Subchronic feeding study of herbicide-tolerant soybean DP-356Ø43-5 in Sprague-Dawley rats

Food and Chemical Toxicology

Volumn 46, Issue 6, 2008, Pages 2201-2213

  Appenzeller, Laura M ^a   Munley, Susan M ^b   Hoban, Denise ^b   Sykes, Greg P ^b   Malley, Linda A ^b   Delaney, Bryan ^a  

^a PIONEER HI BRED INTERNATIONAL INC   (United States)

^b DUPONT COMPANY   (United States)

Author keywords

Biotechnology; Genetically modified; Glyphosate acetyltransferase; Rat; Soybean; Subchronic

Indexed keywords

GLYPHOSATE; HERBICIDE; SULFONYLUREA;

ADVERSE OUTCOME; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD ANALYSIS; BLOOD CLOTTING; BODY WEIGHT; COGNITION; CONTROLLED STUDY; DIETARY INTAKE; DNA MODIFICATION; FEMALE; FOOD INTAKE; GENE SEQUENCE; GRIP STRENGTH; HISTOPATHOLOGY; MALE; MORTALITY; NONHUMAN; ORGAN WEIGHT; RAT; SOYBEAN; TRANSGENIC PLANT; URINALYSIS; VARIETAS; WEIGHT GAIN;

ANIMALS; BEHAVIOR, ANIMAL; BLOOD CELL COUNT; BLOOD CHEMICAL ANALYSIS; BLOOD COAGULATION; BODY WEIGHT; DIET; EATING; EYE DISEASES; FEMALE; HERBICIDES; MALE; MOTOR ACTIVITY; ORGAN SIZE; PLANTS, GENETICALLY MODIFIED; PSYCHOMOTOR PERFORMANCE; RATS; RATS, SPRAGUE-DAWLEY; SOYBEANS; URINALYSIS;

GLYCINE MAX; RATTUS; RODENTIA;

EID: 42749094482     PISSN: 02786915     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.fct.2008.02.017     Document Type: Article

References (69)

