Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-26T05:12:42.502Z Has data issue: false hasContentIssue false
  • English
  • Français

Impact of Glyphosate-Roundup® in the Ileal Structure of Male and Female Rats: A Morphological and Immunohistochemical Study

Part of: Micrographia Collection

Published online by Cambridge University Press:  22 September 2021

Shaimaa M.M. Saleh Open the ORCID record for Shaimaa M.M. Saleh [Opens in a new window] ,
Tasneem A. Elghareeb ,
Mona M. Atia  and
Mohamed Ahmed Ibrahim Ahmed
Shaimaa M.M. Saleh*
Affiliation:
Department of Zoology and Entomology, Faculty of Science, Assiut University, Assiut71516, Egypt
Tasneem A. Elghareeb
Affiliation:
Plant Protection Department, Faculty of Agriculture, Assiut University, Assiut71526, Egypt
Mona M. Atia
Affiliation:
Department of Zoology and Entomology, Faculty of Science, Assiut University, Assiut71516, Egypt
Mohamed Ahmed Ibrahim Ahmed
Affiliation:
Plant Protection Department, Faculty of Agriculture, Assiut University, Assiut71526, Egypt
*
*Corresponding author: Shaimaa M.M. Saleh, E-mail: [email protected]
Get access

Abstract

The current study was aimed to evaluate the effects of variable doses of the weedicide glyphosate on the ileal (the final section of the small intestine) structure of rats of both sexes, using histological, histochemical, and ultrastructural methods. Forty animals were classified into four groups of 10 animals per group (five males and five females). The first group acted as a control, and the remaining groups were treated with glyphosate-Roundup® 25, 50, and 100 mg/kg body weight daily for 15 days. The results indicated extinct histopathological changes manifested in the deformation of villi, foci of leukocytic infiltration in the core of villi, and hyperplasia of goblet cells. Histochemical examination (Alcian blue and Periodic acid–Schiff stain) revealed a strong positive reaction of goblet cells and an increase in their number in all treated groups. In addition, the immunohistochemical investigation revealed the immunoreactivity of matrix metalloproteinase-9 expression. Furthermore, electron microscopic alternations were represented by the deformation of nuclei, destruction of microvilli, and deposition of lipid droplets. Collectively, the present findings indicate that treatment with glyphosate results in extensive morphological alternations to the ileal structure of rats of both sexes and that female rats are more affected than male rats are.

Keywords

glyphosatehistopathologyileal structureimmunohistochemistrymorphological alternations
Type
Micrographia
Information
Microscopy and Microanalysis , Volume 27 , Issue 6 , December 2021 , pp. 1547 - 1563
Check for updates
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of the Microscopy Society of America

