Truth: The Séralini study is the most detailed and thorough study ever done on a GM food and its associated pesticide

Myth at a glance

A study published in 2012 found that a Monsanto GM Roundup-tolerant maize and very low levels of the Roundup herbicide it was engineered to be grown with caused severe organ damage and hormonal disruption in rats fed over a long-term period of two years. Unexpected additional findings were increased rates of large palpable tumours and premature death in some treatment groups.

Starting from just hours after publication, the paper was viciously attacked as “bad science” by pro-GM scientists and commentators. Over a year after it had passed peer review and was published, the journal editor appeared to succumb to the continued pressure and retracted the paper. Scientists worldwide condemned the move as an “act of scientific censorship” and as unjustified on scientific and ethical grounds.

The study, carried out by a team led by Professor Gilles-Eric Séralini, based at the University of Caen, France, remains to date the most detailed and thorough study ever carried out on a GM food crop.

A study published in 2012 found that a Monsanto GM Roundup-tolerant maize and very low levels of the Roundup herbicide it was engineered to be grown with caused severe organ damage and hormonal disruption in rats fed over a long-term period of two years. Unexpected additional observations were increased rates of large palpable tumours and premature death in some treatment groups.1

The study was carried out by a team led by Professor Gilles-Eric Séralini, based at the University of Caen, France.

Why this study?

Séralini designed his two-year rat feeding study1 as a direct follow-up of Monsanto’s short 90-day rat feeding trial on the same GM NK603 maize, which the company had conducted to support its application for regulatory authorization. Monsanto published the results of its trial in 2004,2 the same year that the maize was authorized in the EU.

Differences were found in the GM-fed rats, but the Monsanto authors dismissed the findings as not related to the GM maize and as not “biologically meaningful”.2 The European Food Safety Authority (EFSA) agreed with Monsanto, claiming that the differences were “of no biological significance” and that the maize was as safe as non-GM maize.3

Séralini’s team obtained Monsanto’s raw data and re-analyzed it. They found signs of liver and kidney toxicity in the GM-fed rats, publishing their findings in a peer-reviewed journal in 2009.4

Séralini carried out his 2012 study on NK603 maize and Roundup1 to see whether these initial findings of potential toxicity really were of no biological significance, as Monsanto and EFSA claimed, or whether they developed into serious disease.

The overall experimental design was similar to Monsanto’s, in order to make the two experiments comparable. The differences were that Séralini’s experiment:

  • Was longer (two years to Monsanto’s 90 days) and far more detailed in scope
  • Included three rather than two doses (as Monsanto had used) of the GM maize feed
  • Measured a larger number of bodily functions
  • Was designed to separate out the effects of the GM maize from those of the Roundup herbicide it is engineered to tolerate. This was the first study on a GM crop to distinguish effects in this way.

The methodology

Séralini’s study1 tested the long-term effects of Monsanto’s GM NK603 maize, which is engineered to survive being sprayed with Roundup herbicide, and Roundup, both separately and in combination.

The study used 200 rats divided into ten groups, each of ten males and ten females. The GM maize alone was tested on three groups at 11%, 22% and 33% of the total diet. GM maize that had been sprayed with Roundup in the field was tested on three groups in the same proportions. Roundup alone, given in drinking water at three different doses, was tested on three groups. The lowest dose corresponded to the level of contamination that can be found in some tap water, the intermediate dose to the maximum level permitted in the USA in animal feed, and the highest dose to half the strength of Roundup as used in agriculture. Controls were fed a diet containing 33% non-GM maize and plain drinking water.

The findings in brief – and their implications

Séralini’s findings were alarming. Both GM maize NK603 and Roundup caused serious kidney and liver damage and an increased and earlier development of large palpable tumours, leading to an increased rate of mortality. The first tumours only appeared four months into the study, one month after Monsanto’s test had ended, and peaked at 18 months. Many toxic effects found in the GM maize-treated groups were also found in the Roundup-treated groups, indicating that the two substances had similar toxic effects.1

These serious effects had not shown up in Monsanto’s 90-day test2 simply because it was too short. Chronic diseases like organ damage and tumours take time to develop and become obvious.5

An objective analysis of Séralini’s study would conclude that long-term chronic toxicity and carcinogenicity studies are needed on all GM foods and complete commercial pesticide formulations before they are commercialized.

