Science and Engineering Ethics

, 15:545

The Legacy of the Hwang Case: Research Misconduct in Biosciences

Authors

    • Department of Behavioural Sciences, Medical and Health Sciences CentreUniversity of Debrecen
    • Center for Ethics and Law in BiomedicineCentral European University
Original Paper

DOI: 10.1007/s11948-009-9121-x

Cite this article as:
Kakuk, P. Sci Eng Ethics (2009) 15: 545. doi:10.1007/s11948-009-9121-x

Abstract

This paper focuses on the infamous case of Hwang Woo Suk, the South-Korean national hero and once celebrated pioneer of stem cell research. After briefly discussing the evolution of his publication and research scandal in Science, I will attempt to outline the main reactions that emerged within scientific and bioethical discourses on the problem of research misconduct in contemporary biosciences. What were the ethical lapses in his research? What kind of research misconduct has been identified? How this kind of misconduct affects scientific integrity? How to avoid it? Focusing on these questions, the paper interprets the Hwang’s case as a case study that might shed light on the worst aspects of highstakes global science. This case presents a group of problems that might endanger scientific integrity and public trust. Regulatory oversight, ethical requirements and institutional safeguards are often viewed by the scientific community as merely decelerating scientific progress and causing delays in the application of treatments. The Hwang’s case represents how unimpeded progress works in contemporary science. Thus, the case might shed light on the often neglected benefits of “the social control of science”.

Keywords

Hwang Woo SukStem-cell researchResearch misconductFabricationScientific integrity

Summary of Hwang Woo Suk’s Academic Career

He was a national hero in South Korea, his research lab was probably one of the best funded in the world, and he flew first class anywhere he wanted, any time he wanted, for free, courtesy of Korean Air. He was treated like a rock star. His spectacular fall from one of the most envied positions in science plays out like a Greek tragedy.1

Mr Hwang was a South Korean professor of theriogenology and biotechnology at the Seoul National University (SNU). He was considered to be an outstanding pioneering expert in the field of stem cell research up to 2006, when the allegations of fraud and research misconduct against him and some of his colleagues were confirmed. He was best known for two articles published in the journal Science in 2004 and 2005 wherein he fraudulently reported to have succeeded in creating human embryonic stem cells by cloning. These papers have been editorially retracted after having been found to contain a large amount of fabricated data. He has admitted to various lies and frauds and was dismissed from the University on March 20th 2006.

He became famous in his home country after claiming a series of remarkable breakthroughs in cloning mammals. In 1999 he announced that he had successfully created a cloned dairy cow, Yeongrong-i, and few months later a Korean cow, Yin-i. In the following years, he continued his fantastic announcements saying he had cloned a BSE-resistant cow and planned to clone a Siberian tiger. His announcements were well received via generous media coverage highlighting the enormous economic and medical prospects deriving from his research.2

His first scientific publication that gained international attention in the wider scientific community appeared in the March 12th issue of Science [1]. Hwang allegedly used the somatic cell nuclear transfer (SCNT) method and it was received as the first reported success in human somatic cell cloning, and as such, it was regarded as a revolutionary biotechnological breakthrough. According to this publication, his research team used 242 eggs to create a single cell line. Shortly afterwards he announced an even greater achievement in the June 11th issue of Science, namely that his team had been successful in improving the success rate by a factor of 14 as compared to the results reported in his previous paper. His research team claimed to have created 11 human embryonic stem cells (with somatic cells from patients of different ages and gender) using 185 eggs [2]. This new technological advance would provide a method to create biological materials that are immunologically and genetically matched to patients. This brought significantly closer the medical viability of SCNT technology and the prospect of providing patients with custom-made treatments without immune reactions. Moreover, it might be used for other research purposes, such as creating stem-cell lines that faithfully model human diseases.

On August 3rd 2005, Hwang announced that his researcher team became the first team to successfully clone a dog, an Afghan hound, which was quite innovatively named SNUppy [3]. This paper was published in Nature in January 2005 and the results proved to be genuine, independent of Hwang’s later scandal.3

From Ethical Violations to Scientific Misconduct

Just before the scandal broke out, Hwang’s American colleague Gerald Schatten announced his decision to terminate his nearly 2-year long collaboration with the South Korean research team’s leader. As Schatten commented on the issue in an interview: “my decision is grounded solely on concerns regarding oocyte (egg) donations in Dr. Hwang’s research reported in 2004.” He also requested that the editors of Science remove his name from their joint paper. Schatten’s attempt to distance himself from Hwang’s work led to a chain reaction of events, which culminated in the close scrutiny of the scientific validity of his joint work with Hwang.4, 5

The first ethical violation discussed relating to Hwang’s research was the issue of egg donation. In a news conference Hwang’s colleague, the head of MizMedi Woman’s hospital, Roh Sung-il, has acknowledged that the procurement procedures were questionable, while he admitted that he had paid women 1400 US$ each for donating their eggs. Some members of his research lab also donated their eggs. Although Hwang failed to acknowledge his responsibility regarding this egg-procurement procedure, he offered his resignation from his post. Most commentators agreed that, although coercion could be judged slightly differently in the East, nonetheless Hwang’s attempt to cover up the truth about donation clearly illustrates the questionable nature of his practice [4]. Later on, South Korea’s National Board of Bioethics indicated that not all the donors received information about the serious risks of egg donation, furthermore, 16 donors required in-hospital treatment for adverse effects following the procedure [5].