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ågren, MS, Jorgensen, LN, Andersen, M, Viljanto, J & Gottrup, F (1998). Matrix metalloproteinase 9 level predicts optimal collagen deposition during early wound repair in humans. Br J Surg 85, 68–71. doi:10.1046/j.1365-2168.1998.00556.xCrossRefGoogle ScholarPubMed
Bai, SH & Ogbourne, SM (2016). Glyphosate: Environmental contamination, toxicity and potential risks to human health via food contamination. Environ Sci Pollut Res 23, 18988–19001. doi:10.1007/s11356-016-7425-3CrossRefGoogle ScholarPubMed
Barkai, O, Assalia, A, Gleizarov, E & Ahmad Mahajna, A (2019). Gender differences in response to abdominal compartment syndrome in rats. BMC Res Notes 12, 321. doi:10.1186/s13104-019-4353-6CrossRefGoogle ScholarPubMed
Bauer, AT, Bürgers, HF, Rabie, T & Marti, HH (2010). Matrix metalloproteinase-9 mediates hypoxia-induced vascular leakage in the brain via tight junction rearrangement. J Cereb Blood Flow Metab 30, 837–848. doi:10.1038/jcbfm.2009.248CrossRefGoogle Scholar
Benbrook, CM (2016). Trends in glyphosate herbicide use in the United States and globally. Environ Sci Eur 28(3), 1–15. doi:10.1186/s12302-016-0070-0CrossRefGoogle ScholarPubMed
Cathcart, J, Pulkoski-Gross, A & Cao, J (2015). Targeting matrix metalloproteinases in cancer: Bringing new life to old ideas. Genes Dis 2, 26–34. doi:10.1016/j.gendis.2014.12.002CrossRefGoogle ScholarPubMed
Cheville, NF (1988). Introduction to Veterinary Pathology. Ames, IA: Iowa State University Press, 537 pp. Available at https://lib.ugent.be/catalog/rug01:000195559.Google Scholar
Collado, MC, Grześkowiak, L & Salminen, S (2007). Probiotic strains and their combination inhibit in vitro adhesion of pathogens to pig intestinal mucosa. Curr Microbiol 55(3), 260–265. doi:10.1007/s00284-007-0144-8CrossRefGoogle ScholarPubMed
Connolly, A, Leahy, M, Jones, K, Kenny, L & Coggins, MA (2018). Glyphosate in Irish adults—A pilot study in 2017. Environ Res 165, 235–236. doi:10.1016/j.envres.2018.04.025CrossRefGoogle ScholarPubMed
Conrad, A, Schröter-Kermani, C, Hoppe, W, Rüther, M, Pieper, S & Kolossa-Gehring, M (2016). Glyphosate in German adults − Time trend (2001 to 2015) of human exposure to a widely used herbicide. J Hyg Environ Health 220, 8–16. doi:10.1016/j.ijheh.2016.09.016CrossRefGoogle ScholarPubMed
Drury, RA & Wallington, EA (1980). Carleton's Histological Techniques, 5th ed. New York: Oxford University Press, p. 195.Google Scholar
Duke, SO (1988). Glyphosate. In Herbicides: Chemistry, Degradation, and Mode of Action, Kearney, PC & Kaufman, DD (Eds.), pp. 1–70. New York: Dekker.Google Scholar
Duncan, M & Grant, G (2003). Oral and intestinal mucositis—Causes and possible treatments. Aliment Pharmacol Ther 18, 853–874. doi:10.1046/j.1365-2036.2003.01784.xCrossRefGoogle ScholarPubMed
Elghareeb, TA, Ahmed, MAI, Mohamed, IA, Ahmed, SMM & Ezz El-Din, HA (2018). Synergistic action of glyphosate on novel pesticides against Culex pipiens L. (Diptera: Culicidae) mosquitoes under laboratory conditions. Aust J Basic Appl Sci 12, 45–52. doi:10.22587/ajbas.2018.12.4.9Google Scholar
El-Shenawy, NS (2009). Oxidative stress responses of rats exposed to Roundup and its active ingredient glyphosate. Environ Toxicol Pharmacol 28(3), 379–385. doi:10.1016/j.etap.2009.06.001CrossRefGoogle ScholarPubMed
