Developmental Neuroendocrinology of Early-Life Stress: Impact on Child Development and Behavior
- Authors: Nicolaides N.1, Kanaka-Gantenbein C.2, Pervanidou P.3
-
Affiliations:
- Division of Endocrinology, Metabolism and Diabetes, First Department of Pediatric, National and Kapodistrian Uni- versity of Athens, School of Medicine, Aghia Sophia Children's Hospital
- Division of Endocrinology, Metabolism and Diabetes, First Department of Pediatrics, National and Kapodistrian Uni- versity of Athens, School of Medicine, Aghia Sophia Children's Hospital
- Unit of Developmental and Behavioral Pediatrics, First Department of Pediatrics, School of Medicine,, National and Kapodistrian University of Athens, "Aghia Sophia" Children's Hospital
- Issue: Vol 22, No 3 (2024)
- Pages: 461-474
- Section: Neurology
- URL: https://rjpbr.com/1570-159X/article/view/644696
- DOI: https://doi.org/10.2174/1570159X21666230810162344
- ID: 644696
Cite item
Full Text
Abstract
Our internal balance, or homeostasis, is threatened or perceived as threatened by stressful stimuli, the stressors. The stress system is a highly conserved system that adjusts homeostasis to the resting state. Through the concurrent activation of the hypothalamic-pituitary-adrenal axis and the locus coeruleus/norepinephrine-autonomic nervous systems, the stress system provides the appropriate physical and behavioral responses, collectively termed as "stress response", to restore homeostasis. If the stress response is prolonged, excessive or even inadequate, several acute or chronic stress-related pathologic conditions may develop in childhood, adolescence and adult life. On the other hand, earlylife exposure to stressors has been recognized as a major contributing factor underlying the pathogenesis of non-communicable disorders, including neurodevelopmental disorders. Accumulating evidence suggests that early-life stress has been associated with an increased risk for attention deficit hyperactivity disorder and autism spectrum disorder in the offspring, although findings are still controversial. Nevertheless, at the molecular level, early-life stressors alter the chemical structure of cytosines located in the regulatory regions of genes, mostly through the addition of methyl groups. These epigenetic modifications result in the suppression of gene expression without changing the DNA sequence. In addition to DNA methylation, several lines of evidence support the role of non-coding RNAs in the evolving field of epigenetics. In this review article, we present the anatomical and functional components of the stress system, discuss the proper, in terms of quality and quantity, stress response, and provide an update on the impact of early-life stress on child development and behavior.
About the authors
Nicolas Nicolaides
Division of Endocrinology, Metabolism and Diabetes, First Department of Pediatric, National and Kapodistrian Uni- versity of Athens, School of Medicine, Aghia Sophia Children's Hospital
Email: info@benthamscience.net
Christina Kanaka-Gantenbein
Division of Endocrinology, Metabolism and Diabetes, First Department of Pediatrics, National and Kapodistrian Uni- versity of Athens, School of Medicine, Aghia Sophia Children's Hospital
Email: info@benthamscience.net
Panagiota Pervanidou
Unit of Developmental and Behavioral Pediatrics, First Department of Pediatrics, School of Medicine,, National and Kapodistrian University of Athens, "Aghia Sophia" Children's Hospital
Author for correspondence.
Email: info@benthamscience.net
References
- Chrousos, G.P. Stress and disorders of the stress system. Nat. Rev. Endocrinol., 2009, 5(7), 374-381. doi: 10.1038/nrendo.2009.106 PMID: 19488073
- Chrousos, G.P.; Gold, P.W. The concepts of stress and stress system disorders. Overview of physical and behavioral homeostasis. JAMA, 1992, 267(9), 1244-1252. doi: 10.1001/jama.1992.03480090092034 PMID: 1538563
- Nicolaides, N.C.; Kyratzi, E.; Lamprokostopoulou, A.; Chrousos, G.P.; Charmandari, E. Stress, the stress system and the role of glucocorticoids. Neuroimmunomodulation, 2015, 22(1-2), 6-19. doi: 10.1159/000362736 PMID: 25227402
- Stavrou, S.; Nicolaides, N.C.; Critselis, E.; Darviri, C.; Charmandari, E.; Chrousos, G.P. Paediatric stress: From neuroendocrinology to contemporary disorders. Eur. J. Clin. Invest., 2017, 47(3), 262-269. doi: 10.1111/eci.12724
- Nicolaides, N.C.; Charmandari, E.; Kino, T.; Chrousos, G.P. Stress-related and circadian secretion and target tissue actions of glucocorticoids: Impact on health. Front. Endocrinol., 2017, 8, 70. doi: 10.3389/fendo.2017.00070 PMID: 28503165
- Nicolaides, N.C.; Galata, Z.; Kino, T.; Chrousos, G.P.; Charmandari, E. The human glucocorticoid receptor: Molecular basis of biologic function. Steroids, 2010, 75(1), 1-12. doi: 10.1016/j.steroids.2009.09.002 PMID: 19818358
- Nicolaides, N.C.; Chrousos, G.; Kino, T. Endotext; MDText.comIn: Inc.: South Dartmouth (MA),; , 2000.