The wider attention that followed the surfacing of this ethical lapse in Hwang’s research is catalyzed efforts to further investigate into the details of his publications. Consequently, soon after the problematic donation issue, a more profound discovery was made that shocked the South Korean public and biotech business, and became labeled as the most scandalous research misconduct case ever. However, following the early criticism in November 2005, the South Korean public and media and some leading scientific personalities still full heartedly supported Hwang and were opposed to any critical stance on the issue. The first instance of well-supported criticism about the scientific validity of the Science paper emerged from a website dedicated to biologists, called the Biological Research Information Center (BRIC).6 One of its members discovered the discrepancies in DNA analysis data in Hwang’s paper and made it public. Another piece of criticism arrived from an online community of digital camera enthusiasts—Science Gallery of DC Inside–that revealed other aspects of Hwang’s misconduct regarding illegitimate fabrications of photos in the Science publication.

On the 15th December Soul National University (SNU) decided to form an investigative panel on the misconduct allegations and within a surprisingly short period of time—after 4 weeks of work—the 50 page report was published. The university panel also published a press release summarizing the main points of the report.7 The committee’s role was to investigate nearly all the emerging problematic aspects of the Hwang case. Thus, it had to determine the technical competence of Hwang’s team, the validity of both the 2004 and 2005 Science publications, the real status of the cloned dog, and the truth regarding the egg donations. With respect to the 2005 publication the report arrived at the conclusion that instead of 11 human embryonic stem-cell lines, data was available only for two. The other cell lines were fabricated via digital manipulation of the pictures and the two valid cell lines were derived not from somatic cell nuclear transfer (SCNT), but from in vitro fertilized (IVF) eggs. The SNU report discusses the method and the process of fabrication in detail, furthermore it establishes that all the data of the 2005 publication was fabricated, including: results of tests from DNA fingerprinting, photographs of teratoma, embryoid bodies, MHC-HLA isotype matches and karyotyping. Regarding the 2004 paper, 23 samples were examined for DNA fingerprinting analysis by three independent centers, and all of these obtained identical results that brought forth the conclusion of the panel: “results described in 2004 Science article including DNA fingerprinting analyses and photographs of cells have also been fabricated”.8

The SNU committee investigated the issue of technical expertise necessary for somatic cell nuclear transfer. According to the committee Hwang’s team was highly efficient in the enucleation of human eggs, however this technique cannot be considered a unique or novel. Contrary to Hwang’s record, that stated a 10% success rate of blastocyst formation following human nuclear transfer, the real results must have been much lower, while most blastocysts were in poor condition. However, the committee couldn’t deny the team’s competence in its entirety regarding this stage of the technique, and arrived at the conclusion that “some nevertheless appear to have successfully developed into blastocysts, implying that the team was in possession of technique of creating cloned human blastocyst”.9 The statement regarding the successful establishment of stem cell lines is not supported by scientific evidence, while the required criteria for the establishment of ES cell lines (the ability to differentiate through embryoid body formation or to form teratoma for example) are not satisfied: “Professor Hwangs team regarded the initial formation of cell colony as the successful establishment of ES cell line, and no record of further confirmatory experiments could be found”.10

Snuppy’s status as a cloned dog—which had been published in a 2005 article in Nature—was confirmed by analyzing the collected samples from the egg donor, from the somatic cell provider and from the surrogate mother: “Results from analyses of 27 markers that allow distinguishing amongst extremely-inbred animals and of mitochondrial DNA sequencing indicate that Snuppy is a somatic cell clone of Tie”.11

Acquiring information from the hospitals and individuals that were involved in the egg procurement procedure, the committee established that from: “November of 2002 to November of 2005, a total of 2061 eggs from 129 females have been collected from four hospitals and provided to Professor Hwang's team”. According to this finding, the number of eggs that could have been used by Hwang is much more than could be expected based on the publications’ data on eggs used for the research. However, this time period cannot be matched to the research period of the publication. Some laboratory notes indicated that instead of the published data about the usage of 185 eggs: “at least 273 eggs have been used from September 17 of 2004 to February 7 of 2005”.12 The committee reached the conclusion that egg donations were voluntary, but eight current and former lab members supported the claim that Hwang knew about and took part in the egg donation procedure.

Following the publication of the official investigative report of the Seoul National University, Hwang apologized for the fiasco at a press conference, but he denied deceit. In this talk at Seoul’s National Press Center on the 12th January he accused the other members of the research team of deceiving him with false data, he referred to conspiracy, sabotage and the possibility of theft of materials from the laboratory. The double message of Hwang’s reaction and the confusing narratives by his team members hardly enables one to have a clear and detailed picture about what really happened. A certain part of the South Korean public still think about the issue in terms of a US conspiracy against their national hero and against a competitively developing South Korean biotech industry.

Commentators on the Scandal

“While the fallen researcher’s future looks uncertain, 12 months on, “Hwang-gate” seems to have left a lasting legacy elsewhere” [6].

