Anogenital distance as a marker of androgen exposure in humans
Open accessAbstract
Abnormal foetal testis development has been proposed to underlie common disorders of the male reproductive system such as cryptorchidism, hypospadias, reduced semen quality and testicular germ cell tumour, which are regarded as components of a 'testicular dysgenesis syndrome'. The increasing trends and geographical variation in their incidence have been suggested to result from in utero exposure to environmental chemicals acting as endocrine disruptors. In rodents, the anogenital distance (AGD), measured from the anus to the base of genital tubercle, is a sensitive biomarker of androgen exposure during a critical embryonic window of testis development. In humans, several epidemiological studies have shown alterations in AGD associated with prenatal exposure to several chemicals with potential endocrine disrupting activity. However, the link between AGD and androgen exposure in humans is not well-defined. This review focuses on the current evidence for such a relationship. As in rodents, a clear gender difference is detected during foetal development of the AGD in humans which is maintained thereafter. Reduced AGD in association with clinically relevant outcomes of potential environmental exposures, such as cryptorchidism or hypospadias, is in keeping with AGD as a marker of foetal testicular function. Furthermore, AGD may reflect variations in prenatal androgen exposure in healthy children as shorter AGD at birth is associated with reduced masculine play behaviour in preschool boys. Several studies provide evidence linking shorter AGD with lower fertility, semen quality and testosterone levels in selected groups of adults attending andrology clinics. Overall, the observational data in humans are consistent with experimental studies in animals and support the use of AGD as a biomarker of foetal androgen exposure. Future studies evaluating AGD in relation to reproductive hormones in both infants and adults, and to gene polymorphisms, will help to further delineate the effect of prenatal and postnatal androgen exposures on AGD.
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Higher androgen levels result in greater AGD length, and lower levels result in shorter AGD length.
“Higher androgen levels result in greater AGD length, and lower levels result in shorter AGD length.”
From Prenatal Origins of Endometriosis Pathology and Pain: Reviewing the Evidence of a Role for Low Testosterone (2023) · cites this paper as [12]
The Introduction (page unavailable) describes AGD as a marker of prenatal androgen action, and the Conclusion (page unavailable) reports observational evidence linking AGD with fetal androgen exposure. But the Introduction says causal evidence in humans is indirect; the claim presents the relationship as a definite result of higher or lower androgen levels without limiting it to fetal exposure. (LLM, conf=0.87)
Experimental — accuracy not yet measuredAnogenital distance (AGD) provides a proxy for androgen levels during the early programming window of fetal development in both sexes.
“The anogenital distance (AGD), measured either from the anus to the posterior fourchette (AGD-AF) or the anus to the clitoral surface (AGD-AC) (Figure 1),12 provides a convenient, easily measurable proxy for androgen levels present during the early “programming window” of fetal development in both sexes.”
From Prenatal Origins of Endometriosis Pathology and Pain: Reviewing the Evidence of a Role for Low Testosterone (2023) · cites this paper as [12]
The Conclusion links human AGD to fetal androgen exposure, and the Definition and measurement methods section describes AGD measurements in both sexes. However, the paper describes the critical masculinisation programming window specifically in fetal male development; it does not establish that AGD reflects androgen levels during that same early window in both sexes. (LLM, conf=0.84)
Experimental — accuracy not yet measuredAltered androgen exposure during the second trimester is likely a significant factor in the etiology of hypospadias.
“The etiology of hypospadias is probably multifactorial, but it is likely that altered androgen exposure during the second trimester is a significant factor [9].”
From Alternative (backdoor) androgen production and masculinization in the human fetus (2019) · cites this paper as [9]
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Cites
Evidence for decreasing quality of semen during past 50 years.
