Skip to main content

Animal feeding studies for nutritional and safety assessments of feeds from genetically modified plants: a review

Abstract

In the future there will be a very strong competition between arable land use for phytogenic biomass production for feed/food, fuel, fibre and other industrial materials, as well as for settlements and natural conservation areas because of the growing population and limited natural resources. Therefore plants with high and stable yields, and requiring low external inputs (low input varieties) should be the main aim of plant breeding. In addition to traditional breeding, plant biotechnology seems to have the potential to contribute to this objective. Nutritional and safety studies with feed/food made from such modified plants are one of the most important prerequisite for public acceptance, and to improve knowledge in the feed/food sciences. The first step for the nutritional and safety assessment of such modified plants is the compositional analysis of potential feed/food, including the newly expressed proteins and other new constituents, and its comparison with conventional counterparts. In vitro studies and experiments with laboratory animals comprise the next steps of the assessment. About 70–90 % of the harvested biomass from genetically modified plants (GMPs) is consumed by food producing animals. Therefore, feeding studies with target animals are of special concern for nutritional assessment, and these are considered in more detail in the present paper. Up to now most studies have been done with GMPs of the 1st generation (plants with input traits, but without substantial changes in composition). Other experimental designs for nutritional and safety assessments are recommended for GMPs with output traits or with substantial changes in composition (plants of the 2nd generation).

Zusammenfassung

Zukünftig ist infolge weiter ansteigender Erdbevölkerung und knapper werdender natürlicher Ressourcen ein noch intensiverer Wettbewerb um landwirtschaftliche Nutzfläche bzw. pflanzliche Biomasse für die Erzeugung von Lebens- und Futtermitteln, Energie, industriellen Rohstoffen als auch um Flächen für Siedlungen und Naturschutz zu erwarten. Deshalb sollte die Entwicklung von Pflanzen mit hohen und stabilen Erträgen bei geringem Ressourceneinsatz (low input varieties) das Hauptziel der Pflanzenzüchtung sein. Neben der traditionellen Pflanzenzüchtung scheint die Pflanzenbiotechnologie ein beachtliches Potenzial zur Realisierung dieser Zielstellung zu haben. Entsprechende Studien zur Bewertung des ernährungsphysiologischen Wertes und der Sicherheit sind eine wesentliche Voraussetzung für die öffentliche Akzeptanz der aus diesen Pflanzen hergestellten Futter- und Lebensmittel. Derartige Studien leisten auch bedeutsame Beiträge zur Verbesserung der Kenntnisse auf dem Gebiet der Futter und Lebensmittelkunde. Der erste Schritt zur ernährungsphysiologischen und Sicherheitsbewertung von Futter-/Lebensmitteln aus gentechnisch veränderten Pflanzen (GVP) ist die Bestimmung der Inhaltsstoffe einschließlich des/der neu ausgeprägten Proteins/e sowie weiterer neu gebildeter Stoffe und der Vergleich mit herkömmlichen (isogenen) Partnern. In vitro Studien und Versuche mit Labortieren sind die nächsten Schritte der Bewertung. Da 70–90 % der von GVP geernteten Biomasse in der Tierernährung eingesetzt werden, sind Fütterungsstudien mit Lebensmittel liefernden Tiere (Zieltieren) von besonderer Bedeutung für die ernährungsphysiologische Bewertung der Futtermittel und werden im Beitrag im Detail betrachtet. Bisher wurden vor allem Fütterungsversuche mit Futtermitteln aus GVP der 1. Generation (ohne wesentliche Veränderungen von Inhaltsstoffen; Pflanzen mit Input traits) durchgeführt. Andere Versuchsansätze sind zur ernährungsphysiologischen und Sicherheitsbewertung von Futter- und Lebensmitteln aus GVP der 2. Generation (Pflanzen mit substantiellen Veränderungen von Inhaltsstoffen; Pflanzen mit Output traits) erforderlich.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Alexander TW, Reuter T, Aulrich K, Sharma R, Okine EK, Dixon WT, McAllister TA (2007) A review of the detection and fate of novel plant molecules derived from biotechnology in livestock production. Anim Feed Sci Technol 133:31–62

    Article  CAS  Google Scholar 

  • ANSES (Agence nationale de sécurité sanitaire de l’alimentation, de l’environnement et du travail) (2011) Opinion of the French Agency for Food, Environmental and Occupational Health and Safety—recommendation of carrying our statistical analyses of data from 90-day rat feeding studies in the context of marketing authorisation applications for GM organisms. Request no 2009-SA-0285

