Patterns of Fetal and Infant Growth and Brain Morphology at Age 10 Years

Carolina C.V. Silva; Hanan El Marroun; Sara Sammallahti; Meike W. Vernooij; Ryan L. Muetzel; Susana Santos; Vincent W.V. Jaddoe

doi:10.1001/jamanetworkopen.2021.38214

Patterns of Fetal and Infant Growth and Brain Morphology at Age 10 Years

Carolina C.V. Silva, Hanan El Marroun, Sara Sammallahti, Meike W. Vernooij, Ryan L. Muetzel, Susana Santos, Vincent W.V. Jaddoe^*

^*Corresponding author for this work

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

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Abstract

Importance: Preterm birth and low birth weight are associated with brain developmental and neurocognitive outcomes in childhood; however, not much is known about the specific critical periods in fetal life and infancy for these outcomes.

Objective: To examine the associations of fetal and infant growth patterns with brain morphology in children at school age.

Design, Setting, and Participants: This population-based, prospective cohort study was conducted from February 1 to April 16, 2021, as a part of the Generation R Study in Rotterdam, the Netherlands. The study included 3098 singleton children born between April 1, 2002, and January 31, 2006.

Exposures: Fetal weight was estimated in the second and third trimesters of pregnancy by ultrasonography. Infant weight was measured at birth and at 6, 12, and 24 months. Fetal and infant weight acceleration or deceleration were defined as a change in SD scores greater than 0.67 between time points. Infant measurements also included peak weight velocity, and age and body mass index reached at adiposity peak.

Main Outcomes and Measures: Brain structure, including global and regional brain volumes, was quantified by magnetic resonance imaging at age 10 years.

Results: The study evaluated 3098 children (mean [SD] age at follow-up, 10.1 [0.6] years; 1557 girls [50.3%]; and 1753 Dutch [57.8%]). One SD score-higher weight gain until the second and third trimesters, birth, and 6, 12, and 24 months was associated with larger total brain volume independently of growth during any other age windows (second trimester: 5.7 cm³; 95% CI, 1.2-10.2 cm³; third trimester: 15.3 cm³; 95% CI, 11.0-19.6 cm³; birth: 20.8 cm³; 95% CI, 16.4-25.1 cm³; 6 months: 15.6 cm³; 95% CI, 11.2-19.9 cm³; 12 months: 11.3 cm³; 95% CI, 7.0-15.6 cm³; and 24 months: 11.1 cm³; 95% CI, 6.8-15.4 cm³). Compared with children with normal fetal and infant growth, those with fetal and infant growth deceleration had the smallest total brain volume (-32.5 cm³; 95% CI, -53.2 to -11.9 cm³). Children with fetal weight deceleration followed by infant catch-up growth had similar brain volumes as children with normal growth. Higher peak weight velocity and body mass index reached at adiposity peak were associated with larger brain volumes. Similar results were observed for cerebral and cerebellar gray and white matter volumes.

Conclusions and Relevance: This cohort study's findings suggest that both fetal and infant weight growth might be critical for cerebral and cerebellar brain volumes during childhood. Whether these associations link to neurocognitive outcomes should be further studied..

Original language	English
Article number	e2138214
Journal	JAMA network open
Volume	4
Issue number	12
DOIs	https://doi.org/10.1001/jamanetworkopen.2021.38214
Publication status	Published - 9 Dec 2021

Bibliographical note

Funding Information:
Muetzel, Santos. Statistical analysis: Silva, Santos. Obtained funding: Jaddoe. Administrative, technical, or material support: Muetzel, Jaddoe. Supervision: El Marroun, Santos, Jaddoe. Conflict of Interest Disclosures: None reported. Funding/Support: The general design of the Generation R Study is made possible by financial support from the Erasmus Medical Center, Rotterdam, the Erasmus University Rotterdam, the Netherlands, Organisation for Health Research and Development, the Netherlands Organisation for Scientific Research (NWO), and the Ministry of Health, Welfare and Sport. Dr Jaddoe received grants from the European Research Council (ERC-2014-CoG-648916). This project was supported by funding support from the European Union’s Horizon 2020 research and innovation program under grant agreement 733206 (LifeCycle). Dr El Marroun was supported by Stichting Volksbond Rotterdam, the Dutch Brain Foundation (project number GH2016.2.01), and the National Alliance for Research on Schizophrenia and Depression Young Investigator Grant from the Brain and Behavior Research Foundation (grant 27853). Dr Sammallahti was supported by Orionin Tutkimussäätiö (Orion Research Foundation) and the Marie Skłodowska-Curie COFUND LEaDing Fellows Programme. Dr Muetzel was supported by the Sophia Fundation (S18-20). Supercomputing computations were supported by the NWO Physical Sciences Division: Exacte Wetenschappen, and SURFsara: Cartesius computer cluster (www.surfsara.nl).

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© 2021 American Medical Association. All rights reserved.

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@article{955a5c3a96cf447cac1f06f0a90a2ada,

title = "Patterns of Fetal and Infant Growth and Brain Morphology at Age 10 Years",

abstract = "Importance: Preterm birth and low birth weight are associated with brain developmental and neurocognitive outcomes in childhood; however, not much is known about the specific critical periods in fetal life and infancy for these outcomes. Objective: To examine the associations of fetal and infant growth patterns with brain morphology in children at school age. Design, Setting, and Participants: This population-based, prospective cohort study was conducted from February 1 to April 16, 2021, as a part of the Generation R Study in Rotterdam, the Netherlands. The study included 3098 singleton children born between April 1, 2002, and January 31, 2006. Exposures: Fetal weight was estimated in the second and third trimesters of pregnancy by ultrasonography. Infant weight was measured at birth and at 6, 12, and 24 months. Fetal and infant weight acceleration or deceleration were defined as a change in SD scores greater than 0.67 between time points. Infant measurements also included peak weight velocity, and age and body mass index reached at adiposity peak. Main Outcomes and Measures: Brain structure, including global and regional brain volumes, was quantified by magnetic resonance imaging at age 10 years. Results: The study evaluated 3098 children (mean [SD] age at follow-up, 10.1 [0.6] years; 1557 girls [50.3%]; and 1753 Dutch [57.8%]). One SD score-higher weight gain until the second and third trimesters, birth, and 6, 12, and 24 months was associated with larger total brain volume independently of growth during any other age windows (second trimester: 5.7 cm3; 95% CI, 1.2-10.2 cm3; third trimester: 15.3 cm3; 95% CI, 11.0-19.6 cm3; birth: 20.8 cm3; 95% CI, 16.4-25.1 cm3; 6 months: 15.6 cm3; 95% CI, 11.2-19.9 cm3; 12 months: 11.3 cm3; 95% CI, 7.0-15.6 cm3; and 24 months: 11.1 cm3; 95% CI, 6.8-15.4 cm3). Compared with children with normal fetal and infant growth, those with fetal and infant growth deceleration had the smallest total brain volume (-32.5 cm3; 95% CI, -53.2 to -11.9 cm3). Children with fetal weight deceleration followed by infant catch-up growth had similar brain volumes as children with normal growth. Higher peak weight velocity and body mass index reached at adiposity peak were associated with larger brain volumes. Similar results were observed for cerebral and cerebellar gray and white matter volumes. Conclusions and Relevance: This cohort study's findings suggest that both fetal and infant weight growth might be critical for cerebral and cerebellar brain volumes during childhood. Whether these associations link to neurocognitive outcomes should be further studied..",

author = "Silva, {Carolina C.V.} and {El Marroun}, Hanan and Sara Sammallahti and Vernooij, {Meike W.} and Muetzel, {Ryan L.} and Susana Santos and Jaddoe, {Vincent W.V.}",

note = "Funding Information: Muetzel, Santos. Statistical analysis: Silva, Santos. Obtained funding: Jaddoe. Administrative, technical, or material support: Muetzel, Jaddoe. Supervision: El Marroun, Santos, Jaddoe. Conflict of Interest Disclosures: None reported. Funding/Support: The general design of the Generation R Study is made possible by financial support from the Erasmus Medical Center, Rotterdam, the Erasmus University Rotterdam, the Netherlands, Organisation for Health Research and Development, the Netherlands Organisation for Scientific Research (NWO), and the Ministry of Health, Welfare and Sport. Dr Jaddoe received grants from the European Research Council (ERC-2014-CoG-648916). This project was supported by funding support from the European Union{\textquoteright}s Horizon 2020 research and innovation program under grant agreement 733206 (LifeCycle). Dr El Marroun was supported by Stichting Volksbond Rotterdam, the Dutch Brain Foundation (project number GH2016.2.01), and the National Alliance for Research on Schizophrenia and Depression Young Investigator Grant from the Brain and Behavior Research Foundation (grant 27853). Dr Sammallahti was supported by Orionin Tutkimuss{\"a}{\"a}ti{\"o} (Orion Research Foundation) and the Marie Sk{\l}odowska-Curie COFUND LEaDing Fellows Programme. Dr Muetzel was supported by the Sophia Fundation (S18-20). Supercomputing computations were supported by the NWO Physical Sciences Division: Exacte Wetenschappen, and SURFsara: Cartesius computer cluster (www.surfsara.nl). Publisher Copyright: {\textcopyright} 2021 American Medical Association. All rights reserved.",

year = "2021",

month = dec,

day = "9",

doi = "10.1001/jamanetworkopen.2021.38214",

language = "English",

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T1 - Patterns of Fetal and Infant Growth and Brain Morphology at Age 10 Years

AU - Silva, Carolina C.V.

AU - El Marroun, Hanan

AU - Sammallahti, Sara

AU - Vernooij, Meike W.

AU - Muetzel, Ryan L.

AU - Santos, Susana

AU - Jaddoe, Vincent W.V.

N1 - Funding Information: Muetzel, Santos. Statistical analysis: Silva, Santos. Obtained funding: Jaddoe. Administrative, technical, or material support: Muetzel, Jaddoe. Supervision: El Marroun, Santos, Jaddoe. Conflict of Interest Disclosures: None reported. Funding/Support: The general design of the Generation R Study is made possible by financial support from the Erasmus Medical Center, Rotterdam, the Erasmus University Rotterdam, the Netherlands, Organisation for Health Research and Development, the Netherlands Organisation for Scientific Research (NWO), and the Ministry of Health, Welfare and Sport. Dr Jaddoe received grants from the European Research Council (ERC-2014-CoG-648916). This project was supported by funding support from the European Union’s Horizon 2020 research and innovation program under grant agreement 733206 (LifeCycle). Dr El Marroun was supported by Stichting Volksbond Rotterdam, the Dutch Brain Foundation (project number GH2016.2.01), and the National Alliance for Research on Schizophrenia and Depression Young Investigator Grant from the Brain and Behavior Research Foundation (grant 27853). Dr Sammallahti was supported by Orionin Tutkimussäätiö (Orion Research Foundation) and the Marie Skłodowska-Curie COFUND LEaDing Fellows Programme. Dr Muetzel was supported by the Sophia Fundation (S18-20). Supercomputing computations were supported by the NWO Physical Sciences Division: Exacte Wetenschappen, and SURFsara: Cartesius computer cluster (www.surfsara.nl). Publisher Copyright: © 2021 American Medical Association. All rights reserved.

PY - 2021/12/9

Y1 - 2021/12/9

N2 - Importance: Preterm birth and low birth weight are associated with brain developmental and neurocognitive outcomes in childhood; however, not much is known about the specific critical periods in fetal life and infancy for these outcomes. Objective: To examine the associations of fetal and infant growth patterns with brain morphology in children at school age. Design, Setting, and Participants: This population-based, prospective cohort study was conducted from February 1 to April 16, 2021, as a part of the Generation R Study in Rotterdam, the Netherlands. The study included 3098 singleton children born between April 1, 2002, and January 31, 2006. Exposures: Fetal weight was estimated in the second and third trimesters of pregnancy by ultrasonography. Infant weight was measured at birth and at 6, 12, and 24 months. Fetal and infant weight acceleration or deceleration were defined as a change in SD scores greater than 0.67 between time points. Infant measurements also included peak weight velocity, and age and body mass index reached at adiposity peak. Main Outcomes and Measures: Brain structure, including global and regional brain volumes, was quantified by magnetic resonance imaging at age 10 years. Results: The study evaluated 3098 children (mean [SD] age at follow-up, 10.1 [0.6] years; 1557 girls [50.3%]; and 1753 Dutch [57.8%]). One SD score-higher weight gain until the second and third trimesters, birth, and 6, 12, and 24 months was associated with larger total brain volume independently of growth during any other age windows (second trimester: 5.7 cm3; 95% CI, 1.2-10.2 cm3; third trimester: 15.3 cm3; 95% CI, 11.0-19.6 cm3; birth: 20.8 cm3; 95% CI, 16.4-25.1 cm3; 6 months: 15.6 cm3; 95% CI, 11.2-19.9 cm3; 12 months: 11.3 cm3; 95% CI, 7.0-15.6 cm3; and 24 months: 11.1 cm3; 95% CI, 6.8-15.4 cm3). Compared with children with normal fetal and infant growth, those with fetal and infant growth deceleration had the smallest total brain volume (-32.5 cm3; 95% CI, -53.2 to -11.9 cm3). Children with fetal weight deceleration followed by infant catch-up growth had similar brain volumes as children with normal growth. Higher peak weight velocity and body mass index reached at adiposity peak were associated with larger brain volumes. Similar results were observed for cerebral and cerebellar gray and white matter volumes. Conclusions and Relevance: This cohort study's findings suggest that both fetal and infant weight growth might be critical for cerebral and cerebellar brain volumes during childhood. Whether these associations link to neurocognitive outcomes should be further studied..

AB - Importance: Preterm birth and low birth weight are associated with brain developmental and neurocognitive outcomes in childhood; however, not much is known about the specific critical periods in fetal life and infancy for these outcomes. Objective: To examine the associations of fetal and infant growth patterns with brain morphology in children at school age. Design, Setting, and Participants: This population-based, prospective cohort study was conducted from February 1 to April 16, 2021, as a part of the Generation R Study in Rotterdam, the Netherlands. The study included 3098 singleton children born between April 1, 2002, and January 31, 2006. Exposures: Fetal weight was estimated in the second and third trimesters of pregnancy by ultrasonography. Infant weight was measured at birth and at 6, 12, and 24 months. Fetal and infant weight acceleration or deceleration were defined as a change in SD scores greater than 0.67 between time points. Infant measurements also included peak weight velocity, and age and body mass index reached at adiposity peak. Main Outcomes and Measures: Brain structure, including global and regional brain volumes, was quantified by magnetic resonance imaging at age 10 years. Results: The study evaluated 3098 children (mean [SD] age at follow-up, 10.1 [0.6] years; 1557 girls [50.3%]; and 1753 Dutch [57.8%]). One SD score-higher weight gain until the second and third trimesters, birth, and 6, 12, and 24 months was associated with larger total brain volume independently of growth during any other age windows (second trimester: 5.7 cm3; 95% CI, 1.2-10.2 cm3; third trimester: 15.3 cm3; 95% CI, 11.0-19.6 cm3; birth: 20.8 cm3; 95% CI, 16.4-25.1 cm3; 6 months: 15.6 cm3; 95% CI, 11.2-19.9 cm3; 12 months: 11.3 cm3; 95% CI, 7.0-15.6 cm3; and 24 months: 11.1 cm3; 95% CI, 6.8-15.4 cm3). Compared with children with normal fetal and infant growth, those with fetal and infant growth deceleration had the smallest total brain volume (-32.5 cm3; 95% CI, -53.2 to -11.9 cm3). Children with fetal weight deceleration followed by infant catch-up growth had similar brain volumes as children with normal growth. Higher peak weight velocity and body mass index reached at adiposity peak were associated with larger brain volumes. Similar results were observed for cerebral and cerebellar gray and white matter volumes. Conclusions and Relevance: This cohort study's findings suggest that both fetal and infant weight growth might be critical for cerebral and cerebellar brain volumes during childhood. Whether these associations link to neurocognitive outcomes should be further studied..

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Patterns of Fetal and Infant Growth and Brain Morphology at Age 10 Years

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