Document Type : Review Articles
Authors
1 HIV/AIDS Virology, HIV/AIDS Research Center, Institute of Health, Shiraz University of Medical Sciences, Shiraz, Iran
2 HIV/AIDS Research Center, Institute of Health, Shiraz University of Medical Sciences, Shiraz, Iran
3 Department of Immunology, Shiraz Medical School, Shiraz University of Medical Sciences, Shiraz, Iran
Abstract
Background: There are some debates about the possible unintended effects of genetically modified (GM) crops on consumer health. The gut microbiota plays an important role in maintaining the health of the host, especially in gastrointestinal diseases. The current review focuses on the studies with the aim of evaluating whether their outcomes indicate any adverse effects of feeding genetically modified (GM) crops on alteration and the count of gut microbiota.
Methods: A structured literature search was performed independently by three authors on Scopus, Web of Science, PubMed, and Embase on the 1st of July 2019. In total, 333 publications were obtained by the search strategy, which decreased to 306 after excluding the duplicates. Furthermore, experimental studies that have designed a control group and were written in English were included in the review. After reviewing the full texts, 16 studies were included. To access the quality of articles, we used the Cochrane checklist.
Results: Ten publications (62.5%) used 50% or more genetically modified (GM) diet in the treatment group. In 11 studies (68.7%), the duration of animal feeding was 90 days or more. There were no significant differences in the experimental and control groups of both male and female rats on the 90th day; it can be concluded that non-genetically modified (GM) and genetically modified (GM) rice diets did not cause any changes in the gut bacteria. Data analysis of different animal models showed that the most changes in the microbial flora were observed in the chicken and the least in the rat. In the studies in this review, all microbial isolates were anaerobic, and the Lactobacillus and Enterococcus families were common organisms.
Conclusion: Based on our literature review, we claim that there is not any significant difference in gut microbiota between the control group and the group with a transgenic diet. The mechanisms of the effects of genetically modified (GM) foods on the gut microbiota in animals should be explicated in future studies. Nevertheless, this study provides valuable information for research on genetically modified (GM) foods and whether they are useful or detrimental to human health.
Highlights
Maryam Nejabat (Google Scholar)
Mohammadreza Heydari (Google Scholar)
Keywords
- de Vos CJ, Swanenburg M. Health effects of feeding genetically modified (GM) crops to livestock animals: A review. Food Chem Toxicol. 2018 Jul:117:3-12. doi: 10.1016/j.fct.2017.08.031.
- Yuan Y, Xu W, Luo Y, Liu H, Lu J, Su C, et al. Effects of genetically modified T2A-1 rice on faecal microflora of rats during 90 day supplementation. J Sci Food Agric. 2011;91(11):2066-72. doi: 10.1002/jsfa.4421.
- Newell-McGloughlin M. Nutritionally improved agricultural crops. Plant Physiol. 2008 Jul;147(3):939-53. doi: 10.1104/pp.108.121947.
- Zhang C, Wohlhueter R, Zhang H. Genetically modified foods: A critical review of their promise and problems. Food Science and Human Wellness. 2016;5(3):116-23. doi: 10.1016/j.fshw.2016.04.002.
- Brookes G, Barfoot P. Environmental impacts of genetically modified (GM) crop use 1996–2018: impacts on pesticide use and carbon emissions. GM Crops & Food. 2020;11(4):215-41. doi: 10.1080/21645698.2020.1773198.
- Ganesan M, Poluektova LY, Kharbanda KK, Osna NA. Liver as a target of human immunodeficiency virus infection. World J Gastroenterol. 2018 Nov 14; 24(42): 4728–4737. doi: 10.3748/wjg.v24.i42.4728.
- Zou S, Lu J, Luo Y, Qi X, Delaney B, Xu W, et al. The food safety of DP-356Ø43 soybeans on SD rats reflected by physiological variables and fecal microbiota during a 90-day feeding study. Regulatory Toxicology and Pharmacology. 2018;97:144-51. doi: 10.1016/j.yrtph.2018.06.016.
- Mohajeri MH, La Fata G, Steinert RE, Weber P. Relationship between the gut microbiome and brain function. Nutr Rev. 2018 Jul 1;76(7):481-496. doi: 10.1093/nutrit/nuy009. PMID: 29701810.
