Abstract
Hepatic encephalopathy (HE) is a neurological or neuropsychological complication due to liver failure or portosystemic shunting. The clinical manifestation is highly variable, which can exhibit mild cognitive or motor impairment initially, or gradually progress to a coma, even death, without treatment. Neuroimaging plays a critical role in uncovering the neural mechanism of HE. In particular, multimodality MR imaging is able to assess both structural and functional derangements of the brain with HE in focal or neural network perspectives. In recent years, there has been rapid development in novel MR technologies and applications to investigate the pathophysiological mechanism of HE. Therefore, it is necessary to update the latest MR findings regarding HE by use of multimodality MRI to refine and deepen our understanding of the neural traits in HE. Herein, this review highlights the latest MR imaging findings in HE to refresh our understanding of MRI application in HE.
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References
Ahluwalia V, Wade JB, White MB, Gilles HS, Heuman DM, Fuchs M, Gavis EA, Fagan A, Tinsley F, Ganapathy D, Thacker LR, Sterling RK, Stravitz RT, Puri P, Sanyal AJ, Siddiqui MS, Matherly S, Luketic V, Steinberg J, Moeller FG, Bajaj JS (2016) Liver transplantation significantly improves global functioning and cerebral processing. Liver Transpl 22(10):1379–1390
Ahluwalia V, Wade JB, Heuman DM et al (2014) Enhancement of functional connectivity, working memory and inhibitory control on multi-modal brain MR imaging with Rifaximin in cirrhosis: Implications for the gut-liver-brain axis. Metab Brain Dis 29:1017–1025
Alonso J, Cordoba J, Rovira A (2014) Brain magnetic resonance in hepatic encephalopathy. Semin Ultrasound CT MRI 35(2):136–152
Arnold SM, Els T, Spreer J, Schumacher M (2001) Acute hepatic encephalopathy with diffuse cortical lesions. Neuroradiology 43(7):551–554
Ashburner J, Friston KJ (2001) Why voxel-based morphometry should be used. NeuroImage 14(6):1238–1243
Ashburner J, Friston KJ (2000) Voxel-based morphometry-the method. NeuroImage 11(6 Pt 1):805–821
Atluri DK, Prakash R, Mullen KD (2011) Pathogenesis, diagnosis, and treatment of hepatic encephalopathy. J Clin Exp Hepatol 1(2):77–86
Bajaj JS, Ahluwalia V, Thacker LR et al (2017) Brain training with video games in covert hepatic encephalopathy. Am J Gastroenterol 112:316–324
Cordoba J (2014) Hepatic encephalopathy: from the pathogenesis to the new treatments. ISRN Hepatol 2014:236268
Chavarria L, Alonso J, Garcia-Martinez R, Aymerich FX, Huerga E, Jacas C, Vargas V, Cordoba J, Rovira A (2011) Biexponential analysis of diffusion-tensor imaging of the brain in patients with cirrhosis before and after liver transplantation. AJNR Am J Neuroradiol 32(8):1510–1517
Chen HJ, Zhu XQ, Shu H, Yang M, Zhang Y, Ding J, Wang Y, Teng GJ (2012a) Structural and functional cerebral impairments in cirrhotic patients with a history of overt hepatic encephalopathy. Eur J Radiol 81(10):2463–2469
