Early Life Stress, Growth and Neurodevelopment in Childhood
Main Article Content
Abstract
Follow up studies of children with congenital heart disease, premature birth, small for gestational age syndrome and attention deficit hyperactivity disorder show significantly reduced 24-hours heart rate variability (HRV) that indicate autonomic dysfunction. The underlying pathophysiological process is of high clinical importance if autonomic dysfunction in these children is related to neurocognitive impairment, an enhanced cardiovascular risk, and a higher risk of short stature. Elevated norepinephrine levels, reduced HRV and MRI imaging indicate brain injury very early in life. We introduce the term autonomic imprinting to explain how early life stress have a lifelong imprinting effect on the autonomic nervous system. Many efforts are done for a careful management of infants in pediatric intensive care units. However, early life stress cannot be prevented if sympathetic activation is part of the underlying disease most of all due to congestive heart failure. We could demonstrate that beside a careful management, pharmacotherapy has a high impact on autonomic dysfunction in children with heart failure, attention deficit disorder and short stature. Moreover, online HRV monitoring is a complete noninvasive tool to monitor early life stress if it uses the data from routine heart rate monitoring. HRV online monitoring on the pediatric intensive care unit and Holter ECG monitoring in a daily life setting are clinical routine in our department for each pharmacotherapy affecting the autonomic nervous system. In the same time as monitoring of early life stress becomes clinically routine, the situation of children will improve if we realize which interventions increase early life stress or improve its detrimental damages in longtime follow up.
Article Details
How to Cite
BUCHHORN, Reiner.
Early Life Stress, Growth and Neurodevelopment in Childhood.
Medical Research Archives, [S.l.], v. 8, n. 10, oct. 2020.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/2260>. Date accessed: 21 dec. 2024.
doi: https://doi.org/10.18103/mra.v8i10.2260.
Section
Research Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
1. Buchhorn R, Hulpke-Wette M, Nothroff J, Paul T. Heart rate variability in infants with heart failure due to congenital heart disease: reversal of depressed heart rate variability by propranolol. Med Sci Monit. 2002;8(10):CR661-CR6.
2. Buchhorn R, Baumann C, Willaschek C. Alleviation of arrhythmia burden in children with frequent idiopathic premature ventricular contractions by omega-3-fatty acid supplementation. International journal of cardiology. 2019;291:52-6. doi:10.1016/j.ijcard.2019.05.054.
3. Buchhorn R, Baumann C, Gündogdu S, Rakowski U, Willaschek C. Diagnosis and management of an inappropriate sinus tachycardia in adolescence based upon a Holter ECG: A retrospective analysis of 479 patients. PloS one. 2020;15(8):e0238139.
4. Buchhorn R, Hammersen A, Bartmus D, Bursch J. The pathogenesis of heart failure in infants with congenital heart disease. Cardiol Young. 2001;11(5):498-504.
5. Buchhorn R. Why are psychiatric disorders in children becoming more and more common? Int J Emerg Ment Health. 2014;16(2):322-5.
6. Buchhorn R, Meint S, Willaschek C. The Impact of Early Life Stress on Growth and Cardiovascular Risk: A Possible Example for Autonomic Imprinting? PLoS ONE. 2016;11(11):e0166447.
7. Thayer JF, Lane RD. The role of vagal function in the risk for cardiovascular disease and mortality. Biol Psychol. 2007;74(2):224-42.
8. Porges SW. The Polyvagal Theory: phylogenetic contributions to social behavior. Physiol Behav. 2003;79(3):503-13.
9. Tyborowska A, Volman I, Niermann HCM, Pouwels JL, Smeekens S, Cillessen AHN et al. Early-life and pubertal stress differentially modulate grey matter development in human adolescents. Scientific reports. 2018;8(1):9201. doi:10.1038/s41598-018-27439-5.
10. Saboory E, Ghasemi M, Mehranfard N. Norepinephrine, neurodevelopment and behavior. Neurochemistry international. 2020;135:104706. doi:10.1016/j.neuint.2020.104706.
11. Thayer JF, Ahs F, Fredrikson M, Sollers JJ, III, Wager TD. A meta-analysis of heart rate variability and neuroimaging studies: implications for heart rate variability as a marker of stress and health. Neurosci Biobehav Rev. 2012;36(2):747-56.
12. Kirschen MP, Francoeur C, Murphy M, Traynor D, Zhang B, Mensinger JL et al. Epidemiology of Brain Death in Pediatric Intensive Care Units in the United States. JAMA pediatrics. 2019;173(5):469-76. doi:10.1001/jamapediatrics.2019.0249.