The first reactions to the scandal focused on the straightforward consequences of the case: the detrimental effects on public trust toward science and stem cell research, the economic damages in the field’s funding, the loss in the market value of the biotech industry, and also the negative effects on the policy debate. The story appeared in all the big media brands surfaces, often with special coverage of the story, including interviews with scientists and experts. Scientific magazines started to discuss the emerging issues of the case and associations began to form special panels on issues related to some aspects of the case.

The early reactions of the scientific and stem-cell research community were concerned by the decelerating effect of the scandal as an event that will cause a significant delay in attaining the therapeutic goals of the stem-cell field. As Erika Check’s paper expressed in its title “Where now for stem-cell cloners?”. Scientists became perplexed and predicted that: “problems with landmark paper may set field back by years” [7]. In a similar vein, others considered the issue a setback for scientists who are working on cloning and also expressed their concerns about using the case for promoting a negative picture of the stem-cell field [8]. A column of Scientific American interpreted the consequences of the case based on interviews with the field’s experts speculating whether stem-cell research would recover from the scandal, and how this recovery might be managed. The same questions were asked regarding the possible effects on funding, on the policy debate and on public trust while also raising the question regarding how the issue of the “apparent lack of safeguards against misconduct” would be addressed by the scientific community and the public [9].

The problems that have been raised by the scientific magazines and the press in reaction to the Hwang case had a lasting presence in the science policy arena. Although ethical and policy issues connected to research misconduct had been widely discussed in the last two decades before Hwang’s appearance, the case seems to function as a catalyst in the policy arena.

The Role of the Journal Science

The role of the publication process and more specifically the validity of scientific peer-reviews have been widely questioned by commentators on the scandal. Some accorded responsibility to the publication process of the journal Science. In the summer of 2006 the journal decided to establish an independent panel to investigate how Hwang’s papers went through their publication process. As a result, the journal decided to intensify the screening process by introducing some modifications at certain levels. The panel’s report recommended that it should: “red-flag studies that claim major breakthroughs in high-visibility fields—such as climate change and human health—that could influence public policy” and in cases where the authors stand to gain financially from the publication [10]. The explicit criteria for establishing which manuscripts would require these more stringent review tracks remain to be identified by the editorial staff.

However, it remains uncertain whether more stringent checks on the received manuscripts would significantly decrease the number of fraudulent products passing through the peer-review and editorial process. Reviewers and editors look for errors in logic, flawed experiments and inconsistencies with the established literature without having an absolute overview of the whole research process and the entirety of research records. Adding a new requirement to the peer-review process to check the research records that have been accumulated through the research process would face reviewers with an insurmountable and pointless task. Furthermore, trust cannot be totally eliminated from the process of publication, editors cannot handle every paper as a special issue requiring additional in depth investigations. Nevertheless, the panel investigating the publication process of Science urged that papers should include more primary data. Moreover, some journals have already made changes in their processes: for example photographic pictures are checked by some journals—the Journal of Cell Biology (JCB) hired a staff for this purpose, and published guidelines on defining what is acceptable as legitimate forms of manipulating digital pictures. The JCB’s detailed guidelines about the legitimate usage of digital photo manipulation tools basically require that nothing should be done to any part of the illustration that does not affect all other parts equally. Since JCB started to scan the received paper’s digital illustrations in 2002, a quarter of accepted manuscripts have not fulfilled the guideline’s requirements but only 1% of these turned out to be fraudulent [11]. Had Science used this software surely it wouldn’t have published the second Hwang article. However, this was not the sole reason why Science started to apply this new measure adopted by the JCB.

Debated Responsibilities: Authorship

Like other customs, authorship is usually not determined by explicit criteria and not discussed in polite company [12].

“…it is well to remember that having one’s name on a paper is not necessarily beneficial to one’s scientific reputation” [13]

The Hwang case gave new impetus to commentators discussing the issue of authorship in international collaborations. The scientific community had to confront this problem, while Hwang, as a defense stressed the responsibility of his colleagues in the fraud as it became public that there was an instance of “gift authorship” in one of the Science publications. Moreover, Schatten’s unsuccessful attempt in November to withdraw his authorship (and responsibility) in the Science publication and escape from the radioactive vicinity of Hwang’s team also highlighted some of the problematic aspects of authorship in contemporary biosciences. In order to step up accountability regarding published results the investigative panel of Science also stressed that studies with multiple authors should spell out the role of each contributor, as has been a requirement of other journals for some years.

The need to react to issues of authorship arose in the 1990s. Both the number of authors and the prevalence of abuses started to heavily increase in biomedical publications. An extreme example could be the 976 authors of the GUSTO paper in 1993 [14]. Horton and Smith, the editor of Lancet and the (ex)editor BMJ decided to organize a conference in June 1996 on the issue in Nottingham, England [15]. This conference led several journals to modify their authorship guidelines and a few years later, in response, the International Committee of Medical Journal Editors (ICMJE) also decided to make changes in its statement on authorship in May 2000 at the Copenhagen Meeting [16].13 The Council of Science Editors established earlier a Task Force on Authorship in May 1998, and also issued a white paper after the Hwang case while revisiting both its own recommendations as well as those of the ICMJE guidelines on issues of scientific publications.14, 15 Although a growing number of leading journals follow the new guidelines on authorship, they still seem to represent a minority on an international level.

