Cited by 196Effects and risks of endocrine disrupting chemicalsPesticide Exposure and ToxicitySperm and Testicular Function

The DOI matches its Crossref record; 61 of the 61 references it cites were found in a registry or an index.

Glyphosate impairs male offspring reproductive development by disrupting gonadotropin expression

Romano, Marco Aurelio, Romano, Renata Marino, Santos, Luciana Dalazen, Wisniewski, Patricia, Campos, Daniele Antonelo, de Souza, Paula Bargi, Viau, Priscila, Bernardi, Maria Martha, Nunes, Maria Tereza, de Oliveira, Claudio Alvarenga·2012·Archives of Toxicology

DOI 10.1007/s00204-011-0788-9

Open this paper in CoChat — free account

Abstract

Sexual differentiation in the brain takes place from late gestation to the early postnatal days. This is dependent on the conversion of circulating testosterone into estradiol by the enzyme aromatase. The glyphosate was shown to alter aromatase activity and decrease serum testosterone concentrations. Thus, the aim of this study was to investigate the effect of gestational maternal glyphosate exposure (50 mg/kg, NOAEL for reproductive toxicity) on the reproductive development of male offspring. Sixty-day-old male rat offspring were evaluated for sexual behavior and partner preference; serum testosterone concentrations, estradiol, FSH and LH; the mRNA and protein content of LH and FSH; sperm production and the morphology of the seminiferous epithelium; and the weight of the testes, epididymis and seminal vesicles. The growth, the weight and age at puberty of the animals were also recorded to evaluate the effect of the treatment. The most important findings were increases in sexual partner preference scores and the latency time to the first mount; testosterone and estradiol serum concentrations; the mRNA expression and protein content in the pituitary gland and the serum concentration of LH; sperm production and reserves; and the height of the germinal epithelium of seminiferous tubules. We also observed an early onset of puberty but no effect on the body growth in these animals. These results suggest that maternal exposure to glyphosate disturbed the masculinization process and promoted behavioral changes and histological and endocrine problems in reproductive parameters. These changes associated with the hypersecretion of androgens increased gonadal activity and sperm production.

Integrity signals

Registry

Crossref · 10.1007/s00204-011-0788-9

Cites

61 of 61 references verified0 citation errors · 0 not checkable

Statistics

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

Claims the paper makes

This paper’s full text isn’t openly available, 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?

A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding
Bradford, M. M. (1976) · Analytical Biochemistry · doi:10.1016/0003-2697(76)90527-3 · Cited by 255,302
Single-Step Method of RNA Isolation by Acid Guanidinium Thiocyanate–Phenol–Chloroform Extraction
Chomczynski, P., & Sacchi, N. (1987) · Analytical Biochemistry · doi:10.1006/abio.1987.9999 · Cited by 65,515
A new mathematical model for relative quantification in real-time RT-PCR
Pfaffl, M. W. (2001) · Nucleic Acids Research · doi:10.1093/nar/29.9.e45 · Cited by 34,610
The Physiology of Reproduction
Legendre, M., & Jalabert, B. (1988) · Annals of Internal Medicine · doi:10.7326/0003-4819-109-2-176_1 · Cited by 7,876
Quantification of mRNA using real-time RT-PCR
Nolan, T., Hands, R. E., & Bustin, S. A. (2006) · Nature Protocols · doi:10.1038/nprot.2006.236 · Cited by 2,247
ORGANIZING ACTION OF PRENATALLY ADMINISTERED TESTOSTERONE PROPIONATE ON THE TISSUES MEDIATING MATING BEHAVIOR IN THE FEMALE GUINEA PIG 1
PHOENIX, C. H., GOY, R. W., GERALL, A. A., & YOUNG, W. C. (1959) · Endocrinology · doi:10.1210/endo-65-3-369 · Cited by 1,934
Sexual Differentiation of the Central Nervous System
MacLusky, N. J., & Naftolin, F. (1981) · Science · doi:10.1126/science.6163211 · Cited by 1,469
Handbook of Pesticide Toxicology
(2001) · Elsevier eBooks · doi:10.1016/b978-0-12-426260-7.x5000-9 · Cited by 1,325
Research Needs for the Risk Assessment of Health and Environmental Effects of Endocrine Disruptors: A Report of the U.S. EPA-Sponsored Workshop
Kavlock, R. J., Daston, G. P., DeRosa, C., Fenner-Crisp, P. A., Gray, L. E., Kaattari, S. L., Lucier, G. W., Luster, M. I., Mac, M. J., Maczka, C., et al. (1996) · Environmental Health Perspectives · doi:10.1289/ehp.96104s4715 · Cited by 1,235
The physiology of male sexual behavior
Meisel, R. (1994) · Medical Entomology and Zoology · Cited by 988

