The DOI matches its Crossref record; 252 of the 254 references it cites were found in a registry or an index.
Developmental variations in environmental influences including endocrine disruptors on pubertal timing and neuroendocrine control: Revision of human observations and mechanistic insight from rodents
Open accessAbstract
Puberty presents remarkable individual differences in timing reaching over 5 years in humans. We put emphasis on the two edges of the age distribution of pubertal signs in humans and point to an extended distribution towards earliness for initial pubertal stages and towards lateness for final pubertal stages. Such distortion of distribution is a recent phenomenon. This suggests changing environmental influences including the possible role of nutrition, stress and endocrine disruptors. Our ability to assess neuroendocrine effects and mechanisms is very limited in humans. Using the rodent as a model, we examine the impact of environmental factors on the individual variations in pubertal timing and the possible underlying mechanisms. The capacity of environmental factors to shape functioning of the neuroendocrine system is thought to be maximal during fetal and early postnatal life and possibly less important when approaching the time of onset of puberty.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The text we found for this paper looks like another document, so the self-check wasn’t run.
Citations
Cites
Positional cloning of the mouse obese gene and its human homologue
Zhang, Y., Proenca, R., Maffei, M., Barone, M., Leopold, L., & Friedman, J. M. (1994) · Nature · doi:10.1038/372425a0 · Cited by 13,419
Tanner, J. M. (1978) · Medical Entomology and Zoology · Cited by 3,742
Campfield, L. A., Smith, F. J., Guisez, Y., Devos, R., & Burn, P. (1995) · Science · doi:10.1126/science.7624778 · Cited by 3,243
INFANT MORTALITY, CHILDHOOD NUTRITION, AND ISCHAEMIC HEART DISEASE IN ENGLAND AND WALES
BARKER, D. (1986) · The Lancet · doi:10.1016/s0140-6736(86)91340-1 · Cited by 2,892
Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54
de Roux, N., Genin, E., Carel, J.-C., Matsuda, F., Chaussain, J.-L., & Milgrom, E. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1834399100 · Cited by 2,431
Role of Brain Insulin Receptor in Control of Body Weight and Reproduction
Brüning, J. C., Gautam, D., Burks, D. J., Gillette, J., Schubert, M., Orban, P. C., Klein, R., Krone, W., Müller-Wieland, D., & Kahn, C. R. (2000) · Science · doi:10.1126/science.289.5487.2122 · Cited by 2,235
MAEDA, K., OHKURA, S., & Tsukamura, H. (2000) · Elsevier eBooks · doi:10.1016/b978-012426400-7/50048-0 · Cited by 2,136
Parent, A.-S., Teilmann, G., Juul, A., Skakkebaek, N. E., Toppari, J., & Bourguignon, J.-P. (2003) · Endocrine Reviews · doi:10.1210/er.2002-0019 · Cited by 1,762
Herman-Giddens, M. E., Slora, E. J., Wasserman, R. C., Bourdony, C. J., Bhapkar, M. V., Koch, G. G., & Hasemeier, C. M. (1997) · PEDIATRICS · doi:10.1542/peds.99.4.505 · Cited by 1,709
Trophic Action of Leptin on Hypothalamic Neurons That Regulate Feeding
Bouret, S. G., Draper, S. J., & Simerly, R. B. (2004) · Science · doi:10.1126/science.1095004 · Cited by 1,247
Cited by
Sorted by citations
Items 101–175 of 175
Rahimi, F., Mirghafourvand, M., Farvareshi, M., & Yavarikia, P. (2023) · BMC Psychiatry · doi:10.1186/s12888-023-05216-7 · Cited by 8
The Gonadal Axis: A Life Perspective