13. Piantino JA, Lin A, Crowder D, Williams CN, Perez-Alday E, Tereshchenko LG et al. Early Heart Rate Variability and Electroencephalographic Abnormalities in Acutely Brain-Injured Children Who Progress to Brain Death. Pediatric critical care medicine : a journal of the Society of Critical Care Medicine and the World Federation of Pediatric Intensive and Critical Care Societies. 2019;20(1):38-46. doi:10.1097/pcc.0000000000001759.
14. Oliveira V, Martins R, Liow N, Teiserskas J, von Rosenberg W, Adjei T et al. Prognostic Accuracy of Heart Rate Variability Analysis in Neonatal Encephalopathy: A Systematic Review. Neonatology. 2019;115(1):59-67. doi:10.1159/000493002.
15. Martin JA, Hamilton BE, Osterman MJK. Births in the United States, 2017. NCHS data brief. 2018(318):1-8.
16. Luu TM, Rehman Mian MO, Nuyt AM. Long-Term Impact of Preterm Birth: Neurodevelopmental and Physical Health Outcomes. Clinics in perinatology. 2017;44(2):305-14. doi:10.1016/j.clp.2017.01.003.
17. Clements KM, Barfield WD, Ayadi MF, Wilber N. Preterm birth-associated cost of early intervention services: an analysis by gestational age. Pediatrics. 2007;119(4):e866-74. doi:10.1542/peds.2006-1729.
18. Schieve LA, Tian LH, Rankin K, Kogan MD, Yeargin-Allsopp M, Visser S et al. Population impact of preterm birth and low birth weight on developmental disabilities in US children. Annals of epidemiology. 2016;26(4):267-74. doi:10.1016/j.annepidem.2016.02.012.
19. Plomgaard AM, Alderliesten T, van Bel F, Benders M, Claris O, Cordeiro M et al. No neurodevelopmental benefit of cerebral oximetry in the first randomised trial (SafeBoosC II) in preterm infants during the first days of life. Acta Paediatr. 2019;108(2):275-81. doi:10.1111/apa.14463.
20. Nist MD, Harrison TM, Steward DK. The biological embedding of neonatal stress exposure: A conceptual model describing the mechanisms of stress-induced neurodevelopmental impairment in preterm infants. Research in nursing & health. 2019;42(1):61-71. doi:10.1002/nur.21923.
21. Evans DJ, MacGregor RJ, Dean HG, Levene MI. Neonatal catecholamine levels and neurodevelopmental outcome: a cohort study. Archives of disease in childhood Fetal and neonatal edition. 2001;84(1):F49-52. doi:10.1136/fn.84.1.f49.
22. Yam KY, Schipper L, Reemst K, Ruigrok SR, Abbink MR, Hoeijmakers L et al. Increasing availability of omega-3 fatty acid in the early-life diet prevents the early-life stress-induced cognitive impairments without affecting metabolic alterations. Faseb j. 2019:fj201802297R. doi:10.1096/fj.201802297R.
23. Jafri SK, Ehsan L, Abbas Q, Ali F, Chand P, Ul Haque A. Frequency and Outcome of Acute Neurologic Complications after Congenital Heart Disease Surgery. Journal of pediatric neurosciences. 2017;12(4):328-31. doi:10.4103/jpn.JPN_87_17.
24. Tsao PC, Lee YS, Jeng MJ, Hsu JW, Huang KL, Tsai SJ et al. Additive effect of congenital heart disease and early developmental disorders on attention-deficit/hyperactivity disorder and autism spectrum disorder: a nationwide population-based longitudinal study. European child & adolescent psychiatry. 2017;26(11):1351-9. doi:10.1007/s00787-017-0989-8.
25. Longin E, Schaible T, Lenz T, Konig S. Short term heart rate variability in healthy neonates: normative data and physiological observations. Early Hum Dev. 2005;81(8):663-71.
26. Gruber EM, Laussen PC, Casta A, Zimmerman AA, Zurakowski D, Reid R et al. Stress response in infants undergoing cardiac surgery: a randomized study of fentanyl bolus, fentanyl infusion, and fentanyl-midazolam infusion. Anesthesia and analgesia. 2001;92(4):882-90.
27. Dimitrijevic L, Bjelakovic B, Colovic H, Mikov A, Zivkovic V, Kocic M et al. Assessment of general movements and heart rate variability in prediction of neurodevelopmental outcome in preterm infants. Early human development. 2016;99:7-12. doi:10.1016/j.earlhumdev.2016.05.014.
