Misconduct accounts for the majority of retracted scientific publications

In addition to confirming a recent rise in the incidence of retractions, this study provides a number of additional insights. Perhaps most significantly, we find that most retracted articles result from misconduct, and nearly half of retractions are for fraud or suspected fraud. In addition to a larger sample size encompassing all retractions in the biomedical research literature, this study differs from some previous analyses in the use of alternative sources of information, such as reports from the Office of Research Integrity, Retraction Watch, news media, and other public records. The US Office of Research Integrity was formed in 1992 and is charged with the oversight of misconduct allegations involving federally sponsored research. As the consideration of secondary sources led to changes in the perceived cause of retraction in 158 instances (Table S1), we conclude that for many retractions, the retraction notice is insufficient to ascertain the true cause of a retraction.

We further note that not all articles suspected of fraud have been retracted. The Lancet and British Medical Journal expressed serious reservations about the validity of the Indo-Mediterranean Diet Heart Study after the primary author was unable to present original records to document ethics review and informed consent (18, 19), yet the original articles have not been retracted (20, 21). Several articles authored by Mark Spector when he was working in the laboratory of Efraim Racker remain in the literature (22, 23), despite documentation that Spector committed data fabrication (24). R. K. Chandra was found to have committed fraud in the performance of clinical trials, but only a single article was retracted (25), even though considerable evidence was obtained to suggest that other publications were also fraudulent (26). Therefore, the current number of articles retracted because of fraud represents an underestimation of the actual number of fraudulent articles in the literature.

Although some retraction announcements are specific and detailed, many are uninformative or opaque. In 119 instances, no information regarding the reason for retraction was provided by the journal. Announcements are often written by the authors of the retracted article themselves (27), who may be understandably reluctant to implicate themselves in misconduct. Furthermore, investigation of suspected misconduct is a lengthy process, and retraction notices are frequently made before the full results of investigations are available. Among 285 investigations concluded by the Office of Research Integrity from 2001 to 2010, the length of investigation averaged 20.48 mo in duration and ranged up to more than 9 y (28). Policies regarding retraction announcements vary widely among journals, and some, such as the Journal of Biological Chemistry, routinely decline to provide any explanation for retraction. These factors have contributed to the systematic underestimation of the role of misconduct and the overestimation of the role of error in retractions (3, 4), and speak to the need for uniform standards regarding retraction notices (5).

Differences in the temporal and geographic patterns of retraction according to cause (Figs. 1A and 2) militate against a simple explanation for retractions. One factor is the increased detection of misconduct. The first discernible increase in retractions followed the formation of the Office of Scientific Integrity (the predecessor of the Office of Research Integrity) and passage of the Whistleblower Protection Act in 1989. The recent increase in the incidence of retractions and the differing patterns by region (Fig. 2) argue that incentives may vary with the type of misconduct. Most articles retracted for fraud have originated in countries with longstanding research traditions (e.g., United States, Germany, Japan) and are particularly problematic for high-impact journals. In contrast, plagiarism and duplicate publication often arise from countries that lack a longstanding research tradition, and such infractions often are associated with lower-impact journals (Fig. 3 and Table 1). A highly significant correlation was found between the journal-impact factor and the number of retractions for fraud or suspected fraud and error (Fig. 3 A and B); the mean impact factor was found to be significantly higher for articles retracted for fraud, suspected fraud, or error, compared with those retracted for plagiarism or duplicate publication (Fig. 3D). An association between impact factor and retraction for fraud or error has been noted previously (4, 6, 29, 30). This finding may reflect the greater scrutiny accorded to articles in high-impact journals and the greater uncertainty associated with cutting-edge research. Alternatively, the disproportionately high payoffs to scientists for publication in prestigious venues can be an incentive to perform work with excessive haste (31) or to engage in unethical practices (4). The modest correlation between impact factor and time-to-retraction argues against an explanation based on increased scrutiny alone, but the higher proportion of fraud in highly prestigious journals is consistent with the suggestion that the benefits of publishing in such venues are powerful incentives for fraud (4, 6, 32). The 20 most highly cited retracted articles (Table 3) include no articles retracted for plagiarism or duplicate publication. Recent technological advances facilitating word processing and access to electronic publications may have made plagiarism easier to perform but have also facilitated its detection (33). The impact of plagiarism and duplicate publication on science is therefore limited; although these practices are to be discouraged, the present study suggests that the reduction of fraud and error should be a higher priority (32).

