Peer Reviewed Publications on the Safety of GM Foods
Results of a search of the PubMed database for publications on feeding studies for GM crops.
By Dr. Christopher Preston,
Senior Lecturer in Weed Management,
University of Adelaide;
There has been considerable recent comment on the lack of peer-reviewed scientific studies on the effect of GM food and feed on livestock, other animals and humans. A report by Pryme and Lembcke (2003) described 10 such studies. This report and the small number of studies is often quoted by groups opposed to the use of GM crops as justification for banning their use in the food chain. To determine the current state of the literature, I conducted a search of the PubMed database for publications on this topic.
The search strategy I used included the search terms (genetically and modified and food) coupled with crop species with known genetic modifications, including maize, soybean, canola, cotton, potatoes, tomatoes and peas. Searches also included the word transgenic instead of genetically and modified. A large number of hits were obtained by this search strategy, with most having little or nothing to do with GM food tests.
I collected papers that had:
1. An abstract in PubMed;
2. Were a research publication, not a review or commentary
3. Reported a feeding study involving food or food products from GM crops (not purified proteins from other sources such as bacteria or other GM products) in the abstract;
4. Test subjects were mammals, birds or fish; and 5. Reported at least one measure of comparison with non-GM food.
In all, 42 publications abstracted in PubMed passed these tests. The search strategy extracted most of the studies covered by Pryme and Lembcke (2003). The ones absent were not apparently abstracted in PubMed (e.g. Pusztai 1998) or were reviews (Pusztai 2002). My search uncovered several publications between 1999 and 2001 that were not captured by Pryme and Lembcke (2003).
Of the 42 publications, most examined the effects of feeding GM crop products to livestock including cattle, pigs and poultry. A smaller number examined effects on rats and mice with two on fish. As reported in the abstracts of the publications, 36 studies found no significant effect of GM crop products on the parameters measured or concluded GM and non-GM products were equivalent. Four studies reported a positive effect of the GM feed (however, two of these were GM plants engineered for improved food quality) and two reported negative effects. The studies reporting negative effects were published in 1998 and 1999 (references 3 and 4 in the list). Since 2000, 35 publications have reported no important differences or positive effects of feeding GM crops.
Almost two thirds (27) the publications extracted from the database have been published since 2002. Many of these examined the potential effects of GM crop on livestock performance and were clearly aimed at determining whether the reports of dangers of GM crops to livestock in the press were true.
There are at least 42 publications extractable from the PubMed database that describe research reports of feeding studies of GM feed or food products derived from GM crops. The overwhelming majority of publications report that GM feed and food produced no significant differences in the test animals. The two studies reporting negative results were published in 1998 and 1999 and no confirmation of these effects have since been published. Many studies have been published since 2002 and all have reported no negative impact of feeding GM feed to the test species.
Pryme, IF, Lembcke R. 2003. In vivo studies on possible health consequences of genetically modified food and feed - with particular regard to ingredients consisting of genetically modified plant material.
Nutr Health 17:1-8.
Pusztai A. 1998. SOAFED flexible fund project RO818 (cited in Pryme and Lembcke 2003).
Psztai A. 2002. Can science give us the tools for recognizing possible health risks of GM food'? Nutr. Health 16:73-84.
List of publications collected from PubMed by year.
1. Hammond BG, Vicini JL, Hartnell GF, Naylor MW, Knight CD, Robinson EH, Fuchs RL, Padgette SR. 1996 The feeding value of soybeans fed to rats, chickens, catfish and dairy cattle is not altered by genetic incorporation of glyphosate tolerance. J Nutr. 126:717-27.
2. Brake J, Vlachos D. 1998 Evaluation of transgenic event 176 "Bt" corn in broiler chickens. Poult Sci. 77:648-53.
3. Fares NH, El-Sayed AK. 1998 Fine structural changes in the ileum of mice fed on delta-endotoxin-treated potatoes and transgenic potatoes. Nat Toxins. 6:219-33.
4. Ewen SW, Pusztai A. 1999 Effect of diets containing genetically modified potatoes expressing Galanthus nivalis lectin on rat small intestine. Lancet. 354:1353-4.
5. Hashimoto W, Momma K, Yoon HJ, Ozawa S, Ohkawa Y, Ishige T, Kito M, Utsumi S, Murata K. 1999 Safety assessment of transgenic potatoes with soybean glycinin by feeding studies in rats. Biosci Biotechnol Biochem. 63:1942-6.
6. Pusztai A, Bardocz GG, Alonso R, Chrispeels MJ, Schroeder HE, Tabe LM, Higgins TJ. 1999 Expression of the insecticidal bean alpha-amylase inhibitor transgene has minimal detrimental effect on the nutritional value of peas fed to rats at 30% of the diet. J Nutr. 129:1597-603.
7. Tutel'ian VA, Kravchenko LV, Lashneva NV, Avren'eva LI, Guseva GV, Sorokina EIu, Chernysheva ON 1999 [Medical and biological evaluation of safety of protein concentrate from genetically-modified soybeans. Biochemical studies] [Article in Russian]. Vopr Pitan. 68:9-12.