- Nicolaides, N.C.; Charmandari, E. Primary generalized glucocorticoid resistance and hypersensitivity syndromes: A 2021 update. Int. J. Mol. Sci., 2021, 22(19), 10839. doi: 10.3390/ijms221910839 PMID: 34639183
- Agorastos, A.; Nicolaides, N.C.; Bozikas, V.P.; Chrousos, G.P.; Pervanidou, P. Multilevel interactions of stress and circadian system: Implications for traumatic stress. Front. Psychiatry, 2020, 10, 1003. doi: 10.3389/fpsyt.2019.01003 PMID: 32047446
- Charmandari, E.; Kino, T.; Souvatzoglou, E.; Chrousos, G.P. Pediatric stress: Hormonal mediators and human development. Horm. Res., 2003, 59(4), 161-179. PMID: 12649570
- Charmandari, E.; Tsigos, C.; Chrousos, G. Endocrinology of the stress response. Annu. Rev. Physiol., 2005, 67(1), 259-284. doi: 10.1146/annurev.physiol.67.040403.120816 PMID: 15709959
- Chrousos, G.P. The hypothalamic-pituitary-adrenal axis and immune-mediated inflammation. N. Engl. J. Med., 1995, 332(20), 1351-1363. doi: 10.1056/NEJM199505183322008 PMID: 7715646
- Chrousos, G.P.; Calabrese, J.R.; Avgerinos, P.; Kling, M.A.; Rubinow, D.; Oldfield, E.H.; Schuermeyer, T.; Kellner, C.H.; Cutler, G.B., Jr; Loriaux, D.L.; Gold, P.W. Corticotropin releasing factor: Basic studies and clinical applications. Prog. Neuropsychopharmacol. Biol. Psychiatry, 1985, 9(4), 349-359. doi: 10.1016/0278-5846(85)90187-3 PMID: 2999871
- Calogero, A.E.; Bernardini, R.; Gold, P.W.; Chrousos, G.P. Regulation of rat hypothalamic corticotropin-releasing hormone secretion in vitro: Potential clinical implications. Adv. Exp. Med. Biol., 1988, 245, 167-181. doi: 10.1007/978-1-4899-2064-5_13 PMID: 2906518
- Smith, M.A.; Kling, M.A.; Whitfield, H.J.; Brandt, H.A.; Demitrack, M.A.; Geracioti, T.D.; Chrousos, G.P.; Gold, P.W. Corticotropin-releasing hormone: From endocrinology to psychobiology. Horm. Res., 1989, 31(1-2), 66-71. doi: 10.1159/000181089 PMID: 2656470
- Bornstein, S.R.; Chrousos, G.P. Clinical review 104: Adrenocorticotropin (ACTH)- and non-ACTH-mediated regulation of the adrenal cortex: neural and immune inputs. J. Clin. Endocrinol. Metab., 1999, 84(5), 1729-1736. doi: 10.1210/jcem.84.5.5631 PMID: 10323408
- Nicolaides, N.C.; Chrousos, G.P. Adrenal Cortex Hormones.In:Hormonal Signaling in Biology and Medicine: Comprehensive Modern Endocrinology; Litwack, G., Ed.; Academic Press, 2020, pp. 619-633. doi: 10.1016/B978-0-12-813814-4.00028-6
- Chrousos, G.P.; Kino, T. Intracellular glucocorticoid signaling: A formerly simple system turns stochastic. Sci. STKE, 2005, 2005(304), pe48. doi: 10.1126/stke.3042005pe48 PMID: 16204701
- Nicolaides, N.C. The human glucocorticoid receptor beta: From molecular mechanisms to clinical implications. Endocrinology, 2022, 163(11), bqac150. doi: 10.1210/endocr/bqac150 PMID: 36059139
- Lu, N.Z.; Cidlowski, J.A. Translational regulatory mechanisms generate N-terminal glucocorticoid receptor isoforms with unique transcriptional target genes. Mol. Cell, 2005, 18(3), 331-342. doi: 10.1016/j.molcel.2005.03.025 PMID: 15866175
- Nader, N.; Chrousos, G.P.; Kino, T. Circadian rhythm transcription factor CLOCK regulates the transcriptional activity of the glucocorticoid receptor by acetylating its hinge region lysine cluster: Potential physiological implications. FASEB J., 2009, 23(5), 1572-1583. doi: 10.1096/fj.08-117697 PMID: 19141540
- Charmandari, E.; Chrousos, G.P.; Lambrou, G.I.; Pavlaki, A.; Koide, H.; Ng, S.S.M.; Kino, T. Peripheral CLOCK regulates target-tissue glucocorticoid receptor transcriptional activity in a circadian fashion in man. PLoS One, 2011, 6(9), e25612. doi: 10.1371/journal.pone.0025612 PMID: 21980503
- Song, I.H.; Buttgereit, F. Non-genomic glucocorticoid effects to provide the basis for new drug developments. Mol. Cell. Endocrinol., 2006, 246(1-2), 142-146. doi: 10.1016/j.mce.2005.11.012 PMID: 16388891
- Hinz, B.; Hirschelmann, R. Rapid non-genomic feedback effects of glucocorticoids on CRF-induced ACTH secretion in rats. Pharm. Res., 2000, 17(10), 1273-1277. doi: 10.1023/A:1026499604848 PMID: 11145234