Chen HJ, Zhu XQ, Yang M, Liu B, Zhang Y, Wang Y, Teng GJ (2012b) Changes in the regional homogeneity of resting-state brain activity in minimal hepatic encephalopathy. Neurosci Lett 507(1):5–9
Chen HJ, Zhu XQ, Jiao Y, Li PC, Wang Y, Teng GJ (2012c) Abnormal baseline brain activity in low-grade hepatic encephalopathy: a resting-state fMRI study. J Neurol Sci 318(1–2):140–145
Chen HJ, Jiao Y, Zhu XQ, Zhang HY, Liu JC, Wen S, Teng GJ (2013) Brain dysfunction primarily related to previous overt hepatic encephalopathy compared with minimal hepatic encephalopathy: resting-state functional MR imaging demonstration. Radiology 266(1):261–270
Chen HJ, Wang Y, Zhu XQ, Li PC, Teng GJ (2014) Classification of cirrhotic patients with or without minimal hepatic encephalopathy and healthy subjects using resting-state attention-related network analysis. PLoS One 9(3):e89684
Chen HJ, Chen R, Yang M, Teng GJ, Herskovits EH (2015a) Identification of minimal hepatic encephalopathy in patients with cirrhosis based on white matter imaging and Bayesian data mining. AJNR Am J Neuroradiol 36(3):481–487
Chen HJ, Jiang LF, Sun T, Liu J, Chen QF, Shi HB (2015b) Resting-state functional connectivity abnormalities correlate with psychometric hepatic encephalopathy score in cirrhosis. Eur J Radiol 84(11):2287–2295
Chen HJ, Zhang L, Jiang LF, Chen QF, Li J, Shi HB (2016a) Identifying minimal hepatic encephalopathy in cirrhotic patients by measuring spontaneous brain activity. Metab Brain Dis 31(4):761–769
Chen HJ, Chen QF, Liu J, Shi HB (2016b) Aberrant salience network and its functional coupling with default and executive networks in minimal hepatic encephalopathy: a resting-state fMRI study. Sci Rep 6:27092
Chen QF, Chen HJ, Liu J, Sun T, Shen QT (2016) Machine learning classification of cirrhotic patients with and without minimal hepatic encephalopathy based on regional homogeneity of intrinsic brain activity. PLoS One 11(3):e0151263
Cheng Y, Huang L, Zhang X, Zhong J, Ji Q, Xie S, Chen L, Zuo P, Zhang LJ, Shen W (2015) Liver transplantation nearly normalizes brain spontaneous activity and cognitive function at 1 month: a resting-state functional MRI study. Metab Brain Dis 30(4):1–10
Cheng Y, Huang LX, Zhang L, Ma M, Xie SS, Ji Q, Zhang XD, Zhang GY, Zhang XN, Ni HY, Shen W (2017) Longitudinal intrinsic brain activity changes in cirrhotic patients before and one month after liver transplantation. Korean J Radiol 18(2):370–377
Dharel N, Bajaj JS (2015) Definition and nomenclature of hepatic encephalopathy. J Clin Exp Hepatol 5(Suppl 1):S37–S41
Felipo V, Urios A, Giménezgarzó C, Cauli O, Andrés-Costa MJ, González O, Serra MA, Sánchez-González J, Aliaga R, Giner-Durán R, Belloch V, Montoliu C (2014) Non-invasive blood flow measurement in cerebellum detects minimal hepatic encephalopathy earlier than psychometric tests. World J Gastroenterol 20(33):11815–11825
Gómez-Ansón B, Román E, Fernández de Bobadilla R, Pires-Encuentra P, Díaz-Manera J, Núñez F, Martinez-Horta S, Vives-Gilabert Y, Pagonabarraga J, Kulisevsky J, Cordoba J, Guarner C, Soriano G (2015) Alterations in cerebral white matter and neuropsychology in patients with cirrhosis and falls. Plos One 10(3):e0118930.