28. Goulding RM, Stevenson NJ, Murray DM, Livingstone V, Filan PM, Boylan GB. Heart rate variability in hypoxic ischemic encephalopathy: correlation with EEG grade and 2-y neurodevelopmental outcome. Pediatr Res. 2015;77(5):681-7.
29. von Rhein M, Buchmann A, Hagmann C, Huber R, Klaver P, Knirsch W et al. Brain volumes predict neurodevelopment in adolescents after surgery for congenital heart disease. Brain : a journal of neurology. 2014;137(Pt 1):268-76. doi:10.1093/brain/awt322.
30. Miller SP, McQuillen PS, Hamrick S, Xu D, Glidden DV, Charlton N et al. Abnormal brain development in newborns with congenital heart disease. The New England journal of medicine. 2007;357(19):1928-38. doi:10.1056/NEJMoa067393.
31. Schiller RM, H IJ, Madderom MJ, Rietman AB, Smits M, van Heijst AFJ et al. Neurobiologic Correlates of Attention and Memory Deficits Following Critical Illness in Early Life. Crit Care Med. 2017;45(10):1742-50. doi:10.1097/ccm.0000000000002553.
32. Natalucci G, Bucher HU, Von Rhein M, Borradori Tolsa C, Latal B, Adams M. Population based report on health related quality of life in adolescents born very preterm. Early human development. 2017;104:7-12. doi:10.1016/j.earlhumdev.2016.11.002.
33. Botellero VL, Skranes J, Bjuland KJ, Haberg AK, Lydersen S, Brubakk AM et al. A longitudinal study of associations between psychiatric symptoms and disorders and cerebral gray matter volumes in adolescents born very preterm. BMC pediatrics. 2017;17(1):45. doi:10.1186/s12887-017-0793-0.
34. Kumar R, Yadav SK, Palomares JA, Park B, Joshi SH, Ogren JA et al. Reduced regional brain cortical thickness in patients with heart failure. PloS one. 2015;10(5):e0126595. doi:10.1371/journal.pone.0126595.
35. Woo MA, Kumar R, Macey PM, Fonarow GC, Harper RM. Brain injury in autonomic, emotional, and cognitive regulatory areas in patients with heart failure. Journal of cardiac failure. 2009;15(3):214-23. doi:10.1016/j.cardfail.2008.10.020.
36. Rosch KS, Crocetti D, Hirabayashi K, Denckla MB, Mostofsky SH, Mahone EM. Reduced subcortical volumes among preschool-age girls and boys with ADHD. Psychiatry research Neuroimaging. 2018;271:67-74. doi:10.1016/j.pscychresns.2017.10.013.
37. Suffren S, Angulo D, Ding Y, Reyes P, Marin J, Hernandez JT et al. Long-term attention deficits combined with subcortical and cortical structural central nervous system alterations in young adults born small for gestational age. Early human development. 2017;110:44-9. doi:10.1016/j.earlhumdev.2017.04.016.
38. Wei L, Chen H, Wu GR. Heart rate variability associated with grey matter volumes in striatal and limbic structures of the central autonomic network. Brain research. 2018;1681:14-20. doi:10.1016/j.brainres.2017.12.024.
39. Willaschek C, Meint S, Rager K, Buchhorn R. Modified Clonidine Testing for Growth Hormone Stimulation Reveals alpha2-Adrenoreceptor Sub Sensitivity in Children with Idiopathic Growth Hormone Deficiency. PLoS ONE. 2015;10(9):e0137643.
40. Wulsin LR, Horn PS, Perry JL, Massaro JM, D'Agostino RB. Autonomic Imbalance as a Predictor of Metabolic Risks, Cardiovascular Disease, Diabetes, and Mortality. J Clin Endocrinol Metab. 2015;100(6):2443-8.
41. Manhardt LB, Norozi K, Muller C, Willaschek C, Kostuch B, Buchhorn R. NT-Pro-B-Type Natriuretic Peptide Levels in Infants with Failure to Thrive due to Caloric Deprivation. Int J Pediatr. 2010;2010:983468.
42. Paul MA, Backer CL, Binns HJ, Mavroudis C, Webb CL, Yogev R et al. B-Type Natriuretic Peptide and Heart Failure in Patients with Ventricular Septal Defect: A Pilot Study. Pediatr Cardiol. 2009.
43. Fujioka K, Mizobuchi M, Sakai H, Iwatani S, Wada K, Yoshimoto S et al. N-terminal pro-brain natriuretic peptide levels in monochorionic diamniotic twins with selective intrauterine growth restriction. J Perinatol. 2014;34(1):6-10.
