Retracting Inconclusive Research: Lessons from the Séralini GM Maize Feeding Study

Articles

Abstract

In September 2012, Gilles-Eric Séralini and seven coauthors published an article in Food and Chemical Toxicology claiming that rats fed Roundup©-resistant genetically modified maize alone, genetically modified maize with Roundup©, or Roundup© for 2 years had a higher percentage of tumors and kidney and liver damage than normal controls. Shortly after this study was published, numerous scientists and several scientific organizations criticized the research as methodologically and ethically flawed. In January 2014, the journal retracted the article without the authors’ consent on the grounds that the research was inconclusive. In June 2014, Environmental Sciences Europe published a slightly modified version of the retracted paper. The publication, retraction and subsequent republication of the Séralini study raise important scientific and ethical issues for journal editors. Decisions to retract an article should be made on the basis of well-established policies. Articles should be retracted only for serious errors that undermine the reliability of the data or results, or for serious ethical lapses, such as research misconduct or mistreatment of animal or human subjects. Inconclusiveness, by itself, is not a sufficient reason for retracting an article, though a flawed study design might be. Retracted articles that are submitted for republication should undergo scientific review to ensure that they meet appropriate standards. Republished articles should be linked to the original, retracted publication. Journals that are reviewing studies with significant scientific and social implications should take special care to ensure that peer review is rigorous and fair.

Keywords

Genetically modified foods Retraction Peer review Ethics Scientific methodology 

Notes

Acknowledgments

This research was supported by the Intramural Program of the National Institute of Environmental Health Sciences, National Institutes of Health.