Huhtaniemi, I. T., Howard, S. R., Dunkel, L., & Anderson, R. A. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803592-4.00066-3 · Cited by 9
Choe, Y., Kim, K., Lee, Y. J., Kim, J. I., Kim, B.-N., Lim, Y.-H., Hong, Y., Shin, C. H., & Lee, Y. A. (2024) · Environmental Research · doi:10.1016/j.envres.2024.120056 · Cited by 8
Ikeda, A., Yamaguchi, T., Bamai, Y. A., Roggeman, M., Ikenaka, Y., Zeng, Y., Yasuda, A., Ketema, R. M., Marsela, M., Gys, C., et al. (2025) · Environmental Science & Technology · doi:10.1021/acs.est.4c11436 · Cited by 8
Gan, H., Zhu, B., Zhou, F., Ding, Z., Liu, J., & Ye, X. (2022) · Environmental Science and Pollution Research · doi:10.1007/s11356-022-22328-x · Cited by 8
Xu, L.-N., Li, H., Liu, S., Jiang, J., Liu, Y., Cheng, H. M., Yu, Y., Cao, J.-M., & Zhang, P. (2022) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2022.113723 · Cited by 7
Li, D., Xiong, J., & Cheng, G. (2024) · BMC Public Health · doi:10.1186/s12889-024-18209-2 · Cited by 7
Gaml‐Sørensen, A., Brix, N., Lunddorf, L. L. H., Ernst, A., Høyer, B. B., Olsen, S. F., Granström, C., Toft, G. V., Henriksen, T. B., & Ramlau‐Hansen, C. H. (2023) · Paediatric and Perinatal Epidemiology · doi:10.1111/ppe.12981 · Cited by 6
Xiong, J., Tian, Y., Ma, G., Wang, X., Shan, S., & Cheng, G. (2022) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.202200486 · Cited by 6
Continuous body temperature as a window into adolescent development
Grant, A. D., & Kriegsfeld, L. J. (2023) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2023.101221 · Cited by 6
Goering, M., Albright, M. G., & Mrug, S. (2023) · Journal of Youth and Adolescence · doi:10.1007/s10964-023-01814-6 · Cited by 7
Wang, G., Chen, Y., Lü, W., Chen, H., & Chen, X. (2023) · Chinese Journal of Chromatography · doi:10.3724/sp.j.1123.2023.04005 · Cited by 6
Azogu, I., Cossette, I., Mukunzi, J. N., Ibeke, O., & Plamondon, H. (2019) · Hormones and Behavior · doi:10.1016/j.yhbeh.2019.04.006 · Cited by 7
Genetic regulation in pubertal delay
Howard, S. R. (2019) · Journal of Molecular Endocrinology · doi:10.1530/jme-19-0130 · Cited by 6
Is puberty starting earlier than before?
Oehme, N. H. B., Bruserud, I. S., Madsen, A., & Júlíusson, P. B. (2020) · Tidsskrift for Den norske legeforening · doi:10.4045/tidsskr.20.0043 · Cited by 6
Transient central precocious puberty: a new entity among the spectrum of precocious puberty?
Assirelli, V., Baronio, F., Ortolano, R., Maltoni, G., Zucchini, S., Natale, V. D., & Cassio, A. (2021) · The Italian Journal of Pediatrics/Italian journal of pediatrics · doi:10.1186/s13052-021-01163-9 · Cited by 6
Martino, R. M., Hollinsaid, N. L., Colich, N. L., McLaughlin, K. A., & Hatzenbuehler, M. L. (2025) · Scientific Reports · doi:10.1038/s41598-025-00378-8 · Cited by 7
Messina, A., Langlet, F., & Prévot, V. (2017) · médecine/sciences · doi:10.1051/medsci/20173305014 · Cited by 5
Wang, S., Fang, J., Li, J., Wang, S., Su, P., Wan, Y., Tao, F., & Sun, Y. (2023) · Physiology & Behavior · doi:10.1016/j.physbeh.2023.114305 · Cited by 5
Characterization of pubertal development of girls in rural Bangladesh
Hur, J., Schulze, K. J., Thorne‐Lyman, A., Wu, L. S. F., Shaikh, S., Ali, H., Labrique, A. B., & West, K. P. (2021) · PLoS ONE · doi:10.1371/journal.pone.0247762 · Cited by 4
Paediatric and adolescent gynaecology
Hannema, S. E., & ten Kate‐Booij, M. J. (2019) · Bohn Stafleu van Loghum eBooks · doi:10.1007/978-90-368-2131-5_9 · Cited by 4
Disorders of Puberty: Take a Good History!
