractions, which outstrips the increase in the number of annual publications. From about 1980, there has been an increase in retraction rate from less than 5/100 000 publications to about 35/100 000 publications in 2011.13 This increase had been most evident in the last 5 years. The website Retraction Watch now acts as an important repository of retracted papers and in addition provides a commentary on individual cases.14 The majority of these retractions are because of discovered misconduct, with only about 11% attributable to genuine errors.13 There has been an analysis of the relationship between journal impact factor and retraction index; there appears to be a fairly strong linear relationship between journal impact factor and retraction index with journals such as Cell, Lancet, Nature, New England Journal of Medicine, and Science having the highest retraction rates.13 This would suggest that research misconduct occurs across the research quality spectrum and might be particularly evident at the most competitive end. While researchers are the primary perpetrators of research misconduct, there are other players that may also breach the fundamental rules of good publication and research conduct. Editors and journal owners and publishers have been criticized for manipulating impact factors by encouraging submitting authors to add more references from the journal in their bibliography.15 It has been shown that there is a fairly close correlation between self-citation rate and impact factor. Editors have also been accused of sloppy review processes when competing for what they perceive to be groundbreaking papers.16 It has been suggested that this was a factor in some of the high-profile retractions in Nature and Science. Journals have also been criticized for being positively biased toward publishing major clinical trials sponsored by the pharmaceutical industry, which they know will attract a large number of purchased reprints. At the same time, there is a continuing concern that journals are biased against publishing negative studies, a practice that will inevitably skew the published literature. There is also a concern that further bias is introduced by authors and sponsors when they are selective about the data that are chosen to include in the publication. There is particular concern, for example, in the data selected when publishing the results of a clinical trial or metaanalyses to ensure a positive outcome.17 Clinical trial investigators often do not see the full analysis of the whole dataset, and the draft reports are usually written by a professional writer, leading to a further degree of separation of the investigators from the data. These are a few examples of where misconduct can exist beyond the direct reach of the researcher.
What can we do to prevent it? There is a key question I sometimes ask myself: is there a gap in our perception between initiatives to promote RCR and the
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apparent increase in proven cases of research misconduct? Is it enough to publish and promote guidance on good/best practice, or should there be additional measures to encourage researchers to apply the guidance in their everyday conduct? While heads of universities and research institutes may have confidence in their guidance documents on the RCR and have codes of conduct for the investigation of allegations of research misconduct, they may find it difficult to totally assure themselves and their governing bodies that all of the research conducted in their institution is compliant with this guidance. Many will trust and hope it is, but the monitoring of research practices and the audit of research processes and outcomes, I would suggest, are not currently sufficient to allow this to be stated with confidence. So what additional measures would be required to allow research leaders to be able to give that assurance to others about their research outputs? Commitment by researchers to follow guidance. I believe we need to do more to discourage and detect research misconduct. While the majority of research-intensive universities and research institutes have good guidance documents, they are not always widely read or assimilated. An increasing number of institutions are requiring researchers to confirm in writing that they have read these documents prior to taking up an appointment and that they will comply with their contents. There will always be a need to embed the principles of good practice not just in individuals but also in research groups to ensure a high-quality, honest and supportive culture. Enhanced monitoring and audit. In addition, I would suggest that there will also be a need for the introduction of measures to monitor research practice to enable institutions to be able to give assurance to their funders and governing bodies that the research is not only of high-quality but also of impeccable integrity. This will inevitably mean the promotion of even higher quality supervision and monitoring by the leaders of research groups and research disciplines, and a requirement that evidence should be provided that it has actually taken place. This monitoring process might be enhanced further by random spot audits of research projects and programs. This should be an internal but formal structured process, perhaps incorporating the use of digital technology to check for plagiarism, digital image analysis to determine whether unacceptable manipulation has taken place, and forensic examination of numeric datasets to confirm their validity. The recent major case of misconduct in social science research7 indicates that greater care will also be needed to assure the integrity of questionnaire-based research, both quantitative and qualitative. Registration of clinical trials and other major research studies. There has been a powerful movement during the past decade to demand that all clinical trials should be registered such that their progress can be tracked and the outcomes of those trials placed in the public domain.18 There has also been a call for patients to boycott studies in which they are invited to participate unless they have assurance that the trial will ultimately be published.19 The UK Health Technology Assessment Programme has an excellent record in registering and publishing 424
