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Cerebral perfusion in Parkinson's disease with depression: An arterial spin labeling MRI study
LI Xinyang  TIAN Yaotian  WANG Xiaonan  SU Wen  LI Shuhua  MA Xinxin  LI Chunmei  CHEN Min 

Cite this article as: LI X Y, TIAN Y T, WANG X N, et al. Cerebral perfusion in Parkinson’s disease with depression: An arterial spin labeling MRI study[J]. Chin J Magn Reson Imaging, 2023, 14(1): 6-12. DOI:10.12015/issn.1674-8034.2023.01.002.


[Abstract] Objective To explore the cerebral perfusion alteration in Parkinson's disease (PD) with depression and to investigate the associations of these alteration with depression.Materials and Methods A total of 34 PD patients [19 Parkinson's disease without depression (PD-n) patients, 15 Parkinson's disease with depression (PD-d) patients] and 30 sex-age matched normal controls (NC) were enrolled from September 2021 to July 2022. The depressive symptom was defined according to the Hamilton Depression Rating Scale (HAMD). T1-weighted magnetization-prepared rapid acquisition gradient echo (T1 MPRAGE) and pseudo-continuous arterial spin labeling (pCASL) imaging were performed. SPM12 based on MATLAB were used for data processing to generate quantitative cerebral blood flow (CBF) values of each brain region. Independent samples t-test was used to compare regional CBF between PD group and NC group, PD-n group and PD-d group, controlled by false discovery rate correction. The associations between the HAMD score and CBF values of the brain were investigated using partial correlations.Results Compared with the NC group, cerebral blood flow of the right putamen, right hippocampus, right insula and the bilateral parietal lobe, occipital lobe, temporal lobe gray matter and white matter was significantly lower in the PD group (P<0.05). Cerebral blood flow of the left thalamus, left hippocampus, right cingulate gyrus and the bilateral parietal gray matter, the bilateral occipital white matter was significantly lower in the PD-d group compared with the PD-n group (P<0.05). Additionally, the CBF value of the right occipital white matter (r=-0.370, P=0.034) and the right cingulate gyrus (r=-0.410, P=0.018) was negative correlated with the HAMD score.Conclusions The arterial spin labeling MRI was used to observe the changes of cerebral perfusion in PD patients, and the hypoperfusion of PD patients in several brain regions may be one of the basic characteristics. Besides, there is a correlation between decreased cerebral perfusion of limbic system and PD with depression.
[Keywords] Parkinson's disease;depression;magnetic resonance imaging;arterial spin labeling;cerebral blood flow

LI Xinyang1, 2   TIAN Yaotian1, 2   WANG Xiaonan1, 2   SU Wen3   LI Shuhua3   MA Xinxin3   LI Chunmei1, 2*   CHEN Min1, 2  

1 Department of Radiology, Beijing Hospital, National Center of Gerontology, Institute of Geriatric Medicine, Chinese Academy of Medical Sciences, Beijing 100730, China

2 Graduate School of Peking Union Medical College, Chinese Academy of Medical Sciences Beijing 100730, China

3 Department of Neurology, Beijing Hospital, National Center of Gerontology, Institute of Geriatric Medicine, Chinese Academy of Medical Sciences, Beijing 100730, China

Corresponding author: Li CM, E-mail: bee9020@126.com

Conflicts of interest   None.

ACKNOWLEDGMENTS National Natural Science Foundation of China (No. 82071891).
Received  2022-09-20
Accepted  2022-12-30
DOI: 10.12015/issn.1674-8034.2023.01.002
Cite this article as: LI X Y, TIAN Y T, WANG X N, et al. Cerebral perfusion in Parkinson’s disease with depression: An arterial spin labeling MRI study[J]. Chin J Magn Reson Imaging, 2023, 14(1): 6-12. DOI:10.12015/issn.1674-8034.2023.01.002.

