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Current Neuropharmacology


ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

General Review Article

Early Biomarkers and Intervention Programs for the Infant Exposed to Prenatal Stress

Author(s): Marta C. Antonelli*, Martin G. Frasch, Mercedes Rumi, Ritika Sharma, Peter Zimmermann, Maria S. Molinet and Silvia M. Lobmaier

Volume 20, Issue 1, 2022

Page: [94 - 106] Pages: 13

DOI: 10.2174/1570159X19666210125150955

Price: $65


Functional development of affective and reward circuits, cognition and response inhibition later in life exhibits vulnerability periods during gestation and early childhood. Extensive evidence supports the model that exposure to stressors in the gestational period and early postnatal life increases an individual's susceptibility to future impairments of functional development. Recent versions of this model integrate epigenetic mechanisms of the developmental response. Their understanding will guide the future treatment of the associated neuropsychiatric disorders. A combination of non-invasively obtainable physiological signals and epigenetic biomarkers related to the principal systems of the stress response, the Hypothalamic-Pituitary axis (HPA) and the Autonomic Nervous System (ANS), are emerging as the key predictors of neurodevelopmental outcomes. Such electrophysiological and epigenetic biomarkers can prove to timely identify children benefiting most from early intervention programs. Such programs should ameliorate future disorders in otherwise healthy children. The recently developed Early Family-Centered Intervention Programs aim to influence the care and stimuli provided daily by the family and improving parent/child attachment, a key element for healthy socio-emotional adult life. Although frequently underestimated, such biomarker-guided early intervention strategy represents a crucial first step in the prevention of future neuropsychiatric problems and in reducing their personal and societal impact.

Keywords: Maternal stress, epigenetic biomarkers, FHR, PRSA, early intervention programs, neurodevelopment.

Graphical Abstract
Barker, D.J.; Gluckman, P.D.; Godfrey, K.M.; Harding, J.E.; Owens, J.A.; Robinson, J.S. Fetal nutrition and cardiovascular disease in adult life. Lancet, 1993, 341(8850), 938-941.
[] [PMID: 8096277]
Edwards, C.R.W.; Benediktsson, R.; Lindsay, R.S.; Seckl, J.R. Dysfunction of placental glucocorticoid barrier: link between fetal environment and adult hypertension? Lancet, 1993, 341(8841), 355-357.
[] [PMID: 8094124]
Van den Bergh, B.R.H.; van den Heuvel, M.I.; Lahti, M.; Braeken, M.; de Rooij, S.R.; Entringer, S.; Hoyer, D.; Roseboom, T.; Raikkonen, K.; King, S.; Schwab, M. Prenatal developmental origins of behavior and mental health: The influence of maternal stress in pregnancy. Neurosci. Biobehav. Rev., 2017, 117, 26-64.
[] [PMID: 28757456]
Rakers, F.; Rupprecht, S.; Dreiling, M.; Bergmeier, C.; Witte, O.W.; Schwab, M. Transfer of maternal psychosocial stress to the fetus. Neurosci. Biobehav. Rev., 2017, S0149-7634(16), 30719-9.
[PMID: 28237726]
Rothenberger, S.E.; Resch, F.; Doszpod, N.; Moehler, E. Prenatal stress and infant affective reactivity at five months of age. Early Hum. Dev., 2011, 87(2), 129-136.
[] [PMID: 21194854]
Braithwaite, E.C.; Ramchandani, P.G.; O’Connor, T.G.; van Ijzendoorn, M.H.; Bakermans-Kranenburg, M.J.; Glover, V.; Netsi, E.; Evans, J.; Meaney, M.J.; Murphy, S.E. No moderating effect of 5-HTTLPR on associations between antenatal anxiety and infant behavior. J. Am. Acad. Child Adolesc. Psychiatry, 2013, 52(5), 519-526.
[] [PMID: 23622853]
Peltola, M.J.; Mäkelä, T.; Paavonen, E.J.; Vierikko, E.; Saarenpää-Heikkilä, O.; Paunio, T.; Hietanen, J.K.; Kylliäinen, A. Respiratory sinus arrhythmia moderates the impact of maternal prenatal anxiety on infant negative affectivity. Dev. Psychobiol., 2017, 59(2), 209-216.
[] [PMID: 27761915]
Blair, M.M.; Glynn, L.M.; Sandman, C.A.; Davis, E.P. Prenatal maternal anxiety and early childhood temperament. Stress, 2011, 14(6), 644-651.
[] [PMID: 21790468]
Lin, Y.; Xu, J.; Huang, J.; Jia, Y.; Zhang, J.; Yan, C.; Zhang, J. Effects of prenatal and postnatal maternal emotional stress on toddlers’ cognitive and temperamental development. J. Affect. Disord., 2017, 207, 9-17.