clinical trials, and the European Medicines Agency has agreed to publish all trial data by 2014.18 Thus, although progress is being made, there are still a large number of clinical trials that remain unpublished, leaving a hole in the literature and the risk that meta-analyses will be biased toward a positive outcome. There is also a powerful campaign to insist that the pharmaceutical industry places all of the information that it has about the drug in the public domain, a movement that is now supported by politicians and the new director of the National Institute for Clinical Excellence in the UK.20 The argument might be extended to include all major research studies, whether they are publicly or privately funded. It would follow that such an approach might go a long way to prevent the publication of large numbers of fabricated studies from an author as editors might be encouraged to ask why a major study that had been submitted to their journal had not been registered at its inception. Perhaps editors should be encouraged to expect a more detailed declaration about the funding of studies that are submitted to their journal. What would the serial offenders like Boldt,6 Stapel,7 and Melendez21 have said when asked about the funding of the multitude of studies that have subsequently been found to have been fabricated and/or falsified? These interventions might be the equivalent of “speed cameras” for the research community and enable the institutional research leaders to give the sort of assurance about the integrity of its research that will be required in the future. Despite the dislike by many motorists of these “watchful eyes” on their behavior, there is increasing evidence that they reduce speed, reduce the frequency of accidents, reduce serious injuries, and save lives! In the recently published Concordat for the support of research integrity in the UK, there are two important words in the last of the five key commitments: “monitor” and “assurance.”22 The monitoring of the conduct of research in my experience is variable in frequency and intensity. An assiduous research supervisor will do an excellent job with his/her doctoral and postdoctoral students, and the work that emerges is usually exemplary. But this is not always the case, particularly as research groups grow in size and the supervisor builds an international reputation as a “flying professor.” The time spent scrutinizing raw data may diminish, although there is usually no relaxation of the pressure on researchers to produce. This is a potentially toxic vacuum that might be filled by using QRP or worse. Finally, the question remains as to who monitors the “boss”? Many of the high-profile, multiple retraction cases of research misconduct have been perpetrated by senior professors! Some research, however, is routinely audited in a formal way, notably the large multicenter clinical trials conducted by the pharmaceutical industry. It is now increasingly difficult for investigators to fabricate patients in such trials because of the requirement to match clinical records with the study report for each patient, and further assurances can be provided when the results are compared across centers to look for any outliers. Lead investigators know that this is the case, and I believe that it is a strong incentive for them to conduct the study honestly. This proposal to increase monitoring and audit will not be welcomed by some researchers or probably by their institutions. There will be claims of excessive interference and unnecessary bureaucracy. However, before we protest too much, research should be put into the wider context of activities that are
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undertaken by research-intensive universities and research institutes. Every university is required on an annual basis to have procedures in place for internal and external audit of its finances and its financial processes. This usually includes random, “deep dives” into areas in which the auditors might have concerns. In addition, in the UK, the Quality Assurance Agency (QAA) audits the teaching and learning in all UK universities on a regular basis. Again, the QAA has the freedom to inspect any area within the portfolio about which they might have concerns. Why is there no equivalent process for research which in the research-intensive universities can account for between 20–50% of total annual turnover? Schools and universities are increasingly using plagiarism detection software to discourage and detect; there is some evidence that this is already having a positive impact on the frequency of plagiarism.23 There has been an apparent upsurge in the frequency of image manipulation, particularly of gels and blots, although this began well before Photoshop became available to all! Many science journals are now requiring a full disclosure from authors about any changes they have made digitally to the original, but this sort of scrutiny should of course be conducted as a routine by the lead investigator of the research group.24 In addition, large numerical datasets can be assessed for their validity by wellestablished methodologies to determine, for example, whether they have been generated honestly in a biological system or whether they could have been constructed “on the desktop.”
Enhanced measures for detection of misconduct. While I believe that it is essential to introduce measures to actively discourage researchers from committing misconduct, there should also be enhanced approaches to the detection of misconduct when it has occurred. It is quite unacceptable for individuals to be able to publish large numbers of fraudulent papers (current record being 172 over a period of 23 years25), which is inevitably damaging to public confidence in science and research in general. Some of the preventive measures described above may go some way in addressing this challenge, but alone they will be insufficient. Those who express concerns about dubious research practices, the “whistle-blowers,” remain one of the most important components in the process to reveal misconduct. There has been a practice in the past to ignore complaints from anonymous “whistleblowers.” However, there has been an increasing trend to work sympathetically with these individuals to help them gain sufficient confidence to make a formal complaint and ultimately to reveal their identity. The emergence of websites that place concerns in the public domain14 and the use of the Internet to make contact with large numbers of individuals to express concerns about individual researchers and their institutions have progressed rapidly during the last 5 years. The use of digital media both to make allegations about research, notably image manipulation, and to broadcast this widely to the research community is unprecedented and probably unstoppable. Needless to say, this approach has had a mixed reception. In the UK, the University of Cardiff was subject to anonymous allegations of image manipulation on a grand scale. Initially, allegations were made about six published papers; these allegations were the subject of a formal internal investigation, but ultimately they were
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forced into extending the investigation by the anonymous “whistle-blower” to a total of 43. The final report, however, found deficiencies in four of these 43 papers examined.26 On the basis of this, the university has declared that it will no longer investigate complaints on an anonymous basis. This is not a view shared by all and has been criticized by the website Retraction Watch. Other organizations, such as Committee on Publication ethics and UK Research Integrity Office, have taken a more moderate stance, although clearly there has to be a balance, particularly if there is concern about the allegation being vexatious.