- Liang D, Leung RK-K, Guan W, Au WW. Involvement of gut microbiome in human health and disease: brief overview, knowledge gaps and research opportunities. Gut Pathogens. 2018;10(1):3. doi: 10.1186/s13099-018-0230-4.
- Liu Q, Yang W, Li M, Wang Y, Zhang H, Wu Y, et al. Effects of Transgenic Bt Rice Containing the Cry1Ab Protein on the Gastrointestinal Health of Highly Inbred Wuzhishan Pigs after Two Generations of Feeding. J Agric Food Chem. 2018;66(40):10575-87. doi: 10.1021/acs.jafc.8b02431. Epub 2018 Sep 26.
- Yuan Y, Xu W, He X, Liu H, Cao S, Qi X, et al. Effects of genetically modified T2A-1 rice on the GI health of rats after 90-day supplement. Scientific Reports. 2013;3. doi: 10.1038/srep01962.
- Blandino G, Inturri R, Lazzara F, Di Rosa M, Malaguarnera L. Impact of gut microbiota on diabetes mellitus. Diabetes Metab. 2016;42(5):303-15. doi: 10.1016/j.diabet.2016.04.004. Epub 2016 May 11.
- Al Bander Z, Nitert MD, Mousa A, Naderpoor N. The Gut Microbiota and Inflammation: An Overview. Int J Environ Res Public Health. 2020;17(20):7618. doi: 10.3390/ijerph17207618.
- Buzoianu SG, Walsh MC, Rea MC, Quigley L, O'Sullivan O, Cotter PD, et al. Sequence-based analysis of the intestinal microbiota of sows and their offspring fed genetically modified maize expressing a truncated form of Bacillus thuringiensis Cry1Ab protein (Bt maize). Appl Environ Microbiol. 2013;79(24):7735-44. doi: 10.1128/AEM.02937-13.
- Xu W, Li L, Lu J, Luo Y, Shang Y, Huang K. Analysis of Caecal Microbiota in Rats Fed with Genetically Modified Rice by Real-Time Quantitative PCR. J Food Sci. 2011;76(1):M88-M93. doi: 10.1111/j.1750-3841.2010.01967.x.
- Buzoianu SG, Walsh MC, Rea MC, O'Sullivan O, Crispie F, Cotter PD, et al. The effect of feeding Bt MON810 maize to pigs for 110 days on intestinal microbiota. PloS one. 2012;7(5). doi: 10.1371/journal.pone.0033668.
- Buzoianu SG, Walsh MC, Rea MC, O'Sullivan O, Cotter PD, Ross RP, et al. High-throughput sequence-based analysis of the intestinal microbiota of weanling pigs fed genetically modified MON810 maize expressing Bacillus thuringiensis Cry1Ab (Bt Maize) for 31 Days. Appl Environ Microbiol. 2012;78(12):4217-24. doi: 10.1128/AEM.00307-12. Epub 2012 Mar 30.
- Lili G, Deng X, Minhong Z, Changlong S, Jinghai F, Fuping S, et al. High-throughput sequencing-based analysis of the intestinal microbiota of broiler chickens fed genetically modified rice expressing Cry1Ac/Cry1Ab chimeric Bacillus thuringiensis protein. J Poult Sci. 2018;55(1):10-6. doi: 10.2141/jpsa.0170029. Epub 2017 Aug 25.
- Lang T, Zou S, Huang K, Guo M, Liu X, He X. Safety assessment of transgenic canola RF3 with bar and barstar gene on Sprague-Dawley (SD) rats by 90-day feeding test. Regul Toxicol Pharmacol.. 2017;91:226-34. doi: 10.1016/j.yrtph.2017.10.018. Epub 2017 Oct 23.
- Buzoianu SG, Walsh MC, Rea MC, O’Sullivan O, Crispie F, Cotter PD, et al. The effect of feeding Bt MON810 maize to pigs for 110 days on intestinal microbiota. PLoS One. 2012;7(5):e33668. doi: 10.1371/journal.pone.0033668.
