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• Clinical Article •
Analysis of resting-state voxel-mirrored homotopic connectivity in severe obstructive sleep apnea
SHEN Guo  ZHANG Huiyan  GAO Jing  WU Dan  HUANG Gang  ZHANG Wenwen  ZHAO Lianping 

Cite this article as: SHEN G, ZHANG H Y, GAO J, et al. Analysis of resting-state voxel-mirrored homotopic connectivity in severe obstructive sleep apnea[J]. Chin J Magn Reson Imaging, 2023, 14(11): 12-17, 61. DOI:10.12015/issn.1674-8034.2023.11.003.


[Abstract] Objective To utilize the resting-state functional magnetic resonance imaging technology to explore the changes of voxel-mirrored homotopic connectivity (VMHC) in patients with severe obstructive sleep apnea (OSA).Materials and Methods A total of fifty patients with OSA and fifty healthy controls, matched in terms of age, sex, and education, were included in this study. The data of clinical situations, neuropsychological scale assessment and brain magnetic resonance imaging of all participants were further collected. VMHC and the seed-based functional connectivity (FC) were calculated and compared between these two groups. Additionally, Pearson correlation analysis was conducted to examine the relationship between the significant brain areas for VMHC and FC, and the clinical variables and neuropsychological scale scores.Results Compared to control group, patients with severe OSA exhibited lower cognitive scores, and higher depression and anxiety scores. In patients with OSA, the VMHC of the bilateral calcarine and the bilateral superior parietal gyrus was significantly decreased. The FC was found to be abnormal in the bilateral lingual gyrus, right middle occipital gyrus, and left middle temporal gyrus (gaussian random field correction, voxel level P<0.001, cluster level P＜0.05). The VMHC value of bilateral calcarine gyrus in severe OSA patients showed a negative correlation with the apnea hypopnea index (r=-0.31, P=0.027), and a positive correlation with mean blood oxygen saturation (SaO2) (r=0.30, P=0.033). Additionally, the VMHC value of the bilateral superior parietal gyrus was positively correlated with the mean and minimum SaO2 (r=0.29, P=0.039; r=0.31, P=0.028). Furthermore the FC value between the left superior parietal gyrus and the angle gyrus was positively correlated with the mean SaO2 (r=0.29, P=0.041).Conclusions Cognitive function impairment and potential risk of depression and anxiety are observed in severe OSA patients. The alteration of interhemispheric coordination and abnormal FC of the bilateral calcarine and the bilateral superior parietal gyrus may be significant neuropathological mechanisms contributing to cerebral impairments in patients with OSA.
[Keywords] obstructive sleep apnea；resting state magnetic resonance imaging；voxel-mirrored homotopic connectivity；functional connectivity；cognitive dysfunction；emotional abnormalities

SHEN Guo1, 2   ZHANG Huiyan1, 2   GAO Jing3   WU Dan3   HUANG Gang2   ZHANG Wenwen2   ZHAO Lianping2*  

1 School of Clinical Medicine, Ningxia Medical University, Yinchuan 750004, China

2 Department of Radiology, Gansu Provincial Hospital, Lanzhou 730099, China

3 The First Clinical Medical College, Gansu University of Chinese Medicine, Lanzhou 730000, China

Corresponding author: ZHAO L P, E-mail: lianping_zhao007@163.com

Conflicts of interest   None.

ACKNOWLEDGMENTS National Natural Science Foundation of China (No. 81901724); Natural Science Foundation of Gansu Province (No. 21JR7RA593).
Received  2023-06-27
Accepted  2023-10-27
DOI: 10.12015/issn.1674-8034.2023.11.003
Cite this article as: SHEN G, ZHANG H Y, GAO J, et al. Analysis of resting-state voxel-mirrored homotopic connectivity in severe obstructive sleep apnea[J]. Chin J Magn Reson Imaging, 2023, 14(11): 12-17, 61. DOI:10.12015/issn.1674-8034.2023.11.003.