[] [PMID: 27665073]
Polanska, K.; Krol, A.; Merecz-Kot, D.; Jurewicz, J.; Makowiec-Dabrowska, T.; Chiarotti, F.; Calamandrei, G.; Hanke, W. Maternal stress during pregnancy and neurodevelopmental outcomes of children during the first 2 years of life. J. Paediatr. Child Health, 2017, 53(3), 263-270.
[] [PMID: 28168801]
Persson, P.; Rossin-Slater, M. Family ruptures, stress, and the mental health of the next generation. Am. Econ. Rev., 2018, 108(4), 1214-1252.
[] [PMID: 30091569]
Bromer, C.; Marsit, C.J.; Armstrong, D.A.; Padbury, J.F.; Lester, B. Genetic and epigenetic variation of the glucocorticoid receptor (NR3C1) in placenta and infant neurobehavior. Dev. Psychobiol., 2013, 55(7), 673-683.
[PMID: 22714792]
Lester, B.M.; Salisbury, A.L.; Hawes, K.; Dansereau, L.M.; Bigsby, R.; Laptook, A.; Taub, M.; Lagasse, L.L.; Vohr, B.R.; Padbury, J.F. 18-month follow-up of infants cared for in a single- family room neonatal intensive care unit. J. Pediatr., 2016, 177, 84-89.
[] [PMID: 27470693]
Sajedi, F.; Ahmadi, D.M.; Vameghi, R.; Mazaheri, M.A.; Akbarzadehbaghban, A. Relationship of mothers’ psychological status with development of kindergarten children. Iran. J. Child. Neurol., 2016, 10(3), 61-72.
[PMID: 27375758]
Sidor, A.; Fischer, C.; Cierpka, M. The link between infant regulatory problems, temperament traits, maternal depressive symptoms and children’s psychopathological symptoms at age three: a longitudinal study in a German at-risk sample. Child Adolesc. Psychiatry Ment. Health, 2017, 11, 10.
[] [PMID: 28286548]
Huizink, A.C.; Menting, B.; De Moor, M.H.M.; Verhage, M.L.; Kunseler, F.C.; Schuengel, C.; Oosterman, M. From prenatal anxiety to parenting stress: a longitudinal study. Arch. Women Ment. Health, 2017, 20(5), 663-672.
[] [PMID: 28634716]
Black, M.M.; Walker, S.P.; Fernald, L.C.H.; Andersen, C.T.; DiGirolamo, A.M.; Lu, C.; McCoy, D.C.; Fink, G.; Shawar, Y.R.; Shiffman, J.; Devercelli, A.E.; Wodon, Q.T.; Vargas-Barón, E.; Grantham-Mc, G.S. Early childhood development coming of age: science through the life course. Lancet, 2017, 389(10064), 77-90.
[] [PMID: 27717614]
O’Donnell, K.J.; Meaney, M.J. Fetal origins of mental health: the developmental origins of health and disease hypothesis. Am. J. Psychiatry, 2017, 174(4), 319-328.
[] [PMID: 27838934]
Barker, D.J. Fetal origins of coronary heart disease. BMJ, 1995, 311(6998), 171-174.
[] [PMID: 7613432]
Barker, D.J. The origins of the developmental origins theory. J. Intern. Med., 2007, 261(5), 412-417.
[] [PMID: 17444880]
Gluckman, P.D.; Hanson, M.A.; Spencer, H.G. Predictive adaptive responses and human evolution. Trends Ecol. Evol., 2005, 20(10), 527-533.
[] [PMID: 16701430]
Hanson, M.A.; Gluckman, P.D. Developmental origins of health and disease: new insights. Basic Clin. Pharmacol. Toxicol., 2008, 102(2), 90-93.
[] [PMID: 18226060]
Rosenfeld, C.S. Homage to the ‘H’ in developmental origins of health and disease. J. Dev. Orig. Health Dis., 2017, 8(1), 8-29.
[] [PMID: 27577791]
Van den Bergh, B.R. Developmental programming of early brain and behaviour development and mental health: a conceptual framework. Dev. Med. Child Neurol., 2011, 53(Suppl. 4), 19-23.
[] [PMID: 21950389]
Kundakovic, M.; Jaric, I. The epigenetic link between prenatal adverse environments and neurodevelopmental disorders. Genes (Basel), 2017, 8(3), E104.
[] [PMID: 28335457]
Alyamani, R.A.S.; Murgatroyd, C. Epigenetic programming by early-life stress. Prog. Mol. Biol. Transl. Sci., 2018, 157, 133-150.
[] [PMID: 29933948]
Bermúdez, E.F.; Carbajal, N.E. Evaluación del desarrollo psicomotriz en niños de 0 a 24 meses TT - Psycomotive development evaluation of children aged 0-24 months. Arch. Argent. Pediatr., 1995.
Gupta, R.; Patel, N.V. Trial of a screening technique of the developmental assessment of infants and young children (6 weeks-2 years). Indian Pediatr., 1991, 28(8), 859-867.