- Karst, H.; Berger, S.; Turiault, M.; Tronche, F.; Schütz, G.; Joëls, M. Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone. Proc. Natl. Acad. Sci. USA, 2005, 102(52), 19204-19207. doi: 10.1073/pnas.0507572102 PMID: 16361444
- Hafezi-Moghadam, A.; Simoncini, T.; Yang, Z.; Limbourg, F.P.; Plumier, J.C.; Rebsamen, M.C.; Hsieh, C.M.; Chui, D.S.; Thomas, K.L.; Prorock, A.J.; Laubach, V.E.; Moskowitz, M.A.; French, B.A.; Ley, K.; Liao, J.K. Acute cardiovascular protective effects of corticosteroids are mediated by non-transcriptional activation of endothelial nitric oxide synthase. Nat. Med., 2002, 8(5), 473-479. doi: 10.1038/nm0502-473 PMID: 11984591
- Löwenberg, M.; Verhaar, A.P.; Bilderbeek, J.; van Marle, J.; Buttgereit, F.; Peppelenbosch, M.P.; van Deventer, S.J.; Hommes, D.W. Glucocorticoids cause rapid dissociation of a T‐cell‐receptor‐associated protein complex containing LCK and FYN. EMBO Rep., 2006, 7(10), 1023-1029. doi: 10.1038/sj.embor.7400775 PMID: 16888650
- Nicolaides, N.C.; Kino, T.; Roberts, M.L.; Katsantoni, E.; Sertedaki, A.; Moutsatsou, P.; Psarra, A.G.; Chrousos, G.P.; Charmandari, E. The role of S-palmitoylation of the human glucocorticoid receptor (hGR) in mediating the nongenomic glucocorticoid actions. J. Mol. Biochem., 2017, 6(1), 3-12. PMID: 28775968
- Sapolsky, R.M.; Romero, L.M.; Munck, A.U. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev., 2000, 21(1), 55-89. PMID: 10696570
- Galon, J.; Franchimont, D.; Hiroi, N.; Frey, G.; Boettner, A.; Ehrhart-Bornstein, M.; Oshea, J.J.; Chrousos, G.P.; Bornstein, S.R. Gene profiling reveals unknown enhancing and suppressive actions of glucocorticoids on immune cells. FASEB J., 2002, 16(1), 61-71. doi: 10.1096/fj.01-0245com PMID: 11772937
- Groeneweg, F.L.; Karst, H.; de Kloet, E.R.; Joëls, M. Rapid non-genomic effects of corticosteroids and their role in the central stress response. J. Endocrinol., 2011, 209(2), 153-167. doi: 10.1530/JOE-10-0472 PMID: 21357682
- Prager, E.M.; Johnson, L.R. Stress at the synapse: signal transduction mechanisms of adrenal steroids at neuronal membranes. Sci. Signal., 2009, 2(86), re5. doi: 10.1126/scisignal.286re5 PMID: 19724063
- Tasker, J.G.; Di, S.; Malcher-Lopes, R. Minireview: Rapid glucocorticoid signaling via membrane-associated receptors. Endocrinology, 2006, 147(12), 5549-5556. doi: 10.1210/en.2006-0981 PMID: 16946006
- Nicolaides, N.C.; Makridakis, M.; Stroggilos, R.; Lygirou, V.; Koniari, E.; Papageorgiou, I.; Sertedaki, A.; Zoidakis, J.; Charmandari, E. Plasma proteomics in healthy subjects with differences in tissue glucocorticoid sensitivity identifies a novel proteomic signature. Biomedicines, 2022, 10(1), 184. doi: 10.3390/biomedicines10010184 PMID: 35052863
- Manzari, N.; Matvienko-Sikar, K.; Baldoni, F.; OKeeffe, G.W.; Khashan, A.S. Prenatal maternal stress and risk of neurodevelopmental disorders in the offspring: A systematic review and meta-analysis. Soc. Psychiatry Psychiatr. Epidemiol., 2019, 54(11), 1299-1309. doi: 10.1007/s00127-019-01745-3 PMID: 31324962
- Charil, A.; Laplante, D.P.; Vaillancourt, C.; King, S. Prenatal stress and brain development. Brain Res. Brain Res. Rev., 2010, 65(1), 56-79. doi: 10.1016/j.brainresrev.2010.06.002 PMID: 20550950
- Davis, E.P.; Sandman, C.A.; Buss, C.; Wing, D.A.; Head, K. Fetal glucocorticoid exposure is associated with preadolescent brain development. Biol. Psychiatry, 2013, 74(9), 647-655. doi: 10.1016/j.biopsych.2013.03.009 PMID: 23611262
- Kassotaki, I.; Valsamakis, G.; Mastorakos, G.; Grammatopoulos, D.K. Placental CRH as a signal of pregnancy adversity and impact on fetal neurodevelopment. Front. Endocrinol., 2021, 12(August), 714214. doi: 10.3389/fendo.2021.714214 PMID: 34408727
- Anifantaki, F.; Pervanidou, P.; Lambrinoudaki, I.; Panoulis, K.; Vlahos, N.; Eleftheriades, M. Maternal prenatal stress, thyroid function and neurodevelopment of the offspring: A mini review of the literature. Front. Neurosci., 2021, 15, 692446. doi: 10.3389/fnins.2021.692446 PMID: 34566560
