Cited by 208Pesticide Exposure and ToxicityParaquat toxicity studies and treatmentsDrug-Induced Hepatotoxicity and Protection

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Oxidative stress responses of rats exposed to Roundup and its active ingredient glyphosate

El-Shenawy, Nahla S.·2009·Environmental Toxicology and Pharmacology

DOI 10.1016/j.etap.2009.06.001

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Abstract

Glyphosate is the active ingredient and polyoxyethyleneamine, the major component, is the surfactant present in the herbicide Roundup formulation. The objective of this study was to analyze potential cytotoxicity of the Roundup and its fundamental substance (glyphosate). Albino male rats were intraperitoneally treated with sub-lethal concentration of Roundup (269.9mg/kg) or glyphosate (134.95mg/kg) each 2 days, during 2 weeks. Hepatotoxicity was monitored by quantitative analysis of the serum alanine aminotransferase (ALT), aspartate aminotransferase (AST), alkaline phosphatase (ALP) activities, total protein, albumin, triglyceride and cholesterol. Creatinine and urea were used as the biochemical markers of kidney damages. The second aim of this study to investigate how glyphosate alone or included in herbicide Roundup affected hepatic reduced glutathione (GSH) and lipid peroxidation (LPO) levels of animals as an index of antioxidant status and oxidative stress, respectively, as well as the serum nitric oxide (NO) and alpha tumour necrosis factor (TNF-α) were measured. Treatment of animals with Roundup induced the leakage of hepatic intracellular enzymes, ALT, AST and ALP suggesting irreversible damage in hepatocytes starting from the first week. It was found that the effects were different on the enzymes in Roundup and glyphosate-treated groups. Significant time-dependent depletion of GSH levels and induction of oxidative stress in liver by the elevated levels of LPO, further confirmed the potential of Roundup to induce oxidative stress in hepatic tissue. However, glyphosate caused significant increases in NO levels more than Roundup after 2 weeks of treatment. Both treatments increased the level of TNF-α by the same manner. The results suggest that excessive antioxidant disruptor and oxidative stress is induced with Roundup than glyphosate.