[PMID: 1808073]
Lejarraga, H.; Menendez, A.M.; Menzano, E.; Guerra, L.; Biancato, S.; Pianelli, P.; Del Pino, M.; Fattore, M.J.; Contreras, M.M. Screening for developmental problems at primary care level: a field programme in San Isidro, Argentina. Paediatr. Perinat. Epidemiol., 2008, 22(2), 180-187.
[] [PMID: 18298693]
Frasch, M.G.; Lobmaier, S.M.; Stampalija, T.; Desplats, P.; Pallarés, M.E.; Pastor, V.; Brocco, M.A.; Wu, H.; Schulkin, J.; Herry, C.L.; Seely, A.J.E.; Metz, G.A.S.; Louzoun, Y.; Antonelli, M.C. Non-invasive biomarkers of fetal brain development reflecting prenatal stress: An integrative multi-scale multi-species perspective on data collection and analysis. Neurosci. Biobehav. Rev., 2020, 117, 165-183.
[] [PMID: 29859198]
Braun, K.; Bock, J.; Wainstock, T.; Matas, E.; Gaisler-Salomon, I.; Fegert, J.; Ziegenhain, U.; Segal, M. Experience-induced transgenerational (re-)programming of neuronal structure and functions: Impact of stress prior and during pregnancy. Neurosci. Biobehav. Rev., 2020, 117, 281-296.
[PMID: 28571876]
Jawahar, M.C.; Murgatroyd, C.; Harrison, E.L.; Baune, B.T. Epigenetic alterations following early postnatal stress: a review on novel aetiological mechanisms of common psychiatric disorders. Clin. Epigenetics, 2015, 7, 122.
[] [PMID: 26583053]
Van den Hove, D.L.A.; Steinbusch, H.W.M.; Scheepens, A.; Van de Berg, W.D.J.; Kooiman, L.A.M.; Boosten, B.J.G.; Prickaerts, J.; Blanco, C.E. Prenatal stress and neonatal rat brain development. Neuroscience, 2006, 137(1), 145-155.
[] [PMID: 16242847]
Meaney, M.J.; Szyf, M. Environmental programming of stress responses through DNA methylation: life at the interface between a dynamic environment and a fixed genome. Dialogues Clin. Neurosci., 2005, 7(2), 103-123.
[] [PMID: 16262207]
Weaver, I.C.; Korgan, A.C.; Lee, K.; Wheeler, R.V.; Hundert, A.S.; Goguen, D. Stress and the emerging roles of chromatin remodeling in signal integration and stable transmission of reversible phenotypes. Front. Behav. Neurosci., 2017, 11, 41.
[] [PMID: 28360846]
Cao-lei, L.; Rooij, S.R.D.; King, S.; Matthews, S.G.; Metz, G.A.S.; Roseboom, T.J.; Szyf, M. Neuroscience and biobehavioral reviews prenatal stress and epigenetics. Neurosci. Biobehav. Rev., 2017, 117, 198-210.
Ladd-Acosta, C. Epigenetic signatures as biomarkers of exposure. Curr. Environ. Health Rep., 2015, 2(2), 117-125.
[] [PMID: 26231361]
Boyce, W.T.; Kobor, M.S. Development and the epigenome: the ‘synapse’ of gene-environment interplay. Dev. Sci., 2015, 18(1), 1-23.
[] [PMID: 25546559]
Illingworth, R.S.; Bird, A.P. CpG islands-‘a rough guide’. FEBS Lett., 2009, 583(11), 1713-1720.
[] [PMID: 19376112]
Weaver, I.C.G.; Cervoni, N.; Champagne, F.A.; D’Alessio, 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.
[] [PMID: 15220929]
Hackman, D.A.; Farah, M.J.; Meaney, M.J. Socioeconomic status and the brain: mechanistic insights from human and animal research. Nat. Rev. Neurosci., 2010, 11(9), 651-659.
[] [PMID: 20725096]
Murgatroyd, C.; Patchev, A.V.; Wu, Y.; Micale, V.; Bockmühl, Y.; Fischer, D.; Holsboer, F.; Wotjak, C.T.; Almeida, O.F.X.; Spengler, D. Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat. Neurosci., 2009, 12(12), 1559-1566.
[] [PMID: 19898468]
Mueller, B.R.; Bale, T.L. Sex-specific programming of offspring emotionality after stress early in pregnancy. J. Neurosci., 2008, 28(36), 9055-9065.
[] [PMID: 18768700]
Kundakovic, M.; Champagne, F.A. Early-life experience, epigenetics, and the developing brain. Neuropsychopharmacology, 2015, 40(1), 141-153.
[] [PMID: 24917200]
Caldji, C.; Hellstrom, I.C.; Zhang, T.Y.; Diorio, J.; Meaney, M.J. Environmental regulation of the neural epigenome. FEBS Lett., 2011, 585(13), 2049-2058.
