Recommendations for Maximum Incorporation Rates of Whole Food in 90-Day Rat Feeding Studies

Authors

  • Laurie Goodwin CropLife International https://orcid.org/0000-0002-5479-5756
  • Kevin Glenn Aulora Technologies, LLC
  • Jay Petrick Bayer Crop Science
  • Rakesh Ranjan BASF Corporation
  • Jason Roper Corteva Agriscience https://orcid.org/0000-0002-3594-666X
  • Alaina Sauve-Ciencewicki Syngenta Crop Protection
  • Patricia Bauman Syngenta Crop Protection
  • Kimberly Hodge-Bell Bayer Crop Science
  • Elizabeth Lipscomb BASF Corporation

Keywords:

incorporation rate, feeding studies, rat feeding studies, genetically modified

Abstract

More than 25 years of 90-day rat feeding studies with GM crops have consistently shown that these studies provide no additional value to safety assessments in the absence of a testable hypothesis. However, some regulatory authorities continue to require these studies while also specifying that the test material should be relevant to the product to be consumed and tested at the maximum incorporation rate not causing nutritional imbalance. In the absence of known or suspected adverse effects, dose range-finding studies are not feasible, yet scientifically justified incorporation rates are needed to balance the nutritional requirements of the animals and to achieve the goal of observing adverse effects, should they occur. When 90-day rat feeding studies are required for GM crop safety assessments, the following maximum incorporation rates (w/w), are recommended: 50 percent maize, 30 percent soybean, 60 percent rice, 15 percent canola, and 10 percent cottonseed. These recommendations are based on empirical data regarding maximum exposure to test material and avoidance of nutritional imbalances and/or exposure to anti-nutrients or toxins naturally present in the whole food. Each recommended maximum incorporation rate provides test material consumption at levels substantially higher than the highest human worldwide chronic consumption and is fully sufficient to address regulatory requirements.

https://doi.org/10.21423/jrs-v09i2goodwin

References

Alam, M. S., Watanabe, W. O., Carroll, P. M., Gabel, J. E., Corum, M. A., Seaton, P., Wedegaertner, T. C., Rathore, K. S., & Dowd, M. K. (2018). Evaluation of genetically-improved (glandless) and genetically-modified low-gossypol cottonseed meal as alternative protein sources in the diet of juvenile southern flounder Paralichthys lethostigma reared in a recirculating aquaculture system. Aquaculture, 489, 3645. https://doi.org/10.1016/j.aquaculture.2018.02.006

Australia New Zealand Food Authority. (2000). Draft Analysis Report, Application A363: Food produced from glyphosate-tolerant canola line GT73. Australia New Zealand Food Authority. Retrieved from http://www.foodstandards.gov.au/code/applications/documents/A363%20FA.pdf

Appenzeller, L. M., Malley, L., Mackenzie, S. A., Hoban, D., & Delaney, B. (2009). Subchronic feeding study with genetically modified stacked trait lepidopteran and coleopteran resistant (DAS-Ø15Ø7-1xDAS-59122-7) maize grain in Sprague-Dawley rats. Food and Chemical Toxicology, 47(7), 1512-1520. https://doi.org/10.1016/j.fct.2009.03.041

Appenzeller, L. M., Munley, S. M., Hoban, D., Sykes, G. P., Malley, L. A., & Delaney, B. (2008). Subchronic feeding study of herbicide-tolerant soybean DP-356Ø43-5 in Sprague-Dawley rats. Food and Chemical Toxicology, 46(6), 2201-2213. https://doi.org/10.1016/j.fct.2008.02.017

Appenzeller, L. M., Munley, S. M., Hoban, D., Sykes, G. P., Malley, L. A., & Delaney, B. (2009). Subchronic feeding study of grain from herbicide-tolerant maize DP-Ø9814Ø-6 in Sprague-Dawley rats. Food and Chemical Toxicology, 47(9), 2269-2280. https://doi.org/10.1016/j.fct.2009.06.014

Arntfield, S., & Hickling, D. (2011). Meal nutrition and utilization. In J. K. Daun, N. A. M. Neskin, & D. Hickling (Eds.), Canola - Chemistry, Production, Processing and Utilization (pp. 281-312). AOCS Press.

Australian Oilseed Federation (AOF). (2007). Australian Canola Meal Guide for the Feed Industry. Retrieved from http://www.australianoilseeds.com/__data/assets/pdf_file/0017/2591/Meal_Booklet-Net.pdf

Barlow, S. M., Greig, J. B., Bridges, J. W., Carere, A., Carpy, A. J. M., Galli, C. L., Kleiner, J., Knudsen, I., Koëter, H. B. W. M., Levy, L. S., Madsen, C., Mayer, S., Narbonne, J. F., Pfannkuch, F., Prodanchuk, M. G., Smith, M. R., & Steinberg, P. (2002). Hazard identification by methods of animal-based toxicology. Food and Chemical Toxicology, 40(2-3), 145-191. https://doi.org/10.1016/S0278-6915(01)00117-X

Bartholomaeus, A., Parrott, W., Bondy, G., & Walker, K. (2013). The use of whole food animal studies in the safety assessment of genetically modified crops: Limitations and recommendations. Critical Reviews in Toxicology, 43(Suppl. 2), 1-24. https://doi.org/10.3109/10408444.2013.842955

Bell, J. M., Benjamin, B. R., & Giovannetti, P. M. (1972). Histopathology of Thyroids and Livers of Rats and Mice Fed Diets Containing Brassica Glucosinolates. Canadian Journal of Animal Science, 52(2), 395-406. https://doi.org/10.4141/cjas72-045

Blasi, D. A., & Drouillard, J. (2002). Composition and Feeding Value of Cottonseed Feed Products for Beef Cattle. K-State Research and Extension.

