Brain network hypersensitivity underlies pain crises in sickle cell disease

Abstract Sickle cell disease (SCD) is a genetic disorder causing painful and unpredictable Vaso-occlusive crises (VOCs) through blood vessel blockages. In this study, we propose explosive synchronization (ES) as a novel approach to comprehend the hypersensitivity and occurrence of VOCs in the SCD br...

Full description

Bibliographic Details
Main Authors: Pangyu Joo, Minkyung Kim, Brianna Kish, Vidhya Vijayakrishnan Nair, Yunjie Tong, Ziyue Liu, Andrew R. W. O’Brien, Steven E. Harte, Richard E. Harris, UnCheol Lee, Ying Wang
Format: Article
Language:English
Published: Nature Portfolio 2024-03-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-024-57473-5
_version_ 1827301178670579712
author Pangyu Joo
Minkyung Kim
Brianna Kish
Vidhya Vijayakrishnan Nair
Yunjie Tong
Ziyue Liu
Andrew R. W. O’Brien
Steven E. Harte
Richard E. Harris
UnCheol Lee
Ying Wang
author_facet Pangyu Joo
Minkyung Kim
Brianna Kish
Vidhya Vijayakrishnan Nair
Yunjie Tong
Ziyue Liu
Andrew R. W. O’Brien
Steven E. Harte
Richard E. Harris
UnCheol Lee
Ying Wang
author_sort Pangyu Joo
collection DOAJ
description Abstract Sickle cell disease (SCD) is a genetic disorder causing painful and unpredictable Vaso-occlusive crises (VOCs) through blood vessel blockages. In this study, we propose explosive synchronization (ES) as a novel approach to comprehend the hypersensitivity and occurrence of VOCs in the SCD brain network. We hypothesized that the accumulated disruptions in the brain network induced by SCD might lead to strengthened ES and hypersensitivity. We explored ES's relationship with patient reported outcome measures (PROMs) as well as VOCs by analyzing EEG data from 25 SCD patients and 18 matched controls. SCD patients exhibited lower alpha frequency than controls. SCD patients showed correlation between frequency disassortativity (FDA), an ES condition, and three important PROMs. Furthermore, stronger FDA was observed in SCD patients with a higher frequency of VOCs and EEG recording near VOC. We also conducted computational modeling on SCD brain network to study FDA's role in network sensitivity. Our model demonstrated that a stronger FDA could be linked to increased sensitivity and frequency of VOCs. This study establishes connections between SCD pain and the universal network mechanism, ES, offering a strong theoretical foundation. This understanding will aid predicting VOCs and refining pain management for SCD patients.
first_indexed 2024-04-24T16:18:40Z
format Article
id doaj.art-6ec4a414d51445dba80383c2da802b56
institution Directory Open Access Journal
issn 2045-2322
language English
last_indexed 2024-04-24T16:18:40Z
publishDate 2024-03-01
publisher Nature Portfolio
record_format Article
series Scientific Reports
spelling doaj.art-6ec4a414d51445dba80383c2da802b562024-03-31T11:19:47ZengNature PortfolioScientific Reports2045-23222024-03-0114111310.1038/s41598-024-57473-5Brain network hypersensitivity underlies pain crises in sickle cell diseasePangyu Joo0Minkyung Kim1Brianna Kish2Vidhya Vijayakrishnan Nair3Yunjie Tong4Ziyue Liu5Andrew R. W. O’Brien6Steven E. Harte7Richard E. Harris8UnCheol Lee9Ying Wang10Department of Anesthesiology, Center for Consciousness Science, Center for the Study of Complex Systems, Michigan Psychedelic Center, University of MichiganDepartment of Anesthesiology, Center for Consciousness Science, Center for the Study of Complex Systems, Michigan Psychedelic Center, University of MichiganWeldon School of Biomedical Engineering, Purdue UniversityWeldon School of Biomedical Engineering, Purdue UniversityWeldon School of Biomedical Engineering, Purdue UniversityIndiana Center for Musculoskeletal