[1]
QI S, YIN P, WANG L, et al. Prevalence of Parkinson's Disease: A Community-Based Study in China[J]. Mov Disord, 2021, 36(12): 2940-2944. DOI: 10.1002/mds.28762.
[2]
BLOEM B R, OKUN M S, KLEIN C. Parkinson's disease[J]. Lancet, 2021, 397(10291): 2284-2303. DOI: 10.1016/s0140-6736(21)00218-x.
[3]
GULUNAY A, CAKMAKLI G Y, YON M I, et al. Frequency of non-motor symptoms and their impact on the quality of life in patients with Parkinson's disease: a prospective descriptive case series[J]. Psychogeriatrics, 2020, 20(2): 206-211. DOI: 10.1111/psyg.12489.
[4]
SEPPI K, CHAUDHURI K RAY, COELHO M, et al. Update on treatments for nonmotor symptoms of Parkinson's disease-an evidence-based medicine review[J]. Mov Disord, 2019, 34(2): 180-198. DOI: 10.1002/mds.27602.
[5]
TSAI W C, LIN H C, CHANG C C, et al. Neuropsychiatric symptoms in Parkinson's disease: association with caregiver distress and disease severity[J]. Int Psychogeriatr, 2020, 32(6): 733-739. DOI: 10.1017/s1041610219001510.
[6]
JONES J D, KURNIADI N E, KUHN T P, et al. Depressive symptoms precede cognitive impairment in de novo Parkinson's disease patients: Analysis of the PPMI cohort[J]. Neuropsychology, 2019, 33(8): 1111-1120. DOI: 10.1037/neu0000583.
[7]
STORCH A, EBERSBACH G, FUCHS G, et al. Depression in Parkinson's disease. Part 1: epidemiology, signs and symptoms, pathophysiology and diagnosis[J]. Fortschr Neurol Psychiatr, 2008, 76(12): 715-724. DOI: 10.1055/s-2008-1038293.
[8]
PRANGE S, KLINGER H, LAURENCIN C, et al. Depression in Patients with Parkinson's Disease: Current Understanding of its Neurobiology and Implications for Treatment[J]. Drugs Aging, 2022, 39(6): 417-439. DOI: 10.1007/s40266-022-00942-1.
[9]
JEZZARD P, CHAPPELL M A, OKELL T W. Arterial spin labeling for the measurement of cerebral perfusion and angiography[J]. J Cereb Blood Flow Metab, 2018, 38(4): 603-626. DOI: 10.1177/0271678x17743240.
[10]
DUHAMEAU B, FERRÉ J C, JANNIN P, et al. Chronic and treatment-resistant depression: a study using arterial spin labeling perfusion MRI at 3Tesla[J]. Psychiatry Res, 2010, 182(2): 111-116. DOI: 10.1016/j.pscychresns.2010.01.009.
[11]
MATSUI H, NISHINAKA K, ODA M, et al. Minor depression and brain perfusion images in Parkinson's disease[J]. Mov Disord, 2006, 21(8): 1169-1174. DOI: 10.1002/mds.20923.
[12]
Parkinson's Disease and Movement Disorders Study Group of Neurology Branch of Chinese Medical Association, Parkinson's disease and Movement Disorders Professional Committee of Neurophysicians Branch of Chinese Medical Doctor Association. Diagnostic criteria of Parkinson's disease in China[J]. Chin J Urol, 2016, 49(4): 268-271. DOI: 10.3760/cma.j.issn.1006‐7876.2016.04.002.
[13]
Parkinson's Disease and Movement Disorders Study Group of Neurology Branch of Chinese Medical Association, Parkinson's Disease and Movement Disorders Study Group of Neurophysicist Branch of Chinese Medical Doctor Association, Neuropsychology and Behavioral Neurology Disorders Study Group of Neurology Branch of Chinese Medical Association. The diagnostic criteria and treatment guideline for Parkinson's disease dementia (second version)[J]. Chin J Urol, 2021, 54(8): 762-771. DOI: 10.3760/cma.j.cn113694-20210130-00078.
[14]
STARKSTEIN S, DRAGOVIC M, JORGE R, et al. Diagnostic criteria for depression in Parkinson's disease: a study of symptom patterns using latent class analysis[J]. Mov Disord, 2011, 26(12): 2239-2245. DOI: 10.1002/mds.23836.