  • Aumaitre A, Aulrich K, Chesson A, Flachowsky G, Piva G (2002) New feeds from genetically modified plants: Substantial equivalence, nutritional equivalence, digestibility, and safety for animals and the food chain. Livest Prod Sci 74:223–238

    Article  Google Scholar 

  • Baranowski A, Rosochacki S, Parada R, Jaszczak K, Zimny J, Poloszynowicz J (2006) The effect of diet containing modified triticale on growth and transgenic DNA fate in selected tissues of mice. Anim Sci Pap Rep 24:129–142

    CAS  Google Scholar 

  • BEETLE (2009) Long-term effects of genetically modified (GM) crops on health and the environment (including biodiversity), Executive Summary and Main Report. Federal Office of Consumer Protection and Food Safety (BVL), BLaU-Umweltstudien and Genius GmbH, Berlin

  • Bernal-Santos B, O`Donell SM, Vicine JL, Hartnell GF, Bauman DE (2010) Hot topic: enhancing omega-3 fatty acids in milk fat of dairy cows by using stearidonic acid-enriched soybean oil from genetically modified soybeans. J Dairy Sci 93:32–37

    Article  PubMed  CAS  Google Scholar 

  • Brake DE, Evenson DP (2004) A generational study of glyphosate-tolerant soybeans on mouse fetal, postnatal and adult testicular development. Food Chem Toxicol 42:29–36

    Article  PubMed  CAS  Google Scholar 

  • 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 52:2097–2102

    Article  PubMed  CAS  Google Scholar 

  • Brookes G, Barfoot P (2008) GMcrop: global socio-economic and environmental impacts 1996–2006. PG Economics Ltd, Dorchester

  • CAST (2006) Safety of meat, milk, and eggs from animals fed crops derived from modern biotechnology. No 34

  • Cellini F, Chesson A, Coquhonn I, Constable A, Davies HV, Engel K-H, Gatehouse AMR, Kärenlampi S, Kok EJ, Legnay JJ, Lehesranta S, Noteborn HPJM, Pedersen J, Smith M (2004) Unintended effects and their detection in genetically modified crops. Food Chem Toxicol 42:1089–1123

    Article  PubMed  CAS  Google Scholar 

  • Clark JH, Ipharraguerre IR (2001) Livestock performance: feeding biotech crops. J Dairy Sci 84(E. Suppl. E9–E18):237–249

  • Davis HV, Kuiper HA (2011) GM-risk assessment in the EU: Current perspective. Aspects Appl Biol 110:37–45

    Google Scholar 

  • DBT (Department Biotechnology) (2008) Protocols for food and feed safety assessment of GE crops. Dept. of Biotechn., Min. Science and Technol., India

  • Delaney B, Astwood JD, Cunny H (2008) Evaluation of protein safety in the context of agricultural biotechnology. Food Chem Toxicol 46:S71–S97

    PubMed  CAS  Google Scholar 

  • DLG (2012) DLG-Datenbank Futtermittel (database feedstuffs). http://www.dlg.org/futtermitteldatenbank.html

  • EFSA (European Food Safety Authority) (2006) Guidance document of the Scientific Panel on Genetically Modified Organisms for the risk assessment of genetically modified plants and derived food and feed. EFSA J 99:1–100

    Google Scholar 

  • EFSA (European Food Safety Authority) (2008) Safety and nutritional assessment of GM plant derived food and feed. The role of animal feeding trials. Food Chem Toxicol 46:2–70

    Google Scholar 

  • EFSA (European Food Safety Authority) (2011b) Scientific opinion on EFSA guidance on repeated-dose 90-day oral toxicity study in rodents on whole food/feed. EFSA J 9(12):2438

    Google Scholar 

  • EFSA Panel on Genetically Modified Organisms (GMO) (2011a) Scientific opinion on guidance for risk assessment of food and feed from genetically modified plants. EFSA J 9(5):2150

    Google Scholar 

  • FAO (Food and Agricultural Organisation of the UN) (2009) The state of food and agriculture. Livestock in the balance. Rome

  • FDA (Food and Drug Administration; Redbook) (2000) Guidance for industry and other stakeholders, toxicological principles for the safety assessment of food ingredients. U.S. Department of Health and Human Services, Food and Drug Administration, Centre for Food Safety and Applied Nutrition. http://www.cfsan.fda.gov/guidance.html

