Autonomic nervous system maturation in the premature extrauterine milieu.
Autonomic Nervous System
/ growth & development
Electrocardiography
Female
Gestational Age
Heart Rate
Humans
Infant, Extremely Premature
Infant, Newborn
Infant, Premature
/ physiology
Intensive Care Units, Neonatal
Intensive Care, Neonatal
Longitudinal Studies
Male
Pregnancy
Prospective Studies
Regression Analysis
Journal
Pediatric research
ISSN: 1530-0447
Titre abrégé: Pediatr Res
Pays: United States
ID NLM: 0100714
Informations de publication
Date de publication:
03 2021
03 2021
Historique:
received:
17
01
2020
accepted:
28
04
2020
revised:
08
04
2020
pubmed:
13
5
2020
medline:
15
1
2022
entrez:
13
5
2020
Statut:
ppublish
Résumé
In premature infants, we investigated whether the duration of extrauterine development influenced autonomic nervous system (ANS) maturation. We performed a longitudinal cohort study of ANS maturation in preterm infants. Eligibility included birth gestational age (GA) < 37 weeks, NICU admission, and expected survival. The cohort was divided into three birth GA groups: Group 1 (≤29 weeks), Group 2 (30-33 weeks), and Group 3 (≥34 weeks). ECG data were recorded weekly and analyzed for sympathetic and parasympathetic tone using heart rate variability (HRV). Quantile regression modeled the slope of ANS maturation among the groups by postnatal age to term-equivalent age (TEA) (≥37 weeks). One hundred infants, median (Q1-Q3) birth GA of 31.9 (28.7-33.9) weeks, were enrolled: Group 1 (n = 35); Group 2 (n = 40); and Group 3 (n = 25). Earlier birth GA was associated with lower sympathetic and parasympathetic tone. However, the rate of autonomic maturation was similar, and at TEA there was no difference in HRV metrics across the three groups. The majority of infants (91%) did not experience significant neonatal morbidities. Premature infants with low prematurity-related systemic morbidity have maturational trajectories of ANS development that are comparable across a wide range of ex-utero durations regardless of birth GA. Heart rate variability can evaluate the maturation of the autonomic nervous system. Metrics of both the sympathetic and parasympathetic nervous system show maturation in the premature extrauterine milieu. The autonomic nervous system in preterm infants shows comparable maturation across a wide range of birth gestational ages. Preterm newborns with low medical morbidity have maturation of their autonomic nervous system while in the NICU. Modern NICU advances appear to support autonomic development in the preterm infant.
Sections du résumé
BACKGROUND
In premature infants, we investigated whether the duration of extrauterine development influenced autonomic nervous system (ANS) maturation.
METHODS
We performed a longitudinal cohort study of ANS maturation in preterm infants. Eligibility included birth gestational age (GA) < 37 weeks, NICU admission, and expected survival. The cohort was divided into three birth GA groups: Group 1 (≤29 weeks), Group 2 (30-33 weeks), and Group 3 (≥34 weeks). ECG data were recorded weekly and analyzed for sympathetic and parasympathetic tone using heart rate variability (HRV). Quantile regression modeled the slope of ANS maturation among the groups by postnatal age to term-equivalent age (TEA) (≥37 weeks).
RESULTS
One hundred infants, median (Q1-Q3) birth GA of 31.9 (28.7-33.9) weeks, were enrolled: Group 1 (n = 35); Group 2 (n = 40); and Group 3 (n = 25). Earlier birth GA was associated with lower sympathetic and parasympathetic tone. However, the rate of autonomic maturation was similar, and at TEA there was no difference in HRV metrics across the three groups. The majority of infants (91%) did not experience significant neonatal morbidities.
CONCLUSION
Premature infants with low prematurity-related systemic morbidity have maturational trajectories of ANS development that are comparable across a wide range of ex-utero durations regardless of birth GA.
IMPACT
Heart rate variability can evaluate the maturation of the autonomic nervous system. Metrics of both the sympathetic and parasympathetic nervous system show maturation in the premature extrauterine milieu. The autonomic nervous system in preterm infants shows comparable maturation across a wide range of birth gestational ages. Preterm newborns with low medical morbidity have maturation of their autonomic nervous system while in the NICU. Modern NICU advances appear to support autonomic development in the preterm infant.