Carlsen, E., Giwercman, A., Keiding, N., & Skakkebæk, N. E. (1992) · BMJ · doi:10.1136/bmj.305.6854.609 · Cited by 2,768 · see citing works
Consensus Statement on Management of Intersex Disorders
Lee, P. A., Houk, C. P., Ahmed, S. F., Hughes, I. A., & in collaboration with the participants in the International Consensus Conference on Intersex organized by the Lawson Wilkins Pediatric Endocrine Society and the European Society for Paediatric Endocrinology (2006) · Pediatrics · doi:10.1542/peds.2006-0738 · Cited by 2,324 · see citing works
Self-citationSkakkebæk, N. E., Meyts, E. R., & Main, K. M. (2001) · Human Reproduction · doi:10.1093/humrep/16.5.972 · Cited by 2,261 · see citing works
Decrease in anogenital distance among male infants with prenatal phthalate exposure
Swan, S. H., Main, K. M., Liu, F., Stewart, S. L., Kruse, R. L., Calafat, A. M., Mao, C. S., Redmon, J. B., Ternand, C. L., Sullivan, S., et al. (2005) · Environmental Health Perspectives · doi:10.1289/ehp.8100 · Cited by 1,586 · see citing works
Consensus statement on management of intersex disorders
Hughes, I. A. (2005) · Archives of Disease in Childhood · doi:10.1136/adc.2006.098319 · Cited by 1,414 · see citing works
Self-citationGlobal Disorders of Sex Development Update since 2006: Perceptions, Approach and Care
Lee, P. A., Nordenström, A., Houk, C. P., Ahmed, S. F., Auchus, R. J., Baratz, A. B., Dalke, K. B., Liao, L., Lin‐Su, K., Looijenga, L. H. J., et al. (2016) · Hormone Research in Paediatrics · doi:10.1159/000442975 · Cited by 1,292 · see citing works
Chamberlain, N. L., Driver, E. D., & Miesfeld, R. L. (1994) · Nucleic Acids Research · doi:10.1093/nar/22.15.3181 · Cited by 1,149 · see citing works
Welsh, M., Saunders, P. T. K., Fisken, M., Scott, H. M., Hutchison, G. R., Smith, L. B., & Sharpe, R. M. (2008) · Journal of Clinical Investigation · doi:10.1172/jci34241 · Cited by 781 · cited 8× · see citing works
“Hypospadias and cryptorchidism are relevant clinical disorders to evaluate the possible role of endocrine disruption, for which there is ample evidence from animal studies (Welsh et al., 2008; van den Driesche et al., 2012).”
InfluentialMcDade, T. W., Williams, S., & Snodgrass, J. J. (2007) · Demography · doi:10.1353/dem.2007.0038 · Cited by 712 · see citing works
Yeh, S., Tsai, M.-Y., Xu, Q., Mu, X., Lardy, H. A., Huang, K., Lin, H., Yeh, S.-D., Altuwaijri, S., Zhou, X., et al. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.212474399 · Cited by 668 · see citing works
Androgen insensitivity syndrome
Hughes, I. A., Davies, J. D., Bunch, T., Pasterski, V., Mastroyannopoulou, K., & MacDougall, J. (2012) · The Lancet · doi:10.1016/s0140-6736(12)60071-3 · Cited by 556 · see citing works
Self-citationAbbott, D. H., Barnett, D. K., Bruns, C. M., & Dumesic, D. A. (2005) · Human Reproduction Update · doi:10.1093/humupd/dmi013 · Cited by 555 · see citing works
Early Androgens Are Related to Childhood Sex-Typed Toy Preferences
Berenbaum, S. A., & Hines, M. (1992) · Psychological Science · doi:10.1111/j.1467-9280.1992.tb00028.x · Cited by 481 · see citing works
Activation of the hypothalamic-pituitary-gonadal axis in infancy: minipuberty
Kuiri-Hänninen, T., Sankilampi, U., & Dunkel, L. (2014) · Hormone Research in Paediatrics · doi:10.1159/000362414 · Cited by 470 · see citing works
Biological functions of hCG and hCG-related molecules
