Guidance on the environmental risk assessment of genetically modified plants

EFSA Panel on Genetically Modified Organisms (GMO)

doi:10.2903/j.efsa.2010.1879

Cited by 428Genetically Modified Organisms ResearchAgricultural safety and regulationsRisk Perception and Management

Guidance on the environmental risk assessment of genetically modified plants

Open access

EFSA Panel on Genetically Modified Organisms (GMO)·2010·EFSA Journal

DOI 10.2903/j.efsa.2010.1879PMC PMC13129916

Open this paper in CoChat — free account

Abstract

This document provides guidance for the environmental risk assessment (ERA) of genetically modified (GM) plants submitted within the framework of Regulation (EC) No. 1829/2003 on GM food and feed or under Directive 2001/18/EC on the deliberate release into the environment of genetically modified organisms (GMOs). This document provides guidance for assessing potential effects of GM plants on the environment and the rationales for the data requirements for a comprehensive ERA of GM plants. The ERA should be carried out on a case-by-case basis, following a step-by-step assessment approach. This document describes the six steps for the ERA of GM plants, as indicated in Directive 2001/18/EC, starting with (1) problem formulation including hazard identification; (2) hazard characterisation; (3) exposure characterisation; (4) risk characterisation; (5) risk management strategies; and (6) an overall risk evaluation. The scientific Panel on Genetically Modified Organisms (of the European Food Safety Authority (EFSA GMO Panel) considers seven specific areas of concern to be addressed by applicants and risk assessors during the ERA (1) persistence and invasiveness of the GM plant, or its compatible relatives, including plant-to-plant gene transfer; (2) plant-to-micro-organism gene transfer; (3) interaction of the GM plant with target organisms and (4) interaction of the GM plant with non-target organisms, including criteria for selection of appropriate species and relevant functional groups for risk assessment; (5) impact of the specific cultivation, management and harvesting techniques; including consideration of the production systems and the receiving environment(s); (6) effects on biogeochemical processes; and (7) effects on human and animal health. Each specific area of concern is considered in a structured and systematic way following the above-mentioned steps (1 to 6). In addition, the guidance document is supplemented with several general cross-cutting considerations (e.g. choice of comparator, receiving environment(s), general statistical principles, long-term effects) that need to be considered in the ERA.

Integrity signals

Registry

Crossref · 10.2903/j.efsa.2010.1879

Cites

137 of 137 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

The data available do not support the proposal that in-planta studies are needed to fully assess Bt-plant effects on natural enemies.
“Thus, the data available do not support the proposal by some scientists (Arpaia et al., 2017) and the European Food Safety Authority (EFSA) (EFSA, 2010) that in-planta studies are needed to fully assess the Bt-plant effects on natural enemies (see Devos et al., 2016 for detailed discussion).”
From Genetically engineered crops help support conservation biological control (2019) · cites this paper as EFSA, 2010