[] [PMID: 21420958]
Szyf, M.; Weaver, I.C.; Champagne, F.A.; Diorio, J.; Meaney, M.J. Maternal programming of steroid receptor expression and phenotype through DNA methylation in the rat. Front. Neuroendocrinol., 2005, 26(3-4), 139-162.
[] [PMID: 16303171]
McGowan, P.O.; Sasaki, A.; D’Alessio, A.C.; Dymov, S.; Labonté, B.; Szyf, M.; Turecki, G.; Meaney, M.J. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat. Neurosci., 2009, 12(3), 342-348.
[] [PMID: 19234457]
Oberlander, T.F.; Weinberg, J.; Papsdorf, M.; Grunau, R.; Misri, S.; Devlin, A.M. Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics, 2008, 3(2), 97-106.
[] [PMID: 18536531]
Kertes, D.A.; Kamin, H.S.; Hughes, D.A.; Rodney, N.C.; Bhatt, S.; Mulligan, C.J. Prenatal maternal stress predicts methylation of genes regulating the hypothalamic-pituitary-adrenocortical system in mothers and newborns in the democratic republic of congo. Child Dev., 2016, 87(1), 61-72.
[] [PMID: 26822443]
Strimbu, K.; Tavel, J.A. What are biomarkers? Curr. Opin. HIV AIDS, 2010, 5(6), 463-466.
[] [PMID: 20978388]
Armstrong, D.A.; Lesseur, C.; Conradt, E.; Lester, B.M.; Marsit, C.J. Global and gene-specific DNA methylation across multiple tissues in early infancy: implications for children’s health research. FASEB J., 2014, 28(5), 2088-2097.
[] [PMID: 24478308]
Essex, M.J.; Boyce, W.T.; Hertzman, C.; Lam, L.L.; Armstrong, J.M.; Neumann, S.M.A.; Kobor, M.S. Epigenetic vestiges of early developmental adversity: childhood stress exposure and DNA methylation in adolescence. Child Dev., 2013, 84(1), 58-75.
[] [PMID: 21883162]
Kwon, J.M.; Goate, A.M. The candidate gene approach. Alcohol Res. Health, 2000, 24(3), 164-168.
[PMID: 11199286]
Rosenberg, R.N.; Pascual, J.M. Rosenberg’s Molecular and Genetic Basis of Neurological and Psychiatric Disease, 5th ed; , 2014.
Vidal, A.C.; Benjamin Neelon, S.E.; Liu, Y.; Tuli, A.M.; Fuemmeler, B.F.; Hoyo, C.; Murtha, A.P.; Huang, Z.; Schildkraut, J.; Overcash, F.; Kurtzberg, J.; Jirtle, R.L.; Iversen, E.S.; Murphy, S.K. Maternal stress, preterm birth, and DNA methylation at imprint regulatory sequences in humans. Genet. Epigenet., 2014, 6, 37-44.
[] [PMID: 25512713]
Vangeel, E.B.; Izzi, B.; Hompes, T.; Vansteelandt, K.; Lambrechts, D.; Freson, K.; Claes, S. DNA methylation in imprinted genes IGF2 and GNASXL is associated with prenatal maternal stress. Genes Brain Behav., 2015, 14(8), 573-582.
[] [PMID: 26333472]
Rijlaarsdam, J.; Pappa, I.; Walton, E.; Bakermans-Kranenburg, M.J.; Mileva-Seitz, V.R.; Rippe, R.C.A.; Roza, S.J.; Jaddoe, V.W.V.; Verhulst, F.C.; Felix, J.F.; Cecil, C.A.M.; Relton, C.L.; Gaunt, T.R.; McArdle, W.; Mill, J.; Barker, E.D.; Tiemeier, H.; van IJzendoorn, M.H. An epigenome-wide association meta-analysis of prenatal maternal stress in neonates: A model approach for replication. Epigenetics, 2016, 11(2), 140-149.
[] [PMID: 26889969]
Wikenius, E.; Myhre, A.M.; Page, C.M.; Moe, V.; Smith, L.; Heiervang, E.R.; Undlien, D.E.; LeBlanc, M. Prenatal maternal depressive symptoms and infant DNA methylation: a longitudinal epigenome-wide study. Nord. J. Psychiatry, 2019, 73(4-5), 257-263.
[] [PMID: 31070508]
Non, A.L.; Binder, A.M.; Kubzansky, L.D.; Michels, K.B. Genome-wide DNA methylation in neonates exposed to maternal depression, anxiety, or SSRI medication during pregnancy. Epigenetics, 2014, 9(7), 964-972.