Witchel, S. F. (2016) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2016-2116 · Cited by 4
Postnatal Development of GnRH Neuronal Function
Terasawa, E. (2018) · Wiley eBooks · doi:10.1002/9781119233275.ch4 · Cited by 4
Abey, N. O., Ebuehi, O. A. T., & Imaga, N. A. (2021) · Current Research in Physiology · doi:10.1016/j.crphys.2021.12.003 · Cited by 3
Ivell, R., Vinggaard, A. M., Soyama, H., & Anand‐Ivell, R. (2022) · Andrologia · doi:10.1111/and.14566 · Cited by 3
Liu, Y. (2017) · Deep Blue (University of Michigan) · Cited by 3
Huang, Y., Zhang, H., Lv, Y., Yu, L., Liu, H., Xu, S., Chen, T., & Li, Y. (2024) · Environmental Monitoring and Assessment · doi:10.1007/s10661-024-13534-w · Cited by 2
Prenatal exposure to 33 endocrine-disrupting chemicals and pubertal development at age 9 in Spain
Beneíto, A., Carrizosa, C., Alvarez, O., Sarzo, B., Llop, S., Esplugues, A., Grimalt, J. O., Schettgen, T., Sakhi, A. K., Murcia, M., et al. (2026) · Environmental Research · doi:10.1016/j.envres.2026.124527 · Cited by 1
Disorders of Pubertal Development: Precocious Puberty
Cappa, M., & Chioma, L. (2021) · Trends in andrology and sexual medicine · doi:10.1007/978-3-030-80015-4_6 · Cited by 2
Endocrine Disruption in Women: A Cause of PCOS, Early Puberty, or Endometriosis
Wenger, J. M., & Marci, R. (2023) · Springer eBooks · doi:10.1007/978-3-031-36494-5_5 · Cited by 3
Indications of younger age at menarche in Greek adolescents but with no relation to body mass index
Papageorgiou, A., Charmandari, E., Efthymiou, V., Vlachakis, D., & Bacopoulou, F. (2024) · HORMONES · doi:10.1007/s42000-024-00557-8 · Cited by 2
Howard, S. R., & Dunkel, L. (2017) · Springer eBooks · doi:10.1007/978-3-319-53298-1_4 · Cited by 2
Le récepteur neural des œstrogènes bêta
Naulé, L., & Mhaouty‐Kodja, S. (2016) · médecine/sciences · doi:10.1051/medsci/20163205009 · Cited by 2
The Role of the Environment in Female Reproductive Disorders
Papalou, O., & Kandaraki, E. (2023) · Endocrinology · doi:10.1007/978-3-030-39044-0_7 · Cited by 2
Focus on reproductive health and alterations in women
Santosh, W. (2023) · Elsevier eBooks · doi:10.1016/b978-0-12-824464-7.00025-8 · Cited by 2
DiVall, S. A., & Blasi, C. C. D. (2016) · Endocrinology · doi:10.1007/978-3-319-27318-1_25-1 · Cited by 2
Neuroendocrine Regulation of Puberty
Terasawa, E., & Levine, J. E. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803592-4.00106-1 · Cited by 2
Influence of Stress on the GnRH Neuronal Network
Grachev, P., & O'Byrne, K. T. (2018) · Wiley eBooks · doi:10.1002/9781119233275.ch14 · Cited by 2
The Effects of Endocrine Disruptors on Female Gonadal Axis: an Update
Μacut, D. (2023) · Acta Endocrinologica (Bucharest) · doi:10.4183/aeb.2023.81 · Cited by 2
Acrylamide exposure, sex hormones, and pubertal status in Japanese adolescents
Nagata, C., Wada, K., Yamakawa, M., Sugino, M., Mori, T., Ueyama, J., & Sumoto, Y. (2024) · International Journal of Environmental Health Research · doi:10.1080/09603123.2024.2401578 · Cited by 1
Associations between food contaminants exposure and pubertal development at 10 and 13 years old
Costa, S. A., Severo, M., Silva, C. C., Lopes, C. M. M., & Torres, D. P. M. (2026) · Environmental Research · doi:10.1016/j.envres.2026.124905 · Cited by 1
EndoCompass project: environmental endocrinology