Borzelleca, J. F. (1996). A Proposed Model for Safety Assessment of Macronutrient Substitutes. Regulatory Toxicology and Pharmacology, 23(1), S15-S18. https://doi.org/10.1006/rtph.1996.0017

Bos, C., Airinei, G., Mariotti, F., Benamouzig, R., Be'erot, S., Evrard, J., Fe'enart, E., Tome'e, D., & Gaudichon, C. (2007). The Poor Digestibility of Rapeseed Protein Is Balanced by Its Very High Metabolic Utilization in Humans. The Journal of Nutrition, 137(3), 594-600. https://doi.org/10.1093/jn/137.3.594

Brookes, G., & Barfoot, P. (2020). GM crops: global socio-economic and environmental impacts 1996-2016. Retrieved from https://www.agrobio.org/wp-content/uploads/2016/03/globalimpactstudyfinalreportJune2018.pdf

Canadian Bio-Systems. (2015). New Canola seed could increase options for meal use. Canadian Bio-Systems. Retrieved from http://www.agprofessional.com/news/new-Canola-seed-could-increase-options-meal-use

Canadian Grain Commission. (2015). Western Canadian Canola – scientific analysis of harvest and export quality, 2014 report. Retrieved August 31, 2015 from http://www.grainscanada.gc.ca/Canola/hqcm-mqrc-eng.htm

Canola Council of Canada. (2018). Canola Oil. Canola Council of Canada. Retrieved from https://www.canolacouncil.org/oil-and-meal/canola-oil/

Cao, S., He, X., Xu, W., Luo, Y., Yuan, Y., Liu, P., Cao, B., Shi, H., & Huang, K. (2012). Safety assessment of transgenic Bacillus thuringiensis rice T1c-19 in Sprague-Dawley rats from metabonomics and bacterial profile perspectives. International Union of Biochemistry and Molecular Biology (IUBMB) Life, 64(3), 242-250. https://doi.org/10.1002/iub.601

Carré, P., Quinsac, A., Citeau, M., & Fine, F. (2015). A re-examination of the technical feasibility and economic viability of rapeseed dehulling. Oilseeds & fats, Crops, and Lipids, 22(3), D304. https://doi.org/10.1051/ocl/2014044

Cellini, F., Chesson, A., Colquhoun, I., Constable, A., Davies, H. V., Engel, K. H., Gatehouse, A. M. R., Kärenlampi, S., Kok, E. J., Leguay, J.-J., Lehesranta, S., Noteborn, H. P. J. M., Pedersen, J., & Smith, M. (2004). Unintended effects and their detection in genetically modified crops. Food and Chemical Toxicology, 42(7), 1089-1125. https://doi.org/10.1016/j.fct.2004.02.003

Chassy, B., Egnin, M., Gao, Y., Glenn, K., Kleter, G. A., Nestel, P., Newell-McGloughlin, M., Phipps, R. H., & Shillito, R. (2008). Nutritional and Safety Assessments of Foods andFeeds Nutritionally Improved through Biotechnology: Case Studies. Comprehensive Reviews in Food Science and Food Safety, 7(1), 50-113. https://doi.org/10.1111/j.1750-3841.2007.00579.x

Chassy, B., Hlywka, J. J., Kleter, G. A., Kok, E. J., Kuiper, H. A., McGloughlin, M., Munro, I. C., Phipps, R. H., & Reid, J. A. (2004). Nutritional and Safety Assessments of Foods and Feeds Nutritionally Improved through Biotechnology. Comprehensive Reviews in Food Science and Food Safety, 3(2), 38-104.

Chukwudebe, A., Privalle, L., Reed, A., Wandelt, C., Contri, D., Dammann, M., Groeters, S., Kaspers, U., Strauss, V., & van Ranenzwaaay, B. (2012). Health and nutritional status of Wistar rats following subchronic exposure to CV127 soybeans. Food and Chemical Toxicology, 50(3-4) 956-971. https://doi.org/10.1016/j.fct.2011.11.034

Codex Alimentarius Commission. (2009). Foods derived from modern biotechnology, Ed 2. Retrieved from http://www.fao.org/3/a-a1554e.pdf

Curran, K. L., Festa, A. R., Goddard, S. D., Harrigan, G. G., & Taylor, M. L. (2015). Kernel Compositions of Glyphosate-Tolerant and Corn Rootworm-Protected MON 88017 Sweet Corn and Insect-Protected MON 89034 Sweet Corn Are Equivalent to That of Conventional Sweet Corn (Zea mays). Journal of Agricultural and Food Chemistry, 63(11), 3046-3052. https://doi.org/10.1021/jf505687s

Daun, J. K. (2011). Origin, Distribution, and Production. In J. K. Daun, N. A. M. Eskin, & D. Hickling (Eds.), Canola: Chemistry, Production, Processing, and Utilization (Vol. 4, pp. 1-27). AOCS Press.

Delaney, B., Appenzeller, L. M., Munley, S. M., Hoban, D., Sykes, G. P., Malley, L. A., & Sanders, C. (2008). Subchronic feeding study of high oleic acid soybeans (Event DP-3Ø5423-1) in Sprague-Dawley rats. Food and Chemical Toxicology, 46(12), 3808-3817. https://doi.org/10.1016/j.fct.2008.10.003

Delaney, B., Appenzeller, L. M., Roper, J. M., Mukerji, P., Hoban, D., & Sykes, G. P. (2014). Thirteen week rodent feeding study with processed fractions from herbicide tolerant (DP-Ø73496-4) canola. Food and Chemical Toxicology, 66, 173-184. https://doi.org/10.1016/j.fct.2014.01.042

Dimov, Z., Suprianto, E., Hermann, F., & Möllers, C. (2012). Genetic variation for seed hull and fibre content in a collection of European winter oilseed rape material (Brassica napus L.) and development of NIRS calibrations. Plant Breeding, 131(3), 361-368. https://doi.org/10.1111/j.1439-0523.2012.01951.x

Dryzga, M. D., Yano, B. L., Andrus, A. K., & Mattsson, J. L. (2007). Evaluation of the safety and nutritional equivalence of a genetically modified cottonseed meal in a 90-day dietary toxicity study in rats. Food and Chemical Toxicology, 45(10), 1994-2004. https://doi.org/http://dx.doi.org/10.1016/j.fct.2007.04.017

European Food Safety Authority (EFSA). (2004). Opinion of the Scientific Panel on Genetically Modified Organisms on a request from the Commission related to the Notification (Reference C/NL/98/11) for the placing on the market of herbicide-tolerant oilseed rape GT73, for import and processing, under Part C of Directive 2001/18/EC from Monsanto. The European Food Safety Authority Journal, 29, 1-19. https://doi.org/10.2903/j.efsa.2004.29