The “traditional” approach to the conceptualization of authorship–insofar as it can be read from most journals’ guidelines - applies as in the following definition: “… an author is someone who has made a significant scientific contribution to a paper and will share responsibility for the accountability of results. All others should be listed in the acknowledgments”.16 According to this conceptualization there is a significant difference between an author and a helper, or those who contributed significantly and those who provided some additional help. What is considered to be a significant contribution? The answer, the simple act of judging the extent of a contribution, remains obscure, which is a silent justification for arbitrary decisions about who is provided with the status of co-authorship in a given research. The appropriateness of the “old” system of authorship is questionable while neither the proper decision on authorship, nor the proper extent of responsibility of a given person is explicitly stated. As had been suggested a decade earlier by Rennie et al. we could achieve an increase in the accountability of contributions in scientific publications by fundamentally changing the current system of authorship [17]. Their conceptual suggestions would drop the outmoded notion of author in favor of the more realistic contributor, and would also require all authors to specify their contribution to both the research and the manuscript. These specifications would bring credit and responsibility for the product in a transparent way, and require of authors what Kassirer described earlier in Science as “public responsibility for content” [18]. Fortunately, new guidelines like that of the ICMJE seem to move to this direction, but without the full recognition of the scientific community. According to a 1994 study, 21% of authors of basic science papers and 30% of authors of clinical studies could not fulfill the ICMJE requirements for authorship as they had no involvement in the conception or design of a project, the design of a study, the analysis and interpretation of data, or the writing or revision of a project [19]. Another contrasting reality to the ICMJE guidelines is the fact that from amongst thousand postdoctoral fellows less then half knew about any guidelines concerning research and publication, and roughly 50% believed that being the head of a laboratory is a self sufficient criterion of authorship. Moreover, according to some recent studies the practice of “ghost authorship” has a significant prevalence in industry sponsored research. Interviewing the authors of industry sponsored trials, a study found that around two thirds of the publications could be accused of representing experts who actually were not being involved in the research as authors [20].

The Role of South Korea?

Most commentators focused on two aspects of the Hwang case; first they emphasized the moral responsibility of the researcher(s) and second, they discussed the possible shortcomings in the publication process, concentrating on the responsibility of editors and the peer-review system. However important a function peer-review serves in maintaining fundamental scientific standards, it remains but a single element within the larger system of scientific governance. Considering the broader institutional and social context of Hwang’s working environment, as a third aspect might bring important insights. These aspects are much less emphasized and discussed in the attempt to understand the factors that allowed for the emergence of this specific case and scientific frauds more generally.

Taking a closer look at Hwang’s working environment and at the social context of South Korean biotech, we might find some signs indicatory of a deficient system of science governance in the country [21]. In 1990s South Korea started to build an ambitious project of creating a world class biotech industry. The government plan was launched in 1994 under the title of Biotech 2000 with the goal of making South Korea into one of the seven leading biotech nations within a few years. The government and the industry pledged to spend about 18 billion US$ over a 14-year period on biotechnological research and development. Hwang’s career developed in this ambitious context and he soon became a prominent figure within the South Korean biotech plan. The government provided Hwang’s laboratory with about 65 million US$ to spend within a short period of time on research and facilities and also established the status of the “Supreme Scientist” which was first bestowed upon Hwang with an award of 1.5 million US$. Building a new research field with such concentrated funding was to the exclusion of broader merit-based funding that would have enabled the emergence of several laboratories and the growth of a scientific community where each other’s results could be assessed and where checks and follow ups by colleagues could be carried out [22]. Moreover, large amounts of concentrated funding create an overwhelming pressure to produce published results (impact factory) and an environment of unhealthy competition where losing or just gaining second position comes at an unaffordable high price.

Hwang’s access to financial support and his privileged status with connections to politicians, decision makers and elites clearly indicate the feudal nature of the social environment of South Korean science. Grants and financial support are highly dependent on the relations one can build with the political elite. In this feudal framework, illegitimately giving authorship to Park Ky Yong—(ex)advisor to the president for Science and Technology (!)—in one of the Science papers in order to secure a good and important relationship becomes a necessary part of scientific life. Hwang managed his relationships well, which is apparent in the South Korean president’s, Roh Moo Hyun’s comment, that: “it is not possible, nor desirable to prohibit research, just because there are concerns that it may lead to a direction that is deemed unethical” or in order to express his support for Hwang’s work Roh said, that “politicians have the responsibility to manage bioethical controversies not to get in the way of this outstanding research and progress”. Another oddity that characteristic of this social environment: Yang Sam Sung, the head of South Korea’s National Bioethics Board, participated in several panel meetings while he was still Hwang’s lawyer. This obvious conflict of interests becomes more worrisome in light of the fact that this was the committee that allowed Hwang to proceed with lax ethical oversight. South Korea allowed its scientists to continue research while the ethical requirements were being discussed, and the “shaping of ES cell regulations in South Korea was delayed until 2005, when the Bioethics and Biosafety Act came into effect” [21].