Show all 61 references

Sorted by citations

Trends in glyphosate herbicide use in the United States and globally
Benbrook, C. M. (2016) · Environmental Sciences Europe · doi:10.1186/s12302-016-0070-0 · Cited by 1,890
“changes through endocrine-mediated mechanisms [54, 73, 75, 76, 79, 81, 83].”
Concerns over use of glyphosate-based herbicides and risks associated with exposures: a consensus statement
Myers, J. P., Antoniou, M. N., Blumberg, B., Carroll, L., Colborn, T., Everett, L. G., Hansen, M., Landrigan, P. J., Lanphear, B. P., Mesnage, R., et al. (2016) · Environmental Health · doi:10.1186/s12940-016-0117-0 · Cited by 907
Potential toxic effects of glyphosate and its commercial formulations below regulatory limits
Mesnage, R., Defarge, N., de Vendômois, J. S., & Séralini, G. (2015) · Food and Chemical Toxicology · doi:10.1016/j.fct.2015.08.012 · Cited by 536
Glyphosate: environmental contamination, toxicity and potential risks to human health via food contamination
Bai, S. H., & Ogbourne, S. M. (2016) · Environmental Science and Pollution Research · doi:10.1007/s11356-016-7425-3 · Cited by 439
Ethoxylated adjuvants of glyphosate-based herbicides are active principles of human cell toxicity
Mesnage, R., Bernay, B., & Séralini, G.-E. (2013) · Toxicology · doi:10.1016/j.tox.2012.09.006 · Cited by 424
RETRACTED: Long term toxicity of a Roundup herbicide and a Roundup-tolerant genetically modified maize
Séralini, G.-E., Clair, E., Mesnage, R., Gress, S., Defarge, N., Malatesta, M., Hennequin, D., & de Vendômois, J. S. (2012) · Food and Chemical Toxicology · doi:10.1016/j.fct.2012.08.005 · Cited by 397
“, 2009) and toxic effects thereafter (Benachour and Seralini, 2009), including in vivo (Romano et al., 2012).”
Background
Retracted
The impact and toxicity of glyphosate and glyphosate-based herbicides on health and immunity
Peillex, C., & Pelletier, M. (2020) · Journal of Immunotoxicology · doi:10.1080/1547691x.2020.1804492 · Cited by 348
Republished study: long-term toxicity of a Roundup herbicide and a Roundup-tolerantgenetically modified maize
Séralini, G.-E., Clair, E., Mesnage, R., Gress, S., Defarge, N., Malatesta, M., Hennequin, D., & de Vendômois, J. S. (2014) · Environmental Sciences Europe · doi:10.1186/s12302-014-0014-5 · Cited by 299
Effects of Glyphosate and its Formulation, Roundup, on Reproduction in Zebrafish (Danio rerio)
Webster, T. M. U., Laing, L. V., Florance, H., & Santos, E. M. (2013) · Environmental Science & Technology · doi:10.1021/es404258h · Cited by 238
Glyphosate, a chelating agent—relevant for ecological risk assessment?
Mertens, M., Höss, S., Neumann, G., Afzal, J., & Reichenbecher, W. (2018) · Environmental Science and Pollution Research · doi:10.1007/s11356-017-1080-1 · Cited by 235
Assessment of Glyphosate Induced Epigenetic Transgenerational Inheritance of Pathologies and Sperm Epimutations: Generational Toxicology
Kubsad, D., Nilsson, E. E., King, S. E., Sadler‐Riggleman, I., Beck, D., & Skinner, M. K. (2019) · Scientific Reports · doi:10.1038/s41598-019-42860-0 · Cited by 234
Co-Formulants in Glyphosate-Based Herbicides Disrupt Aromatase Activity in Human Cells below Toxic Levels
Defarge, N., Takács, E., Lozano, V., Mesnage, R., Spiroux de Vendômois, J., Séralini, G.-E., & Székács, A. (2016) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph13030264 · Cited by 205
Transcriptome profile analysis reflects rat liver and kidney damage following chronic ultra-low dose Roundup exposure
Mesnage, R., Arno, M. J., Costanzo, M., Malatesta, M., Séralini, G., & Antoniou, M. N. (2015) · Environmental Health · doi:10.1186/s12940-015-0056-1 · Cited by 198
Roundup disrupts male reproductive functions by triggering calcium-mediated cell death in rat testis and Sertoli cells
Cavalli, V. L. D. L. O., Cattani, D., Rieg, C. E. H., Pierozan, P., Zanatta, L. C. B., Parisotto, E. B., Filho, D. W., Silva, F. R. M. B., Pessoa‐Pureur, R., & Zamoner, A. (2013) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2013.06.043 · Cited by 201
Glyphosate and the key characteristics of an endocrine disruptor: A review
Muñoz, J. P., Bleak, T. C., & Calaf, G. M. (2020) · Chemosphere · doi:10.1016/j.chemosphere.2020.128619 · Cited by 187
Is it time to reassess current safety standards for glyphosate-based herbicides?