Ecosystems and Human Well-being: Synthesis
Assessment, M. E. (2005) · Island Press · doi:10.5281/zenodo.18167309 · Cited by 10,665 · see citing works
A comparison of the Two One-Sided Tests Procedure and the Power Approach for assessing the equivalence of average bioavailability
Schuirmann, D. J. (1987) · Journal of Pharmacokinetics and Biopharmaceutics · doi:10.1007/bf01068419 · Cited by 2,696 · see citing works
Uncertainty
Morgan, M. G., & Henrion, M. (1990) · Cambridge University Press eBooks · doi:10.1017/cbo9780511840609 · Cited by 1,711 · see citing works
Structure and Function of Stream Ecosystems
Cummins, K. W. (1974) · BioScience · doi:10.2307/1296676 · Cited by 1,413 · cited 1× · see citing works
“Functional groups: are defined as non-phylogenetic, aggregated units of species sharing an important ecological characteristic and playing an equivalent role in the community (Cummins, 1974, Smith, 1997, Steneck, 2001, Blondel, 2003).”
Biotechnology in agriculture and forestry
Bajaj, Y. P. S. (1989) · Cited by 1,052 · see citing works
Insect resistance to Bt crops: evidence versus theory
Tabashnik, B. E., Gassmann, A. J., Crowder, D. W., & Carrière, Y. (2008) · Nature Biotechnology · doi:10.1038/nbt1382 · Cited by 780 · see citing works
Rectangular and hexagonal grids used for observation, experiment and simulation in ecology
Birch, C., Oom, S. P., & Beecham, J. A. (2007) · Ecological Modelling · doi:10.1016/j.ecolmodel.2007.03.041 · Cited by 667 · see citing works
Discovery and Characterization of Field Resistance to Bt Maize: Spodoptera frugiperda (Lepidoptera: Noctuidae) in Puerto Rico
Storer, N. P., Babcock, J. M., Schlenz, M., Meade, T., Thompson, G. D., Bing, J. W., & Huckaba, R. M. (2010) · Journal of Economic Entomology · doi:10.1603/ec10040 · Cited by 641 · see citing works
Pesticide resistance: Strategies and tactics for management
Brown, K. (1987) · Trends in Ecology & Evolution · doi:10.1016/0169-5347(87)90102-9 · Cited by 634 · see citing works
Release and persistence of extracellular DNA in the environment
Nielsen, K. M., Johnsen, P. J., Bensasson, D., & Daffonchio, D. G. (2007) · Environmental Biosafety Research · doi:10.1051/ebr:2007031 · Cited by 616 · see citing works
Scientific Opinion on the assessment of allergenicity of GM plants and microorganisms and derived food and feed
Panel), E. P. O. G. M. O. (. (2010) · EFSA Journal · doi:10.2903/j.efsa.2010.1700 · Cited by 610 · see citing works
Assessment of risk of insect-resistant transgenic crops to nontarget arthropods
Romeis, J., Bartsch, D. K., Bigler, F., Candolfi, M. P., Gielkens, M. M. C., Hartley, S. E., Hellmich, R. L., Huesing, J. E., JEPSON, P. C., Layton, R. J., et al. (2008) · Nature Biotechnology · doi:10.1038/nbt1381 · Cited by 501 · see citing works
Guilds or functional groups: does it matter?
Blondel, J. (2003) · Oikos · doi:10.1034/j.1600-0706.2003.12152.x · Cited by 458 · see citing works
Farmland Biodiversity and the Footprint of Agriculture
Butler, S. J., Vickery, J. A., & Norris, K. J. (2007) · Science · doi:10.1126/science.1136607 · Cited by 445 · see citing works
A Meta-Analysis of Effects of Bt Cotton and Maize on Nontarget Invertebrates
Marvier, M., McCreedy, C., Regetz, J., & Kareiva, P. (2007) · Science · doi:10.1126/science.1139208 · Cited by 445 · see citing works
Plant Functional Types: Their Relevance to Ecosystem Properties and Global Change
Hicks, D., Smith, T. M., Shugart, H. H., & Woodward, F. I. (1998) · Systematic Botany · doi:10.2307/2419578 · Cited by 428 · see citing works
Rapid evolution in plant chitinases: Molecular targets of selection in plant-pathogen coevolution
Bishop, J. G., Dean, A. M., & Mitchell‐Olds, T. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.10.5322 · Cited by 366 · see citing works
First report of field resistance by the stem borer, Busseola fusca (Fuller) to Bt-transgenic maize
van Rensburg, J. B. J. (2007) · South African Journal of Plant and Soil · doi:10.1080/02571862.2007.10634798 · Cited by 334 · see citing works
Initial frequency of alleles for resistance to Bacillus thuringiensis toxins in field populations of Heliothis virescens
Gould, F. L., Anderson, A., Jones, A., Sumerford, D. V., Heckel, D. G., López, J. D., Micinski, S., Leonard, R., & Laster, M. L. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.8.3519 · Cited by 330 · see citing works
Global pesticide resistance in arthropods
(2008) · CABI eBooks · doi:10.1079/9781845933531.0000 · Cited by 327 · see citing works
Testing Statistical Hypotheses of Equivalence
Wellek, S. (2002) · Chapman & Hall/CRC eBooks · doi:10.1201/9781420035964 · Cited by 323 · see citing works
Ecology of transgenic oilseed rape in natural habitats
Crawley, M. J., Hails, R. S., Rees, M., et al. (1993) · Nature · doi:10.1038/363620a0 · Cited by 319 · see citing works
Dangerous liaisons?: when cultivated plants mate with their wild relatives
(2004) · Choice Reviews Online · doi:10.5860/choice.41-4658 · Cited by 308 · see citing works
F2 Screen for Rare Resistance Alleles
Andow, D. A., & Alstad, D. N. (1998) · Journal of Economic Entomology · doi:10.1093/jee/91.3.572 · Cited by 308 · see citing works
A new European Landscape Classification (LANMAP): A transparent, flexible and user-oriented methodology to distinguish landscapes
Mücher, C. A., Klijn, J. A., Wascher, D. M., & Schaminée, J. H. J. (2009) · Ecological Indicators · doi:10.1016/j.ecolind.2009.03.018 · Cited by 300 · see citing works
The analysis of ordered categorical data: An overview and a survey of recent developments
Liu, I., & Agresti, A. (2005) · Test · doi:10.1007/bf02595397 · Cited by 299 · see citing works
