Prepubertal exposure to commercial formulation of the herbicide glyphosate alters testosterone levels and testicular morphology
Abstract
Glyphosate is a herbicide widely used to kill weeds both in agricultural and non-agricultural landscapes. Its reproductive toxicity is related to the inhibition of a StAR protein and an aromatase enzyme, which causes an in vitro reduction in testosterone and estradiol synthesis. Studies in vivo about this herbicide effects in prepubertal Wistar rats reproductive development were not performed at this moment. Evaluations included the progression of puberty, body development, the hormonal production of testosterone, estradiol and corticosterone, and the morphology of the testis. Results showed that the herbicide (1) significantly changed the progression of puberty in a dose-dependent manner; (2) reduced the testosterone production, in semineferous tubules' morphology, decreased significantly the epithelium height (P < 0.001; control = 85.8 +/- 2.8 microm; 5 mg/kg = 71.9 +/- 5.3 microm; 50 mg/kg = 69.1 +/- 1.7 microm; 250 mg/kg = 65.2 +/- 1.3 microm) and increased the luminal diameter (P < 0.01; control = 94.0 +/- 5.7 microm; 5 mg/kg = 116.6 +/- 6.6 microm; 50 mg/kg = 114.3 +/- 3.1 microm; 250 mg/kg = 130.3 +/- 4.8 microm); (4) no difference in tubular diameter was observed; and (5) relative to the controls, no differences in serum corticosterone or estradiol levels were detected, but the concentrations of testosterone serum were lower in all treated groups (P < 0.001; control = 154.5 +/- 12.9 ng/dL; 5 mg/kg = 108.6 +/- 19.6 ng/dL; 50 mg/dL = 84.5 +/- 12.2 ng/dL; 250 mg/kg = 76.9 +/- 14.2 ng/dL). These results suggest that commercial formulation of glyphosate is a potent endocrine disruptor in vivo, causing disturbances in the reproductive development of rats when the exposure was performed during the puberty period.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
R appears to be a sex endocrine disruptor in vivo, also in males.
“In addition, R appears to be a sex endocrine disruptor in vivo, also in males (Romano et al., 2010).”
From RETRACTED: Long term toxicity of a Roundup herbicide and a Roundup-tolerant genetically modified maize (2012) · cites this paper as Romano et al., 2010
Cites
1 retracted
Williams, G. M., Kroes, R., & Munro, I. C. (2000) · Regulatory Toxicology and Pharmacology · doi:10.1006/rtph.1999.1371 · Cited by 864 · see citing works
RetractedThe 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 · see citing works
Handbook of Pesticide Toxicology
(2001) · Elsevier eBooks · doi:10.1016/b978-0-12-426260-7.x5000-9 · Cited by 1,325 · see citing works
Handbook of Pesticide Toxicology
Scott, J. G. (1992) · Journal of Environmental Quality · doi:10.2134/jeq1992.00472425002100030037x · Cited by 965 · see citing works
(1976) · Australian Veterinary Journal · doi:10.1111/j.1751-0813.1976.tb05428.x · Cited by 941 · see citing works
(1971) · Annals of Internal Medicine · doi:10.7326/0003-4819-75-4-654_2 · Cited by 714 · see citing works
(2000) · Wiley eBooks · doi:10.1002/9781119265306 · Cited by 697 · see citing works
Differential effects of glyphosate and roundup on human placental cells and aromatase
Richard, S., Moslemi, S., Sipahutar, H., Benachour, N., & Seralini, G.-E. (2005) · Environmental Health Perspectives · doi:10.1289/ehp.7728 · Cited by 619 · see citing works
Tsui, M. T., & Chu, L. M. (2003) · Chemosphere · doi:10.1016/s0045-6535(03)00306-0 · Cited by 610 · see citing works
(1996) · Choice Reviews Online · doi:10.5860/choice.33-6336 · Cited by 464 · see citing works
Caron, K. M., Soo, S.-C., Wetsel, W. C., Stocco, D. M., Clark, B. J., & Parker, K. L. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.21.11540 · Cited by 449 · see citing works
Ojeda, S. R., & Skinner, M. K. (2006) · Elsevier eBooks · doi:10.1016/b978-012515400-0/50043-9 · Cited by 413 · see citing works
Unidentified Inert Ingredients in Pesticides: Implications for Human and Environmental Health