8. Momma K, Hashimoto W, Yoon HJ, Ozawa S, Fukuda Y, Kawai S, Takaiwa F, Utsumi S, Murata K. 2000 Safety assessment of rice genetically modified with soybean glycinin by feeding studies on rats. Biosci Biotechnol Biochem. 64:1881-6.
9. Palombo JD, DeMichele SJ, Liu JW, Bistrian BR, Huang YS. 2000 Comparison of growth and fatty acid metabolism in rats fed diets containing equal levels of gamma-linolenic acid from high gamma-linolenic acid canola oil or borage oil. Lipids. 35:975-81
10. Sidhu RS, Hammond BG, Fuchs RL, Mutz JN, Holden LR, George B, Olson T. 2000 Glyphosate-tolerant corn: the composition and feeding value of grain from glyphosate-tolerant corn is equivalent to that of conventional corn (Zea mays L.). J Agric Food Chem. 48:2305-12.
11. Spencer JD, Allee GL, Sauber TE. 2000 Growing-finishing performance and carcass characteristics of pigs fed normal and genetically modified low-phytate corn. J Anim Sci. 78:1529-36.
12. Aulrich K, Bohme H, Daenicke R, Halle I, Flachowsky G. 2001 Genetically modified feeds in animal nutrition. 1st communication: Bacillus thuringiensis (Bt) corn in poultry, pig and ruminant nutrition. Arch Tierernahr. 54:183-95.
13. Barriere Y, Verite R, Brunschwig P, Surault F, Emile JC. 2001 Feeding value of corn silage estimated with sheep and dairy cows is not altered by genetic incorporation of Bt1376 resistance to Ostrinia nubilalis. J Dairy Sci. 84:1863-71.
14. Bohme H, Aulrich K, Daenicke R, Flachowsky G. 2001 Genetically modified feeds in animal nutrition. 2nd communication: glufosinate tolerant sugar beets (roots and silage) and maize grains for ruminants and pigs. Arch Tierernahr. 54:197-207.
15. Tutel'ian VA, Kravchenko LV, Sorokina EIu, Korolev AA, Avren'eva LI, Guseva GV, Chernysheva ON, Tyshko NV. 2001 [Medical and biological assessment of the safety of genetically modified corn lines MON 810 and GA 21: a toxicological-biochemical study] [Article in Russian]. Vopr Pitan. 70:28-31.
16. Chrenkova M, Sommer A, Ceresnakova Z, Nitrayova S, Prostredna M. 2002 Nutritional evaluation of genetically modified maize corn performed on rats. Arch Tierernahr. 56:229-35.
17. Cromwell GL, Lindemann MD, Randolph JH, Parker GR, Coffey RD, Laurent KM, Armstrong CL, Mikel WB, Stanisiewski EP, Hartnell GF. 2002 Soybean meal from roundup ready or conventional soybeans in diets for growing-finishing swine. J Anim Sci. 80:708-15.
18. Folmer JD, Grant RJ, Milton CT, Beck J. 2002 Utilization of Bt corn residues by grazing beef steers and Bt corn silage and grain by growing beef cattle and lactating dairy cows. J Anim Sci. 80:1352-61.
19. Humphrey BD, Huang N, Klasing KC. 2002 Rice expressing lactoferrin and lysozyme has antibiotic-like properties when fed to chicks. J Nutr. 132:1214-8.
20. Reuter T, Aulrich K, Berk A, Flachowsky G. 2002 Investigations on genetically modified maize (Bt-maize) in pig nutrition: chemical composition and nutritional evaluation. Arch Tierernahr. 56:23-31.
21. Reuter T, Aulrich K, Berk A. 2002 Investigations on genetically modified maize (Bt-maize) in pig nutrition: fattening performance and slaughtering results. Arch Tierernahr. 56:319-26.
22. Teshima R, Watanabe T, Okunuki H, Isuzugawa K, Akiyama H, Onodera H, Imai T, Toyoda M, Sawada J. 2002 Effect of subchronic feeding of genetically modified corn (CBH351) on immune system in BN rats and B10A mice. Shokuhin Eiseigaku Zasshi. 43:273-9.
23. Brake J, Faust MA, Stein J. 2003 Evaluation of transgenic event Bt11 hybrid corn in broiler chickens. Poult Sci. 82:551-9.
24. Brown PB, Wilson KA, Jonker Y, Nickson TE. 2003 Glyphosate tolerant canola meal is equivalent to the parental line in diets fed to rainbow trout. J Agric Food Chem. 51:4268-72.
25. Chen ZL, Gu H, Li Y, Su Y, Wu P, Jiang Z, Ming X, Tian J, Pan N, Qu LJ. 2003 Safety assessment for genetically modified sweet pepper and tomato. Toxicology. 188:297-307.
