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GM Soy

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 literature reviews conducted by Nicolia et al. and Sanchez et al. to claim all GM foods currently on the market are as safe as their conventional counterparts.

Purpose:

To examine animal feeding studies using animals comparable to humans fed single event 40-3-2 glyphosate tolerant soy foods, and health parameters, which were reviewed by Nicolia et al. and Sanchez et al.  Since the claim is that all GM foods currently on the market are as safe as their conventional counterparts, if even 1 GM food on the market is determined to be less safe then this claim will have been demonstrated to be false. We chose GM soy with event 40-3-2 as it is the most grown, has the most animal feeding studies according to Sanchez et al. and is one of the most approved GMOs internationally.

Data Sources and Selection:

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

Data Extraction:

Relevant studies were identified using GTS 40-3-2.

Results:

Sanchez et al.

75% of relevant studies reviewed by Sanchez et al. suggest adverse effects or biomarkers indicative of adverse effects from the GM soy 40-3-2 diet.

100% of the medium and long-term studies, of 6 months feeding duration or longer, reviewed by Sanchez et al. suggest adverse effects or biomarkers indicative of adverse effects from the GM soy 40-3-2 diet.

88.5% of the relevant studies that should have been used by Sanchez et al. suggest adverse effects or biomarkers indicative of adverse effects from the GM soy 40-3-2 diet.

Nicolia et al.

88.9% of relevant studies reviewed by Nicolia et al. suggest adverse effects or biomarkers indicative of adverse effects from the GM soy 40-3-2 diet.

100% of the medium and long-term studies, of 6 months feeding duration or longer, reviewed by Nicolia et al. suggest adverse effects or biomarkers indicative of adverse effects from the GM soy 40-3-2 diet.

94.4% of the relevant studies that should have been used by Nicolia et al. suggest adverse effects or biomarkers indicative of adverse effects from the GM soy 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 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. Our systematic review of the scientific evidence indicates in most of the relevant animal feeding studies adverse effects or biomarkers indicative of adverse effects were observed.

Introduction:

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 AAAS Board of Director’s statement  mentions animal feeding studies as evidence for the safety of GM foods.(AAAS Board)  Narrative reviews of animal feeding studies are often cited to claim there is a consensus that GM foods currently on the market are as safe as their conventional counterparts.  Reviews done by Nicolia et al. and Sanchez et al. are some of the most cited reviews used to claim this consensus.(Blair 2020)

GTS 40-3-2 glyphosate tolerant soy is the most grown GM crop internationally(Aldemita 2015), is the most analyzed, having the greatest number of animal health studies(Sanchez 2015), and is approved for consumption by the second most number of countries.(ISAAA 2017) 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 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 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 feeds. Therefore, we reviewed peer reviewed studies using animals comparable to humans, health parameters and single event 40-3-2 glyphosate tolerant soy foods 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 tell a specific narrative which reflects the author’s opinion.  A narrative review does not need to be able to be replicated and 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 they 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 et al. and Sanchez et al., 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 for the opinions of health groups and surveys of health practitioners(See Reports 1 and 2) appear to conflict with a recent narrative review(Sanchez 2017).  This review by Sanchez et al. concluded that only 5% of the studies using GM foods observed adverse effects.  Sanchez et al. also concluded that a greater number of studies reporting adverse effects had a conflict of interest compared to those that reported no 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 GTS 40-3-2 soy 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 impossible to verify or replicate their claims.  References cited on the internet could include numerous posts on Facebook, Twitter, and other social media platforms as well as websites.  Since Sanchez et al. does not provide any details as to what they actually reviewed their claims cannot be verified and therefore their conclusion is unreliable.