Gore JC (2003) Principles and practice of functional MRI of the human brain. J Clin Invest 112(1):4–9
Grover VP, Crossey MM, Fitzpatrick JA, Saxby BK, Shaw R, Waldman AD, Morgan MY, Taylor-Robinson SD (2016) Quantitative magnetic resonance imaging in patients with cirrhosis: a cross-sectional study. Metab Brain Dis 31(6):1315–1325
Guevara M, Baccaro ME, Gomez-Anson B, Frisoni G, Testa C, Torre A, Molinuevo JL, Rami L, Pereira G, Sotil EU, Córdoba J, Arroyo V, Ginès P (2011) Cerebral magnetic resonance imaging reveals marked abnormalities of brain tissue density in patients with cirrhosis without overt hepatic encephalopathy. J Hepatol 55(3):564–573
Gupta RK, Yadav SK, Rangan M, Rathore RK, Thomas MA, Prasad KN, Pandey CM, Saraswat VA (2010) Serum proinflammatory cytokines correlate with diffusion tensor imaging derived metrics and 1 H-MR spectroscopy in patients with acute liver failure. Metab Brain Dis 25(3):355–361
He Y, Chen ZJ, Evans AC (2007) Small-world anatomical networks in the human brain revealed by cortical thickness from MRI. Cereb Cortex 17(10):2407–2419
Holecek M (2015) Ammonia and amino acid profiles in liver cirrhosis: effects of variables leading to hepatic encephalopathy. Nutrition 31(1):14–20
Hsu TW, Wu CW, Cheng YF, Chen HL, Lu CH, Cho KH, Lin WC, Lin CP (2012) Impaired small-world network efficiency and dynamic functional distribution in patients with cirrhosis. PLoS One 7(5):e35266
Iwasa M, Mifuji-Moroka R, Kuroda M, Moroka H, Fujita N, Kobayashi Y, Adachi Y, Gabazza EC, Matsuda H, Takei Y (2012) Regional reduction in gray and white matter volume in brains of cirrhotic patients: voxel-based analysis of MRI. Metab Brain Dis 27(4):551–557
Jao T, Schröter M, Chen CL, Cheng YF, Lo CY, Chou KH, Patel AX, Lin WC, Lin CP, Bullmore ET (2015) Functional brain network changes associated with clinical and biochemical measures of the severity of hepatic encephalopathy. NeuroImage 122:332–344
Kale RA, Gupta RK, Saraswat VA, Hasan KM, Trivedi R, Mishra AM, Ranjan P, Pandey CM, Narayana PA (2006) Demonstration of interstitial cerebral edema with diffusion tensor MR imaging in type C hepatic encephalopathy. Hepatology 43(4):698–706
Kong X, Luo S, Wu JR, Wu S, De Cecco CN, Schoepf UJ, Spandorfer AJ, Wang CY, Tian Y, Chen HJ, Lu GM, Yang GF, Zhang LJ (2016) 18F-DPA-714 PET imaging for detecting neuroinflammation in rats with chronic hepatic encephalopathy. Theranostics 6(8):1220–1231
Kumar R, Gupta RK, Elderkin-Thompson V, Huda A, Sayre J, Kirsch C, Guze B, Han S, Thomas MA (2008) Voxel-based diffusion tensor magnetic resonance imaging evaluation of low-grade hepatic encephalopathy. J Magn Reson Imaging 27(5):1061–1068
Liao LM, Zhou LX, Le HB, Yin JJ, Ma SH (2012) Spatial working memory dysfunction in minimal hepatic encephalopathy: an ethology and BOLD-fMRI study. Brain Res 1445:62–72
Lin WC, Hsu TW, Chen CL, Lu CH, Chen HL, Cheng YF, Lin CP (2014) Reestablishing brain networks in patients without overt hepatic encephalopathy after liver transplantation. J Cereb Blood Flow Metab 34(12):1877–1886
Lin WC, Hsu TW, Chen CL, Lu CH, Chen HL, Cheng YF (2015) Resting state-fMRI with ReHo analysis as a non-invasive modality for the prognosis of cirrhotic patients with overt hepatic encephalopathy. PLoS One 10(5):e0126834