European Food Safety Authority (EFSA). (2006). Guidance document for the risk assessment of genetically modified plants and derived food and feed by the Scientific Panel on Genetically Modified Organisms (GMO) - including draft document updated in 2008. The European Food Safety Authority Journal, 4(4). https://doi.org/10.2903/j.efsa.2006.99

European Food Safety Authority (EFSA). (2008). Safety and nutritional assessment of GM plants and derived food and feed: The role of animal feeding trials; Report of the EFSA GMO Panel Working Group on Animal Feeding Trials. Food and Chemical Toxicology, 46, S2-S70. https://doi.org/10.1016/j.fct.2008.02.008

European Food Safety Authority (EFSA). (2008). Scientific Opinion: Gossypol as undesirable substance in animal feed. The European Food Safety Authority Journal, 908, 1-55. https://doi.org/10.2903/j.efsa.2009.908

European Food Safety Authority (EFSA). (2011). Guidance for risk assessment of food and feed from genetically modified plants. The European Food Safety Authority Journal, 9(5), 2150. https://doi.org/10.2903/j.efsa.2011.2150

European Food Safety Authority (EFSA). (2013). EFSA NDA Panel on Dietetic Products, Nutrition and Allergies. The European Food Safety Authority Journal, 11(10), 3420. http://dx.doi.org/10.2903/j.efsa.2013.3420

European Food Safety Authority (EFSA). (2013). EFSA Panel on Genetically Modified Organisms (GMO); Scientific Opinion on application (EFSA-GMO-NL-2010-87) for the placing on the market of genetically modified herbicide tolerant oilseed rape GT73 for food containing or consisting of, and food produced from or containing ingredients produced from oilseed rape GT73 (with the exception of refined oil and food additives) under Regulation (EC) No 1829/2003 from Monsanto. The European Food Safety Authority Journal, 11(2), 3079. http://dx.doi.org/10.2903/j.efsa.2013.3079

European Food Safety Authority (EFSA). (2014). Explanatory statement for the applicability of the Guidance of the EFSA Scientific Committee on conducting repeated-dose-90-day oral toxicity study in rodents on whole food/feed for GMO risk assessment. The European Food Safety Authority Journal, 12(10), 3871. https://doi.org/10.2903/j.efsa.2014.3871

European Food Safety Authority (EFSA). (2014). Scientific Opinion on applications (EFSA-GMO-UK-2008-57 and EFSAGMO-RX-MON15985) for the placing on the market of insect-resistant genetically modified cotton MON 15985 for food and feed uses, import and processing, and for the renewal of authorisation of existing products produced from cotton MON 15985, both under Regulation (EC) No 1829/003 from Monsanto. The European Food Safety Authority Journal, 12(7), 3770. https://doi.org/10.2903/j.efsa.2014.3770

European Food Safety Authority (EFSA). (2018). Assessment of genetically modified cotton GHB614 × T304‐40 × GHB119 for food and feed uses, import and processing under Regulation (EC) No 1829/2003 (application EFSA‐GMO‐NL‐2014‐122). The European Food Safety Authority Journal, 16(7), 5349. https://doi.org/10.2903/j.efsa.2018.5349

European Food Safety Authority (EFSA). (2019). Ad hoc meeting with industry representatives. European Food Safety Authority. Retrieved from https://www.efsa.europa.eu/en/events/event/ad-hoc-meeting-industry-representatives

El-Mezawy, A., Wu, L., & Shah, S. (2009). A seed coat-specific promoter for canola. Biotechnology Letters, 31(12), 1961-1965. https://doi.org/10.1007/s10529-009-0098-y

Erickson, D. R. (1995). Overview of modern soybean processing and links between processors. In D. R. Erickson (Ed.), Practical Handbook of Soybean Processing and Utilization (pp. 56-64). AOCS Press.

European Commission. (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. Official Journal of the European Communities, L253, 1-36. Retrieved from https://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:31997H0618&rid=1

European Commission. (2010). Directive 2010/63/EU of the European Parliament and of the Council of 22 September 2010 on the protection of animals used for scientific purposes. Official Journal of the European Union, L276, 33-79. Retrieved from https://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2010:276:0033:0079:en:PDF

European Commission. (2013). COMMISSION IMPLEMENTING REGULATION (EU) No 503/2013 of 3 April 2013 on applications for authorisation of genetically modified food and feed in accordance with Regulation (EC) No 1829/2003 of the European Parliament and of the Council and amending Commission Regulations (EC) No 641/2004 and (EC) No 1981/2006. Official Journal of the European Union, L 157, 1-48. Retrieved from https://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2013:157:0001:0048:EN:PDF

Fang, J., Feng, Y., Zhi, Y., Zhang, L., Zhou, Y., & Jia, X. (2017). A 90-day toxicity study of GmTMT transgenic maize in Sprague-Dawley rats. Regulatory Toxicology and Pharmacology, 85, 48-54. https://doi.org/10.1016/j.yrtph.2017.01.004

Flachowsky, G. (2013). In G. Flachowsky (Ed.), Animal Nutrition with Transgenic Plants. Wallingford and Boston.

Flecknell, P. (2002). Replacement, reduction and refinement. Altex, 19(2), 73-78.

Glenn, K. C., Alsop, B., Bell, E., Goley, M., Jenkinson, J., Liu, B., Martin, C., Parrott, W., Souder, C., Sparks, O., Urquhart, W., Ward, J. M., & Vicini, J. L. (2017). Bringing New Plant Varieties to Market: Plant Breeding and Selection Practices Advance Beneficial Characteristics while Minimizing Unintended Changes. Crop Science, 57(6), 2906-2921. https://doi.org/10.2135/cropsci2017.03.0199

Hamilton, K. A., Goodman, R. E., & Fuchs, R. L. (2002). In J. A. Thomas & R. L. Fuchs (Eds.), Biotechnology and Safety Assessment. Academic Press.