Supplementary Table 5. 40-3-2 and Glyphosate tolerant Soy 1993-2014

Glyphosate Tolerant Soy 40-3-2 Systematic Review:

We, therefore, took a fresh look at the data purported to be used according to 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 rodents and pigs. 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 and appear to represent the majority of the studies. According to Sanchez 2017, GM soy event 40-3-2 has been the most analyzed.  We, therefore, reviewed animal health studies that were published during the timeframe used by Sanchez 2015 and found in the Sanchez 2015 and Sanchez 2017 reviews. We also used studies cited on 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 Facebook posts from GMO Free USA.  All of these were published before Sanchez et al. 2017 and therefore would have been accessible to the authors.

Results:

Only 3 animal health studies specifically mentioning, or providing a reference that specifically mentioned, the use of 40-3-2 are used by Sanchez 2015 which the authors claim have no adverse effects (See Supplementary Table 5 Zhu 2004, Reichert 2012, Bednarek 2013). However, 9 studies specifically mentioning, or providing a reference that specifically mentioned, the use of 40-3-2 are used by Sanchez 2017 which the authors claim adverse effects or biomarkers indicative of adverse effects (See Supplementary Table 5 Battistelli 2008, Battistelli 2010, Cisterna 2008, Malatesta 2002a, Malatesta 2002b, Malatesta 2003, Malatesta 2005, Malatesta 2008a, Vecchio 2004). In other words, most (75%) studies suggest adverse effects or biomarkers indicative of adverse effects from the GM soy 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.(See Report 1) 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).

According to Sanchez et al. 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 being “Roundup tolerant” or “glyphosate tolerant”, or 3. mentioning that GM soybeans are “Roundup tolerant” or “glyphosate tolerant”.  Although soybeans having the gene cp4 epsps could indicate it is 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 suggesting no adverse effects were observed to 9(See Supplementary Table 5 Zhu 2004, Reichert 2012, Bednarek 2013, Teshima 2000, Sbruzzi 2013, Brake 2004, Sakamoto 2007, Sakamoto 2008, Daleprane 2010)and 13 stating adverse effects or biomarkers indicative of adverse effects were observed or that non-GM soy had a greater health benefit than GM soy(See Supplementary Table 5 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 (about 59.1%) studies show 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 9 studies where the authors concluded no adverse effects there are examples where other researchers looked at the same data and came to different conclusions(Seralini 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 40-3-2 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, claiming no-adverse effects were not originally in English(Sakamoto 2007, Sakamoto 2008).  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 studies are included only 3 studies specifically mentioning, or providing a reference that specifically mentioned, the use of 40-3-2 are used by Sanchez 2015 which the authors claim have no adverse effects (See Supplementary Table 5 Zhu 2004, Reichert 2012, Bednarek 2013).   However, 23 studies specifically mentioning, or providing a reference that specifically mentioned, the use of 40-3-2 are claimed to be used by Sanchez 2017, which the authors of the studies report adverse effects or biomarkers indicative of adverse effects (See Supplementary Table 5 Battistelli 2008, Battistelli 2010, Cisterna 2008, Malatesta 2002a, Malatesta 2002b, Malatesta 2003, Malatesta 2005, Malatesta 2008a, Vecchio 2004, 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 (about 88.5%) studies suggest adverse effects or biomarkers indicative of adverse effects from the GM soy 40-3-2 diet.

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, 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 suggesting no adverse effects were observed is 9(See Supplementary Table 5 Zhu 2004, Reichert 2012, Bednarek 2013, Teshima 2000, Sbruzzi 2013, Brake 2004, Sakamoto 2007, Sakamoto 2008, Daleprane 2010).  However, 31 state adverse effects or biomarkers indicative of adverse effects were observed or that non-GM soy had a greater health benefit than GM soy (See Supplementary Table 5  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, 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 2013, Long 2014, Venâncio 2012, Zhou 2012b).  In other words, most (about 77.5%) studies suggest adverse effects or biomarkers indicative of adverse effects from the GMO diet.