- Espley RV, Butts CA, Laing WA, Martell S, Smith H, McGhie TK, et al. Dietary flavonoids from modified apple reduce inflammation markers and modulate gut microbiota in mice. J Nutr. 2014;144(2):146-54. doi: 10.3945/jn.113.182659.
- Lu L, Guo J, Li S, Li A, Zhang L, Liu Z, et al. Influence of Phytase Transgenic Corn on the Intestinal Microflora and the Fate of Transgenic DNA and Protein in Digesta and Tissues of Broilers. PloS one.2015;10(11):e0143408. doi: 10.1371/journal.pone.0143408.
- Zhao K, Ren F, Han F, Liu Q, Wu G, Xu Y, et al. Edible safety assessment of genetically modified rice T1C-1 for Sprague Dawley rats through horizontal gene transfer, allergenicity and intestinal microbiota. PloS one. 2016;11(10). doi: 10.1371/journal.pone.0163352.
- Qi X, Chen S, Sheng Y, Guo M, Liu Y, He X, et al. Safety assessment of genetically modified rice expressing human serum albumin from urine metabonomics and fecal bacterial profile. Food Chem Toxicol. 2015;76:1-10. doi: 10.1016/j.fct.2014.11.022. Epub 2014 Dec 2.
- Zhang X, Zhang T, Shi J, Zou S, Guo M, He X, et al. A 90-day subchronic toxicology screen of genetically modified rice Lac-3 and its effects on the gut microbiota in Sprague-Dawley rats. Regul Toxicol Pharmacol. 2019;103:292-300. doi: 10.1016/j.yrtph.2019.02.005. Epub 2019 Feb 7.
- Walsh CJ, Guinane CM, O’Toole PW, Cotter PD. Beneficial modulation of the gut microbiota. FEBS letters. 2014;588(22):4120-30. doi: 10.1016/j.febslet.2014.03.035.
- Warren FJ, Fukuma NM, Mikkelsen D, Flanagan BM, Williams BA, Lisle AT, et al. Food starch structure impacts gut microbiome composition. Msphere. 2018;3(3):e00086-18. doi: 10.1128/mSphere.00086-18. eCollection 2018 May-Jun.
- de Ronde JA, Laurie RN, Caetano T, Greyling MM, Kerepesi I. Comparative study between transgenic and non-transgenic soybean lines proved transgenic lines to be more drought tolerant. Euphytica. 2004;138(2):123-32. doi: 10.1023/B:EUPH.0000046806.68554.5b.
- Kim YS, Unno T, Kim B-Y, Park M-S. Sex differences in gut microbiota. World J Mens Health. 2019;37. doi: 10.5534/wjmh.190009. PMCID: PMC6920072.
- Ozdal T, Sela DA, Xiao J, Boyacioglu D, Chen F, Capanoglu E. The reciprocal interactions between polyphenols and gut microbiota and effects on bioaccessibility. Nutrients. 2016;8(2):78. doi: 10.3390/nu8020078. PMCID: PMC4772042.
- Mueller S, Saunier K, Hanisch C, Norin E, Alm L, Midtvedt T, et al. Differences in fecal microbiota in different European study populations in relation to age, gender, and country: a cross-sectional study. Appl Environ Microbiol. 2006;72(2):1027-33. doi: 10.1128/AEM.72.2.1027-1033.2006.
- Cabal A, Wassenaar TM, Ussery DW. Gender Differences in the Gut Microbiome and How These Affect Cardiovascular Diseases. Gender Differences in the Pathogenesis and Management of Heart Disease: Springer; 2018. p. 89-100. doi: 10.1007/978-3-319-71135-5_7.
- Fransen F, van Beek AA, Borghuis T, Meijer B, Hugenholtz F, van der Gaast-de Jongh C, et al. The impact of gut microbiota on gender-specific differences in immunity. Front. Immunol. 2017;8:754. doi: 10.3389/fimmu.2017.00754.
- Flemer B, Gaci N, Borrel G, Sanderson IR, Chaudhary PP, Tottey W, et al. Fecal microbiota variation across the lifespan of the healthy laboratory rat. Gut microbes. 2017;8(5):428-39. doi: 10.1080/19490976.2017.1334033. PMCID: PMC5628645.
)