Lv XF, Qiu YW, Tian JZ, Xie CM, Han LJ, Su HH, Liu ZY, Peng JP, Lin CL, Wu MS, Jiang GH, Zhang XL (2013a) Abnormal regional homogeneity of resting-state brain activity in patients with HBV-related cirrhosis without overt hepatic encephalopathy. Liver Int 33(3):375–383
Lv XF, Ye M, Han LJ, Zhang XL, Cai PQ, Jiang GH, Qiu YW, Qiu SJ, Wu YP, Liu K, Liu ZY, Wu PH, Xie CM (2013b) Abnormal baseline brain activity in patients with HBV-related cirrhosis without overt hepatic encephalopathy revealed by resting-state functional MRI. Metab Brain Dis 28(3):485–492
Lv XF, Liu K, Qiu YW, Cai PQ, Li J, Jiang GH, Deng YJ, Zhang XL, Wu PH, Xie CM, Wen G (2015) Anomalous gray matter structural networks in patients with hepatitis B virus-related cirrhosis without overt hepatic encephalopathy. PLoS One 10(3):e0119339
Lv XF, Wu HW, Tian L, Han LJ, Li J, Qiu YW, Jiang GH, Zhang XL, Zhang R, Xie CM (2016) Aberrant resting-state functional connectivity density in patients with hepatitis B virus-related cirrhosis. Biomed Res Int 2016:4168512
Mardini H, Smith FE, Record CO, Blamire AM (2011) Magnetic resonance quantification of water and metabolites in the brain of cirrhotics following induced hyperammonaemia. J Hepatol 54(6):1154–1160
Mcphail MJ, Taylor-Robinson SD (2010) The role of magnetic resonance imaging and spectroscopy in hepatic encephalopathy. Metab Brain Dis 25(1):65–72
McPhail MJ, Patel NR, Taylor-Robinson SD (2012) Brain imaging and hepatic encephalopathy. Clin Liver Dis 16(1):57–72
McPhail MJ, Leech R, Grover VP, Fitzpatrick JA, Dhanjal NS, Crossey MM, Pflugrad H, Saxby BK, Wesnes K, Dresner MA, Waldman AD, Thomas HC, Taylor-Robinson SD (2013) Modulation of neural activation following treatment of hepatic encephalopathy. Neurology 80(11):1041–1047
McKinney AM, Lohman BD, Sarikaya B, Uhlmann E, Spanbauer J, Singewald T, Brace JR (2010) Acute hepatic encephalopathy: diffusion-weighted and fluid-attenuated inversion recovery findings, and correlation with plasma ammonia level and clinical outcome. AJNR Am J Neuroradiol 31(8):1471–1479
McKinney AM, Sarikaya B, Spanbauer J, Lohman BD, Uhlmann E (2011) Acutehepatic (or hyper-ammonemic) encephalopathy: diffuse cortical injury and the significance of ammonia. AJNR Am J Neuroradiol 32(7):E142
Monfort P, Cauli O, Montoliu C, Rodrigo R, Llansola M, Piedrafita B, El Mlili N, Boix J, Agustí A, Felipo V (2009) Mechanisms of cognitive alterations in hyperammonemia and hepatic encephalopathy: therapeutical implications. Neurochem Int 55(1–3):106–112
Montoliu C, Gonzalez-Escamilla G, Atienza M, Urios A, Gonzalez O, Wassel A, Aliaga R, Giner-Duran R, Serra MA, Rodrigo JM, Belloch V, Felipo V, Cantero JL (2012) Focal cortical damage parallels cognitive impairment in minimal hepatic encephalopathy. NeuroImage 61(4):1165–1175
Mullen KD (2007) Review of the final report of the 1998 Working Party on definition, nomenclature and diagnosis of hepatic encephalopathy. Aliment Pharmacol Ther 25(Suppl 1):11–16
Ni L, Qi R, Zhang LJ, Zhong J, Zheng G, Zhang Z, Zhong Y, Xu Q, Liao W, Jiao Q, Wu X, Fan X, Lu GM (2012) Altered regional homogeneity in the development of minimal hepatic encephalopathy: a resting-state functional MRI study. PLoS One 7(7):e42016
Ni L, Qi R, Zhang LJ, Zhong J, Zheng G, Wu X, Fan X, Lu GM (2014) Brain regional homogeneity changes following transjugular intrahepatic portosystemic shunt in cirrhotic patients support cerebral adaptability theory--a resting-state functional MRI study. Eur J Radiol 83(3):578–583