[15]
SCHMITTER D, ROCHE A, MARÉCHAL B, et al. An evaluation of volume-based morphometry for prediction of mild cognitive impairment and Alzheimer's disease[J]. Neuroimage Clin, 2015, 7: 7-17. DOI: 10.1016/j.nicl.2014.11.001.
[16]
BUXTON R B, FRANK L R, WONG E C, et al. A general kinetic model for quantitative perfusion imaging with arterial spin labeling[J]. Magn Reson Med, 1998, 40(3): 383-396. DOI: 10.1002/mrm.1910400308.
[17]
WANG J, LI R, LIU M, et al. Impaired cerebral hemodynamics in late-onset depression: computed tomography angiography, computed tomography perfusion, and magnetic resonance imaging evaluation[J]. Quant Imaging Med Surg, 2020, 10(9): 1763-1774. DOI: 10.21037/qims-19-402.
[18]
RITTER C, BUCHMANN A, MÜLLER S T, et al. Cerebral perfusion in depression: Relationship to sex, dehydroepiandrosterone sulfate and depression severity[J/OL]. Neuroimage Clin, 2021, 32: 102840 [2022-09-19]. https://pubmed.ncbi.nlm.nih.gov/34628302/. DOI: 10.1016/j.nicl.2021.102840.
[19]
KILROY E, APOSTOLOVA L, LIU C, et al. Reliability of two-dimensional and three-dimensional pseudo-continuous arterial spin labeling perfusion MRI in elderly populations: comparison with 15O-water positron emission tomography[J]. J Magn Reson Imaging, 2014, 39(4): 931-939. DOI: 10.1002/jmri.24246.
[20]
RIEDERER I, BOHN K P, PREIBISCH C, et al. Alzheimer Disease and Mild Cognitive Impairment: Integrated Pulsed Arterial Spin-Labeling MRI and 18F-FDG PET[J]. Radiology, 2018, 288(1): 198-206. DOI: 10.1148/radiol.2018170575.
[21]
LIN W C, CHEN P C, HUANG C C, et al. Autonomic Function Impairment and Brain Perfusion Deficit in Parkinson's Disease[J/OL]. Front Neurol, 2017, 8: 246 [2022-09-19]. https://pubmed.ncbi.nlm.nih.gov/28642732/. DOI: 10.3389/fneur.2017.00246.
[22]
RANE S, KOH N, OAKLEY J, et al. Arterial spin labeling detects perfusion patterns related to motor symptoms in Parkinson's disease[J]. Parkinsonism Relat Disord, 2020, 76: 21-28. DOI: 10.1016/j.parkreldis.2020.05.014.
[23]
MELZER T R, WATTS R, MACASKILL M R, et al. Arterial spin labelling reveals an abnormal cerebral perfusion pattern in Parkinson's disease[J]. Brain, 2011, 134(Pt 3): 845-855. DOI: 10.1093/brain/awq377.
[24]
TEUNE L K, RENKEN R J, DE JONG B M, et al. Parkinson's disease-related perfusion and glucose metabolic brain patterns identified with PCASL-MRI and FDG-PET imaging[J]. Neuroimage Clin, 2014, 5: 240-244. DOI: 10.1016/j.nicl.2014.06.007.
[25]
ZHANG Q, WEBER M A, NARAYANAN N S. Medial prefrontal cortex and the temporal control of action[J]. Int Rev Neurobiol, 2021, 158: 421-441. DOI: 10.1016/bs.irn.2020.11.004.
[26]
THOTA N, LENKA A, GEORGE L, et al. Impaired frontal lobe functions in patients with Parkinson's disease and psychosis[J]. Asian J Psychiatr, 2017, 30: 192-195. DOI: 10.1016/j.ajp.2017.10.013.
[27]
SYRIMI Z J, VOJTISEK L, ELIASOVA I, et al. Arterial spin labelling detects posterior cortical hypoperfusion in non-demented patients with Parkinson's disease[J]. J Neural Transm (Vienna), 2017, 124(5): 551-557. DOI: 10.1007/s00702-017-1703-1.
[28]
SUO X, LEI D, CHENG L, et al. Multidelay multiparametric arterial spin labeling perfusion MRI and mild cognitive impairment in early stage Parkinson's disease[J]. Hum Brain Mapp, 2019, 40(4): 1317-1327. DOI: 10.1002/hbm.24451.
[29]
PELIZZARI L, DI TELLA S, ROSSETTO F, et al. Parietal Perfusion Alterations in Parkinson's Disease Patients Without Dementia[J/OL]. Front Neurol, 2020, 11: 562 [2022-09-19]. https://pubmed.ncbi.nlm.nih.gov/32655485/. DOI: 10.3389/fneur.2020.00562.
