Skip to main content
Top
Published in: Metabolic Brain Disease 4/2015

01-08-2015 | Research Article

Liver transplantation nearly normalizes brain spontaneous activity and cognitive function at 1 month: a resting-state functional MRI study

Authors: Yue Cheng, Lixiang Huang, Xiaodong Zhang, Jianhui Zhong, Qian Ji, Shuangshuang Xie, Lihua Chen, Panli Zuo, Long Jiang Zhang, Wen Shen

Published in: Metabolic Brain Disease | Issue 4/2015

Login to get access

Abstract

To investigate the short-term brain activity changes in cirrhotic patients with Liver transplantation (LT) using resting-state functional MRI (fMRI) with regional homogeneity (ReHo) method. Twenty-six cirrhotic patients as transplant candidates and 26 healthy controls were included in this study. The assessment was repeated for a sub-group of 12 patients 1 month after LT. ReHo values were calculated to evaluate spontaneous brain activity and whole brain voxel-wise analysis was carried to detect differences between groups. Correlation analyses were performed to explore the relationship between the change of ReHo with the change of clinical indexes pre- and post-LT. Compared to pre-LT, ReHo values increased in the bilateral inferior frontal gyrus (IFG), right inferior parietal lobule (IPL), right supplementary motor area (SMA), right STG and left middle frontal gyrus (MFG) in patients post-LT. Compared to controls, ReHo values of post-LT patients decreased in the right precuneus, right SMA and increased in bilateral temporal pole, left caudate, left MFG, and right STG. The changes of ReHo in the right SMA, STG and IFG were correlated with change of digit symbol test (DST) scores (P < 0.05 uncorrected). This study found that, at 1 month after LT, spontaneous brain activity of most brain regions with decreased ReHo in pre-LT was substantially improved and nearly normalized, while spontaneous brain activity of some brain regions with increased ReHo in pre-LT continuously increased. ReHo may provide information on the neural mechanisms of LT’ effects on brain function.
Literature
go back to reference Bajaj JS, Hafeezullah M, Hoffmann RG, Saeian K (2007) Minimal hepatic encephalopathy: a vehicle for accidents and traffic violations. Am J Gastroenterol 102:1903–1909PubMedCrossRef Bajaj JS, Hafeezullah M, Hoffmann RG, Saeian K (2007) Minimal hepatic encephalopathy: a vehicle for accidents and traffic violations. Am J Gastroenterol 102:1903–1909PubMedCrossRef
go back to reference Bajaj JS, Wade JB, Sanyal AJ (2009a) Spectrum of neurocognitive impairment in cirrhosis: Implications for the assessment of hepatic encephalopathy. Hepatology 50:2014–2021PubMedCrossRef Bajaj JS, Wade JB, Sanyal AJ (2009a) Spectrum of neurocognitive impairment in cirrhosis: Implications for the assessment of hepatic encephalopathy. Hepatology 50:2014–2021PubMedCrossRef
go back to reference Bajaj JS, Saeian K, Schubert CM, Hafeezullah M, Franco J, Varma RR, Gibson DP, Hoffmann RG, Stravitz RT, Heuman DM, Sterling RK, Shiffman M, Topaz A, Boyett S, Bell D, Sanyal AJ (2009b) Minimal hepatic encephalopathy is associated with motor vehicle crashes: the reality beyond the driving test. Hepatology 50:1175–1183PubMedCentralPubMedCrossRef Bajaj JS, Saeian K, Schubert CM, Hafeezullah M, Franco J, Varma RR, Gibson DP, Hoffmann RG, Stravitz RT, Heuman DM, Sterling RK, Shiffman M, Topaz A, Boyett S, Bell D, Sanyal AJ (2009b) Minimal hepatic encephalopathy is associated with motor vehicle crashes: the reality beyond the driving test. Hepatology 50:1175–1183PubMedCentralPubMedCrossRef