1. Borzelleca J.F. A proposed model for safety assessment of macronutrient substitutes. Regul. Pharmacol. Toxicol. 23 (1996) S15-S18
2. Castle L.A., Siehl D.L., Gorton R., Patten P., Chen Y.H., Bertain S., Cho H.J., Duck N., Wong J., Liu D., and Lassner M. Discovery and directed evolution of a glyphosate tolerance gene. Science 304 (2004) 1151-1154
3. Challeff R.S., and Mauvais C.J. Acetolactate synthase is the site of action of two sulfonylurea herbicides in higher plants. Science 224 (1984) 1443-1445
4. Codex, 2007. Joint FAO/WHO food standards programme, Codex Alimentarius Commission. Report of the sixth session of the codex ad hoc intergovernmental task force on foods derived from biotechnology. Alinorm 07/30/34. Food and Agriculture Organisation, Rome, Italy. Available from: .
5. Codex, 2003a. Joint FAO/WHO food standards programme, Codex Alimentarius Commission. Report of the fourth session of the codex ad hoc intergovernmental task force on foods derived from biotechnology. Alinorm 03/34A. Food and Agriculture Organisation, Rome, Italy. Available from: .
6. Codex, 2003b. Guideline for the conduct of food safety assessments of foods derived from recombinant-DNA plants. CAC/GL 45-2003. Joint FAO/WHO food standards programme, Codex Alimentarius Commission. Food and Agriculture Organisation, Rome, Italy. Available from: .
7. Delaney B. Strategies to evaluate the safety of bioengineered foods. Int. J. Toxicol. 26 (2007) 389-399
8. Delaney B., Zhang J., Carlson G., Davis T., Schmidt J., Stagg B., Comstock B., Babb A., Finlay C., Cressman R., Ladics G., Cogburn A., Siehl D., Bardina L., Sampson H., and Han Y. A gene-shuffled glyphosate acetyltransferase protein from Bacillus licheniformis (GAT4601) shows no evidence of allergenicity or toxicity. Toxicol. Sci. 102 (2008) 425-432
9. Dempster A.P., Selwyn M.R., Patel C.M., and Roth A.J. Statistical and computational aspects of mixed model analysis. J. Royal Statist. Soc. Ser. C (Appl. Statist.) 33 2 (1984) 203-214
10. Dunn O.J. Multiple contrasts using rank sums. Technometrics 6 (1964) 241-252
11. EC, 1997. Commission recommendation of 29 July 1997 concerning the scientific aspects and the presentation of information necessary to support applications for the placing on the market of novel foods and novel food ingredients and the preparation of initial assessment reports under Regulation (EC) No. 258/97 of the European Parliament and of the Council (97/618/EC). Official J. Euro. Commun. L253, 1-36.
12. EC, 2001. Commission Directive 2001/59/EC Part B.26 of Annex 5D, methods for the determination of toxicity. Official J. Euro. Commun. L225, 150-156. Available from: .
13. EC, 2003a. Regulation (EC) 1829/2003 of the European parliament and of the council of 22 September 2003 on genetically modified food and feed. Official J. Euro. Commun. L268, 1-23. Available from: .
14. EC, 2003b. Guidance document for the risk assessment of genetically modified plants and derived food and feed. The joint working group on novel foods and GMOs, European commission document. European commission, Brussels, Belgium. Available from: .
15. EC, 2004. Genetically modified crops in the EU: food safety assessment, regulation, and public concerns - overarching report. ENTRANSFOOD. European communities, Luxembourg, Belgium, 99 pp. Available from: .
16. EFSA, 2006a. Risk assessment of genetically modified plants and derived food and feed. Guidance document of the scientific panel on genetically modified organisms of the European food safety authority (EFSA). EFSA J. 99, 1-100. Available from: .
17. EFSA, 2006b. Safety and nutritional assessment of GM plant derived foods/feed: the role of animal feeding trials. Draft report of the scientific panel on genetically modified organisms of the European food safety authority (EFSA). Available from: .
18. FAO, 1996. Biotechnology and food safety. Report of a joint FAO/WHO Consultation 30 September-4 October. FAO Food and Nutrition Paper 61. Food and Agriculture Organization of the United Nations, Rome, Italy.
