Changes in the intracranial volume from early adulthood to the sixth decade of life: A longitudinal study

Y. Caspi, R.M. Brouwer, H.G. Schnack, M.E. van de Nieuwenhuijzen, W. Cahn, R.S. Kahn, W.J. Niessen, A. van der Lugt, H.H. Pol

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

© 2020 The Author(s)Normal brain-aging occurs at all structural levels. Excessive pathophysiological changes in the brain, beyond the normal one, are implicated in the etiology of brain disorders such as severe forms of the schizophrenia spectrum and dementia. To account for brain-aging in health and disease, it is critical to study the age-dependent trajectories of brain biomarkers at various levels and among different age groups. The intracranial volume (ICV) is a key biological marker, and changes in the ICV during the lifespan can teach us about the biology of development, aging, and gene X environment interactions. However, whether ICV changes with age in adulthood is not resolved. Applying a semi-automatic in-house-built algorithm for ICV extraction on T1w MR brain scans in the Dutch longitudinal cohort (GROUP), we measured ICV changes. Individuals between the ages of 16 and 55 years were scanned up to three consecutive times with 3.32±0.32 years between consecutive scans (N = 482, 359, 302). Using the extracted ICVs, we calculated ICV longitudinal aging-trajectories based on three analysis methods; direct calculation of ICV differences between the first and the last scan, fitting all ICV measurements of individuals to a straight line, and applying a global linear mixed model fitting. We report statistically significant increase in the ICV in adulthood until the fourth decade of life (average change +0.03%/y, or about 0.5 ml/y, at age 20), and decrease in the ICV afterward (−0.09%/y, or about −1.2 ml/y, at age 55). To account for previous cross-sectional reports of ICV changes, we analyzed the same data using a cross-sectional approach. Our cross-sectional analysis detected ICV changes consistent with the previously reported cross-sectional effect. However, the reported amount of cross-sectional changes within this age range was significantly larger than the longitudinal changes. We attribute the cross-sectional results to a generational effect. In conclusion, the human intracranial volume does not stay constant during adulthood but instead shows a small increase during young adulthood and a decrease thereafter from the fourth decade of life. The age-related changes in the longitudinalmeasure are smaller than those reported using cross-sectional approaches and unlikely to affect structural brain imaging studies correcting for intracranial volume considerably. As to the possible mechanisms involved, this awaits further study, although thickening of the meninges and skull bones have been proposed, as well as a smaller amount of brain fluids addition above the overall loss of brain tissue.
Original languageEnglish
Article number116842
JournalNeuroImage
Volume220
DOIs
Publication statusPublished - 15 Oct 2020
Externally publishedYes

Funding

The authors would like to thank Hakim Achterberg, Marcel Koek, Adriaan Versteeg, Thomas Phil, Thomas Kroes, Baldur van Lew, Marcel Zwiers and Seyed Mostafa Kia for a collaboration within the BBMRI-NL work-package 3. This work was supported by the Netherlands Organization for Scientific Research (NWO 184.033.111), Biobanking and BioMolecular resources Research Infrastructure The Netherlands (BBMRI-NL2.0), and by the ENIGMA World Aging Center grant (NIH 1R56AG058854-01, subaward 112068003). The infrastructure for the GROUP study is funded through the Geestkracht programme of the Dutch Health Research Council (Zon-Mw, grant number 10-000-1001), and matching funds from participating pharmaceutical companies (Lundbeck, AstraZeneca, Eli Lilly, Janssen Cilag) and universities and mental health care organizations (Amsterdam: Academic Psychiatric Centre of the Academic Medical Center and the mental health institutions: GGZ Ingeest, Arkin, Dijk en Duin, GGZ Rivierduinen, Erasmus Medical Centre, GGZ Noord Holland Noord. Groningen: University Medical Center Groningen and the mental health institutions: Lentis, GGZ Friesland, GGZ Drenthe, Dimence, Mediant, GGNet Warnsveld, Yulius Dordrecht and Parnassia psycho-medical center The Hague. Maastricht: Maastricht University Medical Centre and the mental health institutions: GGzE, GGZ Breburg, GGZ Oost-Brabant, Vincent van Gogh voor Geestelijke Gezondheid, Mondriaan, Virenze riagg, Zuyderland GGZ, MET ggz, Universitair Centrum Sint-Jozef Kortenberg, CAPRI University of Antwerp, PC Ziekeren Sint-Truiden, PZ Sancta Maria Sint-Truiden, GGZ Overpelt, OPZ Rekem. Utrecht: University Medical Center Utrecht and the mental health institutions Altrecht, GGZ Centraal and Delta. The infrastructure for the GROUP study is funded through the Geestkracht programme of the Dutch Health Research Council (Zon-Mw, grant number 10-000-1001 ), and matching funds from participating pharmaceutical companies (Lundbeck, AstraZeneca, Eli Lilly, Janssen Cilag) and universities and mental health care organizations (Amsterdam: Academic Psychiatric Centre of the Academic Medical Center and the mental health institutions: GGZ Ingeest, Arkin, Dijk en Duin, GGZ Rivierduinen, Erasmus Medical Centre, GGZ Noord Holland Noord. Groningen: University Medical Center Groningen and the mental health institutions: Lentis, GGZ Friesland, GGZ Drenthe, Dimence, Mediant, GGNet Warnsveld, Yulius Dordrecht and Parnassia psycho-medical center The Hague. Maastricht: Maastricht University Medical Centre and the mental health institutions: GGzE, GGZ Breburg, GGZ Oost-Brabant, Vincent van Gogh voor Geestelijke Gezondheid, Mondriaan, Virenze riagg, Zuyderland GGZ, MET ggz, Universitair Centrum Sint-Jozef Kortenberg, CAPRI University of Antwerp, PC Ziekeren Sint-Truiden, PZ Sancta Maria Sint-Truiden, GGZ Overpelt, OPZ Rekem. Utrecht: University Medical Center Utrecht and the mental health institutions Altrecht, GGZ Centraal and Delta. This work was supported by the Netherlands Organization for Scientific Research (NWO 184.033.111 ), Biobanking and BioMolecular resources Research Infrastructure The Netherlands ( BBMRI-NL2.0 ), and by the ENIGMA World Aging Center grant ( NIH 1R56AG058854-01 , subaward 112068003).

FundersFunder number
CAPRI University of Antwerp
Dutch Health Research Council10-000-1001
ENIGMA World Aging Center
Erasmus Medical Centre
GGZ Noord Holland Noord
Maastricht University Medical Centre
Netherlands Organization for Scientific Research
PZ Sancta Maria Sint-Truiden
Universitair Centrum Sint-Jozef Kortenberg
National Institutes of Health112068003
National Institute on AgingR56AG058854
Erasmus Medisch Centrum
Nederlandse Organisatie voor Wetenschappelijk OnderzoekBBMRI-NL2.0, 184.033.111

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