Most Studies Indicate Popular GM Food Not as Safe as Conventional Counterpart

Background:

Genetically modified (GM) food safety is a controversial subject. Some use the narrative reviews Nicolia 2014 and Sanchez 2017 to claim that the consensus in the scientific literature is that all GM foods currently on the market are as safe as their conventional counterparts.

Purpose:

To examine feeding studies using animals comparable to humans fed GM soy with single event GTS 40-3-2, and health parameters, which were reviewed by Nicolia 2014 and Sanchez 2017. Since the claim is that all GM foods currently on the market are as safe as their conventional counterparts, if the consensus in the scientific literature is that even a single GM food on the market is less safe, then this claim must be rejected. We chose GTS 40-3-2 as it is one of the most grown, has the most animal feeding studies according to Sanchez 2017 and is one of the most approved GM foods internationally.

Data Sources and Selection:

Review of all sources purported to be used by Nicolia 2014 and Sanchez 2017 pertaining to relevant animal feeding studies using GM food GTS 40-3-2.

Data Extraction:

Relevant studies were identified which used GTS 40-3-2.

Results:

Sanchez 2017

71.4% of relevant studies reviewed in Sanchez 2017 suggest adverse effects or biomarkers indicative of adverse effects from the GTS 40-3-2 diet.

100% of the medium and long-term studies, of 6 months feeding duration or longer, reviewed in Sanchez 2017 suggest adverse effects or biomarkers indicative of adverse effects from the GTS 40-3-2 diet.

86.2% of the relevant studies that should have been reviewed in Sanchez 2017 suggest adverse effects or biomarkers indicative of adverse effects from the GTS 40-3-2 diet.

Nicolia 2014

90% of relevant studies reviewed by Nicolia et al. suggest adverse effects or biomarkers indicative of adverse effects from the GTS 40-3-2 diet.

100% of the medium and long-term studies, of 6 months feeding duration or longer, reviewed in Nicolia 2014 suggest adverse effects or biomarkers indicative of adverse effects from the GTS 40-3-2 diet.

94.7% of the relevant studies that should have been reviewed in Nicolia 2014 suggest adverse effects or biomarkers indicative of adverse effects from the GTS 40-3-2 diet.

Conclusion:

Based on the results of our systematic review, the claim that all GM foods currently on the market are as safe as their conventional counterparts is not supported by the weight of the scientific evidence. Instead, a clear consensus in the scientific literature regarding the popular GM food GTS 40-3-2, considered to be the most tested GM food, has emerged. Our systematic review of the scientific evidence indicates that in most of the relevant animal feeding studies there were adverse effects or biomarkers indicative of adverse effects reported.

These results are consistent with systematic reviews indicating an overwhelming consensus among health groups and individual health professionals on GM foods. The consensus among these health experts is that GM foods currently on the market cannot presently be considered as safe as their conventional counterparts (GMO Free Florida 2022, GMO Free Florida 2022a). Therefore, we call upon the health community, who are the experts on health, to continue to inform the public of the potential harms from GM foods and to choose non-GMO and organic foods to avoid those potential harms. We urge the governments of the world to impose a moratorium on all GM foods until each GM food has been demonstrated as safe in independent long-term and multigenerational chronic toxicity/carcinogenicity studies using both rodents and non-rodents comparable to humans. We also call upon all who have published papers claiming that there is a consensus that all GM foods on the market are safe to provide corrections, or formally retract their papers if necessary. Our systematic reviews indicate this claim is not supported by the consensus, nor does it appear this claim was ever supported by the consensus.

A precautionary approach should be taken especially since there is now a consensus among health groups and individual health professionals that GM foods currently on the market cannot be considered as safe as their conventional counterparts at this present time and a consensus in the scientific literature that some GM foods currently on the market may be unsafe compared to their conventional counterparts.

Disclaimer: Neither GMO Free Florida, our fiscal sponsor GMO Free USA, nor any person acting on behalf of GMO Free Florida or GMO Free USA are responsible for the use, actions or decisions taken as a result of the information in this report. The views expressed in this report are those of the unpaid volunteers who authored this report and are not necessarily the views of GMO Free Florida or GMO Free USA. The authors declare no conflicts of interest.

Introduction:

Genetically modified (GM) foods are also referred to as genetically engineered (GE) or bioengineered (BE) foods. These include foods modified through techniques such as transgenesis, intragenesis, cisgenesis, zinc finger proteins, transcription activator-like effector nucleases, and clustered, regularly interspaced, short, palindromic repeats. The process of genetic modification can result in unexpected consequences, potentially causing the plant to produce toxins, create foreign proteins, or other unanticipated results (Ho 2013, Wilson 2006, Dona 2009, Rang 2005, Mesnage 2016, Eckerstorfer 2019). GM food safety is, therefore, a controversial subject.

Animal feeding studies are one of the main lines of evidence used to claim GM foods currently on the market are as safe as conventional foods. For example, the American Association for the Advancement of Science Board of Director’s statement mentions animal feeding studies as evidence for the safety of GM foods (American Association for the Advancement of Science 2012). Narrative reviews which include animal feeding studies are often cited to claim there is a consensus that all GM foods currently on the market are as safe as their conventional counterparts. The narrative reviews Nicolia 2014 and Sanchez 2017 are some of the most cited reviews when making this claim (Blair 2020).

Glyphosate tolerant soy varieties have consistently been the most grown GM crop internationally (ISAAA 2019) with GTS 40-3-2 being the dominant event over most of that time (Bøhn 2014). GTS 40-3-2 continues to be one of the most grown GM soy events in countries such as the United States and Brazil where most of the GM soy is grown (Soga 2020). GTS 40-3-2 is also the most analyzed GM food, having the greatest number of animal health studies (Sanchez 2017), and is approved for consumption by the second most number of countries (ISAAA 2019). GM soy has been detected in foods sold in many countries around the world (Grazina 2017, Carvajal 2017, Sakr 2014, Elsanhoty 2013, Rosculete 2018, Nikolić 2009, Ujhelyi 2008, Viljoen 2006). Even in many countries that require GMO labeling, GM soy has been detected in unlabeled foods above the threshold for labeling (Grazina 2017, Rosculete 2018, Ujhelyi 2008, Nikolić 2009).

Since people in most countries are generally consuming GM soy, in many cases without even knowing, it would not be valid to just compare disease rates of different countries to look for harm specific to GM soy. For example, an examination of disease rates for North America compared with western Europe would not be valid, as both groups would generally be consuming GM soy. In the absence of human studies, and with significant challenges for epidemiological studies, animal feeding studies using animals comparable to humans likely provide the best available evidence of safety or harm from GM foods currently available. Therefore, we reviewed peer reviewed studies using animals comparable to humans, health parameters and single event 40-3-2 glyphosate tolerant soy feed which were published between 1993 and 2014. This was used to establish whether the consensus claim on GM food safety is supported by a systematic review of the scientific literature.

