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Structural connectivity mediates the relationship between blood oxygenation and cognitive function in sickle cell anemia

Structural connectivity mediates the relationship between blood oxygenation and cognitive function in sickle cell anemia
Structural connectivity mediates the relationship between blood oxygenation and cognitive function in sickle cell anemia
In sickle cell disease (SCD), the relative importance of reduced hemoglobin and peripheral oxygen saturation (SpO2) on brain structure remains uncertain. We applied graph-theoretical analysis to diffusion MRI data to investigate the effect of structural brain connectivity on cognitive function, alongside presence/absence, number and volume of silent cerebral infarction (SCI). In patients, we investigated the relationships between network properties, blood oxygenation and cognition (working memory, WMI, and processing speed, PSI, indices). Based on streamline counts and fractional anisotropy (FA), we identified a subnetwork with weakened connectivity in 92 SCA patients (49 males; 8.0-38.8 years), compared to 54 non-SCA controls (22 males; 6.7-30.6 years). Multiple regression analyses showed a significant effect of hemoglobin on full-network edge density (p<0.05), and of peripheral SpO2 on streamline-weighted subnetwork efficiency (p<0.01). There were effects of FA-weighted full-network and subnetwork efficiency on WMI (both p<0.05), and of streamline-weighted subnetwork efficiency on PSI (p=0.05) but no effects on SCI. Streamline-weighted efficiency was progressively lower with lower SpO2, with a downstream effect on PSI. In path analysis, indirect relationships between blood oxygenation and cognition, mediated by network properties, were better supported than direct alternatives, with an indirect relationship between low SpO2 and PSI in patients, mediated by structural connectivity efficiency in a subnetwork of the brain differing from controls. Our findings are consistent with the notion that cognitive impairment is primarily mediated by hypoxic-ischemic effects on normal-appearing white matter, and highlight the utility of network-based methods in providing biomarkers of cognitive dysfunction in SCA patients.
2473-9529
Clayden, Jonathan D
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Stotesbury, Hanne
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Kawadler, Jamie M
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Slee, April
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Koelbel, Melanie
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Saunders, Dawn E
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Hood, Anna M
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Wilkey, Olu
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Layton, Mark
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Inusa, Baba Pd
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Pelidis, Maria
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Chakravorty, Subarna
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Rees, David C
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Howard, Jo
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Awogbade, Moji
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Liossi, Christina
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Kirkham, Fenella J
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Clark, Chris A
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Clayden, Jonathan D
1f384d07-9591-4dd4-80e0-50244283d314
Stotesbury, Hanne
1104423d-f215-4585-bb50-29b7fdd6c518
Kawadler, Jamie M
425d1643-3623-453a-9db0-6505d8065e70
Slee, April
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Koelbel, Melanie
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Saunders, Dawn E
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Hood, Anna M
aec0f143-3f19-4a0e-b13c-92ecfd3363a5
Wilkey, Olu
adb1eb81-8a3f-4966-820e-2d4d2d78a476
Layton, Mark
f1c49157-82fd-46a6-b308-f993c28f4b91
Inusa, Baba Pd
475127b2-d546-43d9-b4ef-eafbe53d1b12
Pelidis, Maria
8dcd6334-d986-4097-b4a2-e46656001b39
Chakravorty, Subarna
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Rees, David C
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Howard, Jo
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Awogbade, Moji
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Liossi, Christina
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Kirkham, Fenella J
1dfbc0d5-aebe-4439-9fb2-dac6503bcd58
Clark, Chris A
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Clayden, Jonathan D, Stotesbury, Hanne, Kawadler, Jamie M, Slee, April, Koelbel, Melanie, Saunders, Dawn E, Hood, Anna M, Wilkey, Olu, Layton, Mark, Inusa, Baba Pd, Pelidis, Maria, Chakravorty, Subarna, Rees, David C, Howard, Jo, Awogbade, Moji, Liossi, Christina, Kirkham, Fenella J and Clark, Chris A (2022) Structural connectivity mediates the relationship between blood oxygenation and cognitive function in sickle cell anemia. Blood Advances. (doi:10.1182/bloodadvances.2021006751).

Record type: Article

Abstract

In sickle cell disease (SCD), the relative importance of reduced hemoglobin and peripheral oxygen saturation (SpO2) on brain structure remains uncertain. We applied graph-theoretical analysis to diffusion MRI data to investigate the effect of structural brain connectivity on cognitive function, alongside presence/absence, number and volume of silent cerebral infarction (SCI). In patients, we investigated the relationships between network properties, blood oxygenation and cognition (working memory, WMI, and processing speed, PSI, indices). Based on streamline counts and fractional anisotropy (FA), we identified a subnetwork with weakened connectivity in 92 SCA patients (49 males; 8.0-38.8 years), compared to 54 non-SCA controls (22 males; 6.7-30.6 years). Multiple regression analyses showed a significant effect of hemoglobin on full-network edge density (p<0.05), and of peripheral SpO2 on streamline-weighted subnetwork efficiency (p<0.01). There were effects of FA-weighted full-network and subnetwork efficiency on WMI (both p<0.05), and of streamline-weighted subnetwork efficiency on PSI (p=0.05) but no effects on SCI. Streamline-weighted efficiency was progressively lower with lower SpO2, with a downstream effect on PSI. In path analysis, indirect relationships between blood oxygenation and cognition, mediated by network properties, were better supported than direct alternatives, with an indirect relationship between low SpO2 and PSI in patients, mediated by structural connectivity efficiency in a subnetwork of the brain differing from controls. Our findings are consistent with the notion that cognitive impairment is primarily mediated by hypoxic-ischemic effects on normal-appearing white matter, and highlight the utility of network-based methods in providing biomarkers of cognitive dysfunction in SCA patients.

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Accepted/In Press date: 2 July 2022
e-pub ahead of print date: 10 August 2022
Published date: 10 August 2022
Additional Information: Copyright © 2022 American Society of Hematology.

Identifiers

Local EPrints ID: 470250
URI: http://eprints.soton.ac.uk/id/eprint/470250
ISSN: 2473-9529
PURE UUID: 5a602ff4-c04b-43ef-b8d0-cb3d874375eb
ORCID for Christina Liossi: ORCID iD orcid.org/0000-0003-0627-6377
ORCID for Fenella J Kirkham: ORCID iD orcid.org/0000-0002-2443-7958

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Date deposited: 05 Oct 2022 16:34
Last modified: 17 Mar 2024 03:04

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Contributors

Author: Jonathan D Clayden
Author: Hanne Stotesbury
Author: Jamie M Kawadler
Author: April Slee
Author: Melanie Koelbel
Author: Dawn E Saunders
Author: Anna M Hood
Author: Olu Wilkey
Author: Mark Layton
Author: Baba Pd Inusa
Author: Maria Pelidis
Author: Subarna Chakravorty
Author: David C Rees
Author: Jo Howard
Author: Moji Awogbade
Author: Chris A Clark

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