[1]
LEE M H, YUN C H, MIN A, et al. Altered structural brain network resulting from white matter injury in obstructive sleep apnea[J/OL]. Sleep, 2019, 42(9): zsz120 [2023-06-27]. https://pubmed.ncbi.nlm.nih.gov/31260533/. DOI: 10.1093/sleep/zsz120.
[2]
SENARATNA C V, PERRET J L, LODGE C J, et al. Prevalence of obstructive sleep apnea in the general population: a systematic review[J/OL]. Sleep Med Rev, 2017, 34: 70-81 [2023-06-27]. https://pubmed.ncbi.nlm.nih.gov/27568340/. DOI: 10.1016/j.smrv.2016.07.002.
[3]
SWEED R A, HASSAN S, ELWAHAB N H A, et al. Comorbidities associated with obstructive sleep apnea: a retrospective Egyptian study on 244 patients[J]. Sleep Breath, 2019, 23(4): 1079-1085. DOI: 10.1007/s11325-019-01783-w.
[4]
WANG J F, FANG J R, XIE Y P, et al. Research on the effects of CPAP for OSA combined CHD long-term prognosis[J]. J Clin Otorhinolaryngol Head Neck Surg, 2019, 33(11): 1031-1035, 1039. DOI: 10.13201/j.issn.1001-1781.2019.11.006.
[5]
WU Y, ZHAO W R, CHEN X Y, et al. Aberrant awake spontaneous brain activity in obstructive sleep apnea: a review focused on resting-state EEG and resting-state fMRI[J/OL]. Front Neurol, 2020, 11: 768 [2023-06-27]. https://pubmed.ncbi.nlm.nih.gov/32849223/. DOI: 10.3389/fneur.2020.00768.
[6]
LAM A, HAROUTONIAN C, GRUMMITT L, et al. Sleep-dependent memory in older people with and without MCI: the relevance of sleep microarchitecture, OSA, hippocampal subfields, and episodic memory[J]. Cereb Cortex, 2021, 31(6): 2993-3005. DOI: 10.1093/cercor/bhaa406.
[7]
BARIL A A, MARTINEAU-DUSSAULT M È, SANCHEZ E, et al. Obstructive sleep apnea and the brain: a focus on gray and white matter structure[J/OL]. Curr Neurol Neurosci Rep, 2021, 21(3): 11 [2023-06-27]. https://pubmed.ncbi.nlm.nih.gov/33586028/. DOI: 10.1007/s11910-021-01094-2.
[8]
BARIL A A, CARRIER J, LAFRENIÈRE A, et al. Biomarkers of dementia in obstructive sleep apnea[J/OL]. Sleep Med Rev, 2018, 42: 139-148 [2023-06-27]. https://pubmed.ncbi.nlm.nih.gov/30241998/. DOI: 10.1016/j.smrv.2018.08.001.
[9]
ZHOU L, SHAN X X, PENG Y T, et al. Reduced regional homogeneity and neurocognitive impairment in patients with moderate-to-severe obstructive sleep apnea[J/OL]. Sleep Med, 2020, 75: 418-427 [2023-06-27]. https://pubmed.ncbi.nlm.nih.gov/32980663/. DOI: 10.1016/j.sleep.2020.09.009.
[10]
CHEN T, YANG M, LIU B, et al. Regional homogeneity changes in patients with obstructive sleep apnea-hypopnea syndrome: resting-state functional MRI study[J]. Natl Med J China, 2016, 96(11): 868-873. DOI: 10.3760/cma.j.issn.0376-2491.2016.11.009.
[11]
LI H J, DAI X J, GONG H H, et al. Aberrant spontaneous low-frequency brain activity in male patients with severe obstructive sleep apnea revealed by resting-state functional MRI[J/OL]. Neuropsychiatr Dis Treat, 2015, 11: 207-214 [2023-06-27]. https://pubmed.ncbi.nlm.nih.gov/25653530/. DOI: 10.2147/NDT.S73730.
[12]
DUAN W W, LIU X, PING L L, et al. Distinct functional brain abnormalities in insomnia disorder and obstructive sleep apnea[J]. Eur Arch Psychiatry Clin Neurosci, 2023, 273(2): 493-509. DOI: 10.1007/s00406-022-01485-7.
[13]
LIU X, SHU Y Q, YU P F, et al. Classification of severe obstructive sleep apnea with cognitive impairment using degree centrality: a machine learning analysis[J/OL]. Front Neurol, 2022, 13: 1005650 [2023-06-27]. https://pubmed.ncbi.nlm.nih.gov/36090863/. DOI: 10.3389/fneur.2022.1005650.
[14]
GAO J, TIAN J, HUANG G, et al. Study on the change of resting state degree centrality and correlation in patients with obstructive sleep apnea[J]. Chin J Magn Reson Imag, 2022, 13(4): 79-83, 88. DOI: 10.12015/issn.1674-8034.2022.04.014.