The above outlined framework of feudal relationships gave rise to deficiencies in the system of science governance by obscuring financial and political accountability, transparency and regulation. We can only wonder how many other countries might have similar constellation to South Korea’s, where the modernization of research facilities was not followed by the modernization of the non-technical requirements of good research practices. These similar countries are all taking a hardly perceptible risk of endangering the reputation of the whole scientific community in the country, stigmatizing the institutions involved, and damaging certain parts of the economic sector. In the case of South Korea, after the Hwang’s case the number of accepted publications by South Korean scientist has already decreased in prestigious journals. Although statistically it might occurred as a normal anomaly, but some referred to their personal experiences of journals mistrusting them: “Its about reputation. We have no other choice but to rebuild” [23]. After Hwang’s second Science publication the market value of biotech industry rose threefold; but the bubble soon burst, which generated an economic loss with further consequences for research and development in the biotech field.

The above mentioned deficiencies in the South Korean system of science governance are prime candidates within the various explanatory attempts of the Hwang’s scandal. However, as a final explanation, it has some weaknesses. The SNU investigative panel fulfilled its task quickly and effectively. Thus, we might argue that the South Korean system of science governance was functioning well, at least in this respect. Could we expect a similarly straightforward investigative process in European countries that are supposed to have a more developed system of science governance? I am not sure [24].

Several countries witnessed quite similar scandals in recent decades, and high profile cases emerged in the USA, in the UK, in Norway, in Denmark and in Germany too. However, these cases that later became scandals seem to be rarities regarding the extent of contemporary research practices, and seem to function as promoters to formulate policy and responses. The Hwang case certainly gave a new impetus to foster these policy approaches, borne of the feeling that “something has to be done”. But what should we do?

Research Misconduct: Under Control?

In order to act we need to know. But what do we know about the minute reality of research misconduct and about the related phenomena in the world of contemporary research? In order to be able to formulate an adequate policy answer to the problem of research misconduct, we need to consider the nature and extent of our knowledge about research misconduct. What is it? Why is it problematic regarding the integrity of science? How often does it occur? Is it becoming more frequent? If so, then why?

Formulating international standards for research on humans emerged after the Second World War and resulted in the establishment of the World Medical Association and its Declaration of Helsinki. The need for addressing regulations on research misconduct emerged in the 1980s when several high profile cases of research misconduct became the subject of congressional investigations in the USA [25]. Congress directed the Department of Health and Human Services (DHHS) to develop regulations that were issued in 1989 with a special focus on research misconduct [26].17 Two years later the National Science Foundation adopted a similar but slightly modified version [27]. These initial steps in policy launched a debate on the proper definition of research misconduct and made other organizations come forward with proposals and definitions. The primary objections criticized the phrase of “other practices that seriously deviate” because it was too vague, it could be applied to unorthodox but defensible research practices and it could discourage innovative science. The initial definition’s wording fostered the fear that sanctioning based on this obscure norm could be used against unpopular scientists or as an unfair tool in the competitive research arena.

The counterproposal arrived in 1995 from the National Academy of Sciences with the creation of a special label of “questionable research practices” that should not be defined as misconduct but which merits our attention: “actions that violate traditional values of the research enterprise and that may be detrimental to the research process” [28].18 In the same year, the DHHS Commission on Research Integrity came up with a general definition without the exhaustive listing of improper behaviors. This brought about again the already formulated critique regarding vagueness and generality that endangers innovative research practices [29].19 As an uneasy settlement the Office of Science and Technology Policy published the so called final Federal Policy on Research Misconduct with the now widely familiar definition that: “fabrication, falsification, plagiarism, in proposing, performing, or reviewing research, or in reporting research results” [30]. This definition specifies each of the listed offences and requires that the prohibited actions be committed intentionally, knowingly, or recklessly. This might be criticized as too narrow a definition, because it opens a wide door for referring to non-intentionally committed errors as negligent behavior that would fall outside of the concept of research misconduct proper. Dresser interpreted this 11-year-old battle on the regulation of misconduct as the profession’s attempt to resist further regulation affecting its everyday practice and also mentioned another aspect, that: “limiting the scope of federal oversight, officials have given the scientific community to curtail the less culpable but still blameworthy conduct that contributes to poor-quality research” [25].

Other policy efforts to define research misconduct also appeared elsewhere with quite diverse results, like the Norwegian approach that opted for a broad definition as “all serious deviation from accepted ethical research practice in proposing, performing, and reporting research” [31], or the still broader definition of Britain that was formed at the consensus conference in Edinburgh 2000: “behavior by a researcher, intentional or not, that falls short of good ethical and scientific standards20. The British definition does not require the action to seriously or significantly deviate from good standards nor to depend on the uncertain fact of intention.

However long the debate has already persisted, we are still expecting it to continue because an increasing number of international collaborative research projects find themselves in the midst of a confusion of standards and regulations. The Hwang scandal served as a warning signal to the international research community to do something in order to harmonize the existing approaches. A promising international initiative was the first meeting of the two widest authorities—of the European Science Foundation and the US based Office of Research Integrity—in issues regarding research misconduct.21

Before a common framework for handling research misconduct emerges from a consensus based concept of research misconduct we seem to be left with uncertain estimations regarding the scale of the problem on a global level. As Richard Smith mentioned, one of the unanswered questions of scientific fraud and research misconduct is how commonly it occurs [32]. The answer would obviously depend on how research misconduct is defined, and also on how effective the procedures are in detecting and publicizing the cases. Regarding the latter, it can be stated that the available data is extremely biased due to underreporting of the cases. Research institutions and universities are lacking in commitment or are simply not interested in the establishment and operation of effective procedures for the detection and documentation of misconduct. In some countries the issue is still not taken seriously enough and most of them hold the view that investigations of suspicious cases are directly harmful for the reputation of the institute concerned without providing any benefit. Although this means that we lack clear data on the prevalence of misconduct, we can still rest on our limited experience and on the existing databases and surveys in the attempt to build a fragmented map of research misconduct in contemporary research practices.