Do escaped transgenes persist in nature? The case of an herbicide resistance transgene in a weedy Brassica rapa population
Warwick, S. I., Légère, A., Simard, M., & James, T. (2007) · Molecular Ecology · doi:10.1111/j.1365-294x.2007.03567.x · Cited by 298 · see citing works
Strategies for antiviral resistance in transgenic plants
Prins, M., Laimer, M., Noris, E., et al. (2007) · Molecular Plant Pathology · doi:10.1111/j.1364-3703.2007.00447.x · Cited by 295 · see citing works
Improving the Content of Essential Amino Acids in Crop Plants: Goals and Opportunities
Ufaz, S., & Galili, G. (2008) · PLANT PHYSIOLOGY · doi:10.1104/pp.108.118091 · Cited by 268 · see citing works
Transgenic crops in natural habitats
Crawley, M. J., Brown, S. L., Hails, R. S., Kohn, D. D., & Rees, M. (2001) · Nature · doi:10.1038/35055621 · Cited by 252 · see citing works
Genetic engineering of plants to enhance resistance to fungal pathogensa review of progress and future prospects
Punja, Z. K. (2001) · Canadian Journal of Plant Pathology · doi:10.1080/07060660109506935 · Cited by 239 · see citing works
Responses of plants and invertebrate trophic groups to contrasting herbicide regimes in the Farm Scale Evaluations of genetically modified herbicide–tolerant crops
The American Association for Research into Nervous and Mental Diseases, Hawes, C., Haughton, A. J., et al. (2003) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2003.1406 · Cited by 235 · see citing works
Nutritionally Improved Agricultural Crops
Newell‐McGloughlin, M. (2008) · PLANT PHYSIOLOGY · doi:10.1104/pp.108.121947 · Cited by 215 · see citing works
An introduction to the Farm‐Scale Evaluations of genetically modified herbicide‐tolerant crops
Firbank, L. G., Heard, M. S., Woiwod, I. P., et al. (2003) · Journal of Applied Ecology · doi:10.1046/j.1365-2664.2003.00787.x · Cited by 204 · see citing works
Costs of transgenic herbicide resistance introgressed from Brassica napus into weedy B. rapa
Snow, A. A., Andersen, B. A., & Jørgensen, R. B. (1999) · Molecular Ecology · doi:10.1046/j.1365-294x.1999.00596.x · Cited by 202 · see citing works
Problem formulation in the environmental risk assessment for genetically modified plants
Wolt, J. D., Keese, P. K., Raybould, A. F., Fitzpatrick, J. W., Burachik, M., Gray, A. J., Olin, S. S., Schiemann, J., Sears, M. K., & Wu, F. (2009) · Transgenic Research · doi:10.1007/s11248-009-9321-9 · Cited by 192 · see citing works
Gene Flow, Invasiveness, and Ecological Impact of Genetically Modified Crops
Warwick, S. I., Beckie, H. J., & Hall, L. M. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04576.x · Cited by 184 · see citing works
Scientific Opinion on the development of specific protection goal options for environmental risk assessment of pesticides, in particular in relation to the revision of the Guidance Documents on Aquatic and Terrestrial Ecotoxicology (SANCO/3268/2001 and SA
(PPR), E. P. O. P. P. P. A. T. R. (2010) · EFSA Journal · doi:10.2903/j.efsa.2010.1821 · Cited by 180 · see citing works
Weeds in fields with contrasting conventional and genetically modified herbicide–tolerant crops. I. Effects on abundance and diversity
The American Association for Research into Nervous and Mental Diseases, Heard, M. S., Hawes, C., et al. (2003) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2003.1402 · Cited by 179 · see citing works
Risks from GMOs due to horizontal gene transfer.
Keese, P. (2008) · Environmental Biosafety Research · doi:10.1051/ebr:2008014 · Cited by 175 · see citing works
Agricultural Field Experiments
Petersen, R. G. (1994) · CRC Press eBooks · doi:10.1201/9781482277371 · Cited by 174 · see citing works
Hybridisation within Brassica and allied genera: evaluation of potential for transgene escape
FitzJohn, R. G., Armstrong, T., Newstrom‐Lloyd, L. E., et al. (2007) · Euphytica · doi:10.1007/s10681-007-9444-0 · Cited by 171 · see citing works
The impact of transgenic plants on natural enemies: a critical review of laboratory studies
Löveï, G. L., & Arpaia, S. (2005) · Entomologia Experimentalis et Applicata · doi:10.1111/j.0013-8703.2005.00235.x · Cited by 170 · see citing works
A Comparison of Acute Mortality and Population Growth Rate as Endpoints of Toxicological Effect
Walthall, W. K., & Stark, J. D. (1997) · Ecotoxicology and Environmental Safety · doi:10.1006/eesa.1997.1521 · Cited by 159 · see citing works
Enhancing Plant Seed Oils for Human Nutrition
Damude, H. G., & Kinney, A. J. (2008) · PLANT PHYSIOLOGY · doi:10.1104/pp.108.121681 · Cited by 152 · see citing works
Design, analysis and statistical power of the Farm‐Scale Evaluations of genetically modified herbicide‐tolerant crops
PERRY, J. N., ROTHERY, P., Clark, S. J., Heard, M. S., & Hawes, C. (2003) · Journal of Applied Ecology · doi:10.1046/j.1365-2664.2003.00786.x · Cited by 150 · see citing works
Delaying insect resistance to transgenic crops
Tabashnik, B. E. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0810763106 · Cited by 146 · see citing works
The Benefits of Probabilistic Exposure Assessment: Three Case Studies Involving Contaminated Air, Water, and Soil1
Finley, B. L., & Paustenbach, D. J. (1994) · Risk Analysis · doi:10.1111/j.1539-6924.1994.tb00028.x · Cited by 145 · see citing works
Perspective on the development of stem borer resistance to Bt maize and refuge compliance at the Vaalharts irrigation scheme in South Africa
Kruger, M., van Rensburg, J. B. J., & den Berg, J. V. (2009) · Crop Protection · doi:10.1016/j.cropro.2009.04.001 · Cited by 144 · see citing works
Problem formulation and hypothesis testing for environmental risk assessments of genetically modified crops
Raybould, A. F. (2006) · Environmental Biosafety Research · doi:10.1051/ebr:2007004 · Cited by 143 · see citing works