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Gigante, P., Berni, M., Bussolati, S., Grasselli, F., Grolli, S., Ramoni, R., & Basini, G. (2018) · Animal Reproduction Science · doi:10.1016/j.anireprosci.2018.05.023 · Cited by 55
Glyphosate: Hepatotoxicity, Nephrotoxicity, Hemotoxicity, Carcinogenicity, and Clinical Cases of Endocrine, Reproductive, Cardiovascular, and Pulmonary System Intoxication
Mazuryk, J., Klepacka, K., Kutner, W., & Sharma, P. S. (2024) · ACS Pharmacology & Translational Science · doi:10.1021/acsptsci.4c00046 · Cited by 55
Effects of Glyphosate on Growth Rate, Metabolic Rate and Energy Reserves of Early Juvenile Crayfish, Cherax quadricarinatus M.
Avigliano, L., Fassiano, A. V., Medesani, D. A., de Molina, M. C. R., & Rodríguez, E. M. (2014) · Bulletin of Environmental Contamination and Toxicology · doi:10.1007/s00128-014-1240-7 · Cited by 50
Carcinogenic effects of long-term exposure from prenatal life to glyphosate and glyphosate-based herbicides in Sprague–Dawley rats
Panzacchi, S., Tibaldi, E., Angelis, L. D., Falcioni, L., Giovannini, R., Gnudi, F., Iuliani, M., Manservigi, M., Manservisi, F., Manzoli, I., et al. (2025) · Environmental Health · doi:10.1186/s12940-025-01187-2 · Cited by 49
“Glyphosate and GBHs appear to induce oxidative stress in the liver in different rat strains, also at relatively low doses [47–49].”
Exposure to glyphosate during pregnancy induces neurobehavioral alterations and downregulation of Wnt5a-CaMKII pathway
Coullery, R. P., Pacchioni, A. M., & Rosso, S. B. (2020) · Reproductive Toxicology · doi:10.1016/j.reprotox.2020.08.006 · Cited by 51
“potentiated by the presence of adjuvants [4], or by some synergic reaction between Glyph and the other formulation ingredients [5,6].”
Background
Influence of the spray adjuvant on the toxicity effects of a glyphosate formulation
Coalova, I., de Molina, M. D. C. R., & Chaufan, G. (2014) · Toxicology in Vitro · doi:10.1016/j.tiv.2014.06.014 · Cited by 48
Effects of paraoxon on serum biochemical parameters and oxidative stress induction in various tissues of Wistar and Norway rats
Jafari, M., Salehi, M., Asgari, A., Ahmadi, S., Abbasnezhad, M., Hajihoosani, R., & Hajigholamali, M. (2012) · Environmental Toxicology and Pharmacology · doi:10.1016/j.etap.2012.08.011 · Cited by 48
Toxicity of glyphosate in feed for weanling piglets and the mechanism of glyphosate detoxification by the liver nuclear receptor CAR/PXR pathway
Fu, H., Qiu, S., Yao, X., Gao, F., Tan, P., Teng, T., & Shi, B. (2019) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2019.121707 · Cited by 47
Subchronic exposure to kalach 360 SL-induced endocrine disruption and ovary damage in female rats
Hamdaoui, L., Naifar, M., Rahmouni, F., Harrabi, B., Ayadi, F. M., Sahnoun, Z., & Rebaï, T. (2017) · Archives of Physiology and Biochemistry · doi:10.1080/13813455.2017.1352606 · Cited by 45
The effect of glyphosate-based herbicide Roundup and its co-formulant, POEA, on the motoric activity of rat intestine – In vitro study
Chłopecka, M., Mendel, M., Dziekan, N., & Karlik, W. (2016) · Environmental Toxicology and Pharmacology · doi:10.1016/j.etap.2016.12.010 · Cited by 44
Health effect of agricultural pesticide use in China: implications for the development of GM crops
Zhang, C., Hu, R., Huang, J., Huang, X., Shi, G., Li, Y., Yin, Y., & Chen, Z. (2016) · Scientific Reports · doi:10.1038/srep34918 · Cited by 44
Effects of Sublethal Exposure to a Glyphosate-Based Herbicide Formulation on Metabolic Activities of Different Xenobiotic-Metabolizing Enzymes in Rats
Larsen, K., Najle, R., Lifschitz, A., Maté, L., Lanusse, C., & Virkel, G. (2014) · International Journal of Toxicology · doi:10.1177/1091581814540481 · Cited by 44
“Several investigations reported on the ability of GLP to induce oxidative stress and/or an impairment of the antioxidant defensive mechanisms.(34,35) Generally, shortterm exposure periods to this herbicide lead to increased TBARS production and depleted GSH levels in different tissues.”
Background
Intranasal glyphosate-based herbicide administration alters the redox balance and the cholinergic system in the mouse brain
Gallegos, C. E., Bartos, M., Gumilar, F., Raisman‐Vozari, R., Minetti, A., & Baier, C. J. (2020) · NeuroToxicology · doi:10.1016/j.neuro.2020.01.007 · Cited by 40
Glyphosate potentiates insulin resistance in skeletal muscle through the modulation of IRS-1/PI3K/Akt mediated mechanisms: An in vivo and in silico analysis
Jayaraman, S., Krishnamoorthy, K., Prasad, M., Veeraraghavan, V. P., Krishnamoorthy, R., Alshuniaber, M. A., Gatasheh, M. K., Elrobh, M. S., & Gunassekaran (2023) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2023.124917 · Cited by 41
Toxicological concerns regarding glyphosate, its formulations, and co-formulants as environmental pollutants: a review of published studies from 2010 to 2025
Klátyik, S., Simon, G., Takács, E., Oláh, M., Zaller, J. G., Antoniou, M. N., Benbrook, C., Mesnage, R., & Székács, A. (2025) · Archives of Toxicology · doi:10.1007/s00204-025-04076-2 · Cited by 45
“Oxidative stress, as well as glutamatergic excitotoxicity, neuroinflammation, deformities, and mitochondrial dysfunction, can be induced (El-Shenawy 2009; Paganelli et al. 2010; Cattani et al. 2017; Winstone et al. 2022), resulting in neuronal death via necrosis, apoptosis, or autophagy.”
Morus alba leaf extract mediates neuroprotection against glyphosate-induced toxicity and biochemical alterations in the brain