Health, Indiana UniversityDivision of Hematology/Oncology, Department of Medicine, Indiana University School of MedicineDepartment of Anesthesiology, Chronic Pain and Fatigue Research Center, University of MichiganDepartment of Anesthesiology, Chronic Pain and Fatigue Research Center, University of MichiganDepartment of Anesthesiology, Center for Consciousness Science, Center for the Study of Complex Systems, Michigan Psychedelic Center, University of MichiganDivision of Hematology/Oncology, Department of Medicine, Indiana University School of MedicineAbstract Sickle cell disease (SCD) is a genetic disorder causing painful and unpredictable Vaso-occlusive crises (VOCs) through blood vessel blockages. In this study, we propose explosive synchronization (ES) as a novel approach to comprehend the hypersensitivity and occurrence of VOCs in the SCD brain network. We hypothesized that the accumulated disruptions in the brain network induced by SCD might lead to strengthened ES and hypersensitivity. We explored ES's relationship with patient reported outcome measures (PROMs) as well as VOCs by analyzing EEG data from 25 SCD patients and 18 matched controls. SCD patients exhibited lower alpha frequency than controls. SCD patients showed correlation between frequency disassortativity (FDA), an ES condition, and three important PROMs. Furthermore, stronger FDA was observed in SCD patients with a higher frequency of VOCs and EEG recording near VOC. We also conducted computational modeling on SCD brain network to study FDA's role in network sensitivity. Our model demonstrated that a stronger FDA could be linked to increased sensitivity and frequency of VOCs. This study establishes connections between SCD pain and the universal network mechanism, ES, offering a strong theoretical foundation. This understanding will aid predicting VOCs and refining pain management for SCD patients.https://doi.org/10.1038/s41598-024-57473-5
spellingShingle Pangyu Joo
Minkyung Kim
Brianna Kish
Vidhya Vijayakrishnan Nair
Yunjie Tong
Ziyue Liu
Andrew R. W. O’Brien
Steven E. Harte
Richard E. Harris
UnCheol Lee
Ying Wang
Brain network hypersensitivity underlies pain crises in sickle cell disease
Scientific Reports
title Brain network hypersensitivity underlies pain crises in sickle cell disease
title_full Brain network hypersensitivity underlies pain crises in sickle cell disease
title_fullStr Brain network hypersensitivity underlies pain crises in sickle cell disease
title_full_unstemmed Brain network hypersensitivity underlies pain crises in sickle cell disease
title_short Brain network hypersensitivity underlies pain crises in sickle cell disease
title_sort brain network hypersensitivity underlies pain crises in sickle cell disease
url https://doi.org/10.1038/s41598-024-57473-5
work_keys_str_mv AT pangyujoo brainnetworkhypersensitivityunderliespaincrisesinsicklecelldisease
AT minkyungkim brainnetworkhypersensitivityunderliespaincrisesinsicklecelldisease
AT briannakish brainnetworkhypersensitivityunderliespaincrisesinsicklecelldisease
AT vidhyavijayakrishnannair brainnetworkhypersensitivityunderliespaincrisesinsicklecelldisease
AT yunjietong brainnetworkhypersensitivityunderliespaincrisesinsicklecelldisease
AT ziyueliu brainnetworkhypersensitivityunderliespaincrisesinsicklecelldisease
AT andrewrwobrien brainnetworkhypersensitivityunderliespaincrisesinsicklecelldisease
AT steveneharte brainnetworkhypersensitivityunderliespaincrisesinsicklecelldisease
AT richardeharris brainnetworkhypersensitivityunderliespaincrisesinsicklecelldisease
AT uncheollee brainnetworkhypersensitivityunderliespaincrisesinsicklecelldisease
AT yingwang brainnetworkhypersensitivityunderliespaincrisesinsicklecelldisease