Systematic Review vs. Narrative Review

A systematic review includes a focused question, consistent standard for inclusion and exclusion criteria, a comprehensive search that can be replicated and a conclusion based on the weight of the scientific evidence. A narrative review can include or exclude studies in an arbitrary, or biased, and inconsistent manner to convey a specific narrative which reflects the author’s opinion. A narrative review does not need to be able to be replicated and the conclusion does not have to be based on the weight of the scientific evidence (Rys 2009). Since narrative reviews have a large potential to be biased, apply double standards and omit relevant studies, such reviews are not considered high quality evidence (UTHealth 2020). Therefore, narrative reviews should not be used as evidence to claim a consensus that all GM foods on the market are as safe as their conventional counterparts (Icahn Undated). Unlike Nicolia 2014 and Sanchez 2017, our systematic review can be replicated, does not apply inconsistent standards or omit relevant studies, or use other forms of bias. Our systematic review also relies on the weight of the scientific evidence to answer a focused question about the safety of one of the most popular GM foods on the market, GM soy GTS 40-3-2.

Sanchez Reviews

The results of our systematic reviews on the opinions of health groups and surveys of health practitioners (GMO Free Florida 2022, GMO Free Florida 2022a) appear to conflict with a recent narrative review (Sanchez 2017). The Sanchez 2017 review concluded that only 5% of the studies using GM foods reported adverse effects. Sanchez 2017 also concluded that a greater number of studies reporting adverse effects had a conflict of interest (COI) compared to those that did not report adverse effects. We attempted to determine the reason for these conflicting views by examining the Sanchez 2017 narrative review in detail. We focused specifically on relevant animal health studies using GM soy GTS 40-3-2 as Sanchez 2017 states this is the most analyzed GM food.

Results Cannot Be Verified or Replicated:

Sanchez 2017 reports using references cited on the internet by GMO Free USA, Coalition for a GM Free India and GM Watch, but does not identify the exact sources used. Therefore, it is not possible to verify or replicate many of the claims made. References cited in the internet could include numerous posts on Facebook, Twitter, and other social media platforms as well as websites. Since Sanchez 2017 does not provide any details as to what sources were actually reviewed, their claims cannot be verified and, therefore, their conclusions are unreliable.

Glyphosate Tolerant Soy GTS 40-3-2 Systematic Review:

We, therefore, took a fresh look at the data purported to be used in Sanchez 2017. In Sanchez 2015 it was declared that the category of “Animal health” had the most studies. We reviewed animal health studies limiting our search to in vivo studies using rodents, pigs, dogs, non-human primates and humans  as subjects, however, no studies were found using dogs, non-human primates and humans. Such studies are one of the main lines of evidence used to claim GM foods currently on the market are as safe as conventional foods. Animal health studies also appear to represent the majority of the studies, and GM soy event 40-3-2 has been the most analyzed according to Sanchez 2017.

We, therefore, reviewed animal health studies that were published in peer reviewed journals during the timeframe used by Sanchez 2015 and found in the Sanchez 2015 and Sanchez 2017 reviews. We also used studies cited in the Internet by the Coalition for a GM Free India document “Adverse Impacts of Transgenic Crops/Foods a Compilation of Scientific References With Abstracts” and from the GMO Free USA website from April 2016 and from 1 Facebook post by GMO Free USA (GMO Free USA 2017). All of these were published before Sanchez 2017 and therefore would have been accessible to the authors.

Results:  See Supplementary Table Report 3.

Only 4 animal health studies specifically mentioning, or providing a reference that specifically mentioned, the use of GTS 40-3-2 were used in Sanchez 2015 in which the authors do not report adverse effects (Zhu 2004, Reichert 2012, Bednarek 2013, Świątkiewicz 2013). However, 10 such peer reviewed studies specifically mentioning, or providing a reference that specifically mentioned, the use of GTS 40-3-2 are used in Sanchez 2017 in which the authors report adverse effects or biomarkers indicative of adverse effects (Battistelli 2008, Battistelli 2010, Cisterna 2008, Magaña-Gómez 2008, Malatesta 2002a, Malatesta 2002b, Malatesta 2003, Malatesta 2005, Malatesta 2008a, Vecchio 2004). In other words, most studies (71.4%) suggest adverse effects or biomarkers indicative of adverse effects in the animals fed the GM soy GTS 40-3-2 diet.

GM foods are generally intended to be consumed for a lifetime by humans and animals of different ages, sexes, and with different medical conditions. Therefore, many health practitioners have concluded that these novel foods should be tested in long-term studies before approval (GMO Free Florida 2022). When we examine the medium and long-term studies, of 6 months feeding duration or longer, 100% of the peer reviewed studies suggest adverse effects or biomarkers indicative of adverse effects from the GM soy GTS 40-3-2 diet (Battistelli 2010, Malatesta 2002a, Malatesta 2002b, Malatesta 2003, Malatesta 2008a, Vecchio 2004).

According to Sanchez 2017 when studies “do not indicate which event was evaluated,” this “makes it impossible to replicate the experiments or interpret the results” (Sanchez 2017).  However, in order to ensure that these results were not skewed by omitting studies which did not mention the event we also included studies which: 1. mention the soybean having the gene cp4 epsps, 2. Mention the soy used being “Roundup tolerant” or “glyphosate tolerant”, or 3. mention that GM soybeans in general are “Roundup tolerant” or “glyphosate tolerant”. Although soybeans having the gene cp4 epsps could indicate it is event 40-3-2, it is also possible that it could be the experimental line 61-67-1 (Hammond 1996) or another line such as MON-89788-1. The same possibility exists for studies stating the soy is “Roundup tolerant” or “glyphosate tolerant”.

Using the criteria above increases the number of studies not reporting adverse effects to 10 (Zhu 2004, Reichert 2012, Bednarek 2013, Świątkiewicz 2013, Teshima 2000, Sbruzzi 2013, Brake 2004, Sakamoto 2007, Sakamoto 2008, Daleprane 2010). However, 13 peer reviewed studies report adverse effects or biomarkers indicative of adverse effects were observed or that non-GMO soy had a greater health benefit than GM soy (Azevedo 2010, Battistelli 2008, Battistelli 2010, Cisterna 2008, Malatesta 2002a, Malatesta 2002b, Malatesta 2003, Malatesta 2005, Malatesta 2008a, Vecchio 2004, Magaña-Gómez 2008, Brasil 2009, Venâncio 2012). In other words, most studies (about 56.5%) report adverse effects or biomarkers indicative of adverse effects from the GM soy diet or that non-GM had a greater health benefit than GM soy. However, of the 10 studies where the authors did not report adverse effects there are examples where other researchers looked at the same data and came to different conclusions (Séralini 2011) or concluded these studies were inadequate to suggest safety (Zdziarski 2014).

When we examine the medium and long-term studies, of 6 months feeding duration or longer, 70% of studies suggest adverse effects or biomarkers indicative of adverse effects from the GM soy diet (Battistelli 2010, Malatesta 2002a, Malatesta 2002b, Malatesta 2003, Malatesta 2008a, Vecchio 2004, Brasil 2009, Sakamoto 2007, Sakamoto 2008, Daleprane 2010)

Results from analyzing Sanchez 2015 and 2017, using a consistent standard, references claimed to have been used and above criteria:

It should also be noted that 2 of the studies used by Sanchez 2015, which met the above criteria and did not report adverse effects were in a language other than English (Sakamoto 2007, Sakamoto 2008). Sanchez 2017, however, applied an English language, or Tower of Babel, bias and excluded any studies where adverse effects were observed that were not in English. While an English language bias itself could alter the results of a systematic review, Sanchez took this bias even further and applied favoritism by allowing non-English studies with no adverse effects reported to be included in their overall tally, but excluded any studies where adverse effects were reported that were not in English. Therefore, in order to apply a consistent standard we also included studies from the references claimed to be used by Sanchez 2017 that were not in English.