go back to reference Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34:537–541PubMedCrossRef Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34:537–541PubMedCrossRef
go back to reference Blei AT, Cordoba J, Practice Parameters Committee of the American College of G (2001) Hepatic encephalopathy. Am J Gastroenterol 96:1968–1976PubMedCrossRef Blei AT, Cordoba J, Practice Parameters Committee of the American College of G (2001) Hepatic encephalopathy. Am J Gastroenterol 96:1968–1976PubMedCrossRef
go back to reference Budhu A, Wang XW (2006) The role of cytokines in hepatocellular carcinoma. J Leukoc Biol 80:1197–1213PubMedCrossRef Budhu A, Wang XW (2006) The role of cytokines in hepatocellular carcinoma. J Leukoc Biol 80:1197–1213PubMedCrossRef
go back to reference Cadranel JF, Lebiez E, Di Martino V, Bernard B, El Koury S, Tourbah A, Pidoux B, Valla D, Opolon P (2001) Focal neurological signs in hepatic encephalopathy in cirrhotic patients: an underestimated entity? Am J Gastroenterol 96:515–518PubMedCrossRef Cadranel JF, Lebiez E, Di Martino V, Bernard B, El Koury S, Tourbah A, Pidoux B, Valla D, Opolon P (2001) Focal neurological signs in hepatic encephalopathy in cirrhotic patients: an underestimated entity? Am J Gastroenterol 96:515–518PubMedCrossRef
go back to reference Campagna F, Biancardi A, Cillo U, Gatta A, Amodio P (2010) Neurocognitive-neurological complications of liver transplantation: a review. Metab Brain Dis 25:115–124PubMedCrossRef Campagna F, Biancardi A, Cillo U, Gatta A, Amodio P (2010) Neurocognitive-neurological complications of liver transplantation: a review. Metab Brain Dis 25:115–124PubMedCrossRef
go back to reference Chao-Gan Y, Yu-Feng Z (2010) DPARSF: a MATLAB toolbox for “pipeline” data analysis of resting-state fMRI. Front Syst Neurosci 4:13PubMedCentralPubMed Chao-Gan Y, Yu-Feng Z (2010) DPARSF: a MATLAB toolbox for “pipeline” data analysis of resting-state fMRI. Front Syst Neurosci 4:13PubMedCentralPubMed
go back to reference Chen HJ, Zhu XQ, Yang M, Liu B, Zhang Y, Wang Y, Teng GJ (2012a) Changes in the regional homogeneity of resting-state brain activity in minimal hepatic encephalopathy. Neurosci Lett 507:5–9PubMedCrossRef Chen HJ, Zhu XQ, Yang M, Liu B, Zhang Y, Wang Y, Teng GJ (2012a) Changes in the regional homogeneity of resting-state brain activity in minimal hepatic encephalopathy. Neurosci Lett 507:5–9PubMedCrossRef
go back to reference Chen HJ, Zhu XQ, Shu H, Yang M, Zhang Y, Ding J, Wang Y, Teng GJ (2012b) Structural and functional cerebral impairments in cirrhotic patients with a history of overt hepatic encephalopathy. Eur J Radiol 81:2463–2469PubMedCrossRef Chen HJ, Zhu XQ, Shu H, Yang M, Zhang Y, Ding J, Wang Y, Teng GJ (2012b) Structural and functional cerebral impairments in cirrhotic patients with a history of overt hepatic encephalopathy. Eur J Radiol 81:2463–2469PubMedCrossRef
go back to reference Chen JD, Liu F, Xun GL, Chen HF, Hu MR, Guo XF, Xiao CQ, Wooderson SC, Guo WB, Zhao JP (2012c) Early and late onset, first-episode, treatment-naive depression: same clinical symptoms, different regional neural activities. J Affect Disord 143:56–63PubMedCrossRef Chen JD, Liu F, Xun GL, Chen HF, Hu MR, Guo XF, Xiao CQ, Wooderson SC, Guo WB, Zhao JP (2012c) Early and late onset, first-episode, treatment-naive depression: same clinical symptoms, different regional neural activities. J Affect Disord 143:56–63PubMedCrossRef