Palaniyappan L, Liddle PF (2012) Differential effects of surface area, gyrification and cortical thickness on voxel based morphometric deficits in schizophrenia. NeuroImage 60(1):693–699
Qi R, Xu Q, Zhang LJ, Zhong J, Zheng G, Wu S, Zhang Z, Liao W, Zhong Y, Ni L, Jiao Q, Zhang Z, Liu Y, Lu G (2012a) Structural and functional abnormalities of default mode network in minimal hepatic encephalopathy: a study combining DTI and fMRI. PLoS One 7(7):e41376
Qi R, Zhang L, Wu S, Zhong J, Zhang Z, Zhong Y, Ni L, Zhang Z, Li K, Jiao Q, Wu X, Fan X, Liu Y, Lu G (2012b) Altered resting-state brain activity at functional MR imaging during the progression of hepatic encephalopathy. Radiology 264:187–195
Qi R, Zhang LJ, Zhong J, Wu S, Zhang Z, Zhong Y, Ni L, Zheng G, Jiao Q, Wu X, Fan X, Liu Y, Lu G (2012c) Dynamic changes of intrinsic brain activity in cirrhotic patients after transjugular intrahepatic portosystemic shunt: A resting-state fMRI study. PLoS One 7(10):e46681
Qi R, Zhang LJ, Xu Q, Zhong J, Wu S, Zhang Z, Liao W, Ni L, Zhang Z, Chen H, Zhong Y, Jiao Q, Wu X, Fan X, Liu Y, Lu G (2012d) Selective impairments of resting-state networks in minimal hepatic encephalopathy. PLoS One 7(5):e37400
Qi R, Zhang LJ, Zhong J, Zhu T, Zhang Z, Xu C, Zheng G, Lu GM (2013a) Grey and white matter abnormalities in minimal hepatic encephalopathy: a study combining voxel-based morphometry and tract-based spatial statistics. Eur Radiol 23(12):3370–3378
Qi R, Zhang LJ, Zhong J, Zhang Z, Ni L, Zheng G, Lu GM (2013b) Disrupted thalamic resting-state functional connectivity in patients with minimal hepatic encephalopathy. Eur J Radiol 82(5):850–856
Qi R, Zhang LJ, Luo S, Ke J, Kong X, Xu Q, Liu C, Lu H, Lu GM (2014a) Default mode network functional connectivity: A promising biomarker for diagnosing minimal hepatic encephalopathy: CONSORT-compliant article. Medicine 93(27):e227
Qi R, Zhang LJ, Xu Q, Liang X, Luo S, Zhang Z, Huang W, Zheng L, Lu GM (2014b) Abnormal functional connectivity within the default mode network in patients with HBV-related cirrhosis without hepatic encephalopathy revealed by resting-state functional MRI. Brain Res 1576:73–80
Qi R, Zhang LJ, Chen HJ, Zhong J, Luo S, Ke J, Xu Q, Kong X, Liu C, Lu GM (2015) Role of local and distant functional connectivity density in the development of minimal hepatic encephalopathy. Sci Rep 5:13720
Romero-Gómez M, Montagnese S, Jalan R (2015) Hepatic encephalopathy in patients with acute decompensation of cirrhosis and acute-on-chronic liver failure. J Hepatol 62(2):437–447
Rovira A, Alonso J, Cordoba J (2008) MR imaging findings in hepatic encephalopathy. AJNR Am J Neroradiol 29(9):1612–1621
Singh V, Chertkow H, Lerch JP, Evans AC, Dorr AE, Kabani NJ (2006) Spatial patterns of cortical thinning in mild cognitive impairment and Alzheimer’s disease. Brain 129(Pt 11):2885–2893
Snyder AZ, Raichle ME (2012) A brief history of the resting state: the Washington University perspective. NeuroImage 62(2):902–910
Su YY, Yang GF, Lu GM, Wu S, Zhang LJ (2015) PET and MR imaging of neuroinflammation in hepatic encephalopathy. Metab Brain Dis 30(1):31–45
Tao R, Zhang J, You Z, Wei L, Fan Y, Cui J, Wang J (2013) The thalamus in cirrhotic patients with and without hepatic encephalopathy: a volumetric MRI study. Eur J Radiol 82(11):e715–e720