Rebai, O., Belkhir, M., Boujelben, A., Fattouch, S., & Amri, M. (2017) · Environmental Science and Pollution Research · doi:10.1007/s11356-017-8584-6 · Cited by 40
“dative stress and neuroinflammation (El-Shenawy 2009 ; Astiz et al. 2012).”
Silver nanoparticles testicular toxicity in rat
Elsharkawy, E. E., El-Nasser, M. A., & Kamaly, H. F. (2019) · Environmental Toxicology and Pharmacology · doi:10.1016/j.etap.2019.103194 · Cited by 40
Mapping the key characteristics of carcinogens for glyphosate and its formulations: A systematic review
Rana, I., Nguyen, P. K., Rigutto, G., Louie, A., Lee, J. E., Smith, M. T., & Zhang, L. (2023) · Chemosphere · doi:10.1016/j.chemosphere.2023.139572 · Cited by 39
Effects of chronic glyphosate exposure to pregnant mice on hepatic lipid metabolism in offspring
Ren, X., Dai, P., Perveen, A., Tang, Q., Zhao, L., Jia, X. F., Li, Y., & Li, C. (2019) · Environmental Pollution · doi:10.1016/j.envpol.2019.07.074 · Cited by 39
“Previous research had detected a time-dependent enhancement in triglyceride and cholesterol levels as glyphosate-treated subjects aged (El-Shenawy, 2009; Mesnage et al., 2017), whereas there were contradictory results shown in bullfrog tadpoles (Dornelles and Oliveira, 2016).”
Result
Effects of glyphosate-based herbicide-contaminated diets on reproductive organ toxicity and hypothalamic-pituitary-ovarian axis hormones in weaned piglets
Fu, H., Gao, F., Wang, X., Tan, P., Qiu, S., Shi, B., & Shan, A. (2020) · Environmental Pollution · doi:10.1016/j.envpol.2020.115596 · Cited by 37
Alterations at biochemical, proteomic and transcriptomic levels in liver of tilapia (Oreochromis niloticus) under chronic exposure to environmentally relevant level of glyphosate
Jia, R., Hou, Y., Feng, W., Li, B. J., & Zhu, J. X. (2022) · Chemosphere · doi:10.1016/j.chemosphere.2022.133818 · Cited by 35
The effects of low-toxic herbicide Roundup and glyphosate on mitochondria
Strilbytska, O. M., Tsiumpala, S. A., Kozachyshyn, I. I., Strutynska, T. R., Burdyliuk, N., Lushchak, V. I., & Lushchak, O. V. (2021) · EXCLI journal · doi:10.17179/excli2021-4478 · Cited by 34
“In addition, while glyphosate increased the permeability of the inner mitochondrial membrane for protons and Ca2+, it may induce oxidative stress itself or in its formulations in vivo (El-Shenawy, 2009; Gehin et al., 2006; Olorunsogo, 1990).”
Background
The effect of glyphosate, its metabolites and impurities on erythrocyte acetylcholinesterase activity
Kwiatkowska, M., Nowacka-Krukowska, H., & Bukowska, B. (2014) · Environmental Toxicology and Pharmacology · doi:10.1016/j.etap.2014.04.008 · Cited by 34
Pesticides and the Microbiome-Gut-Brain Axis: Convergent Pathways in the Pathogenesis of Parkinson’s Disease
Kulcsarova, K., Bang, C., Berg, D., & Schaeffer, E. (2023) · Journal of Parkinson’s Disease · doi:10.3233/jpd-230206 · Cited by 40
“…in plants but not in mammals, it is now classiﬁed as probably being carcinogenic to humans (group 2A) [88] and directly neurotoxic for the CNS, inducing changes in the levels of monoaminergic neurotransmitters [89], generating an oxidative environment [90] or glutamatergic excitotoxicity [91].”
Background
Is the Use of Glyphosate in Modern Agriculture Resulting in Increased Neuropsychiatric Conditions Through Modulation of the Gut-brain-microbiome Axis?
Barnett, J. A., Bandy, M. L., & Gibson, D. L. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.827384 · Cited by 38
“Both high dose (65) and low-dose (66) glyphosate exposure reduce key enzymes necessary for reducing ROS including superoxide dismutase and glutathione reductase.”
Background
Effects of exposure to glyphosate on oxidative stress, inflammation, and lung function in maize farmers, Northern Thailand
Sidthilaw, S., Sapbamrer, R., Pothirat, C., Wunnapuk, K., & Khacha-ananda, S. (2022) · BMC Public Health · doi:10.1186/s12889-022-13696-7 · Cited by 35
“The loss of glutathione comes from this antioxidant breaking down glyphosate through the activity of GHS-peroxidase [43].”
Background
Serum biochemical assessment of hepatic and renal functions of rats during oral exposure to glyphosate with zinc
Tizhe, E. V., Ibrahim, N. D.-G., Fatihu, M. Y., Igbokwe, I. O., George, B.-D. J., Ambali, S. F., & Shallangwa, J. M. (2013) · Comparative Clinical Pathology · doi:10.1007/s00580-013-1740-6 · Cited by 32
“It was found that Roundup® and glyphosate caused a relatively high albumin concentration in rats (El-Shenawy 2009).”
BackgroundResultInfluential
The surfactant polyethoxylated tallowamine (POEA) reduces lifespan and inhibits fecundity in Drosophila melanogaster- In vivo and in vitro study
Bednářová, A., Kropf, M., & Krishnan, N. (2019) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2019.109883 · Cited by 32
Glyphosate disrupts redox status and up-regulates metallothionein I and II genes expression in the liver of adult rats. Alleviation by quercetin
Soudani, N., Chaâbane, M., Ghorbel, I., Elwej, A., Boudawara, T. S., & Zeghal, N. (2019) · General Physiology and Biophysics · doi:10.4149/gpb_2018043 · Cited by 31
“Our results were consistent with the previous findings of El-Shenawy (2009) in liver of rats treated with sub-lethal doses of glyphosate.”
BackgroundResultInfluential
Ameliorative effect of N ‐acetylcysteine on the testicular tissue of adult male albino rats after glyphosate‐based herbicide exposure
Hashim, A. R., Bashir, D. W., Yasin, N. A. E., Rashad, M. M., & El-Gharbawy, S. M. (2022) · Journal of Biochemical and Molecular Toxicology · doi:10.1002/jbt.22997 · Cited by 35