Cole, L. A. (2010) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-8-102 · Cited by 462 · see citing works
Mylchreest, E. (2000) · Toxicological Sciences · doi:10.1093/toxsci/55.1.143 · Cited by 452 · see citing works
Hines, M., Brook, C. G. D., & Conway, G. S. (2004) · The Journal of Sex Research · doi:10.1080/00224490409552215 · Cited by 437 · see citing works
Hypophyso-Gonadal Function in Humans during the First Year of Life
Forest, M. G., Sizonenko, P. C., Cathiard, A. M., & Bertrand, J. (1974) · Journal of Clinical Investigation · doi:10.1172/jci107621 · Cited by 429 · see citing works
Association between prenatal exposure to phthalates and the health of newborns☆
Huang, P., KUO, P., CHOU, Y., LIN, S., & Lee, C.-L. (2008) · Environment International · doi:10.1016/j.envint.2008.05.012 · Cited by 338 · see citing works
Pasterski, V., Geffner, M. E., Brain, C. E., Hindmarsh, P. C., Brook, C. G. D., & Hines, M. (2005) · Child Development · doi:10.1111/j.1467-8624.2005.00843.x · Cited by 335 · see citing works
Self-citationDean, A., & Sharpe, R. M. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-4057 · Cited by 286 · see citing works
Prenatal Phthalate Exposures and Anogenital Distance in Swedish Boys
Bornehag, C., Carlstedt, F., Jönsson, B., Lindh, C. H., Jensen, T. K., Bodin, A., Jonsson, C., Janson, S., & Swan, S. H. (2014) · Environmental Health Perspectives · doi:10.1289/ehp.1408163 · Cited by 276 · see citing works
Gallavan, R. H., Holson, J. F., Stump, D. G., Knapp, J. T. H., & Reynolds, V. L. (1999) · Reproductive Toxicology · doi:10.1016/s0890-6238(99)00036-2 · Cited by 275 · see citing works
Early androgen exposure and human gender development
Hines, M., Constantinescu, M., & Spencer, D. (2015) · Biology of Sex Differences · doi:10.1186/s13293-015-0022-1 · Cited by 263 · see citing works
Anogenital distance in human male and female newborns: a descriptive, cross-sectional study
Salazar-Martı́nez, E., Romano-Riquer, P., Yanez-Marquez, E., Longnecker, M. P., & Hernández‐Ávila, M. (2004) · Environmental Health · doi:10.1186/1476-069x-3-8 · Cited by 244 · see citing works
Mcintyre, B. (2001) · Toxicological Sciences · doi:10.1093/toxsci/62.2.236 · Cited by 239 · see citing works
Boas, M., Boisen, K. A., Virtanen, H., Kaleva, M., Suomi, A.-M., Schmidt, I. M., Damgaard, I., Kai, C. M., Chellakooty, M., Skakkebaek, N., et al. (2006) · European Journal of Endocrinology · doi:10.1530/eje.1.02066 · Cited by 226 · see citing works
Skakkebæk, N. E., Meyts, E. R. D., & Main, K. M. (2001) · Apmis · doi:10.1111/j.1600-0463.2001.tb05770.x · Cited by 224 · see citing works
Bergadá, I., Milani, C., Bedecarrás, P., Andreone, L., Ropelato, M. G., Gottlieb, S., Bergadá, C., Campo, S., & Rey, R. A. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-1079 · Cited by 219 · see citing works
Shorter Anogenital Distance Predicts Poorer Semen Quality in Young Men in Rochester, New York
Mendiola, J., Stahlhut, R. W., Jørgensen, N., Liu, F., & Swan, S. H. (2011) · Environmental Health Perspectives · doi:10.1289/ehp.1103421 · Cited by 216 · see citing works
The Relationship between Anogenital Distance, Fatherhood, and Fertility in Adult Men
Eisenberg, M. L., Hsieh, M. H., Walters, R. C., Krasnow, R. E., & Lipshultz, L. I. (2011) · PLoS ONE · doi:10.1371/journal.pone.0018973 · Cited by 213 · see citing works