Vandenberg, L. N., Blumberg, B., Antoniou, M. N., Benbrook, C., Carroll, L., Colborn, T., Everett, L. G., Hansen, M., Landrigan, P. J., Lanphear, B. P., et al. (2017) · Journal of Epidemiology & Community Health · doi:10.1136/jech-2016-208463 · Cited by 173
Evaluation of estrogen receptor alpha activation by glyphosate-based herbicide constituents
Mesnage, R., Phedonos, A., Biserni, M., Arno, M. J., Balu, S., Corton, J. C., Ugarte, R., & Antoniou, M. N. (2017) · Food and Chemical Toxicology · doi:10.1016/j.fct.2017.07.025 · Cited by 153
Re-registration Challenges of Glyphosate in the European Union
Székács, A., & Darvas, B. (2018) · Frontiers in Environmental Science · doi:10.3389/fenvs.2018.00078 · Cited by 138
Zebrafish: A Versatile Animal Model for Fertility Research
Hoo, J. Y., Kumari, Y., Shaikh, M. F., Hue, S. M., & Goh, B. H. (2016) · BioMed Research International · doi:10.1155/2016/9732780 · Cited by 144
DNA damage and methylation induced by glyphosate in human peripheral blood mononuclear cells (in vitro study)
Kwiatkowska, M., Reszka, E., Woźniak, K., Jabłońska, E., Michałowicz, J., & Bukowska, B. (2017) · Food and Chemical Toxicology · doi:10.1016/j.fct.2017.03.051 · Cited by 129
Effect of glyphosate on the sperm quality of zebrafish Danio rerio
Lopes, F. M., Varela, A. S., Corcini, C. D., da Silva, A. C., Costa, V. G. G., Tavares, G. C., & da Rosa, C. E. (2014) · Aquatic Toxicology · doi:10.1016/j.aquatox.2014.07.006 · Cited by 127
Global transcriptomic profiling demonstrates induction of oxidative stress and of compensatory cellular stress responses in brown trout exposed to glyphosate and Roundup
Webster, T. M. U., & Santos, E. M. (2015) · BMC Genomics · doi:10.1186/s12864-015-1254-5 · Cited by 130
The Ramazzini Institute 13-week pilot study on glyphosate and Roundup administered at human-equivalent dose to Sprague Dawley rats: effects on the microbiome
Mao, Q., Manservisi, F., Panzacchi, S., Mandrioli, D., Menghetti, I., Vornoli, A., Bua, L., Falcioni, L., Lesseur, C., Chen, J., et al. (2018) · Environmental Health · doi:10.1186/s12940-018-0394-x · Cited by 124
Evaluation of carcinogenic potential of the herbicide glyphosate, drawing on tumor incidence data from fourteen chronic/carcinogenicity rodent studies
Greim, H. A., Saltmiras, D. A., Mostert, V., & Strupp, C. (2015) · Critical Reviews in Toxicology · doi:10.3109/10408444.2014.1003423 · Cited by 109
The effect of metabolites and impurities of glyphosate on human erythrocytes (in vitro)
Kwiatkowska, M., Huras, B., & Bukowska, B. (2014) · Pesticide Biochemistry and Physiology · doi:10.1016/j.pestbp.2014.01.003 · Cited by 110
An acute exposure to glyphosate-based herbicide alters aromatase levels in testis and sperm nuclear quality
Cassault-Meyer, E., Gress, S., Séralini, G., & Galeraud-Denis, I. (2014) · Environmental Toxicology and Pharmacology · doi:10.1016/j.etap.2014.05.007 · Cited by 104
The Ramazzini Institute 13-week pilot study glyphosate-based herbicides administered at human-equivalent dose to Sprague Dawley rats: effects on development and endocrine system
Manservisi, F., Lesseur, C., Panzacchi, S., Mandrioli, D., Falcioni, L., Bua, L., Manservigi, M., Spinaci, M., Galeati, G., Mantovani, A., et al. (2019) · Environmental Health · doi:10.1186/s12940-019-0453-y · Cited by 102
Perinatal Exposure to Glyphosate and a Glyphosate-Based Herbicide Affect Spermatogenesis in Mice
Pham, T. H., Derian, L., Kervarrec, C., Kernanec, P.-Y., Jégou, B., Smagulova, F. O., & Gély-Pernot, A. (2019) · Toxicological Sciences · doi:10.1093/toxsci/kfz039 · Cited by 99
Glyphosate and glyphosate‐based herbicide exposure during the peripartum period affects maternal brain plasticity, maternal behaviour and microbiome
Dechartres, J., Pawluski, J. L., Guéguen, M., Jablaoui, A., Maguin, E., Rhimi, M., & Charlier, T. D. (2019) · Journal of Neuroendocrinology · doi:10.1111/jne.12731 · Cited by 100
Daily exposure to silver nanoparticles during prepubertal development decreases adult sperm and reproductive parameters
Mathias, F. T., Romano, R. M., Kizys, M. M. L., Kasamatsu, T. S., Giannocco, G., Chiamolera, M. I., Dias-da-Silva, M. R., & Romano, M. A. (2014) · Nanotoxicology · doi:10.3109/17435390.2014.889237 · Cited by 97
Self-citation
A comprehensive analysis of the animal carcinogenicity data for glyphosate from chronic exposure rodent carcinogenicity studies
Portier, C. J. (2020) · Environmental Health · doi:10.1186/s12940-020-00574-1 · Cited by 96