Andersson, A., Cianfarani, S., Köhrle, J., Main, K. M., Parent, A., Peeters, R. P., Reincke, M., Saravinovska, K., & Street, M. E. (2025) · European Journal of Endocrinology · doi:10.1093/ejendo/lvaf071 · Cited by 3
Erkudov, V., Rozumbetov, K., Arachchi, S., Rathnayake, U., Матчанов, А. Т., Pugovkin, A., & Lytaev, S. A. (2025) · Global Health Journal · doi:10.1016/j.glohj.2025.10.003 · Cited by 1
Lopez-Rodriguez, D., Aylwin, C. F., Delli, V., Sevrin, E., Campanile, M., Martin, M., Franssen, D., Gerard, A., Blacher, S., Tirelli, E., et al. (2022) · Yearbook of pediatric endocrinology · doi:10.1530/ey.19.7.13 · Cited by 1
Effects of cadmium on children and adolescents development (systematic review)
Bobrisheva-Pushkina, N. D., Kuznetsova, L. Y., Mozganov, M. Y., Araslanova, A. N., Kordina, A. A., & Onishchenko, G. G. (2023) · Hygiene and Sanitation · doi:10.47470/0016-9900-2023-102-9-947-953 · Cited by 1
Dietary quality in mid-pregnancy and pubertal timing in offspring: A population-based cohort study
Wibrand, C., Gaml‐Sørensen, A., Bjerregaard, A. A., Olsen, S. F., & Ramlau‐Hansen, C. H. (2025) · Clinical Nutrition ESPEN · doi:10.1016/j.clnesp.2025.09.006 · Cited by 1
Mazzarino, J., Puel, O., & Jésuran-Pérelroizen, M. (2019) · Archives de Pédiatrie · doi:10.1016/j.arcped.2018.11.009 · Cited by 1
DiVall, S. A., & Blasi, C. C. D. (2018) · Endocrinology · doi:10.1007/978-3-319-44675-2_25 · Cited by 2
Neuroendocrine Disruption of Reproduction
Fudvoye, J., Bourguignon, J.-P., & Parent, A. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-801238-3.65356-4 · Cited by 1
Tet Enzymes: Developmental Fleas of Gnrh Gene Methylation
Anderson, G. M. (2016) · Endocrinology · doi:10.1210/en.2016-1489
Neuroendocrine Disruption of Reproduction
Fudvoye, J., Bourguignon, J.-P., & Parent, A. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-801238-3.11074-8
Howard, S. R., & Dunkel, L. (2019) · Contemporary Endocrinology · doi:10.1007/978-3-030-11339-1_13
Precocious puberty: how about the accelerated bone maturation?
Păduraru, D. N., Botezan, O., Bolocan, A., Andronic, O., Morar, A., Moldovan, C., Alexandra, E. N. E., Socea, B., TURTUREA, R., Carşote, M., et al. (2019) · Archives of the Balkan Medical Union · doi:10.31688/abmu.2019.54.4.26
Tremblay, L., & Larivière, M. A. S. (2020) · The Encyclopedia of Child and Adolescent Development · doi:10.1002/9781119171492.wecad352
Bisphenol A and Puberty Onset in Female Mice: Developmental Effects of Low-Dose Exposure
Schmidt, S. (2020) · Environmental Health Perspectives · doi:10.1289/ehp6574
双酚 A 与雌性小鼠青春期开始时间——低剂量暴露对发育的影响
Schmidt, S. (2020) · Huanjing yu jiankang zhanwang · doi:10.1289/ehp6574-zh
Dong, W., He, J., Wang, J., Sun, W. C., Sun, Y., & Yu, J. (2021) · Research Square · doi:10.21203/rs.3.rs-968620/v1
Eaton, J. L. (2022) · Fertility and Sterility · doi:10.1016/j.fertnstert.2022.05.003
Normale und gestörte Pubertät: Diagnostik und Therapie
Saner, C. C. S., & Flück, C. E. (2022) · Springer Reference Medizin · doi:10.1007/978-3-662-47329-0_13-1
The Role of the Environment in Female Reproductive Disorders
Papalou, O., & Kandaraki, E. (2023) · Endocrinology · doi:10.1007/978-3-030-38366-4_7-1
Disorders of Puberty and Their Management
Dunkel, L., Saengkaew, T., & Howard, S. R. (2023) · Endocrinology · doi:10.1007/978-3-030-18901-3_6-1
Associação entre Bisfenol A e Ftalatos e o desenvolvimento da puberdade precoce em meninas
Soriano, T. M., Bachião, B. P., de, I. B., Gonçalves, B. C. D., & Duarte, A. M. S. C. (2023) · Journal Archives of Health · doi:10.46919/archv4n3-019