High stake cases and serious misconducts, like the Korean case seem to be quite rare when compared to the extremely high number of biomedical researches and publications. There was a drastic rise in the number of scientific journals published around the world: within two decades numbers rose from 25,000 to more than 54,000, according to Ulrich’s Periodicals Directory. Both the Office of Research Integrity and the National Science Foundation acknowledged that data on the low prevalence of research misconduct is the result of underreporting and the widespread practice of resolving the allegations within the walls of the institutions concerned without reporting it to federal agencies.22 Following the US and the Scandinavian countries the UK established a Research Integrity Office in 2006, but as it is a very recent establishment there is no data available that for sketching the prevalence of misconduct cases. An earlier British initiative, the Committee on Publication Ethics (COPE) that was launched in 1998 by biomedical journals, could be used primarily as guidance for editors in dealing with misconduct cases, but as the number of member journals increased exponentially it could also be used as a data source.23 According to the estimate of Mike Farthing, the chairman of the COPE, major institutions in Britain have 50 cases a year which equals to roughly one serious case a year per institution [33].

However, the relatively rare occurrence of serious misconduct cases cannot be interpreted as a reassuring fact regarding the overall level of the integrity of science. Not only due to the already mentioned uncertainty about the real extent of serious misconducts, but also because we might obtain a different picture of scientists behaving badly if we turn away from the narrow definition of serious misconduct as being plagiarism, falsification and fabrication. Martinson, Anderson and De Vries found—in an interesting study on the prevalence of misconduct in science—that one third of the researchers committed certain forms of misbehavior in recent years that could have a more serious effect on the integrity of science than the high-profile misconduct cases, such as the South Korean [34]. The point of departure was—behind the same authors’ similar research survey—to avoid the usage of the ORI’s official but all too narrow research misconduct definition that rests on a predetermined, rigid list of misbehavior (FFP: fabrication, falsification and plagiarism) [35]. Instead of focusing on these serious violations of the norms of scientific practice, the new way to conceptualize types of misbehavior enabled them to provide a description of the more mundane, everyday behavior researchers regard as most threatening to the integrity of scientific practice.

Martinson et al. investigations are important because, it turns our attention toward the often neglected experiences of scientists regarding common behavior that they see as problematic. First, the authors conducted six focus groups of 51 scientists working in different universities in the USA to create an adequate concept about misbehavior. Then, they collected data from a survey based on the focus groups’ opinions from few thousands NIH funded scientists. According to their result, scientists did not see FFP as “the real problem” instead they described more common problems that were put into four categories: (1) the meaning of data, (2) the rules of science, (3) life with colleagues, (4) pressures of production in science. The confessed modes of misbehavior (like minor misusage of funds, cutting corners in a hurry, inadequate record keeping etc.) ranged 10–50% in the sample population of researchers. Further analyses made them realize that these problems and the attendant misbehaviors are not solely associated with ordinary human frailties, but as much with the characteristics of the working environments in contemporary labs. Laboratory work in the biosciences has passed through fundamental changes in the last few decades. These developments occurred so rapidly that the norms governing the usage of new research techniques and new knowledge could not crystallize out. Thus, researchers often remain uncertain, and are left to improvise or negotiate standards of good conduct.

Summary

The Hwang’s case was labeled as the greatest ever fabrication case in science and gained widespread international publicity. An outstanding feature of the case is the involvement of a whole list of ethically problematic behaviors. The case involved the violation of international ethical norms of biomedical research on humans, while fundamental requirements of research subjects’ autonomous decision was highly problematic from several aspects: some of the egg donors had dependent relation to Hwang, researchers failed to provide appropriate information about the risk of the procedure, and donors received excessive payments. At center stage of the case appeared the issue of fabrication in two high stake publications. Guidelines and basic norms regarding authorship were not followed in the publications. Furthermore, authorship was given to individuals as a “gift”. Serious conflict of interests appeared, while Hwang’s lawyer was the head of the National Bioethics Board of South Korea that was responsible for the ethical oversight of his research. Moreover, funding and expenditure were far from being transparent, and corruption occurred, while significant amounts arrived illegitimately at various bank accounts.

Labeling the case as the greatest ever fabrication might be questioned on several grounds except that it was certainly one of the most widely publicized misconduct cases. Thus, the public perception of the case and also its social context provided by the controversial nature of the stem-cell field were primary factors that contributed to represent the Hwang case as the biggest fraud ever. However, regarding the extent of the fraud, and the quantity of fraudulent reports one might argue that others, like the Norwegian Jan Sudbo, acted deceptively in reporting scientific findings in a more extensive and much more fraudulent way.