[] [PMID: 24751725]
Nieratschker, V.; Massart, R.; Gilles, M.; Luoni, A.; Suderman, M.J.; Krumm, B.; Meier, S.; Witt, S.H.; Nöthen, M.M.; Suomi, S.J.; Peus, V.; Scharnholz, B.; Dukal, H.; Hohmeyer, C.; Wolf, I.A.C.; Cirulli, F.; Gass, P.; Sütterlin, M.W.; Filsinger, B.; Laucht, M.; Riva, M.A.; Rietschel, M.; Deuschle, M.; Szyf, M. MORC1 exhibits cross-species differential methylation in association with early life stress as well as genome-wide association with MDD. Transl. Psychiat, 2014, 4(8), 429.
Cao-Lei, L.; Massart, R.; Suderman, M.J.; Machnes, Z.; Elgbeili, G.; Laplante, D.P.; Szyf, M.; King, S. DNA methylation signatures triggered by prenatal maternal stress exposure to a natural disaster: project ice Storm. PLoS One, 2014, 9(9), e107653.
[] [PMID: 25238154]
Hamada, H.; Matthews, S.G. Prenatal programming of stress responsiveness and behaviours: Progress and perspectives. J. Neuroendocrinol., 2019, 31(3), e12674.
[] [PMID: 30582647]
Lee, S.R.; Choi, B.; Paul, S.; Seo, J.H.; Back, D.B.; Han, J.S.; Choi, D.H.; Kwon, K.J.; Shin, C.Y.; Lee, J.; Han, S.H.; Kim, H.Y. Depressive-like behaviors in a rat model of chronic cerebral hypoperfusion. Transl. Stroke Res., 2015, 6(3), 207-214.
[] [PMID: 25541087]
Matrisciano, F.; Tueting, P.; Dalal, I.; Kadriu, B.; Grayson, D.R.; Davis, J.M.; Nicoletti, F.; Guidotti, A. Epigenetic modifications of GABAergic interneurons are associated with the schizophrenia- like phenotype induced by prenatal stress in mice. Neuropharmacology, 2013, 68, 184-194.
[] [PMID: 22564440]
Zucchi, F.C.R.; Yao, Y.; Ward, I.D.; Ilnytskyy, Y.; Olson, D.M.; Benzies, K.; Kovalchuk, I.; Kovalchuk, O.; Metz, G.A.S. Maternal stress induces epigenetic signatures of psychiatric and neurological diseases in the offspring. PLoS One, 2013, 8(2), e56967.
[] [PMID: 23451123]
Monteleone, M.C.; Adrover, E.; Pallarés, M.E.; Antonelli, M.C.; Frasch, A.C.; Brocco, M.A. Prenatal stress changes the glycoprotein GPM6A gene expression and induces epigenetic changes in rat offspring brain. Epigenetics, 2014, 9(1), 152-160.
[] [PMID: 23959066]
Monteleone, M.C.; Pallarés, M.E.; Billi, S.C.; Antonelli, M.C.; Brocco, M.A. In vivo and in vitro neuronal plasticity modulation by epigenetic regulators. J. Mol. Neurosci., 2018, 65(3), 301-311.
[] [PMID: 29931501]
Benoit, J.D.; Rakic, P.; Frick, K.M. Prenatal stress induces spatial memory deficits and epigenetic changes in the hippocampus indicative of heterochromatin formation and reduced gene expression. Behav. Brain Res., 2015, 281, 1-8.
[] [PMID: 25496779]
Van den Hove, D.L.A.; Kenis, G.; Brass, A.; Opstelten, R.; Rutten, B.P.F.; Bruschettini, M.; Blanco, C.E.; Lesch, K.P.; Steinbusch, H.W.M.; Prickaerts, J. Vulnerability versus resilience to prenatal stress in male and female rats; implications from gene expression profiles in the hippocampus and frontal cortex. Eur. Neuropsychopharmacol., 2013, 23(10), 1226-1246.
[] [PMID: 23199416]
Dawes, G.S.; Serra-Serra, V.; Moulden, M.; Redman, C.W.G. Dexamethasone and fetal heart rate variation. Br. J. Obstet. Gynaecol., 1994, 101(8), 675-679.
[] [PMID: 7947501]
Derks, J.B.; Mulder, E.J.H.; Visser, G.H.A. The effects of maternal betamethasone administration on the fetus. Br. J. Obstet. Gynaecol., 1995, 102(1), 40-46.
[] [PMID: 7833309]
Mulder, E.J.H.; Derks, J.B.; Visser, G.H.A. Antenatal corticosteroid therapy and fetal behaviour: a randomised study of the effects of betamethasone and dexamethasone. Br. J. Obstet. Gynaecol., 1997, 104(11), 1239-1247.
[] [PMID: 9386023]
Senat, M.V.; Minoui, S.; Multon, O.; Fernandez, H.; Frydman, R.; Ville, Y. Effect of dexamethasone and betamethasone on fetal heart rate variability in preterm labour: a randomised study. Br. J. Obstet. Gynaecol., 1998, 105(7), 749-755.