Single-cell transcriptome analysis reveals liver injury induced by glyphosate in mice
Wu, J., Sun, X., Wu, C., Hong, X., Xie, L., Shi, Z., Zhao, L., Du, Q., Xiao, W. L., Sun, J., et al. (2023) · Cellular & Molecular Biology Letters · doi:10.1186/s11658-023-00426-z · Cited by 31
“3E and Additional file 2: Table S10), displaying consistency with former statements that GLY could induce inflammatory response in multiple organs, including liver, lung, and small intestine [17, 46, 47].”
BackgroundInfluential
Disruption of cytochrome P450 enzymes in the liver and small intestine in chicken embryos in ovo exposed to glyphosate
Fathi, M. A., Han, G., Kang, R., Shen, D., Shen, J., & Li, C. (2020) · Environmental Science and Pollution Research · doi:10.1007/s11356-020-08269-3 · Cited by 33
“TNF-α is a cytokine involved in systemic inflammation and stimulation of the acute phase reaction, and the primary role of TNF is the regulation of immune cells (Ghareeb et al. 2013).”
Background
Comparative studies on endogenic stress hormones, antioxidant, biochemical and hematological status of metabolic disturbance in albino rat exposed to roundup herbicide and its active ingredient glyphosate
Owagboriaye, F. O., Dedeke, G. A., Ademolu, K. O., Olujimi, O. O., Aladesida, A. A., & Adeleke, M. T. (2019) · Environmental Science and Pollution Research · doi:10.1007/s11356-019-04759-1 · Cited by 32
“In a similar trend, a study conducted by El-Shenawy (2009) compared oxidative stress responses in rats exposed to Roundup and its active ingredient glyphosate for 2 weeks.”
BackgroundResult
A Mixture of Endocrine Disruptors and the Pesticide Roundup® Induce Oxidative Stress in Rabbit Liver When Administered under the Long-Term Low-Dose Regimen: Reinforcing the Notion of Real-Life Risk Simulation
Vardakas, P., Veskoukis, A. S., Rossiou, D., Gournikis, C., Kapetanopoulou, T., Karzi, V., Docea, A. O., Tsatsakis, A. M., & Kouretas, D. (2022) · Toxics · doi:10.3390/toxics10040190 · Cited by 30
Ultrastructural hepatocytic alterations induced by silver nanoparticle toxicity
Almansour, M. I., Sajti, L., Melhim, W., & Jarrar, B. M. (2016) · Ultrastructural Pathology · doi:10.3109/01913123.2016.1150377 · Cited by 28
“Mitochondrial cristae play an important role in the function of this organelle [46 – 48].”
Oral Application of Charcoal and Humic acids to Dairy Cows Influences Clostridium botulinum Blood Serum Antibody Level and Glyphosate Excretion in Urine
Gerlach, A. (2014) · Journal of Clinical Toxicology · doi:10.4172/2161-0495.1000186 · Cited by 27
“ROS and lipid peroxidation are induced by glyphosate [45,46].”
Background
Glyphosate: Impact on the microbiota-gut-brain axis and the immune-nervous system, and clinical cases of multiorgan toxicity
Mazuryk, J., Klepacka, K., Kutner, W., & Sharma, P. S. (2024) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2024.115965 · Cited by 27
The Herbicide Glyphosate and Its Apparently Controversial Effect on Human Health: An Updated Clinical Perspective
Caiati, C., Pollice, P., Favale, S., & Lepera, M. E. (2019) · Endocrine Metabolic & Immune Disorders - Drug Targets · doi:10.2174/1871530319666191015191614 · Cited by 26
Effects of melatonin in rats in the initial third stage of pregnancy exposed to sub-lethal doses of herbicides
de Almeida, L. L., Teixeira, Á. A. C., Soares, A. F., da Cunha, F. M., da Silva, V. A., Filho, L. D. V., & Teixeira, V. W. (2017) · Acta Histochemica · doi:10.1016/j.acthis.2017.01.003 · Cited by 24
“Consequently, enzyme inactivity, DNA damages, lipid perxidation and cell death ensue (El-Shenawy, 2009; Hermes-Lima, 004) which probably explains our morphometric results.”
Glyphosate-based herbicide has soil-mediated effects on potato glycoalkaloids and oxidative status of a potato pest
Rainio, M. J., Margus, A., Virtanen, V., Lindström, L., Salminen, J., Saikkonen, K., & Helander, M. L. (2020) · Chemosphere · doi:10.1016/j.chemosphere.2020.127254 · Cited by 25
Roundup-induced biochemical and histopathological changes in the liver and kidney of rats: the ameliorative effects of Linum usitatissimum oil
Djaber, N., Ounaceur, L. S., Moubine, B. N., Khaldi, T., Rouag, M., Berrouague, S., Amara, H., Taïbi, F., Boumendjel, M., Boumendjel, A., et al. (2020) · Acta Biochimica Polonica · doi:10.18388/abp.2020_2898 · Cited by 26
“This was due to the oxidation of GSH to GSSG to protect cells against oxidative damage (El-Shenawy, 2009; Hamdaoui et al., 2016; Kasmi et al., 2018).”
BackgroundMethodInfluential
Low Doses of Glyphosate/Roundup Alter Blood–Testis Barrier Integrity in Juvenile Rats
Gorga, A., Rindone, G. M., Centola, C. L., Sobarzo, C., Pellizzari, E. H., Camberos, M. D. C., Marín-Briggiler, C. I., Cohen, D. J., Riera, M. F., Galardo, M. N., et al. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.615678 · Cited by 24
“As it has been observed that G and R increase oxidative stress in rat liver (61, 62), we then hypothesized that herbicides might cause a disturbance in redox balance that could be responsible for the alteration in BTB permeability.”
Background
Trends in science on glyphosate toxicity: a scientometric study
Rezende, E. C. N., Carneiro, F. M., de Moraes, J. B., & Wastowski, I. J. (2021) · Environmental Science and Pollution Research · doi:10.1007/s11356-021-14556-4 · Cited by 25
“In El-Shenawy 2009 evaluated the cytotoxic potential of glyphosate and Roundup.”
Background