Contrary to Sudbo’s academic career Hwang had significant scientific achievements in his previous scientific activity.24 One might pose the question: why someone who was apparently so successful chose to throw it all away with such a blatant lie? In the midst of confusing and contradicting narratives by Hwang and his colleagues, we are left to speculate. It might be that he was too trusting and accepted the works done by the members of his research team at face value. May be he knew every bit of details of what went on in his laboratory, but hoped to get away with this lie? After such successful years, he might become overconfident in what he can achieve in his lab, that he deceived himself as well. It also might be that he knew that the background results and findings of his research are problematic at least, but felt that he must go ahead of the publication because stakes became too high, both for his career, for his financial and political support, and also for his country.

The egg procurement procedures could be judged as unethical, unless one does not question international guidance on the issue. Thus, the problem was that these regulations were not followed. Similarly, regarding the fabrication issue one might argue that the main problem was not the lack of regulations, but the failure to follow existing norms, or the lack of knowledge about these norms. An editorial reported that 85% of over 900 biotechnology researchers surveyed in South Korea did not know what the Declaration of Helsinki was, and that 42% did not know about Institutional Review Boards, and also that half of them has never received ethics education.25 The feudal nature of the social environment of South Korean science opened a wide terrain, where violating almost every existing norms for good governance in research could take place. Centralized and concentrated funding, lack of transparency, serious conflicts of interests, obscured accountability are those elements that highlight deficiencies in this system of science governance. The “social control of science” is still often viewed by scientists as just having the sole function of decelerating their research. The Hwang case shows us how science works in the absence of good science governance.

The case also highlighted the need for internationally accepted guidelines that define ethical standards for the conduct of research. In this regard the Lisbon Meeting on research integrity is a promising initiative that in the long run might result in the construction of such documents based on a wide international consensus.26

Past regulatory efforts concerning research practices focused mainly on a few types of serious misconducts with a list of bad practices to be avoided and procedures for detecting, judging and reporting suspected cases. This could be labeled as the narrow warning approach in securing scientific integrity that stresses a warning against a narrowly defined dishonesty. Establishing codes of good practice and elaborating the norms for the responsible conduct of research (RCR) could better serve integrity. Instead of, or beyond the prohibition of FFP, the elaboration and propagation of RCR seems to be the adequate response as an approach towards the idea of integrity.

The restricted misconduct concept of FFP is proper as a legal tool that can be used for legal action against individuals. The wider concept, like the one used by Martinson et al., is suitable as an empirical tool for mapping contemporary scientific practices. Without extending its usage to a legal or disciplining terrain, it might serve well a long term approach trying to prevent the proliferation of grey zone activities by mapping them and informing RCR educational activities.

Recently some countries began their reform by establishing educational programs on RCR to raise scientists’ consciousness about constantly emerging ethically difficult questions surrounding the acquisition and analysis of data, publication and authorship, collaborations and conflicts of interests and other problematic aspects of scientific research [36]. However, RCR education cannot serve as a final tool in the elimination of Hwang-like cases, but it could still result in raising awareness about the ethical issues and lead to more detailed elaboration of ethical uncertainties or the lack of clear norms within scientific practices.

The way science is practiced and the process of scientific knowledge production has changed greatly in the past two decades. Not only the number of research projects, scientific publications, and journals increased exponentially, but science arrived at a post-academic phase with the increasing number of university–industry relationships and also underwent a fundamental change regarding the usage of new technologies, equipment and analytical processes. The attempt to secure the integrity of science or even to raise the overall level of its integrity by prohibiting certain behavior could hardly be brought to bear in the midst of such fundamental changes. Some norms or imperatives that govern the behavior of scientists (that were not unknown in science before) gained new prominence in these changes. Consider the imperative of being productive in the context of RCR education. Productivity has been pushed to the extreme, leading to the “publish or perish” paradigm. Scientists acquire this paradigm, and the attached values, norms and imperatives through their socialization into the web of contemporary scientific practices. It can be described as a life long educational process that parallel to the informal curriculum certainly involves a hidden curriculum, like it has been demonstrated in the case of medical education [37]. From this perspective, the main problem of RCR education will be the discrepancy of messages in the hidden and the informal curriculum of scientists. The first says that salami publication is in the grey zone, the second says that you will be in trouble if you do not publish as much as possible. However large significance we wish to put on RCR education, it is useful to remember that its effectiveness in changing scientists’ behavior is rather limited, as some studies on these early initiatives have already shown [36]. It seems that some modifications on factors that are involved in the construction of the hidden curriculum are unavoidable. A prime example would be the change to be made on the academic system of reward and merit.

Serious misconduct and research scandals are harmful to the reputation of science and to the institutions concerned, but as these cases are exposed, at least in the long run, the integrity of science is not endangered. The relatively small number of these cases and the practical infeasibility of total elimination of their occurrence could make us realize the need for a change in focus as regards research misconduct and scientific integrity. This is not to question the usefulness or imperative of detecting and investigating major dishonest behavior, but to look for new approaches in fostering scientific integrity.

Postscript

After having finished this paper I thought that the Hwang case was close to its termination. However it continued, and occupied some space in the public arena with two events that made me feel that these issues had to be addressed here additionally. Firstly, more facts arose regarding the issue of criminal charges against Hwang that mainly focused on the financial aspects of his research. Prosecutors were investigated how 24.6 billion that was part of 36.9 billion from state supports and private funds got lost in different pathways. The investigation could support allegations that some segments of the missing amount went to private bank accounts that belonged to his family, to prominent social figures, to politicians, to colleagues, and he also made extensive payments to women who provided their ova.