go back to reference Ferenci P, Lockwood A, Mullen K, Tarter R, Weissenborn K, Blei AT (2002) Hepatic encephalopathy--definition, nomenclature, diagnosis, and quantification: final report of the working party at the 11th World Congresses of Gastroenterology, Vienna, 1998. Hepatology 35:716–721PubMedCrossRef Ferenci P, Lockwood A, Mullen K, Tarter R, Weissenborn K, Blei AT (2002) Hepatic encephalopathy--definition, nomenclature, diagnosis, and quantification: final report of the working party at the 11th World Congresses of Gastroenterology, Vienna, 1998. Hepatology 35:716–721PubMedCrossRef
go back to reference Gale SD, Hopkins RO (2004) Effects of hypoxia on the brain: neuroimaging and neuropsychological findings following carbon monoxide poisoning and obstructive sleep apnea. J Int Neuropsychol Soc 10:60–71PubMed Gale SD, Hopkins RO (2004) Effects of hypoxia on the brain: neuroimaging and neuropsychological findings following carbon monoxide poisoning and obstructive sleep apnea. J Int Neuropsychol Soc 10:60–71PubMed
go back to reference Gerber T, Schomerus H (2000) Hepatic encephalopathy in liver cirrhosis: pathogenesis, diagnosis and management. Drugs 60:1353–1370PubMedCrossRef Gerber T, Schomerus H (2000) Hepatic encephalopathy in liver cirrhosis: pathogenesis, diagnosis and management. Drugs 60:1353–1370PubMedCrossRef
go back to reference Guarino M, Stracciari A, Pazzaglia P, Sterzi R, Santilli I, Donato F, D'Alessandro R (1996) Neurological complications of liver transplantation. J Neurol 243:137–142PubMedCrossRef Guarino M, Stracciari A, Pazzaglia P, Sterzi R, Santilli I, Donato F, D'Alessandro R (1996) Neurological complications of liver transplantation. J Neurol 243:137–142PubMedCrossRef
go back to reference Guarino M, Benito-Leon J, Decruyenaere J, Schmutzhard E, Weissenborn K, Stracciari A, EFNS (2006) EFNS guidelines on management of neurological problems in liver transplantation. Eur J Neurol 13:2–9PubMedCrossRef Guarino M, Benito-Leon J, Decruyenaere J, Schmutzhard E, Weissenborn K, Stracciari A, EFNS (2006) EFNS guidelines on management of neurological problems in liver transplantation. Eur J Neurol 13:2–9PubMedCrossRef
go back to reference Guo WB, Liu F, Xue ZM, Yu Y, Ma CQ, Tan CL, Sun XL, Chen JD, Liu ZN, Xiao CQ, Chen HF, Zhao JP (2011) Abnormal neural activities in first-episode, treatment-naive, short-illness-duration, and treatment-response patients with major depressive disorder: a resting-state fMRI study. J Affect Disord 135:326–331PubMedCrossRef Guo WB, Liu F, Xue ZM, Yu Y, Ma CQ, Tan CL, Sun XL, Chen JD, Liu ZN, Xiao CQ, Chen HF, Zhao JP (2011) Abnormal neural activities in first-episode, treatment-naive, short-illness-duration, and treatment-response patients with major depressive disorder: a resting-state fMRI study. J Affect Disord 135:326–331PubMedCrossRef
go back to reference Guo WB, Liu F, Xue ZM, Xu XJ, Wu RR, Ma CQ, Wooderson SC, Tan CL, Sun XL, Chen JD, Liu ZN, Xiao CQ, Chen HF, Zhao JP (2012) Alterations of the amplitude of low-frequency fluctuations in treatment-resistant and treatment-response depression: a resting-state fMRI study. Prog Neuro-Psychopharmacol Biol Psychiatry 37:153–160CrossRef Guo WB, Liu F, Xue ZM, Xu XJ, Wu RR, Ma CQ, Wooderson SC, Tan CL, Sun XL, Chen JD, Liu ZN, Xiao CQ, Chen HF, Zhao JP (2012) Alterations of the amplitude of low-frequency fluctuations in treatment-resistant and treatment-response depression: a resting-state fMRI study. Prog Neuro-Psychopharmacol Biol Psychiatry 37:153–160CrossRef