Toppari, J., Virtanen, H. E., Main, K. M., & Skakkebæk, N. E. (2010) · Birth Defects Research Part A Clinical and Molecular Teratology · doi:10.1002/bdra.20707 · Cited by 212 · see citing works
Foetal exposure to phthalate esters and anogenital distance in male newborns
Suzuki, Y., Yoshinaga, J., Mizumoto, Y., Serizawa, S., & Shiraishi, H. (2011) · International Journal of Andrology · doi:10.1111/j.1365-2605.2011.01190.x · Cited by 211 · see citing works
Associations among hypospadias, cryptorchidism, anogenital distance, and endocrine disruption
Hsieh, M. H., Breyer, B. N., Eisenberg, M. L., & Baskin, L. S. (2008) · Current Urology Reports · doi:10.1007/s11934-008-0025-0 · Cited by 207 · see citing works
Anogenital Distance from Birth to 2 Years: a Population Study
Thankamony, A., Ong, K. K., Dunger, D. B., Acerini, C. L., & Hughes, I. A. (2009) · Environmental Health Perspectives · doi:10.1289/ehp.0900881 · Cited by 204 · see citing works
Self-citationHunt, P. A., Sathyanarayana, S., Fowler, P., & Trasande, L. (2016) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2015-2873 · Cited by 199 · see citing works
Pasterski, V., Hindmarsh, P. C., Geffner, M. E., Brook, C. G. D., Brain, C. E., & Hines, M. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.05.015 · Cited by 184 · see citing works
Self-citationThe descriptive epidemiology of congenital and acquired cryptorchidism in a UK infant cohort
Acerini, C. L., Miles, H. L., Dunger, D. B., et al. (2009) · Archives of Disease in Childhood · doi:10.1136/adc.2008.150219 · Cited by 182 · see citing works
Self-citationHauser, R. B., Skakkebæk, N. E., Hass, U., Toppari, J., Juul, A., Andersson, A., Kortenkamp, A., Heindel, J. J., & Trasande, L. (2015) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2014-4325 · Cited by 180 · see citing works
Thorup, J. M., McLachlan, R. I., Cortes, D., Nation, T. R., Balic, A., Southwell, B. R., & Hutson, J. M. (2010) · Journal of Pediatric Surgery · doi:10.1016/j.jpedsurg.2010.07.030 · Cited by 178 · see citing works
Testosterone measured in infancy predicts subsequent sex-typed behavior in boys and in girls
Lamminmäki, A., Hines, M., Kuiri‐Hänninen, T., Kilpeläinen, L., Dunkel, L., & Sankilampi, U. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.02.013 · Cited by 174 · see citing works
Hughes, I. A., Nihoul‐Feketé, C., Thomas, B., & Cohen‐Kettenis, P. T. (2007) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2007.06.003 · Cited by 173 · see citing works
Self-citationPossible fetal determinants of male infertility
Juul, A., Almstrup, K., Andersson, A., Jensen, T. K., Jørgensen, N., Main, K. M., Meyts, E. R., Toppari, J., & Skakkebæk, N. E. (2014) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2014.97 · Cited by 168 · see citing works
Jørgensen, N., Asklund, C., Carlsen, E., & Skakkebæk, N. E. (2006) · International Journal of Andrology · doi:10.1111/j.1365-2605.2005.00635.x · Cited by 164 · see citing works
In utero exposure to bisphenol-A and anogenital distance of male offspring
Miao, M., Yuan, W., He, Y., Zhou, Z., Wang, J., Gao, E., Li, G., & Li, D. (2011) · Birth Defects Research Part A Clinical and Molecular Teratology · doi:10.1002/bdra.22845 · Cited by 150 · see citing works
Adverse trends in male reproductive health: we may have reached a crucial ‘tipping point’
Andersson, A., Jørgensen, N., Main, K. M., Toppari, J., Meyts, E. R., Leffers, H. C. B., Juul, A., Jensen, T. K., & Skakkebæk, N. E. (2008) · International Journal of Andrology · doi:10.1111/j.1365-2605.2007.00853.x · Cited by 147 · see citing works