44. Waterland RA, Garza C. Potential mechanisms of metabolic imprinting that lead to chronic disease. Am J Clin Nutr. 1999;69(2):179-97.
45. Barker DJ, Winter PD, Osmond C, Margetts B, Simmonds SJ. Weight in infancy and death from ischaemic heart disease. Lancet. 1989;2(8663):577-80.
46. Martorell R, Horta BL, Adair LS, Stein AD, Richter L, Fall CH et al. Weight gain in the first two years of life is an important predictor of schooling outcomes in pooled analyses from five birth cohorts from low- and middle-income countries. J Nutr. 2010;140(2):348-54.
47. Wood AR, Esko T, Yang J, Vedantam S, Pers TH, Gustafsson S et al. Defining the role of common variation in the genomic and biological architecture of adult human height. Nat Genet. 2014;46(11):1173-86.
48. Simeone P, Alberti S. Epigenetic heredity of human height. Physiol Rep. 2014;2(6).
49. Sandberg DE, Voss LD. The psychosocial consequences of short stature: a review of the evidence. Best Pract Res Clin Endocrinol Metab. 2002;16(3):449-63.
50. Buchhorn R, Willaschek C. Growth Hormone Treatment, Cardiovascular Risk and Autonomic Maturation in Children and Adolescents with Growth Hormone Deficiency or Born Small for Gestational Age. Open Journal of Pediatrics. 2020;10:12-29.
51. Buchhorn R, Conzelmann A, Willaschek C, Stork D, Taurines R, Renner TJ. Heart rate variability and methylphenidate in children with ADHD. Atten Defic Hyperact Disord. 2012;4(2):85-91.
52. Myers KA, Bello-Espinosa LE, Symonds JD, Zuberi SM, Clegg R, Sadleir LG et al. Heart rate variability in epilepsy: A potential biomarker of sudden unexpected death in epilepsy risk. Epilepsia. 2018;59(7):1372-80. doi:10.1111/epi.14438.
53. Mueller SG, Nei M, Bateman LM, Knowlton R, Laxer KD, Friedman D et al. Brainstem network disruption: A pathway to sudden unexplained death in epilepsy? Human brain mapping. 2018;39(12):4820-30. doi:10.1002/hbm.24325.
54. Buchhorn R, Hulpke-Wette M, Hilgers R, Bartmus D, Wessel A, Bursch J. Propranolol treatment of congestive heart failure in infants with congenital heart disease: The CHF-PRO-INFANT Trial. Congestive heart failure in infants treated with propanol. Int J Cardiol. 2001;79(2-3):167-73.
55. Buchhorn R, Christian W. Ventricular arrhythmias in children with attention deficit disorder - a symptom of autonomic imbalance? Cardiol Young. 2013:1-6.
56. Cohen BE, Edmondson D, Kronish IM. State of the Art Review: Depression, Stress, Anxiety, and Cardiovascular Disease. Am J Hypertens. 2015;28(11):1295-302.
57. Koenig J, Rash JA, Kemp AH, Buchhorn R, Thayer JF, Kaess M. Resting state vagal tone in attention deficit (hyperactivity) disorder: A meta-analysis. World J Biol Psychiatry. 2016:1-15.
58. Habel LA, Cooper WO, Sox CM, Chan KA, Fireman BH, Arbogast PG et al. ADHD medications and risk of serious cardiovascular events in young and middle-aged adults. JAMA. 2011;306(24):2673-83.
59. Cooper WO, Habel LA, Sox CM, Chan KA, Arbogast PG, Cheetham TC et al. ADHD drugs and serious cardiovascular events in children and young adults. N Engl J Med. 2011;365(20):1896-904.
60. Conradt E, Flannery T, Aschner JL, Annett RD, Croen LA, Duarte CS et al. Prenatal Opioid Exposure: Neurodevelopmental Consequences and Future Research Priorities. Pediatrics. 2019;144(3). doi:10.1542/peds.2019-0128.
61. Nederend I, Jongbloed MRM, de Geus EJC, Blom NA, Ten Harkel ADJ. Postnatal Cardiac Autonomic Nervous Control in Pediatric Congenital Heart Disease. Journal of cardiovascular development and disease. 2016;3(2). doi:10.3390/jcdd3020016.
62. Ohuchi H, Takasugi H, Ohashi H, Yamada O, Watanabe K, Yagihara T et al. Abnormalities of neurohormonal and cardiac autonomic nervous activities relate poorly to functional status in fontan patients. Circulation. 2004;110(17):2601-8.