Erkudov, V. O., Rozumbetov, K. U., Матчанов, А. Т., Пуговкин, А. П., Nisanova, I. I. N. S. N., Kalmuratova, M. A., Кочубеев, А. В., & Рогозин, С. С. (2024) · Pediatrician (St Petersburg) · doi:10.17816/ped625943
Disorders of Puberty and Their Management
Dunkel, L., Saengkaew, T., & Howard, S. R. (2024) · Endocrinology · doi:10.1007/978-3-030-23709-7_6
Phenanthrene exposure disrupts puberty onset in SD rats by influencing hypothalamic neural networks
Chen, Z., Zhang, Q., Huang, T., Zhang, J., Wu, D., Wu, W., Tian, Y., He, Z., Wang, W., Feng, X., et al. (2025) · Environmental Pollution · doi:10.1016/j.envpol.2025.126933
Male Puberty: Neuroendocrine Disruption of Reproduction
Fudvoye, J., & Parent, A. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-21477-6.00502-2
Neuroendocrine disruption of reproduction
Moralia, M.-A., Fudvoye, J., & Parent, A. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-13825-6.00276-4
Menant, L., Rouget, F., Tillaut, H., Warembourg, C., Rouxel, E., Lainé, F., Gaudreau, É., Cordier, S., Garlantézec, R., Monfort, C., et al. (2025) · Environment International · doi:10.1016/j.envint.2025.109845
EndoCompass Project: Environmental Endocrinology
Andersson, A., Cianfarani, S., Köhrle, J., Main, K. M., Parent, A., Peeters, R. P., Reincke, M., Saravinovska, K., & Street, M. E. (2025) · Hormone Research in Paediatrics · doi:10.1159/000549151 · Cited by 1
Li, D., Xiong, J., & Cheng, G. (2024) · Figshare · doi:10.6084/m9.figshare.25347058
Ashrap, P., Meeker, J. D., Sánchez, B. N., Basu, N., Tamayo-Ortiz, M., Solano-González, M., Mercado-García, A., Téllez-Rojo, M. M., Peterson, K. E., & Watkins, D. J. (2020) · Figshare · doi:10.6084/m9.figshare.13291160
Light pollution and health outcomes in children and adolescents: A systematic review
Ma, J., Sun, Y., & Wang, X. (2026) · Preventive Medicine · doi:10.1016/j.ypmed.2026.108661
Metadata
- Authors
- Parent, A.-S., Franssen, D., Fudvoye, J., Gérard, A., & Bourguignon, J.-P.
- Affiliations
- University of Liège (BE)
- Corresponding author
- Bourguignon, Jean-Pierre
- Venue
- Frontiers in Neuroendocrinology
- Publisher
- Elsevier BV
- Published
- 2015-07
- Volume
- 38
- Pages
- 12-36
- ISSN
- 0091-3022 (ISSN-L)
- OpenAlex
- W2089917595
- Cited by
- 175
- References
- 254
- Citations by year
- 2026: 3 · 2025: 11 · 2024: 12 · 2023: 26 · 2022: 18 · 2021: 16 · 2020: 14 · 2019: 19 · 2018: 13 · 2017: 12 · 2016: 20 · 2015: 11
- FWCI
- 2.80
- Type
- journal article
- Language
- en
- Open access
- green
- orbi.uliege.be
- Licence
- Locations
- Frontiers in Neuroendocrinology (publishedVersion)
- PubMed (publishedVersion)
- Open Repository and Bibliography (University of Liège) (submittedVersion, other-oa)
- Funders
- Belgian Foundation for Research
- European Commission
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Sexual Differentiation and Disorders
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Effects and risks of endocrine disrupting chemicals
- Keywords
- pubertal timing, endocrine disruptors, neuroendocrine regulation, puberty onset, developmental origins of health and disease, nutrition, stress, rodent models
- MeSH terms
- Animals, Environment, Environmental Exposure, Humans, Neurosecretory Systems, Rodentia, Sexual Maturation, Endocrine Disruptors
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