R ISK A SSESSMENT OF V IRUS-RESISTANT T RANSGENIC P LANTS
Tepfer, M. M. (2002) · Annual Review of Phytopathology · doi:10.1146/annurev.phyto.40.120301.093728 · Cited by 142 · see citing works
Can Population Effects of Pesticides Be Predicted from Demographic Toxicological Studies?
Stark, J. D., & Wennergren, U. (1995) · Journal of Economic Entomology · doi:10.1093/jee/88.5.1089 · Cited by 142 · see citing works
Field-evolved resistance to Bt toxins
Moar, W., Roush, R., Shelton, A. M., Ferré, J., Macintosh, S. C., Leonard, B. R., & Abel, C. A. (2008) · Nature Biotechnology · doi:10.1038/nbt1008-1072 · Cited by 136 · see citing works
On the rationale and interpretation of the Farm Scale Evaluations of genetically modified herbicide-tolerant crops
The American Association for Research into Nervous and Mental Diseases, Squire, G. R., Brooks, D. R., Bohan, D. A., Champion, G. T., Daniels, R. E., Haughton, A. J., Hawes, C., Heard, M. S., Hill, M. O., et al. (2003) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2003.1403 · Cited by 135 · see citing works
Frequency of alleles conferring resistance to Bt maize in French and US corn belt populations of the European corn borer, Ostrinia nubilalis
Bourguet, D., Chaufaux, J., Séguin, M., Buisson, C., Hinton, J. L., Stodola, T. J., Porter, P., Cronholm, G. B., Buschman, L. L., & Andow, D. A. (2002) · Theoretical and Applied Genetics · doi:10.1007/s00122-002-1172-1 · Cited by 132 · see citing works
Crop management and agronomic context of the Farm Scale Evaluations of genetically modified herbicide–tolerant crops
The American Association for Research into Nervous and Mental Diseases, Champion, G. T., May, M. J., Bennett, S., Brooks, D. R., Clark, S. J., Daniels, R. E., Firbank, L. G., Haughton, A. J., Hawes, C., et al. (2003) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2003.1405 · Cited by 128 · see citing works
Extrapolating non-target risk of Bt crops from laboratory to field
Duan, J. J., Lundgren, J. G., Naranjo, S., & Marvier, M. (2010) · Biology Letters · doi:10.1098/rsbl.2009.0612 · Cited by 127 · see citing works
Crop-to-wild gene flow, introgression and possible fitness effects of transgenes
Jenczewski, E., Ronfort, J., & Chèvre, A. (2003) · Environmental Biosafety Research · doi:10.1051/ebr:2003001 · Cited by 125 · see citing works
Resistance monitoring of field populations of the corn borers Sesamia nonagrioides and Ostrinia nubilalis after 5 years of Bt maize cultivation in Spain
Farinós, G. P., de la Poza, M., Hernández‐Crespo, P., Ortego, F., & Castañera, P. (2003) · Entomologia Experimentalis et Applicata · doi:10.1111/j.0013-8703.2004.00116.x · Cited by 119 · see citing works
How Governmental Regulation Can Help or Hinder the Integration of Bt Crops within IPM Programs
Matten, S. R., Head, G., & Quemada, H. D. (2008) · Springer eBooks · doi:10.1007/978-1-4020-8373-0_2 · Cited by 116 · see citing works
Ecological versus ecotoxicological methods for assessing the environmental risks of transgenic crops
Raybould, A. F. (2007) · Plant Science · doi:10.1016/j.plantsci.2007.09.003 · Cited by 116 · see citing works
Functional ecological genomics to demonstrate general and specific responses to abiotic stress
Roelofs, D., Aarts, M. G. M., Schat, H., & van Straalen, N. M. (2007) · Functional Ecology · doi:10.1111/j.1365-2435.2007.01312.x · Cited by 115 · see citing works
Effects on weed and invertebrate abundance and diversity of herbicide management in genetically modified herbicide-tolerant winter-sown oilseed rape
Bohan, D. A., Boffey, C., Brooks, D. R., et al. (2005) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2004.3049 · Cited by 114 · see citing works
Impact of farm-scale Bt maize on abundance of predatory arthropods in Spain
de la Poza, M., Pons, X., Farinós, G. P., López, C., Ortego, F., Eizaguirre, M., Castañera, P., & Albajes, R. (2005) · Crop Protection · doi:10.1016/j.cropro.2004.12.003 · Cited by 111 · see citing works
Burial and seed survival in Brassica napus subsp. oleifera and Sinapis arvensis including a comparison of transgenic and non–transgenic lines of the crop
Hails, R. S., Rees, M., Kohn, D. D., et al. (1997) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1997.0001 · Cited by 102 · see citing works
Non‐inferiority trials: the ‘at least as good as’ criterion
Laster, L. L., & Johnson, M. F. K. (2002) · Statistics in Medicine · doi:10.1002/sim.1137 · Cited by 101 · see citing works
Crop ferality: Implications for novel trait confinement
Bagavathiannan, M., & Acker, R. C. V. (2008) · Agriculture Ecosystems & Environment · doi:10.1016/j.agee.2008.03.009 · Cited by 92 · see citing works
IMPROVING RISK ASSESSMENT FOR NONTARGET SAFETY OF TRANSGENIC CROPS
Marvier, M. (2002) · Ecological Applications · doi:10.1890/1051-0761(2002)012[1119:irafns]2.0.co;2 · Cited by 92 · see citing works
A mathematical model of exposure of non-target Lepidoptera toBt-maize pollen expressing Cry1Ab within Europe
Perry, J. N., Devos, Y., Arpaia, S., Bartsch, D., Gathmann, A., Hails, R. S., Kiss, J., Lheureux, K., Manachini, B., Mestdagh, S., et al. (2010) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2009.2091 · Cited by 91 · see citing works
General principles for risk assessment of living modified organisms: Lessons from chemical risk assessment
Hill, R. A., & Sendashonga, C. (2003) · Environmental Biosafety Research · doi:10.1051/ebr:2003004 · Cited by 90 · see citing works
Impact of ecological factors on the initial invasion of Bt transgenes into wild populations of birdseed rape (Brassica rapa)