Identifiants
pubmed: 32396923
doi: 10.1038/s41390-020-0952-0
pii: 10.1038/s41390-020-0952-0
pmc: PMC8011288
mid: NIHMS1591340
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
863-868Subventions
Organisme : NCATS NIH HHS
ID : KL2 TR001877
Pays : United States
Organisme : NCATS NIH HHS
ID : UL1 TR001876
Pays : United States
Références
Mulkey, S. B. & Plessis, A. D. The critical role of the central autonomic nervous system in fetal-neonatal transition. Semin. Pediatr. Neurol. 28, 29–37 (2018).
doi: 10.1016/j.spen.2018.05.004
Longin, E., Gerstner, T., Schaible, T., Lenz, T. & Konig, S. Maturation of the autonomic nervous system: differences in heart rate variability in premature vs. term infants. J. Perinat. Med. 34, 303–308 (2006).
doi: 10.1515/JPM.2006.058
Fyfe, K. L. et al. The effect of gestational age at birth on post-term maturation of heart rate variability. Sleep 38, 1635–1644 (2015).
doi: 10.5665/sleep.5064
Task Force of the European Society of Cardiology the North American Society of Pacing Electrophysiology. Heart rate variability. Standards of measurement, physiological interpretation, and clinical use. Eur. Heart J. 93, 1043–1065 (1996).
Malliani, A., Lombardi, F. & Pagani, M. Power spectrum analysis of heart rate variability: a tool to explore neural regulatory mechanisms. Br. Heart J. 71, 1–2 (1994).
doi: 10.1136/hrt.71.1.1
Mulkey, S. B. et al. Autonomic nervous system depression at term in neurologically normal premature infants. Early Hum. Dev. 123, 11–16 (2018).
doi: 10.1016/j.earlhumdev.2018.07.003
Yiallourou, S. R., Witcombe, N. B., Sands, S. A., Walker, A. M. & Horne, R. S. The development of autonomic cardiovascular control is altered by preterm birth. Early Hum. Dev. 89, 145–152 (2013).
doi: 10.1016/j.earlhumdev.2012.09.009
Tuzcu, V., Nas, S., Ulusar, U., Ugur, A. & Kaiser, J. R. Altered heart rhythm dynamics in very low birth weight infants with impending intraventricular hemorrhage. Pediatrics 123, 810–815 (2009).
doi: 10.1542/peds.2008-0253
Massaro, A. N. et al. Heart rate variability in encephalopathic newborns during and after therapeutic hypothermia. J. Perinatol. 34, 836–841 (2014).
doi: 10.1038/jp.2014.108
Fairchild, K. D. & O’Shea, T. M. Heart rate characteristics: physiomarkers for detection of late-onset neonatal sepsis. Clin. Perinatol. 37, 581–598 (2010).
doi: 10.1016/j.clp.2010.06.002
Al-Shargabi, T. et al. Changes in autonomic tone in premature infants developing necrotizing enterocolitis. Am. J. Perinatol. 35, 1079–1086 (2018).
doi: 10.1055/s-0038-1639339
Nino, G. et al. Premature infants rehospitalized because of an apparent life-threatening event had distinctive autonomic developmental trajectories. Am. J. Respir. Crit. Care Med. 194, 379–381 (2016).
doi: 10.1164/rccm.201601-0150LE
Mulkey, S. B. & du Plessis, A. J. Autonomic nervous system development and its impact on neuropsychiatric outcome. Pediatr. Res. 85, 120–126 (2019).
doi: 10.1038/s41390-018-0155-0
Haraldsdottir, K. et al. Heart rate recovery after maximal exercise is impaired in healthy young adults born preterm. Eur. J. Appl. Physiol. 119, 857–866 (2019).
doi: 10.1007/s00421-019-04075-z
Patural, H. et al. Autonomic cardiac control of very preterm newborns: a prolonged dysfunction. Early Hum. Dev. 84, 681–687 (2008).
doi: 10.1016/j.earlhumdev.2008.04.010
Thiriez, G. et al. Altered autonomic control in preterm newborns with impaired neurological outcomes. Clin. Auton. Res. 25, 233–242 (2015).
doi: 10.1007/s10286-015-0298-6
de Bijl-Marcus, K., Brouwer, A. J., De Vries, L. S., Groenendaal, F. & Wezel-Meijler, G. V. Neonatal care bundles are associated with a reduction in the incidence of intraventricular haemorrhage in preterm infants: a multicentre cohort study. Arch. Dis. Child Fetal Neonatal Ed. (2019). https://doi.org/10.1136/archdischild-2018-316692 . [Epub ahead of print]
Ulusar, U. D. et al. Adaptive rule based fetal QRS complex detection using Hilbert transform. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2009, 4666–4669 (2009).