The findings in detail

Toxicological effects

The main findings were multiple organ damage in rats fed the GM maize, whether or not the crop had been sprayed with Roundup, and independently, in rats fed low levels of Roundup in drinking water.

Statistical analysis was conducted on the biochemical measurements of blood and urine samples taken at 15 months, the latest time point when at least 90% of the rats were still alive in each treatment group. Statistically significant damage was found to mammary tissues, liver, kidneys, and pituitary glands of the rats fed the GM maize grown with and without Roundup, and in the rats given Roundup alone in drinking water.

The main objective of the study was to see if the signs of liver and kidney toxicity seen in Monsanto’s 90-day investigation vanished or escalated into serious health problems over an extended period of two years. The study found that the signs of liver and kidney toxicity seen at 90 days did indeed escalate into serious organ damage and failure over a two-year period. Thus the main objective of the study was comprehensively met.

Mortality and tumours

Unexpectedly, both the timing and rate of mortality and tumour growth were affected by the treatments.

Mortality reflected both spontaneous deaths and euthanasia due to tumours that impeded functions such as breathing, nutrition, and digestion. Spontaneous deaths accounted for most male mortality, while euthanasia accounted for most female mortality during the study.

Male and female rats responded differently to the GM maize and Roundup treatments. Whereas 30% of control males and 20% of control females died before the mean survival time, up to 50% of males and 70% of females died prematurely in some groups containing GM maize. However, the rate of mortality did not increase proportionately with the treatment dose, reaching a threshold at the lowest dose (11%) or, for some groups, the mid dose (22%) of GM maize, both with and without Roundup spraying during treatment.

In males, the maximum difference between treatment groups and controls was five times more deaths occurring during the 17th month in the group consuming 11% GM maize, and in females six times greater mortality during the 21st month on the 22% GM maize diet with and without Roundup. In the female treatment groups, there were two to three times more deaths compared with controls by the end of the experiment, and these occurred earlier. Females were more sensitive to the presence of Roundup in drinking water than males, as evidenced by a shorter lifespan. The most common causes of death were linked to large mammary tumours in females, and liver and kidney damage in males.

Three types of tumours were reported: non-regressive palpable tumours (NRPTs), small internal tumours, and metastatic (spreading to other parts of the body) tumours. As with mortality, tumour incidence appeared to vary between male and female animals. Small internal tumours accounted for most tumours in males, and roughly half of those in females, although the proportion varied among treatments. NRPTs in female rats were largely mammary tumours. Metastatic tumours were rare.

None of the treatments affected incidence of small internal or metastatic tumours, but all treatments increased NRPTs as compared to the controls. Furthermore, NRPTs began to occur earlier in treated than in control rats. For male and female animals, respectively, the first NRPT occurred at about 700 and 400 days in controls, compared with 100 and 200-300 days in GM maize treatments, and at around 530–600 and 200–400 days in Roundup-dosed water treatments.

While this was not a carcinogenicity study but a chronic toxicity study, tumour occurrence is relevant for two reasons. First, researchers are required to report tumours even in toxicity studies, according to the chronic toxicity protocol set by the Organization for Economic Cooperation and Development (OECD).6 Second, some types of tumours may indicate metabolic dysfunctions to be explored in further studies.

Nonetheless, of pivotal importance to GMO safety testing is the timing of the tumour onset. The first NRPTs were detected at 4 and 7 months for male and female rats respectively, with most tumours occurring after 18 months. This illustrates the futility of relying on 90-day feeding trials to detect potential risks from chronic exposure to GMOs and their associated pesticides.

Hormonal effects

Both GM NK603 maize and Roundup significantly and independently disrupted hormonal regulation. Substances that do this are known as endocrine disruptors. Séralini’s team suggested possible avenues through which this might happen.

The GM trait inserted into NK603 maize causes the over-expression of a key enzyme that would otherwise be suppressed by glyphosate. The GM version of the enzyme is unaffected by glyphosate, meaning that the GM plant can survive despite being sprayed with glyphosate herbicide.