When non-English language studies are included only 4 studies specifically mentioning, or providing a reference that specifically mentioned, the use of GTS 40-3-2 are used in Sanchez 2015 that the authors do not report adverse effects (Zhu 2004, Reichert 2012, Bednarek 2013, Świątkiewicz 2013). However, there are 25 peer reviewed studies specifically mentioning, or providing a reference that specifically mentioned, the use of GTS 40-3-2, from sources claimed to be used in Sanchez 2017, in which adverse effects or biomarkers indicative of adverse effects are reported (Battistelli 2008, Battistelli 2010, Cisterna 2008, Magaña-Gómez 2008, Malatesta 2002a, Malatesta 2002b, Malatesta 2003, Malatesta 2005, Malatesta 2008a, Vecchio 2004, Dolaychuk 2013, Ermakova 2008, Ermakova 2009, Gorbach 2012, Gubin-Vakulik 2012, Gubin Vakulik 2013, Gubina-Vakulik 2014, Maligin 2008, Nazarova 2010, Samsonyk 2012, Samsonyk 2013a, Samsonyk 2013b, Samsonyk 2014, Semenov 2014, Zinoviev 2014). In other words, most studies (about 86.2%) suggest adverse effects or biomarkers indicative of adverse effects in the GM soy GTS 40-3-2 diet groups.

When we examine the medium and long-term studies, of 6 months feeding duration or longer, 100% of studies suggest adverse effects or biomarkers indicative of adverse effects in the GM soy GTS 40-3-2 diet groups (Battistelli 2010, Malatesta 2002a, Malatesta 2002b, Malatesta 2003, Malatesta 2008a, Vecchio 2004, Gorbach 2012, Gubin-Vakulik 2012, Gubin-Vakulik 2013, Zinoviev 2014).

Using the criteria above of including studies which: 1. mention the soybean having the gene cp4 epsps, 2. Mention the soy being “Roundup tolerant” or “glyphosate tolerant” or, 3. mentioning that GM soybeans are “Roundup tolerant” or “glyphosate tolerant”, the number of studies not reporting adverse effects were observed is 10 (Zhu 2004, Reichert 2012, Bednarek 2013, Świątkiewicz 2013, Teshima 2000, Sbruzzi 2013, Brake 2004, Sakamoto 2007, Sakamoto 2008, Daleprane 2010). However, 31 peer reviewed studies report that adverse effects or biomarkers indicative of adverse effects were observed or that non-GMO soy had a greater health benefit than GM soy (Azevedo 2010, Battistelli 2008, Battistelli 2010, Cisterna 2008, Magaña-Gómez 2008, Malatesta 2002a, Malatesta 2002b, Malatesta 2003, Malatesta 2005, Malatesta 2008a, Vecchio 2004, Brasil 2009, Dolaychuk 2013, Ermakova 2008, Ermakova 2009, Gorbach 2012, Gubin-Vakulik 2012, Gubin Vakulik 2013, Gubina-Vakulik 2014, Maligin 2008, Nazarova 2010, Samsonyk 2012, Samsonyk 2013a, Samsonyk 2013b, Samsonyk 2014, Semenov 2014, Zinoviev 2014, Kulik 2014, Long 2014, Venâncio 2012, Zhou 2012a). In other words, most studies (about 75.6%) suggest adverse effects or biomarkers indicative of adverse effects in the GM soy diet groups.

When we examine the medium and long-term studies, of 6 months feeding duration or longer, then 80% of studies suggest adverse effects or biomarkers indicative of adverse effects in the GM soy diet groups (Battistelli 2010, Malatesta 2002a, Malatesta 2002b, Malatesta 2003, Malatesta 2008a, Vecchio 2004, Gorbach 2012, Gubin-Vakulik 2012, Gubin Vakulik 2013, Zinoviev 2014, Brasil 2009, Kulik 2014, Sakamoto 2007, Sakamoto 2008, Daleprane 2010).

Discussion – Glyphosate Tolerant Soy GTS 40-3-2 Systematic Review:

Sanchez 2017 is fundamentally flawed in a number of ways. The authors fail to identify the exact sources used from GMO Free USA, GMWatch and Coalition for a GM Free India making the results of Sanchez 2017 impossible to replicate. The results of our review, however, indicate that when a consistent standard is applied 86.2% of peer reviewed studies indicate adverse effects or biomarkers indicative of adverse effects from the GM soy GTS 40-3-2 diet. Of the medium and long-term studies using the GM soy GTS 40-3-2 diet, 100% indicate adverse effects or biomarkers indicative of adverse effects.

With regards to the studies where adverse effects were reported that were reviewed in Sanchez 2017 the authors claim, “In general terms, all papers analysed here violate at least one of the basic standards for assessment of GM food/feed safety”. For this claim they reference a European Food Safety Authority (EFSA) 2011 report which states, “Internationally agreed test methods described by the OECD (OECD, b) or by the European Commission (EC, 2002) should be used for toxicity testing” (European Food Safety Authority 2011). The Organisation for Economic Co-operation and Development (OECD), as its name implies, was designed to stimulate the economies of the world by progressing world trade.

In the 1970’s during an FDA audit it was determined that 71% of studies done by Industrial Bio-Test Laboratories (IBT) were considered invalid for having “numerous discrepancies between the study conduct and data” (Seaton 2017). Included among these studies were studies done for Monsanto, developers of GM soy GTS 40-3-2, on the herbicide glyphosate, sprayed on GM soy GTS 40-3-2, for which an EPA reviewer stated, “It is also somewhat difficult not to doubt the scientific integrity of a study when the IBT stated that it took specimens from the uteri (of male rabbits) for histopathological examination” (Jackson 2015).

This led Congress to enact Good Laboratory Practice (GLP) Regulations for the FDA (Seaton 2017) which was based on a draft written by G.D. Searle & Company, a laboratory the FDA also determined had numerous problems with regard to scientific integrity and quality control (Baldeshwiler 2003). In this way GLP was written by industry for industry. A remarkably similar GLP document was then adopted by the OECD a few years later (Huntsinger 2008). GLP, however, has not stopped scientific misconduct. For example, in 1991 Craven Laboratories, was determined to have been involved in scientific misconduct in its testing of pesticides during the same time it was hired to conduct studies on glyphosate for Monsanto (Jackson 2015).

OECD guidelines are intended to be the minimal standard for industry to claim no harm, used to try to avoid cases of fraud, and is not the highest standard. For example, the OECD Test Guidelines at the time of the studies reviewed here were not sensitive enough to detect some toxicity (Buonsante 2014). The OECD Test Guidelines are standards for industry to use when conducting studies themselves, they are not the standard required for non-industry studies to be considered relevant. For example, EFSA also states, “the fact that a study may not be conducted in accordance with Good Laboratory Practice (GLP) does not imply that the study is irrelevant” (European Food Safety Authority 2011a).