- Davis, E.P.; Sandman, C.A. The timing of prenatal exposure to maternal cortisol and psychosocial stress is associated with human infant cognitive development. Child Dev., 2010, 81(1), 131-148. doi: 10.1111/j.1467-8624.2009.01385.x PMID: 20331658
- Bomysoad, R.N.; Francis, L.A. Adverse childhood experiences and mental health conditions among adolescents. J. Adolesc. Health, 2020, 67(6), 868-870. doi: 10.1016/j.jadohealth.2020.04.013 PMID: 32576484
- Li, J.; Olsen, J.; Vestergaard, M.; Obel, C. Attention-deficit/hyperactivity disorder in the offspring following prenatal maternal bereavement: A nationwide follow-up study in Denmark. Eur. Child Adolesc. Psychiatry, 2010, 19(10), 747-753. doi: 10.1007/s00787-010-0113-9 PMID: 20495989
- Class, Q.A.; Abel, K.M.; Khashan, A.S.; Rickert, M.E.; Dalman, C.; Larsson, H.; Hultman, C.M.; Långström, N.; Lichtenstein, P.; DOnofrio, B.M. Offspring psychopathology following preconception, prenatal and postnatal maternal bereavement stress. Psychol. Med., 2014, 44(1), 71-84. doi: 10.1017/S0033291713000780 PMID: 23591021
- Say, G.N. Karabekiroğlu, K.; Babadağı Z.; Yüce, M. Maternal stress and perinatal features in autism and attention deficit/hyperactivity disorder. Pediatr. Int., 2016, 58(4), 265-269. doi: 10.1111/ped.12822 PMID: 26338105
- Rodriguez, A.; Bohlin, G. Are maternal smoking and stress during pregnancy related to ADHD symptoms in children? J. Child Psychol. Psychiatry, 2005, 46(3), 246-254. doi: 10.1111/j.1469-7610.2004.00359.x PMID: 15755301
- Shao, S.; Wang, J.; Huang, K.; Wang, S.; Liu, H.; Wan, S.; Yan, S.; Hao, J.; Zhu, P.; Tao, F. Prenatal pregnancy-related anxiety predicts boys ADHD symptoms via placental C-reactive protein. Psychoneuroendocrinology, 2020, 120, 104797. doi: 10.1016/j.psyneuen.2020.104797 PMID: 32682173
- Grizenko, N.; Shayan, Y.R.; Polotskaia, A.; Ter-Stepanian, M.; Joober, R. Relation of maternal stress during pregnancy to symptom severity and response to treatment in children with ADHD. J. Psychiatry Neurosci., 2008, 33(1), 10-16. PMID: 18197267
- Brown, N.M.; Brown, S.N.; Briggs, R.D.; Germán, M.; Belamarich, P.F.; Oyeku, S.O. Associations between adverse childhood experiences and ADHD diagnosis and severity. Acad. Pediatr., 2017, 17(4), 349-355. doi: 10.1016/j.acap.2016.08.013 PMID: 28477799
- Walker, C.S.; Walker, B.H.; Brown, D.C.; Buttross, S.; Sarver, D.E. Defining the role of exposure to ACEs in ADHD: Examination in a national sample of US children. Child Abuse Negl., 2021, 112, 104884. doi: 10.1016/j.chiabu.2020.104884 PMID: 33360863
- Windle, M.; Haardörfer, R.; Getachew, B.; Shah, J.; Payne, J.; Pillai, D.; Berg, C.J. A multivariate analysis of adverse childhood experiences and health behaviors and outcomes among college students. J. Am. Coll. Health, 2018, 66(4), 246-251. doi: 10.1080/07448481.2018.1431892 PMID: 29405856
- Hunt, T.K.A.; Slack, K.S.; Berger, L.M. Adverse childhood experiences and behavioral problems in middle childhood. Child Abuse Negl., 2017, 67(12), 391-402. doi: 10.1016/j.chiabu.2016.11.005 PMID: 27884508
- Jimenez, M.E.; Wade, R., Jr; Schwartz-Soicher, O.; Lin, Y.; Reichman, N.E. Adverse childhood experiences and ADHD diagnosis at age 9 years in a national urban sample. Acad. Pediatr., 2017, 17(4), 356-361. doi: 10.1016/j.acap.2016.12.009 PMID: 28003143
- González, R.A.; Vélez-Pastrana, M.C.; McCrory, E.; Kallis, C.; Aguila, J.; Canino, G.; Bird, H. Evidence of concurrent and prospective associations between early maltreatment and ADHD through childhood and adolescence. Soc. Psychiatry Psychiatr. Epidemiol., 2019, 54(6), 671-682. doi: 10.1007/s00127-019-01659-0 PMID: 30903235
- Roberts, A.L.; Lyall, K.; Rich-Edwards, J.W.; Ascherio, A.; Weisskopf, M.G. Maternal exposure to childhood abuse is associated with elevated risk of autism. JAMA Psychiatry, 2013, 70(5), 508-515. doi: 10.1001/jamapsychiatry.2013.447 PMID: 23553149
- Kinney, D.K.; Miller, A.M.; Crowley, D.J.; Huang, E.; Gerber, E. Autism prevalence following prenatal exposure to hurricanes and tropical storms in Louisiana. J. Autism Dev. Disord., 2008, 38(3), 481-488. doi: 10.1007/s10803-007-0414-0 PMID: 17619130