However, in its original, unmodified state, this enzyme catalyzes the first step in the shikimic acid pathway, a major metabolic trunk with many outcomes. One of those outcomes is the production of the metabolites, caffeic and ferulic acids, which may inhibit the growth of tumours. Ferulic acid is also known to modulate estrogenic activity in mammals and the growth of most mammary tumours is dependent on estrogen. Séralini and colleagues suggested in their paper that the reduced levels of caffeic and ferulic acid found in GM NK603 maize could have contributed to the observed trend of increased tumour occurrence, and specifically to the increased incidence of mammary tumours.

In addition to possible downstream metabolic impacts from the GM trait, it is also necessary to account for the independent effect of glyphosate. Roundup, which may be present as a residue in the sprayed GM maize treatments as well as in the dosed water treatments, is known to disrupt aromatase. This enzyme, also known as estrogen synthetase, catalyzes the conversion of androgen to estrogen. Roundup has further been shown in studies cited by Séralini’s team to impact upon androgen and estrogen receptors, and to act as an endocrine disruptor of sex hormones.

Furthermore, in studies carried out in vitro (laboratory experiments carried out in test tubes or flasks, not in living animals or humans), glyphosate has been shown to act as an estrogen substitute capable of stimulating the growth of estrogen-dependent breast cancer cells at very low doses.7 This may be a contributing factor to the more rapid growth of mammary tumours in the Roundup treatment groups.

Thus both the GM maize and the Roundup herbicide it relies upon had toxic effects on the mammalian physiology in a gender-specific way. In other words, the effects on males were different from the effects on females.

Treatment responses recorded in this study were non-linear, meaning that the effect did not increase in proportion to the dose. They appeared to be more reflective of a threshold-type response. For example, incidence of NRPTs in female rats was uniform across all three doses of Roundup in drinking water. This would suggest that even the lowest dose was high enough to meet the threshold for a full response. Endocrine disruptor effects can act at extremely low concentrations and can be non-linear.8 This may explain why mortality appeared to be higher in male rats fed a diet containing 11% GM maize than a diet containing 22% or 33% GM maize.

The findings of the study challenge the central premise of GM, namely that it is feasible to insert a GM gene to confer a single specific trait without compromising the expression of other apparently unrelated traits.

Study “a bomb”

Séralini’s study was called “a bomb” by Corinne Lepage, a French Member of the European Parliament and France’s former minister for the environment. Lepage explained that the study exposed the weakness of industry studies conducted for regulatory authorization.9 The GM maize had previously been judged safe by regulators around the world, including the European Food Safety Authority (EFSA),3 on the basis of a short 90-day study by Monsanto.2

If the study were taken seriously, it could cause the collapse of the GMO industry worldwide and of the regulatory systems that have approved GM foods as safe since the 1990s.

As an example of the study’s power, seven expert witnesses tried but failed to rebut it in a court case brought by Greenpeace Asia against the Philippines government. The court ruled in Greenpeace’s favour and banned the release of GM Bt brinjal (eggplant/aubergine) on precautionary grounds.10

Campaign to discredit the study

Within hours of the study’s release,1 it came under sustained attack from pro-GM lobbyists and scientists. Leading the campaign to discredit the study was the UK’s Science Media Centre,11 an organization that defends and promotes GM technology and has taken funding from GMO companies like Monsanto and Syngenta.12,13

Séralini’s critics soon turned their attention to trying to get the journal that had published the study to retract it. Many of the critics had undisclosed conflicts of interest with the GM industry or industry-funded lobby groups, or with organizations with vested interests in public acceptance of GM technology.14,15

The study was also dismissed by regulatory agencies, including the European Food Safety Authority (EFSA).16,17,18,19 However, these were the same agencies that had previously approved this or other GM foods as safe. For example, in 2003 EFSA had issued an opinion that GM NK603 maize was as safe as non-GM maize,3 an opinion that had served as the basis for its authorization in Europe for use in food and feed.