go back to reference He Y, Wang L, Zang Y, Tian L, Zhang X, Li K, Jiang T (2007) Regional coherence changes in the early stages of Alzheimer's disease: a combined structural and resting-state functional MRI study. NeuroImage 35:488–500PubMedCrossRef He Y, Wang L, Zang Y, Tian L, Zhang X, Li K, Jiang T (2007) Regional coherence changes in the early stages of Alzheimer's disease: a combined structural and resting-state functional MRI study. NeuroImage 35:488–500PubMedCrossRef
go back to reference Inoue E, Hori S, Narumi Y, Fujita M, Kuriyama K, Kadota T, Kuroda C (1991) Portal-systemic encephalopathy: presence of basal ganglia lesions with high signal intensity on MR images. Radiology 179:551–555PubMedCrossRef Inoue E, Hori S, Narumi Y, Fujita M, Kuriyama K, Kadota T, Kuroda C (1991) Portal-systemic encephalopathy: presence of basal ganglia lesions with high signal intensity on MR images. Radiology 179:551–555PubMedCrossRef
go back to reference Ishihara T, Ito M, Niimi Y, Tsujimoto M, Senda J, Kawai Y, Watanabe H, Ishigami M, Ito T, Kamei H, Onishi Y, Nakamura T, Goto H, Naganawa S, Kiuchi T, Sobue G (2013) Clinical and radiological impact of liver transplantation for brain in cirrhosis patients without hepatic encephalopathy. Clin Neurol Neurosurg 115:2341–2347PubMedCrossRef Ishihara T, Ito M, Niimi Y, Tsujimoto M, Senda J, Kawai Y, Watanabe H, Ishigami M, Ito T, Kamei H, Onishi Y, Nakamura T, Goto H, Naganawa S, Kiuchi T, Sobue G (2013) Clinical and radiological impact of liver transplantation for brain in cirrhosis patients without hepatic encephalopathy. Clin Neurol Neurosurg 115:2341–2347PubMedCrossRef
go back to reference Jiang L, Xu T, He Y, Hou XH, Wang J, Cao XY, Wei GX, Yang Z, He Y, Zuo XN (2014) Toward neurobiological characterization of functional homogeneity in the human cortex: regional variation, morphological association and functional covariance network organization. Brain Struct Funct Jiang L, Xu T, He Y, Hou XH, Wang J, Cao XY, Wei GX, Yang Z, He Y, Zuo XN (2014) Toward neurobiological characterization of functional homogeneity in the human cortex: regional variation, morphological association and functional covariance network organization. Brain Struct Funct
go back to reference Joebges EM, Heidemann M, Schimke N, Hecker H, Ennen JC, Weissenborn K (2003) Bradykinesia in minimal hepatic encephalopathy is due to disturbances in movement initiation. J Hepatol 38:273–280PubMedCrossRef Joebges EM, Heidemann M, Schimke N, Hecker H, Ennen JC, Weissenborn K (2003) Bradykinesia in minimal hepatic encephalopathy is due to disturbances in movement initiation. J Hepatol 38:273–280PubMedCrossRef
go back to reference Lin WC, Chou KH, Chen CL, Chen HL, Lu CH, Li SH, Huang CC, Lin CP, Cheng YF (2014) Longitudinal brain white matter alterations in minimal hepatic encephalopathy before and after liver transplantation. PLoS One 9:e105887PubMedCentralPubMedCrossRef Lin WC, Chou KH, Chen CL, Chen HL, Lu CH, Li SH, Huang CC, Lin CP, Cheng YF (2014) Longitudinal brain white matter alterations in minimal hepatic encephalopathy before and after liver transplantation. PLoS One 9:e105887PubMedCentralPubMedCrossRef