When we examine the medium and long-term studies, of 6 months feeding duration or longer, about 80% 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, Gorbach 2012, Gubin-Vakulik 2012, Gubin Vakulik 2013, Zinoviev 2014, Brasil 2009, Kulik 2014, Sakamoto 2007, Sakamoto 2008, Daleprane 2010).

Discussion:

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.  According to Sanchez 2017, “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 an 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.”(EFSA 2011)  It should be noted that some scientists have stated that OECD Test Guidelines are not sensitive enough to detect some toxicity.(Buonsante 2014). However, even when examining the 3 studies finding no adverse effects for GM soy 40-3-2 it can be seen they also violate at least one of these standards.  Reichert 2012 and Bednarek 2013 both 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)  Reichert 2012 and Bednarek 2013, however, use only one concentration of 10% soy.  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, several of these results are missing from Reichert 2012 and Bednarek 2013.  Zhu 2004 also fails to adequately report their results.(Zdziarski 2014).

Inconsistent standard and flaws in assessment of Animal Health Studies:

Sanchez et al. claim that, “While the 35 studies showing adverse effects only tested 11 events, the 204 other articles that assess animal health evaluate 94 different events.”  However, there are problems with this claim.  First, there are not 204 “other” articles.  Sanchez 2015 lists 204 total studies as “Animal Health” of these 18 are listed (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) in Supplementary Table 1 of Sanchez 2015 which are also listed in Sanchez 2017 as part of the 35.

Sanchez 2015 also included studies in the “Animal Health” section that appear to have nothing to do with GMOs.(Kim 2010).  Studies which mention GMOs, but do not actually test GMOs and instead tested the glyphosate based herbicide Roundup were also included.(Malatesta 2008b)  If studies testing glyphosate based herbicides were intentionally included in Sanchez 2015 then hundreds of studies found on the GMO Free USA website are missing from Sanchez 2017.(GMO Free USA Glyphosate Studies)   Sanchez 2015 also seems to have mislabeled studies as being “Animal Health” when in fact these studies did not examine health effects.(Aris 2011).  As well as studies that looked at nutrient absorption, not health effects, which should have been classified as “Animal Nutrition”.(Shireen 2002, Tso 2002).

Sanchez et al. also fails to mention that one of the reasons for the difference in number of events listed as “Animal Health”.  That is, because many of the studies using these other events have financial or professional conflicts of interest being either conducted by employees of, or funded by the company that made the GM crop.  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, Delaney 2007, Chukwudebe 2012, Delaney 2008, Hammond 2008, Lemke 2010, MacKenzie 2007, Appenzeller 2009a, Malley 2007, He 2008, Juberg 2009, Appenzeller 2009b, Stagg 2012, Delaney 2013, Hardisty 2013, Delaney 2014, Wainwright 2003, Liu 2004, He 2009).

Conflicts of interest (COI) are often associated with outcomes favorable to the interests of GM crop companies.(Guillemaud 2016) Therefore adverse effects would not be expected to be observed for events where only studies with a COI exist.

Many studies listed by Sanchez 2015 as “Animal Health” were also in a language other than English(Sakamoto 2007, Sakamoto 2008, Tutel’ian 2010, Tyshko 2010), or used a purified protein (Vazquez-Padron 1999, Vázquez 1999, Vazquez-Padron 2000, Moreno-Fierros 2000). In Sanchez 2017  studies suggesting adverse effects that were not in English or used a purified protein were excluded.  Yet, in Sanchez 2015 such studies were included.  This inconsistent standard distorts the data in favor of the biotech companies these authors are affiliated with.

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.”