How should we deal with it? Finally, there is a dilemma as to what is appropriate action when research misconduct is found after formal investigation. Are we sure that the punishment always fits the crime? Often, we do not know the outcome as the findings of an investigation remain confidential within an institution; in some situations, sanctions appear lenient, while in others they may seem harsh. I am uncertain as to whether we are doing enough to encourage a culture where mistakes can be acknowledged, and then followed by support and remediation. For example, UK doctors in clinical practice who have made a clinical error are now encouraged to declare this to their patients at the earliest opportunity and to make it clear what they intend to do to make amends. Perhaps we need to think about ways in which we could include such an approach in our guidance documents for researchers? In a move for greater transparency, Canadian researchers receiving public research funding must waive their right of privacy in cases of research misconduct. This might complement a move by employers to require all new research staff to make a declaration on appointment that they have no active investigations of alleged research misconduct in progress; they might also be expected to disclose whether there had been any allegations of misconduct in the past and their outcome. There has also been a recent call for the research community to be more sympathetic to younger researchers who, because of funding pressures for example, are allured to committing research misconduct. Brian Deer has spoken up in support of the British researcher Professor Peter Francis working in the USA, who fabricated a pilot study in a grant application.27 Deer is critical of the funding agency on the basis that “funders want the answer before they are willing to pay to ask the question”! Peter Francis has been allowed to continue to work as an investigator but under supervision for a period of 2 years.
Global challenges for the future? Enhanced case reporting. For the future, it will be important to collect and collate cases of research misconduct both nationally and internationally. This should be an important component of the assessment of any interventions to enhance the RCR, and to monitor progress of measures aimed at discouraging, detecting, and dealing with the research misconduct. This has proven to be difficult, except when an agency representing research integrity is nationally recognized, such as the ORI in the USA, and has authority to request that research institutions under its aegis should make annual returns on the cases that they have
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dealt with during the period. Nonetheless, this is a goal that we should strive to achieve in the future, and one that perhaps needs high-level governmental support and international collaboration to bring to fruition. This will go some way to provide data on the scope and scale of research misconduct globally, and support the evaluation of new interventions to reduce misconduct. Improved interinstitutional communication. There is also a need for there to be better communication between research institutions and in sharing their experiences of research misconduct. There appear to be major disincentives for institutions to place their reports on research misconduct cases into the public domain. In some cases, compromise agreements have constrained both the employer and the employee to make available a full declaration of what went wrong to the wider research community.28 Only when an external regulator is involved, such as the General Medical Council in the UK, will the outcome of the case be made public as a routine. Since the majority of university researchers are not subject to the rules of conduct of a professional body, their name will only routinely enter the public domain if a paper is formally retracted, and even then the reasons for the retraction are not always evident. The danger of this practice is that it can allow serial offenders to move from university to university largely unimpeded. Professor Anthony Segal at University College London (UCL) made this point recently when one of his postdoctoral researchers had been subject to allegations of research misconduct at two other leading universities before coming to UCL;29 his work with Professor Segal was eventually found to be wanting, and a high-profile paper was formally retracted from Nature. Ways must be found to allow institutions to exchange information of this nature without fear of litigation. A similar situation has occurred in the case of Professor Melendez, where investigation of allegations of research misconduct have been conducted at three universities: two in the UK, University of Liverpool and the University of Glasgow, and at the National University of Singapore. So far, these investigations have resulted in 12 retractions from leading journals, but it is reported that the universities felt unable to communicate freely about the investigations even though there must have been some overlap as Melendez had worked in all three institutions.22 Professor Segal has suggested that there should be a register for laboratory scientists and that maintenance of registration would be an indication of a researcher’s integrity.29 The concept of the “research passport” has already been entertained and might go some way to affirm the importance for a researcher to have a clean record with, say, a relevant professional body or learned society. For medical and dental researchers in the UK, for example, a finding of serious research misconduct could put their registration in jeopardy and could limit the right to work in the UK as a practitioner. Might it be reasonable to put similar stipulations on other researchers who currently escape this sanction by not being subject to the regulations of a professional regulator? More research. Finally, I would suggest that we need more research to understand better the motivations of those that commit misconduct and why they feel able to go against the high-level principles that are now accepted to be intrinsic to the integrity of 426
research across the disciplines. How important is the notion that research misconduct is worth the risk because the chances of getting caught appear to be slight? In a fascinating article in The New York Times Magazine (April 28, 2013) by Yudhijit Battacharjee, the story behind the 55 retractions by the Dutch social psychologist, Professor Diederik Stapel, is revealed in a face-to-face interview.7 Battacharjee writes: his lifelong obsession with elegance and order, Stapel says, led him to concoct sexy results that journals found attractive: “It was a quest for aesthetics, for beauty—instead of the truth.” I am not sure whether this alone is a compelling explanation, but there must be ways of detecting aberrant behaviors before they become a 10-year or a 23-year habit6,7,9! Research is increasingly undertaken by scholars who cross national boundaries either through direct collaborations or as research migrants. The globalization of research demands greater collaboration between organizations that are responsible for ensuring standards of research integrity; the need for international standards and guidance, such as the Singapore Statement,30 has never been greater.
