Application of Meta-analysis in the Safety Assessments of Transgenic Crops

doi:10.16409/j.cnki.2095-039x.2019.05.012

Abstract

Abstract: The ecological risks and scientific assessment methods of transgenic crops have drawn growing public attention. There have been a series of studies focusing on the ecological safety assessments of transgenic crops, while these results vary from each other. Meta-analysis provides a scientific assessment to quantitatively review and synthesize the multiple independent experiments of a certain subject. This method has been widely used in the areas of medicine and ecology, but rarely used in the ecological safety assessments of transgenic crops. Here we introduced the concept and procedure of meta-analysis and its application in the safety assessment of transgenic crops, we also recognized the limitation of meta-analysis. This review may promote a wide application of meta-analysis in the future.

Key words: Meta-analysis, transgenic crops, safety assessment, ecological risks

CLC Number:

S476

DANG Cong, WANG Fang, LU Zengbin, YE Gongyin. Application of Meta-analysis in the Safety Assessments of Transgenic Crops[J]. Chinese Journal Of Biological Control, 2020, 36(1): 17-23.

References

[1] Chen M, Shelton A, Ye G Y. Insect-resistant genetically modified rice in China:from research to commercialization[J]. Annual Review of Entomology, 2011, 56:81-101.
[2] Yu H L, Li Y H, Wu K M. Risk assessment and ecological effects of transgenic Bacillus thuringiensis crops on non-target organisms[J]. Journal of Integrative Plant Biology, 2011, 53(7):520-538.
[3] Li Y H, Hallerman E M, Liu Q S, et al. The development and status of Bt rice in China[J]. Plant Biotechnology Journal, 2016, 14:839-848.
[4] Marvier M, McCreedy C, Regetz J, et al. A meta-analysis of effects of Bt cotton and maize on nontarget invertebrates[J]. Science, 2007, 316(5830):1475-1477.
[5] Glass G V. Primary, secondary, and meta-analysis of research[J]. Educational Researcher,1976, 5(10):3-8.
[6] Werf E V. Lack's clutch size hypothesis:an examination of the evidence using meta-analysis[J]. Ecology, 1992, 73(5):1699-1705.
[7] Dickersin K, Berlin J A. Meta-analysis:state-of-the-science[J]. Epidemiologic Reviews, 1992,14:154-176.
[8] Hedges L V, Olkin I. Statistical method for meta-analysis[M]. San Diego, CA, USA:Academic Press, 1985.
[9] Tonhasca A, Byrne D N. The effects of crop diversification on herbivorous insects:a meta analysis approach[J]. Ecological Entomology, 1994, 19(3):239-244.
[10] 彭少麟, 唐小焱. Meta分析及其在生态学上的应用[J]. 生态学杂志, 1998, 17(5):75-80.
[11] 郑凤英, 彭少麟. 捕食关系的Meta分析[J]. 生态学报, 1999, 19(4):448-451.
[12] 郑凤英, 彭少麟. 植物生理生态指标对大气CO₂浓度倍增响应的整合分析[J]. 植物学报, 2001, 43(11):1101-1109.
[13] 彭少麟, 郑凤英. Meta分析:综述中的一次大革命[J]. 生态学杂志, 1999, 18(6):65-70.
[14] 李静, 秦莉, 刘鸣. 系统评价的基本方法[J]. 中国循证医学, 2001, 1(1):34-38.
[15] Shelton A M, Naranjo S E, Romeis J, et al. Setting the record straight:a rebuttal to an erroneous analysis on transgenic insecticidal crops and natural enemies[J]. Transgenic Research, 2009, 18(3):317-322.
[16] Julian P H, Sally G. Cochrane handbook for systematic reviews of interventions (Version 5.1.0)[M]. 2011. http://handbook.cochrane.org.