Vacher, C., Weis, A. E., Hermann, D., et al. (2004) · Theoretical and Applied Genetics · doi:10.1007/s00122-004-1696-7 · Cited by 89 · see citing works
Long-Term Selection for Resistance to Bacillus thuringiensis Cry1Ac Endotoxin in a Minnesota Population of European Corn Borer (Lepidoptera: Crambidae)
Bolin, P. C., Hutchison, W. D., & Andow, D. A. (1999) · Journal of Economic Entomology · doi:10.1093/jee/92.5.1021 · Cited by 85 · see citing works
Bt-cotton and secondary pests
Wang, S., Just, D. R., & Andersen, P. P. (2008) · International Journal of Biotechnology · doi:10.1504/ijbt.2008.018348 · Cited by 84 · see citing works
Weed seed resources for birds in fields with contrasting conventional and genetically modified herbicide-tolerant crops
GIBBONS, D. W., Bohan, D. A., ROTHERY, P., et al. (2006) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2006.3522 · Cited by 84 · see citing works
Survival of Kansas Dipel-Resistant European Corn Borer (Lepidoptera: Crambidae) on Bt and Non-Bt Corn Hybrids
Huang, F., Buschman, L. L., Higgins, R. A., et al. (2002) · Journal of Economic Entomology · doi:10.1603/0022-0493-95.3.614 · Cited by 84 · see citing works
Modelling impacts of cropping systems and climate on maize cross-pollination in agricultural landscapes: The MAPOD model
Angevin, F., Klein, E. K., Choimet, C., et al. (2008) · European Journal of Agronomy · doi:10.1016/j.eja.2007.11.010 · Cited by 83 · see citing works
Expressions of likelihood and confidence in the IPCC uncertainty assessment process
Risbey, J. S., & Kandlikar, M. (2007) · Climatic Change · doi:10.1007/s10584-007-9315-7 · Cited by 83 · see citing works
Chronic Exposure of the European Corn Borer (Lepidoptera: Crambidae) to Cry1Ab Bacillus thuringiensis Toxin
Chaufaux, J., Seguin, M., Swanson, J. J., Bourguet, D., & Siegfried, B. D. (2001) · Journal of Economic Entomology · doi:10.1603/0022-0493-94.6.1564 · Cited by 82 · see citing works
Susceptibility of Spanish Populations of the Corn BorersSesamia nonagrioides(Lepidoptera: Noctuidae) andOstrinia nubilalis(Lepidoptera: Crambidae) to aBacillus thuringiensisEndotoxin
González, M., Ortego, F., & Castañera, P. (2000) · Journal of Economic Entomology · doi:10.1603/0022-0493-93.2.459 · Cited by 80 · see citing works
Multiple-comparison Procedures: A Dissenting View
PERRY, J. N. (1986) · Journal of Economic Entomology · doi:10.1093/jee/79.5.1149 · Cited by 79 · see citing works
Crops Come from Wild Plants — How Domestication, Transgenes, and Linkage Together Shape Ferality
Stewart, C. N., & Warwick, S. I. (2005) · CRC Press eBooks · doi:10.1201/9781420037999.ch2 · Cited by 77 · see citing works
A review on interspecific gene flow from oilseed rape to wild relatives.
Chèvre, A., Ammitzbøll, H., Breckling, B., et al. (2004) · CABI Publishing eBooks · doi:10.1079/9780851998169.0235 · Cited by 71 · see citing works
Ecological risk assessment for Bt crops
Andow, D. A., Löveï, G. L., & Arpaia, S. (2006) · Nature Biotechnology · doi:10.1038/nbt0706-749 · Cited by 70 · see citing works
Diversity and seasonal phenology of aboveground arthropods in conventional and transgenic maize crops in Central Spain
Farinós, G. P., de la Poza, M., Hernández‐Crespo, P., Ortego, F., & Castañera, P. (2008) · Biological Control · doi:10.1016/j.biocontrol.2007.11.007 · Cited by 67 · see citing works
A conceptual framework for the design of environmental post-market monitoring of genetically modified plants
Sanvido, O., Widmer, F., Winzeler, M., et al. (2005) · Environmental Biosafety Research · doi:10.1051/ebr:2005008 · Cited by 67 · see citing works
Scientific Opinion on the assessment of potential impacts of genetically modified plants on non‐target organisms
(GMO), E. P. O. G. M. O. (2010) · EFSA Journal · doi:10.2903/j.efsa.2010.1877 · Cited by 66 · see citing works
Self-citation
Impact of Bt maize pollen (MON810) on lepidopteran larvae living on accompanying weeds
Gathmann, A., Wirooks, L., Hothorn, L. A., Bartsch, D. K., & Schuphan, I. (2006) · Molecular Ecology · doi:10.1111/j.1365-294x.2006.02962.x · Cited by 62 · see citing works
Antibiotic resistance markers in genetically modified plants: a risk to human health?
Gay, P. B., & Gillespie, S. H. (2005) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(05)70241-3 · Cited by 60 · see citing works
Cross-Resistance of Cry1Ab-Selected Ostrinia nubilalis (Lepidoptera: Crambidae) to Bacillus thuringiensis δ-Endotoxins
Siqueira, H. A. A., Moellenbeck, D. J., Spencer, T. A., et al. (2004) · Journal of Economic Entomology · doi:10.1603/0022-0493(2004)097[1049:coconl]2.0.co;2 · Cited by 59 · see citing works
Commentary: Statistical aspects of environmental risk assessment of GM plants for effects on non-target organisms
PERRY, J. N., ter Braak, C. J. F., Dixon, P. M., Duan, J. J., Hails, R. S., Hüsken, A., Lavielle, M., Marvier, M., Scardi, M., Schmidt, K., et al. (2009) · Environmental Biosafety Research · doi:10.1051/ebr/2009009 · Cited by 58 · see citing works
Proceedings of the 16th Australian Weeds Conference
van Klinken, R. D., Osten, V. A., Panetta, F. D., et al. (2008) · Queensland Department of Agriculture and Fisheries archive of scientific and research publications (Queensland Department of Agriculture and Fisheries) · Cited by 57 · see citing works
Characterization of cDNAs encoding three trypsin-like proteinases and mRNA quantitative analysis in Bt-resistant and -susceptible strains of Ostrinia nubilalis
Li, H., Oppert, B., Higgins, R. A., et al. (2005) · Insect Biochemistry and Molecular Biology · doi:10.1016/j.ibmb.2005.03.004 · Cited by 56 · see citing works
Engineering oilseeds to produce nutritional fatty acids
Damude, H. G., & Kinney, A. J. (2007) · Physiologia Plantarum · doi:10.1111/j.1399-3054.2007.00998.x · Cited by 55 · see citing works