However, even when examining the 4 studies finding no adverse effects for GM soy GTS 40-3-2 it can be seen they also violate at least one of the OECD standards. Reichert 2012, Bednarek 2013 and Świątkiewicz 2013 all use pigs as subjects and therefore would fall under OECD Test No. 409. This test states, “Three concentrations, at least, should be used” (OECD 1998). However, Reichert 2012 does not specifically mention the concentration(s) used. Bednarek 2013 uses only one concentration for the same group of porkers of 18% when they are younger growers and 14% as older finishing pigs and one concentration for sows of 4% in the low in grower and 14% in high in sow mixture. Świątkiewicz 2013 uses only 1 concentration for the same group of sows of 4% when they are pregnant and 14% when lactating and 26% for their piglet group. The OECD Test No. 409 also states, “The results of this study include: measurements (weighing at least once a week, food/water consumption) and daily (preferably at the same time) and detailed observations (ophtalmological examination, haematology, clinical biochemistry and urinalysis), as well as gross necropsy and histopathology” (OECD 1998). However, the results for several of these parameters are missing from Reichert 2012, Bednarek 2013 and Świątkiewicz 2013. Also, Zhu 2004 fails to adequately report their results (Zdziarski 2014). This makes all of these studies noncompliant with OECD guidelines.

Studies claiming no harm must indeed meet all of the OECD requirements, at an absolute minimum, to make this claim. Yet even then, a claim of no harm would still be suspect as the OECD standards cannot detect some toxicity (Buonsante 2014). Studies which do not meet all of the OECD standards, however,  can be used to claim harm. For example, studies that do not make detailed observations of all of the parameters listed by OECD can still determine adverse effects (e.g., an examination of only a single organ can determine if that organ is damaged). However, studies that examine a limited number of parameters, and not all of the parameters listed by OECD, cannot determine that no adverse effects occurred (e.g., an examination of a single organ cannot be used to claim there are no damaged organs in the entire body).

The results of this review indicate that all studies reviewed were published in journals with similar impact factors, and generally did not test for and/or publish isoflavone results. On the other hand, all of the studies claiming no adverse effects suffer from numerous flaws, primarily that a limited number of parameters were tested and short-durations were used. Contrary to the claim made in Sanchez 2017, none of these studies which do not report adverse effects have met the OECD standard and therefore, have not been conducted under a robust study design. On the other hand, the studies which do report adverse effects do not have to comply with the OECD guidelines to adequately report adverse effects.

The results of this review are alarming as it would be expected that most studies would not report adverse effects because of using such a limited number of parameters and short duration. Yet, the large majority of GTS 40-3-2 studies report adverse effects. At a time when science has a reproducibility crisis, (Ioannidis 2005) the fact that many of these studies report very similar adverse effects only further raises concern as these results are often validated by several studies.

Limitations

It should be noted that we limited our inclusion of references cited on the internet by Coalition for a GM Free India to one document and for inclusion of references cited by GMO Free USA to only their website and 1 Facebook post. Therefore, it is possible that we missed studies that reported adverse effects that were posted by Coalition for a GM Free India and GMO Free USA. It should also be noted that even though Sanchez 2017 mentioned using GM Watch as a source, we did not include any articles from GM Watch in our search. GM Watch was established in 1998 and they often post more than once per day (GMWatch Undated). This would have required including thousands of additional articles in our search and, therefore, it is possible that some relevant studies found on the GM Watch website or social media pages were not included in our review. In fact, it is highly likely that we missed some studies reporting adverse effects that met our criteria, since some such studies are listed in the GMO Research database (https://gmoresearch.org/) and a more recent Facebook post by GMO Free USA (GMO Free USA 2021) that were not included in our review (e.g., Long 2013).

Our review does have some other limitations. Although we included all of the references listed as “Animal Health” from Sanchez 2015, it is possible that Sanchez 2015 was not a thorough review of the studies on GM foods. If Sanchez 2015 did not include several studies, this could explain why so few studies mentioning GTS 40-3-2 did not report adverse effects. This is supported by the fact that we identified many animal health studies mentioning GTS 40-3-2 which reported adverse effects that were not listed in Sanchez 2015. However, this could also just indicate that most of the studies using GTS 40-3-2 report adverse effects.

It is also possible that in Sanchez 2015 studies were mislabeled and put in other categories which should have been labeled as “Animal Health”. As we identified in this review, in Sanchez 2015 some studies were mislabeled as “Animal Health” that either had nothing to do with GMOs or should have been labeled as “Animal Nutrition” or another category. Therefore, it is possible that some actual “Animal Health” studies were miscategorized in Sanchez 2015 and were not included in our review.

Another limitation is that we only reviewed studies from 1993 to 2014, so it is also possible that recent GTS 40-3-2 studies, published after 2014, have not reported adverse effects. However, there are also many studies using GTS 40-3-2 which report adverse effects that were published after 2014 that can be found in the GMO Research database (http://gmoresearch.org) and a more recent Facebook post by GMO Free USA (GMO Free USA 2021). Another limitation is that we only reviewed peer reviewed studies to mimic the criteria used in Sanchez 2015. Systematic reviews, however, should include gray literature (National Institutes of Health 2021, Cochrane Collaboration Undated). Some evidence suggests that including unpublished and/or gray literature in systematic reviews may alter the results (Schmucker 2017). However, there are also several studies using GTS 40-3-2 which report adverse effects in the unpublished and/or gray literature as well that can be found on the GMO Research database (http://gmoresearch.org) and a more recent Facebook post by GMO Free USA (GMO Free USA 2021).

Reevaluation of Sanchez 2015/2017

According to Sanchez 2017 only 5% of studies show adverse effects. Yet, no explanation was given for how they came to this conclusion. Therefore, we took a fresh look at Sanchez 2015 and 2017 to try to determine how they came to this conclusion. As our focus is on the health of animals comparable to humans, we looked at the “Animal Health” studies reported by Sanchez 2015 and 2017 limiting our search to in vitro and in vivo studies using rodents, pigs, dogs, non-human primates and humans. Such studies are one of the main lines of evidence used to claim GM foods currently on the market are as safe as conventional foods. We also used studies cited in the Internet by the Coalition for a GM Free India document “Adverse Impacts of Transgenic Crops/Foods a Compilation of Scientific References With Abstracts”, and from the GMO Free USA website from April 2016 and 1 Facebook post from GMO Free USA (GMO Free USA 2017). All of these were published before Sanchez 2017 and therefore would have been accessible to the authors.

Sanchez 2015 included a study in the “Animal Health” section that appears to have nothing to do with GMOs (Kim 2010). Also included was a study which mentions GMOs, but did not test GMOs and instead tested a glyphosate based herbicide (Malatesta 2008b). If studies testing glyphosate based herbicides were intentionally included in Sanchez 2015 then many studies reporting adverse effects found on the GMO Free USA website were missing in Sanchez 2017 (GMO Free USA Glyphosate Studies). Sanchez 2015 also seems to have mislabeled some studies as being “Animal Health” when these studies should have been labeled as “Transgene Degradation” (Aris 2011) or otherwise did not examine health effects (Soria-Guerra 2011, Madduri 2012). As well as studies that looked at nutrient absorption, not health effects, which should have been labeled as “Animal Nutrition” (Shireen 2002, Tso 2002, Molvig 1997). There was also a literature review that should have been excluded (Knudsen 2007). These were all excluded from our reevaluation.