Are glyphosate and glyphosate-based herbicides endocrine disruptors that alter female fertility?
Ingaramo, P. I., Alarcón, R., Muñoz‐de‐Toro, M., & Luque, E. H. (2020) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2020.110934 · Cited by 99
Perinatal exposure to a glyphosate-based herbicide impairs female reproductive outcomes and induces second-generation adverse effects in Wistar rats
Milesi, M. M., Lorenz, V., Pacini, G., Repetti, M. R., Demonte, L. D., Varayoud, J., & Luque, E. H. (2018) · Archives of Toxicology · doi:10.1007/s00204-018-2236-6 · Cited by 94
Glyphosate-based herbicides influence antioxidants, reproductive hormones and gut microbiome but not reproduction: A long-term experiment in an avian model
Ruuskanen, S., Rainio, M. J., Gómez-Gallego, C., Selenius, O., Salminen, S., Collado, M. C., Saikkonen, K., Saloniemi, I., & Helander, M. L. (2020) · Environmental Pollution · doi:10.1016/j.envpol.2020.115108 · Cited by 91
Effect of glyphosate on reproductive organs in male rat
Dai, P., Hu, P., Tang, J., Li, Y., & Li, C. (2016) · Acta Histochemica · doi:10.1016/j.acthis.2016.05.009 · Cited by 90
Perinatal exposure to glyphosate-based herbicide alters the thyrotrophic axis and causes thyroid hormone homeostasis imbalance in male rats
de Souza, J. S., Kizys, M. M. L., da Conceição, R. R., Glebocki, G., Romano, R. M., Ortiga-Carvalho, T. M., Giannocco, G., da Silva, I. D. C. G., Dias-da-Silva, M. R., Romano, M. A., et al. (2016) · Toxicology · doi:10.1016/j.tox.2016.11.005 · Cited by 85
Self-citation
Association of Lifetime Exposure to Glyphosate and Aminomethylphosphonic Acid (AMPA) with Liver Inflammation and Metabolic Syndrome at Young Adulthood: Findings from the CHAMACOS Study
Eskenazi, B., Gunier, R. B., Rauch, S. A., Kogut, K. R., Perito, E. R., Mendez, X., Limbach, C., Holland, N., Bradman, A., Harley, K. G., et al. (2023) · Environmental Health Perspectives · doi:10.1289/ehp11721 · Cited by 80
Effects of Roundup and its main component, glyphosate, upon mammalian sperm function and survival
Nerozzi, C., Recuero, S., Galeati, G., Bucci, D., Spinaci, M., & Yeste, M. (2020) · Scientific Reports · doi:10.1038/s41598-020-67538-w · Cited by 81
Formulants of glyphosate-based herbicides have more deleterious impact than glyphosate on TM4 Sertoli cells
Vanlaeys, A., Dubuisson, F., Séralini, G., & Travert, C. (2018) · Toxicology in Vitro · doi:10.1016/j.tiv.2018.01.002 · Cited by 72
Reproductive toxicity due to herbicide exposure in freshwater organisms
Yang, C., Lim, W., & Song, G. (2021) · Comparative Biochemistry and Physiology Part C Toxicology & Pharmacology · doi:10.1016/j.cbpc.2021.109103 · Cited by 67
Pesticides as endocrine disruptors: programming for obesity and diabetes
Miranda, R. A., Silva, B. S., de Moura, E. G., & Lisboa, P. C. (2022) · Endocrine · doi:10.1007/s12020-022-03229-y · Cited by 69
Effects of neonatal exposure to a glyphosate-based herbicide on female rat reproduction
Ingaramo, P. I., Varayoud, J., Milesi, M. M., Schimpf, M. G., Muñoz‐de‐Toro, M., & Luque, E. H. (2016) · Reproduction · doi:10.1530/rep-16-0171 · Cited by 64
Detection of glyphosate residues in companion animal feeds
Zhao, J. J., Pacenka, S., Wu, J. F., Richards, B. K., Steenhuis, T. S., Simpson, K. W., & Hay, A. G. (2018) · Environmental Pollution · doi:10.1016/j.envpol.2018.08.100 · Cited by 62
Controversies on Endocrine and Reproductive Effects of Glyphosate and Glyphosate-Based Herbicides: A Mini-Review
de Araújo-Ramos, A. T., Passoni, M. T., Romano, M. A., Romano, R. M., & Martino‐Andrade, A. J. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.627210 · Cited by 61
Self-citation
Review: Mechanisms of Glyphosate and Glyphosate-Based Herbicides Action in Female and Male Fertility in Humans and Animal Models
Serra, L., Estienne, A., Vasseur, C., Froment, P., & Dupont, J. (2021) · Cells · doi:10.3390/cells10113079 · Cited by 63
Analysis of endocrine disruption effect of Roundup ® in adrenal gland of male rats
Pandey, A., & Medhamurthy, R. (2015) · Toxicology Reports · doi:10.1016/j.toxrep.2015.07.021 · Cited by 61
Prepubertal subchronic exposure to soy milk and glyphosate leads to endocrine disruption
Nardi, J., Bonamigo, M. P., Koeppe, C., Dallegrave, E., Leal, M. B., & Rossato‐Grando, L. G. (2016) · Food and Chemical Toxicology · doi:10.1016/j.fct.2016.12.030 · Cited by 61
Glyphosate-based herbicide formulations and reproductive toxicity in animals