Bowman, C., Barlow, N. J., Turner, K. J., Wallace, D. G., & Foster, P. M. D. (2003) · Toxicological Sciences · doi:10.1093/toxsci/kfg128 · Cited by 146 · see citing works
Anogenital ratio: Measure of fetal virilization in premature and full-term newborn infants
Callegari, C. C., Everett, S. L., Ross, M. G., & Brasel, J. A. (1987) · The Journal of Pediatrics · doi:10.1016/s0022-3476(87)80075-6 · Cited by 145 · see citing works
Genome-wide Association Study Identifies Candidate Genes for Male Fertility Traits in Humans
Kosova, G., Scott, N. M., NIEDERBERGER, C. S., Prins, G. S., & Ober, C. (2012) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2012.04.016 · Cited by 144 · see citing works
Thankamony, A., Lek, N., Carroll, D., Williams, M. P. L., Dunger, D. B., Acerini, C. L., Ong, K. K., & Hughes, I. A. (2013) · Environmental Health Perspectives · doi:10.1289/ehp.1307178 · Cited by 143 · see citing works
Self-citationBay, K., Virtanen, H. E., Hartung, S., Ivell, R., Main, K. M., Skakkebæk, N. E., Andersson, A., & Toppari, J. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-0974 · Cited by 141 · see citing works
Hormonal Changes in 3-Month-Old Cryptorchid Boys
Suomi, A., Main, K. M., Kaleva, M. M., Schmidt, I. M., Chellakooty, M., Virtanen, H. E., Boisen, K. A., Damgaard, I. N., Kai, C. M., Skakkebæk, N. E., et al. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-2318 · Cited by 132 · see citing works
Ruth, K. S., Campbell, P. J., Chew, S., Lim, E. M., Hadlow, N., Stuckey, B. G., Brown, S. J., Feenstra, B., Joseph, J., Surdulescu, G. L., et al. (2016) · European Journal of Human Genetics · doi:10.1038/ejhg.2015.102 · Cited by 121 · see citing works
Mendiola, J., Roca, M., Mínguez-Alarcón, L., Mira-Escolano, M.-P., López-Espín, J. J., Barrett, E. S., Swan, S. H., & Torres-Cantero, A. M. (2012) · Environmental Health · doi:10.1186/1476-069x-11-90 · Cited by 114 · see citing works
Low Birth Weight and Subsequent Male Subfertility
François, I., de Zegher, F., Spiessens, C., D’Hooghe, T. M., & Vanderschueren, D. (1997) · Pediatric Research · doi:10.1203/00006450-199712000-00029 · Cited by 113 · see citing works
Barros, C. C., Haro, A. S., Russo, F. J., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0040573 · Cited by 109 · see citing works
Caucasian male infants and boys with hypospadias exhibit reduced anogenital distance
Hsieh, M. H., Eisenberg, M. L., Hittelman, A. B., Wilson, J. M., Tasian, G. E., & Baskin, L. S. (2012) · Human Reproduction · doi:10.1093/humrep/des087 · Cited by 107 · see citing works
Measurement and correlates of ano‐genital distance in healthy, newborn infants
Sathyanarayana, S., Beard, L. A., Zhou, C., & Grady, R. W. (2010) · International Journal of Andrology · doi:10.1111/j.1365-2605.2009.01044.x · Cited by 106 · see citing works
Dadze, S., Wieland, C., Jakubiczka, S., Funke, K. A., Schroder, E., Royer‐Pokora, B., Willers, R., & Wieacker, P. F. (2000) · Molecular Human Reproduction · doi:10.1093/molehr/6.3.207 · Cited by 104 · see citing works
Mira‐Escolano, M., Mendiola, J., Mínguez‐Alarcón, L., Melgarejo, M., Cutillas‐Tolín, A., Roca, M., López‐Espín, J., Noguera‐Velasco, J., & Torres‐Cantero, A. (2014) · BJOG: An International Journal of Obstetrics & Gynaecology · doi:10.1111/1471-0528.12627 · Cited by 101 · see citing works