It is claimed by Sanchez 2017 that studies supported by the Committee of Independent Research and Information on Genetic Engineering (CRIIGEN) have a conflict of interest. This is based on the claim that CRIIGEN is financed by the Charles Leopold Mayer Foundation for the Progress of Humankind (FPH).  According to Sanchez et al., “This foundation has publicly supported anti-GMOs  initiatives like Inf’OGM, Foundation, Sciences Citoyennes; the European Network of Scientists for Social and Environmental Responsibility (ENSSER), Combat Monsanto and Stop OGM, among others”.  However, no evidence is provided to support a claim that these groups are, “anti-GMOs initiatives.”  Such a claim of conflict of interest sets an absurd standard by which any group which has ever made a statement in favor of GMOs is therefore a “pro-GMO initiative” and any group which shares funders with such a group automatically has a conflict of interest as well.

In comparison, 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).  Both the ASDA and the ASAS have received funding directly from Monsanto.(Animal and Dairy News 2002) Between the years of at least 2006-2014 Gary Hartnell from Monsanto Company has been involved with the Scientific Advisory Committee on Biotechnology of the Federation of Animal Science Societies.(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 Federation of Animal Science Societies 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 by Sanchez 2015 and 13 studies published in these journals were considered to be without a conflict of interest(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.  Yet, Sanchez 2017 strangely considers it a COI to receive funding from a group that may or may not fund other groups that may or may not be anti-GMO and that the group who received the funding may or may not even know about.

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 by Sanchez 2015 and 7 studies published in these journals were considered to be without a conflict of interest(Molvig 1997, Schubbert 1997, Catchpole 2005, Kristensen 2005, Regina 2006, Batista 2008, Kogel 2010)

Sanchez 2017 also argues that, “J.L.Domingo, author of another review here assessed (Domingo and Bordonaba, 2011), was an editor of Food and Chemical Toxicology when the Seralini study was accepted.”  In this case Sanchez et al. argues that because Domingo published a literature review which questioned the lack of safety testing for GMOs that, somehow, implies a COI.  Even though Sanchez 2017 provides no evidence for J.L. Domingo having a conflict of interest.  By this logic everyone who has ever conducted a study or review and concluded in favor of GMOs must also have a conflict of interest for no reason other than their conclusion.

In comparison, Wallace Hayes was the editor of the journal Food Chemical Toxicology from 2012-2014.  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)  However, Sanchez 2015 lists 8 studies published in Food Chemical Toxicology between 2012 and 2014 which were considered to be without a conflict of interest(Wang 2014, Zhang 2014, Zhu 2013, Wang 2013, Mishra 2012, Liu 2012, Qi 2012, Zhou 2012a).

Conclusion regarding Sanchez Reviews :

Our review does have some limitations.  Although we included all of the referencences listed as “Animal Health” from Sanchez 2015, it is possible that Sanchez 2015 did not do a thorough review of the studies.  If Sanchez et al. missed several studies, this could explain why so few studies mentioning 40-3-2 did not observe adverse effects.  This is supported by the fact that we identified many animal health studies mentioning 40-3-2 observing adverse effects that were not listed by 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 Sanchez 2015 mislabeled studies in other categories that should have been labeled as “Animal Health”.  As we identified in this review, Sanchez 2015 mislabeled some studies  as “Animal Health” that either had nothing to do with GMOs or should have been labeled as “Animal Nutrition”.  Therefore, it is possible that some actual “Animal Health” studies were missed.

Another limitation is that we only reviewed studies from 1993 to 2014, so it is also possible that recent 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 GMOResearch database.(http://gmoresearch.org) Another limitation is that we only reviewed peer reviewed studies.  Some evidence suggests that including unpublished and/or gray literature in systematic reviews may alter the results.(Schmucker 2017)

Further reviews may be necessary, but the results of our review, however, indicate that when a consistent standard is applied 88.5% of studies indicate adverse effects or biomarkers indicative of adverse effects from the GM soy 40-3-2 diet.  Of the medium and long-term studies using the GM soy 40-3-2 diet, 100% indicate adverse effects or biomarkers indicative of 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 et al. conclude, “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.”  Nicolia et al. claim, 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, 40-3-2, observed 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.  Studies included were in vivo, using rodents and pigs, 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 40-3-2, the most analyzed according to Sanchez et al., as whole feed or processed in a way humans would consume it were included.