- Roberts, A.L.; Lyall, K.; Rich-Edwards, J.W.; Ascherio, A.; Weisskopf, M.G. Maternal exposure to intimate partner abuse before birth is associated with autism spectrum disorder in offspring. Autism, 2016, 20(1), 26-36. doi: 10.1177/1362361314566049 PMID: 25662292
- Rai, D.; Golding, J.; Magnusson, C.; Steer, C.; Lewis, G.; Dalman, C. Prenatal and early life exposure to stressful life events and risk of autism spectrum disorders: Population-based studies in Sweden and England. PLoS One, 2012, 7(6), e38893. doi: 10.1371/journal.pone.0038893 PMID: 22719977
- Cattane, N.; Richetto, J.; Cattaneo, A. Prenatal exposure to environmental insults and enhanced risk of developing Schizophrenia and Autism Spectrum Disorder: focus on biological pathways and epigenetic mechanisms. Neurosci. Biobehav. Rev., 2020, 117, 253-278. doi: 10.1016/j.neubiorev.2018.07.001 PMID: 29981347
- Beversdorf, D.Q.; Manning, S.E.; Hillier, A.; Anderson, S.L.; Nordgren, R.E.; Walters, S.E.; Nagaraja, H.N.; Cooley, W.C.; Gaelic, S.E.; Bauman, M.L. Timing of prenatal stressors and autism. J. Autism Dev. Disord., 2005, 35(4), 471-478. doi: 10.1007/s10803-005-5037-8 PMID: 16134032
- Kerns, C.M.; Newschaffer, C.J.; Berkowitz, S.J. Traumatic childhood events and autism spectrum disorder. J. Autism Dev. Disord., 2015, 45(11), 3475-3486. doi: 10.1007/s10803-015-2392-y PMID: 25711547
- Kerns, C.M.; Newschaffer, C.J.; Berkowitz, S.; Lee, B.K. Examining the association of autism and adverse childhood experiences in the National Survey of Childrens Health: the important role of income and co-occurring mental health conditions. J. Autism Dev. Disord., 2017, 47(7), 2275-2281. doi: 10.1007/s10803-017-3111-7 PMID: 28378271
- Stack, A.; Lucyshyn, J. Autism spectrum disorder and the experience of traumatic events: Review of the current literature to inform modifications to a treatment model for children with autism. J. Autism Dev. Disord., 2019, 49(4), 1613-1625. doi: 10.1007/s10803-018-3854-9 PMID: 30539370
- Hoover, D.W.; Kaufman, J. Adverse childhood experiences in children with autism spectrum disorder. Curr. Opin. Psychiatry, 2018, 31(2), 128-132. doi: 10.1097/YCO.0000000000000390 PMID: 29206686
- Makris, G.; Eleftheriades, A.; Pervanidou, P. Early life stress, hormones and neurodevelopmental disorders. Horm. Res. Paediatr., 2022. PMID: 35259742
- Makris, G.; Agorastos, A.; Chrousos, G.P.; Pervanidou, P. Stress system activation in children and adolescents with autism spectrum disorder. Front. Neurosci., 2022, 15, 756628. doi: 10.3389/fnins.2021.756628 PMID: 35095389
- Anesiadou, S.; Makris, G.; Michou, M.; Bali, P.; Papassotiriou, I.; Apostolakou, F.; Korkoliakou, P.; Papageorgiou, C.; Chrousos, G.; Pervanidou, P. Salivary cortisol and alpha‐amylase daily profiles and stress responses to an academic performance test and a moral cognition task in children with neurodevelopmental disorders. Stress Health, 2021, 37(1), 45-59. doi: 10.1002/smi.2971 PMID: 32608561
- Angeli, E.; Korpa, T.; Johnson, E.O.; Apostolakou, F.; Papassotiriou, I.; Chrousos, G.P.; Pervanidou, P. Salivary cortisol and alpha-amylase diurnal profiles and stress reactivity in children with Attention Deficit Hyperactivity Disorder. Psychoneuroendocrinology, 2018, 90, 174-181. doi: 10.1016/j.psyneuen.2018.02.026 PMID: 29501948
- Korpa, T.; Pervanidou, P.; Angeli, E.; Apostolakou, F.; Papanikolaou, K.; Papassotiriou, I.; Chrousos, G.P.; Kolaitis, G. Mothers parenting stress is associated with salivary cortisol profiles in children with attention deficit hyperactivity disorder. Stress, 2017, 20(2), 149-158. doi: 10.1080/10253890.2017.1303472 PMID: 28264636
- Pervanidou, P.; Agorastos, A.; Chrousos, G.P. Editorial: Stress and neurodevelopment. Front. Neurosci., 2022, 16, 898872. doi: 10.3389/fnins.2022.898872 PMID: 35495052
- Khoury, L.; Tang, Y.L.; Bradley, B.; Cubells, J.F.; Ressler, K.J. Substance use, childhood traumatic experience, and Posttraumatic Stress Disorder in an urban civilian population. Depress. Anxiety, 2010, 27(12), 1077-1086. doi: 10.1002/da.20751 PMID: 21049532