Sathyanarayana, S., Grady, R. W., Redmon, J. B., Lanciotti, K. I., Barrett, E. S., Janssen, S. J., Nguyen, R. H. N., & Swan, S. H. (2015) · Journal of Pediatric Urology · doi:10.1016/j.jpurol.2014.11.018 · Cited by 96 · see citing works
Acquired cryptorchidism is frequent in infancy and childhood
Wohlfahrt‐Veje, C., Boisen, K. A., Boas, M., et al. (2009) · International Journal of Andrology · doi:10.1111/j.1365-2605.2008.00946.x · Cited by 96 · see citing works
Corbier, P., Dehennin, L., Castanier, M., et al. (1990) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-71-5-1344 · Cited by 96 · see citing works
Jain, V. G., & Singal, A. K. (2013) · Human Reproduction · doi:10.1093/humrep/det286 · Cited by 91 · see citing works
Jensen, M. S., Wilcox, A. J., Olsen, J., Bonde, J. P., Thulstrup, A. M., Ramlau‐Hansen, C. H., & Henriksen, T. B. (2012) · American Journal of Epidemiology · doi:10.1093/aje/kwr421 · Cited by 85 · see citing works
The Critical Role of Androgens in Prostate Development
Wilson, J. D. (2011) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/j.ecl.2011.05.003 · Cited by 81 · see citing works
Pasterski, V., Geffner, M. E., Brain, C. E., Hindmarsh, P. C., Brook, C. G. D., & Hines, M. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.02.007 · Cited by 78 · see citing works
Self-citationThe Measurement of Gender Role Behaviour in Pre‐School Children: a Research Note
Golombok, S. E., & Rust, J. N. (1993) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.1993.tb01072.x · Cited by 78 · see citing works
Endocrine disrupting chemicals: a new and emerging public health problem?
Acerini, C. L. (2006) · Archives of Disease in Childhood · doi:10.1136/adc.2005.088500 · Cited by 76 · see citing works
Self-citationMitchell, R. T., Mungall, W., McKinnell, C., Sharpe, R. M., Cruickshanks, L., Milne, L., & Smith, L. B. (2014) · Endocrinology · doi:10.1210/en.2014-1534 · Cited by 72 · see citing works
Papadopoulou, E., Vafeiadi, M., Agramunt, S., Basagaña, X., Mathianaki, K., Karakosta, P., Spanaki, A., Koutis, A. D., Chatzi, L., Vrijheid, M., et al. (2012) · Paediatric and Perinatal Epidemiology · doi:10.1111/ppe.12022 · Cited by 72 · see citing works
Birth weight and the risk of testicular cancer: A meta‐analysis
Michos, A., Xue, F., & Michels, K. B. (2007) · International Journal of Cancer · doi:10.1002/ijc.22771 · Cited by 71 · see citing works
Mini puberty and its interpretation
Kurtoğlu, S., & Baştuğ, O. (2014) · Türk Pediatri Arşivi · doi:10.5152/tpa.2014.2038 · Cited by 71 · see citing works
The Critical Time Window for Androgen-Dependent Development of the Wolffian Duct in the Rat
Welsh, M., Saunders, P. T. K., & Sharpe, R. M. (2007) · Endocrinology · doi:10.1210/en.2007-0028 · Cited by 70 · see citing works
Wallerand, H., Rémy-Martin, A., Chabannes, É., et al. (2001) · Fertility and Sterility · doi:10.1016/s0015-0282(01)01987-2 · Cited by 69 · see citing works
Pasterski, V., Acerini, C., Dunger, D., Ong, K., Hughes, I., Thankamony, A., & Hines, M. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.01.002 · Cited by 69 · see citing works
Self-citationWolf, C. J. (2004) · Toxicological Sciences · doi:10.1093/toxsci/kfh018 · Cited by 69 · see citing works
Romano-Riquer, S. P., Hernández‐Ávila, M., Gladen, B. C., et al. (2007) · Paediatric and Perinatal Epidemiology · doi:10.1111/j.1365-3016.2007.00810.x · Cited by 67 · see citing works