go back to reference Liu F, Hu M, Wang S, Guo W, Zhao J, Li J, Xun G, Long Z, Zhang J, Wang Y, Zeng L, Gao Q, Wooderson SC, Chen J, Chen H (2012) Abnormal regional spontaneous neural activity in first-episode, treatment-naive patients with late-life depression: a resting-state fMRI study. Prog Neuro-Psychopharmacol Biol Psychiatry 39:326–331CrossRef Liu F, Hu M, Wang S, Guo W, Zhao J, Li J, Xun G, Long Z, Zhang J, Wang Y, Zeng L, Gao Q, Wooderson SC, Chen J, Chen H (2012) Abnormal regional spontaneous neural activity in first-episode, treatment-naive patients with late-life depression: a resting-state fMRI study. Prog Neuro-Psychopharmacol Biol Psychiatry 39:326–331CrossRef
go back to reference Liu F, Guo W, Liu L, Long Z, Ma C, Xue Z, Wang Y, Li J, Hu M, Zhang J, Du H, Zeng L, Liu Z, Wooderson SC, Tan C, Zhao J, Chen H (2013) Abnormal amplitude low-frequency oscillations in medication-naive, first-episode patients with major depressive disorder: a resting-state fMRI study. J Affect Disord 146:401–406PubMedCrossRef Liu F, Guo W, Liu L, Long Z, Ma C, Xue Z, Wang Y, Li J, Hu M, Zhang J, Du H, Zeng L, Liu Z, Wooderson SC, Tan C, Zhao J, Chen H (2013) Abnormal amplitude low-frequency oscillations in medication-naive, first-episode patients with major depressive disorder: a resting-state fMRI study. J Affect Disord 146:401–406PubMedCrossRef
go back to reference Liu F, Xie B, Wang Y, Guo W, Fouche JP, Long Z, Wang W, Chen H, Li M, Duan X, Zhang J, Qiu M, Chen H (2014) Characterization of post-traumatic stress disorder using resting-state fMRI with a multi-level parametric classification approach. Brain Topogr Liu F, Xie B, Wang Y, Guo W, Fouche JP, Long Z, Wang W, Chen H, Li M, Duan X, Zhang J, Qiu M, Chen H (2014) Characterization of post-traumatic stress disorder using resting-state fMRI with a multi-level parametric classification approach. Brain Topogr
go back to reference Liu F, Guo W, Fouche JP, Wang Y, Wang W, Ding J, Zeng L, Qiu C, Gong Q, Zhang W, Chen H (2015) Multivariate classification of social anxiety disorder using whole brain functional connectivity. Brain Struct Funct 220:101–115PubMedCrossRef Liu F, Guo W, Fouche JP, Wang Y, Wang W, Ding J, Zeng L, Qiu C, Gong Q, Zhang W, Chen H (2015) Multivariate classification of social anxiety disorder using whole brain functional connectivity. Brain Struct Funct 220:101–115PubMedCrossRef
go back to reference 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 (2013a) Abnormal baseline brain activity in patients with HBV-related cirrhosis without overt hepatic encephalopathy revealed by resting-state functional MRI. Metab Brain Dis 28:485–492PubMedCrossRef 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 (2013a) Abnormal baseline brain activity in patients with HBV-related cirrhosis without overt hepatic encephalopathy revealed by resting-state functional MRI. Metab Brain Dis 28:485–492PubMedCrossRef
go back to reference Lv XF, Qiu YW, Tian JZ, Xie CM, Han LJ, Su HH, Liu ZY, Peng JP, Lin CL, Wu MS, Jiang GH, Zhang XL (2013b) Abnormal regional homogeneity of resting-state brain activity in patients with HBV-related cirrhosis without overt hepatic encephalopathy. Liver Int 33:375–383PubMedCrossRef Lv XF, Qiu YW, Tian JZ, Xie CM, Han LJ, Su HH, Liu ZY, Peng JP, Lin CL, Wu MS, Jiang GH, Zhang XL (2013b) Abnormal regional homogeneity of resting-state brain activity in patients with HBV-related cirrhosis without overt hepatic encephalopathy. Liver Int 33:375–383PubMedCrossRef
go back to reference Mankinen K, Long XY, Paakki JJ, Harila M, Rytky S, Tervonen O, Nikkinen J, Starck T, Remes J, Rantala H, Zang YF, Kiviniemi V (2011) Alterations in regional homogeneity of baseline brain activity in pediatric temporal lobe epilepsy. Brain Res 1373:221–229PubMedCrossRef Mankinen K, Long XY, Paakki JJ, Harila M, Rytky S, Tervonen O, Nikkinen J, Starck T, Remes J, Rantala H, Zang YF, Kiviniemi V (2011) Alterations in regional homogeneity of baseline brain activity in pediatric temporal lobe epilepsy. Brain Res 1373:221–229PubMedCrossRef