Fathi, MA, Han, G, Kang, R, Shen, D, Shen, J & Li, C (2020). Disruption of cytochrome P450 enzymes in the liver and small intestine in chicken embryos in ovo exposed to glyphosate. Environ Sci Pollut Res 27, 16865–16875. doi:10.1007/s11356-020-08269-3CrossRefGoogle ScholarPubMed
Gillezeau, C, van Gerwen, M, Shaffer, RM, Rana, I, Zhang, L, Sheppard, L & Taioli, E (2019). The evidence of human exposure to glyphosate: A review. Environ Health 18, 1–14. doi:10.1186/s12940-018-0435-5CrossRefGoogle ScholarPubMed
Gomes, MP, Smedbol, E, Chalifour, A, Hénaultethier, L, Labrecque, M, Lepage, L, Lucotte, M & Ph, J (2014). Alteration of plant physiology by glyphosate and its by-product aminomethylphosphonic acid: An overview. J Exp Bot 65, 4691–4703. doi:10.1093/jxb/eru269CrossRefGoogle ScholarPubMed
Hamdamin, PS, Rasul, KH & Aziz, FM (2017). Histopathological effects of methomyl pesticide and mobile phone electromagnetic radiation on duodenum of male albino rats. ZANCO J Pure Appl Sci 29(4), 1–11. doi:10.21271/ZJPAS.29.4.1Google Scholar
Hasnain, SZ, Wang, H, Ghia, JE, Haq, N, Deng, Y, Velcich, A, Grencis, R, David, J, Thornton, DJ & Khan, WI (2010). Mucin gene deficiency in mice impairs host resistance to an enteric parasitic infection. Gastroenterology 138, 1763–1771. doi:10.1053/j.gastro.2010.01.045CrossRefGoogle Scholar
Hershko, C & Patz, J (2008). Ironing out the mechanism of anemia in celiac disease. Haematologica 93(12), 1761–1765. doi:10.3324/haematol.2008.000828CrossRefGoogle ScholarPubMed
Holm, G, Norrgren, L, Andresson, T & Thuren, A (1993). Effects of exposure to food contaminated with PBDE, PCN or PCB on reproduction, liver morphology and cytochrome P450 activity in the three-spined stickleback, Gasterosteus aculeatus. Aquatic Toxicol 27, 33–50. doi:10.1016/0166-445X(93)90045-3CrossRefGoogle Scholar
Kiernan, JA (2001). Histological and Histochemical Methods: Theory and Practice, 3rd ed. London, New York and New Delhi: Arnold Publisher, pp. 111–162 and 219–240. doi:10.1016/j.ijheh.2016.09.016Google Scholar
Kosik-Bogacka, DI & Kolasa, A (2012). Histopathological changes in small and large intestines during hymenolepidosis in rats. Folia Biol 60(3–4), 195–198. doi:10.3409/fb60_3-4.195-198CrossRefGoogle ScholarPubMed
Lazăr, L, Loghin, A, Bud, ES, Cerghizan, D, Horváth, E & Nagy, EE (2015). Cyclooxygenase-2 and matrix metalloproteinase-9 expressions correlate with tissue inflammation degree in periodontal disease. Rom J Morphol Embryol 56(4), 1441–1446.Google ScholarPubMed
Ma, T, Iwamoto, GK, Hoa, NT, Akotia, V, Pedram, A, Boivin, MA & Said, HM (2004). TNF-alpha-induced increase in intestinal epithelial tight junction permeability requires NF-kappa B activation. Am J Physiol Gastrointest Liver Physiol 286, G367–G376. doi:10.1152/ajpgi.00173.2003CrossRefGoogle ScholarPubMed
Mesnage, R, Defarge, N, de Vendômois, JS & Séralini, GE (2015). Potential toxic effects of glyphosate and its commercial formulations below regulatory limits. Food Chem Toxicol 84, 133–153. doi:10.1016/j.fct.2015.08.012CrossRefGoogle ScholarPubMed
Mesnage, R, Renney, G, Séralini, GF, Ward, M & Antoniou, M (2017). Multiomics reveal non-alcoholic fatty liver disease in rats following chronic exposure to an ultra-low dose of Roundup herbicide. Sci Rep 6, 1–15. doi:10.1038/srep39328Google Scholar