  • Flachowsky G (ed) (2006) Possibilities of decontamination of “Undesirable substances of Annex 5 of the Feed Law (2006)”. Landbauforschung Völkenrode – FAL Agric Res, Spec. Issue 294 (in German)

  • Flachowsky G (2008) What do animal nutritionists expect from plant breeding? Outlook Agric 37:95–103

    Article  Google Scholar 

  • Flachowsky G (2010) Global food security: is there any solution? NovoArgumente 105(3–4):64–68 (in German)

    Google Scholar 

  • Flachowsky G, Aulrich K (2001) Nutritional assessment of GMO in animal nutrition. J Anim Feed Sci 10(Suppl. 1):181–194

    Google Scholar 

  • Flachowsky G, Böhme H (2005) Proposals for nutritional assessments of feed from genetically modified plants. J Anim Feed Sci 14:49–70

    Google Scholar 

  • Flachowsky G, Chesson A, Aulrich K (2005a) Animal nutrition with feeds from genetically modified plants. Arch Anim Nutr 59:1–40

    Article  PubMed  Google Scholar 

  • Flachowsky G, Halle I, Aulrich K (2005b) Long term feeding of Bt-corn—a ten generation study with quails. Arch Anim Nutr 59:449–451

    Article  PubMed  Google Scholar 

  • Flachowsky G, Aulrich K, Böhme H, Halle I (2007) Studies on feeds from genetically modified plants (GMP) contributions to nutritional and safety assessment. Anim Feed Sci Technol 133:2–30

    Article  CAS  Google Scholar 

  • Foley JA, Ramankutty N, Brauman KA, Cassidy ES, Gerber JS (2011) Solutions for a cultivated planet. Nature 478:337–342

    Article  PubMed  CAS  Google Scholar 

  • Forster IP, Dominy WG, Obaldo LC, Hartnell GF, Sanders EF, Hickman TC, Ruebelt MC (2011) The effect of soybean oil containing stearidonic acid on growth performance, n-3 fatty acid deposition and sensory characteristics of pacific white shrimp (Litopenaeus vannamei). Aquacult Nutr 17:200–213

    Article  CAS  Google Scholar 

  • FSANS (2007) The role of animal feeding studies in the safety assessment of genetically modified foods. Rep. Workshop of Food Standards Australia New Zealand, Canberra

  • Gibbs RA, Rymer C, Givens DI (2010) Long-chain n-3 PUFA intakes in the UK and the potential of a chicken meat prototype to increase them. Proc Nutr Soc 69:144–155

    Article  PubMed  CAS  Google Scholar 

  • Godfray HCJ, Beddington JR, Crute IR, Haddad L, Wawrence D, Muir J, Pretty J, Robinson S, Thomas SM, Toulmin C (2010) Food security: the challenge of feeding 9 billion people. Science 327:812–818

    Article  PubMed  CAS  Google Scholar 

  • Halle I, Aulrich K, Flachowsky G (2006) Four generations feeding GMO-corn to laying hens. Proc Soc Nutr Physiol 15:114 (Abstr.)

    Google Scholar 

  • Howe JA, Tanumihardjo SA (2006) Cartenoid-biofortified maize maintains adequate vitamin A status in Mongolian gerbils. J Nutr 136:2562–2567

    PubMed  CAS  Google Scholar 

  • ILSI (2003a) Best practices for the conduct of animal studies to evaluate crops genetically modified for input traits. International Life Sciences Institute, Washington, D.C. http//www.ilsi.org/file/bestpracticescas.pdf

  • ILSI (2003b) Crop compositional database. Accessed 2003 July 14; Update 2009

  • ILSI (2007) Best practices for the conduct of animal studies to evaluate crops genetically modified for output traits. Int Life Sci Inst, Washington DC

    Google Scholar 

  • James C (2012) Global status of commercialized biotech/GM crops: 2011. ISAAA Brief No. 43. ISAAA, Ithaca

  • Kilic A, Akay MT (2008) A three generation study with genetically modified Bt corn in rats: biochemical and histopathological investigation. Food Chem Toxicol 46:1164–1170

    Article  PubMed  CAS  Google Scholar 

  • Kitessa SM, Young P (2011) Enriched milk fat with n-3 polyunsaturated fatty acids by supplementing grazing dairy cows with ruminally protected echium oil. Anim Feed Sci Technol 170:35–44