Monitoring the Cry1Ab Susceptibility of European Corn Borer in Germany
Saeglitz, C., Bartsch, D. K., Eber, S., Gathmann, A., Priesnitz, K., & Schuphan, I. (2006) · Journal of Economic Entomology · doi:10.1603/0022-0493-99.5.1768 · Cited by 52 · see citing works
Letter to the Editor
Andow, D. A., & Alstad, D. N. (1999) · Journal of Economic Entomology · doi:10.1093/jee/92.4.755 · Cited by 52 · see citing works
Toxicity and Mode of Action of Bacillus thuringiensis Cry Proteins in the Mediterranean Corn Borer, Sesamia nonagrioides (Lefebvre)
González‐Cabrera, J., Farinós, G. P., Caccia, S., Díaz‐Mendoza, M., Castañera, P., Leonardi, M. G., Giordana, B., & Ferré, J. (2006) · Applied and Environmental Microbiology · doi:10.1128/aem.72.4.2594-2600.2006 · Cited by 48 · see citing works
Management of genetically modified herbicide–tolerant sugar beet for spring and autumn environmental benefit
May, M. J., Champion, G. T., DEWAR, A. M., et al. (2005) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2004.2948 · Cited by 46 · see citing works
Tiered tests to assess the environmental risk of fitness changes in hybrids between transgenic crops and wild relatives: the example of virus resistantBrassica napus
Raybould, A. F., & Cooper, I. (2005) · Environmental Biosafety Research · doi:10.1051/ebr:2005018 · Cited by 45 · see citing works
Fate of transgenic plant DNA in the environment
Pontiroli, A., Simonet, P., Frostegård, Å., Vogel, T. M., & Monier, J.-M. (2007) · Environmental Biosafety Research · doi:10.1051/ebr:2007037 · Cited by 44 · see citing works
How to model and simulate the effects of cropping systems on population dynamics and gene flow at the landscape level: example of oilseed rape volunteers and their role for co-existence of GM and non-GM crops
Colbach, N. (2008) · Environmental Science and Pollution Research · doi:10.1007/s11356-008-0080-6 · Cited by 42 · see citing works
Resistance in tomato to the greenhouse whitefly: analysis of population dynamics
Romanow, L. R., de Ponti, O. M. B., & Mollema, C. (1991) · Entomologia Experimentalis et Applicata · doi:10.1111/j.1570-7458.1991.tb01545.x · Cited by 42 · see citing works
Will plant vigor and tolerance be genetically correlated? Effects of intrinsic growth rate and self-limitation on regrowth
Weis, A. E., Simms, E. L., & Hochberg, M. (2000) · Evolutionary Ecology · doi:10.1023/a:1010950932468 · Cited by 41 · see citing works
Predicting longer‐term changes in weed populations under GMHT crop management
Heard, M. S., ROTHERY, P., PERRY, J. N., et al. (2005) · Weed Research · doi:10.1111/j.1365-3180.2005.00465.x · Cited by 41 · see citing works
The variability of processes involved in transgene dispersal—case studies from Brassica and related genera
Jørgensen, R. B., Hauser, T. P., D’Hertefeldt, T., et al. (2009) · Environmental Science and Pollution Research · doi:10.1007/s11356-009-0142-4 · Cited by 41 · see citing works
A screening method for prioritizing non-target invertebrates for improved biosafety testing of transgenic crops
Todd, J. H., Ramankutty, P., Barraclough, E. I., & Malone, L. A. (2008) · Environmental Biosafety Research · doi:10.1051/ebr:2008003 · Cited by 39 · see citing works
Reducing uncertainty in regulatory decision-making for transgenic crops: More ecological research or clearer environmental risk assessment?
Raybould, A. F. (2010) · GM Crops · doi:10.4161/gmcr.1.1.9776 · Cited by 38 · see citing works
Generic Assessment Endpoints Are Needed for Ecological Risk Assessment
Suter, G. W. (2000) · Risk Analysis · doi:10.1111/0272-4332.202018 · Cited by 37 · see citing works
Verifying an F1 screen for identification and quantification of rare Bacillus thuringiensis resistance alleles in field populations of the sugarcane borer, Diatraea saccharalis
Yue, B., Huang, F., Leonard, B. R., et al. (2008) · Entomologia Experimentalis et Applicata · doi:10.1111/j.1570-7458.2008.00761.x · Cited by 37 · see citing works
Fitness and beyond: Preparing for the arrival of GM crops with ecologically important novel characters
Wilkinson, M. J., & Tepfer, M. M. (2009) · Environmental Biosafety Research · doi:10.1051/ebr/2009003 · Cited by 35 · see citing works
Long-Term Assessment of the Effects of TransgenicBtCotton on the Function of the Natural Enemy Community
Naranjo, S. E. (2005) · Environmental Entomology · doi:10.1093/ee/34.5.1211 · Cited by 35 · see citing works
Evaluation and use of a spatio-temporal model of cropping system effects on gene escape from transgenic oilseed rape varieties
Colbach, N., Fargue, A., Sausse, C., et al. (2004) · European Journal of Agronomy · doi:10.1016/j.eja.2004.06.004 · Cited by 35 · see citing works
Mitigation of indirect environmental effects of GM crops
Pidgeon, J. D., May, M. J., PERRY, J. N., & Poppy, G. M. (2007) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2007.0401 · Cited by 34 · see citing works
Environmental risk assessments for transgenic crops producing output trait enzymes
Raybould, A. F., Tuttle, A., Shore, S. K., & Stone, T. B. (2009) · Transgenic Research · doi:10.1007/s11248-009-9343-3 · Cited by 32 · see citing works
Advancing environmental risk assessment for transgenic biofeedstock crops
Wolt, J. D. (2009) · Biotechnology for Biofuels · doi:10.1186/1754-6834-2-27 · Cited by 32 · see citing works
Competitive interactions and the effect of herbivory on Bt‐Brassica napus, Brassica rapa and Lolium perenne
Damgaard, C. F., & Kjær, C. (2009) · Journal of Applied Ecology · doi:10.1111/j.1365-2664.2009.01689.x · Cited by 29 · see citing works
Spatial distribution ofAglais urticae(L.) and its host plantUrtica dioica(L.) in an agricultural landscape: implications forBtmaize risk assessment and post-market monitoring