63. Siddiqui S, Fifer WP, Ordonez-Retamar M, Nugent JD, Williams IA. An antenatal marker of neurodevelopmental outcomes in infants with congenital heart disease. Journal of perinatology : official journal of the California Perinatal Association. 2017;37(8):953-7. doi:10.1038/jp.2017.59.
64. Haraldsdottir K, Watson AM, Goss KN, Beshish AG, Pegelow DF, Palta M et al. Impaired autonomic function in adolescents born preterm. Physiol Rep. 2018;6(6):e13620. doi:10.14814/phy2.13620.
65. Harrison TM, Brown R. Autonomic Nervous System Function After a Skin-to-Skin Contact Intervention in Infants With Congenital Heart Disease. The Journal of cardiovascular nursing. 2017;32(5):E1-e13. doi:10.1097/jcn.0000000000000397.
66. Fairchild KD, Schelonka RL, Kaufman DA, Carlo WA, Kattwinkel J, Porcelli PJ et al. Septicemia mortality reduction in neonates in a heart rate characteristics monitoring trial. Pediatric research. 2013;74(5):570-5. doi:10.1038/pr.2013.136.
2. Buchhorn R, Baumann C, Willaschek C. Alleviation of arrhythmia burden in children with frequent idiopathic premature ventricular contractions by omega-3-fatty acid supplementation. International journal of cardiology. 2019;291:52-6. doi:10.1016/j.ijcard.2019.05.054.
3. Buchhorn R, Baumann C, Gündogdu S, Rakowski U, Willaschek C. Diagnosis and management of an inappropriate sinus tachycardia in adolescence based upon a Holter ECG: A retrospective analysis of 479 patients. PloS one. 2020;15(8):e0238139.
4. Buchhorn R, Hammersen A, Bartmus D, Bursch J. The pathogenesis of heart failure in infants with congenital heart disease. Cardiol Young. 2001;11(5):498-504.
5. Buchhorn R. Why are psychiatric disorders in children becoming more and more common? Int J Emerg Ment Health. 2014;16(2):322-5.
6. Buchhorn R, Meint S, Willaschek C. The Impact of Early Life Stress on Growth and Cardiovascular Risk: A Possible Example for Autonomic Imprinting? PLoS ONE. 2016;11(11):e0166447.
7. Thayer JF, Lane RD. The role of vagal function in the risk for cardiovascular disease and mortality. Biol Psychol. 2007;74(2):224-42.
8. Porges SW. The Polyvagal Theory: phylogenetic contributions to social behavior. Physiol Behav. 2003;79(3):503-13.
9. Tyborowska A, Volman I, Niermann HCM, Pouwels JL, Smeekens S, Cillessen AHN et al. Early-life and pubertal stress differentially modulate grey matter development in human adolescents. Scientific reports. 2018;8(1):9201. doi:10.1038/s41598-018-27439-5.
10. Saboory E, Ghasemi M, Mehranfard N. Norepinephrine, neurodevelopment and behavior. Neurochemistry international. 2020;135:104706. doi:10.1016/j.neuint.2020.104706.
11. Thayer JF, Ahs F, Fredrikson M, Sollers JJ, III, Wager TD. A meta-analysis of heart rate variability and neuroimaging studies: implications for heart rate variability as a marker of stress and health. Neurosci Biobehav Rev. 2012;36(2):747-56.
12. Kirschen MP, Francoeur C, Murphy M, Traynor D, Zhang B, Mensinger JL et al. Epidemiology of Brain Death in Pediatric Intensive Care Units in the United States. JAMA pediatrics. 2019;173(5):469-76. doi:10.1001/jamapediatrics.2019.0249.
13. Piantino JA, Lin A, Crowder D, Williams CN, Perez-Alday E, Tereshchenko LG et al. Early Heart Rate Variability and Electroencephalographic Abnormalities in Acutely Brain-Injured Children Who Progress to Brain Death. Pediatric critical care medicine : a journal of the Society of Critical Care Medicine and the World Federation of Pediatric Intensive and Critical Care Societies. 2019;20(1):38-46. doi:10.1097/pcc.0000000000001759.
14. Oliveira V, Martins R, Liow N, Teiserskas J, von Rosenberg W, Adjei T et al. Prognostic Accuracy of Heart Rate Variability Analysis in Neonatal Encephalopathy: A Systematic Review. Neonatology. 2019;115(1):59-67. doi:10.1159/000493002.
15. Martin JA, Hamilton BE, Osterman MJK. Births in the United States, 2017. NCHS data brief. 2018(318):1-8.
16. Luu TM, Rehman Mian MO, Nuyt AM. Long-Term Impact of Preterm Birth: Neurodevelopmental and Physical Health Outcomes. Clinics in perinatology. 2017;44(2):305-14. doi:10.1016/j.clp.2017.01.003.