pmcid: 2954062
Fyfe, K. L., Yiallourou, S. R., Wong, F. Y. & Horne, R. S. The development of cardiovascular and cerebral vascular control in preterm infants. Sleep. Med. Rev. 18, 299–310 (2014).
doi: 10.1016/j.smrv.2013.06.002
Peng, C. K., Havlin, S., Stanley, H. E. & Goldberger, A. L. Quantification of scaling exponents and crossover phenomena in nonstationary heartbeat time series. Chaos 5, 82–87 (1995).
doi: 10.1063/1.166141
Govindan, R. B., Massaro, A. N., Niforatos, N. & du Plessis, A. Mitigating the effect of non-stationarity in spectral analysis-an application to neonate heart rate analysis. Comput. Biol. Med. 43, 2001–2006 (2013).
doi: 10.1016/j.compbiomed.2013.09.019
Govindan, R. B., Preissl, H., Eswaran, H., Campbell, J. Q. & Lowery, C. L. Detrended fluctuation analysis of short data sets: an application to fetal cardiac. Phys. D: Nonlinear Phenom. 226, 23–31 (2007).
doi: 10.1016/j.physd.2006.10.019
Patural, H. et al. Birth prematurity determines prolonged autonomic nervous system immaturity. Clin. Auton. Res. 14, 391–395 (2004).
doi: 10.1007/s10286-004-0216-9
Clairambault, J., Curzi-Dascalova, L., Kauffmann, F., Medigue, C. & Leffler, C. Heart rate variability in normal sleeping full-term and preterm neonates. Early Hum. Dev. 28, 169–183 (1992).
doi: 10.1016/0378-3782(92)90111-S
Tulppo, M. P. et al. Physiological background of the loss of fractal heart rate dynamics. Circulation 112, 314–319 (2005).
doi: 10.1161/CIRCULATIONAHA.104.523712
Bohanon, F. J. et al. Heart rate variability analysis is more sensitive at identifying neonatal sepsis than conventional vital signs. Am. J. Surg. 210, 661–667 (2015).
doi: 10.1016/j.amjsurg.2015.06.002
Goudjil, S. et al. Patent ductus arteriosus in preterm infants is associated with cardiac autonomic alteration and predominant parasympathetic stimulation. Early Hum. Dev. 89, 631–634 (2013).
doi: 10.1016/j.earlhumdev.2013.04.008
Sanders, M. R. & Hall, S. L. Trauma-informed care in the newborn intensive care unit: promoting safety, security and connectedness. J. Perinatol. 38, 3–10 (2018).
doi: 10.1038/jp.2017.124
Gomes, E. et al. Autonomic responses of premature newborns to body position and environmental noise in the neonatal intensive care unit. Rev. Bras. Ter. Intensiv. 31, 296–302 (2019).
Feldman, R., Rosenthal, Z. & Eidelman, A. I. Maternal-preterm skin-to-skin contact enhances child physiologic organization and cognitive control across the first 10 years of life. Biol. Psychiatry 75, 56–64 (2014).
doi: 10.1016/j.biopsych.2013.08.012
Tarvainen, M. P., Niskanen, J. P., Lipponen, J. A., Ranta-Aho, P. O. & Karjalainen, P. A. Kubios HRV-heart rate variability analysis software. Comput. Methods Prog. Biomed. 113, 210–220 (2014).
doi: 10.1016/j.cmpb.2013.07.024
Shayani, L. A., da Cruz, C. J., Porto, L. G. G. & Molina, G. E. Cardiac autonomic function in the first hours of postnatal life: an observational cross-sectional study in term neonates. Pediatr. Cardiol. 40, 1703–1708 (2019).
doi: 10.1007/s00246-019-02207-y
Mulkey, S. B. et al. The effect of labor and delivery mode on electrocortical and brainstem autonomic function during neonatal transition. Sci. Rep. 9, 11020 (2019).
doi: 10.1038/s41598-019-47306-1
Aye, C. Y. L. et al. Neonatal autonomic function after pregnancy complications and early cardiovascular development. Pediatr. Res. 84, 85–91 (2018).
doi: 10.1038/s41390-018-0021-0