Sanchez 2015 also included several studies using animals not comparable to humans (Zhang 2000a, Humphrey 2002, Glencross 2003, Singh 2003, Shimada 2003, Hemre 2005, Sanden 2005, Shimada 2006a, Sanden 2006, Sung 2006, Koch 2006, Shimada 2006b, Hemre 2007, Sagstad 2007, Bakke‐McKellep 2007, Stumpff 2007, Frøystad 2008, Sagstad 2008, Bondzio 2008, Trabalza-Marinucci 2008, Bakke-McKellep 2008, Sissener 2009, Sissener 2009a, Frøystad‐Sauge 2009, Grisolia 2009a, Sissener 2010, Scholtz 2010, Anilkumar 2010, Brusetti 2011, Sissener 2011, Tripathi 2011, Tripathi 2012, Guertler 2012, Sanden 2013, Gu 2013, Gao 2013, Gao 2014). These studies were excluded from our reevaluation.

Many studies listed by Sanchez 2015 used a purified protein or a item not consumed by humans (Vazquez-Padron 1999, Vázquez 1999, Vazquez-Padron 2000, Vazquez-Padron 2000a, Moreno-Fierros 2000, Moreno-Fierros 2002, Atkinson 2004, Hileman 2006, Shimada 2006, Peng 2007, Onose 2008, Peng 2008, Grisolia 2009, Xu 2009, Verdin‐Terán 2009, Guimaraes 2010, Quemada 2010, Cao 2010, Galbas 2011, Bondzio 2013, Fuchs 1993, Hérouet 2005, Delaney 2007, Herouet-Guicheney 2009, Juberg 2009, Mathesius 2009, Stagg 2012, Dryzga 2007). In Sanchez 2017 studies suggesting adverse effects that used a purified protein were excluded. Yet, in Sanchez 2015 such studies were included. This inconsistent standard distorts the review data. Therefore, we excluded all studies using purified proteins and non-food items.

Many studies listed by Sanchez 2015 as “Animal Health” were in a language other than English (Wang 2000, Sakamoto 2007, Sakamoto 2008, Tutel’ian 2010, Tyshko 2010, Zhuo 2004, Zhuo 2004a, Chen 2004, Li 2004, Li 2004a, Li 2004b, Tutel’ian 2008, Tyshko 2008, Tutel’ian 2009, Tyshko 2009, Li 2010, Tyshko 2011, Hu 2012, Liang 2012). In Sanchez 2017 studies suggesting adverse effects that were not in English were excluded. Yet, in Sanchez 2015 non-English studies were included. This inconsistent standard, once again, distorts the review data. Since there was no purpose mentioned for excluding non-English studies from Sanchez 2017, we included all non-English studies from Sanchez 2015, as well as the non-English studies that should have been included in Sanchez 2017 to form a consistent standard. We also added in English language studies from Sanchez 2017 as well as English language studies that were missed in Sanchez 2017 that were found on the GMO Free USA website (El-Nahas 2011, Marrelli 2013).

We identified 50 studies reporting adverse effects or that the non-GMO food was healthier than the GM food (Fares 1998, Ewen 1999, Malatesta 2002a, Malatesta 2002b, Malatesta 2003, Vecchio 2004, Malatesta 2005, Kosieradzka 2005, Seralini 2007, Cisterna 2008, Kılıç 2008, Malatesta 2008a, Finamore 2008, Magaña-Gómez 2008, Brasil 2009, De Vendômois 2009, Battistelli 2010, Azevedo 2010, Venâncio 2012, Seralini 2014, Dolaychuk 2013, Ermakova 2008, Ermakova 2009, Gorbach 2012, Gubin-Vakulik 2012, Gubin Vakulik 2013, Gubina-Vakulik 2014, Maligin 2008, Nazarova 2010, Samsonyk 2012, Samsonyk 2013a, Samsonyk 2013b, Samsonyk 2014, Semenov 2014, Zinoviev 2014, Kulik 2014, Long 2014, Zhou 2012a, Alba 2012, El-Nahas 2011, Marrelli 2013, Oraby 2015, Prescott 2005, Battistelli 2008, Kiliçgün 2013, El-Shamei 2012, Gab-Alla 2012, Abdo 2014, Carman 2013, El-Kholy 2014).

We also identified another 18 studies reporting unintended effects or which the authors otherwise could not conclude safety (Hashimoto 1999, Momma 2000, Kosieradzka 2004, Krzyzowska 2010, Pusztai 1999, Richards 2003, Juśkiewicz 2004, Poulsen 2007, Poulsen 2007a, Schrøder 2007, Kroghsbo 2008, Yonemochi 2010, Li 2010a, Li 2010, Xu 2011, Buzoianu 2012, Walsh 2013, Wang 2013a).

We identified 39 studies not reporting adverse/unintended effects, or where the authors did not specifically state they could not conclude on the safety of the GM food used (Teshima 2000, Wang 2000, Teshima 2002, Zhu 2004, Brake 2004, Brake 2004a, Zdunczyk 2005, Kosieradzka 2005a, Seek Rhee 2005, Sakamoto 2007, Sakamoto 2008, Tsai 2008, Tutel’ian 2008, Tyshko 2008, Fallarero 2009, Domon 2009, Singh 2009, Tutel’ian 2009, Tyshko 2009, Daleprane 2010, Tutel’ian 2010, Tyshko 2010, Stoykova 2011, Yen 2011, Adel-Patient 2011, Tyshko 2011, Buzoianu 2012a, Reichert 2012, Arjó 2012, Buzoianu 2012b, Buzoianu 2012c, Walsh 2012, Langkilde 2012, Buzoianu 2013, Bednarek 2013, Lin 2013, Buzoianu 2013a, Sbruzzi 2013, Tyshko 2014).

We also identified 52 studies not reporting adverse/unintended effects, or where the authors did not specifically state they could not conclude on the safety of the GM food used, with financial or professional conflicts of interest. COIs include: 1. authors that were either developers of GM crops/foods or employees of a company that develops GM crops/foods. 2. study was funded by a company, foundation, etc. that develops or funds the development of GM crops/foods. These include, but are not limited to, every “Animal Health” study listed for events 356043, CV127 soy, 305423, Stearidonic acid-enriched soybean, 1507, 1507 x59122, 59122, 98140, DAS-40278-9, 4114, 73496, high-γ-linolenic acid canola and Y642 lysine maize (Appenzeller 2008, Chukwudebe 2012, Delaney 2008, Hammond 2008, Lemke 2010, MacKenzie 2007, Appenzeller 2009, Malley 2007, He 2008, Appenzeller 2009a, Delaney 2013, Delaney 2014, Wainwright 2003, Liu 2004, He 2009, Chen 2003, Hammond 2004, Hammond 2006, Hammond 2006a, Regina 2006, Doull 2007, Healy 2008, Jaszczak 2008, Harris 2008, MacKenzie 2010, Powell 2010, Qi 2012, Hardisty 2013, Wang 2002, Zhuo 2004, Zhuo 2004a, Chen 2004, Li 2004, Li 2004a, Li 2004b, Zhou 2011, Yuan 2011, Liu 2012, Zhou 2012, Cao 2012, Zhu 2012, Tang 2012, Tang 2012a, Hu 2012, Liang 2012, Liang 2013, Zhu 2013, Wang 2013, Yuan 2013, Wang 2014, Zhang 2014, Song 2014).