17. Clements KM, Barfield WD, Ayadi MF, Wilber N. Preterm birth-associated cost of early intervention services: an analysis by gestational age. Pediatrics. 2007;119(4):e866-74. doi:10.1542/peds.2006-1729.
18. Schieve LA, Tian LH, Rankin K, Kogan MD, Yeargin-Allsopp M, Visser S et al. Population impact of preterm birth and low birth weight on developmental disabilities in US children. Annals of epidemiology. 2016;26(4):267-74. doi:10.1016/j.annepidem.2016.02.012.
19. Plomgaard AM, Alderliesten T, van Bel F, Benders M, Claris O, Cordeiro M et al. No neurodevelopmental benefit of cerebral oximetry in the first randomised trial (SafeBoosC II) in preterm infants during the first days of life. Acta Paediatr. 2019;108(2):275-81. doi:10.1111/apa.14463.
20. Nist MD, Harrison TM, Steward DK. The biological embedding of neonatal stress exposure: A conceptual model describing the mechanisms of stress-induced neurodevelopmental impairment in preterm infants. Research in nursing & health. 2019;42(1):61-71. doi:10.1002/nur.21923.
21. Evans DJ, MacGregor RJ, Dean HG, Levene MI. Neonatal catecholamine levels and neurodevelopmental outcome: a cohort study. Archives of disease in childhood Fetal and neonatal edition. 2001;84(1):F49-52. doi:10.1136/fn.84.1.f49.
22. Yam KY, Schipper L, Reemst K, Ruigrok SR, Abbink MR, Hoeijmakers L et al. Increasing availability of omega-3 fatty acid in the early-life diet prevents the early-life stress-induced cognitive impairments without affecting metabolic alterations. Faseb j. 2019:fj201802297R. doi:10.1096/fj.201802297R.
23. Jafri SK, Ehsan L, Abbas Q, Ali F, Chand P, Ul Haque A. Frequency and Outcome of Acute Neurologic Complications after Congenital Heart Disease Surgery. Journal of pediatric neurosciences. 2017;12(4):328-31. doi:10.4103/jpn.JPN_87_17.
24. Tsao PC, Lee YS, Jeng MJ, Hsu JW, Huang KL, Tsai SJ et al. Additive effect of congenital heart disease and early developmental disorders on attention-deficit/hyperactivity disorder and autism spectrum disorder: a nationwide population-based longitudinal study. European child & adolescent psychiatry. 2017;26(11):1351-9. doi:10.1007/s00787-017-0989-8.
25. Longin E, Schaible T, Lenz T, Konig S. Short term heart rate variability in healthy neonates: normative data and physiological observations. Early Hum Dev. 2005;81(8):663-71.
26. Gruber EM, Laussen PC, Casta A, Zimmerman AA, Zurakowski D, Reid R et al. Stress response in infants undergoing cardiac surgery: a randomized study of fentanyl bolus, fentanyl infusion, and fentanyl-midazolam infusion. Anesthesia and analgesia. 2001;92(4):882-90.
27. Dimitrijevic L, Bjelakovic B, Colovic H, Mikov A, Zivkovic V, Kocic M et al. Assessment of general movements and heart rate variability in prediction of neurodevelopmental outcome in preterm infants. Early human development. 2016;99:7-12. doi:10.1016/j.earlhumdev.2016.05.014.
28. Goulding RM, Stevenson NJ, Murray DM, Livingstone V, Filan PM, Boylan GB. Heart rate variability in hypoxic ischemic encephalopathy: correlation with EEG grade and 2-y neurodevelopmental outcome. Pediatr Res. 2015;77(5):681-7.
29. von Rhein M, Buchmann A, Hagmann C, Huber R, Klaver P, Knirsch W et al. Brain volumes predict neurodevelopment in adolescents after surgery for congenital heart disease. Brain : a journal of neurology. 2014;137(Pt 1):268-76. doi:10.1093/brain/awt322.
30. Miller SP, McQuillen PS, Hamrick S, Xu D, Glidden DV, Charlton N et al. Abnormal brain development in newborns with congenital heart disease. The New England journal of medicine. 2007;357(19):1928-38. doi:10.1056/NEJMoa067393.
31. Schiller RM, H IJ, Madderom MJ, Rietman AB, Smits M, van Heijst AFJ et al. Neurobiologic Correlates of Attention and Memory Deficits Following Critical Illness in Early Life. Crit Care Med. 2017;45(10):1742-50. doi:10.1097/ccm.0000000000002553.