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 and Chemical Toxicology, 42(6), 1003-1014. https://doi.org/10.1016/j.fct.2004.02.013

Hammond, B. G., Dudek, R., Lemen, J. K., & Nemeth, M. A. (2006). Results of a 90-day safety assurance study with rats fed grain from corn borer-protected corn. Food and Chemical Toxicology, 44(7), 1092-1099. https://doi.org/10.1016/j.fct.2006.01.003

Hammond, B. G., & Jez, J. M. (2011). Impact of food processing on the safety assessment for proteins introduced into biotechnology-derived soybean and corn crops. Food and Chemical Toxicology, 49(4), 711-721. https://doi.org/10.1016/j.fct.2010.12.009

Hammond, B. G., Lemen, J. K., Ahmed, G., Miller, K. D., Kirkpatrick, J., & Fleeman, T. (2008). Safety assessment of SDA soybean oil: Results of a 28-day gavage study and a 90-day/one generation reproduction feeding study in rats. Regulatory Toxicology and Pharmacology, 52(3), 311-323. https://doi.org/10.1016/j.yrtph.2008.08.015

He, X., de Brum, P. A. R., Chukwudebe, A., Privalle, L., Reed, A., Wang, Y., Zhou, C., Wang, C., Lu, J., Huang, K., Contri, D., Nakatani, A., de Avila, V. S., Klein, C. H., de Lima, G. J. M. M., & Lipscomb, E. A. (2016). Rat and poultry feeding studies with soybean meal produced from imidazolinone-tolerant (CV127) soybeans. Food and Chemical Toxicology, 88, 48-56. https://doi.org/10.1016/j.fct.2015.12.012

He, X. Y., Huang, K. L., Li, X., Qin, W., Delaney, B., & Luo, Y. B. (2008). Comparison of grain from corn rootworm resistant transgenic DAS-59122-7 maize with non-transgenic maize grain in a 90-day feeding study in Sprague-Dawley rats. Food and Chemical Toxicology, 46(6), 1994-2002. https://doi.org/10.1016/j.fct.2008.01.039

He, X. Y., Tang, M. Z., Luo, Y. B., Li, X., Cao, S. S., Yu, J. J., Delaney, B., & Huang, K. L. (2009). A 90-day toxicology study of transgenic lysine-rich maize grain (Y642) in Sprague–Dawley rats. Food and Chemical Toxicology, 47(2), 425-432. https://doi.org/10.1016/j.fct.2008.11.032

Healy, C., Hammond, B., & Kirkpatrick, J. (2008). Results of a 13-week safety assurance study with rats fed grain from corn rootworm-protected, glyphosate-tolerant MON 88017 corn. Food and Chemical Toxicology, 46(7), 2517-2524. https://doi.org/10.1016/j.fct.2008.04.005

Herman, R. A., & Price, W. D. (2013). Unintended compositional changes in genetically modified (GM) crops: 20 years of research. Journal of Agricultural and Food Chemistry, 61(48), 11695-11701. https://doi.org/10.1021/jf400135r

Heuzé, V., Tran, G., Hassoun, P., Bastianelli, D., & Lebas, F. (2019). Cottonseed meal. Feedipedia, a programme by INRA, CIRAD, AFZ and FAO. Retrieved February 8, 2019 from https://feedipedia.org/node/550

Hong, B., Du, Y., Mukerji, P., Roper, J. M., & Appenzeller, L. M. (2017). Safety Assessment of Food and Feed from GM Crops in Europe: Evaluating EFSA’s Alternative Framework for the Rat 90-day Feeding Study. Journal of Agricultural and Food Chemistry, 65(27), 5545-5560. https://doi.org/10.1021/acs.jafc.7b01492

Howlett, J., Edwards, D., Cockburn, A., Hepburn, P., Kleiner, J., Knorr, D., Kozianowski, G., Müller, D., Peijnenburg, A., Perrin, I., Poulsen, M., & Walker, R. (2003). The safety assessment of Novel Foods and concepts to determine their safety in use. International Journal of Food Sciences and Nutrition, 54(5), S1-S32. http://doi.org/10.1080/09637480310001610308

Ibrahim, D. M. (2015). Reduce, Refine, Replace. The failure of the three R`s and the future of animal experimentation. University of Chicago Legal Forum 206(1), 192-229. http://chicagounbound.uchicago.edu/uclf/vol2006/iss1/7

International Service for the Acquisition of Agri-biotech Applications (ISAAA). (2018). Global Status of Commercialized Biotech/GM Crops in 2018: Biotech Crops Continue to Help Meet the Challenges of Increased Population and Climate Change. Retrieved from https://www.isaaa.org/resources/publications/briefs/54/default.asp

Juma, C. (2016). Innovation and Its Enemies: Why People Resist New Technologies. Oxford University Press. https://doi.org/10.1093/acprof:oso/9780190467036.001.0001

Kessler, D. A., Taylor, M. R., Maryanski, J. H., Flamm, E. L., & Kahl, L. S. (1992). The Safety of Foods Developed by Biotechnology. Science, 256(5056), 1747-1749, https://doi.org/10.1126/science.1615315

Kyndt, T., Quispe, D., Zhai, H., Jarret, R., Ghislain, M., Liu, Q., Gheysen, G., & Kreuze, J. F. (2015). The genome of cultivated sweet potato contains Agrobacterium T-DNAs with expressed genes: An example of a naturally transgenic food crop. Proceedings of the National Academy of Sciences of the United States of America, 112(18), 5844-5849. https://doi.org/10.1073/pnas.1419685112

Ladics, G. S., Bartholomaeus, A., Bregitzer, P., Doerrer, N. G., Gray, A., Holzhauser, T., Jordan, M., Keese, P., Kok, E., Macdonald, P., Parrott, W., Privalle, L., Raybould, A., Rhee, S. Y., Rice, E., Romeis, J., Vaughn, J., Wal, J.-M., & Glenn, K. (2015). Genetic basis and detection of unintended effects in genetically modified crop plants. Transgenic Research, 24(4), 587–603. https://doi.org/10.1007/s11248-015-9867-7

Liener, I. E. (1994). Implications of Antinutritional Components in Soybean Foods. Critical Reviews in Food Science and Nutrition, 34(1), 31-67. https://doi.org/10.1080/10408399409527649