Conflicts of interest are often associated with outcomes favorable to the interests of GM seed companies (Guillemaud 2016). Therefore, adverse effects are unlikely to be reported for events where only studies with a COI exist. It should be noted that in several studies funding sources and/or other conflicts of interest were not disclosed. In one study a relationship was found between absence of declaration of funding and outcomes favorable to the interests of GM seed companies (Diels 2011). It is also possible that some of the authors or their funders were developers of GM crops and this was not disclosed. Even when conflict of interest statements declare that GM seed companies were not involved in the study, this may not be accurate as GM seed company employees have already secretly ghostwritten or edited parts of papers without the authors declaring this conflict of interest (Krimsky 2018). Therefore, the number of studies with conflicts of interest could be higher than what is indicated here.

The results of our reevaluation indicate that 63.6% of studies without a conflict of interest report adverse effects, that the non-GMO food was healthier than the GM food, unintended effects were reported, or that the authors otherwise could not conclude safety. As with our review on GTS 40-3-2, and unnamed glyphosate tolerant soy, it should be noted that we limited our inclusion of references cited on the internet by Coalition for a GM Free India to one document and by GMO Free USA to only their website and 1 Facebook post and we did not include any articles from GM Watch in our search. Therefore, it is possible that we missed studies that reported adverse effects that were posted by Coalition for a GM Free India, GMO Free USA and GM Watch. In fact, it is highly likely that we missed some studies reporting adverse effects that met our criteria since some such studies are listed in the GMO Research database (https://gmoresearch.org/) and a more recent Facebook post by GMO Free USA (GMO Free USA 2021) that were not included in our review (e.g., Long 2013).

Inconsistent standard and flaws in assessment of Animal Health Studies:

While Sanchez 2017 does not explain how they came to the conclusion that only 5% of studies using GM foods report adverse effects, it would appear they used the 698 references from Sanchez 2015 which included 18 of the 35 listed as adverse in Sanchez 2017 (Fares 1998, Ewen 1999, Malatesta 2002a, Malatesta 2002b, Malatesta 2003, Vecchio 2004, Malatesta 2005, Seralini 2007, Cisterna 2008, Kilic 2008, Malatesta 2008a, Finamore 2008, Magaña‐Gómez 2008, Trabalza-Marinucci 2008, Brasil 2009, De Vendômois 2009, Battistelli 2010, Seralini 2014) leaving an additional 17 studies reporting adverse effects. This added together makes 715 total studies of which Sanchez 2017 identified 35 reporting adverse effects, or about 4.9% reporting adverse effects. There are, however, an abundance of problems with this claim, namely in Sanchez 2017 double standards for inclusion criteria were applied, there were also miscategorized reports and omission of relevant reports.

For example, in Sanchez 2017 a double standard was applied of allowing reports not in English of their choosing, but excluding studies reporting adverse effects that were not in English. Also, the double standard of allowing studies using purified proteins, but excluding any which indicated adverse effects was applied. Sanchez 2015 also has 106 studies listed as “Equivalence” which has little relevance for safety,  since one can transform a plant to express a toxin that could kill humans and that plant could still have similar basic vitamin, mineral, etc. content. Nutritional equivalence, by itself, does not equal safety and those studies do not support a claim of safety. For equivalence only a limited number of biologically active substances are considered in isolation and not how they interact with trait-related characteristics (Miyazaki 2019, Benevenuto 2022).

In Sanchez 2015 there is also 111 studies that are listed as “Animal Nutrition” which again does not consider health parameters such as toxicity or carcinogenicity and cannot be used to claim safety. Even if in Sanchez 2017 the authors mistakenly believed such studies were relevant, this would not explain why they omitted studies from the GMO Free USA website, for example, which report nutritional non-equivalence (e.g., Abdo 2013, Lappe 1999, Bøhn 2014). It is only through double standards for inclusion criteria, miscategorized reports, inclusion of irrelevant reports and omission of relevant reports that Sanchez 2017 could come to such an unsubstantiated conclusion that only 5% of studies using GM foods report adverse effects.

As with our review of GTS 40-3-2 studies, all of the “Animal Health” studies not reporting adverse effects suffer from numerous flaws, mostly that a limited number of parameters were tested and the durations were very short. As we previously mentioned, studies that examine a limited number of parameters can determine adverse effects, however, they cannot determine that no adverse effects occurred. Therefore, contrary to the claim made in Sanchez 2017, none of these studies reporting no adverse effects, “have been conducted under a robust study design”.

Of the reviewed studies with no conflicts of interest, the research group including V.A. Tutel’ian has the greatest number of studies reporting no adverse effects with a total of 8 such studies. Yet, in a 2017 review involving V.A. Tutel’ian it was stated that toxicological tests that are only using one mammal and only lasting  90 days are insufficient, and toxicology studies should be extended for the full life span of the test organism and more than one mammal should be used (Tsatsakis 2017). This indicates that even the most prolific independent author of studies indicating no adverse effects still recognizes that these studies by themselves are insufficient to claim safety and further research is necessary. In this same review it states, “Recent claims of consensus over the safety of genetically modified organisms (GMOs) seems to be an artificial and misguided perpetuated construct” (Tsatsakis 2017). Therefore, the evidence is clearly insufficient to claim any GM foods are safe, yet there is an abundance of evidence from animal studies that GTS 40-3-2 is not as safe as its conventional counterparts.

Inconsistent Standard for Conflicts of Interest:

Sanchez 2017 also applies an inconsistent standard for conflict of interest. In Sanchez 2015 conflict of interest is described as, “financial COIs—those that arise when research is fully or partially funded by a party with a stake in the development of GM crops; and also for professional COIs—those that arise when at least one author is affiliated with a company developing GM crops, even if the research is supported through public funding“.

In Sanchez 2017, however, COIs are described as, “Financial COIs arise when research is fully or partially funded by a party with a stake in the development of GM crops or in activities anti-GMO, whereas professional COIs arise when at least one author is affiliated with a company developing GM crops or anti-GMO institutions, even if the research is supported through public funding.”

Even if the standard stated in Sanchez 2017 is used, it was applied selectively. For example it is argued in Sanchez 2017 that J.L. Domingo, author of a review on GM foods (Domingo 2011), had a COI when he was an editor of Food and Chemical Toxicology journal at the time a study by G.E. Séralini (Séralini 2014a) was accepted. In this case Sanchez 2017 argues that because Domingo published a literature review which questioned the lack of safety testing for GM foods that, somehow, implies a COI even though Sanchez 2017 provides no evidence for Domingo having a conflict of interest. By this logic everyone who has ever conducted a study or published a review and concluded in favor of GM foods or crops must also have a conflict of interest for no reason other than their conclusion.