19. FAO/WHO, 2000. Safety aspects of genetically modified foods of plant origin. Report of a joint FAO/WHO expert consultation on foods derived from biotechnology. FAO Food and Nutrition Paper 29. Food and Agriculture Organization of the United Nations, Rome, Italy.
20. Faust, M.A., Smith, B., Hinds, M., Dana, G., 2003. Dairy cattle performance, health, and milk composition when fed silage and grain from Bt (Cry1F) and near-isogenic control hybrids. Presentation, 2003 ADSA/ASAS Joint Meeting, Abstract #246. Available from: .
21. Fisher R.A. Statistical Methods for Research Workers. 13th ed. (1985), Haffner, New York, NY
22. Flachowsky G., Aulrich K., Böhme H., and Halle I. Studies on feeds from genetically modified plants (GMP) - contributions to nutritional and safety assessment. Anim. Feed Sci. Technol. 133 (2007) 2-30
23. Green J.M. Review of glyphosate and ALS-inhibiting herbicide crop resistance and resistant weed management. Weed Technol. 21 (2007) 547-558
24. Hammond B., Dudek R., Lemen J., and Nemeth M. Results of a 13 week safety assurance study with rats fed grain from glyphosate tolerant corn. Food Chem. Toxicol. 42 (2004) 1003-1014
25. Hammond B.G., Dudek R., Lemen J.K., and Nemeth M.A. Results of a 90-day safety assurance study with rats fed grain from corn borer-protected corn. Food Chem. Toxicol. 44 (2006) 1092-1099
26. Hammond B., Lemen J., Dudek R., Ward D., Jiang C., Nemeth M., and Burns J. Results of a 90 day safety assurance study with rats fed grain from corn rootworm-protected corn. Food Chem. Toxicol. 44 (2006) 147-160
27. Herman R.A., Storer N.P., Phillips A.M., Prochaska L.M., and Windels P. Compositional assessment of event DAS-59122-7 maize using substantial equivalence. Regul. Toxicol. Pharmacol. 47 (2007) 37-47
28. Herouet C., Esdaile D.J., Mallyon B.A., Debruyne E., Schulz A., Currier T., Hendrickx K., van der Klis R.-J., and Rouan D. Safety evaluation of the phosphoinothricin acetyltransferase proteins encoded by the pat and bar sequences that confer tolerance to glufosinate ammonium herbicide in transgenic plants. Regul. Toxicol. Pharmacol. 41 (2005) 134-149
29. Hocking R.A. The Analysis of Linear Models (1985), Brooks/Cole, Monterey, CA
30. Holm S. A simple sequentially rejective multiple test procedure. Scand. J. Statist. 6 (1979) 65-70
31. Huls, T.J., Erickson, G.E., Klopfenstein, T.J., Luebbe, M.K., Vander Pol, K.J., Rice, D.W., Smith, B., Hinds, M., Owens, F., Liebergesell, M., 2007. Effect of feeding DAS-59122-7 corn grain and non-transgenic corn grain to finishing feedlot steers. Presentation, 2007 ADSA/ASAS/PSA/AMPA Joint Meeting, Abstract #160. Available from: .
32. ILSI, 1997. International Life Sciences Institute (ILSI) Europe novel foods task force: the safety assessment of novel foods. Food Chem. Toxicol. 34, 931-940.
33. ILSI, 2003. The safety assessment of novel foods and concepts to determine their safety in use. Expert group report, ILSI Europe Novel Food Task Force. International Life Sciences Institute, Brussels, Belgium. Available from: .
34. ILSI, 2004. Nutritional and safety assessments of foods and feeds nutritionally improved through biotechnology. Comp. Rev. Food Sci. Food Safety 3, 35-104. Available from: .
35. Jacobs, C.M., Utterback, P.L., Parsons, C.M., Smith, B., Hinds, M., Rice, D.W., Liebergesell, M., Sauber, T., 2007. Feeding performance in laying hens fed diets containing DAS-59122-7 maize grain compared with diets containing non-transgenic maize grain. Poster, 2007 ADSA/ASAS/PSA/AMPA Joint Meeting, Abstract #W177. Available from: .
36. Lee K.Y., Townsend J., Tepperman J., Black M., Chui C.F., Mazur B., Dunsmuir P., and Bedbrook J. The molecular basis of sulfonylurea resistance in tobacco. EMBO J. 7 (1988) 1241-1248
37. Levene H. Robust test for equality of variances. In: Olkin J. (Ed). Contributions to Probability and Statistics (1960), Stanford University Press, Palo Alto, CA 278-292