Jarrell, Z. R., Ahammad, M. U., & Benson, A. P. (2020) · Veterinary and Animal Science · doi:10.1016/j.vas.2020.100126 · Cited by 66
Validation of a simple ion chromatography method for simultaneous determination of glyphosate, aminomethylphosphonic acid and ions of Public Health concern in water intended for human consumption
Dovidauskas, S., Okada, I. A., & dos Santos, F. R. (2020) · Journal of Chromatography A · doi:10.1016/j.chroma.2020.461603 · Cited by 59
Effects of Prepubertal Exposure to Silver Nanoparticles on Reproductive Parameters in Adult Male Wistar Rats
Sleiman, H. K., Romano, R. M., de Oliveira, C. A., & Romano, M. A. (2013) · Journal of Toxicology and Environmental Health · doi:10.1080/15287394.2013.831723 · Cited by 58
Self-citation
Effects of parental exposure to glyphosate-based herbicides on embryonic development and oxidative status: a long-term experiment in a bird model
Ruuskanen, S., Rainio, M. J., Uusitalo, M., Saikkonen, K., & Helander, M. L. (2020) · Scientific Reports · doi:10.1038/s41598-020-63365-1 · Cited by 56
Answers to critics: Why there is a long term toxicity due to a Roundup-tolerant genetically modified maize and to a Roundup herbicide
Séralini, G., Mesnage, R., Defarge, N., Gress, S., Hennequin, D., Emilie Clair, A., Malatesta, M., & de Vendômois, J. S. (2012) · Food and Chemical Toxicology · doi:10.1016/j.fct.2012.11.007 · Cited by 56
In vitro evaluation of genomic damage induced by glyphosate on human lymphocytes
Santovito, A., Ruberto, S., Gendusa, C., & Cervella, P. (2018) · Environmental Science and Pollution Research · doi:10.1007/s11356-018-3417-9 · Cited by 53
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
New insights for male infertility revealed by alterations in spermatic function and differential testicular expression of thyroid-related genes
Romano, R. M., Gomes, S. N., Cardoso, N. C. S., Schiessl, L., Romano, M. A., & de Oliveira, C. A. (2016) · Endocrine · doi:10.1007/s12020-016-0952-3 · Cited by 52
Self-citation
Exposure to Roundup® affects behaviour, head regeneration and reproduction of the freshwater planarian Girardia tigrina
López, A. M., Sarmento, R. A., Saraiva, A. D. S., Pereira, R. R., Soares, A. M. V. M., & Pestana, J. L. T. (2019) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2019.04.234 · Cited by 51
Review of Glyphosate-Based Herbicide and Aminomethylphosphonic Acid (AMPA): Environmental and Health Impacts
Ojelade, B. S., Durowoju, O. S., Adesoye, P. O., Gibb, S. W., & Ekosse, G.-I. (2022) · Applied Sciences · doi:10.3390/app12178789 · Cited by 57
Influence of a Roundup formulation on glyphosate effects on steroidogenesis and proliferation of bovine granulosa cells in vitro
Perego, M. C., Caloni, F., Cortinovis, C., Schütz, L. F., Albonico, M., Tsuzukibashi, D., & SPICER, L. J. (2017) · Chemosphere · doi:10.1016/j.chemosphere.2017.09.007 · Cited by 50
Thyroid hormone, gene expression, and Central Nervous System: Where we are
Giannocco, G., Kizys, M. M. L., Maciel, R. M. B., & de Souza, J. S. (2020) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2020.09.007 · Cited by 55
Maternal glyphosate-based herbicide exposure alters antioxidant-related genes in the brain and serum metabolites of male rat offspring
de Souza, J. S., Laureano‐Melo, R., Herai, R. H., da Conceição, R. R., Oliveira, K. C., da Silva, I. D. C. G., Dias-da-Silva, M. R., Romano, R. M., Romano, M. A., Maciel, R. M. B., et al. (2019) · NeuroToxicology · doi:10.1016/j.neuro.2019.06.004 · Cited by 47
Self-citation
Glyphosate-based herbicide exposure during pregnancy and lactation malprograms the male reproductive morphofunction in F1 offspring
Teleken, J. L., Gomes, E. C. Z., Marmentini, C., Moi, M. B., Ribeiro, R. A., Balbo, S. L., Porto, E. M., & Bonfleur, M. L. (2019) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174419000382 · Cited by 48
Epigenetic disruption of estrogen receptor alpha is induced by a glyphosate-based herbicide in the preimplantation uterus of rats
Lorenz, V., Milesi, M. M., Schimpf, M. G., Luque, E. H., & Varayoud, J. (2018) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2018.10.022 · Cited by 49
Ecotoxicology of glyphosate and recent advances in its mitigation by adsorption
Ighalo, J. O., Ajala, O. J., Adeniyi, A. G., Babatunde, E. O., & Ajala, M. A. (2020) · Environmental Science and Pollution Research · doi:10.1007/s11356-020-11521-5 · Cited by 47