[30]
KONG X Z, MATHIAS S R, GUADALUPE T, et al. Mapping cortical brain asymmetry in 17,141 healthy individuals worldwide via the ENIGMA Consortium[J/OL]. Proc Natl Acad Sci U S A, 2018, 115(22): E5154-E5163 [2022-09-19]. https://pubmed.ncbi.nlm.nih.gov/29764998/. DOI: 10.1073/pnas.1718418115.
[31]
YAZBEK S, HAGE S, MALLAK I, et al. Tractography of the arcuate fasciculus in healthy right-handed and left-handed multilingual subjects and its relation to language lateralization on functional MRI[J/OL]. Sci Rep, 2021, 11(1): 20936 [2022-09-19]. https://pubmed.ncbi.nlm.nih.gov/34686728/. DOI: 10.1038/s41598-021-00490-5.
[32]
HERSHEY T, BLACK K J, CARL J L, et al. Long term treatment and disease severity change brain responses to levodopa in Parkinson's disease[J]. J Neurol Neurosurg Psychiatry, 2003, 74(7): 844-851. DOI: 10.1136/jnnp.74.7.844.
[33]
XIONG Y, JI L, HE L, et al. Effects of Levodopa Therapy on Cerebral Arteries and Perfusion in Parkinson's Disease Patients[J]. J Magn Reson Imaging, 2022, 55(3): 943-953. DOI: 10.1002/jmri.27903.
[34]
DISSANAYAKA N N, O'SULLIVAN J D, SILBURN P A, et al. Assessment methods and factors associated with depression in Parkinson's disease[J]. J Neurol Sci, 2011, 310(1-2): 208-210. DOI: 10.1016/j.jns.2011.06.031.
[35]
IMAMURA K, OKAYASU N, NAGATSU T. The relationship between depression and regional cerebral blood flow in Parkinson's disease and the effect of selegiline treatment[J]. Acta Neurol Scand, 2011, 124(1): 28-39. DOI: 10.1111/j.1600-0404.2010.01443.x.
[36]
KIM Y D, JEONG H S, SONG I U, et al. Brain perfusion alterations in depressed patients with Parkinson's disease[J]. Ann Nucl Med, 2016, 30(10): 731-737. DOI: 10.1007/s12149-016-1119-2.
[37]
MENTIS M J, MCINTOSH A R, PERRINE K, et al. Relationships among the metabolic patterns that correlate with mnemonic, visuospatial, and mood symptoms in Parkinson's disease[J]. Am J Psychiatry, 2002, 159(5): 746-754. DOI: 10.1176/appi.ajp.159.5.746.
[38]
VAN AALST J, DEVROME M, VAN WEEHAEGHE D, et al. Regional glucose metabolic decreases with ageing are associated with microstructural white matter changes: a simultaneous PET/MR study[J]. Eur J Nucl Med Mol Imaging, 2022, 49(2): 664-680. DOI: 10.1007/s00259-021-05518-6.
[39]
DI PAOLA M, PHILLIPS O, ORFEI M D, et al. Corpus Callosum Structure is Topographically Correlated with the Early Course of Cognition and Depression in Alzheimer's Disease[J]. J Alzheimers Dis, 2015, 45(4): 1097-1108. DOI: 10.3233/jad-142895.
[40]
LIU Z, ZHANG Y, WANG H, et al. Altered cerebral perfusion and microstructure in advanced Parkinson's disease and their associations with clinical features[J]. Neurol Res, 2022, 44(1): 47-56. DOI: 10.1080/01616412.2021.1954842.
[41]
JÄRNUM H, STEFFENSEN E G, KNUTSSON L, et al. Perfusion MRI of brain tumours: a comparative study of pseudo-continuous arterial spin labelling and dynamic susceptibility contrast imaging[J]. Neuroradiology, 2010, 52(4): 307-317. DOI: 10.1007/s00234-009-0616-6.
[42]
DABOUDI M, PAPADAKI E, VAKIS A, et al. Brain SPECT and perfusion MRI: do they provide complementary information about the tumour lesion and its grading?[J/OL]. Clin Radiol, 2019, 74(8): 652.e1-652.e9 [2022-09-19]. https://pubmed.ncbi.nlm.nih.gov/31164195/. DOI: 10.1016/j.crad.2019.03.025.

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