Gathmann, A., Wirooks, L., Eckert, J., et al. (2006) · Environmental Biosafety Research · doi:10.1051/ebr:2006014 · Cited by 29 · see citing works
Oilseed Rape: Co‐existence and Gene Flow from Wild Species
Ørgensen, R. B. (2007) · Advances in botanical research · doi:10.1016/s0065-2296(07)45016-9 · Cited by 28 · see citing works
Characterization of Roundup Ready Flex Cotton, ‘MON 88913’, for Use in Ecological Risk Assessment: Evaluation of Seed Germination, Vegetative and Reproductive Growth, and Ecological Interactions
Horak, M. J., Rosenbaum, E. W., Woodrum, C. L., et al. (2007) · Crop Science · doi:10.2135/cropsci2006.02.0063 · Cited by 26 · see citing works
Cumulative impact of GM herbicide-tolerant cropping on arable plants assessed through species-based and functional taxonomies
Squire, G. R., Hawes, C., Begg, G. S., et al. (2008) · Environmental Science and Pollution Research · doi:10.1007/s11356-008-0072-6 · Cited by 26 · see citing works
ECOGEN–Soil ecological and economic evaluation of genetically modified crops
Krogh, P. H., & Griffiths, B. S. (2007) · Pedobiologia · doi:10.1016/j.pedobi.2007.05.001 · Cited by 25 · see citing works
Biodiversity and non-target impacts: a case study of Bt maize in Kenya.
Birch, A. N. E., Wheatley, R., Anyango, B., et al. (2004) · CABI Publishing eBooks · doi:10.1079/9780851998619.0117 · Cited by 24 · see citing works
Methodology to support non-target and biodiversity risk assessment.
Hilbeck, A., Andow, D. A., Arpaia, S., et al. (2006) · CABI Publishing eBooks · doi:10.1079/9781845930004.0108 · Cited by 23 · see citing works
A simulation study of the medium-term effects of field patterns on cross-pollination rates in oilseed rape (Brassica napus L.)
Colbach, N., Monod, H., & Lavigne, C. (2009) · Ecological Modelling · doi:10.1016/j.ecolmodel.2008.11.020 · Cited by 22 · see citing works
Inheritance of Resistance to the Cry1Ab Bacillus thuringiensis Toxin in Ostrinia nubilalis (Lepidoptera: Crambidae)
Alves, A. P., Spencer, T. A., Tabashnik, B. E., et al. (2006) · Journal of Economic Entomology · doi:10.1603/0022-0493-99.2.494 · Cited by 21 · see citing works
Providing the evidence base for environmental risk assessments of novel farm management practices
Storkey, J., Bohan, D. A., Haughton, A. J., et al. (2008) · Environmental Science & Policy · doi:10.1016/j.envsci.2008.06.001 · Cited by 19 · see citing works
Genetic Structure of Sesamia nonagrioides (Lefebvre) Populations in the Mediterranean Area
de la Poza, M., Farinós, G. P., Beroiz, B., et al. (2008) · Environmental Entomology · doi:10.1603/0046-225x(2008)37[1354:gsosnl]2.0.co;2 · Cited by 18 · see citing works
Guidance document for the risk assessment of genetically modified microorganisms and their derived products intended for food and feed use by the Scientific Panel on Genetically Modified Organisms (GMO)
(EFSA), E. F. S. A. (2006) · EFSA Journal · doi:10.2903/j.efsa.2006.374 · Cited by 18 · see citing works
Scientific Opinion on Guidance for the risk assessment of genetically modified plants used for non‐food or non‐feed purposes
(EFSA), E. F. S. A. (2009) · EFSA Journal · doi:10.2903/j.efsa.2009.1164 · Cited by 17 · see citing works
Achieving plant disease resistance by antibody expression
Fischer, R., Emans, N., & Schillberg, S. (2001) · Canadian Journal of Plant Pathology · doi:10.1080/07060660109506936 · Cited by 15 · see citing works
Introgression from genetically modified plants into wild relatives and its consequences
den Nijs, J. C. M., Bartsch, D. K., & Sweet, J. (2004) · Cited by 15 · see citing works
Oviposition of the Colorado potato beetle (Leptinotarsa decemlineata) and natural predation on its egg masses in Bt-expressing fields
Arpaia, S., Schmidt, J. E. U., Leo, G. M. D., & Fiore, M. C. (2009) · Biocontrol Science and Technology · doi:10.1080/09583150903243896 · Cited by 8 · see citing works
Introgression of GM plants and the EU guidance note for monitoring.
den Nijs, H. C. M., & Bartsch, D. K. (2004) · CABI Publishing eBooks · doi:10.1079/9780851998169.0365 · Cited by 7 · see citing works
STRUCTURAL-BASED DIFFERENCES IN ECOTOXICITY OF BENZOQUINOLINE ISOMERS TO THE ZEBRA MUSSEL (DREISSENA POLYMORPHA)
Kraak, M. H. S., Wijnands, P., Govers, H. A. J., Admiraal, W. A., & de Voogt, P. (1997) · Environmental Toxicology and Chemistry · doi:10.1897/1551-5028(1997)016 · Cited by 7 · see citing works
Outcome of the public consultation on the draft Scientific Opinion of the Scientific Panel on Genetically Modified Organisms (GMO) on the assessment of potential impacts of genetically modified plants on non‐target organisms
Authority, E. F. S. (2010) · EFSA Journal · doi:10.2903/j.efsa.2010.1878 · Cited by 5 · see citing works
Scientific report of EFSA prepared by the GMO Unit on Public Consultation on the Updated Guidance Document of the Scientific Panel on Genetically Modified Organisms (GMO) for the risk assessment of genetically modified plants and derived food and feed
(EFSA), E. F. S. A. (2009) · EFSA Journal · doi:10.2903/j.efsa.2009.293r · Cited by 4 · see citing works
EFSA and GMO risk assessment for human and animal health and the environment
(EFSA), E. F. S. A. (2009) · EFSA Supporting Publications · doi:10.2903/sp.efsa.2009.en-95 · Cited by 4 · see citing works
Outcome of the public consultation on the draft Scientific Opinion of the Scientific Panel on Genetically Modified Organisms (GMO) on the guidance document on the environmental risk assessment of genetically modified plants
Authority, E. F. S. (2010) · EFSA Journal · doi:10.2903/j.efsa.2010.1880 · Cited by 1 · see citing works