[] [PMID: 9692416]
Braithwaite, E.C.; Kundakovic, M.; Ramchandani, P.G.; Murphy, S.E.; Champagne, F.A. Maternal prenatal depressive symptoms predict infant NR3C1 1F and BDNF IV DNA methylation. Epigenetics, 2015, 10(5), 408-417.
[] [PMID: 25875334]
Fink, N.S.; Urech, C.; Berger, C.T.; Hoesli, I.; Holzgreve, W.; Bitzer, J.; Alder, J. Maternal laboratory stress influences fetal neurobehavior: cortisol does not provide all answers. J. Matern. Fetal Neonatal Med., 2010, 23(6), 488-500.
[] [PMID: 20298130]
Makino, I.; Matsuda, Y.; Yoneyama, M.; Hirasawa, K.; Takagi, K.; Ohta, H.; Konishi, Y. Effect of maternal stress on fetal heart rate assessed by vibro acoustic stimulation. J. Int. Med. Res., 2009, 37(6), 1780-1788.
[] [PMID: 20146876]
Monk, C.; Myers, M.M.; Sloan, R.P.; Ellman, L.M.; Fifer, W.P. Effects of women’s stress-elicited physiological activity and chronic anxiety on fetal heart rate. J. Dev. Behav. Pediatr., 2003, 24(1), 32-38.
[] [PMID: 12584483]
Kinsella, M.T.; Monk, C. Impact of maternal stress, depression and anxiety on fetal neurobehavioral development. Clin. Obstet. Gynecol., 2009, 52(3), 425-440.
[] [PMID: 19661759]
Gao, Y.; Huang, Y.; Li, X. Interaction between prenatal maternal stress and autonomic arousal in predicting conduct problems and psychopathic traits in children. J. Psychopathol. Behav. Assess., 2017, 39(1), 1-14.
[] [PMID: 28286370]
Bauer, A.; Kantelhardt, J.W.; Barthel, P.; Schneider, R.; Mäkikallio, T.; Ulm, K.; Hnatkova, K.; Schömig, A.; Huikuri, H.; Bunde, A.; Malik, M.; Schmidt, G. Deceleration capacity of heart rate as a predictor of mortality after myocardial infarction: cohort study. Lancet, 2006, 367(9523), 1674-1681.
[] [PMID: 16714188]
Kantelhardt, J.W.; Bauer, A.; Schumann, A.Y.; Barthel, P.; Schneider, R.; Malik, M.; Schmidt, G. Phase-rectified signal averaging for the detection of quasi-periodicities and the prediction of cardiovascular risk. Chaos, 2007, 17(1), 015112.
[] [PMID: 17411269]
Graatsma, E.M.; Mulder, E.J.H.; Vasak, B.; Lobmaier, S.M.; Pildner von Steinburg, S.; Schneider, K.T.M.; Schmidt, G.; Visser, G.H.A. Average acceleration and deceleration capacity of fetal heart rate in normal pregnancy and in pregnancies complicated by fetal growth restriction. J. Matern. Fetal Neonatal Med., 2012, 25(12), 2517-2522.
[] [PMID: 22725720]
Huhn, E.A.; Lobmaier, S.; Fischer, T.; Schneider, R.; Bauer, A.; Schneider, K.T.; Schmidt, G. New computerized fetal heart rate analysis for surveillance of intrauterine growth restriction. Prenat. Diagn., 2011, 31(5), 509-514.
[] [PMID: 21360555]
Lobmaier, S.M.; Huhn, E.A.; Pildner von Steinburg, S.; Müller, A.; Schuster, T.; Ortiz, J.U.; Schmidt, G.; Schneider, K.T. Phase-rectified signal averaging as a new method for surveillance of growth restricted fetuses. J. Matern. Fetal Neonatal Med., 2012, 25(12), 2523-2528.
[] [PMID: 22630786]
Lobmaier, S. M.; Mensing van Charante, N.; Ferrazzi, E.; Giussani, D. A.; Shaw, C. J.; Müller, A.; Ortiz, J. U.; Ostermayer, E.; Haller, B.; Prefumo, F.; Frusca, T.; Hecher, K.; Arabin, B.; Thilaganathan, B.; Papageorghiou, A. T.; Bhide, A.; Martinelli, P.; Duvekot, J. J.; van Eyck, J.; Visser, G. H. A.; Schmidt, G.; Ganzevoort, W.; Lees, C. C.; Schneider, K. T. M.; Bilardo, C. M.; Brezinka, C.; Diemert, A.; Derks, J. B.; Schlembach, D.; Todros, T.; Valcamonico, A.; Marlow, N.; van Wassenaer-Leemhuis, A. Phase-rectified signal averaging method to predict perinatal outcome in infants with very preterm fetal growth restriction- a secondary analysis of TRUFFLE-trial. Am. J. Obstetrics Gynecol., 2016, 215(5), 630 e1-630 e7.