Taylor-Robinson SD, Oatridge A, Hajnal J, Burroughs AK, McIntyre N, deSouza NM (1995) MR imaging of the basal ganglia in chronic liver disease: correlation of T1-weighted and magnetization transfer contrast measurements with liver dysfunction and neuropsychiatric status. Metab Brain Dis 10(2):175–188
U-King-Im JM, Yu E, Bartlett E, Soobrah R, Kucharczyk W (2011) Acute hyperammonemic encephalopathy in adults: imaging findings. AJNR Am J Neuroradiol 32(2):413–418
Vilstrup H, Amodio P, Bajaj JS, Cordoba J, Ferenci P, Mullen KD, Weissenborn K, Wong P (2014) Hepatic encephalopathy in chronic liver disease: 2014 practice guideline by the American association for the study of liver diseases and the European association for the study of the liver. Hepatology 60(2):715–735
Weissenborn K (2013) Psychometric tests for diagnosing minimal hepatic encephalopathy. Metab Brain Dis 28(2):227–229
Weiss N, Jalan R, Thabut D (2017) Understanding hepatic encephalopathy. Intensive Care Med
Wu X, Lv XF, Zhang YL, Wu HW, Cai PQ, Qiu YW, Zhang XL, Jiang GH (2015) Cortical signature of patients with HBV-related cirrhosis without overt hepatic encephalopathy: a morphometric analysis. Front Neuroanat 9:82
Zafiris O, Kircheis G, Rood HA, Boers F, Häussinger D, Zilles K (2004) Neural mechanism underlying impaired visual judgement in the dysmetabolic brain: an fMRI study. NeuroImage 22(2):541–552
Zang YF, Jiang T, Lu Y, He Y, Tian L (2004) Regional homogeneity approach to fMRI data analysis. Neuroimage 22(1):394–400
Zang YF, He Y, Zhu CZ, Cao QJ, Sui MQ, Liang M, Tian LX, Jiang TZ, Wang YF (2007) Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. Brain and Development 29(2):83–91
Zhang G, Cheng Y, Shen W, Liu B, Huang L, Xie S (2016) The short-term effect of liver transplantation on the low-frequency fluctuation of brain activity in cirrhotic patients with and without overt hepatic encephalopathy. Brain Imaging & Behavior
Zhang G, Cheng Y, Liu B (2017) Abnormalities of voxel-based whole-brain functional connectivity patterns predict the progression of hepatic encephalopathy. Brain Imaging Behav 11(3):784–796
Zhang LJ, Yang G, Yin J, Liu Y, Qi J (2007) Neural mechanism of cognitive control impairment in patients with hepatic cirrhosis: a functional magnetic resonance imaging study. Acta Radiol 48(5):577–587
Zhang LJ, Lu GM, Yin JZ, Qi J (2010) Metabolic changes of anterior cingulate cortex in patients with hepatic cirrhosis: a magnetic resonance spectroscopy study. Hepatol Res 40(8):777–785
Zhang LJ, Qi R, Zhong J, Xu Q, Zheng G, Lu GM (2012a) The effect of hepatic encephalopathy, hepatic failure, and portosystemic shunt on brain volume of cirrhotic patients: a voxel-based morphometry study. PLoS One 7(8):e42824
Zhang LJ, Qi R, Wu S, Zhong J, Zhong Y, Zhang Z, Zhang Z, Lu G (2012b) Brain default-mode network abnormalities in hepatic encephalopathy: A resting-state functional MRI study. Hum Brain Mapp 33(6):1384–1392
Zhang LJ, Zheng G, Zhang L, Zhong J, Wu S, Qi R, Li Q, Wang L, Lu G (2012c) Altered brain functional connectivity in patients with cirrhosis and minimal hepatic encephalopathy: a functional MR imaging study. Radiology 265(2):528–536
Zhang LJ, Zhong J, Lu GM (2013a) Multimodality MR imaging findings of low-grade brain edema in hepatic encephalopathy. AJNR Am J Neuroradiol 34(4):707–715