    Article  CAS  Google Scholar 

  • Kleter GA, Kok EJ (2010) Safety assessment of biotechnology used in animal production, including genetically modified (GM) feed and GM animals—a review. Anim Sci Pap Rep 28:105–114

    Google Scholar 

  • Kok E, Kuiper H (2003) Comparative safety assessment of biotech crops. Trends Biotechnol 21:439–444

    Article  PubMed  CAS  Google Scholar 

  • Kok EJ, Keijer J, Kleter GA, Kuiper HA (2008) Comparative safety assessment of plant-derived feeds. Reg Toxicol Pharmacol 50:98–113

    Article  CAS  Google Scholar 

  • Krzyzowska M, Wincenciak M, Winnicka A, Baranowski A, Jaszczak K, Zimny J, Niemialtowski M (2010) The effect of multigenerational diet containing genetically modified triticale on immune system in mice. Polish J Vet Sci 13:423–430

    CAS  Google Scholar 

  • Ladics GS, Knippels LM, Penninks AH (2010) Review of animal models to predict the potential allergenicity of novel proteins in genetically modified crops. Regul Toxicol Pharmacol 56:212–224

    Article  PubMed  CAS  Google Scholar 

  • Mazza R, Soave M, Morlacchini M, Piva G, Marocco A (2005) Assessing the transfer of genetically modified DNA from feed to animal tissues. Transgenic Res 14:775–785

    Article  PubMed  CAS  Google Scholar 

  • Meja L, Jacobs CM, Utterback PL, Parsons CM, Rice D, Sanders C, Smith B, Iiams C, Sauber T (2010) Evaluation of the nutritional equivalency of soybean meal with the genetically modified trait DP-3O5423-1 when fed to laying hens. Poultry Sci 89:2634–2639

    Article  Google Scholar 

  • Nemeth A, Wurz A, Artim L, Charlton S, Dana G, Glenn K, Hunst P, Jennings I, Shilto R, Song P (2004) Sensitive PCR analysis of animal tissue samples for fragments of endogenous and transgenic plant DNA. J Agric Food Chem 52:6129–6135

    Article  PubMed  CAS  Google Scholar 

  • NRC (National Research Council) (1995) Nutrient requirements for laboratory animals. Forth revised ed., National Academy Press, Washington, DC

  • OECD (1993) Safety evaluation of foods derived by modern biotechnology. Concepts and principles. OECD, Paris

    Google Scholar 

  • OECD (1998a) OECD guidelines for the testing of chemicals—Repeated dose 28-day oral toxicity study in rodents, 407. http://browse.oecbookshop.org/oecd/pdfs/free/9740701e.pdf

  • OECD (1998b) Guideline for the testing of chemicals—repeated dose 90-day oral toxicity study in rodents, 408. http://browse.oecdbookshop.org/oecd/pdfs/free/9740801e.pdf

  • OECD (2001a) Series on the safety of novel foods and feeds no. 1. Consensus document on key nutrients and key toxicants in low erucic acid rapeseed (canola). OECD, Paris

  • OECD (2001b) Series on the safety of novel foods and feeds no. 2: Consensus document on compositional considerations for new varieties of soybean: key food and feed nutrients and anti-nutrients. OECD, Paris

  • OECD (2003) Series on the safety of novel foods and feeds no. 7: consensus document on compositional considerations for new varieties of bread wheat (Triticum aestivum): key food and feed nutrients, anti-nutrients and toxicants. OECD, Paris

  • OECD (2004a) Series on the afety of novel foods and feeds no. 10: consensus document on compositional considerations for new varieties of rice (Oryza sativa): key food and feed nutrients and anti-nutrients. OECD, Paris

  • OECD (2004b) Series on the safety of novel foods and feeds no. 11: consensus document on compositional considerations for new varieties of cotton (Gossypium hirsutum and Gossypium barbadense): key food and feed nutrients and anti-nutrients. OECD, Paris

  • OECD (2004c) Series on the safety of novel foods and feeds no. 12: consensus document on compositional considerations for new varieties of barley (Hordeum vulgare L.): key food and feed nutrients and anti-nutrients. OECD, Paris

  • Rhee GS, Cho DH, Won YH, Soek JH, Kim SS, Kwack SJ, Lee RD, Chae SY, Kim JW, Lee BM, Park KL, Choi KS (2005) Multigeneration reproductive and developmental toxicity study of bar gene inserted intogenetically modified potato on rats. J Toxicol Environ Health 68:2263–2276