go back to reference Mattarozzi K, Cretella L, Guarino M, Stracciari A (2012) Minimal hepatic encephalopathy: follow-up 10 years after successful liver transplantation. Transplantation 93:639–643PubMed Mattarozzi K, Cretella L, Guarino M, Stracciari A (2012) Minimal hepatic encephalopathy: follow-up 10 years after successful liver transplantation. Transplantation 93:639–643PubMed
go back to reference McCrea M, Cordoba J, Vessey G, Blei AT, Randolph C (1996) Neuropsychological characterization and detection of subclinical hepatic encephalopathy. Arch Neurol 53:758–763PubMedCrossRef McCrea M, Cordoba J, Vessey G, Blei AT, Randolph C (1996) Neuropsychological characterization and detection of subclinical hepatic encephalopathy. Arch Neurol 53:758–763PubMedCrossRef
go back to reference Mechtcheriakov S, Graziadei IW, Mattedi M, Bodner T, Kugener A, Hinterhuber HH, Marksteiner J, Vogel W (2004) Incomplete improvement of visuo-motor deficits in patients with minimal hepatic encephalopathy after liver transplantation. Liver Transpl 10:77–83PubMedCrossRef Mechtcheriakov S, Graziadei IW, Mattedi M, Bodner T, Kugener A, Hinterhuber HH, Marksteiner J, Vogel W (2004) Incomplete improvement of visuo-motor deficits in patients with minimal hepatic encephalopathy after liver transplantation. Liver Transpl 10:77–83PubMedCrossRef
go back to reference Naugler WE, Karin M (2008) The wolf in sheep’s clothing: the role of interleukin-6 in immunity, inflammation and cancer. Trends Mol Med 14:109–119PubMedCrossRef Naugler WE, Karin M (2008) The wolf in sheep’s clothing: the role of interleukin-6 in immunity, inflammation and cancer. Trends Mol Med 14:109–119PubMedCrossRef
go back to reference 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:e42016PubMedCentralPubMedCrossRef 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:e42016PubMedCentralPubMedCrossRef
go back to reference 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 83:578–583PubMedCrossRef 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 83:578–583PubMedCrossRef
go back to reference Song XW, Dong ZY, Long XY, Li SF, Zuo XN, Zhu CZ, He Y, Yan CG, Zang YF (2011) REST: a toolkit for resting-state functional magnetic resonance imaging data processing. PLoS One 6:e25031PubMedCentralPubMedCrossRef Song XW, Dong ZY, Long XY, Li SF, Zuo XN, Zhu CZ, He Y, Yan CG, Zang YF (2011) REST: a toolkit for resting-state functional magnetic resonance imaging data processing. PLoS One 6:e25031PubMedCentralPubMedCrossRef
go back to reference Watanabe A, Murakami J, Ando T, Hioki O, Wakabayashi H, Higuchi K (1993) Reduction of increased signal intensity in the basal ganglia on T1-weighted MR images during treatment of hepatic encephalopathy. Intern Med 32:10–14PubMedCrossRef Watanabe A, Murakami J, Ando T, Hioki O, Wakabayashi H, Higuchi K (1993) Reduction of increased signal intensity in the basal ganglia on T1-weighted MR images during treatment of hepatic encephalopathy. Intern Med 32:10–14PubMedCrossRef
go back to reference Weissenborn K, Ehrenheim C, Hori A, Kubicka S, Manns MP (1995) Pallidal lesions in patients with liver cirrhosis: clinical and MRI evaluation. Metab Brain Dis 10:219–231PubMedCrossRef Weissenborn K, Ehrenheim C, Hori A, Kubicka S, Manns MP (1995) Pallidal lesions in patients with liver cirrhosis: clinical and MRI evaluation. Metab Brain Dis 10:219–231PubMedCrossRef