Cox, C. S., & Surgan, M. H. (2006) · Environmental Health Perspectives · doi:10.1289/ehp.9374 · Cited by 370 · see citing works
Walsh, L. P., McCormick, C., Martin, C. F., & Stocco, D. (2000) · Environmental Health Perspectives · doi:10.1289/ehp.00108769 · Cited by 339 · see citing works
Cholesterol and the interaction of proteins with membrane domains
Epand, R. M. (2006) · Progress in Lipid Research · doi:10.1016/j.plipres.2006.02.001 · Cited by 309 · see citing works
Comparative effects of the Roundup and glyphosate on mitochondrial oxidative phosphorylation
Peixoto, F. (2005) · Chemosphere · doi:10.1016/j.chemosphere.2005.03.044 · Cited by 259 · see citing works
Estrogen regulation of testicular function
Akingbemi, B. T. (2005) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-3-51 · Cited by 244 · see citing works
Time- and dose-dependent effects of Roundup on human embryonic and placental cells
Benachour, N., Sipahutar, H., Moslemi, S., Gasnier, C., Travert, C., & Séralini, G. E. (2007) · Archives of Environmental Contamination and Toxicology · doi:10.1007/s00244-006-0154-8 · Cited by 226 · see citing works
Curwin, B., Hein, M. J., Sanderson, W. T., Striley, C., Heederik, D. J. J., Kromhout, H., Reynolds, S. J., & Alavanja, M. (2006) · The Annals of Occupational Hygiene · doi:10.1093/annhyg/mel062 · Cited by 225 · see citing works
Pre- and postnatal toxicity of the commercial glyphosate formulation in Wistar rats
Dallegrave, E., Mantese, F. D. G., de Oliveira, R. T., Martino‐Andrade, A. J., Dalsenter, P. R., & Langeloh, A. (2007) · Archives of Toxicology · doi:10.1007/s00204-006-0170-5 · Cited by 211 · see citing works
Goldman, J., Laws, S., Balchak, S. K., Cooper, R., & Kavlock, R. (2000) · Critical Reviews in Toxicology · doi:10.1080/10408440091159185 · Cited by 200 · see citing works
Stoker, T., Parks, L., Gray, L., & Cooper, R. (2000) · Critical Reviews in Toxicology · doi:10.1080/10408440091159194 · Cited by 185 · see citing works
Rout, U. K., Saed, G. M., & Diamond, M. P. (2005) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-3-1 · Cited by 171 · see citing works
Pesticide Contamination Inside Farm and Nonfarm Homes
Curwin, B., Hein, M. J., Sanderson, W. T., et al. (2005) · Journal of Occupational and Environmental Hygiene · doi:10.1080/15459620591001606 · Cited by 152 · see citing works
Environment and health: 6. Endocrine disruption and potential human health implications.
Solomon, G. M., & Schettler, T. H. (2000) · PubMed · Cited by 137 · see citing works
Neonatal Estrogen Exposure of Male Rats Alters Reproductive Functions at Adulthood1
Goyal, H. O., Robateau, A., Braden, T. D., Williams, C. S., Srivastava, K. K., & Ali, K. (2003) · Biology of Reproduction · doi:10.1095/biolreprod.102.010637 · Cited by 131 · see citing works
Pesticide Roundup Provokes Cell Division Dysfunction at the Level of CDK1/Cyclin B Activation
Marc, J., Mulner‐Lorillon, O., Boulben, S., Hureau, D., Durand, G., & Bellé, R. (2002) · Chemical Research in Toxicology · doi:10.1021/tx015543g · Cited by 131 · see citing works
Brausch, J. M., & Smith, P. N. (2006) · Archives of Environmental Contamination and Toxicology · doi:10.1007/s00244-006-0151-y · Cited by 129 · see citing works
Effect of Roundup Ultra on Microbial Activity and Biomass from Selected Soils
Haney, R. L., Senseman, S. A., & Hons, F. M. (2002) · Journal of Environmental Quality · doi:10.2134/jeq2002.7300 · Cited by 125 · see citing works
The effects of sub-chronic exposure of Wistar rats to the herbicide Glyphosate-Biocarb®
Benedetti, A. L., Vituri, C. D. L., Trentin, A. G., Domingues, M. A. C., & Alvarez‐Silva, M. (2004) · Toxicology Letters · doi:10.1016/j.toxlet.2004.04.008 · Cited by 123 · see citing works
A Review of the Acceptable Daily Intakes of Pesticides Assessed by WHO
Lu, F. C. (1995) · Regulatory Toxicology and Pharmacology · doi:10.1006/rtph.1995.1049 · Cited by 116 · see citing works
Environmental Contaminants and Human Infertility: Hypothesis or Cause for Concern?