Linnemann, A. R., & Dijkstra, D. S. (2002). Toward Sustainable Production of Protein-Rich Foods: Appraisal of Eight Crops for Western Europe. PART I. Analysis of the Primary Links of the Production Chain. Critical Reviews in Food Science and Nutrition, 42(4), 377-401. https://doi.org/10.1080/20024091054193

MacKenzie, S. A., Lamb, I., Schmidt, J., Deege, L., Morrisey, M. J., Harper, M., Layton, R. J., Prochaska, L. M., Sanders, C., Locke, M., Mattsson, J. L., Fuentes, A., & Delaney, B. (2007). Thirteen week feeding study with transgenic maize grain containing event DAS-Ø15Ø7-1 in Sprague-Dawley rats. Food and Chemical Toxicology, 45(4), 551-562. https://doi.org/10.1016/j.fct.2006.09.016

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., Mattsson, J. L., & Delaney, B. (2007). Subchronic feeding study of DAS-59122-7 maize grain in Sprague-Dawley rats. Food and Chemical Toxicology, 45(7), 1277-1292. https://doi.org/10.1016/j.fct.2007.01.013

Matveeva, T. V., & Otten, L. (2019). Widespread occurrence of natural genetic transformation of plants by Agrobacterium. Plant Molecular Biology, 101(4), 415-437. https://doi.org/10.1007/s11103-019-00913-y

Morgan, S. E. (2015). Gossypol Toxicity in Livestock. Oklahoma State University, Division of Agricultural Sciences and Natural Resources, VTMD-9116. Retrieved from http://pods.dasnr.okstate.edu/docushare/dsweb/Get/Document-1952/VTMD-9116-2015.pdf

Naczk, M., Amarowicz, R., Sullivan, A., & Shahidi, F. (1998). Current research developments on polyphenolics of rapeseed/canola: a review. Food Chemistry, 62(4), 489-502. https://doi.org/10.1016/S0308-8146(97)00198-2

National Academic Press. (2004). Safety of Genetically Engineered Foods: Approaches to Assessing Unintended Health Effects. National Academic Press.

National Corn Growers Association. (2020). Corn Usage by Segment 2019. National Corn Growers Association. Retrieved from http://www.worldofcorn.com/#corn-usage-by-segment

NSW Government. (2014). Variability of quality traits in canola seed, oil and meal - a review. NSW Department of Primary Industries. Retrieved from https://www.dpi.nsw.gov.au/__data/assets/pdf_file/0007/517786/variability-of-quality-traits-in-canola-a-review.pdf

Organization for Economic Cooperation and Development (OECD). (1997). Report of the OECD Workshop on the Toxicological and Nutritional Testing of Novel Foods. Retrieved from http://www.oecd.org/env/ehs/biotrack/SG-ICGB(98)1-FINAL-ENG%20-Novel-Foods-Aussois-report.pdf

Organization for Economic Cooperation and Development (OECD). (1998). OECD Guideline for the Testing of Chemicals 408: Repeated Dose 90-day Oral Toxicity Study in Rodents. Retrieved from https://www.oecd-ilibrary.org/environment/test-no-408-repeated-dose-90-day-oral-toxicity-study-in-rodents_9789264070707-en

Organization for Economic Cooperation and Development (OECD). (2002). Consensus Document on Compositional Considerations for New Varieties of Maize (Zea Mays): Key Food and Feed Nutrients, Anti-Nutrients and Secondary Plant Metabolites. Retrieved from https://www.oecd.org/env/ehs/biotrack/46815196.pdf

Organization for Economic Cooperation and Development (OECD). (2009). Consensus Document on Compositional Considerations for New Varieties of Cotton (Gossypium hirsutum and Gossypium barbadense): Key Food and Feed Nutrients and Anti-Nutrients. Retrieved from https://www.oecd.org/env/ehs/biotrack/46815236.pdf

Organization for Economic Cooperation and Development (OECD). (2011). Revised Consensus Document on Compositional Considerations for New Varieties of Low Erucic Acid Rapeseed (Canola): Key Food and Feed Nutrients, Anti-Nutrients and Toxicants. Retrieved from http://www.oecd.org/science/biotrack/49343153.pdf

Organization for Economic Cooperation and Development (OECD). (2012). Revised Consensus Document on Compositional Considerations for New Varieties of Soybean [Glycine max (L.) Merr]: Key Food and Feed Nutrients, Anti-nutrients, Toxicants and Allergens. Retrieved from http://www.oecd.org/officialdocuments/publicdisplaydocumentpdf/?cote=env/jm/mono(2012)24&doclanguage=en

Organization for Economic Cooperation and Development (OECD). (2016). Revised Consensus Document on Compositional Considerations for New Varieties of Rice (Oryza sativa): Key Food and Feed Nutrients, Anti-Nutrients and Other Constituents. Retrieved from https://one.oecd.org/document/ENV/JM/MONO%282016%2938/en/pdf

Organization for Economic Cooperation and Development (OECD). (2018). Repeated dose 90-day oral toxicity study in rodents. Retrieved from https://www.oecd-ilibrary.org/environment/test-no-408-repeated-dose-90-day-oral-toxicity-study-in-rodents_9789264070707-en

Paoletti, C., Flamm, E., Yan, W., Meek, S., Renckens, S., Fellous, M., & Kuiper, H. (2008). GMO risk assessment around the world: Some examples. Trends in Food Science & Technology, 19(Suppl. 1), S70-S78. https://doi.org/10.1016/j.tifs.2008.07.007

Papineni, S., Murray, J. A., Ricardo, E., Dunville, C. M., Sura, R. K., & Thomas, J. (2017). Evaluation of the safety of a genetically modified DAS-444Ø6-6 soybean meal and hulls in a 90-day dietary toxicity study in rats. Food and Chemical Toxicology, 109, 245-252. https://doi.org/10.1016/j.fct.2017.08.048

Papineni, S., Passage, J. K., Ekmay, R. D., & Thomas, J. (2018). Evaluation of 30% DAS-444Ø6-6 soybean meal in a subchronic rat toxicity study. Regulatory Toxicology and Pharmacology, 94, 57-69. https://doi.org/10.1016/j.yrtph.2018.01.005