EFSA had also previously argued that 90-day feeding trials were sufficient to see even chronic (long-term) toxic effects, adding that even these short tests were not always necessary.20 Yet the first tumours in Séralini’s experiment had only shown up four months into the study, a full month after a 90-day trial would have ended.1 Séralini’s study showed that 90-day tests are inadequate to see chronic effects. So for EFSA to accept that the study had any validity would have been equivalent, as the French Member of the European Parliament and former minister for the environment Corinne Lepage said, to “cutting off the branch on which the agency has sat for years”.21

The French Academy of Sciences issued a statement attacking Séralini’s study, but it was strongly challenged by an eminent member of the Academy, Paul Deheuvels (see Myth 2.2, “Gilles-Eric Séralini”, for details).22

Criticisms misrepresent the study

The main criticisms levelled at Séralini’s study are addressed on a website, gmoseralini.org, set up by scientists and citizens who were concerned that important findings were being buried. Séralini’s team has also replied to the critics in the pages of the journal that published their original research.23

The criticisms rely on a misrepresentation of the study – that it was a flawed carcinogenicity (cancer) study. In fact it was a long-term (chronic) toxicity study, as is made clear in the title and introduction.1 Criticizing the study on these grounds is equivalent to criticizing a cat for not being a dog. It is simply an irrelevance, apparently introduced in order to distract from the main findings of the study, which were toxicological in nature and included severe organ damage and hormonal disturbances.

The “too few rats” criticism

The criticism levelled against the statistical aspect of Séralini’s study is that the numbers of rats in the experiments (ten per sex per group) were too small to draw any conclusions about tumours. The critics claimed that given the relatively low numbers of rats and the tendency of the Sprague-Dawley strain of rat to develop tumours spontaneously, the dramatic increase in large palpable tumours in treated groups of rats was only due to random variation and not to the effects of the GM maize and Roundup herbicide.11

However, Séralini’s study was not a carcinogenicity study, for which larger groups of rats are generally used. It was a chronic toxicity study that unexpectedly found an increase in tumour incidence. The number of rats used was appropriate for a chronic toxicity study.24 For example, the chronic toxicity protocol set by the Organisation for Economic Cooperation and Development for industry testing of chemicals recommends that 20 rats per sex per group be used, but stipulates that only 50% (10 per sex per group) need to be analyzed for blood and urine chemistry.6 This is the same number that Séralini used in total, so his experiment yielded the same amount of data as the OECD chronic toxicity studies that form the basis for authorization of thousands of chemicals worldwide.

In addition, the fact that Séralini analyzed 100% of the animals in his study means that he avoided the selection bias introduced by the OECD practice of allowing only 50% of the animals to be analyzed.

The eminent statistician and member of the French Academy of Sciences Paul Deheuvels has defended the statistical aspects of Séralini’s study, including the numbers of rats used. Deheuvels argues that larger numbers of rats (typically 50 per sex per group) are only needed in cancer studies that test the safety of a substance for regulatory assessments. The larger numbers are designed to avoid false negative error, in which a toxic effect exists but is missed because too few rats are used to reliably show it.25

Deheuvels’s point is confirmed by the OECD guideline 116 on how to carry out carcinogenicity and chronic toxicity studies, which states that the purpose of using higher numbers of animals is “in order to increase the sensitivity of the study”.26 Lack of sensitivity of study design was not an issue with Séralini’s investigation, since a dramatic increase in tumour incidence was seen in the treated groups of rats, despite the relatively small size of the groups. Deheuvels said this provided strong evidence that the GM maize and Roundup tested were indeed toxic.25

Peter Saunders, emeritus professor of mathematics at King’s College London, agreed with Deheuvels that the fact Séralini had used smaller groups “makes the results if anything more convincing, not less”. Saunders explained: “Using a smaller number of rats actually made it less likely to observe any effect. The fact that an effect was observed despite the small number of animals made the result all the more serious.”27

The “wrong strain of rat” criticism

Séralini was also criticized for using the Sprague-Dawley strain of rat, which the critics claimed is unusually prone to tumours.11 The reasoning is that the rats could have got tumours anyway, even without being exposed to GM NK603 maize and Roundup.