Vafeiadi, M., Agramunt, S., Papadopoulou, E., Besselink, H. T., Mathianaki, K., Karakosta, P., Spanaki, A., Koutis, A. D., Chatzi, L., Vrijheid, M., et al. (2012) · Environmental Health Perspectives · doi:10.1289/ehp.1205221 · Cited by 65 · see citing works
van den Driesche, S., Kolovos, P., Platts, S., Drake, A. J., & Sharpe, R. M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0030111 · Cited by 63 · see citing works
Adibi, J. J., Lee, M. K., Naimi, A. I., Barrett, E. S., Nguyen, R. H. N., Sathyanarayana, S., Zhao, Y., Thiet, M.-P., Redmon, J. B., & Swan, S. H. (2015) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2015-2370 · Cited by 63 · see citing works
Human Fetal Adenohypophysis: Morphologic and Functional Analysis in vitro
Asa, S. L., Kovacs, K., & Singer, W. (2008) · Neuroendocrinology · doi:10.1159/000125775 · Cited by 61 · see citing works
Safarinejad, M. R., Shafiei, N., & Safarinejad, S. (2010) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2010.06.011 · Cited by 60 · see citing works
The relationship between anogenital distance and azoospermia in adult men
Eisenberg, M. L., Shy, M., Walters, R. C., & Lipshultz, L. I. (2012) · International Journal of Andrology · doi:10.1111/j.1365-2605.2012.01275.x · Cited by 59 · see citing works
Anogenital distance and its application in environmental health research
Liu, C., Xu, X., & Huo, X. (2014) · Environmental Science and Pollution Research · doi:10.1007/s11356-014-2570-z · Cited by 58 · see citing works
Spreading the Clinical Window for Diagnosing Fetal-Onset Hypogonadism in Boys
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- Authors
- Thankamony, A., Pasterski, V., Ong, K. K., Acerini, C. L., & Hughes, I. A.
- Affiliations
- University of Copenhagen (DK)
- University of Cambridge (GB)
- Corresponding author
- Thankamony, A.
- Venue
- Andrology
- Publisher
- Wiley
- Published
- 2016-02-04
- Volume
- 4
- Issue
- 4
- Pages
- 616-625
- ISSN
- 2047-2919 (ISSN-L)
- 2047-2927
- PMC
- PMC6225986
- OpenAlex
- W2254998737
- Cited by
- 238
- References
- 103
- Citations by year
- 2026: 21 · 2025: 16 · 2024: 19 · 2023: 24 · 2022: 33 · 2021: 27 · 2020: 28 · 2019: 30 · 2018: 19 · 2017: 17 · 2016: 3
- FWCI
- 2.08
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Andrology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Apollo (University of Cambridge) (acceptedVersion)
- Funders
- Fifth Framework Programme
- World Cancer Research Fund
- Medical Research Council
- Newlife Foundation for Disabled Children
- Evelyn Trust
- National Institute on Handicapped Research
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sexual Differentiation and Disorders
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Effects and risks of endocrine disrupting chemicals
- Health Sciences › Medicine › Urology › Urological Disorders and Treatments
- Keywords
- anogenital distance, androgen exposure, prenatal androgen exposure, testicular dysgenesis, cryptorchidism, hypospadias, endocrine disruptors, biomarkers, masculinization, semen quality, male fertility, testosterone, sex differences, genetic polymorphism
- MeSH terms
- Androgens, Anthropometry, Female, Genitalia, Female, Genitalia, Male, Humans, Male, Pregnancy, Prenatal Exposure Delayed Effects
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 ›
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