Georgieva, A.; Papageorghiou, A.T.; Payne, S.J.; Moulden, M.; Redman, C.W.G. Phase-rectified signal averaging for intrapartum electronic fetal heart rate monitoring is related to acidaemia at birth. BJOG, 2014, 121(7), 889-894.
[] [PMID: 24842087]
Weyrich, J.; Ortiz, J.U.; Müller, A.; Schmidt, G.; Brambs, C.E.; Graupner, O.; Kuschel, B.; Lobmaier, S.M. Intrapartum PRSA: a new method to predict fetal acidosis?-a case-control study. Arch. Gynecol. Obstet., 2020, 301(1), 137-142.
[] [PMID: 31883047]
Rivolta, M.W.; Stampalija, T.; Casati, D.; Richardson, B.S.; Ross, M.G.; Frasch, M.G.; Bauer, A.; Ferrazzi, E.; Sassi, R. Acceleration and deceleration capacity of fetal heart rate in an in-vivo sheep model. PLoS One, 2014, 9(8), e104193.
[] [PMID: 25141131]
Lobmaier, S.M.; Ortiz, J.U.; Sewald, M.; Müller, A.; Schmidt, G.; Haller, B.; Oberhoffer, R.; Schneider, K.T.M.; Giussani, D.A.; Wacker-Gussmann, A. Influence of gestational diabetes on fetal autonomic nervous system: a study using phase-rectified signal-averaging analysis. Ultrasound Obstet. Gynecol., 2018, 52(3), 347-351.
[] [PMID: 28782142]
Frasch, M.G.; Xu, Y.; Stampalija, T.; Durosier, L.D.; Herry, C.; Wang, X.; Casati, D.; Seely, A.J.E.; Alfirevic, Z.; Gao, X.; Ferrazzi, E. Correlating multidimensional fetal heart rate variability analysis with acid-base balance at birth. Physiol. Meas., 2014, 35(12), L1-L12.
[] [PMID: 25407948]
Lobmaier, S.M.; Müller, A.; Zelgert, C.; Shen, C.; Su, P.C.; Schmidt, G.; Haller, B.; Berg, G.; Fabre, B.; Weyrich, J.; Wu, H.T.; Frasch, M.G.; Antonelli, M.C. Fetal heart rate variability responsiveness to maternal stress, non-invasively detected from maternal transabdominal ECG. Arch. Gynecol. Obstet., 2020, 301(2), 405-414.
[] [PMID: 31781889]
Barthel, P.; Bauer, A.; Müller, A.; Huster, K.M.; Kanters, J.K.; Paruchuri, V.; Yang, X.; Ulm, K.; Malik, M.; Schmidt, G. Spontaneous baroreflex sensitivity: prospective validation trial of a novel technique in survivors of acute myocardial infarction. Heart Rhythm, 2012, 9(8), 1288-1294.
[] [PMID: 22516186]
Brenhouse, H.C.; Andersen, S.L. Developmental trajectories during adolescence in males and females: a cross-species understanding of underlying brain changes. Neurosci. Biobehav. Rev., 2011, 35(8), 1687-1703.
[] [PMID: 21600919]
Andersen, S. L. Trajectories of brain development: point of vulnerability or window of opportunity? Neurosci. Biobehav. Rev., 2003, 27(1-2), 3-18.
Bonnier, C. Evaluation of early stimulation programs for enhancing brain development. Acta Paediatr., 2008, 97(7), 853-858.
[] [PMID: 18482172]
Cioni, G.; Inguaggiato, E.; Sgandurra, G. Early intervention in neurodevelopmental disorders: underlying neural mechanisms. Dev. Med. Child Neurol., 2016, 58(Suppl. 4), 61-66.
[] [PMID: 27027609]
McQuillan, M.E.; Bates, J.E.; Staples, A.D.; Deater-Deckard, K. Maternal stress, sleep, and parenting. J. Fam. Psychol., 2019, 33(3), 349-359.
[] [PMID: 30762410]
Hagaman, A.; Gallis, J.A.; Bhalotra, S.; Baranov, V.; Turner, E.L.; Sikander, S.; Maselko, J. Psychosocial determinants of sustained maternal functional impairment: Longitudinal findings from a pregnancy-birth cohort study in rural Pakistan. PLoS One, 2019, 14(11), e0225163.
[] [PMID: 31743374]
Cprek, S.E.; Williams, C.M.; Asaolu, I.; Alexander, L.A.; Vanderpool, R.C. Three positive parenting practices and their correlation with risk of childhood developmental, social, or behavioral delays: an analysis of the national survey of children’s health. Matern. Child Health J., 2015, 19(11), 2403-2411.