Effects of a glyphosate‐based herbicide on the uterus of adult ovariectomized rats
Varayoud, J., Durando, M., Ramos, J. G., Milesi, M. M., Ingaramo, P. I., Muñoz‐de‐Toro, M., & Luque, E. H. (2016) · Environmental Toxicology · doi:10.1002/tox.22316 · Cited by 46
Evaluation of the cytotoxic effects of glyphosate herbicides in human liver, lung, and nerve
Hao, Y., Zhang, Y., Ni, H., Gao, J., Yang, Y., Xu, W., & Tao, L. (2019) · Journal of Environmental Science and Health Part B · doi:10.1080/03601234.2019.1633215 · Cited by 46
The effects of fluorene-9-bisphenol on female zebrafish (Danio rerio) reproductive and exploratory behaviors
Mi, P., Zhang, Q., Zhang, S., Wang, C., Zhang, S.-Z., Fang, Y., Gao, J., Feng, D., Chen, D.-Y., & Feng, X. (2019) · Chemosphere · doi:10.1016/j.chemosphere.2019.04.170 · Cited by 45
Roundup® confers cytotoxicity through DNA damage and Mitochondria-Associated apoptosis induction
Hao, Y., Chen, H., Xu, W., Gao, J., Yang, Y., Zhang, Y., & Tao, L. (2019) · Environmental Pollution · doi:10.1016/j.envpol.2019.05.128 · Cited by 41
Glyphosate exposure attenuates testosterone synthesis via NR1D1 inhibition of StAR expression in mouse Leydig cells
Zhao, L., Zhang, J., Yang, L., Zhang, H., Zhang, Y., Gao, D., Jiang, H., Li, Y., Dong, H., Ma, T., et al. (2021) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2021.147323 · Cited by 42
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
The endoplasmic reticulum stress and related signal pathway mediated the glyphosate-induced testosterone synthesis inhibition in TM3 cells
Xia, Y., Yang, X., Lu, J., Xie, Q., Ye, A., & Sun, W. (2020) · Environmental Pollution · doi:10.1016/j.envpol.2020.113949 · Cited by 38
Glyphosate mimics 17β-estradiol effects promoting estrogen receptor alpha activity in breast cancer cells
Muñoz, J. P., Araya‐Osorio, R., Mera‐Adasme, R., & Calaf, G. M. (2022) · Chemosphere · doi:10.1016/j.chemosphere.2022.137201 · Cited by 40
Male mammary gland development and methylation status of estrogen receptor alpha in Wistar rats are modified by the developmental exposure to a glyphosate-based herbicide
Gómez, A. L., Altamirano, G. A., Leturia, J., Bosquiazzo, V. L., Muñoz‐de‐Toro, M., & Kass, L. (2018) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2018.11.005 · Cited by 41
Exposure to a glyphosate-based herbicide formulation, but not glyphosate alone, has only minor effects on adult rat testis
Johansson, H. K. L., Schwartz, C. L., Nielsen, L. N., Boberg, J., Vinggaard, A. M., Bahl, M. I., & Svingen, T. (2018) · Reproductive Toxicology · doi:10.1016/j.reprotox.2018.09.008 · Cited by 36
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
In utero and lactational exposure to fipronil in female rats: Pregnancy outcomes and sexual development
de Barros, A. L., Rosa, J. D. L., Cavariani, M. M., Borges, C. D. S., Silva, P. V. E., Bae, J. H., Anselmo-Franci, J. A., & Arena, A. C. (2016) · Journal of Toxicology and Environmental Health · doi:10.1080/15287394.2016.1149132 · Cited by 34
Glyphosate and its formulation Roundup impair pig oocyte maturation
Spinaci, M., Nerozzi, C., Tamanini, C., Bucci, D., & Galeati, G. (2020) · Scientific Reports · doi:10.1038/s41598-020-68813-6 · Cited by 34
The dietary risk index system: a tool to track pesticide dietary risks
Benbrook, C., & Davis, D. R. (2020) · Environmental Health · doi:10.1186/s12940-020-00657-z · Cited by 32
The effects of Roundup on gametes and early development of common carp (Cyprinus carpio L)
Ługowska, K. (2018) · Fish Physiology and Biochemistry · doi:10.1007/s10695-018-0498-9 · Cited by 32
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
Adjuvant contributes Roundup's unexpected effects on A549 cells
Hao, Y., Zhang, Y., Cheng, J., Xu, W., Xu, Z., Gao, J., & Tao, L. (2020) · Environmental Research · doi:10.1016/j.envres.2020.109306 · Cited by 30
Endocrine, immune and renal toxicity in male largemouth bass after chronic exposure to glyphosate and Rodeo®
María, M. D., Kroll, K. J., Yu, F., Nouri, M., Silva-Sánchez, C., Pérez, J. G., Amador, D. A. M., Zhang, Y., Walsh, M. T., & Denslow, N. D. (2022) · Aquatic Toxicology · doi:10.1016/j.aquatox.2022.106142 · Cited by 29
Herbicide Metolachlor Causes Changes in Reproductive Endocrinology of Male Wistar Rats
Mathias, F. T., Romano, R. M., Sleiman, H. K., de Oliveira, C. A., & Romano, M. A. (2012) · ISRN Toxicology · doi:10.5402/2012/130846 · Cited by 29