Hwang’s other recent “success” story came out August 2007, when the journal Stem Cell published a report about specific investigations regarding the South Korean team’s laboratory experiments and results. The report was written by experts working in the Children’s Hospital in Boston and in the Harvard Stem Cell Institute who established that Hwang successfully created a human embryo through the process called parthenogenesis. Although far from the applicative possibilities of his claimed results in Science, this technique could be regarded as a pioneering breakthrough that might move us much closer to the medical viability of stem-cell science. Consequently, we could meet with similar titles in various media sources as “Stem cell fraudster madevirgin birthbreakthrough”, “Within discredited stem-cell research a true scientific first”. There are some problems with these descriptions regarding their implicit criteria in giving credit for a scientific breakthrough. Hwang did not know these results neither did he attempt to publish them. Instead, he stated the opposite; precisely that he had done tests showing that parthenogenesis was unlikely, and that he had removed the nucleus from every egg. Thus, parthenogenesis occurred accidentally, was a result of a failure, and happened without his knowledge. In addition it might be useful to refer to the SNU investigative panel’s second report of May 2007 where it was already acknowledged that parthenogenesis occurred, although inadvertently.

Footnotes
1

Dr Stephen Minger.The Fall of a ScientificRock Star”. BBC online: (Tuesday, 10 January 2006, 17:53 GMT) http://news.bbc.co.uk/1/hi/sci/tech/4599974.stm.

 
2

Following his first international debut in a scientific publication of a biotechnological breakthrough, even commemorative stamps were issued and sold, with an image of stem cells with silhouettes of a man rising from a wheelchair, walking and running. The short existence of the stamps was between the 12th of February, 2005, and 11th of January 2006.

 
3

For the more recently appeared discussion about Hwang’s success in parthenogenesis see the postscript at the end of the paper.

 
4

Prof. Gerald Schatten of America’s University of Pittsburgh is sought by South Korean prosecution which is investigating Dr. Hwang Woo-Suk’s embryonic cloning research fabrication. The Seoul Times, Wednesday, February 21, 2007 (http://theseoultimes.com/ST/?url=/ST/db/read.php?idx=2983).

 
5

For the procedure of prosecution against Hwang, see the postscript at the end of this paper.

 
7

Summary of Final Report on Professor Hwang Woo-Suk’s Research, Seoul National University Investigation Committee. http://www.useoul.edu (press release).

 
8

Ibid p. 10.

 
9

Ibid.

 
10

Ibid.

 
11

Ibid.

 
12

Ibid.

 
13

International Committee of Medical Journal Editors: Uniform requirements for Manuscripts Submitted to Biomedical Journals. Updated May 2000 (www.icmje.org).

 
14

Who’s the Author? Problems with Biomedical Authorship, and Some Possible Solutions. Report to the Council of Biology Editors (now Council of Science Editors) From the Task Force on Authorship, February 2000 (http://www.councilscienceeditors.org/publications/v23n4p111-119.pdf).

 
15

CSE’s White Paper on Promoting Integrity in Scientific Journal Publications. Approved by the CSE Board of Directors on September 13, 2006. (http://www.councilscienceeditors.org/editorial_policies/white_paper.cfm).

 
16

See http://www.icmje.org/ at p. 28.

 
17

“fabrication, falsification, plagiarism, or other practices that seriously deviate from those that are commonly accepted within the scientific community for proposing, conducting, or reporting research. It does not include honest error or honest differences in interpretations or judgements of data.”

 
18

“fabrication, falsification, or plagiarism, in proposing, performing, or reporting research”.

 
19

“significant misbehaviour that improperly appropriates the intellectual property or contributions of others, that intentionally impedes the progress of research, or that risks corrupting the scientific record or compromising the integrity of scientific practices. Such behaviors are unethical and unacceptable in proposing, conducting, or reporting research, or in reviewing the proposals or research reports of others.”

 
20

Joint Consensus Conference on Misconduct in Biomedical Research. Consensus statement, 28 and 29 October 1999 (http://www.rcpe.ac.uk/esd/consensus/misconduct_99.html).

 
21

The European Science Foundation (ESF) and the US Department of Health and Human Services Office of Research Integrity (ORI) have announced plans to hold a World Conference on Research Integrity in Lisbon, Portugal on September 16–19, 2007 (http://www.esf.org/activities/esf-conferences/details/confdetail242/conference-information.html).

 
22

In 2002, the ORI reported that 99 institutions had 83 cases of misconduct, with 71 institutions reporting a new allegation. Between 1990 and 2002 the Office of Inspector General at the NSF investigated 800 allegations of misconduct in 600 cases.

 
25

Editorial, “Study shows bioethics awareness lacking” Dong-a Ilbo, 25 November 2005, http://english.donga.com/srv/service.php3?biid=2005112564428&path_dir=20051125

 
26

Final Report to ESF and ORI, First World Conference on Research Integrity: Fostering Responsible Research. http://www.esf.org/

 

Acknowledgements

I would like to thank Prof. Judit Sándor for her professional support and advice in presenting an early draft of this paper. I would also like to thank two anonymous reviewers for their valuable and in depth comments for improving the original draft.

Copyright information

© Springer Science+Business Media B.V. 2009