Foster, W. G., Neal, M. S., Han, M.-S., & Domínguez, M. M. R. (2008) · Journal of Toxicology and Environmental Health Part B · doi:10.1080/10937400701873274 · Cited by 108 · see citing works
Relationship between acidity and chemical properties of brazilian soils
Abreu–Junior, C. H., Muraoka, T., & Lavorante, A. F. (2003) · Scientia Agricola · doi:10.1590/s0103-90162003000200019 · Cited by 97 · see citing works
Atanassova, N. N., Walker, M., McKinnell, C., et al. (2005) · Journal of Endocrinology · doi:10.1677/joe.1.05884 · Cited by 93 · see citing works
The impact of pesticides on male fertility
Roeleveld, N., & Bretveld, R. W. (2008) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/gco.0b013e3282fcc334 · Cited by 91 · see citing works
Effects of the herbicide Roundup on the epididymal region of drakes Anas platyrhynchos
de Oliveira, A. G., Telles, L. F., Hess, R. A., Mahecha, G. A. B., & Oliveira, C. A. (2006) · Reproductive Toxicology · doi:10.1016/j.reprotox.2006.11.004 · Cited by 86 · see citing works
Self-citationGoldsborough, L. G., & Brown, D. J. (1993) · Environmental Toxicology and Chemistry · doi:10.1002/etc.5620120702 · Cited by 72 · see citing works
Pesticides and fertility: An epidemiological study in Northeast Italy and review of the literature
Clementi, M., Tiboni, G. M., Causin, R., et al. (2008) · Reproductive Toxicology · doi:10.1016/j.reprotox.2008.05.062 · Cited by 62 · see citing works
Review of potential environmental impacts of transgenic glyphosate-resistant soybean in Brazil
Cerdeira, A. L., Gazziero, D. L. P., Duke, S. O., Matallo, M. B., & Spadotto, C. A. (2007) · Journal of Environmental Science and Health Part B · doi:10.1080/03601230701391542 · Cited by 62 · see citing works
Pesticides in Perspective; Pesticide residues in food
Clark, T., & Shaw, I. C. (2000) · Journal of Environmental Monitoring · doi:10.1039/b001748p · Cited by 53 · see citing works
Testing for Reproductive Toxicity
Parker, R. (2005) · Informa Healthcare eBooks · doi:10.1201/9781420040548.ch10 · Cited by 48 · see citing works
Mineralization of Glyphosate in Compost-Amended Soil Under Controlled Conditions
Getenga, Z. M., & Kengara, F. O. (2004) · Bulletin of Environmental Contamination and Toxicology · doi:10.1007/s00128-003-9004-9 · Cited by 34 · see citing works
DETERMINAÇÃO DE GLIFOSATO E ÁCIDO AMINOMETILFOSFÔNICO EM ÁGUAS SUPERFICIAIS DO ARROIO PASSO DO PILÃO
SILVA, M. D. D., Peralba, M. D. C. R., & Mattos, M. L. T. (2003) · Pesticidas Revista de Ecotoxicologia e Meio Ambiente · doi:10.5380/pes.v13i0.3161 · Cited by 33 · see citing works
A exposição ao glifosato-Roundup causa atraso no início da puberdade em ratos machos
Romano, R. M., Romano, M. A., Moura, M. O., et al. (2008) · LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) · doi:10.11606/issn.1678-4456.bjvras.2008.26672 · Cited by 13 · see citing works
Self-citationDevelopmental and Reproductive Toxicology
Jacobs, A. C. (2006) · CRC Press eBooks · doi:10.1201/b14280-12 · Cited by 12 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Glyphosate-based herbicides are toxic and endocrine disruptors in human cell lines
Gasnier, C., Dumont, C., Benachour, N., Clair, E., Chagnon, M.-C., & Séralini, G.-E. (2009) · Toxicology · doi:10.1016/j.tox.2009.06.006 · Cited by 658 · see citing works
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 · see citing works
“In addition, R appears to be a sex endocrine disruptor in vivo, also in males (Romano et al., 2010).”
BackgroundRetractedDefarge, 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 · see citing works
Glyphosate impairs male offspring reproductive development by disrupting gonadotropin expression
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. (2012) · Archives of Toxicology · doi:10.1007/s00204-011-0788-9 · Cited by 196 · see citing works
Self-citation
- Authors
- Romano, R. M., Romano, M. A., Bernardi, M. M., Furtado, P. V., & Oliveira, C. A.
- Affiliations
- Universidade de São Paulo (BR)
- Corresponding author
- Romano, R. M.
- Venue
- Archives of Toxicology
- Published
- 2009-12-12
- Volume
- 84
- Issue
- 4
- Pages
- 309-317
- ISSN
- 0340-5761 (ISSN-L)
- 1432-0738
- OpenAlex
- W2089279540
- Cited by
- 204
- References
- 45
- Citations by year
- 2026: 6 · 2025: 11 · 2024: 11 · 2023: 15 · 2022: 13 · 2021: 21 · 2020: 21 · 2019: 20 · 2018: 17 · 2017: 12 · 2016: 9 · 2015: 7 · 2014: 9 · 2013: 10 · 2012: 14
- FWCI
- 8.90
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Archives of Toxicology (publishedVersion)
- PubMed (publishedVersion)
- Scientific Electronic Library Online (São Paulo Research Foundation, Latin American and Caribbean Center on Health Sciences Information, Conselho Nacional de Desenvolvimento Científico e Tecnológico) (publishedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Pesticide Exposure and Toxicity
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Effects and risks of endocrine disrupting chemicals
- Health Sciences › Medicine › Reproductive Medicine › Sperm and Testicular Function
- Keywords
- glyphosate, herbicide toxicity, endocrine disruptors, reproductive toxicity, prepubertal exposure, puberty, testosterone, testicular morphology, seminiferous tubules, corticosterone, estradiol, Wistar rats
- MeSH terms
- Glyphosate, Adrenal Glands, Animals, Body Weight, Corticosterone, Environmental Exposure, Estradiol, Glycine, Herbicides, Male, Organ Size, Testis, Testosterone, Rats, Wistar, Growth and Development, Rats
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