32. Natalucci G, Bucher HU, Von Rhein M, Borradori Tolsa C, Latal B, Adams M. Population based report on health related quality of life in adolescents born very preterm. Early human development. 2017;104:7-12. doi:10.1016/j.earlhumdev.2016.11.002.
33. Botellero VL, Skranes J, Bjuland KJ, Haberg AK, Lydersen S, Brubakk AM et al. A longitudinal study of associations between psychiatric symptoms and disorders and cerebral gray matter volumes in adolescents born very preterm. BMC pediatrics. 2017;17(1):45. doi:10.1186/s12887-017-0793-0.
34. Kumar R, Yadav SK, Palomares JA, Park B, Joshi SH, Ogren JA et al. Reduced regional brain cortical thickness in patients with heart failure. PloS one. 2015;10(5):e0126595. doi:10.1371/journal.pone.0126595.
35. Woo MA, Kumar R, Macey PM, Fonarow GC, Harper RM. Brain injury in autonomic, emotional, and cognitive regulatory areas in patients with heart failure. Journal of cardiac failure. 2009;15(3):214-23. doi:10.1016/j.cardfail.2008.10.020.
36. Rosch KS, Crocetti D, Hirabayashi K, Denckla MB, Mostofsky SH, Mahone EM. Reduced subcortical volumes among preschool-age girls and boys with ADHD. Psychiatry research Neuroimaging. 2018;271:67-74. doi:10.1016/j.pscychresns.2017.10.013.
37. Suffren S, Angulo D, Ding Y, Reyes P, Marin J, Hernandez JT et al. Long-term attention deficits combined with subcortical and cortical structural central nervous system alterations in young adults born small for gestational age. Early human development. 2017;110:44-9. doi:10.1016/j.earlhumdev.2017.04.016.
38. Wei L, Chen H, Wu GR. Heart rate variability associated with grey matter volumes in striatal and limbic structures of the central autonomic network. Brain research. 2018;1681:14-20. doi:10.1016/j.brainres.2017.12.024.
39. Willaschek C, Meint S, Rager K, Buchhorn R. Modified Clonidine Testing for Growth Hormone Stimulation Reveals alpha2-Adrenoreceptor Sub Sensitivity in Children with Idiopathic Growth Hormone Deficiency. PLoS ONE. 2015;10(9):e0137643.
40. Wulsin LR, Horn PS, Perry JL, Massaro JM, D'Agostino RB. Autonomic Imbalance as a Predictor of Metabolic Risks, Cardiovascular Disease, Diabetes, and Mortality. J Clin Endocrinol Metab. 2015;100(6):2443-8.
41. Manhardt LB, Norozi K, Muller C, Willaschek C, Kostuch B, Buchhorn R. NT-Pro-B-Type Natriuretic Peptide Levels in Infants with Failure to Thrive due to Caloric Deprivation. Int J Pediatr. 2010;2010:983468.
42. Paul MA, Backer CL, Binns HJ, Mavroudis C, Webb CL, Yogev R et al. B-Type Natriuretic Peptide and Heart Failure in Patients with Ventricular Septal Defect: A Pilot Study. Pediatr Cardiol. 2009.
43. Fujioka K, Mizobuchi M, Sakai H, Iwatani S, Wada K, Yoshimoto S et al. N-terminal pro-brain natriuretic peptide levels in monochorionic diamniotic twins with selective intrauterine growth restriction. J Perinatol. 2014;34(1):6-10.
44. Waterland RA, Garza C. Potential mechanisms of metabolic imprinting that lead to chronic disease. Am J Clin Nutr. 1999;69(2):179-97.
45. Barker DJ, Winter PD, Osmond C, Margetts B, Simmonds SJ. Weight in infancy and death from ischaemic heart disease. Lancet. 1989;2(8663):577-80.
46. Martorell R, Horta BL, Adair LS, Stein AD, Richter L, Fall CH et al. Weight gain in the first two years of life is an important predictor of schooling outcomes in pooled analyses from five birth cohorts from low- and middle-income countries. J Nutr. 2010;140(2):348-54.
47. Wood AR, Esko T, Yang J, Vedantam S, Pers TH, Gustafsson S et al. Defining the role of common variation in the genomic and biological architecture of adult human height. Nat Genet. 2014;46(11):1173-86.
48. Simeone P, Alberti S. Epigenetic heredity of human height. Physiol Rep. 2014;2(6).
49. Sandberg DE, Voss LD. The psychosocial consequences of short stature: a review of the evidence. Best Pract Res Clin Endocrinol Metab. 2002;16(3):449-63.