Zhang LJ, Qi R, Zhong J, Ni L, Zheng G, Xu J, Lu GM (2013b) Disrupted functional connectivity of the anterior cingulate cortex in cirrhotic patients without overt hepatic encephalopathy: a resting state fMRI study. PLoS One 8(1):e53206
Zhang LJ, Wu S, Ren J, Lu GM (2014a) Resting-state functional magnetic resonance imaging in hepatic encephalopathy: current status and perspectives. Metab Brain Dis 29(34):569–582
Zhang LJ, Zheng G, Zhang L, Zhong J, Li Q, Zhao TZ, Lu GM (2014b) Disrupted small world networks in patients without overt hepatic encephalopathy: A resting state fMRI study. Eur J Radiol 83(10):1890–1899
Zhang XD, Zhang LJ, Wu SY, Lu GM (2014) Multimodality magnetic resonance imaging in hepatic encephalopathy: An update. World J Gastroenterol 20(32):11262–11272
Zhang XD, Cheng Y, Poon CS, Qi R, Xu Q, Chen HJ, Kong X, Lu GM, Shen W, Zhang LJ (2015) Long-and short-range functional connectivity density alteration in non-alcoholic cirrhotic patients one month after liver transplantation: A resting-state fMRI study. Brain Res 1620:177–187
Zheng G, Zhang LJ, Wang Z, Qi RF, Shi D, Wang L, Fan X, Lu GM (2012) Changes in cerebral blood flow after transjugular intrahepatic portosystemic shunt can help predict the development of hepatic encephalopathy: an arterial spin labeling MR study. Eur J Radiol 81(12):3851–3856
Zheng G, Zhang LJ, Cao Y, Pan Z, Qi RF, Ni L, Shi D, Fan X, Lu GM (2013a) Transjugular intrahepatic portosystemic shunt induced short- and long-term cerebral blood flow variations in cirrhotic patients: an arterial spin labeling MRI study. Metab Brain Dis 28(3):463–471
Zheng G, Zhang LJ, Zhong J, Wang Z, Qi R, Shi D, Lu GM (2013b) Cerebral blood flow measured by arterial-spin labeling MRI: a useful biomarker for characterization of minimal hepatic encephalopathy in patients with cirrhosis. Eur J Radiol 82(11):1981–1988
Zheng G, Zhang L, Zhang LJ, Li Q, Pan Z, Liang X, Shi D, Lu GM (2014) Altered modular organization of functional connectivity networks in cirrhotic patients without overt hepatic encephalopathy. Biomed Res Int 2014:727452
Zheng G, Lu H, Yu W, Luo S, Liu Y, Liu W, Liu H, Wu L, Zheng L, Kong X, Zhang LJ, Lu GM (2017) Severity-specific alterations in CBF, OEF and CMRO2 in cirrhotic patients with hepatic encephalopathy. Eur Radiol 27(11):4699–4709
Zhong WJ, Zhou ZM, Zhao JN, Wu W, Guo DJ (2016) Abnormal spontaneous brain activity in minimal hepatic encephalopathy: resting-state fMRI study. Diagn Interv Radiol 22(2):196–200
Zhu XQ, Chen HJ, Wang Y, Cui Y, Teng GJ (2012) Aberrant resting-state corticostriatal functional connectivity in cirrhotic patients with hyperintense globus pallidus on T1-weighted MR imaging. PLoS One 7(11):e48886
Acknowledgements
This work was supported by grants from National Natural Science Foundation of China (grants No. 81322020, 81230032 to L.J.Z. and No. 81701679 to X.D.Z.).
We would like to express our great thanks for Drs. Parkwood Griffith and U. Joseph Schoepf, Department of Radiology and Radiological Science, Medical University of South Carolina, USA, for their help to polish this paper.
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Zhang, X.D., Zhang, L.J. Multimodal MR imaging in hepatic encephalopathy: state of the art. Metab Brain Dis 33, 661–671 (2018). https://doi.org/10.1007/s11011-018-0191-9
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DOI: https://doi.org/10.1007/s11011-018-0191-9