Self-citation
Effects on Puberty of Nutrition-Mediated Endocrine Disruptors Employed in Agriculture
Sakali, A.-K., Bargiota, Α., Fatouros, I. G., Jamurtas, A. Z., Μacut, D., Mastorakos, G. P., & Papagianni, M. (2021) · Nutrients · doi:10.3390/nu13114184 · Cited by 29
GLYPHOSATE AND ITS FORMULATIONS - TOXICITY, OCCUPATIONAL AND ENVIRONMENTAL EXPOSURE
Kwiatkowska, M., Jarosiewicz, P., & Bukowska, B. (2013) · Medycyna Pracy · doi:10.13075/mp.5893.2013.0059 · Cited by 26
The role of endocrine disruptors in ocular surface diseases
Pontelli, R. C. N., Souza, M. C. O., Fantucci, M. Z., de Andrade, M., & Rocha, E. M. (2018) · Medical Hypotheses · doi:10.1016/j.mehy.2018.11.009 · Cited by 26
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
Molecular mechanisms regulating spermatogenesis in vertebrates: Environmental, metabolic, and epigenetic factor effects
Guerra‐Carvalho, B., Carrageta, D. F., Crisóstomo, L., Carvalho, R. A., Alves, M. G., & Oliveira, P. F. (2021) · Animal Reproduction Science · doi:10.1016/j.anireprosci.2021.106896 · Cited by 25
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
Hypothyroidism in Adult Male Rats Alters Posttranscriptional Mechanisms of Luteinizing Hormone Biosynthesis
Romano, R. M., Bargi‐Souza, P., Brunetto, E. L., Goulart-Silva, F., Avellar, M. C. W., de Oliveira, C. A., & Nunes, M. T. (2012) · Thyroid · doi:10.1089/thy.2011.0514 · Cited by 24
Self-citation
Subacute toxicity assessment of diflubenzuron, an insect growth regulator, in adult male rats
de Barros, A. L., Cavalheiro, G. F., de Souza, A. V. M., Traesel, G. K., Anselmo-Franci, J. A., Kassuya, C. A. L., & Arena, A. C. (2014) · Environmental Toxicology · doi:10.1002/tox.22054 · Cited by 24
The hypothalamic–pituitary–testicular axis and the testicular function are modulated after silver nanoparticle exposure
Cavallin, M. D., Wilk, R., de Oliveira, I. M., Cardoso, N. C. S., Khalil, N. M., de Oliveira, C. A., Romano, M. A., & Romano, R. M. (2017) · Toxicology Research · doi:10.1039/c7tx00236j · Cited by 24
Self-citation
Roundup and birth defects Is the public being kept in the dark
Antoniou, M. N., El-Din, E., Habib, M., Howard, C. V., Jennings, R. C. K., Leifert, C., Nodari, R. O., Robinson, C., & Fagan, J. (2011) · Cited by 22
Endocrine disruptors on and in fruits and vegetables: Estimation of the potential exposure of the French population
Lee, A., Bensaada, S., Lamothe, V., Lacoste, M., & Bennetau‐Pelissero, C. (2021) · Food Chemistry · doi:10.1016/j.foodchem.2021.131513 · Cited by 22
The High Cost of Pesticides: Human and Animal Diseases
Hoy, J., & Swanson, N. (2015) · Poultry Fisheries & Wildlife Sciences · doi:10.4172/2375-446x.1000132 · Cited by 23
Roundup-Induced AMPK/mTOR-Mediated Autophagy in Human A549 Cells
Hao, Y., Xu, W., Gao, J., Zhang, Y., Yang, Y., & Tao, L. (2019) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.9b04679 · Cited by 22
Chronic Dietary Exposure of Roosters to a Glyphosate-Based Herbicide Increases Seminal Plasma Glyphosate and AMPA Concentrations, Alters Sperm Parameters, and Induces Metabolic Disorders in the Progeny
Serra, L., Estienne, A., Bourdon, G., Ramé, C., Chevaleyre, C., Didier, P., Chahnamian, M., Balkhi, S. E., Froment, P., & Dupont, J. (2021) · Toxics · doi:10.3390/toxics9120318 · Cited by 21
A natural adjuvant shows the ability to improve the effectiveness of glyphosate application
Hao, Y., Zhang, N., Xu, W., Gao, J., Zhang, Y., & Tao, L. (2019) · Journal of Pesticide Science · doi:10.1584/jpestics.d18-066 · Cited by 22
Toxicological Effects of Roundup® on Drosophila melanogaster Reproduction
Muller, K., Herrera, K. N. G., Talyn, B., & Melchiorre, E. B. (2021) · Toxics · doi:10.3390/toxics9070161 · Cited by 18
A systematic review and meta-analysis of the impacts of glyphosate on the reproductive hormones
Mohammadi, K., Sani, M. A., Safaei, P., Rahmani, J., Molaee-Aghaee, E., & Jafari, S. M. (2021) · Environmental Science and Pollution Research · doi:10.1007/s11356-021-16145-x · Cited by 20
Roundup negatively impacts the behavior and nerve function of the Madagascar hissing cockroach (Gromphadorhina portentosa)
Kanabar, M., Bauer, S., Ezedum, Z. M., Dwyer, I. P., Moore, W. S., Rodriguez, G., Mall, A., Littleton, A. T., Yudell, M., Kanabar, J., et al. (2021) · Environmental Science and Pollution Research · doi:10.1007/s11356-021-13021-6 · Cited by 19