[15]
PARK H R, CHA J, JOO E Y, et al. Altered cerebrocerebellar functional connectivity in patients with obstructive sleep apnea and its association with cognitive function[J/OL]. Sleep, 2022, 45(1): zsab209 [2023-06-27]. https://pubmed.ncbi.nlm.nih.gov/34432059/. DOI: 10.1093/sleep/zsab209.
[16]
LIU X, CHEN L T, DUAN W F, et al. Abnormal functional connectivity of hippocampal subdivisions in obstructive sleep apnea: a resting-state functional magnetic resonance imaging study[J/OL]. Front Neurosci, 2022, 16: 850940 [2023-06-27]. https://pubmed.ncbi.nlm.nih.gov/35546892/. DOI: 10.3389/fnins.2022.850940.
[17]
CUI Y, TANG T Y, LU C Q, et al. Disturbed interhemispheric functional and structural connectivity in type 2 diabetes[J]. J Magn Reson Imaging, 2022, 55(2): 424-434. DOI: 10.1002/jmri.27813.
[18]
ZUO X N, KELLY C, DI MARTINO A, et al. Growing together and growing apart: regional and sex differences in the lifespan developmental trajectories of functional homotopy[J]. J Neurosci, 2010, 30(45): 15034-15043. DOI: 10.1523/JNEUROSCI.2612-10.2010.
[19]
MUBASHIR T, ABRAHAMYAN L, NIAZI A, et al. The prevalence of obstructive sleep apnea in mild cognitive impairment: a systematic review[J/OL]. BMC Neurol, 2019, 19(1): 195 [2023-06-27]. https://pubmed.ncbi.nlm.nih.gov/31416438/. DOI: 10.1186/s12883-019-1422-3.
[20]
GOSSELIN N, BARIL A A, OSORIO R S, et al. Obstructive sleep apnea and the risk of cognitive decline in older adults[J]. Am J Respir Crit Care Med, 2019, 199(2): 142-148. DOI: 10.1164/rccm.201801-0204PP.
[21]
GARBARINO S, BARDWELL W A, GUGLIELMI O, et al. Association of anxiety and depression in obstructive sleep apnea patients: a systematic review and meta-analysis[J]. Behav Sleep Med, 2020, 18(1): 35-57. DOI: 10.1080/15402002.2018.1545649.
[22]
MOK Y, MELEHAN K L, PHILLIPS C L, et al. Does CPAP treat depressive symptoms in individuals with OSA? An analysis of two 12-week randomized sham CPAP-controlled trials[J/OL]. Sleep Med, 2020, 73: 11-14 [2023-06-27]. https://pubmed.ncbi.nlm.nih.gov/32769027/. DOI: 10.1016/j.sleep.2020.04.021.
[23]
BJORVATN B, RAJAKULENDREN N, LEHMANN S, et al. Increased severity of obstructive sleep apnea is associated with less anxiety and depression[J/OL]. J Sleep Res, 2018, 27(6): e12647 [2023-06-27]. https://pubmed.ncbi.nlm.nih.gov/29193447/. DOI: 10.1111/jsr.12647.
[24]
RAVINDRAN S, KURIAN G A. Addressing the alterations in cerebral ischemia-reperfusion injury on the brain mitochondrial activity: a possible link to cognitive decline[J]. Biochem Biophys Res Commun, 2019, 518(1): 100-106. DOI: 10.1016/j.bbrc.2019.08.014.
[25]
DEWAN N A, NIETO F J, SOMERS V K. Intermittent hypoxemia and OSA: implications for comorbidities[J]. Chest, 2015, 147(1): 266-274. DOI: 10.1378/chest.14-0500.
[26]
LV R J, LIU X Y, ZHANG Y, et al. Pathophysiological mechanisms and therapeutic approaches in obstructive sleep apnea syndrome[J/OL]. Signal Transduct Target Ther, 2023, 8(1): 218 [2023-06-27]. https://pubmed.ncbi.nlm.nih.gov/37230968/. DOI: 10.1038/s41392-023-01496-3.
[27]
REDLINE S, AZARBARZIN A, PEKER Y. Obstructive sleep apnoea heterogeneity and cardiovascular disease[J]. Nat Rev Cardiol, 2023, 20(8): 560-573. DOI: 10.1038/s41569-023-00846-6.
[28]
LIGUORI C, MERCURI N B, IZZI F, et al. Obstructive sleep apnea is associated with early but possibly modifiable Alzheimer's disease biomarkers changes[J/OL]. Sleep, 2017, 40(5) [2023-06-27]. https://pubmed.ncbi.nlm.nih.gov/28329084/. DOI: 10.1093/sleep/zsx011.
[29]