References

  1. Arjo, G., Portero, M., Pinol, C., Vinas, J., Matias-Guiu, X., Capell, T., et al. (2013). Plurality of opinion, scientific discourse and pseudoscience: An in depth analysis of the Seralini et al. study claiming that Roundup Ready corn or the herbicide Roundup cause cancer in rats. Transgenic Research, 22(2), 255–267.CrossRefGoogle Scholar
  2. Barale-Thomas, E. (2013). The SFPT feels compelled to point out weaknesses in the paper by Séralini et al. (2012). Food and Chemical Toxicology, 53, 473–474.CrossRefGoogle Scholar
  3. Batista, R., & Oliveira, M. M. (2009). Facts and fiction of genetically engineered food. Trends in Biotechnology, 27(5), 277–286.CrossRefGoogle Scholar
  4. Berry, C. (2013). Adverse effects in a feeding study of a GM derived corn in rats. Food and Chemical Toxicology, 53, 445–446.CrossRefGoogle Scholar
  5. Bornmann, L., Mutz, R., & Daniel, H. D. (2010). Reliability-generalization study of journal peer reviews: A multilevel meta-analysis of inter-rater reliability and its determinants. PLoS One, 5(12), e14331.CrossRefGoogle Scholar
  6. Brix, A. E., Nyska, A., Haseman, J. K., Sells, D. M., Jokinen, M. P., & Walker, N. J. (2005). Incidences of selected lesions in control female Harlan Sprague-Dawley rats from two-year studies performed by the National Toxicology Program. Toxicologic Pathology, 33(4), 477–483.CrossRefGoogle Scholar
  7. Buiatti, M., Christou, P., & Pastore, G. (2013). The application of GMOs in agriculture and in food production for a better nutrition: Two different scientific points of view. Genes and Nutrition, 8(3), 255–270.CrossRefGoogle Scholar
  8. Butler, D. (2012). Hyped GM maize study faces growing scrutiny. Food-safety bodies slam feeding study that claims increased cancer incidence in rats. Nature, 490(7419), 158.CrossRefGoogle Scholar
  9. Casassus, B. (2014). Change of journal does not convince critics that rat diseases were caused by genetically modified maize. Nature News, 24 June 2014. Available at http://www.nature.com/news/paper-claiming-gm-link-with-tumours-republished-1.15463 Accessed 15 Jan 2015.
  10. Committee on Publication Ethics. (2009). Retraction guidelines. Available at http://publicationethics.org/files/retraction%20guidelines.pdf. Accessed 15 Jan 2015.
  11. de Souza, L., & Macedo, O. L. (2013). Long term toxicity of a Roundup herbicide and a Roundup-tolerant genetically modified maize. Food and Chemical Toxicology, 53, 440.CrossRefGoogle Scholar
  12. Dwan, K., Gamble, C., Williamson, P. R., Kirkham, J. J., & Reporting Bias Group. (2013). Systematic review of the empirical evidence of study publication bias and outcome reporting bias—an updated review. PLoS One, 8(7), e66844.CrossRefGoogle Scholar
  13. EFSA, GMO Panel Working Group on Animal Feeding Trials. (2008). Safety and nutritional assessment of GM plants and derived food and feed: The role of animal feeding trials. Food and Chemical Toxicology, 46(Supplement 1), S2–S70.Google Scholar
  14. Entine, J. (2014). Profile of Gilles-Éric Séralini, author of republished retracted GMO corn rat study. American Enterprise Institute, June 24, 2014. Available at http://www.aei.org/article/health/profile-of-gilles-eric-seralini/. Accessed 15 Jan 2015.
  15. Environmental Working Group. (2012). Five things you should know about GMOs. Available at http://www.ewg.org/research/five-things-you-should-know-about-gmos. Accessed 15 Jan 2015.
  16. Food and Chemical Toxicology. (2014a). Retraction notice to “Long term toxicity of a Roundup herbicide and a Roundup-tolerant genetically modified maize” [Food Chem. Toxicol. 50 (2012) 4221–4231]. Food and Chemical Toxicology, 63, 244.Google Scholar
  17. Food and Chemical Toxicology. (2014b). Editorial board. Available at http://www.journals.elsevier.com/food-and-chemical-toxicology/editorial-board/. Accessed 15 Jan 2015.
  18. Fugh-Berman, A., & Sherman, T. G. (2014). Rounding up scientific journals. Bioethics Forum, 10 January 2014. Available at http://www.thehastingscenter.org/Bioethicsforum/Post.aspx?id=6684. Accessed 15 Jan 2015.
  19. Grunewald, W., & Bury, J. (2013). Comment on “Long term toxicity of a Roundup herbicide and a Roundup-tolerant genetically modified maize” by Séralini et al. Food and Chemical Toxicology, 53, 447–448.CrossRefGoogle Scholar
  20. Hammond, B., Dudek, R., Lemen, J., & Nemeth, M. (2004). Results of a 13 week safety assurance study with rats fed grain from glyphosate tolerant corn. Food and Chemical Toxicology, 42(6), 1003–1014.CrossRefGoogle Scholar
  21. Hammond, B., Goldstein, D. A., & Saltmiras, D. (2013). Response to original research article, in press, corrected proof, ‘‘Long term toxicity of a Roundup herbicide and a Roundup-tolerant genetically modified maize’’. Food and Chemical Toxicology, 53, 459–464.Google Scholar
  22. Institute of Science and Society. (2013). Retracting Séralini study violates science and ethics. Available at http://www.isis.org.uk/Retracting_Serallini_study_violates_science_and_ethics.php. Accessed 15 Jan 2015.
  23. Langridge, P. (2013). Problems lie at several levels and bring into serious question the quality and standard of the editorial processes in your journal. Food and Chemical Toxicology, 53, 441.CrossRefGoogle Scholar
