Rapid Postnatal Adaptation of Neurodevelopment in Pigs Born Late Preterm

Charlotte Holme Nielsen; Anne Bladt Brandt; Thomas Thymann; Karina Obelitz-Ryom; Pingping Jiang; Charlotte Vanden Hole; Chris van Ginneken; Stanislava Pankratova; Per Torp Sangild

doi:10.1159/000499127

Rapid Postnatal Adaptation of Neurodevelopment in Pigs Born Late Preterm

Charlotte Holme Nielsen, Anne Bladt Brandt, Thomas Thymann, Karina Obelitz-Ryom, Pingping Jiang, Charlotte Vanden Hole, Chris van Ginneken, Stanislava Pankratova, Per Torp Sangild

5 Citationer (Scopus)

Abstract

Preterm birth interrupts intrauterine brain growth and maturation and may induce a delay in postnatal neurodevelopment. Such developmental delays can result from the reduced fetal age at birth, together with the clinical compli-cations of preterm birth (e.g., hypoxia, ischemia, and inflammation). We hypothesized that late preterm birth, inducing only mild clinical complications, has minimal effects on brain-related outcomes such as motor function and behavior. Using the pig as a model for late preterm infants, piglets were cesarean delivered preterm (90%, 106 days gestation) or at full term, reared by identical procedures, and euthanized for tissue collection at birth or after 11 days (e.g., term-corrected age for preterm pigs). Clinical variables and both structural and functional brain endpoints were assessed. The preterm pigs were slow to get on their feet, gained less weight (-30%), and had a higher cerebral hydration level and blood-to-cerebrospinal fluid permeability than the term pigs. At term-corrected age (11 days), the absolute weight of the brain and the weights of its regions were similar between 11-day-old preterm and newborn term pigs, and both were lower than in 11-day-old term pigs. Postnatally, physical activity and movements in an open field were similar, except that preterm pigs showed a reduced normalized stride length and increased normalized maximum stride height. Perinatal brain growth is closely associated with advancing postconceptional age in pigs, and late preterm birth is initially associated with impaired brain growth and physical activity. Postnatally, neuromuscular functions mature rapidly and become similar to those in term pigs, even before term-corrected age. Neuromuscular functions and behavior may show rapid postnatal adaptation to late preterm birth in both pigs and infants.

Originalsprog	Engelsk
Artikelnummer	586–600
Tidsskrift	Developmental Neuroscience
Vol/bind	40
Udgave nummer	5-6
Antal sider	15
ISSN	0378-5866
DOI	https://doi.org/10.1159/000499127
Status	Udgivet - 1 jul. 2019

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10.1159/000499127

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title = "Rapid Postnatal Adaptation of Neurodevelopment in Pigs Born Late Preterm",

abstract = "Preterm birth interrupts intrauterine brain growth and maturation and may induce a delay in postnatal neurodevelopment. Such developmental delays can result from the reduced fetal age at birth, together with the clinical compli-cations of preterm birth (e.g., hypoxia, ischemia, and inflammation). We hypothesized that late preterm birth, inducing only mild clinical complications, has minimal effects on brain-related outcomes such as motor function and behavior. Using the pig as a model for late preterm infants, piglets were cesarean delivered preterm (90%, 106 days gestation) or at full term, reared by identical procedures, and euthanized for tissue collection at birth or after 11 days (e.g., term-corrected age for preterm pigs). Clinical variables and both structural and functional brain endpoints were assessed. The preterm pigs were slow to get on their feet, gained less weight (-30%), and had a higher cerebral hydration level and blood-to-cerebrospinal fluid permeability than the term pigs. At term-corrected age (11 days), the absolute weight of the brain and the weights of its regions were similar between 11-day-old preterm and newborn term pigs, and both were lower than in 11-day-old term pigs. Postnatally, physical activity and movements in an open field were similar, except that preterm pigs showed a reduced normalized stride length and increased normalized maximum stride height. Perinatal brain growth is closely associated with advancing postconceptional age in pigs, and late preterm birth is initially associated with impaired brain growth and physical activity. Postnatally, neuromuscular functions mature rapidly and become similar to those in term pigs, even before term-corrected age. Neuromuscular functions and behavior may show rapid postnatal adaptation to late preterm birth in both pigs and infants.",

author = "{Holme Nielsen}, Charlotte and {Bladt Brandt}, Anne and Thomas Thymann and Karina Obelitz-Ryom and Pingping Jiang and {Vanden Hole}, Charlotte and {van Ginneken}, Chris and Stanislava Pankratova and Sangild, {Per Torp}",

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AU - Holme Nielsen, Charlotte

AU - Bladt Brandt, Anne

AU - Thymann, Thomas

AU - Obelitz-Ryom, Karina

AU - Jiang, Pingping

AU - Vanden Hole, Charlotte

AU - van Ginneken, Chris

AU - Pankratova, Stanislava

AU - Sangild, Per Torp

PY - 2019/7/1

Y1 - 2019/7/1

N2 - Preterm birth interrupts intrauterine brain growth and maturation and may induce a delay in postnatal neurodevelopment. Such developmental delays can result from the reduced fetal age at birth, together with the clinical compli-cations of preterm birth (e.g., hypoxia, ischemia, and inflammation). We hypothesized that late preterm birth, inducing only mild clinical complications, has minimal effects on brain-related outcomes such as motor function and behavior. Using the pig as a model for late preterm infants, piglets were cesarean delivered preterm (90%, 106 days gestation) or at full term, reared by identical procedures, and euthanized for tissue collection at birth or after 11 days (e.g., term-corrected age for preterm pigs). Clinical variables and both structural and functional brain endpoints were assessed. The preterm pigs were slow to get on their feet, gained less weight (-30%), and had a higher cerebral hydration level and blood-to-cerebrospinal fluid permeability than the term pigs. At term-corrected age (11 days), the absolute weight of the brain and the weights of its regions were similar between 11-day-old preterm and newborn term pigs, and both were lower than in 11-day-old term pigs. Postnatally, physical activity and movements in an open field were similar, except that preterm pigs showed a reduced normalized stride length and increased normalized maximum stride height. Perinatal brain growth is closely associated with advancing postconceptional age in pigs, and late preterm birth is initially associated with impaired brain growth and physical activity. Postnatally, neuromuscular functions mature rapidly and become similar to those in term pigs, even before term-corrected age. Neuromuscular functions and behavior may show rapid postnatal adaptation to late preterm birth in both pigs and infants.

AB - Preterm birth interrupts intrauterine brain growth and maturation and may induce a delay in postnatal neurodevelopment. Such developmental delays can result from the reduced fetal age at birth, together with the clinical compli-cations of preterm birth (e.g., hypoxia, ischemia, and inflammation). We hypothesized that late preterm birth, inducing only mild clinical complications, has minimal effects on brain-related outcomes such as motor function and behavior. Using the pig as a model for late preterm infants, piglets were cesarean delivered preterm (90%, 106 days gestation) or at full term, reared by identical procedures, and euthanized for tissue collection at birth or after 11 days (e.g., term-corrected age for preterm pigs). Clinical variables and both structural and functional brain endpoints were assessed. The preterm pigs were slow to get on their feet, gained less weight (-30%), and had a higher cerebral hydration level and blood-to-cerebrospinal fluid permeability than the term pigs. At term-corrected age (11 days), the absolute weight of the brain and the weights of its regions were similar between 11-day-old preterm and newborn term pigs, and both were lower than in 11-day-old term pigs. Postnatally, physical activity and movements in an open field were similar, except that preterm pigs showed a reduced normalized stride length and increased normalized maximum stride height. Perinatal brain growth is closely associated with advancing postconceptional age in pigs, and late preterm birth is initially associated with impaired brain growth and physical activity. Postnatally, neuromuscular functions mature rapidly and become similar to those in term pigs, even before term-corrected age. Neuromuscular functions and behavior may show rapid postnatal adaptation to late preterm birth in both pigs and infants.

U2 - 10.1159/000499127

DO - 10.1159/000499127

M3 - Journal article

C2 - 31141813

SN - 0378-5866

VL - 40

JO - Developmental Neuroscience

JF - Developmental Neuroscience

IS - 5-6

M1 - 586–600

ER -

Rapid Postnatal Adaptation of Neurodevelopment in Pigs Born Late Preterm

Abstract

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