- Pervanidou, P. Biology of post-traumatic stress disorder in childhood and adolescence. J. Neuroendocrinol., 2008, 20(5), 632-638. doi: 10.1111/j.1365-2826.2008.01701.x PMID: 18363804
- Pervanidou, P.; Chrousos, G.P. Neuroendocrinology of post-traumatic stress disorder., Prog. Brain Res., 2010, 182, 149-16. doi: 10.1016/S0079-6123(10)82005-9 PMID: 20541663
- Pervanidou, P.; Makris, G.; Chrousos, G.; Agorastos, A. Early life stress and pediatric posttraumatic stress disorder. Brain Sci., 2020, 10(3), 169. doi: 10.3390/brainsci10030169 PMID: 32183256
- Copeland, W.E.; Keeler, G.; Angold, A.; Costello, E.J. Traumatic events and posttraumatic stress in childhood. Arch. Gen. Psychiatry, 2007, 64(5), 577-584. doi: 10.1001/archpsyc.64.5.577 PMID: 17485609
- Weems, C.F.; Russell, J.D.; Neill, E.L.; McCurdy, B.H. Annual Research Review: Pediatric posttraumatic stress disorder from a neurodevelopmental network perspective. J. Child Psychol. Psychiatry, 2019, 60(4), 395-408. doi: 10.1111/jcpp.12996 PMID: 30357832
- McLaughlin, K.A.; Koenen, K.C.; Hill, E.D.; Petukhova, M.; Sampson, N.A.; Zaslavsky, A.M.; Kessler, R.C. Trauma exposure and posttraumatic stress disorder in a national sample of adolescents. J. Am. Acad. Child Adolesc. Psychiatry, 2013, 52(8), 815-830.e14. doi: 10.1016/j.jaac.2013.05.011 PMID: 23880492
- Merikangas, K.R. Lifetime prevalence of mental disorders in U.S. adolescents: results from the National Comorbidity Survey Replication-Adolescent Supplement (NCS-A). J. Am. Acad. Child Adolesc. Psychiatry, 2010, 49(10), 980-989.
- American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders, 5th ed; , 2013.
- Baker, D.G.; Buxbaum, J.D.; Russo, S.J.; Yehuda, R. New translational perspectives for blood-based biomarkers of PTSD: From glucocorticoid to immune mediators of stress susceptibility. Exp Neurol, 2016, 84((Pt B)), 133-140.
- Agorastos, A.; Pervanidou, P.; Chrousos, G.P.; Baker, D.G. Developmental trajectories of early life stress and trauma: A narrative review on neurobiological aspects beyond stress system dysregulation. Front. Psychiatry, 2019, 10, 118. doi: 10.3389/fpsyt.2019.00118 PMID: 30914979
- Pan, X.; Wang, Z.; Wu, X.; Wen, S.W.; Liu, A. Salivary cortisol in post-traumatic stress disorder: A systematic review and meta-analysis. BMC Psychiatry, 2018, 18(1), 324. doi: 10.1186/s12888-018-1910-9 PMID: 30290789
- Pan, X.; Kaminga, A.C.; Wen, S.W.; Liu, A. Catecholamines in post-traumatic stress disorder: A systematic review and meta-analysis. Front. Mol. Neurosci., 2018, 11, 450. doi: 10.3389/fnmol.2018.00450 PMID: 30564100
- De Bellis, M.D.; Lefter, L.; Trickett, P.K.; Putnam, F.W., Jr Urinary catecholamine excretion in sexually abused girls. J. Am. Acad. Child Adolesc. Psychiatry, 1994, 33(3), 320-327. doi: 10.1097/00004583-199403000-00004 PMID: 8169176
- Cicchetti, D.; Rogosch, F.A. Diverse patterns of neuroendocrine activity in maltreated children. Dev. Psychopathol., 2001, 13(3), 677-693. doi: 10.1017/S0954579401003145 PMID: 11523854
- Gordis, E.B.; Granger, D.A.; Susman, E.J.; Trickett, P.K. Salivary alpha amylasecortisol asymmetry in maltreated youth. Horm. Behav., 2008, 53(1), 96-103. doi: 10.1016/j.yhbeh.2007.09.002 PMID: 17945232
- MacMillan, H.L.; Georgiades, K.; Duku, E.K.; Shea, A.; Steiner, M.; Niec, A.; Tanaka, M.; Gensey, S.; Spree, S.; Vella, E.; Walsh, C.A.; De Bellis, M.D.; Van der Meulen, J.; Boyle, M.H.; Schmidt, L.A. Cortisol response to stress in female youths exposed to childhood maltreatment: Results of the youth mood project. Biol. Psychiatry, 2009, 66(1), 62-68. doi: 10.1016/j.biopsych.2008.12.014 PMID: 19217075
- Trickett, P.K.; Noll, J.G.; Susman, E.J.; Shenk, C.E.; Putnam, F.W. Attenuation of cortisol across development for victims of sexual abuse. Dev. Psychopathol., 2010, 22(1), 165-175. doi: 10.1017/S0954579409990332 PMID: 20102654