On the other hand, Wallace Hayes was the editor of the journal Food Chemical Toxicology from 2012-2014 and retracted the Séralini study previously mentioned (Séralini 2014). Wallace Hayes was under contract with Monsanto starting in 2012 with a reported fee of $400 per hour for up to $16,000 (Authorization Letter to Consulting Agreement 2012). Yet, this COI was not mentioned in Sanchez 2017. However, Sanchez 2015 lists 8 studies published in Food Chemical Toxicology between 2012 and 2014 which were not considered to have a conflict of interest for this reason (Wang 2014, Zhang 2014, Zhu 2013, Wang 2013, Mishra 2012, Liu 2012, Qi 2012, Zhou 2012). This indicates a double standard was applied for COIs in Sanchez 2017.

In another example, the Federation of Animal Science Societies (FASS) is owned by the Poultry Science Association, the American Dairy Science Association (ADSA), and the American Society of Animal Science (ASAS) according to their website (Federation of Animal Science Societies Undated). Both the ADSA and the ASAS have received funding directly from Monsanto (Animal and Dairy News 2002). Between the years of at least 2002-2014, Gary Hartnell from Monsanto Company has been involved with ADSA as a director and then with FASS on their Scientific Advisory Committee on Biotechnology (Animal and Dairy News 2002, Federation of Animal Science Societies 2014). Monsanto’s Gary Hartnell even served as the president of FASS from 2007 to 2008 (Federation of Animal Science Societies 2008). The FASS publishes the following journals: Journal of Animal Science, Journal of Dairy Science, Poultry Science, Journal of Applied Poultry Research. Studies published in these journals are listed in Sanchez 2015, and 13 studies published in these journals were considered to be without a conflict of interest for this reason in Sanchez 2015 (Buzoianu 2013, Kim 2010, Beagle 2006, Wiedemann 2006, Scholtz 2010, Gao 2012 Gao 2013, Zhang 2000, Chowdhury 2003, Guthrie 2004, Roush 2004, Barriere 2001, Ash 2003). Here is a group with direct funding from, and affiliation with, Monsanto that is not considered a COI by Sanchez 2015.

Another example is the journal Proceedings of the National Academy of Sciences of the United States of America which is listed as the official journal of the National Academy of Sciences (NAS). The NAS received funding from biotechnology companies such as Monsanto (Krimsky 2017). Studies published in these journals are listed in Sanchez 2015 and 7 studies published in these journals were not considered to have  a conflict of interest for this reason (Molvig 1997, Schubbert 1997, Catchpole 2005, Kristensen 2005, Regina 2006, Batista 2008, Kogel 2010). It should be noted that this is not an exhaustive list of all the individuals or groups which have involvement with GM seed companies which were not considered a COI in Sanchez 2015.

According to Sanchez 2017, Arpad Pusztai is a recognized opponent of GMOs and therefore any study he conducted or even assisted an author with has a COI. However, Pusztai has published research which states the following, “we conclude that transgenic peas may be used in the diet of mammals, including farm animals, particularly at the moderate levels of dietary inclusion recommended in commercial practice” (Pusztai 1999). This statement, in favor of feeding a GM feed to animals, does not support the claim that Pusztai is a recognized opponent of GMOs in general.

If we were to apply the standard used by Sanchez 2017 consistently, then any individual who has ever made a statement in favor of any GMO has a COI, and any group which has done so is therefore a pro-GMO initiative. Anyone who provides funding to such an individual or group would then be a pro-GMO initiative as well. In this case, every study reporting no adverse effects would have to be considered to have a COI. Therefore, applying such a standard would make all studies have a COI which detracts from actual COIs.

On the other hand, many funders with a stake in the development of GM crops do not appear to have been considered a COI by Sanchez 2015/2017. For example, Bio-oriented Technology Research Advancement Institution of Japan (BRAIN), funds research on the development of GM crops (Ku 1999, Matoba 2001). Yet, animal health studies funded by BRAIN (Hashimoto 1999, Momma 2000) do not seem to be considered as having a COI. The Rockefeller Foundation funds the development of GM crops (Rockefeller Archive Center Undated). Yet, an animal health study funded by the Rockefeller Foundation did not seem to be considered as having a COI (Wang 2002). Many animal health studies appear to have been funded by the Chinese government (Chen 2003, Zhuo 2004, Zhuo 2004a, Chen 2004, Li 2004, Li 2004a, Li 2004b, He 2008, He 2009, Li 2010, Li 2010a, Zhou 2011, Xu 2011, Yuan 2011, Liu 2012, Qi 2012, Zhou 2012, Cao 2012, Zhu 2012, Tang 2012, Tang 2012a, Hu 2012, Liang 2012, Liang 2013, Zhu 2013, Wang 2013, Wang 2013a, Yuan 2013, Wang 2014, Zhang 2014, Song 2014)  The Chinese government funds the development of GM crops (Jia 2002) and ChemChina, now one of the largest GM seed companies, is a Chinese state-owned business. Yet, these studies did not seem to have been considered as having a COI for this reason.

Conclusion Sanchez Reviews

The Sanchez 2017 review suffers from numerous flaws. The results cannot be replicated and the inconsistent standards applied make the claims in Sanchez 2017 largely unscientific. When consistent standards are applied the results indicate an alarming number of studies reporting adverse effects.

Nicolia Review

Sanchez 2017 also claims that Nicolia 2014 supports a claim that only 5% of studies using GM foods report adverse effects. Nicolia 2014 concluded, “that the scientific research conducted so far has not detected any significant hazard directly connected with the use of GM crops”. However, they note, “It appears that knowledge on Gene flow and GE food/feed consumption would have benefited from a higher number of publications considering their high impact on both environmental and food/feed risk assessment.” In Nicolia 2014 it is claimed, for GM foods this, “sometimes resulted in animated debate regarding the suitability of the experimental designs, the choice of the statistical methods or the public accessibility of data,” and that this debate, “has frequently been distorted by the media and often used politically and inappropriately in anti-GE crops campaigns”. The results previously presented in our review, however, have demonstrated that all medium and long-term studies using the most tested and most grown GM crop, GTS 40-3-2, report adverse effects or biomarkers indicative of adverse effects.

Criteria:

We applied the same criteria used to review Sanchez 2015 and 2017 to the studies listed in Nicolia 2014 with the timeframe of 2002-2012, the same timeframe used by Nicolia 2014. Studies included were in vivo, using rodents, pigs, dogs, non-human primates and humans, which are more comparable to humans than birds, fish or cattle. Only studies where animals were fed a single GM feed of non-stacked glyphosate tolerant soy GTS 40-3-2, the most analyzed according to Sanchez 2017, as whole feed or processed in a way that humans would consume it were included.

Results from analyzing Nicolia 2014

Only 1 relevant animal health study specifically mentioning, or providing a reference that specifically mentioned, the use of GTS 40-3-2 is used in Nicolia 2014 in which the authors do not report adverse effects (Zhu 2004). However, 9 studies specifically mentioning, or providing a reference that specifically mentioned, the use of GTS 40-3-2 are used by Nicolia 2014 in which the authors report adverse effects or biomarkers indicative of adverse effects (Battistelli 2010, Cisterna 2008, Magaña-Gómez 2008, Malatesta 2002a, Malatesta 2002b, Malatesta 2003, Malatesta 2005, Malatesta 2008a, Vecchio 2004). This equals 90% of studies suggesting adverse effects were observed.