Pennisi, E. (2016). Shaking up the Tree of Life. Science, 354(6314), 817-821. https://doi.org/10.1126/science.354.6314.817

Poulsen, M., Kroghsbo, S., Schroder, M., Wilcks, A., Jacobsen, H., Miller, A., Frenzel, T., Danier, J., Rychlik, M., Shu, Q., Emami, K., Sudhakar, D., Gatehouse, A., Engel, K. H., & Knudsen, I. (2007). A 90-day safety study in Wistar rats fed genetically modified rice expressing snowdrop lectin Galanthus nivalis (GNA). Food and Chemical Toxicology, 45(3), 350-363. https://doi.org/10.1016/j.fct.2006.09.002

Poulsen, M., Schroder, M., Wilcks, A., Kroghsbo, S., Lindecrona, R. H., Miller, A., Frenzel, T., Danier, J., Rychlik, M., Shu, Q., Emami, K., Taylor, M., Gatehouse, A., Engel, K. H., & Knudsen, I. (2007). Safety testing of GM-rice expressing PHA-E lectin using a new animal test design. Food and Chemical Toxicology, 45(3), 364-377. https://doi.org/10.1016/j.fct.2006.09.003

Prado, J. R., Segers, G., Voelker, T., Carson, D., Dobert, R., Phillips, J., Cook, K., Cornejo, C., Monken, J., Grapes, L., Reynolds, T., & Martino-Catt, S. (2014). Genetically engineered crops: from idea to product. Annual Review of Plant Biology, 65(1), 769–790. https://doi.org/doi:10.1146/annurev-arplant-050213-040039

Privalle, L. S., Chen, J., Clapper, G., Hunst, P., Spiegelhalter, F., & Zhong, C. X. (2012). Development of an agricultural biotechnology crop product: testing from discovery to commercialization. Journal of Agricultural and Food Chemistry, 60(41), 10179–10187. https://doi.org/10.1021/jf302706e

Rathore, K. S., Pandeya, D., Campbell, L. M., Wedegaertner, T. C., Puckhaber, L., Stipanovic, R. D., Thenell, J. S., Hague, S., & Hake, K. (2020). Ultra-low gossypol cottonseed: selective gene silencing opens up a vast resource of plant-based protein to improve human nutrition. Critical Reviews in Plant Sciences, 39(1), 1-29. https://doi.org/https://doi.org/10.1080/07352689.2020.1724433

Ricroch, A. E. (2013). Assessment of GE food safety using '-omics' techniques and long-term animal feeding studies. New Biotechnology, 30(4), 349-354. https://doi.org/10.1016/j.nbt.2012.12.001

Rooney, L. W., & Serna-Saldivar, S. O. (2003). Food Use of Whole Corn and Dry-Milled Fractions. In P. J. White & L. A. Johnson (Eds.), Corn: Chemistry and Technology (2 ed., pp. 495-535). American Association of Cereal Chemists.

Russell, W. M. S., & Burch, R. L. (1959). The Principles of Humane Experimental Technique. Methuen and Co. Ltd.

Sakamoto, Y., Tada, Y., Fukumori, N., K., T., Ando, H., Takahashi, H., Y., K., Nagasawa, A., Yano, N., Yuzawa, K., & Ogata, A. (2008). A 104-week feeding study of genetically modified soybeans in F344 rats. Journal of the Food Hygienic Society of Japan (Shokuhin Eiseigaku Zasshi), 49(4), 272-282. https://doi.org/10.3358/shokueishi.49.272

Sakamoto, Y., Tada, Y., Fukumori, N., K., T., Ando, H., Takahashi, H., Y., K., Nagasawa, A., Yano, N., Yuzawa, K., Ogata, A., & Kamimura, H. (2007). A 52-week feeding study of genetically modified soybeans in F344 rats. Journal of the Food Hygienic Society of Japan (Shokuhin Eiseigaku Zasshi), 48(3), 41-50. https://doi.org/10.3358/shokueishi.48.41

Sauer, W. C., Cichon, R., & Misir, R. (1982). Amino Acid Availability and Protein Quality of Canola and Rapeseed Meal for Pigs and Rats. Journal of Animal Science, 54(2), 292-301. https://doi.org/10.2527/jas1982.542292x

Schnell, J., Steele, M., Bean, J., Neuspiel, M., Girard, C., Dormann, N., Pearson, C., Savoie, A., Bourbonniere, L., & Macdonald, P. (2015). A comparative analysis of insertional effects in genetically engineered plants: considerations for pre-market assessments. Transgenic Research, 24(1), 1-17. https://doi.org/10.1007/s11248-014-9843-7

Schrøder, M., Poulsen, M., Wilcks, A., Kroghsbo, S., Miller, A., Frenzel, T., Danier, J., Rychlik, M., Emami, K., Gatehouse, A., Shu, Q., Engel, K.-H., Altosaar, I., & Knudsen, I. (2007). A 90-day safety study of genetically modified rice expressing Cry1Ab protein (Bacillus thuringiensis toxin) in Wistar rats. Food and Chemical Toxicology, 45(3), 339-349. https://doi.org/10.1016/j.fct.2006.09.001

Sczostak, A. (2009). Cotton Linters: An Alternative Cellulosic Raw Material. Macromolecular Symposia, 280(1), 45-53. https://doi.org/10.1002/masy.200950606

Shahidi, F., & Naczk, M. (1992). An overview of the phenolics of canola and rapeseed: Chemical, sensory and nutritional significance. Journal of the American Oil Chemists' Society, 69(9), 917-924. https://doi.org/10.1007/BF02636344

Sheng, Y., Qi, X., Liu, Y., Guo, M., Chen, S., He, X., Huang, K., & Xu, W. (2014). Subchronic toxicity study in vivo and allergenicity study in vitro for genetically modified rice that expresses pharmaceutical protein (human serum albumin). Food and Chemical Toxicology, 72, 242-246. https://doi.org/10.1016/j.fct.2014.07.030

Snell, C., Bernheim, A., Bergé, J.-B., Kuntz, M., Pascal, G., Paris, A., & Ricroch, A. E. (2012). Assessment of the health impact of GM plant diets in long-term and multigenerational animal feeding trials: A literature review. Food and Chemical Toxicology, 50(3), 1134-1148. https://doi.org/10.1016/j.fct.2011.11.048

