Prenatal tobacco exposure on brain morphometry partially mediated poor cognitive performance in preadolescent children

Pedro J Rodriguez Rivera; Huajun Liang; Amal Isaiah; Christine C Cloak; Miriam S Menken; Meghann C Ryan; Thomas Ernst; Linda Chang

doi:10.1515/nipt-2023-0013

Prenatal tobacco exposure on brain morphometry partially mediated poor cognitive performance in preadolescent children

NeuroImmune Pharm Ther. 2023 Jul 13;2(4):375-386. doi: 10.1515/nipt-2023-0013. eCollection 2023 Dec.

Authors

Pedro J Rodriguez Rivera¹, Huajun Liang¹, Amal Isaiah^{2

3}, Christine C Cloak¹, Miriam S Menken¹, Meghann C Ryan¹, Thomas Ernst¹, Linda Chang^{1

4

5}

Affiliations

¹ Department of Diagnostic Radiology and Nuclear Medicine, University of Maryland School of Medicine, Baltimore, MD, USA.
² Department of Otorhinolaryngology-Head and Neck Surgery, University of Maryland School of Medicine, Baltimore, MD, USA.
³ Department of Pediatrics, University of Maryland School of Medicine, Baltimore, MD, USA.
⁴ Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, MD, USA.
⁵ Department of Neurology, University of Maryland School of Medicine, Baltimore, MD, USA.

Abstract

Objectives: To evaluate whether prenatal tobacco exposure (PTE) is related to poorer cognitive performance, abnormal brain morphometry, and whether poor cognitive performance is mediated by PTE-related structural brain differences.

Methods: The Adolescent Brain Cognitive Development study dataset was used to compare structural MRI data and neurocognitive (NIH Toolbox^®) scores in 9-to-10-year-old children with (n=620) and without PTE (n=10,989). We also evaluated whether PTE effects on brain morphometry mediated PTE effects on neurocognitive scores. Group effects were evaluated using Linear Mixed Models, covaried for socio-demographics and prenatal exposures to alcohol and/or marijuana, and corrected for multiple comparisons using the false-discovery rate (FDR).

Results: Compared to unexposed children, those with PTE had poorer performance (all p-values <0.05) on executive function, working memory, episodic memory, reading decoding, crystallized intelligence, fluid intelligence and overall cognition. Exposed children also had thinner parahippocampal gyri, smaller surface areas in the posterior-cingulate and pericalcarine cortices; the lingual and inferior parietal gyri, and smaller thalamic volumes (all p-values <0.001). Furthermore, among children with PTE, girls had smaller surface areas in the superior-frontal (interaction-FDR-p=0.01), precuneus (interaction-FDR-p=0.03) and postcentral gyri (interaction-FDR-p=0.02), while boys had smaller putamen volumes (interaction-FDR-p=0.02). Smaller surface areas across regions of the frontal and parietal lobes, and lower thalamic volumes, partially mediated the associations between PTE and poorer neurocognitive scores (p-values <0.001).

Conclusions: Our findings suggest PTE may lead to poorer cognitive performance and abnormal brain morphometry, with sex-specific effects in some brain regions, in pre-adolescent children. The poor cognition in children with PTE may result from the smaller areas and subcortical brain volumes.

Keywords: MRI; cognition; mediation; preadolescent; prenatal tobacco; sex-difference.

Abstract

Grants and funding