When we examine the medium and long-term studies, of 6 months feeding duration or longer, 100% of studies suggest adverse effects or biomarkers indicative of adverse effects from the GM soy 40-3-2 diet (Battistelli 2010, Malatesta 2002a, Malatesta 2002b, Malatesta 2003, Malatesta 2008a, Vecchio 2004).

In order to ensure that these results were not skewed by omitting studies which did not mention the event we also included studies which: 1. mention the soybean having the gene cp4 epsps, 2. Mention soy being “Roundup tolerant” or “glyphosate tolerant” or, 3. mentioning that GM soybeans are “Roundup tolerant” or “glyphosate tolerant”.  This resulted in 4 studies not reporting adverse effects (Brake 2004, Zhu 2004, Sakamoto 2008, Daleprane 2010) and 9 studies stating adverse effects or biomarkers indicative of adverse effects were observed (Battistelli 2010, Cisterna 2008, Magaña-Gómez 2008, Malatesta 2002a, Malatesta 2002b, Malatesta 2003, Malatesta 2005, Malatesta 2008a, Vecchio 2004) or about 69.2% of studies reporting adverse effects were observed.

Results from analyzing Nicolia 2014 and references missing from review:

However, none of this takes into consideration the numerous studies which Nicolia 2014 missed that appear on the Coalition for a GMO Free India and GMO Free USA internet posts. When this is taken into consideration there is 1 study specifically mentioning the use of GTS 40-3-2 not reporting adverse effects (Zhu 2004). However, 18 studies specifically mentioning the use of GTS 40-3-2 have authors who report adverse effects or biomarkers indicative of adverse effects were observed (Battistelli 2008, Battistelli 2010, Cisterna 2008, Magaña-Gómez 2008, Malatesta 2002a, Malatesta 2002b, Malatesta 2003, Malatesta 2005, Malatesta 2008a, Vecchio 2004, Magaña-Gómez 2008, Ermakova 2008, Ermakova 2009, Gorbach 2012, Gubin-Vakulik 2012, Maligin 2008, Nazarova 2010, Samsonyk 2012). This is about 94.7% of studies suggesting adverse effects.

For the medium and long-term studies, of 6 months feeding duration or longer, 100% of the GTS 40-3-2 studies indicate adverse effects or biomarkers indicative of adverse effects from the GM soy GTS 40-3-2 diet (Battistelli 2010, Malatesta 2002a, Malatesta 2002b, Malatesta 2003, Malatesta 2008a, Vecchio 2004, Gorbach 2012, Gubin-Vakulik 2012).

In order to ensure that these results were not skewed by omitting studies which did not mention the event we also included studies which: 1. mention the soybean having the gene cp4 epsps, 2. Mention the soy used being “Roundup tolerant” or “glyphosate tolerant” or, 3. mention that GM soybeans are “Roundup tolerant” or “glyphosate tolerant”.  This resulted in 4 studies not reporting adverse effects (Brake 2004, Zhu 2004, Sakamoto 2008, Daleprane 2010) and 19 stating adverse effects or biomarkers indicative of adverse effects were observed (Battistelli 2008, Battistelli 2010, Cisterna 2008, Magaña-Gómez 2008, Malatesta 2002a, Malatesta 2002b, Malatesta 2003, Malatesta 2005, Malatesta 2008a, Vecchio 2004, Brasil 2009, Ermakova 2008, Ermakova 2009, Gorbach 2012, Gubin-Vakulik 2012, Maligin 2008, Nazarova 2010, Samsonyk 2012, Zhou 2012a). This indicates about 82.6% report adverse effects.

Discussion

The narrative reviews Nicolia 2014 and Sanchez 2017 suffer from numerous flaws making their conclusions unreliable. We, therefore, conclude that neither Sanchez 2015/2017 or Nicolia 2014 support a claim that only 5% of studies on GM foods observe adverse effects due to a wide variety of errors and omissions. Both Nicolia 2014 and Sanchez 2015 review a large number of GM events which generally have a small number of studies attributed to them. For example, Sanchez 2017 points out that in Sanchez 2015 they reviewed 204 articles that assess animal health for 94 different events. Of those 204 articles, 28 used GTS 40-3-2 and 25 used MON810. This leaves 151 articles that assess 92 different events, or an average of 1.6 articles per event. Results based on a single study are often inaccurate and so this invalidates the claim made by Sanchez 2017 (Ioannidis 2005). Also, as previously mentioned, many of the events only had studies listed that were done by or funded by the companies or researchers that develop GM crops/foods and therefore have a conflict of interest. Studies with a COI most often have outcomes favorable to the interests of the GM seed companies (Guillemaud 2016). Therefore, adverse effects are unlikely to be reported for events where only studies with a COI exist.

On the other hand, there was on average about 17.1 times more studies found for GTS 40-3-2 than for most other events. In this case, Sanchez 2017 should have recognized that events with only 1 or 2 animal health studies did not have robust evidence to conclude safety (Ioannidis 2005), especially when comparing that to the evidence for GTS 40-3-2. Yet, in the reviews by both Nicolia 2014 and Sanchez 2015/2017 they failed to look at the robust evidence for GTS 40-3-2 and instead relied heavily on the 1 or 2 studies done for a large number of events. In fact, many of the events used in these studies are not even on the market, or these studies used animals that are not comparable to humans. This small number of studies for most events indicates how poorly most GM foods have been tested. This is further illustrated in another systematic review where published rat feeding studies examining the digestive tract were only found for 9 of 47 (about 19%) GM foods approved for human and/or animal consumption (Zdziarski 2014). As can be seen from our review, the overwhelming weight of the peer reviewed scientific evidence indicates that GTS 40-3-2 is not likely to be as safe to consume as its conventional counterparts. Our review also indicates the other GM events reviewed have been inadequately tested and any claims that they are as safe as their conventional counterparts must be rejected as they are not supported by sufficient evidence.

Conclusion

Based on the results of this systematic review the claim that all GM foods currently on the market are as safe as their conventional counterparts is not supported by the scientific evidence. Instead, a clear consensus in the scientific literature using the popular GM soy GTS 40-3-2, considered to be the most tested GM food, has emerged. In about 86.2% of all relevant animal feeding studies reviewed, and 100% of the medium and long-term studies, using GTS 40-3-2, adverse effects or biomarkers indicative of adverse effects were reported. This is consistent with the consensus among health experts that GM foods currently on the market cannot presently be considered as safe as their conventional counterparts. This is either due to lack of evidence of safety, or because of evidence that at least some GM foods currently on the market may be unsafe compared to their conventional counterparts. Our systematic reviews find 91.5% of health groups (GMO Free Florida 2022) with statements on GMO safety and no known conflicts of interest, and health professionals in at least 92.9% of surveys (GMO Free Florida 2022a) agree about GM food safety concerns. The majority of health professionals and health students surveyed either believe GM foods have health risks, or are unsure about the safety of GM foods which coincides with the scientific evidence reviewed in this systematic review.

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