[] [PMID: 26100132]
Garg, E.; Chen, L.; Nguyen, T.T.T.; Pokhvisneva, I.; Chen, L.M.; Unternaehrer, E.; MacIsaac, J.L.; McEwen, L.M.; Mah, S.M.; Gaudreau, H.; Levitan, R.; Moss, E.; Sokolowski, M.B.; Kennedy, J.L.; Steiner, M.S.; Meaney, M.J.; Holbrook, J.D.; Silveira, P.P.; Karnani, N.; Kobor, M.S.; O’Donnell, K.J. The early care environment and DNA methylome variation in childhood; , 2018.
Suor, J.H.; Sturge-Apple, M.L.; Davies, P.T.; Cicchetti, D. A life history approach to delineating how harsh environments and hawk temperament traits differentially shape children’s problem-solving skills. J. Child Psychol. Psychiatry, 2017, 58(8), 902-909.
[] [PMID: 28326540]
Majnemer, A. Benefits of early intervention for children with developmental disabilities. Semin. Pediatr. Neurol., 1998, 5(1), 62-69.
[] [PMID: 9548643]
Glover, V. Maternal depression, anxiety and stress during pregnancy and child outcome; what needs to be done. Best Pract. Res. Clin. Obstet. Gynaecol., 2014, 28(1), 25-35.
[] [PMID: 24090740]
Keilty, B.; Smith, J. Family and practitioner perspectives on prenatal early intervention. Intellect. Dev. Disabil., 2020, 58(1), 1-18.
[] [PMID: 32011222]
Olds, D.; Henderson, C.R., Jr; Cole, R.; Eckenrode, J.; Kitzman, H.; Luckey, D.; Pettitt, L.; Sidora, K.; Morris, P.; Powers, J. Long-term effects of nurse home visitation on children’s criminal and antisocial behavior: 15-year follow-up of a randomized controlled trial. JAMA, 1998, 280(14), 1238-1244.
[] [PMID: 9786373]
Haggerty, K.P.; McGlynn-Wright, A.; Klima, T. Promising parenting programs for reducing adolescent problem behaviors. J. Child. Serv., 2013, 8(4), 10.
[] [PMID: 24416068]
Spittle, A.; Treyvaud, K. The role of early developmental intervention to influence neurobehavioral outcomes of children born preterm. Semin. Perinatol., 2016, 40(8), 542-548.
[] [PMID: 27817913]
Sgandurra, G.; Lorentzen, J.; Inguaggiato, E.; Bartalena, L.; Beani, E.; Cecchi, F.; Dario, P.; Giampietri, M.; Greisen, G.; Herskind, A.; Nielsen, J.B.; Rossi, G.; Cioni, G. A randomized clinical trial in preterm infants on the effects of a home-based early intervention with the ‘CareToy System’. PLoS One, 2017, 12(3), e0173521.
[] [PMID: 28328946]
Spittle, A.; Orton, J.; Anderson, P.J.; Boyd, R.; Doyle, L.W. Early developmental intervention programmes provided post hospital discharge to prevent motor and cognitive impairment in preterm infants. Cochrane Database Syst. Rev., 2015, (11), CD005495.
[] [PMID: 26597166]
Branjerdporn, G.; Meredith, P.; Strong, J.; Green, M. Sensory sensitivity and its relationship with adult attachment and parenting styles. PLoS One, 2019, 14(1), e0209555.
[] [PMID: 30625166]
Planalp, E.M.; O’Neill, M.; Braungart-Rieker, J.M. Parent mind- mindedness, sensitivity, and infant affect: Implications for attachment with mothers and fathers. Infant Behav. Dev., 2019, 57, 101330.
[] [PMID: 31228665]
Hutchon, B.; Gibbs, D.; Harniess, P.; Jary, S.; Crossley, S.L.; Moffat, J.V.; Basu, N.; Basu, A.P. Early intervention programmes for infants at high risk of atypical neurodevelopmental outcome. Dev. Med. Child Neurol., 2019, 61(12), 1362-1367.
[] [PMID: 30828797]
Ferreira, R.C.; Alves, C.R.L.; Guimaraes, M.A.P.; Menezes, K.K.P.; Magalhaes, L.C. Effects of early intervention focused on the family in the development of children born premature and/or at social risk: a meta-analysis. J. Pediatr. (Rio J.), 2020, 96(1), 20-38.
Shenhar-Tsarfaty, S.; Berliner, S.; Bornstein, N.M.; Soreq, H. Cholinesterases as biomarkers for parasympathetic dysfunction and inflammation-related disease. J. Mol. Neurosci., 2014, 53(3), 298-305.
[] [PMID: 24254221]
Gonzalez, D.; Jacobsen, D.; Ibar, C.; Pavan, C.; Monti, J.; Fernandez Machulsky, N.; Balbi, A.; Fritzler, A.; Jamardo, J.; Repetto, E.M.; Berg, G.; Fabre, B. Hair cortisol measurement by an automated method. Sci. Rep., 2019, 9(1), 8213.
[] [PMID: 31160639]

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