Mirastschijski, U, Impola, U, Jahkola, T, Karlsmark, T, Ågren, MS & Saarialho-Kere, U (2002). Ectopic localization of matrix metalloproteinase-9 in chronic cutaneous wounds. Hum Pathol 33, 355–364. doi:10.1053/hupa.2002.32221CrossRefGoogle ScholarPubMed
Mohamed, IA, Ahmed, MAI & Saba, RM (2016). Unique efficacy of certain novel herbicides against Culex pipiens (Diptera: Culicidae) larvae mosquito under laboratory conditions. Adv Environ Biol 10, 104–111.Google Scholar
Olaleye, SB, Adaramoye, OA, Erigbali, PP & Adeniyi, OS (2007). Lead exposure increases oxidative stress in the gastric mucosa of HCl/ethanol-exposed rats. World J Gastroenterol 13, 5121. doi:10.3748/wjg.v13.i38.5121CrossRefGoogle ScholarPubMed
Olubuyide, IO, Williamson, RC, Bristol, JB & Read, AE (1984). Goblet cell hyperplasia is a feature of the adaptive response to jejunoileal bypass in rats. Gut 25(1), 62–68. doi:10.1136/gut.25.1.62CrossRefGoogle ScholarPubMed
O'Sullivan, S, Gilmer, JF & Medina, C (2015). Matrix metalloproteinases in inflammatory bowel disease: An update. Mediators Inflamm, 1–15. doi:10.1155/2015/964131CrossRefGoogle ScholarPubMed
Pérez, GL, Vera, MS & Miranda, L (2011). Effects of herbicide glyphosate and glyphosate-based formulations on aquatic ecosystems. In Herbicides and Environment, Kortekamp, A (Ed.). Rijeka, Croatia: In Tech Publications. ISBN:978-953-307-476-4. doi:10.5772/12877.Google Scholar
Ramírez-Duarte, WF, Iang, S, Rondón-Barragán, IS & Eslava-Mocha, PR (2008). Acute toxicity and histopathological alterations of Roundup® herbicide on “cachama blanca” (Piaractus brachypomus). Pesqui Vet Bras 28(11), 547–554.CrossRefGoogle Scholar
Ruppel, ML, Brightwell, BB, Schaefer, J & Marvel, JT (1977). Metabolism and degradation of glyphosate in soil and water. J Agric Food Chem 25, 517–528. doi:10.1021/jf60211a018CrossRefGoogle Scholar
Saba, RM, Mohamed, IA & Ahmed, MAI (2018). Toxicological and biochemical investigation of certain herbicides on Culex pipiens L. (Diptera: Culicidae) mosquitos under laboratory conditions. Adv Nat Appl Sci 12, 6–12. doi:10.22587/anas.2018.12.2.2Google Scholar
Saleh, SHMM, Elghareeb, TA, Ahmed, MAI, Mohamed, IA & El-Din, HAE (2018). Hepato-morpholoy and biochemical studies on the liver of albino rats after exposure to glyphosate-Roundup®. J Basic Appl Zool 79, 48. doi:10.1186/s41936-018-0060-4CrossRefGoogle Scholar
Samanta, P, Pal, S, Mukherjee, AK & Ghosh, AR (2016 b). Pathological (histological and ultrastructural) study in stomach and intestine of Heteropneustes fossilis (Bloch) to excel Mera 71, a glyphosate-based herbicide. J Gastrointest Dig Syst 6, 6. doi:10.4172/2161-069X.1000479Google Scholar
Samanta, P, Pal, S, Mukherjee, AK, Senapati, T & Ghosh, AR (2016 a). Histopathological and ultrastructural alterations in Anabas testudineus exposed to glyphosate-based herbicide, Excel Mera 71 under field and laboratory conditions. J Aquac Res Dev 7, 436. doi:10.4172/2155-9546.1000436Google Scholar
Samsel, A & Seneff, S (2013). Glyphosate's suppression of cytochrome P450 enzymes and amino acid biosynthesis by the gut microbiome: Pathways to modern diseases. Entropy 15, 1416–1463. doi:10.3390/e15041416CrossRefGoogle Scholar