  24. Lee, C. J., Sugimoto, C. R., Zhang, G., & Cronin, B. (2012). Bias in peer review. Journal of the American Society for Information Science and Technology, 64(1), 2–17.CrossRefGoogle Scholar
  25. Lemaux, P. G. (2008). Genetically engineered plants and foods: A scientist’s analysis of the issues (part I). Annual Review of Plant Biology, 59, 771–812.CrossRefGoogle Scholar
  26. Nicole, W. (2012). A closer look at GE corn findings. Environmental Health Perspectives, 120(11), A421.CrossRefGoogle Scholar
  27. Ollivier, L. (2013). A comment on “Séralini, G.-E. et al., Long term toxicity of a Roundup herbicide and a Roundup-tolerant genetically modified maize. Food Chem. Toxicol. (2012).” http://dx.doi.org/10.1016/j.fct.2012.08.005. Food and Chemical Toxicology, 53, 458.
  28. Panchin, A. Y. (2013). Toxicity of Roundup-tolerant genetically modified maize is not supported by statistical tests. Food and Chemical Toxicology, 53, 475.CrossRefGoogle Scholar
  29. Portier, C. J., Goldman, L. R., & Goldstein, B. D. (2014). Inconclusive findings: Now you see them, now you don’t! Environmental Health Perspectives, 122(2), A36.CrossRefGoogle Scholar
  30. Public Citizen. (2014). Genetically modified organisms. Available at http://www.citizen.org/publications/publicationredirect.cfm?ID=5102. Accessed 15 January 2015.
  31. Resnik, D. B. (2012). Environmental health ethics. Cambridge: Cambridge University Press.Google Scholar
  32. Retraction Watch. (2014). Retracted Seralini GMO-rat study republished. Available at http://retractionwatch.com/2014/06/24/retracted-seralini-gmo-rat-study-republished/. Accessed 15 Jan 2015.
  33. Robert, W., Lerayer, A., Fedoroff, N., Giddings, L. V., Strauss, S. H., Leaver, C., et al. (2013). We request a serious reconsideration of the recent paper by Seraliniet al. alleging tumorigenesis in rats resulting from consumption of corn derived from crops improved through biotechnology (Séralini et al. 2012). Food and Chemical Toxicology, 53, 455–456.CrossRefGoogle Scholar
  34. Sanders, D., Kamoun, S., Williams, B., & Festing, M. (2013). Re: Séralini, G.-E., et al. Long term toxicity of a Roundup herbicide and a Roundup-tolerant genetically modified maize. Food Chem. Toxicol. (2012). Food and Chemical Toxicology, 53, 450–453. Google Scholar
  35. Schorsch, F. (2013). Serious inadequacies regarding the pathology data presented in the paper by Séralini et al. (2012). Food and Chemical Toxicology, 53, 465–466.CrossRefGoogle Scholar
  36. Schroter, S., Black, N., Evans, S., Godlee, F., Osorio, L., & Smith, R. (2008). What errors do peer reviewers detect, and does training improve their ability to detect them? Journal of the Royal Society of Medicine, 101(10), 507–514.CrossRefGoogle Scholar
  37. Séralini, G. E., Clair, E., Mesnage, R., Gress, S., Defarge, N., Malatesta, M., Hennequin, D., & de Vendômois, J. S. (2012). Long term toxicity of a Roundup herbicide and a Roundup-tolerant genetically modified maize. Food and Chemical Toxicology, 50(11), 4221–4231. Retraction in: Food and Chemical Toxicology (2014), 63, 244.Google Scholar
  38. Séralini, G. E., Mesnage, R., Defarge, N., Gress, S., Hennequin, D., Clair, E., et al. (2013). Answers to critics: Why there is a long term toxicity due to a Roundup-tolerant genetically modified maize and to a Roundup herbicide. Food and Chemical Toxicology, 53, 476–483.CrossRefGoogle Scholar
  39. Séralini, G. E., Clair, E., Mesnage, R., Gress, S., Defarge, N., Malatesta, M., et al. (2014a). Republished study: Long-term toxicity of a Roundup herbicide and a Roundup-tolerant genetically modified maize. Environmental Sciences Europe, 26, 14.CrossRefGoogle Scholar
  40. Séralini, G. E., Mesnage, R., Defarge, N., & de Vendômois, J. S. (2014b). Conflicts of interests, confidentiality and censorship in health risk assessment: The example of an herbicide and a GMO. Environmental Sciences Europe, 26, 13.CrossRefGoogle Scholar
  41. Smith, R. (2006). Peer review: A flawed process at the heart of science and journals. Journal of the Royal Society of Medicine, 99(4), 178–182.CrossRefGoogle Scholar
  42. Snell, C., Bernheim, A., Bergé, J. B., Kuntz, M., Pascal, G., Paris, A., & Ricroch, A. E. (2012). Assessment of the health impact of GM plant diets in long-term and multigenerational animal feeding trials: A literature review. Food and Chemical Toxicology, 50(3–4), 1134–1148.CrossRefGoogle Scholar
  43. Tester, M. (2013). It does not become the quality of a journal such as Food and Chemical Toxicology to publish such poor work. Food and Chemical Toxicology, 53, 457.CrossRefGoogle Scholar
  44. Tien, L. D., & Huy, H. L. (2013). Comments on “Long term toxicity of a Roundup herbicide and a Roundup-tolerant genetically modified maize”. Food and Chemical Toxicology, 53, 443–444.CrossRefGoogle Scholar
  45. Zhu, Y., He, X., Luo, Y., Zou, S., Zhou, X., Huang, K., & Xu, W. (2013). A 90-day feeding study of glyphosate-tolerant maize with the G2-aroA gene in Sprague-Dawley rats. Food and Chemical Toxicology, 51, 280–287.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht (outside the USA) 2015

Authors and Affiliations

  1. 1.National Institute of Environmental Health SciencesNational Institutes of HealthResearch Triangle ParkUSA

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