38. MacKenzie S.A., Lamb I., Schmidt J., Deege L., Morrisey M.J., Harper M., Layton R.J., Prochaska L.M., Sanders C., Locke M., Mattson J.L., Fuentes A., and Delaney B. Thirteen week feeding study with transgenic maize grain containing event DAS-Ø15Ø7-1 in Sprague-Dawley rats. Food Chem. Toxicol. 45 (2007) 551-562
39. Malley L.A., Everds N.E., Reynolds J., Mann P.C., Lamb I., Rood T., Schmidt J., Layton R.J., Prochaska L.M., Hinds M., Locke M., Chui C.-F., Claussen F., Mattson J.L., and Delaney B. Subchronic feeding study of DAS-59122-7 maize grain in Sprague-Dawley rats. Food Chem. Toxicol. 45 (2007) 1277-1292
40. Mathesius, C.A., Barnett Jr., J.F., Cressman, R.F., Davis, T., Ding, J., Finlay, C., Ladics, G., Schmidt, J., Zhang, J., Delaney, B., in preparation. Safety assessment of the soybean acetolactate synthase protein (GM-HRA) in the context of agricultural biotechnology.
41. Mazur B.J., and Falco S.C. The development of herbicide resistant crops. Annu. Rev. Plant Physiol. 40 (1989) 441-470
42. McNaughton, J., Delaney, B., Smith, B., 2007a. Nutritional performance of broiler chickens fed diets containing GAT4601 (DP-356Ø43-5) soybean fractions. Poster, 2007 Southern Poultry Meetings, Abstract #P194. International Poultry Scientific Forum Abstracts, p. 63. Available from: .
43. McNaughton J., Roberts M., Smith B., Rice D., Hinds M., Schmidt J., Locke M., Bryant A., Rood T., Layton R., Lamb I., and Delaney B. Comparison of broiler performance when fed diets containing event DP-356Ø43-5 (Optimum™GAT™), nontransgenic near isoline control or commercial reference soybean meal, hulls, and oil. Poult. Sci. 86 (2007) 2569-2581
44. Milliken G.A., and Johnson D.A. Analysis of messy data. Designed Experiments vol. 1 (1984), Lifetime Learning Publications, Belmont, CA
45. Obert J.C., Ridley W.P., Schneider R.W., Riordan S.G., Nemeth M.A., Trujillo W.A., Breeze M.L., Sorbet R., and Astwood J.D. The composition of grain and forage from glyphosate-tolerant wheat is equivalent to that of conventional wheat (Triticum aestivum L.). J. Agric. Food Chem. 52 (2004) 1375-1384
46. OECD, 1993. Safety evaluation of foods produced by modern biotechnology: concepts and principles. Organisation of Economic Co-operation and Development, Paris, France.
47. OECD, 1997. OECD documents: Report of the OECD workshop on the toxicological and nutritional testing of novel foods, SG/ICGB(1998)1. Organisation of Economic Co-operation and Development, Paris, France.
48. OECD, 1998. Section 4 (Part 408), Health Effects: Repeated Dose 90-day Oral Toxicity Study in Rodents, Guideline for the Testing of Chemicals. Organisation of Economic Co-operation and Development, Paris, France.
49. OECD, 2001. Consensus document on compositional considerations for new varieties of soybean: key food and feed nutrients and anti-nutrients. Series on the Safety of Novel Foods and Feeds No. 2, ENV/JM/MONO(2001)15. Organisation of Economic Co-operation and Development, Paris, France.
50. OECD, 2002. Consensus document on compositional considerations for new varieties of maize (Zea mays): key food and feed nutrients, antinutrients, and secondary plant metabolites. Series on the Safety of Novel Foods and Feeds No. 5, ENV/JM/MONO(2002)25. Organisation of Economic Co-operation and Development, Paris, France.
51. OECD, 2003. Considerations for the safety assessment of animal feedstuffs derived from genetically modified plants. Series on the Safety of Novel Foods and Feeds No. 9, ENV/JM/MONO(2003)10. Organisation for Economic Co-operation and Development, Paris, France.
52. Ridley W.P., Sidhu R.S., Pyla P.D., Nemeth M.A., Breeze M.L., and Astwood J.D. Comparison of the nutritional profile of glyphosate tolerant corn event NK603 with that of conventional corn (Zea mays L.). J. Agric. Food Chem. 50 (2002) 7235-7243
53. SAS™ Version 8 on-line documentation, 1999. SAS Institute, Inc., Cary, NC.