But this criticism is absurd. The Sprague-Dawley (SD) rat is a standard strain for long-term chronic toxicity experiments like Séralini’s, as well as carcinogenicity experiments.28 Monsanto used the SD rat in its chronic toxicity, carcinogenicity, and reproductive toxicity rat feeding studies on glyphosate, the main ingredient of Roundup herbicide, which it conducted in support of regulatory authorisation.29,30

If the SD rat was the wrong strain for Séralini to use, then it was the wrong strain in all these other studies, too, and market authorizations for the thousands of chemicals and GM foods that were authorized on the basis of these studies would have to be revoked.

Monsanto also used the SD rat in its 90-day study on GM NK603 maize.2 Séralini chose the same strain in order to make his experiment comparable with Monsanto’s. If he had used a different strain of rat, he undoubtedly would have been criticized for failing to make his experiment comparable with Monsanto’s.

It has been argued that the SD rat is acceptable for carcinogenicity studies using large numbers of animals but not for studies using smaller numbers due to its “tumour-prone” nature. However, as we have pointed out, Séralini’s study was not a carcinogenicity study, but a chronic toxicity study that unexpectedly found an increase in tumour incidence.

In fact, there is every reason to doubt claims that the SD rat is especially tumour-prone. The SD rat is about as prone to developing cancerous tumours as humans living in industrialized countries, as is shown by data from the Ramazzini Institute in Italy, which specialises in carcinogenicity research and uses this strain of rat.31

And while tumours are not necessarily cancerous, the tumour incidence in control animals in Séralini’s experiment was consistent with data on human cancer incidence in the UK. In Séralini’s study, 30% of female control animals developed tumours,1and the lifetime risk of developing cancer in the UK (excluding non-melanoma skin cancer) is 37% for females and 40% for males.32 It should also be noted that only one of the ten male control animals in Séralini’s experiment developed a tumour and that was very late in life.1

Support from scientists

Séralini’s study was supported by hundreds of independent scientists from across the world in a series of petitions, letters, and articles.33,34,35,36,37,38,39

Two public interest scientific research groups condemned the double standards whereby regulatory authorities relentlessly criticized Séralini’s study for perceived weaknesses in methodology, yet accepted at face value far weaker studies carried out by the GMO industry as proof of the products’ safety.3640

While no research study is perfect and all are limited in scope, Séralini’s study is the most carefully designed, thorough, and detailed to date on a GM food.

The retraction

Over a year after Séralini’s study had passed peer review and was published in the Elsevier journal Food and Chemical Toxicology (FCT), Dr A. Wallace Hayes, the editor-in-chief of the journal, apparently gave in to pressure and retracted the paper.41 The retraction followed a non-transparent post-publication second review process by anonymous persons of unknown professional competence using undisclosed terms of reference.42 It also followed the appointment of a former Monsanto scientist, Richard E. Goodman, to the journal’s editorial board.43

The reasons given by Hayes for retracting the study appear to be unprecedented in the history of scientific publishing. According to the Committee on Publication Ethics (COPE), of which FCT is a member,44 retraction is reserved for cases of unreliable findings due to honest error, misconduct, redundant publication or plagiarism, and unethical research.45

Hayes added that the retraction was solely based on the “inconclusive” nature of the outcomes concerning rates of tumour incidence and mortality, based on the relatively low number of animals and the strain of rat used.42

In a later statement, Hayes appeared to contradict his previous statement that the results were “not incorrect”. He now claimed that the paper was an example of unreliable findings due to “honest error”. He wrote: “The data are inconclusive, therefore the claim (i.e. conclusion) that Roundup Ready maize NK603 and/or the Roundup herbicide have a link to cancer is unreliable… it is the entire paper, with the claim that there is a definitive link between GMO and cancer that is being retracted.”46

However, this is a misrepresentation of Séralini’s paper. The authors did not claim that the GM maize NK603 and/or Roundup herbicide have a “link to cancer”, let alone a “definitive link”. In fact, the word “cancer” is not even used in the paper and the authors specified in their introduction that the study was not designed as a carcinogenicity study.1

Moreover, it is unacceptable to retract an entire paper on the grounds of the perceived inconclusiveness of some of its findings. The chronic toxicity findings – the organ damage and hormonal disruption – are solidly based and statistically significant, and have not been challenged by Hayes. Yet these findings have been removed from the record based on the perceived inconclusiveness of a part of the study’s findings – the rates of tumours and mortality.