50. Buchhorn R, Willaschek C. Growth Hormone Treatment, Cardiovascular Risk and Autonomic Maturation in Children and Adolescents with Growth Hormone Deficiency or Born Small for Gestational Age. Open Journal of Pediatrics. 2020;10:12-29.
51. Buchhorn R, Conzelmann A, Willaschek C, Stork D, Taurines R, Renner TJ. Heart rate variability and methylphenidate in children with ADHD. Atten Defic Hyperact Disord. 2012;4(2):85-91.
52. Myers KA, Bello-Espinosa LE, Symonds JD, Zuberi SM, Clegg R, Sadleir LG et al. Heart rate variability in epilepsy: A potential biomarker of sudden unexpected death in epilepsy risk. Epilepsia. 2018;59(7):1372-80. doi:10.1111/epi.14438.
53. Mueller SG, Nei M, Bateman LM, Knowlton R, Laxer KD, Friedman D et al. Brainstem network disruption: A pathway to sudden unexplained death in epilepsy? Human brain mapping. 2018;39(12):4820-30. doi:10.1002/hbm.24325.
54. Buchhorn R, Hulpke-Wette M, Hilgers R, Bartmus D, Wessel A, Bursch J. Propranolol treatment of congestive heart failure in infants with congenital heart disease: The CHF-PRO-INFANT Trial. Congestive heart failure in infants treated with propanol. Int J Cardiol. 2001;79(2-3):167-73.
55. Buchhorn R, Christian W. Ventricular arrhythmias in children with attention deficit disorder - a symptom of autonomic imbalance? Cardiol Young. 2013:1-6.
56. Cohen BE, Edmondson D, Kronish IM. State of the Art Review: Depression, Stress, Anxiety, and Cardiovascular Disease. Am J Hypertens. 2015;28(11):1295-302.
57. Koenig J, Rash JA, Kemp AH, Buchhorn R, Thayer JF, Kaess M. Resting state vagal tone in attention deficit (hyperactivity) disorder: A meta-analysis. World J Biol Psychiatry. 2016:1-15.
58. Habel LA, Cooper WO, Sox CM, Chan KA, Fireman BH, Arbogast PG et al. ADHD medications and risk of serious cardiovascular events in young and middle-aged adults. JAMA. 2011;306(24):2673-83.
59. Cooper WO, Habel LA, Sox CM, Chan KA, Arbogast PG, Cheetham TC et al. ADHD drugs and serious cardiovascular events in children and young adults. N Engl J Med. 2011;365(20):1896-904.
60. Conradt E, Flannery T, Aschner JL, Annett RD, Croen LA, Duarte CS et al. Prenatal Opioid Exposure: Neurodevelopmental Consequences and Future Research Priorities. Pediatrics. 2019;144(3). doi:10.1542/peds.2019-0128.
61. Nederend I, Jongbloed MRM, de Geus EJC, Blom NA, Ten Harkel ADJ. Postnatal Cardiac Autonomic Nervous Control in Pediatric Congenital Heart Disease. Journal of cardiovascular development and disease. 2016;3(2). doi:10.3390/jcdd3020016.
62. Ohuchi H, Takasugi H, Ohashi H, Yamada O, Watanabe K, Yagihara T et al. Abnormalities of neurohormonal and cardiac autonomic nervous activities relate poorly to functional status in fontan patients. Circulation. 2004;110(17):2601-8.
63. Siddiqui S, Fifer WP, Ordonez-Retamar M, Nugent JD, Williams IA. An antenatal marker of neurodevelopmental outcomes in infants with congenital heart disease. Journal of perinatology : official journal of the California Perinatal Association. 2017;37(8):953-7. doi:10.1038/jp.2017.59.
64. Haraldsdottir K, Watson AM, Goss KN, Beshish AG, Pegelow DF, Palta M et al. Impaired autonomic function in adolescents born preterm. Physiol Rep. 2018;6(6):e13620. doi:10.14814/phy2.13620.
65. Harrison TM, Brown R. Autonomic Nervous System Function After a Skin-to-Skin Contact Intervention in Infants With Congenital Heart Disease. The Journal of cardiovascular nursing. 2017;32(5):E1-e13. doi:10.1097/jcn.0000000000000397.
66. Fairchild KD, Schelonka RL, Kaufman DA, Carlo WA, Kattwinkel J, Porcelli PJ et al. Septicemia mortality reduction in neonates in a heart rate characteristics monitoring trial. Pediatric research. 2013;74(5):570-5. doi:10.1038/pr.2013.136.