Our findings confirm that retraction can cause a persistent decline in citation rate (17), but an immediate and severe decline in citations is not inevitable (Fig. S3). The Wakefield article in the Lancet (34) is a special case, given its sequential partial and full retractions, extensive media attention, public health import, and frequent citation as a source of controversy, but it is less obvious why other retracted articles continue to be cited. A PDF version of a 2001 Nature article by Makarova et al. does not indicate that the article has been retracted, and two authors disputed whether iron-containing impurities invalidated the articles conclusions (35), which might contribute to uncertainty as to whether the work remains valid (36). A 2005 Science article by Fukuhara et al. continues to be cited even though both the HTML and PDF versions are clearly marked as retracted, and the PDF version includes a copy of the retraction notice (37). Many scientists continue to cite the article by Fukuhara et al. for its initial identification of visfatin as an adipocytokine, even though the article was retracted because of concerns about the cytokine’s reported insulin mimetic properties (38). This practice suggests that under certain circumstances, scientists continue to find utility in retracted articles, particularly those retracted because of error, and supports a policy of continued access to retracted articles as long as detailed descriptions regarding the reasons for retraction are provided.

The longer average time-to-retraction when articles are retracted because of fraud (Table 2) corroborates earlier studies based on limited datasets (4, 39), and may be attributable in part to the lengthy investigative process required to establish misconduct. The trend toward a longer average time-to-retraction for articles retracted in recent years may reflect a growing tendency for editors to reach back further in time to retract articles. Recognition of fraud can trigger a systematic review of an author’s entire research output, resulting in a cascade of retracted articles. The correlation between time-to-retraction and impact factor (Fig. 4B) suggests that the greater visibility and enhanced scrutiny of high-impact journals may contribute to more rapid retraction of fraudulent papers by these journals, although the effect appears to be quite modest.

Most articles by authors with large numbers of retractions (Table S2) were retracted because of misconduct, and these include some of the most notorious cases in the history of research ethics. The Mori case (Fig. S2) demonstrates that fraudulent articles can go undetected for many years. Such cases may be revealed only fortuitously when exposed by an attentive reviewer or whistleblower (40). Twelve of Mori’s retracted articles had been in the literature for 5 y or more, demonstrating that the impact of serial retractions on the average time-to-retraction can be substantial.

In conclusion, a comprehensive review of 2,047 articles retracted from the biomedical literature reveals that misconduct has played a more prominent role than previously appreciated. Our findings underscore the importance of vigilance by reviewers, editors, and readers, and investigations by institutions, government agencies, and journalists in identifying and documenting research misconduct. Furthermore, our findings suggest a need for increased attention to ethics in the training of scientists. However, this attention alone is unlikely to be successful in curbing poor research practices.

The rise in the rate of retractions raises concern about the health of the scientific enterprise itself (32). Although articles retracted because of fraud represent a very small percentage of the scientific literature (Fig. 1B), it is important to recognize that: (i) only a fraction of fraudulent articles are retracted; (ii) there are other more common sources of unreliability in the literature (41–44); (iii) misconduct risks damaging the credibility of science; and (iv) fraud may be a sign of underlying counterproductive incentives that influence scientists (45, 46). A better understanding of retracted publications can inform efforts to reduce misconduct and error in science.

Given that most scientific work is publicly funded and that retractions because of misconduct undermine science and its impact on society, the surge of retractions suggests a need to reevaluate the incentives driving this phenomenon. We have previously argued that increased retractions and ethical breaches may result, at least in part, from the incentive system of science, which is based on a winner-takes-all economics that confers disproportionate rewards to winners in the form of grants, jobs, and prizes at a time of research funding scarcity (32, 46, 47). We have also proposed a set of reforms to strengthen the scientific enterprise, ranging from improved training of scientists to the identification of mechanisms to provide more consistent funding for science (32, 46). Solutions to address the specific problem of retractions may include the increased use of checklists by authors and reviewers, improved training in logic, probability and statistics, an enhanced focus on ethics, the formation of a centralized database of scientific misconduct, the establishment of uniform guidelines for retractions and retraction notices, and the development of novel reward systems for science (32). Dedicated national agencies, such as the US Office for Research Integrity, can play an invaluable role in supporting and overseeing institutional investigations of alleged misconduct. We hope that the present study will prompt discussion among scientists and the society they serve to find measures to improve the quality and reliability of the scientific literature.

The database used for this study was compiled from a search of all articles indexed by PubMed as retracted publications in English on May 3, 2012. Articles were classified according to cause of retraction as fraud, suspected fraud, error, plagiarism, duplicate publication, other, or unknown on the basis of retraction announcements. In addition, retracted articles were cross-checked against the annual reports of the Office of Research Integrity. An internet search using the Google search engine was performed to seek additional information regarding retracted articles for which the reason for retraction remained unclear, and included Retraction Watch, news media, and other public records. In one case, an author was contacted to clarify a published retraction notice. Each classification decision was independently reviewed by all authors and any discrepancies were resolved. Impact factors were based on the 2011 edition of Journal Citation Reports Science Edition (Thomson Reuters, released June 28, 2012) (48), and 5-y impact factors were used when available. In one case (Acta Crystallographica A), the 2011 impact factor (2.076) was used instead of the 5-y impact factor (30.646), because the latter was felt to be anomalous. Journals without an impact factor were assigned a value of 0.1. Statistical analyses were performed using Prism (GraphPad Software).