Maturation of the Cardiac Autonomic Nervous System Activity in Children and Adolescents

Lisette M. Harteveld; Ineke Nederend; Arend D. J. Ten Harkel; Nienke M. Schutte; Susanne R. De Rooij; Tanja G. M. Vrijkotte; Helena Oldenhof; Arne Popma; Lucres M. C. Jansen; Jill Suurland; Hanna Swaab; Eco J. C. De Geus; Martin Prätzlich; Katharina Ackermann; Rosalind Baker; Molly Batchelor; Sarah Baumann; Anka Bernhard; Roberta Clanton; Dimitris Dikeos; Roberta Dochnal; Lynn Valérie Fehlbaum; Aranzazu Fernández‐rivas; Karen Gonzalez; Maider González De Artaza‐lavesa; Silvina Guijarro; Malou Gundlach; Beate Herpertz‐dahlmann; Amaia Hervas; Linda Kersten; Gregor Kohls; Angeliki Konsta; Helen Lazaratou; Iñaki Kerexeta‐lizeaga; Anne Martinelli; Tisse Van Nimwegen; Ignazio Puzzo; Nora Maria Raschle; Jack Rogers; Réka Siklósi; Areti Smaragdi; Martin Steppan; Stephane De Brito; Graeme Fairchild; Meinhard Kieser; Kerstin Konrad; Christine Freitag; Christina Stadler

doi:10.1161/JAHA.120.017405

Maturation of the Cardiac Autonomic Nervous System Activity in Children and Adolescents

Lisette M. Harteveld
, Ineke Nederend
, Arend D. J. Ten Harkel
, Nienke M. Schutte
, Susanne R. De Rooij
, Tanja G. M. Vrijkotte
, Helena Oldenhof
, Arne Popma
, Lucres M. C. Jansen
, Jill Suurland
, Hanna Swaab
, Eco J. C. De Geus
, Martin Prätzlich
, Katharina Ackermann
, Rosalind Baker
, Molly Batchelor
, Sarah Baumann
, Anka Bernhard
, Roberta Clanton
, Dimitris Dikeos

Roberta Dochnal, Lynn Valérie Fehlbaum, Aranzazu Fernández‐rivas, Karen Gonzalez, Maider González De Artaza‐lavesa, Silvina Guijarro, Malou Gundlach, Beate Herpertz‐dahlmann, Amaia Hervas, Linda Kersten, Gregor Kohls, Angeliki Konsta, Helen Lazaratou, Iñaki Kerexeta‐lizeaga, Anne Martinelli, Tisse Van Nimwegen, Ignazio Puzzo, Nora Maria Raschle, Jack Rogers, Réka Siklósi, Areti Smaragdi, Martin Steppan, Stephane De Brito, Graeme Fairchild, Meinhard Kieser, Kerstin Konrad, Christine Freitag, Christina Stadler

Research output: Contribution to Journal › Article › Academic › peer-review

Abstract

Background
Despite the increasing interest in cardiac autonomic nervous activity, the normal development is not fully understood. The main aim was to determine the maturation of different cardiac sympathetic‐(SNS) and parasympathetic nervous system (PNS) activity parameters in healthy patients aged 0.5 to 20 years. A second aim was to determine potential sex differences.

Methods and Results
Five studies covering the 0.5‐ to 20‐year age range provided impedance‐ and electrocardiography recordings from which heart rate, different PNS‐parameters (eg, respiratory sinus arrhythmia) and an SNS‐parameter (pre‐ejection period) were collected. Age trends were computed in the mean values across 12 age‐bins and in the age‐specific variances. Age was associated with changes in mean and variance of all parameters. PNS‐activity followed a cubic trend, with an exponential increase from infancy, a plateau phase during middle childhood, followed by a decrease to adolescence. SNS‐activity showed a more linear trend, with a gradual decrease from infancy to adolescence. Boys had higher SNS‐activity at ages 11 to 15 years, while PNS‐activity was higher at 5 and 11 to 12 years with the plateau level reached earlier in girls. Interindividual variation was high at all ages. Variance was reasonably stable for SNS‐ and the log‐transformed PNS‐parameters.

Conclusions
Cardiac PNS‐ and SNS‐activity in childhood follows different maturational trajectories. Whereas PNS‐activity shows a cubic trend with a plateau phase during middle childhood, SNS‐activity shows a linear decrease from 0.5 to 20 years. Despite the large samples used, clinical use of the sex‐specific centile and percentile normative values is modest in view of the large individual differences, even within narrow age bands.

Original language	English
Article number	e017405
Pages (from-to)	1-22
Number of pages	22
Journal	Journal of the American Heart Association
Volume	10
Issue number	4
Early online date	2 Feb 2021
DOIs	https://doi.org/10.1161/JAHA.120.017405
Publication status	Published - 16 Feb 2021

Funding

The NTR study was supported by the National Institute of Diabetes and Digestive and Kidney Diseases under grant number RO1DK092127 and the Netherlands Organization for Scientific Research under grant number 022.003.010. The study from Nederend et al. was funded by the VU University Ambulatory Monitoring System fund. MINDS-Leiden was funded by grant number 056-23-001 from the National Initiative for Brain and Cognition Research supported and coordinated by the Netherlands Organization for Scientific Research (NWO). The FemNAT-CD consortium (coordinated by Christine M. Freitag) collaborative project is funded by the European Commission under the 7th Framework Health Program with Grant Agreement no. 602407. The ABCD study was supported by the Netherlands Organization for Health Research and Development (ZonMw) and the Dutch Heart Foundation. The NTR study thanks the members of the twin families registered with The Netherlands Twin Register for continued support of scientific research. The MINDS-Leiden study thanks all families for their participation and the research assistants who contributed to the data collection. The ABCD study thanks the participating mothers and their children, and all other persons and institutions who contributed to the ABCD study: obstetric care providers, primary schools, students, and youth healthcare centers in Amsterdam, The Netherlands. Sources of Funding The NTR study was supported by the National Institute of Diabetes and Digestive and Kidney Diseases under grant number RO1DK092127 and the Netherlands Organization for Scientific Research under grant number 022.003.010. The study from Nederend et al. was funded by the VU University Ambulatory Monitoring System fund. MINDS-Leiden was funded by grant number 056-23-001 from the National Initiative for Brain and Cognition Research supported and coordinated by the Netherlands Organization for Scientific Research (NWO). The FemNAT-CD consortium (coordinated by Christine M. Freitag) collaborative project is funded by the European Commission under the 7th Framework Health Program with Grant Agreement no. 602407. The ABCD study was supported by the Netherlands Organization for Health Research and Development (ZonMw) and the Dutch Heart Foundation.

Funders	Funder number
Dutch Heart Foundation
7th Framework Health Program
youth healthcare centers in Amsterdam
ZonMw
Netherlands Organization for Health Research and Development
European Commission	602407
Vrije Universiteit Amsterdam	056-23-001
Netherlands Organization for Scientific Research	022.003.010
National Institute of Diabetes and Digestive and Kidney Diseases	R01DK092127

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Harteveld, L. M., Nederend, I., Ten Harkel, A. D. J., Schutte, N. M., De Rooij, S. R., Vrijkotte, T. G. M., Oldenhof, H., Popma, A., Jansen, L. M. C., Suurland, J., Swaab, H., De Geus, E. J. C., Prätzlich, M., Ackermann, K., Baker, R., Batchelor, M., Baumann, S., Bernhard, A., Clanton, R., ... Stadler, C. (2021). Maturation of the Cardiac Autonomic Nervous System Activity in Children and Adolescents. Journal of the American Heart Association, 10(4), 1-22. Article e017405. https://doi.org/10.1161/JAHA.120.017405

@article{20fc9bd0f6b043798a24c74cb2b993de,

title = "Maturation of the Cardiac Autonomic Nervous System Activity in Children and Adolescents",

abstract = "Background Despite the increasing interest in cardiac autonomic nervous activity, the normal development is not fully understood. The main aim was to determine the maturation of different cardiac sympathetic‐(SNS) and parasympathetic nervous system (PNS) activity parameters in healthy patients aged 0.5 to 20 years. A second aim was to determine potential sex differences. Methods and Results Five studies covering the 0.5‐ to 20‐year age range provided impedance‐ and electrocardiography recordings from which heart rate, different PNS‐parameters (eg, respiratory sinus arrhythmia) and an SNS‐parameter (pre‐ejection period) were collected. Age trends were computed in the mean values across 12 age‐bins and in the age‐specific variances. Age was associated with changes in mean and variance of all parameters. PNS‐activity followed a cubic trend, with an exponential increase from infancy, a plateau phase during middle childhood, followed by a decrease to adolescence. SNS‐activity showed a more linear trend, with a gradual decrease from infancy to adolescence. Boys had higher SNS‐activity at ages 11 to 15 years, while PNS‐activity was higher at 5 and 11 to 12 years with the plateau level reached earlier in girls. Interindividual variation was high at all ages. Variance was reasonably stable for SNS‐ and the log‐transformed PNS‐parameters. Conclusions Cardiac PNS‐ and SNS‐activity in childhood follows different maturational trajectories. Whereas PNS‐activity shows a cubic trend with a plateau phase during middle childhood, SNS‐activity shows a linear decrease from 0.5 to 20 years. Despite the large samples used, clinical use of the sex‐specific centile and percentile normative values is modest in view of the large individual differences, even within narrow age bands.",

author = "Harteveld, \{Lisette M.\} and Ineke Nederend and \{Ten Harkel\}, \{Arend D. J.\} and Schutte, \{Nienke M.\} and \{De Rooij\}, \{Susanne R.\} and Vrijkotte, \{Tanja G. M.\} and Helena Oldenhof and Arne Popma and Jansen, \{Lucres M. C.\} and Jill Suurland and Hanna Swaab and \{De Geus\}, \{Eco J. C.\} and Martin Pr{\"a}tzlich and Katharina Ackermann and Rosalind Baker and Molly Batchelor and Sarah Baumann and Anka Bernhard and Roberta Clanton and Dimitris Dikeos and Roberta Dochnal and Fehlbaum, \{Lynn Val{\'e}rie\} and Aranzazu Fern{\'a}ndez‐rivas and Karen Gonzalez and \{Gonz{\'a}lez De Artaza‐lavesa\}, Maider and Silvina Guijarro and Malou Gundlach and Beate Herpertz‐dahlmann and Amaia Hervas and Linda Kersten and Gregor Kohls and Angeliki Konsta and Helen Lazaratou and I{\~n}aki Kerexeta‐lizeaga and Anne Martinelli and \{Van Nimwegen\}, Tisse and Ignazio Puzzo and Raschle, \{Nora Maria\} and Jack Rogers and R{\'e}ka Sikl{\'o}si and Areti Smaragdi and Martin Steppan and \{De Brito\}, Stephane and Graeme Fairchild and Meinhard Kieser and Kerstin Konrad and Christine Freitag and Christina Stadler",

year = "2021",

month = feb,

day = "16",

doi = "10.1161/JAHA.120.017405",

language = "English",

volume = "10",

pages = "1--22",

journal = "Journal of the American Heart Association",

issn = "2047-9980",

publisher = "John Wiley \& Sons",

number = "4",

}

Harteveld, LM, Nederend, I, Ten Harkel, ADJ, Schutte, NM, De Rooij, SR, Vrijkotte, TGM, Oldenhof, H, Popma, A, Jansen, LMC, Suurland, J, Swaab, H, De Geus, EJC, Prätzlich, M, Ackermann, K, Baker, R, Batchelor, M, Baumann, S, Bernhard, A, Clanton, R, Dikeos, D, Dochnal, R, Fehlbaum, LV, Fernández‐rivas, A, Gonzalez, K, González De Artaza‐lavesa, M, Guijarro, S, Gundlach, M, Herpertz‐dahlmann, B, Hervas, A, Kersten, L, Kohls, G, Konsta, A, Lazaratou, H, Kerexeta‐lizeaga, I, Martinelli, A, Van Nimwegen, T, Puzzo, I, Raschle, NM, Rogers, J, Siklósi, R, Smaragdi, A, Steppan, M, De Brito, S, Fairchild, G, Kieser, M, Konrad, K, Freitag, C & Stadler, C 2021, 'Maturation of the Cardiac Autonomic Nervous System Activity in Children and Adolescents', Journal of the American Heart Association, vol. 10, no. 4, e017405, pp. 1-22. https://doi.org/10.1161/JAHA.120.017405

TY - JOUR

T1 - Maturation of the Cardiac Autonomic Nervous System Activity in Children and Adolescents

AU - Harteveld, Lisette M.

AU - Nederend, Ineke

AU - Ten Harkel, Arend D. J.

AU - Schutte, Nienke M.

AU - De Rooij, Susanne R.

AU - Vrijkotte, Tanja G. M.

AU - Oldenhof, Helena

AU - Popma, Arne

AU - Jansen, Lucres M. C.

AU - Suurland, Jill

AU - Swaab, Hanna

AU - De Geus, Eco J. C.

AU - Prätzlich, Martin

AU - Ackermann, Katharina

AU - Baker, Rosalind

AU - Batchelor, Molly

AU - Baumann, Sarah

AU - Bernhard, Anka

AU - Clanton, Roberta

AU - Dikeos, Dimitris

AU - Dochnal, Roberta

AU - Fehlbaum, Lynn Valérie

AU - Fernández‐rivas, Aranzazu

AU - Gonzalez, Karen

AU - González De Artaza‐lavesa, Maider

AU - Guijarro, Silvina

AU - Gundlach, Malou

AU - Herpertz‐dahlmann, Beate

AU - Hervas, Amaia

AU - Kersten, Linda

AU - Kohls, Gregor

AU - Konsta, Angeliki

AU - Lazaratou, Helen

AU - Kerexeta‐lizeaga, Iñaki

AU - Martinelli, Anne

AU - Van Nimwegen, Tisse

AU - Puzzo, Ignazio

AU - Raschle, Nora Maria

AU - Rogers, Jack

AU - Siklósi, Réka

AU - Smaragdi, Areti

AU - Steppan, Martin

AU - De Brito, Stephane

AU - Fairchild, Graeme

AU - Kieser, Meinhard

AU - Konrad, Kerstin

AU - Freitag, Christine

AU - Stadler, Christina

PY - 2021/2/16

Y1 - 2021/2/16

N2 - Background Despite the increasing interest in cardiac autonomic nervous activity, the normal development is not fully understood. The main aim was to determine the maturation of different cardiac sympathetic‐(SNS) and parasympathetic nervous system (PNS) activity parameters in healthy patients aged 0.5 to 20 years. A second aim was to determine potential sex differences. Methods and Results Five studies covering the 0.5‐ to 20‐year age range provided impedance‐ and electrocardiography recordings from which heart rate, different PNS‐parameters (eg, respiratory sinus arrhythmia) and an SNS‐parameter (pre‐ejection period) were collected. Age trends were computed in the mean values across 12 age‐bins and in the age‐specific variances. Age was associated with changes in mean and variance of all parameters. PNS‐activity followed a cubic trend, with an exponential increase from infancy, a plateau phase during middle childhood, followed by a decrease to adolescence. SNS‐activity showed a more linear trend, with a gradual decrease from infancy to adolescence. Boys had higher SNS‐activity at ages 11 to 15 years, while PNS‐activity was higher at 5 and 11 to 12 years with the plateau level reached earlier in girls. Interindividual variation was high at all ages. Variance was reasonably stable for SNS‐ and the log‐transformed PNS‐parameters. Conclusions Cardiac PNS‐ and SNS‐activity in childhood follows different maturational trajectories. Whereas PNS‐activity shows a cubic trend with a plateau phase during middle childhood, SNS‐activity shows a linear decrease from 0.5 to 20 years. Despite the large samples used, clinical use of the sex‐specific centile and percentile normative values is modest in view of the large individual differences, even within narrow age bands.

AB - Background Despite the increasing interest in cardiac autonomic nervous activity, the normal development is not fully understood. The main aim was to determine the maturation of different cardiac sympathetic‐(SNS) and parasympathetic nervous system (PNS) activity parameters in healthy patients aged 0.5 to 20 years. A second aim was to determine potential sex differences. Methods and Results Five studies covering the 0.5‐ to 20‐year age range provided impedance‐ and electrocardiography recordings from which heart rate, different PNS‐parameters (eg, respiratory sinus arrhythmia) and an SNS‐parameter (pre‐ejection period) were collected. Age trends were computed in the mean values across 12 age‐bins and in the age‐specific variances. Age was associated with changes in mean and variance of all parameters. PNS‐activity followed a cubic trend, with an exponential increase from infancy, a plateau phase during middle childhood, followed by a decrease to adolescence. SNS‐activity showed a more linear trend, with a gradual decrease from infancy to adolescence. Boys had higher SNS‐activity at ages 11 to 15 years, while PNS‐activity was higher at 5 and 11 to 12 years with the plateau level reached earlier in girls. Interindividual variation was high at all ages. Variance was reasonably stable for SNS‐ and the log‐transformed PNS‐parameters. Conclusions Cardiac PNS‐ and SNS‐activity in childhood follows different maturational trajectories. Whereas PNS‐activity shows a cubic trend with a plateau phase during middle childhood, SNS‐activity shows a linear decrease from 0.5 to 20 years. Despite the large samples used, clinical use of the sex‐specific centile and percentile normative values is modest in view of the large individual differences, even within narrow age bands.

U2 - 10.1161/JAHA.120.017405

DO - 10.1161/JAHA.120.017405

M3 - Article

SN - 2047-9980

VL - 10

SP - 1

EP - 22

JO - Journal of the American Heart Association

JF - Journal of the American Heart Association

IS - 4

M1 - e017405

ER -

Maturation of the Cardiac Autonomic Nervous System Activity in Children and Adolescents

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