go back to reference Weissenborn K, Ennen JC, Schomerus H, Ruckert N, Hecker H (2001) Neuropsychological characterization of hepatic encephalopathy. J Hepatol 34:768–773PubMedCrossRef Weissenborn K, Ennen JC, Schomerus H, Ruckert N, Hecker H (2001) Neuropsychological characterization of hepatic encephalopathy. J Hepatol 34:768–773PubMedCrossRef
go back to reference Wijdicks EF, Wiesner RH, Dahlke LJ, Krom RA (1994) K506-induced neurotoxicity in liver transplantation. Ann Neurol 35:498–501PubMedCrossRef Wijdicks EF, Wiesner RH, Dahlke LJ, Krom RA (1994) K506-induced neurotoxicity in liver transplantation. Ann Neurol 35:498–501PubMedCrossRef
go back to reference Wu T, Long X, Zang Y, Wang L, Hallett M, Li K, Chan P (2009) Regional homogeneity changes in patients with Parkinson's disease. Hum Brain Mapp 30:1502–1510PubMedCrossRef Wu T, Long X, Zang Y, Wang L, Hallett M, Li K, Chan P (2009) Regional homogeneity changes in patients with Parkinson's disease. Hum Brain Mapp 30:1502–1510PubMedCrossRef
go back to reference Zang Y, Jiang T, Lu Y, He Y, Tian L (2004) Regional homogeneity approach to fMRI data analysis. NeuroImage 22:394–400PubMedCrossRef Zang Y, Jiang T, Lu Y, He Y, Tian L (2004) Regional homogeneity approach to fMRI data analysis. NeuroImage 22:394–400PubMedCrossRef
go back to reference Zhang LJ, Zheng G, Zhang L, Zhong J, Wu S, Qi R, Li Q, Wang L, Lu G (2012) Altered brain functional connectivity in patients with cirrhosis and minimal hepatic encephalopathy: a functional MR imaging study. Radiology 265:528–536PubMedCrossRef Zhang LJ, Zheng G, Zhang L, Zhong J, Wu S, Qi R, Li Q, Wang L, Lu G (2012) Altered brain functional connectivity in patients with cirrhosis and minimal hepatic encephalopathy: a functional MR imaging study. Radiology 265:528–536PubMedCrossRef
go back to reference Zuo XN, Xing XX (2014) Test-retest reliabilities of resting-state FMRI measurements in human brain functional connectomics: a systems neuroscience perspective. Eurosci Biobehav Rev 45C:100–118CrossRef Zuo XN, Xing XX (2014) Test-retest reliabilities of resting-state FMRI measurements in human brain functional connectomics: a systems neuroscience perspective. Eurosci Biobehav Rev 45C:100–118CrossRef
go back to reference Zuo XN, Xu T, Jiang L, Yang Z, Cao XY, He Y, Zang YF, Castellanos FX, Milham MP (2013) Toward reliable characterization of functional homogeneity in the human brain: preprocessing, scan duration, imaging resolution and computational space. NeuroImage 65:374–386PubMedCentralPubMedCrossRef Zuo XN, Xu T, Jiang L, Yang Z, Cao XY, He Y, Zang YF, Castellanos FX, Milham MP (2013) Toward reliable characterization of functional homogeneity in the human brain: preprocessing, scan duration, imaging resolution and computational space. NeuroImage 65:374–386PubMedCentralPubMedCrossRef
Metadata
Title
Liver transplantation nearly normalizes brain spontaneous activity and cognitive function at 1 month: a resting-state functional MRI study
Authors
Yue Cheng
Lixiang Huang
Xiaodong Zhang
Jianhui Zhong
Qian Ji
Shuangshuang Xie
Lihua Chen
Panli Zuo
Long Jiang Zhang
Wen Shen
Publication date
01-08-2015
Publisher
Springer US
Published in
Metabolic Brain Disease / Issue 4/2015
Print ISSN: 0885-7490
Electronic ISSN: 1573-7365
DOI
https://doi.org/10.1007/s11011-015-9657-1

Other articles of this Issue 4/2015

Metabolic Brain Disease 4/2015 Go to the issue