[17] Haworth M, Hoshika Y, Killi D. Has the impact of rising CO₂ on plants been exaggerated by meta-analysis of free air CO₂enrichment studies[J]. Frontiers in Plant Science, 2016, 7:1153.
[18] Begg C B, Mazumdar M. Operating characteristics of a rank correlation test for publication bias[J]. Biometrics, 1994, 50(4):1088-1101.
[19] Egger M, Smith G D, Schneider M, et al. Bias in metaanalysis detected by a simple, graphical test[J]. British Medical Journal, 1997, 315(7109):629-634.
[20] Duval S, Tweedie R. Trim and fill:a simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis[J]. Biometrics, 2000, 56(2):455-463.
[21] 郑凤英, 彭少麟. Meta分析中几种常用效应值的介绍[J]. 生态科学, 2001, 20(1-2):81-84.
[22] Hedges L V. Distribution theory for Glass's estimator of effect size and related estimators[J]. Journal of Educational and Behavioral Statistics, 1981, 6(2):107-128.
[23] Hedges L V, Gurevitch J, Curtis P S. The meta-analysis of response ratios in experimental ecology[J]. Ecology, 1999, 80(4):1150-1156.
[24] Naranjo S E. Impacts of Bt crops on non-target invertebrates and insecticide use patterns[J]. CAB Reviews:Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources, 2009, 4(11):1-23.
[25] Wolfenbarger L L, Naranjo S E, Lundgren J G, et al. Bt crop effects on functional guilds of non-target arthropods:a meta-analysis[J]. PLoS ONE, 2008, 3(5):e2118.
[26] 郑凤英, 彭少麟. 整合分析中两种假设模型的介绍及实例分析[J]. 生态科学, 2004, 23(4):292-294.
[27] Borenstein M, Hedges L V, Higgins J, et al. Introduction to meta analysis[M]. Chichester, UK:John Wiley & Sons Ltd, 2009.
[28] Schmidt F L, Oh I S, Hayes T L. Fixed-versus random-effects models in meta-analysis:model properties and an empirical comparison of differences in results[J]. British Journal of Mathematical and Statistical Psychology, 2009, 62(1):97-128.
[29] 郭明, 李新. Meta分析及其在生态环境领域研究中的应用[J]. 中国沙漠, 2009, 29(5):911-919.
[30] 何莉. Cochrane系统评价软件RevMan简介[J]. 中国循证医学, 2001, 1(3):168-169.
[31] Rosenberg M S, Adams D C, Gurevitch J. MetaWin:statistical software for meta-analysis with resampling rests. Version 1[J]. The Quarterly Review of Biology, 1997, 73(1):126-128.
[32] 刘关键, 吴泰相. Meta-分析的森林图及临床意义[J]. 中国循证医学杂志, 2004, 4(3):198-201.
[33] 石修权, 王增珍. Meta回归与亚组分析在异质性处理中的应用[J]. 中华流行病学杂志, 2008, 29(5):497-501.
[34] 王吉耀. 循证医学与临床实践(第2版)[M]. 北京:科学出版社, 2002.
[35] Duan J J, Marvier M, Huesing J, et al. A meta-analysis of effects of Bt crops on honey bees (Hymenoptera:Apidae)[J]. PLoS ONE, 2008, 3(1):e1415.
[36] Duan J J, Lundgren J G, Naranjo S, et al. Extrapolating non-target risk of Bt crops from laboratory to field[J]. Biology Letters, 2010, 6(1):74-77.
[37] Dang C, Lu Z B, Wang L, et al. Does Bt rice pose risks to non-target arthropods? Results of a meta-analysis in China[J]. Plant Biotechnology Journal, 2017, 15:1047-1053.
[38] Romeis J, Meissle M, Naranjo S E, et al. The end of a myth-Bt (Cry1Ab) maize does not harm green lacewings[J]. Frontiers in Plant Science, 2014, 5:391.
[39] Nakasu E Y T, Dias S C, Pires C S S, et al. Bitrophic toxicity of Cry1Ac to Cycloneda sanguinea, a predator in Brazilian cotton[J]. Entomologia Experimentalis et Applicata, 2013, 148(2):105-115.
[40] Peterson J A, Lundgren J G, Harwood J D. Interactions of transgenic Bacillus thuringiensis insecticidal crops with spiders (Araneae)[J]. Journal of Arachnology, 2011, 39(1):1-21.