54. Shapiro S.S., and Wilk M.B. An analysis of variance test for normality (complete samples). Biometrika 52 (1965) 591-611
55. Sidhu R.S., Hammond B.G., Fuchs R.L., Mutz J.N., Holden L.R., George B., and Olson T. 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 (2000) 2305-2312
56. Siehl D.L., Castle L.A., Gorton R., Chen Y.H., Bertain S., Cho H.J., Keenan R., Liu D., and Lassner M.W. Evolution of a microbial acetyltransferase for modification of glyphosate: a novel tolerance strategy. Pest Manag. Sci. 61 (2005) 235-240
57. Siehl D.L., Castle L.A., Gorton R., and Keenan R.J. The molecular basis of glyphosate resistance by an optimized microbial acetyltransferase. J. Biol. Chem. 282 (2007) 11446-11455
58. Snedecor G.W., and Cochran W.G. Statistical Methods. sixth ed. (1967), The Iowa State University Press, Ames, IA pp. 246-248 and 349-352
59. Stein, H.H., Rice, D.W., Smith, B.L., Hinds, M.A., Sauber, T.E., Pedersen, C., Wulf, D.M., Peters, D.N., 2007. Evaluation of corn grain with the genetically modified event DAS-59122-7 fed to growing-finishing pigs. Poster, ADSA/ASAS/PSA/AMPA Joint Meeting, Abstract #W157. J. Anim. Sci. 85, Suppl. 1 and J. Dairy Sci. 97, Suppl. 1 and Poult. Sci. 86, Suppl. 1, p. 512. Available from: .
60. Stein, H.H., Sauber, T., Rice, D., Hinds, M., Dana, G., Hunst, P., 2004. Comparison of corn grain from biotech and non-biotech counterparts for grow-finish pig performance. Poster, ADSA/ASAS/PSA Joint Meeting, Abstract #W65. J. Anim. Sci. 82, Suppl. 1 and J. Dairy Sci. 87, Suppl. 1 and Poult. Sci. 83, Suppl. 1, p. 328. Available from: .
61. Taylor M.L., Hartnell G.F., Nemeth M.A., Karunanandaa K., and George B. Comparison of broiler performance when fed diets containing grain from insect-protected (corn rootworm and European corn borer) and herbicide-tolerant (glyphosate) traits, control corn or commercial reference corn. Poult. Sci. 84 (2003) 587-593
62. Taylor M.L., Hartnell G.F., Riordan S.G., Nemeth M.A., Karunanandaa K., George B., and Astwood J.D. Comparison of broiler performance when fed diets containing grain from YieldGard (MON810), YieldGard × Roundup Ready (GA21), non-transgenic control or commercial corn. Poult. Sci. 82 (2003) 823-830
63. Taylor M.L., Hartnell G.F., Riordan S.G., Nemeth M.A., Karunanandaa K., George B., and Astwood J.D. Comparison of broiler performance when fed diets containing grain from Roundup Ready (NK603), YieldGard × Roundup Ready (MON810 × NK603), non-transgenic control or commercial corn. Poult. Sci. 82 (2003) 443-453
64. Taylor M.L., Hyun Y., Hartnell G.F., Riordan S.G., Nemeth M.A., Karunanandaa K., George B., and Astwood J.D. Comparison of broiler performance when fed diets containing grain from YieldGard Rootworm (MON863), YieldGard Plus (MON810×MON863), nontransgenic control or commercial reference corn hybrids. Poult. Sci. 82 (2003) 1948-1956
65. Teshima R., Akiyama H., Okunuki H., Sakushima J.I., Goda Y., Onodera H., Sawada J.I., and Toyoda M. Effect of GM and non-GM soybeans on the immune system of BN rats and B10A mice. J. Food Hyg. Soc. Jpn. 41 (2000) 188-193
66. US EPA, 1998. Office of Prevention, Pesticides, and Toxic Substances (OPPTS) Health Effects Test Guidelines: OPPTS 870.3100: 90-Day Oral Toxicity in Rodents. US Environmental Protection Agency, Washington, D.C.
67. WHO, 1991. Strategies for assessing the safety of foods produced by biotechnology. Report of a Joint FAO/WHO Consultation. World Health Organization, Geneva, Switzerland.
68. WHO, 1995. Application of the principles of substantial equivalence to the safety evaluation of foods and food components from plants derived from modern biotechnology. Report of WHO Workshop WHO/FNU/FOS/95.1. World Health Organization, Geneva, Switzerland.
69. Zhu Y., Li D., Wang F., Yin J., and Jin H. Nutritional assessment and fate of DNA of soybean meal from Roundup Ready or conventional soybeans using rats. Arch. Anim. Nutr. 58 (2004) 295-310