Results from analyzing Nicolia et al.

Only 1 relevant animal health study specifically mentioning, or providing a reference that specifically mentioned, the use of 40-3-2 is used by Nicolia et al. which the authors claim has no adverse effects(See Supplementary Table 5 Zhu 2004).  However, 8 studies specifically mentioning, or providing a reference that specifically mentioned, the use of 40-3-2 are used by Nicolia 2014 which the authors claim adverse effects or biomarkers indicative of adverse effects(See Supplementary Table 5 Battistelli 2010, Cisterna 2008, Malatesta 2002a, Malatesta 2002b, Malatesta 2003, Malatesta 2005, Malatesta 2008a, Vecchio 2004).  This equals about 88.9% 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 non-adverse(See Supplementary Table 5 Brake 2004, Zhu 2004, Sakamoto 2008, Daleprane 2010) and 9 stating adverse effects or biomarkers indicative of adverse effects were observed(See Supplementary Table 5 Battistelli 2010, Cisterna 2008, Malatesta 2002a, Malatesta 2002b, Malatesta 2003, Malatesta 2005, Malatesta 2008a, Vecchio 2004, Magaña-Gómez 2008) or about 69.2% stating adverse effects.

Results from analyzing Nicolia et al. and references missing from review:

However, none of this takes into consideration the numerous studies which Nicolia et al. 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 40-3-2 claiming no adverse effects(See Supplementary Table 5 Zhu 2004). However, 17 studies specifically mentioning the use of 40-3-2 have authors who claim adverse effects or biomarkers indicative of adverse effects were observed(See Supplementary Table 5 Battistelli 2008, Battistelli 2010, Cisterna 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 94.4% 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 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 being “Roundup tolerant” or “glyphosate tolerant” or, 3. mention that GM soybeans are “Roundup tolerant” or “glyphosate tolerant”.  This resulted in 4 non-adverse(See Supplementary Table 5 Brake 2004, Zhu 2004, Sakamoto 2008, Daleprane 2010) and 19 stating adverse effects or biomarkers indicative of adverse effects were observed(See Supplementary Table 5 Battistelli 2008, Battistelli 2010, Cisterna 2008, Malatesta 2002a, Malatesta 2002b, Malatesta 2003, Malatesta 2005, Malatesta 2008a, Vecchio 2004, Magaña-Gómez 2008, Brasil 2009, Ermakova 2008, Ermakova 2009, Gorbach 2012, Gubin-Vakulik 2012, Maligin 2008, Nazarova 2010, Samsonyk 2012, Zhou 2012). This indicates about 82.6% state adverse effects.  Therefore, we conclude that neither Sanchez 2017, 2015 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.

Discussion

The narrative reviews done by Nicolia et al. and Sanchez et al. suffer from numerous flaws making their conclusions entirely unreliable.  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 1.64 articles per event, so less than 2 studies per event.  As was previously mentioned, Sanchez 2015 misclassified some studies as animal health which were not.  Sanchez 2015 aso included studies using birds, fish and other animals that have little relevance to human health, so this number is actually even lower.  Also, as previously mentioned, many of the events only had studies listed that were done by or funded by the companies or researchers that created the event and therefore have a conflict of interest.

In comparison, there was on average 17.1 times more studies done for GTS 40-3-2 than done for most other events.  In this case, Sanchez et al. should have recognized that events with only 1 or 2 animal health studies did not have robust evidence to conclude safety, 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 the studies are not even on the market, or 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 review where published rat feeding studies 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 evidence indicates that GTS 40-3-2 is not likely to be as safe to consume as its conventional counterpart.

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 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 88.5% 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 observed.  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 75.5% of health groups(Report 1) with statements on GMO safety and no known conflicts of interest, and health professionals in at least 92% of surveys(Report 2) 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.

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