[41] Areal F J, Riesgo L. Probability functions to build composite indicators:a methodology to measure environmental impacts of genetically modified crops[J]. Ecological Indicators, 2015, 52:498-516.
[42] Finger R, El Benni N, Kaphengst T, et al. A meta analysis on farm-level costs and benefits of GM crops[J]. Sustainability, 2011, 3(5):743-762.
[43] Areal F J, Riesgo L, Rodriguez-Cerezo E. Economic and agronomic impact of commercialized GM crops:a meta-analysis[J]. Journal of Agricultural Science, 2013, 151:7-33.
[44] Klumper W, Qaim M. A meta-analysis of the impacts of genetically modified crops[J]. PLoS ONE, 2014, 9(11):e111629.
[45] De Steur H, Wesana J, Blancquaert D, et al. The socioeconomics of genetically modified biofortified crops:a systematic review and meta-analysis[J]. Annals of the New York Academy of Sciences, 2017, 1390(1):14-33.
[46] Witjaksono J, Wei X W, Mao S C, et al. Yield and economic performance of the use of GM cotton worldwide over time:A review and meta-analysis[J]. China Agricultural Economic Review, 2014, 6(4):616-643.
[47] Pellegrino E, Bedini S, Nuti M, et al. Impact of genetically engineered maize on agronomic, environmental and toxicological traits:a meta-analysis of 21 years of field data[J]. Scientific Reports, 2018, 8(1):3113.
[48] Frewer L J, Lans I A, Fischer A R H, et al. Public perceptions of agri-food applications of genetic modification-a systematic review and meta-analysis[J]. Trends in Food Science & Technology, 2013, 30(2):142-152.
[49] Zhou J, Harrigan G G, Berman K H, et al. Stability in the composition equivalence of grain from insect-protected maize and seed from glyphosate-tolerant soybean to conventional counterparts over multiple seasons, locations, and breeding germplasms[J]. Journal of Agricultural and Food Chemistry, 2011, 59(16):8822-8828.
[50] Gassmann A J, Hannon E R, Sisterson M S, et al. Effects of entomopathogenic nematodes on evolution of pink bollworm resistance to Bacillus thuringiensis toxin Cry1Ac[J]. Journal of Economic Entomology, 2012, 105(3):994-1005.
[51] Fleming D, Musser F, Reisig D, et al. Effects of transgenic Bacillus thuringiensis cotton on insecticide use, heliothine counts, plant damage, and cotton yield:A meta-analysis, 1996-2015[J]. PLoS ONE, 2018, 13(7):e0200131.
[52] Heredia Diaz O, Aldaba Meza J L, Baltazar B M, et al. Plant characterization of genetically modified maize hybrids MON-89Ø34-3×MON-88Ø17-3, MON-89Ø34-3×MON-ØØ6Ø3-6, and MON-ØØ6Ø3-6:alternatives for maize production in Mexico[J]. Transgenic Research, 2016, 26:131-151.
[53] Ford C S, Allainguillaume J, Fu T Y R, et al. Assessing the value of imperfect biocontainment nationally:rapeseed in the United Kingdom as an exemplar[J]. New Phytologist, 2015, 205(3):1342-1349.
[54] Zeilinger A R, Olson D M, Andow D A. Competitive release and outbreaks of non-target pests associated with transgenic Bt cotton[J]. Ecological Applications, 2016, 26(4):1047-1054.
[55] Marvier M. Using meta-analysis to inform risk assessment and risk management[J]. Journal of Consumer Protection and Food Safety, 2011, 6(S1):113-118.
[56] Ricroch A, Berge J B, Kuntz M. Is the German suspension of MON810 maize cultivation scientifically justified?[J]. Transgenic Research, 2010, 19(1):1-12.