Seifert, WF, Wobbes, T & Hendriks, T (1996). Divergent patterns of matrix metalloproteinase activity during wound healing in ileum and colon of rats. Gut 39, 114–119. doi:10.1136/gut.39.1.114CrossRefGoogle ScholarPubMed
Senapati, T, Mukrjee, AK & Ghosh, AR (2009). Observations on the effect of glyphosate based herbicide on ultra structure (SEM) and enzymatic activity in different regions of alimentary canal and gill of Channa punctatus (Bloch). J Crop Weed 5(1), 233–242.Google Scholar
Silva, V, Montanarella, L, Jones, A, Fernandez-Ugalde, O, Mol, HGJ, Ritsema, CJ & Geissen, V (2018). Distribution of glyphosate and aminomethylphosphonic acid (AMPA) in agricultural topsoils of the European Union. Sci Total Environ 621, 1352–1359. doi:10.1016/j.scitotenv.2017.10.093CrossRefGoogle ScholarPubMed
Stumpf, M, Klinge, U, Wilms, A, Zabrocki, R, Rosch, R, Junge, K, Krones, C & Schumpelick, V (2005). Changes of the extracellular matrix as a risk factor for anastomotic leakage after large bowel surgery. Surgery 137, 229–234. doi:10.1016/j.surg.2004.07.011CrossRefGoogle ScholarPubMed
Tooley, KL, Howarth, GS & Butler, RN (2009). Mucositis and non-invasive markers of small intestinal function. Cancer Biol Ther 8, 753–758. doi:10.4161/cbt.8.9.8232CrossRefGoogle ScholarPubMed
Torretta, V, Katsoyiannis, I, Viotti, P & Rada, E (2018). Critical review of the effects of glyphosate exposure to the environment and humans through the food supply chain. Sustainability 10(4), 95. doi:10.3390/su10040950CrossRefGoogle Scholar
Turkmen, R, Birdane, YO, Demirel, HH, Yavuz, H, Kabu, M & Ince, S (2019). Antioxidant and cytoprotective effects of N-acetylcysteine against subchronic oral glyphosate-based herbicide-induced oxidative stress in rats. Environ Sci Pollut Res 26, 11427–11437. doi:10.1007/s11356-019-04585-5CrossRefGoogle ScholarPubMed
Turkmen, R & Dogan, I (2020). Determination of acute oral toxicity of glyphosate isopropylamine salt in rats. Environ Sci Pollut Res 27, 19298–19303.CrossRefGoogle ScholarPubMed
Vandooren, J, Van den Steen, PE & Opdenakker, G (2013). Biochemistry and molecular biology of gelatinase B or matrix metalloproteinase-9 (MMP9): The next decade. Crit Rev Biochem Mol Biol 48, 222–272. doi:10.3109/10409238.2013.770819CrossRefGoogle ScholarPubMed
Walter, JB & Isreal, MS (1974). General Pathology, 4th ed. Edinburgh, London, New York: Churchill Livingstone, p. 681. doi:10.1002/path.1711580117Google Scholar
Wardill, HR, Bowen, JM & Gibson, RJ (2012). Chemotherapy-induced gut toxicity: Are alterations to intestinal tight junctions pivotal? Cancer Chemother Pharmacol 70, 627–635. doi:10.1007/s00280-012-1989-5CrossRefGoogle ScholarPubMed
Watelet, JB, Demetter, P, Claeys, C, Van Cauwenberge, P, Cuvelier, C & Bachert, C (2005). Neutrophil-derived metalloproteinase-9 predicts healing quality after sinus surgery. Laryngoscope 115, 56–61. doi:10.1097/01.mlg.0000150674.30237.3fCrossRefGoogle ScholarPubMed
Woods, AE & Stirling, JW (2008). Electron microscopy. In Theory and Practice of Histological Techniques, 6th ed., Bancroft, JD & Gamble, M (Eds.), pp. 601–636. Edinburgh: Churchill Livingstone Elsevier.CrossRefGoogle Scholar
Zhao, J, Pacenka, S, Wu, J, Brian, K, Richards, BK, Steenhuis, T, Simpson, K & Hay, AG (2018). Detection of glyphosate residues in companion animal feeds. Environ Pollut 243, 1113–1118. doi:10.1016/j.envpol.2018.08.100CrossRefGoogle ScholarPubMed