Authors: Romano, M. A., Romano, R. M., Santos, L. D., Wisniewski, P., Campos, D. A., de Souza, P. B., Viau, P., Bernardi, M. M., Nunes, M. T., & de Oliveira, C. A.
Affiliations: Universidade de São Paulo (BR)
Universidade Estadual do Centro-Oeste (BR)
ORCID: Romano, Renata Marino
Santos, Luciana Dalazen
Bernardi, Maria Martha
Nunes, Maria Tereza
Venue: Archives of Toxicology
Publisher: Springer Science and Business Media LLC
Published: 2011-11-26
Volume: 86
Issue: 4
Pages: 663-673
ISSN: 0340-5761 (ISSN-L)
1432-0738
DOI: 10.1007/s00204-011-0788-9
OpenAlex: W2032234709
Semantic Scholar: 88db08f59552be68f6728f8dc2bc605721c9715f
Cited by: 196
References: 61
Citations by year: 2026: 5 · 2025: 7 · 2024: 11 · 2023: 12 · 2022: 13 · 2021: 20 · 2020: 34 · 2019: 21 · 2018: 15 · 2017: 7 · 2016: 14 · 2015: 9 · 2014: 12 · 2013: 8 · 2012: 7
FWCI: 6.48
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Archives of Toxicology (publishedVersion)
PubMed (publishedVersion)
Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT) (publishedVersion)
Funders: Conselho Nacional de Desenvolvimento Científico e Tecnológico
National Institutes of Health
Topics: Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Effects and risks of endocrine disrupting chemicals
Life Sciences › Pharmacology, Toxicology and Pharmaceutics › Toxicology › Pesticide Exposure and Toxicity
Health Sciences › Medicine › Reproductive Medicine › Sperm and Testicular Function
Keywords: glyphosate, prenatal exposure, male reproductive development, gonadotropins, luteinizing hormone, follicle-stimulating hormone, aromatase, testosterone, estradiol, sexual behavior, mate preferences, masculinization, puberty onset, spermatogenesis, seminiferous epithelium, reproductive toxicity, endocrine disruption
MeSH terms: Glyphosate, Animals, Brain, Estradiol, Female, Glycine, Gonadotropins, Pituitary, Herbicides, Luteinizing Hormone, Male, Pituitary Gland, Pregnancy, Prenatal Exposure Delayed Effects, Reproduction, RNA, Messenger, Seminiferous Epithelium, Sexual Maturation, Spermatogenesis, Testosterone, Gene Expression Regulation, Developmental, Maternal Exposure, Rats, Mating Preference, Animal

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

Glyphosate impairs male offspring reproductive development by disrupting gonadotropin expression

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks