Long-Term Associations between Early-Life Family Functioning and Preadolescent White Matter Microstructure

Scott Delaney; Yllza Xerxa; Ryan Muetzel; Tonya White; Sebastien Haneuse; Kerry J. Ressler; Henning Tiemeier; Laura D. Kubzansky

doi:10.1017/S0033291722001404

Long-Term Associations between Early-Life Family Functioning and Preadolescent White Matter Microstructure

Scott Delaney
, Yllza Xerxa
, Ryan Muetzel
, Tonya White
, Sebastien Haneuse
, Kerry J. Ressler
, Henning Tiemeier
, Laura D. Kubzansky

Harvard T.H. Chan School of Public Health
McLean Hospital

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

3 Citations (Scopus)

75 Downloads (Pure)

Abstract

Background.
Causes of childhood behavior problems remain poorly understood. Enriched
family environments and corresponding brain development may reduce the risk of their onset, but research investigating white matter neurodevelopmental pathways explaining associations between the family environment and behavior remains limited. We hypothesized that
more positive prenatal and mid-childhood family functioning – a measure of a family’s problem solving and supportive capacity – would be associated with two markers of preadolescent white matter neurodevelopment related to reduced behavior problems: higher global fractional anisotropy (FA) and lower global mean diffusivity (MD).

Methods.
Data are from 2727 families in the Generation R Study, the Netherlands. Mothers reported family functioning (McMaster Family Assessment Device, range 1–4, higher scores indicate healthier functioning) prenatally and in mid-childhood (mean age 6.1 years). In preadolescence (mean age 10.1), the study collected diffusion-weighted scans. We computed
standardized global MD and FA values by averaging metrics from 27 white matter tracts, and we fit linear models adjusting for possible confounders to examine global and tractspecific outcomes.

Results.
Prenatal and mid-childhood family functioning scores were moderately correlated, r = 0.38. However, only prenatal family functioning – and not mid-childhood functioning – was associated with higher global FA and lower global MD in preadolescence in fully adjusted models: βglobal FA = 0.11 (95% CI 0.00, 0.21) and βglobal MD = −0.15 (95% CI −0.28, −0.03) per
one-unit increase in functioning score. Sensitivity and tract-specific analyses supported these global findings.

Conclusions.
These results suggest high-functioning prenatal or perinatal family environments may confer lasting white matter neurodevelopmental benefits into preadolescence.

Original language	English
Pages (from-to)	4528-4538
Number of pages	11
Journal	Psychological Medicine
Volume	53
Issue number	10
Early online date	25 May 2022
DOIs	https://doi.org/10.1017/S0033291722001404
Publication status	Published - 25 Jul 2023

Bibliographical note

Funding Information:
Design and administration of the Generation R Study are made possible by financial support from the Erasmus Medical Center, Rotterdam, the Erasmus University Rotterdam, the Netherlands Organization for Health Research and Development (ZonMw), the Netherlands Organisation for Scientific Research (NWO), the Ministry of Health, Welfare and Sport, and the Ministry of Youth and Families. Dr Delaney's research contribution reported in this publication was supported by the Eunice Kennedy Shriver National Institute of Child Health & Human Development of the National Institutes of Health under Award Number F31HD096820 and by the National Institute of Mental Health under Award Number T32MH017119. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. Dr Delaney was further supported by the Lee Kum Sheung Center for Health and Happiness at Harvard University and the Doris Duke Charitable Foundation. The work of Yllza Xerxa was supported by funding by an NWO-VICI grant (PI: Henning Tiemeier; NWO-ZonMW: 016.VICI.170.200). R. L. M. and the Generation R neuroimaging infrastructure were supported by the Sophia Foundation (S18-20) and the Erasmus University Fellowship (2019). Supercomputing resources were supported by a grant from the Dutch Research Organization (NWO) and SurfSara awarded to R. L. M. Neuroimaging data collection and image processing were supported in part by the Netherlands Organization for Health Research and Development (ZonMw) TOP project number 91211021 to Dr White. The work of Henning Tiemeier was supported an NWO-VICI grant (NWO-ZonMW: 016.VICI.170.200). Dr Kubzansky's research contribution reported in this publication was supported in part by the Lee Kum Sheung Center for Health and Happiness at Harvard University.

Publisher Copyright:
Copyright © The Author(s), 2022. Published by Cambridge University Press.

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@article{03eaec8d8dd4442ab0ee466a8cc8b3a4,

title = "Long-Term Associations between Early-Life Family Functioning and Preadolescent White Matter Microstructure",

abstract = "Background. Causes of childhood behavior problems remain poorly understood. Enriched family environments and corresponding brain development may reduce the risk of their onset, but research investigating white matter neurodevelopmental pathways explaining associations between the family environment and behavior remains limited. We hypothesized that more positive prenatal and mid-childhood family functioning {\textendash} a measure of a family{\textquoteright}s problem solving and supportive capacity {\textendash} would be associated with two markers of preadolescent white matter neurodevelopment related to reduced behavior problems: higher global fractional anisotropy (FA) and lower global mean diffusivity (MD). Methods. Data are from 2727 families in the Generation R Study, the Netherlands. Mothers reported family functioning (McMaster Family Assessment Device, range 1{\textendash}4, higher scores indicate healthier functioning) prenatally and in mid-childhood (mean age 6.1 years). In preadolescence (mean age 10.1), the study collected diffusion-weighted scans. We computed standardized global MD and FA values by averaging metrics from 27 white matter tracts, and we fit linear models adjusting for possible confounders to examine global and tractspecific outcomes. Results. Prenatal and mid-childhood family functioning scores were moderately correlated, r = 0.38. However, only prenatal family functioning {\textendash} and not mid-childhood functioning {\textendash} was associated with higher global FA and lower global MD in preadolescence in fully adjusted models: βglobal FA = 0.11 (95\% CI 0.00, 0.21) and βglobal MD = −0.15 (95\% CI −0.28, −0.03) per one-unit increase in functioning score. Sensitivity and tract-specific analyses supported these global findings. Conclusions. These results suggest high-functioning prenatal or perinatal family environments may confer lasting white matter neurodevelopmental benefits into preadolescence. ",

author = "Scott Delaney and Yllza Xerxa and Ryan Muetzel and Tonya White and Sebastien Haneuse and Ressler, \{Kerry J.\} and Henning Tiemeier and Kubzansky, \{Laura D.\}",

note = "Funding Information: Design and administration of the Generation R Study are made possible by financial support from the Erasmus Medical Center, Rotterdam, the Erasmus University Rotterdam, the Netherlands Organization for Health Research and Development (ZonMw), the Netherlands Organisation for Scientific Research (NWO), the Ministry of Health, Welfare and Sport, and the Ministry of Youth and Families. Dr Delaney's research contribution reported in this publication was supported by the Eunice Kennedy Shriver National Institute of Child Health \& Human Development of the National Institutes of Health under Award Number F31HD096820 and by the National Institute of Mental Health under Award Number T32MH017119. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. Dr Delaney was further supported by the Lee Kum Sheung Center for Health and Happiness at Harvard University and the Doris Duke Charitable Foundation. The work of Yllza Xerxa was supported by funding by an NWO-VICI grant (PI: Henning Tiemeier; NWO-ZonMW: 016.VICI.170.200). R. L. M. and the Generation R neuroimaging infrastructure were supported by the Sophia Foundation (S18-20) and the Erasmus University Fellowship (2019). Supercomputing resources were supported by a grant from the Dutch Research Organization (NWO) and SurfSara awarded to R. L. M. Neuroimaging data collection and image processing were supported in part by the Netherlands Organization for Health Research and Development (ZonMw) TOP project number 91211021 to Dr White. The work of Henning Tiemeier was supported an NWO-VICI grant (NWO-ZonMW: 016.VICI.170.200). Dr Kubzansky's research contribution reported in this publication was supported in part by the Lee Kum Sheung Center for Health and Happiness at Harvard University. Publisher Copyright: Copyright {\textcopyright} The Author(s), 2022. Published by Cambridge University Press.",

year = "2023",

month = jul,

day = "25",

doi = "10.1017/S0033291722001404",

language = "English",

volume = "53",

pages = "4528--4538",

journal = "Psychological Medicine",

issn = "0033-2917",

publisher = "Cambridge University Press",

number = "10",

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TY - JOUR

T1 - Long-Term Associations between Early-Life Family Functioning and Preadolescent White Matter Microstructure

AU - Delaney, Scott

AU - Xerxa, Yllza

AU - Muetzel, Ryan

AU - White, Tonya

AU - Haneuse, Sebastien

AU - Ressler, Kerry J.

AU - Tiemeier, Henning

AU - Kubzansky, Laura D.