- Goenjian, A.K.; Yehuda, R.; Pynoos, R.S.; Steinberg, A.M.; Tashjian, M.; Yang, R.K.; Najarian, L.M.; Fairbanks, L.A. Basal cortisol, dexamethasone suppression of cortisol, and MHPG in adolescents after the 1988 earthquake in Armenia. Am. J. Psychiatry, 1996, 153(7), 929-934. doi: 10.1176/ajp.153.7.929 PMID: 8659616
- Pervanidou, P.; Kolaitis, G.; Charitaki, S.; Margeli, A.; Ferentinos, S.; Bakoula, C.; Lazaropoulou, C.; Papassotiriou, I.; Tsiantis, J.; Chrousos, G.P. Elevated morning serum interleukin (IL)-6 or evening salivary cortisol concentrations predict posttraumatic stress disorder in children and adolescents six months after a motor vehicle accident. Psychoneuroendocrinology, 2007, 32(8-10), 991-999. doi: 10.1016/j.psyneuen.2007.07.001 PMID: 17825995
- Pervanidou, P.; Kolaitis, G.; Charitaki, S.; Lazaropoulou, C.; Papassotiriou, I.; Hindmarsh, P.; Bakoula, C.; Tsiantis, J.; Chrousos, G.P. The natural history of neuroendocrine changes in pediatric posttraumatic stress disorder (PTSD) after motor vehicle accidents: Progressive divergence of noradrenaline and cortisol concentrations over time. Biol. Psychiatry, 2007, 62(10), 1095-1102. doi: 10.1016/j.biopsych.2007.02.008 PMID: 17624319
- Pervanidou, P.; Chrousos, G.P. Early-life stress: From neuroendocrine mechanisms to stress-related disorders. Horm. Res. Paediatr., 2018, 89(5), 372-379. doi: 10.1159/000488468 PMID: 29886495
- Marchetti, D.; Musso, P.; Verrocchio, M.C.; Manna, G.; Kopala-Sibley, D.C.; De Berardis, D.; De Santis, S.; Falgares, G. Childhood maltreatment, personality vulnerability profiles, and borderline personality disorder symptoms in adolescents. Dev. Psychopathol., 2022, 34(3), 1163-1176. doi: 10.1017/S0954579420002151 PMID: 33494855
- Caldirola, D.; Torti, T.; Cuniberti, F.; Daccò, S.; Alciati, A.; Schruers, K.; Martinotti, G.; De Berardis, D.; Perna, G. No sex differences in self-reported childhood maltreatment in major depressive and bipolar disorders: A retrospective study. Brain Sci., 2022, 12(6), 804. doi: 10.3390/brainsci12060804 PMID: 35741691
- Perna, G.; Daccò, S.; Alciati, A.; Cuniberti, F.; De Berardis, D.; Caldirola, D. Childhood maltreatment history for guiding personalized antidepressant choice in major depressive disorder: Preliminary results from a systematic review. Prog. Neuropsychopharmacol. Biol. Psychiatry, 2021, 107, 110208. doi: 10.1016/j.pnpbp.2020.110208 PMID: 33338557
- Gkesoglou, T.; Pervanidou, P.; Bozikas, V.P.; Agorastos, A. Neurobiology of early life traumatic stress and trauma: Prolonged neuroendocrine dysregulation as a neurodevelopmental risk factor. Psychiatriki, 2022, 34(2) doi: 10.22365/jpsych.2022.059 PMID: 35255464
- Agorastos, A.; Chrousos, G.P. The neuroendocrinology of stress: the stress-related continuum of chronic disease development. Mol. Psychiatry, 2022, 27(1), 502-513. doi: 10.1038/s41380-021-01224-9 PMID: 34290370
- Kazakou, P.; Nicolaides, N.C.; Chrousos, G.P. Basic concepts and hormonal regulators of the stress system. Horm. Res. Paediatr., 2022. PMID: 35272295
- Murgatroyd, C.; Wu, Y.; Bockmühl, Y.; Spengler, D. Genes learn from stress: How infantile trauma programs us for depression. Epigenetics, 2010, 5(3), 194-199. doi: 10.4161/epi.5.3.11375 PMID: 20339319
- Meaney, M.J.; Aitken, D.H.; Bodnoff, S.R.; Iny, L.J.; Tatarewicz, J.E.; Sapolsky, R.M. Early postnatal handling alters glucocorticoid receptor concentrations in selected brain regions. Behav. Neurosci., 1985, 99(4), 765-770. doi: 10.1037/0735-7044.99.4.765 PMID: 3843740
- Meaney, M.J.; Aitken, D.H.; Sapolsky, R.M. Thyroid hormones influence the development of hippocampal glucocorticoid receptors in the rat: A mechanism for the effects of postnatal handling on the development of the adrenocortical stress response. Neuroendocrinology, 1987, 45(4), 278-283. doi: 10.1159/000124741 PMID: 3574606
- Mitchell, J.B.; Iny, L.J.; Meaney, M.J. The role of serotonin in the development and environmental regulation of type II corticosteroid receptor binding in rat hippocampus. Brain Res. Dev. Brain Res., 1990, 55(2), 231-235. doi: 10.1016/0165-3806(90)90204-C PMID: 1701365