    Article  CAS  Google Scholar 

  • Russell WMS, Burch RL (1959) The principles of humane experimental technique, Special Ed., Universities Fed. for Animal Welfare, Potters Bar

  • Rymer C, Hartnell GF, Givens DI (2011) The effect of feeding modified soyabean oil enriched with C18:4 n-3 to broilers on the deposition of n-3 fatty acids in chicken meat. Br J Nutr 105:866–878

    Article  PubMed  CAS  Google Scholar 

  • SCAR (EU Commission—Standing Committee on Agricultural Research (2008) New challenges for agricultural research. Climate change, rural development, agricultural knowledge systems. The 2nd SCAR Foresight Exercise, Brussels

  • Seralini GE, Mesnage R, Clair E, Gress S, de Vendomois JS, Cellier D (2011) Genetically modified crops safety assessments: present limits and possible improvements. Environ Sci Eur 23:10

    Article  Google Scholar 

  • Sharma R, Damgaard D, Alexander TW, Dugan MER, Aalhus JL, Stanford K, McAllister TA (2006) Detection of transgenic and endogenous plant DNA in digesta and tissues of sheep and pigs fed Roundup Ready canola meal. J Agric Food Chem 54:1699–1709

    Article  PubMed  CAS  Google Scholar 

  • Snell C, Bernheim A, Bergé JB, Kuntz M, Gerard P, Paris A, Ricroch AE (2012) Assessment of the health impact of GM plant diets in long-term and multigenerational animal feeding trials. A literature review. Food Chem 50:1134–1148

    Article  CAS  Google Scholar 

  • Spencer JD, Allee GL, Sauber TE (2000) Phosphorus bioavailability and digestibility of normal and genetically modified low-phytate com for pigs. J Anim Sci 78:675–681

    PubMed  CAS  Google Scholar 

  • Spiekers H, Meyer HHD, Schwarz FJ (2009) Effects of long term utilization of genetically modified maize (MON 810) in dairy cattle feeding on performance and metabolism parameters. Schriftenreihe, Bayerische Landesanstalt für Landwirtschaft (LfL), vol 18 (in German)

  • Stein AJ, Rodriguez-Cerezo E (2009) The global pipeline of new GM-crops. JRC/ipts, EUR 23496 EN

  • Steinfeld H, Gerber P, Wassenaar T, Castel V, Rosales M, de Haan C (2006) Livestock’s long shadow: environmental issues and options. Food and Agric Organization of the United Nations (FAO), Rome

    Google Scholar 

  • Tang G, Qin J, Dolnikowski GG, Russell RM, Grusak MA (2009) Golden rice in an effective source of vitamin A. Am J Clin Nutr 89:1776–1783

    Article  PubMed  CAS  Google Scholar 

  • The Royal Society (2009) Reaping the benefits: Science and the sustainable intensification of global agriculture. RS policy document 11/09, issued Oct. 2009 RS 1608. ISBN: 978-0-85403-784-1

  • Trabalza-Marinucci M, Brandi G, Rondine C, Avelini L, Giammarini C, Costarelli S, Acuti G, Orlandi C, Filippini G, Chiradia E, Malatesta M, Crotti S, Antonini C, Amagliani G, Manuali E, Mastrogiacomo AR, Moscati L, Haounet MN, Gaiti A, Magnani M (2008) A three-year longitudinal study on the effects of a diet containing genetically modified Bt176 maize on the health status and performance of sheep. Livest Sci 113:178–190

    Article  Google Scholar 

  • Tudisco R, Mastellone V, Cutrignelli MI, Lombardi P, Bovera F, Mirabella N, Piccolo G, Calabro S, Avallone L, Infascelli F (2010) Fate of transgenic DNA and metabolic effects in goats fed genetically modified soybean and in their offsprings. Animal 4:1662–1671

    Article  PubMed  CAS  Google Scholar 

  • Ursin VM (2003) Modification of plant lipids for human health: development of functional land-based omega-3 fatty acids. J Nutr 133:4271–4274

    PubMed  CAS  Google Scholar 

  • Whelan J (2009) Dietary stearidonic acid is a long chain (n-3) polyunsaturated fatty acid with potential health benefits. J Nutr 139:5–10

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gerhard Flachowsky.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Flachowsky, G., Schafft, H. & Meyer, U. Animal feeding studies for nutritional and safety assessments of feeds from genetically modified plants: a review. J. Verbr. Lebensm. 7, 179–194 (2012). https://doi.org/10.1007/s00003-012-0777-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00003-012-0777-9

Keywords