N1 - Funding Information: Design and administration of the Generation R Study are made possible by financial support from the Erasmus Medical Center, Rotterdam, the Erasmus University Rotterdam, the Netherlands Organization for Health Research and Development (ZonMw), the Netherlands Organisation for Scientific Research (NWO), the Ministry of Health, Welfare and Sport, and the Ministry of Youth and Families. Dr Delaney's research contribution reported in this publication was supported by the Eunice Kennedy Shriver National Institute of Child Health & Human Development of the National Institutes of Health under Award Number F31HD096820 and by the National Institute of Mental Health under Award Number T32MH017119. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. Dr Delaney was further supported by the Lee Kum Sheung Center for Health and Happiness at Harvard University and the Doris Duke Charitable Foundation. The work of Yllza Xerxa was supported by funding by an NWO-VICI grant (PI: Henning Tiemeier; NWO-ZonMW: 016.VICI.170.200). R. L. M. and the Generation R neuroimaging infrastructure were supported by the Sophia Foundation (S18-20) and the Erasmus University Fellowship (2019). Supercomputing resources were supported by a grant from the Dutch Research Organization (NWO) and SurfSara awarded to R. L. M. Neuroimaging data collection and image processing were supported in part by the Netherlands Organization for Health Research and Development (ZonMw) TOP project number 91211021 to Dr White. The work of Henning Tiemeier was supported an NWO-VICI grant (NWO-ZonMW: 016.VICI.170.200). Dr Kubzansky's research contribution reported in this publication was supported in part by the Lee Kum Sheung Center for Health and Happiness at Harvard University. Publisher Copyright: Copyright © The Author(s), 2022. Published by Cambridge University Press.

PY - 2023/7/25

Y1 - 2023/7/25

N2 - Background. Causes of childhood behavior problems remain poorly understood. Enriched family environments and corresponding brain development may reduce the risk of their onset, but research investigating white matter neurodevelopmental pathways explaining associations between the family environment and behavior remains limited. We hypothesized that more positive prenatal and mid-childhood family functioning – a measure of a family’s problem solving and supportive capacity – would be associated with two markers of preadolescent white matter neurodevelopment related to reduced behavior problems: higher global fractional anisotropy (FA) and lower global mean diffusivity (MD). Methods. Data are from 2727 families in the Generation R Study, the Netherlands. Mothers reported family functioning (McMaster Family Assessment Device, range 1–4, higher scores indicate healthier functioning) prenatally and in mid-childhood (mean age 6.1 years). In preadolescence (mean age 10.1), the study collected diffusion-weighted scans. We computed standardized global MD and FA values by averaging metrics from 27 white matter tracts, and we fit linear models adjusting for possible confounders to examine global and tractspecific outcomes. Results. Prenatal and mid-childhood family functioning scores were moderately correlated, r = 0.38. However, only prenatal family functioning – and not mid-childhood functioning – was associated with higher global FA and lower global MD in preadolescence in fully adjusted models: βglobal FA = 0.11 (95% CI 0.00, 0.21) and βglobal MD = −0.15 (95% CI −0.28, −0.03) per one-unit increase in functioning score. Sensitivity and tract-specific analyses supported these global findings. Conclusions. These results suggest high-functioning prenatal or perinatal family environments may confer lasting white matter neurodevelopmental benefits into preadolescence.

AB - Background. Causes of childhood behavior problems remain poorly understood. Enriched family environments and corresponding brain development may reduce the risk of their onset, but research investigating white matter neurodevelopmental pathways explaining associations between the family environment and behavior remains limited. We hypothesized that more positive prenatal and mid-childhood family functioning – a measure of a family’s problem solving and supportive capacity – would be associated with two markers of preadolescent white matter neurodevelopment related to reduced behavior problems: higher global fractional anisotropy (FA) and lower global mean diffusivity (MD). Methods. Data are from 2727 families in the Generation R Study, the Netherlands. Mothers reported family functioning (McMaster Family Assessment Device, range 1–4, higher scores indicate healthier functioning) prenatally and in mid-childhood (mean age 6.1 years). In preadolescence (mean age 10.1), the study collected diffusion-weighted scans. We computed standardized global MD and FA values by averaging metrics from 27 white matter tracts, and we fit linear models adjusting for possible confounders to examine global and tractspecific outcomes. Results. Prenatal and mid-childhood family functioning scores were moderately correlated, r = 0.38. However, only prenatal family functioning – and not mid-childhood functioning – was associated with higher global FA and lower global MD in preadolescence in fully adjusted models: βglobal FA = 0.11 (95% CI 0.00, 0.21) and βglobal MD = −0.15 (95% CI −0.28, −0.03) per one-unit increase in functioning score. Sensitivity and tract-specific analyses supported these global findings. Conclusions. These results suggest high-functioning prenatal or perinatal family environments may confer lasting white matter neurodevelopmental benefits into preadolescence.

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DO - 10.1017/S0033291722001404

M3 - Article

C2 - 35611817

SN - 0033-2917

VL - 53

SP - 4528

EP - 4538

JO - Psychological Medicine

JF - Psychological Medicine

IS - 10

ER -

Long-Term Associations between Early-Life Family Functioning and Preadolescent White Matter Microstructure

Abstract

Bibliographical note

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