- Champagne, F.A. Early environments, glucocorticoid receptors, and behavioral epigenetics. Behav. Neurosci., 2013, 127(5), 628-636. doi: 10.1037/a0034186 PMID: 24128352
- Liu, D.; Diorio, J.; Tannenbaum, B.; Caldji, C.; Francis, D.; Freedman, A.; Sharma, S.; Pearson, D.; Plotsky, P.M.; Meaney, M.J. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science, 1997, 277(5332), 1659-1662. doi: 10.1126/science.277.5332.1659 PMID: 9287218
- Hellstrom, I.C.; Dhir, S.K.; Diorio, J.C.; Meaney, M.J. Maternal licking regulates hippocampal glucocorticoid receptor transcription through a thyroid hormoneserotoninNGFI-A signalling cascade. Philos. Trans. R. Soc. Lond. B Biol. Sci., 2012, 367(1601), 2495-2510. doi: 10.1098/rstb.2012.0223 PMID: 22826348
- Weaver, I.C.G.; Cervoni, N.; Champagne, F.A.; DAlessio, A.C.; Sharma, S.; Seckl, J.R.; Dymov, S.; Szyf, M.; Meaney, M.J. Epigenetic programming by maternal behavior. Nat. Neurosci., 2004, 7(8), 847-854. doi: 10.1038/nn1276 PMID: 15220929
- Rahman, M.F.; McGowan, P.O. Cell-type-specific epigenetic effects of early life stress on the brain. Transl. Psychiatry, 2022, 12(1), 326. doi: 10.1038/s41398-022-02076-9 PMID: 35948532
- Friedman, R.C.; Farh, K.K.H.; Burge, C.B.; Bartel, D.P. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res., 2009, 19(1), 92-105. doi: 10.1101/gr.082701.108 PMID: 18955434
- Weaver, I.C.G.; Champagne, F.A.; Brown, S.E.; Dymov, S.; Sharma, S.; Meaney, M.J.; Szyf, M. Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: Altering epigenetic marking later in life. J. Neurosci., 2005, 25(47), 11045-11054. doi: 10.1523/JNEUROSCI.3652-05.2005 PMID: 16306417
- Meaney, M.J. Nature, nurture, and the disunity of knowledge. Ann. N. Y. Acad. Sci., 2001, 935(1), 50-61. doi: 10.1111/j.1749-6632.2001.tb03470.x PMID: 11411175
- Eleftheriades, M.; Vousoura, E.; Eleftheriades, A.; Pervanidou, P.; Zervas, I.M.; Chrousos, G.; Vlahos, N.F.; Sotiriadis, A. Physical health, media use, stress, and mental health in pregnant women during the COVID-19 pandemic. Diagnostics, 2022, 12(5), 1125. doi: 10.3390/diagnostics12051125 PMID: 35626281
- De Berardis, D.; Di Carlo, F.; Di Giannantonio, M.; Pettorruso, M. Legacy of neuropsychiatric symptoms associated with past COVID-19 infection: A cause of concern. World J. Psychiatry, 2022, 12(6), 773-778. doi: 10.5498/wjp.v12.i6.773 PMID: 35978974
- De Berardis, D.; Fornaro, M.; Orsolini, L.; Ventriglio, A.; Vellante, F.; Di Giannantonio, M. Emotional dysregulation in adolescents: Implications for the development of severe psychiatric disorders, substance abuse, and suicidal ideation and behaviors. Brain Sci., 2020, 10(9), 591. doi: 10.3390/brainsci10090591 PMID: 32858969
- Korpa, T.; Pappa, T.; Chouliaras, G.; Sfinari, A.; Eleftheriades, A.; Katsounas, M.; Kanaka-Gantenbein, C.; Pervanidou, P. Daily behaviors, worries and emotions in children and adolescents with ADHD and learning difficulties during the COVID-19 pandemic. Children, 2021, 8(11), 995. doi: 10.3390/children8110995 PMID: 34828708
- Sfinari, A.; Pervanidou, P.; Chouliaras, G.; Zoumakis, E.; Vasilakis, I.A.; Nicolaides, N.C.; Kanaka-Gantenbein, C. Perceived changes in emotions, worries and everyday behaviors in children and adolescents aged 5-18 years with Type 1 Diabetes during the COVID-19 pandemic. Children, 2022, 9(5), 736. doi: 10.3390/children9050736 PMID: 35626913
- Zisopoulou, T.; Varvogli, L. Stress management methods in children and adolescents - past, present, and future. Horm. Res. Paediatr., 2023, 96(1), 97-107. doi: 10.1159/000526946 PMID: 36096110
- Scott, S.R.; ODaffer, A.G.; Bradford, M.C.; Fladeboe, K.; Lau, N.; Steineck, A.; Taylor, M.; Yi-Frazier, J.P.; Rosenberg, A.R. Adverse childhood experiences (ACEs) and medically traumatic events (TEs) in adolescents and young adults (AYAs) with cancer: A report from the Promoting Resilience in Stress Management (PRISM) randomized controlled trial. Support. Care Cancer, 2021, 29(7), 3773-3781. doi: 10.1007/s00520-020-05888-x PMID: 33219407
Supplementary files