Scientists condemn retraction

Heinemann concluded that in science, getting less than definitive results is “not uncommon” and that such findings must be allowed to stand the test of time and further research.47

David Schubert, a professor with the Salk Institute for Biological Studies in the USA, commented on the purported rationale for the retraction, “The editors claim the reason was that ‘no definitive conclusions can be reached.’ As a scientist, I can assure you that if this were a valid reason for retracting a publication, a large fraction of the scientific literature would not exist.”48

Schubert added, “The major criticisms of the Séralini manuscript were that the proper strain of rats was not used and their numbers were too small. Neither criticism is valid. The strain of rat is that required by the FDA for drug toxicology, and the toxic effects were unambiguously significant.”48

The European Network of Scientists for Social and Environmental Responsibility (ENSSER) said in a statement that the retraction violates the “standards of good science”, adding, “‘Conclusive’ results are rare in science, and certainly not to be decided by one editor and a secret team of persons using undisclosed criteria and methods. Independent science would cease to exist if this were to be an accepted mode of procedure.”49

ENSSER denounced the lack of transparency about how the decision to retract the paper was reached, noting, “In a case like this, where many of those who denounced the study have long-standing, well-documented links to the GM industry and, therefore, a clear interest in having the results of the study discredited, such lack of transparency … is inexcusable, unscientific and unacceptable. It raises the suspicion that the retraction is a favour to the interested industry, notably Monsanto.”49

A group of Mexican scientists also criticized Hayes for giving in to “pressure” from multinational companies to retract the study. Elena Alvarez-Buylla, a member of the Union of Scientists Committed to Society (UCCS), said the retraction “has no scientific basis and is in response to pressures from multinational companies that market GM crops.”50

Three researchers writing in the scientific journal Environmental Health Perspectives stated that the retraction of any paper on grounds of inconclusiveness “has adverse implications on the integrity of the concept of the peer-review process as the critical foundation of unbiased scientific inquiry” and marks “a significant and destructive shift in management of the publication of controversial scientific research”.51

The retraction was condemned as an “act of scientific censorship” by 181 scientists on the website endsciencecensorship.org.52 Some of the scientists authored an article on the website explaining why the retraction was not justified ethically or scientifically. They noted that insofar as definitive conclusions exist in science, “they tend to be found in fields that have been studied for many years. For example, there is a definite conclusion that gravity exists on earth, but no journal would be interested in publishing such known facts. Scientific publications are about new knowledge and new data. This hardly ever arrives accompanied by ‘definitive conclusions’.”53

In a separate initiative, over 1,340 scientists pledged to boycott Elsevier over the retraction on the website of the Institute of Science in Society.54

The French MEP Corinne Lepage commented that the purpose of the retraction was to shut down the possibility of long-term studies on GMOs forever. She said, “The study by Gilles-Eric Séralini should not have happened. But it did happen. Now it must be as if it had never happened.”55

Conclusion

The Séralini study is the most in-depth study ever carried out on a GM food and its associated pesticide.

The attacks on the study and its subsequent retraction by the editor of the journal that published it have been widely condemned by scientists as commercially motivated, based on misrepresentations of the study, and not scientifically justified. The editor’s purported rationale for retraction – inconclusiveness of some aspects of the study – is not credible, since lack of conclusiveness is common in scientific studies.

Also, the main findings of the study, consisting of the organ damage and hormonal disruption, are statistically significant and are not disputed by the journal editor. Nevertheless the entire study has been retracted on the basis of the alleged inconclusiveness of some of its findings – the rates of tumour incidence and mortality.

Any uncertainties and questions raised by the study’s findings can only be resolved by further long-term studies.

In the meantime, GM NK603 maize and Roundup should be withdrawn from the market, as they have not been proven to be safe over the long term and the study by Séralini and colleagues provides evidence that they are not safe.

References

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