Song, H., He, X., Zou, S., Zhang, T., Luo, Y., Huang, K., Zhu, Z., & Xu, W. (2015). A 90-day subchronic feeding study of genetically modified rice expressing Cry1Ab protein in Sprague-Dawley rats. Transgenic Research, 24(2), 295-308. https://doi.org/10.1007/s11248-014-9844-6

Sotelo, A., Montalvo, I., de la Luz Crail, M., & González-Garza, M. T. (1982). Infertility in Male Rats Induced by Diets Containing Whole Cottonseed Flour. The Journal of Nutrition, 112(11), 2052-2057. https://doi.org/10.1093/jn/112.11.2052

Soucy, S. M., Huang, J., & Gogarten, J. P. (2015). Horizontal gene transfer: building the web of life. Nature Reviews. Genetics, 16(8), 472-482. https://doi.org/10.1038/nrg3962

Statista. (2020). Leading countries based on the production of milled rice in 2018/2019 (in million metric tons). Retrieved from https://www.statista.com/statistics/255945/top-countries-of-destination-for-us-rice-exports-2011/

Steinberg, P., Van der Voet, H., Goedhart, P. W., Kleter, G., Kok, E. J., Pla, M., Nadal, A., Zeljenková, D., Aláčová, R., Babincová, J., Rollerová, E., Jaďuďová, S., Kebis, A., Szabova, E., Tulinská, J., Líšková, A., Takácsová, M., Mikušová, M. L., Krivošíková, Z., Spök, A., Racovita, M., de Vriend, H., Alison, R., Alison, C., Baumgärtner, W., Becker, K., Lempp, C., Schmicke, M., Schrenk, D., Pöting, A., Schiemann, J., & Wilhelm, R. (2019). Lack of adverse effects in subchronic and chronic toxicity/carcinogenicity studies on the glyphosate-resistant genetically modified maize NK603 in Wistar Han RCC rats. Archives of Toxicology, 93(4), 1095-1139. https://doi.org/10.1007/s00204-019-02400-1

Tan, S. H., Mailer, R. J., Blanchard, C. L., & Agboola, S. O. (2011). Canola Proteins for Human Consumption: Extraction, Profile, and Functional Properties. Journal of Food Science, 76(1), R16-R28. https://doi.org/10.1111/j.1750-3841.2010.01930.x

Tang, M., Xie, T., Cheng, W., Qian, L., Yang, S., Yang, D., Cui, W., & Li, K. (2012). A 90-day safety study of genetically modified rice expressing rhIGF-1 protein in C57BL/6J rats. Transgenic Research, 21(3), 499-510. https://doi.org/10.1007/s11248-011-9550-6

Tang, X., Han, F., Zhao, K., Xu, Y., Wu, X., Wang, J., Jiang, L., & Shi, W. (2012). A 90-day dietary toxicity study of genetically modified rice T1C-1 expressing Cry1C protein in Sprague Dawley rats. PLoS One, 7(12), e52507. https://doi.org/10.1371/journal.pone.0052507

Teshima, R., Akiyama, H., Okunuki, H., Sakushima, J., Goda, Y., Onodera, H., Sawada, J., & Toyoda, M. (2000). Effect of GM and non-GM soybeans on the immune system of BN rats and B10A mice. Journal of the Food Hygienic Society of Japan (Shokuhin Eiseigaku Zasshi), 41(3), 188-193. https://doi.org/10.3358/shokueishi.41.188

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. Journal of the Food Hygienic Society of Japan (Shokuhin Eiseigaku Zasshi), 43(5), 273-279. https://doi.org/10.3358/shokueishi.43.273

The World Bank. (2019). Arable land (hectares per person). Food and Agriculture Organization, The World Bank. https://data.worldbank.org/indicator/AG.LND.ARBL.HA.PC?end=2016&start=1961&view=chart

Unger, E. H. (2011). Processing. In J. K. Daun, N. A. M. Eskin, & D. Hickling (Eds.), Canola - Chemistry, Production, Processing and Utilization (pp. 163-188). AOCS Press.

United States - Environmental Protection Agency. (1988). Recommendations For And Documentation Of Biological Values For Use In Risk Assessment. Retrieved from https://cfpub.epa.gov/ncea/risk/recordisplay.cfm?deid=34855

United States Department of Agriculture - Economic Research Service. (2017). United States Department of Agriculture, Economic Research Service. Retrieved from https://www.ers.usda.gov/topics/crops/soybeans-oil-crops/canola/

United States Department of Agriculture - Foreign Agricultural Service. (2018). Oilseeds: World Markets and Trade. Retrieved from https://apps.fas.usda.gov/psdonline/circulars/oilseeds.pdf

Venkatesh, T. V., Breeze, M. L., Liu, K., Harrigan, G. G., & Culler, A. H. (2014). Compositional analysis of grain and forage from MON 87427, an inducible male sterile and tissue selective glyphosate-tolerant maize product for hybrid seed production. Journal of Agricultural and Food Chemistry, 62(8), 1964-1973. https://doi.org/10.1021/jf4041589

Venkatesh, T. V., Cook, K., Liu, B., Perez, T., Willse, A., Tichich, R., Feng, P., & Harrigan, G. G. (2015). Compositional differences between near-isogenic GM and conventional maize hybrids are associated with backcrossing practices in conventional breeding. Plant Biotechnology Journal, 13(2), 200-210. https://doi.org/10.1111/pbi.12248

Von Der Haar, D., Müller, K., Bader-Mittermaier, S., & Eisner, P. (2014). Rapeseed proteins – Production methods and possible application ranges. Oilseeds & fats, Crops, and Lipids, 21(1), D104. https://doi.org/10.1051/ocl/2013038

Wang, E. H., Yu, Z., Hu, J., & Xu, H. B. (2013). Effects of 90-day feeding of transgenic Bt rice TT51 on the reproductive system in male rats. Food and Chemical Toxicology, 62, 390-396. https://doi.org/10.1016/j.fct.2013.08.032

Wang, Z. H., Wang, Y., Cui, H.R., Xia, Y.W., Altosaar, I., & Shu, Q.Y. (2002). Toxicological evaluation of transgenic rice flour with a synthetic cry1Ab gene from Bacillus thuringiensis. Journal of the Science of Food and Agriculture, 82(7), 7. https://doi.org/10.1002/jsfa.1105

Watson, S. A. (1988). Corn Marketing, Processing, and Utilization. In G. F. Sprague, G. Sprague, & J. W. Dudley (Eds.), Corn and Corn Improvement (3rd ed., pp. 881-940). American Society of Agronomy.