26. Donkin SS, Velez JC, Totten AK, Stanisiewski EP, Hartnell GF. 2003 Effects of feeding silage and grain from glyphosate-tolerant or insect-protected corn hybrids on feed intake, ruminal digestion, and milk production in dairy cattle. J Dairy Sci. 86:1780-8.
27. Erickson GE, Robbins ND, Simon JJ, Berger LL, Klopfenstein TJ, Stanisiewski EP, Hartnell GF. 2003 Effect of feeding glyphosate-tolerant (roundup-ready events GA21 or nk603) corn compared with reference hybrids on feedlot steer performance and carcass characteristics. J Anim Sci. 81:2600-8.
28. Grant RJ, Fanning KC, Kleinschmit D, Stanisiewski EP, Hartnell GF. 2003 Influence of glyphosate-tolerant (event nk603) and corn rootworm protected (event MON863) corn silage and grain on feed consumption and milk production in Holstein cattle. J Dairy Sci. 86:1707-15.
29. Ipharraguerre IR, Younker RS, Clark JH, Stanisiewski EP, Hartnell GF. 2003 Performance of lactating dairy cows fed corn as whole plant silage and grain produced from a glyphosate-tolerant hybrid (event NK603). J Dairy Sci. 86:1734-41.
30. Taylor ML, Hartnell GF, Riordan SG, Nemeth MA, Karunanandaa K, George B, Astwood JD. 2003 Comparison of broiler performance when fed diets containing grain from roundup ready (NK603), yieldgard x roundup ready (MON810 x NK603), non-transgenic control, or commercial corn. Poult Sci. 82:443-53.
31. Taylor ML, Hartnell GF, Riordan SG, Nemeth MA, Karunanandaa K, George B, Astwood JD. 2003 Comparison of broiler performance when fed diets containing grain from YieldGard (MON810), YieldGard x Roundup Ready (GA21), nontransgenic control, or commercial corn. Poult Sci. 82:823-30.
32. Taylor ML, Hyun Y, Hartnell GF, Riordan SG, Nemeth MA, Karunanandaa K, George B, Astwood JD. 2003 Comparison of broiler performance when fed diets containing grain from YieldGard Rootworm (MON863), YieldGard Plus (MON810 x MON863), nontransgenic control, or commercial reference corn hybrids. Poult Sci. 82:1948-56.
33. Tony MA, Butschke A, Broll H, Grohmann L, Zagon J, Halle I, Danicke S, Schauzu M, Hafez HM, Flachowsky G. 2003 Safety assessment of Bt 176 maize in broiler nutrition: degradation of maize-DNA and its metabolic fate. Arch Tierernahr. 57:235-52.
34. Brake DG, Evenson DP 2004 A generational study of glyphosate-tolerant soybeans on mouse fetal, postnatal, pubertal and adult testicular development. Food Chem Toxicol. 42:29-36.
35. Brake DG, Thaler R, Evenson DP 2004 Evaluation of Bt (Bacillus thuringiensis) corn on mouse testicular development by dual parameter flow cytometry. J Agric Food Chem 52:2097-102.
36. Chen X, Zhuo Q, Piao J, Yang X. 2004 [Immunotoxicologic assessment of transgenetic rice][Article in Chinese]. Wei Sheng Yan Jiu. 33:77-80.
37. El Sanhoty R, El-Rahman AA, Bogl KW. 2004 Quality and safety evaluation of genetically modified potatoes spunta with Cry V gene: compositional analysis, determination of some toxins, antinutrients compounds and feeding study in rats. Nahrung. 48:13-8.
38. Hammond B, Dudek R, Lemen J, Nemeth M. 2004 Results of a 13 week safety assurance study with rats fed grain from glyphosate tolerant corn. Food Chem Toxicol. 42:1003-14.
39. Hyun Y, Bressner GE, Ellis M, Lewis AJ, Fischer R, Stanisiewski EP, Hartnell GF. 2004 Performance of growing-finishing pigs fed diets containing Roundup Ready corn (event nk603), a nontransgenic genetically similar corn, or conventional corn lines. J Anim Sci. 82:571-80.
40. Taylor ML, Stanisiewski EP, Riordan SG, Nemeth MA, George B, Hartnell GF 2004 Comparison of broiler performance when fed diets containing roundup ready (event RT73), nontransgenic control, or commercial canola meal. Poult Sci 83:456-461
41. Zhuo Q, Chen X, Piao J, Gu L. 2004 [Study on food safety of genetically modified rice which expressed cowpea trypsin inhibitor by 90 day feeding test on rats] [Article in Chinese]. Wei Sheng Yan Jiu. 33:176-9. 42. Zhuo Q, Chen X, Piao J, Han C. 2004 [Study on the teratogenicity effects of genetically modified rich which expressed cowpea trypsin inhibitor on rats] [Article in Chinese]. Wei Sheng Yan Jiu. 33:74-7.http://www.agbioworld.org/biotech-info/articles/biotech-art/peer-reviewed-pubs.html