DAKTERZADA F, BENÍTEZ I D, TARGA A, et al. Blood-based lipidomic signature of severe obstructive sleep apnoea in Alzheimer's disease[J/OL]. Alzheimers Res Ther, 2022, 14(1): 163 [2023-06-27]. https://pubmed.ncbi.nlm.nih.gov/36329512/. DOI: 10.1186/s13195-022-01102-8.
[30]
AMAEFULE C O, DYRBA M, WOLFSGRUBER S, et al. Association between composite scores of domain-specific cognitive functions and regional patterns of atrophy and functional connectivity in the Alzheimer's disease spectrum[J/OL]. Neuroimage Clin, 2021, 29: 102533 [2023-06-27]. https://pubmed.ncbi.nlm.nih.gov/33360018/. DOI: 10.1016/j.nicl.2020.102533.
[31]
YANG Y, WEI K, ZHANG H C, et al. Identifying functional brain abnormalities in migraine and depression comorbidity[J]. Quant Imaging Med Surg, 2022, 12(4): 2288-2302. DOI: 10.21037/qims-21-667.
[32]
SHU Y Q, LIU X, YU P F, et al. Inherent regional brain activity changes in male obstructive sleep apnea with mild cognitive impairment: a resting-state magnetic resonance study[J/OL]. Front Aging Neurosci, 2022, 14: 1022628 [2023-06-27]. https://pubmed.ncbi.nlm.nih.gov/36389072/. DOI: 10.3389/fnagi.2022.1022628.
[33]
GIORA E, GALBIATI A, MARELLI S, et al. Evidence of perceptive impairment in OSA patients investigated by means of a visual search task[J/OL]. Cortex, 2017, 95: 136-142 [2023-06-27]. https://pubmed.ncbi.nlm.nih.gov/28869823/. DOI: 10.1016/j.cortex.2017.08.004.
[34]
HUANG J, BEACH P, BOZOKI A, et al. Alzheimer's disease progressively reduces visual functional network connectivity[J]. J Alzheimers Dis Rep, 2021, 5(1): 549-562. DOI: 10.3233/ADR-210017.
[35]
QIN Z Y, BAO H H, KANG D J, et al. ReHo and ALFF studies in the brain of patients with obstructive sleep apnea hypopnea syndrome[J]. Chin J Magn Reson Imag, 2018, 9(9): 648-654. DOI: 10.12015/issn.1674-8034.2018.09.002.
[36]
ROCKLAND K S, GRAVES W W. The angular gyrus: a special issue on its complex anatomy and function[J]. Brain Struct Funct, 2023, 228(1): 1-5. DOI: 10.1007/s00429-022-02596-6.
[37]
PENG D C, DAI X J, GONG H H, et al. Altered intrinsic regional brain activity in male patients with severe obstructive sleep apnea: a resting-state functional magnetic resonance imaging study[J/OL]. Neuropsychiatr Dis Treat, 2014, 10: 1819-1826 [2023-06-27]. https://pubmed.ncbi.nlm.nih.gov/25278755/. DOI: 10.2147/NDT.S67805.
[38]
ZENG Y P, SHU Y Q, LIU X, et al. Frequency-specific alterations in intrinsic low-frequency oscillations in newly diagnosed male patients with obstructive sleep apnea[J/OL]. Front Neurosci, 2022, 16: 987015 [2023-06-27]. https://pubmed.ncbi.nlm.nih.gov/36248662/. DOI: 10.3389/fnins.2022.987015.
[39]
SUN Y F, YANG S X, XIE M, et al. Aberrant amplitude of low-frequency fluctuations in different frequency bands and changes after one-night positive airway pressure treatment in severe obstructive sleep apnea[J/OL]. Front Neurol, 2022, 13: 985321 [2023-06-27]. https://pubmed.ncbi.nlm.nih.gov/36071907/. DOI: 10.3389/fneur.2022.985321.
[40]
CHOKESUWATTANASKUL A, CHIRAKALWASAN N, JAIMCHARIYATAM N, et al. Associations between hypoxia parameters in obstructive sleep apnea and cognition, cortical thickness, and white matter integrity in middle-aged and older adults[J]. Sleep Breath, 2021, 25(3): 1559-1570. DOI: 10.1007/s11325-020-02215-w.
[41]
LI H J, LI L, SHAO Y, et al. Abnormal intrinsic functional hubs in severe male obstructive sleep apnea: evidence from a voxel-wise degree centrality analysis[J/OL]. PLoS One, 2016, 11(10): e0164031 [2023-06-27]. https://pubmed.ncbi.nlm.nih.gov/27723821/. DOI: 10.1371/journal.pone.0164031.

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