References 1 Steneck NH. ORI introduction to the responsible conduct of research. The Office of Research Integrity. Cited 2004. Available from URL: http://ori.hhs.gov 2 Report Codes of Conduct. Cited 2009. Available from URL: http://www.UKRIO.org.uk/publications 3 Report Codes of Conduct. Cited 2011. Available from URL: http://www.ori.gov/general-resources-0 4 Report Codes of Conduct. Cited 2011. Available from URL: http://www.esf.org/publications 5 Macilwain C. Scientific misconduct: more cops, more robbers? Cell 2012; 149: 1417–9. 6 Wise J. Boldt: the great pretender. BMJ 2013; 346: 16–8. 7 Bhattacharjee Y. The New York Times 2013; 28 Apr; 44–52. 8 Report Codes of Conduct. Cited 2008. Available from URL: http://www.ukrio.org/Procedure-for-the-Investigation-of-misconduct -in-research 9 Interlandi J. An unwelcome discovery. Cited 2008. Available from URL: http://www.nytimes.com/2006/10/22/magazine/22sciencefraud 10 John LK, Loewenstein G, Prelec D. Measuring the prevalence of questionable research practices with incentives for truth telling. Psychol. Sci. 2012; 23: 524–32. 11 Report Codes of Conduct. Cited 2013. Available from URL: http://www.ori.gov 12 Fanelli D. How many scientists fabricate and falsify research? A systematic review and meta-analysis of survey data. PLoS ONE 2009; 4: e5738. 13 Grienensen ML, Zhang M. A comprehensive survey of retracted articles from the scholarly literature. PLoS ONE 2012; 7: e44118. 14 Oranksy A, Marons A. Retraction Watch. Cited 2010. Available from URL: http://www.retractionwatch.wordpress.com 15 Fassoulaki A, Papilas K, Paraskeva A, Patris K. Impact factor bias and proposed adjustments for its determination. Acta Anaesthesiol. Scand. 2002; 46: 902–5. 16 Adam D, Knight J. Publish, and be damned. Nature 2002; 419: 772–6. 17 O’Dowd A. NICE is urged to make drug companies supply all trial data. BMJ 2012; 345: e8294. 18 Chalmers I, Glasziou P, Godlee F. All trials must be registered and the results published. BMJ 2013; 346: 8.
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19 Kmietowicz Z. Patients are urged to boycott trials that do not guarantee publication. BMJ 2013; 346: f106. 20 Hawkes N. Firms should release data for all licensed drug trials, say MPs. BMJ 2013; 346: 1. 21 Jump P. Tight-lipped over ethics inquiry. Times Higher Education 2012; 30 Aug: 9. 22 Report Codes of Conduct. Cited 11 Jul 2012. Available from URL: http://www.universitiesuk.ac.uk/concordat 23 Jump P. Turnitin is turning up fewer cases of plagiarism. Times Higher Education 2013; 4 Apr. 24 Gilbert N. Science Journals Crack Down on Image Manipulation. Cited 9 Oct 2009. Available from URL: http://www.nature.com/ news/2009/091009/full/news.2009.991
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25 Benderly B. Cited 9 Oct 2010. Available from URL: http://blogs.sciencemag.org/sciencecareers/2012/10/ 26 Dyer C. Cardiff dean is exonerated after claims that his team manipulated images in research papers. BMJ 2013; 346: f2356. 27 Akst J. Cited 3 Jul 2012. Available from URL: http://www.the -scientist.com/2012/07/03/anesthesiologist-fabricates-172-papers/ 28 Deer B. Doctor Who Admitted Research Fraud in the US Deserves Our Sympathy. Cited 19 Apr 2012. Available from URL: http://www.guardian.co.uk/science/blog/2012/apr19 29 Jump P. Faking it. Times Higher Education 2012; 23 Aug: 30–5. 30 Singapore statement on research integrity. 2010. Cited 22 Sept 2010. Available from URL: http://www.singaporestatement.org/
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