Authors: El-Shenawy, N. S.
Venue: Environmental Toxicology and Pharmacology
Publisher: Elsevier BV
Published: 2009-11
Volume: 28
Issue: 3
Pages: 379-385
ISSN: 1382-6689 (ISSN-L)
DOI: 10.1016/j.etap.2009.06.001
OpenAlex: W2158634663
Cited by: 207
References: 39
Citations by year: 2026: 16 · 2025: 10 · 2024: 13 · 2023: 16 · 2022: 24 · 2021: 18 · 2020: 18 · 2019: 24 · 2018: 9 · 2017: 12 · 2016: 11 · 2015: 3 · 2014: 16 · 2013: 11 · 2012: 4
FWCI: 2.43
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Environmental Toxicology and Pharmacology (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Pharmacology, Toxicology and Pharmaceutics › Toxicology › Pesticide Exposure and Toxicity
Life Sciences › Pharmacology, Toxicology and Pharmaceutics › Toxicology › Paraquat toxicity studies and treatments
Life Sciences › Pharmacology, Toxicology and Pharmaceutics › Pharmacology › Drug-Induced Hepatotoxicity and Protection
Keywords: glyphosate, Roundup, herbicide toxicity, oxidative stress, hepatotoxicity, reduced glutathione, lipid peroxidation, nitric oxide, TNF-α, antioxidant status, alanine aminotransferase, aspartate aminotransferase, alkaline phosphatase, kidney injury, rats

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Oxidative stress responses of rats exposed to Roundup and its active ingredient glyphosate

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