Flagged first, then by citations

Sorted by citations

Genetically engineered crops help support conservation biological control
Romeis, J., Naranjo, S. E., Meissle, M., & Shelton, A. M. (2019) · Biological Control · doi:10.1016/j.biocontrol.2018.10.001 · Cited by 231 · see citing works
“It is thus likely that those results are artifacts, probably resulting from problems in study design (EFSA, 2009; Rauschen, 2010; Ricroch et al., 2010; Romeis et al., 2013a, 2014b).”
Result
Impact of genetically engineered maize on agronomic, environmental and toxicological traits: a meta-analysis of 21 years of field data
Pellegrino, E., Bedini, S., Nuti, M., & Ercoli, L. (2018) · Scientific Reports · doi:10.1038/s41598-018-21284-2 · Cited by 177 · see citing works
No effects of Bacillus thuringiensis maize on nontarget organisms in the field in southern Europe: a meta-analysis of 26 arthropod taxa
Comas, C., Lumbierres, B., Pons, X., & Albajes, R. (2014) · Transgenic Research · doi:10.1007/s11248-013-9737-0 · Cited by 129 · see citing works
EFSA’s scientific activities and achievements on the risk assessment of genetically modified organisms (GMOs) during its first decade of existence: looking back and ahead
Devos, Y., Aguilera, J., Diveki, Z., Gomes, A., Liu, Y., Paoletti, C., du Jardin, P., Herman, L., Perry, J. N., & Waigmann, E. (2014) · Transgenic Research · doi:10.1007/s11248-013-9741-4 · Cited by 95 · see citing works
Assessing environmental impacts of genetically modified plants on non-target organisms: the relevance of in planta studies
Arpaia, S., Birch, A. N. E., Kiss, J., van Loon, J. J. A., Messéan, A., Nuti, M., Perry, J. N., Sweet, J. B., & Tebbe, C. C. (2017) · Science of The Total Environment · doi:10.1016/j.scitotenv.2017.01.039 · Cited by 62 · see citing works
Independent action between DvSnf7 RNA and Cry3Bb1 protein in southern corn rootworm, Diabrotica undecimpunctata howardi and Colorado potato beetle, Leptinotarsa decemlineata
Levine, S. L., Tan, J., Mueller, G. M., Bachman, P. M., Jensen, P. D., & Uffman, J. P. (2015) · PLoS ONE · doi:10.1371/journal.pone.0118622 · Cited by 45 · see citing works
Does the growing of Bt maize change abundance or ecological function of non-target animals compared to the growing of non-GM maize? A systematic review
Meissle, M., Naranjo, S. E., & Romeis, J. (2022) · Environmental Evidence · doi:10.1186/s13750-022-00272-0 · Cited by 41 · see citing works
Environmental risk assessment for the small tortoiseshell Aglais urticae and a stacked Bt‐maize with combined resistances against Lepidoptera and Chrysomelidae in central European agrarian landscapes
SCHUPPENER, M., MÜHLHAUSE, J., MÜLLER, A., & RAUSCHEN, S. (2012) · Molecular Ecology · doi:10.1111/j.1365-294x.2012.05716.x · Cited by 37 · see citing works
Development of Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae) on pollen from Bt-transgenic and conventional maize
Meissle, M., Zünd, J., Waldburger, M., & Romeis, J. (2014) · Scientific Reports · doi:10.1038/srep05900 · Cited by 31 · see citing works
Scientific Opinion on application (EFSA‐GMO‐UK‐2008‐60) for placing on the market of genetically modified herbicide tolerant maize GA21 for food and feed uses, import, processing and cultivation under Regulation (EC) No 1829/2003 from Syngenta Seeds
(GMO), E. P. O. G. M. O. (2011) · EFSA Journal · doi:10.2903/j.efsa.2011.2480 · Cited by 19 · see citing works
Self-citation
Scientific Opinion on an application (EFSA‐GMO‐NL‐2005‐24) for the placing on the market of the herbicide tolerant genetically modified soybean 40‐3‐2 for cultivation under Regulation (EC) No 1829/2003 from Monsanto
(GMO), E. P. O. G. M. O. (2012) · EFSA Journal · doi:10.2903/j.efsa.2012.2753 · Cited by 19 · see citing works
Self-citation
Does the growing of Bt maize change abundance or ecological function of non-target animals compared to the growing of non-GM maize? A systematic review protocol
Meissle, M., Naranjo, S. E., Kohl, C., Riedel, J., & Romeis, J. (2014) · Environmental Evidence · doi:10.1186/2047-2382-3-7 · Cited by 13 · see citing works

Authors: (GMO), E. P. O. G. M. O.
Corresponding author: EFSA Panel on Genetically Modified Organisms (GMO)
Venue: EFSA Journal
Publisher: Wiley
Published: 2010-11
Volume: 8
Issue: 11
Pages: 1879-1879
ISSN: 1831-4732 (ISSN-L)
DOI: 10.2903/j.efsa.2010.1879
PMC: PMC13129916
OpenAlex: W4205573128
Cited by: 428
References: 137
Citations by year: 2026: 15 · 2025: 22 · 2024: 18 · 2023: 22 · 2022: 27 · 2021: 29 · 2020: 41 · 2019: 26 · 2018: 19 · 2017: 26 · 2016: 32 · 2015: 28 · 2014: 32 · 2013: 31 · 2012: 33
FWCI: 35.03
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by-nd
doi.wiley.com/10.1002/tdm_license_1 (tdm, 1765 d)
Locations: EFSA Journal (publishedVersion, cc-by-nd)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
OpenAgrar (submittedVersion, cc-by-nc)
Funders: European Food Safety Authority
European Commission (1829/2003)
Topics: Life Sciences › Agricultural and Biological Sciences › Plant Science › Genetically Modified Organisms Research
Life Sciences › Agricultural and Biological Sciences › Food Science › Agricultural safety and regulations
Social Sciences › Sociology and Political Science › Risk Perception and Management
Keywords: transgenic plants, environmental risk assessment, Directive 2001/18/EC, Regulation (EC) No 1829/2003, non-target organisms, biogeochemical processes, human and animal health, risk management strategies, EFSA GMO Panel

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Guidance on the environmental risk assessment of genetically modified plants

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks