Early Pain Exposure Influences Functional Brain Connectivity in Very Preterm Neonates.

brain connectivity fMRI functional connectivity neonatal neuroimaging nociceptive modulations pain preterm neonates resting state

Journal

Frontiers in neuroscience
ISSN: 1662-4548
Titre abrégé: Front Neurosci
Pays: Switzerland
ID NLM: 101478481

Informations de publication

Date de publication:
2019
Historique:
received: 14 04 2019
accepted: 12 08 2019
entrez: 12 9 2019
pubmed: 12 9 2019
medline: 12 9 2019
Statut: epublish

Résumé

Early exposure to nociceptive events may cause brain structural alterations in preterm neonates, with long-lasting consequences on neurodevelopmental outcome. Little is known on the extent to which early pain may affect brain connectivity. We aim to evaluate brain functional connectivity changes in preterm neonate that underwent multiple invasive procedures during the postnatal period, and to correlate them with the neurodevelopmental outcome at 24 months. In this prospective case-control study, we collected information about exposure to painful events during the early postnatal period and resting-state BOLD-fMRI data at term equivalent age from two groups of preterm neonate: 33 subjected to painful procedures during the neonatal intensive care (mean gestational age 27.9 ± 1.8 weeks) and 13 who did not require invasive procedures (average gestational age 31.2 ± 2.1 weeks). A data-driven principal-component-based multivariate pattern analysis (MVPA) was used to investigate the effect of early pain exposure on brain functional connectivity, and the relationship between connectivity changes and neurodevelopmental outcome at 24 months, assessed with Griffiths, Developmental Scale-Revised: 0-2. Early pain was associated with decreased functional connectivity between thalami and bilateral somatosensory cortex, and between the right insular cortex and ipsilateral amygdala and hippocampal regions, with a more evident effect in preterm neonate undergoing more invasive procedures. Functional connectivity of the right thalamocortical pathway was related to neuromotor outcome at 24 months ( Early exposure to pain is associated with abnormal functional connectivity of developing networks involved in the modulation of noxious stimuli in preterm neonate, contributing to the neurodevelopmental consequence of preterm birth.

Sections du résumé

BACKGROUND BACKGROUND
Early exposure to nociceptive events may cause brain structural alterations in preterm neonates, with long-lasting consequences on neurodevelopmental outcome. Little is known on the extent to which early pain may affect brain connectivity. We aim to evaluate brain functional connectivity changes in preterm neonate that underwent multiple invasive procedures during the postnatal period, and to correlate them with the neurodevelopmental outcome at 24 months.
METHODS METHODS
In this prospective case-control study, we collected information about exposure to painful events during the early postnatal period and resting-state BOLD-fMRI data at term equivalent age from two groups of preterm neonate: 33 subjected to painful procedures during the neonatal intensive care (mean gestational age 27.9 ± 1.8 weeks) and 13 who did not require invasive procedures (average gestational age 31.2 ± 2.1 weeks). A data-driven principal-component-based multivariate pattern analysis (MVPA) was used to investigate the effect of early pain exposure on brain functional connectivity, and the relationship between connectivity changes and neurodevelopmental outcome at 24 months, assessed with Griffiths, Developmental Scale-Revised: 0-2.
RESULTS RESULTS
Early pain was associated with decreased functional connectivity between thalami and bilateral somatosensory cortex, and between the right insular cortex and ipsilateral amygdala and hippocampal regions, with a more evident effect in preterm neonate undergoing more invasive procedures. Functional connectivity of the right thalamocortical pathway was related to neuromotor outcome at 24 months (
CONCLUSION CONCLUSIONS
Early exposure to pain is associated with abnormal functional connectivity of developing networks involved in the modulation of noxious stimuli in preterm neonate, contributing to the neurodevelopmental consequence of preterm birth.

Identifiants

pubmed: 31507370
doi: 10.3389/fnins.2019.00899
pmc: PMC6716476
doi:

Types de publication

Journal Article

Langues

eng

Pagination

899

Références

Arch Dis Child Fetal Neonatal Ed. 1999 Mar;80(2):F146-7
pubmed: 10325795
Exp Physiol. 2002 Mar;87(2):251-8
pubmed: 11856971
J Neuropathol Exp Neurol. 2003 May;62(5):441-50
pubmed: 12769184
Nat Rev Neurosci. 2005 Jul;6(7):507-20
pubmed: 15995722
Neuroimage. 2007 Aug 1;37(1):90-101
pubmed: 17560126
Eur J Pain. 2008 Oct;12(7):945-51
pubmed: 18308597
Expert Rev Neurother. 2008 Nov;8(11):1617-20
pubmed: 18986231
Pain. 2009 Jan;141(1-2):79-87
pubmed: 19026489
Pain. 2009 May;143(1-2):138-46
pubmed: 19307058
Pain. 2009 Dec 15;147(1-3):99-106
pubmed: 19781855
Neuroimage. 2010 Aug 15;52(2):409-14
pubmed: 20451627
Neuroimage. 2011 Feb 14;54(4):2750-63
pubmed: 20969966
Neuron. 1990 Dec;5(6):745-56
pubmed: 2148486
PLoS One. 2011 Apr 14;6(4):e18746
pubmed: 21533194
Ann Neurol. 2011 Oct;70(4):541-9
pubmed: 21976396
Ann Neurol. 2012 Mar;71(3):385-96
pubmed: 22374882
J Pain. 2012 Jun;13(6):590-7
pubmed: 22543043
Brain Connect. 2012;2(3):125-41
pubmed: 22642651
PLoS One. 2013 Oct 18;8(10):e76702
pubmed: 24204657
Neurology. 2013 Dec 10;81(24):2082-9
pubmed: 24212394
J Physiol. 2014 Apr 1;592(7):1535-44
pubmed: 24421353
Pediatr Res. 2014 May;75(5):584-7
pubmed: 24500615
Pediatrics. 2014 Mar;133(3):412-21
pubmed: 24534406
Psychoneuroendocrinology. 2015 Jan;51:151-63
pubmed: 25313535
Brain Struct Funct. 2016 Jan;221(1):487-506
pubmed: 25366970
AJNR Am J Neuroradiol. 2015 Mar;36(3):581-6
pubmed: 25376807
Surg Neurol Int. 2014 Nov 13;5(Suppl 13):S479-89
pubmed: 25506507
AJNR Am J Neuroradiol. 2015 Aug;36(8):1565-71
pubmed: 25929880
Can J Psychiatry. 2015 Apr;60(4):176-80
pubmed: 26174217
Neuroimage. 2016 Jan 1;124(Pt A):267-275
pubmed: 26341027
Brain Struct Funct. 2016 Jul;221(6):3211-22
pubmed: 26341628
Neuroradiol J. 2016 Apr;29(2):137-45
pubmed: 26915895
Eur J Paediatr Neurol. 2017 Jan;21(1):23-48
pubmed: 27567276
Dev Med Child Neurol. 2017 Apr;59(4):433-440
pubmed: 27976377
Neuroimage Clin. 2016 May 09;12:1004-1012
pubmed: 27995066
Arch Dis Child Fetal Neonatal Ed. 2017 Mar;102(2):F176-F182
pubmed: 28011793
Pain. 1989 Oct;39(1):31-6
pubmed: 2812853
Eur Radiol. 2018 Mar;28(3):1157-1166
pubmed: 28956133
Neuroscience. 2018 Sep 1;387:58-71
pubmed: 28978414
J Neurosci. 2018 Jan 24;38(4):878-886
pubmed: 29255007
J Magn Reson Imaging. 2018 Nov;48(5):1199-1207
pubmed: 29746715
Neuroimage Clin. 2019;21:101596
pubmed: 30458986
Front Pediatr. 2018 Nov 29;6:369
pubmed: 30555809
Front Psychol. 2019 Apr 02;10:715
pubmed: 31001173
Nature. 1995 May 25;375(6529):325-8
pubmed: 7753197
Pain. 1994 Mar;56(3):353-9
pubmed: 8022628
Cell. 1993 Jan;72 Suppl:77-98
pubmed: 8428376
J Neurosci. 1998 Aug 15;18(16):6241-53
pubmed: 9698317

Auteurs

Domenico Tortora (D)

Neuroradiology Unit, IRCCS Istituto Giannina Gaslini, Genoa, Italy.

Mariasavina Severino (M)

Neuroradiology Unit, IRCCS Istituto Giannina Gaslini, Genoa, Italy.

Carlo Di Biase (C)

Neonatal Intensive Care Unit, IRCCS Istituto Giannina Gaslini, Genoa, Italy.

Maryia Malova (M)

Neonatal Intensive Care Unit, IRCCS Istituto Giannina Gaslini, Genoa, Italy.

Alessandro Parodi (A)

Neonatal Intensive Care Unit, IRCCS Istituto Giannina Gaslini, Genoa, Italy.

Diego Minghetti (D)

Neonatal Intensive Care Unit, IRCCS Istituto Giannina Gaslini, Genoa, Italy.

Cristina Traggiai (C)

Neonatal Intensive Care Unit, IRCCS Istituto Giannina Gaslini, Genoa, Italy.

Sara Uccella (S)

Child Neuropsychiatry Unit, IRCCS Istituto Giannina Gaslini, Genoa, Italy.

Luca Boeri (L)

Child Neuropsychiatry Unit, IRCCS Istituto Giannina Gaslini, Genoa, Italy.

Giovanni Morana (G)

Neuroradiology Unit, IRCCS Istituto Giannina Gaslini, Genoa, Italy.

Andrea Rossi (A)

Neuroradiology Unit, IRCCS Istituto Giannina Gaslini, Genoa, Italy.

Luca Antonio Ramenghi (LA)

Neonatal Intensive Care Unit, IRCCS Istituto Giannina Gaslini, Genoa, Italy.

Classifications MeSH