World Health Organization & Food and Agriculture Organization of the United Nations. (2008). Consultations and workshops : dietary exposure assessment of chemicals in food : report of a joint FAO/WHO consultation, Annapolis, Maryland, USA, 2-6 May 2005. Retrieved from https://apps.who.int/iris/handle/10665/44027

World Health Organization. (2017). Tracking contaminants in food. Retrieved from https://www.who.int/foodsafety/areas_work/chemical-risks/gems-food/en/

Wu, Y., Xu, Y., Du, Y., Zhao, X., Hu, R., Fan, X., Ren, F., Yao, Q., Peng, R., Tang, X., & Zhao, K. (2017). Dietary safety assessment of genetically modified rice EH rich in beta-carotene. Regulatory Toxicology and Pharmacology, 88, 66-71. https://doi.org/10.1016/j.yrtph.2017.05.019

Xu, Y., Goodacre, R., & Harrigan, G. G. (2014). Compositional Equivalence of Grain from Multi-trait Drought-Tolerant Maize Hybrids to a Conventional Comparator: Univariate and Multivariate Assessments. Journal of Agricultural and Food Chemistry, 62(39), 9597-9608. https://doi.org/10.1021/jf5019609

Yang, Q. Q., He, X. Y., Wu, H. Y., Zhang, C. Q., Zou, S. Y., Lang, T. Q., Sun, S. S., & Liu, Q. Q. (2017). Subchronic feeding study of high-free-lysine transgenic rice in Sprague-Dawley rats. Food and Chem Toxicology, 105, 214-222. https://doi.org/10.1016/j.fct.2017.04.023

Yuan, Y., Xu, W., He, X., Liu, H., Cao, S., Qi, X., Huang, K., & Luo, Y. (2013). Effects of genetically modified T2A-1 rice on the GI health of rats after 90-day supplement. Scientific Reports, 3(1962), 1962. https://doi.org/10.1038/srep01962

Zeljenková, D., Aláčová, R., Ondrejková, J., Ambrušová, K., Bartušová, M., Kebis, A., Kovrižnych, J., Rollerová, E., Szabová, E., Wimmerová, S., Černák, M., Krivošíková, Z., Kuricová, M., Líšková, A., Spustová, V., Tulinská, J., Levkut, M., Révajová, V., Ševčíková, Z., Schmidt, K., Schmidtke, J., Schmidt, P., La Paz, J. L., Corujo, M., Pla, M., Kleter, G. A., Kok, E. J., Sharbati, J., Bohmer, M., Bohmer, N., Einspanier, R., Adel-Patient, K., Spök, A., Pöting, A., Kohl, C., Wilhelm, R., Schiemann, J., & Steinberg, P. (2016). One-year oral toxicity study on a genetically modified maize MON810 variety in Wistar Han RCC rats (EU 7th Framework Programme project GRACE). Archives of Toxicology, 90(10), 2531-2562. https://doi.org/10.1007/s00204-016-1798-4

Zeljenková, D., Ambrušová, K., Bartušová, M., Kebis, A., Kovrižnych, J., Krivošíková, Z., Kuricová, M., Líšková, A., Rollerová, E., Spustová, V., Szabová, E., Tulinská, J., Wimmerová, S., Levkut, M., Révajová, V., Sevčíková, Z., Schmidt, K., Schmidtke, J., La Paz, J. L., Corujo, M., Pla, M., Kleter, G. A., Kok, E. J., Sharbati, J., Hanisch, C., Einspanier, R., Adel-Patient, K., Wal, J.-M., Spök, A., Pöting, A., Kohl, C., Wilhelm, R., Schiemann, J., & Steinberg, P. (2014). Ninety-day oral toxicity studies on two genetically modified maize MON810 varieties in Wistar Han RCC rats (EU 7th Framework Programme project GRACE). Archives of Toxicology, 88(12), 2289-2314. https://doi.org/10.1007/s00204-014-1374-8

Zhou, X. H., Dong, Y., Xiao, X., Wang, Y., Xu, Y., Xu, B., Shi, W. D., Zhang, Y., Zhu, L. J., & Liu, Q. Q. (2011). A 90-day toxicology study of high-amylose transgenic rice grain in Sprague-Dawley rats. Food and Chem Toxicology, 49(12), 3112-3118. https://doi.org/10.1016/j.fct.2011.09.024

Zhu, Y., Dr, D. L., Wang, F., Yin, J., & Jin, H. (2004). Nutritional assessment and fate of dna of soybean meal from roundup ready or conventional soybeans using rats. Archives of Animal Nutrition, 58(4), 295-310. https://doi.org/10.1080/00039420412331273277

Zhu, Y., He, X., Luo, Y., Zou, S., Zhou, X., Huang, K., & Xu, W. (2013). A 90-day feeding study of glyphosate-tolerant maize with the G2-aroA gene in Sprague-Dawley rats. Food and Chemical Toxicology, 51, 280-287. https://doi.org/10.1016/j.fct.2012.09.008

Zou, S., Huang, K., Xu, W., Luo, Y., & He, X. (2016). Safety assessment of lepidopteran insect-protected transgenic rice with cry2A* gene. Transgenic Research, 25(2), 163-172. https://doi.org/10.1007/s11248-015-9920-6

Zywicki, B., Catchpole, G., Draper, J., & Fiehn, O. (2005). Comparison of rapid liquid chromatography-electrospray ionization-tandem mass spectrometry methods for determination of glycoalkaloids in transgenic field-grown potatoes. Analytical Biochemistry, 336(2), 178-186. https://doi.org/10.1016/j.ab.2004.10.013

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