Top

Published in:

01-02-2018 | Original Article

Impact of previous episodes of hepatic encephalopathy on short-term brain function recovery after liver transplantation: a functional connectivity strength study

Authors: Yue Cheng, Gaoyan Zhang, Wen Shen, Li-Xiang Huang, Li Zhang, Shuang-Shuang Xie, Xiao-Dong Zhang, Baolin Liu

Published in: Metabolic Brain Disease | Issue 1/2018

Abstract

Neuropsychological studies have documented an incomplete reversal of pre-existing cognitive dysfunction in cirrhotic patients after liver transplantation (LT) and have found this is more severe in patients with hepatic encephalopathy (HE). In this study, we aimed to investigate the impact of prior HE episodes on post-transplantation brain function recovery. Resting-state functional magnetic resonance imaging data was collected from 30 healthy controls and 33 cirrhotic patients (HE, n = 15 and noHE, n = 18) before and one month after LT. Long- and short-range functional connectivity strength (FCS) analysis indicated that before transplantation both noHE and HE groups showed diffuse FCS abnormalities relative to healthy controls. For the noHE group, the abnormal FCS found before LT largely returned to normal levels after LT, except for in the cerebellum, precuneus, and orbital middle frontal gyrus. However, the abnormal FCS prior to LT was largely preserved in the HE group, including high-level cognition-related (frontal and parietal lobes) and vision-related areas (occipital lobe, cuneus, and precuneus). In addition, comparisons between HE and noHE groups revealed that weaker FCS in default mode network (DMN) in HE group persisted from pre- to post- LT. Correlation analysis showed that changes in FCS in the left postcentral and right middle frontal gyrus correlated with alterations in neuropsychological performance and ammonia levels. In conclusion, the findings in this study demonstrate potential adverse effects of pre-LT episode of HE on post-LT brain function recovery, and reveal that DMN may be the most affected brain region by HE episodes, which can’t be reversed by LT.

Bajaj JS, Wade JB, Sanyal AJ (2009) Spectrum of neurocognitive impairment in cirrhosis: implications for the assessment of hepatic encephalopathy. Hepatology 50(6):2014–2021. https://doi.org/10.1002/hep.23216 CrossRefPubMed

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(4):537–541. https://doi.org/10.1002/mrm.1910340409 CrossRefPubMed

Butterworth R (2007) Neuronal cell death in hepatic encephalopathy. Metab Brain Dis 22(3-4):309–320. https://doi.org/10.1007/s11011-007-9072-3 CrossRefPubMed

Chao-Gan Y, Yu-Feng Z (2010) DPARSF: a MATLAB toolbox for "pipeline" data analysis of resting-state fMRI. Front Syst Neurosci 4:13. https://doi.org/10.3389/fnsys.2010.00013 PubMedPubMedCentral

Chen HJ et al (2012) Structural and functional cerebral impairments in cirrhotic patients with a history of overt hepatic encephalopathy. Eur J Radiol 81(10):2463–2469. https://doi.org/10.1016/j.ejrad.2011.10.008 CrossRefPubMed

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. https://doi.org/10.1148/radiol.12120026 CrossRefPubMed

Cheng Y et al (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):979–988. https://doi.org/10.1007/s11011-015-9657-1 CrossRefPubMed

Dhar R, Young GB, Marotta P (2008) Perioperative neurological complications after liver transplantation are best predicted by pre-transplant hepatic encephalopathy. Neurocrit Care 8(2):253–258. https://doi.org/10.1007/s12028-007-9020-4 CrossRefPubMed

Duque J, Labruna L, Verset S, Olivier E, Ivry RB (2012) Dissociating the role of prefrontal and premotor cortices in controlling inhibitory mechanisms during motor preparation. J Neurosci Off J Soc Neurosci 32(3):806–816. https://doi.org/10.1523/JNEUROSCI.4299-12.2012 CrossRef

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(3):716–721. https://doi.org/10.1053/jhep.2002.31250 CrossRefPubMed

Forss N, Merlet I, Vanni S, Hamalainen M, Mauguiere F, Hari R (1996) Activation of human mesial cortex during somatosensory target detection task. Brain Res 734(1-2):229–235. https://doi.org/10.1016/0006-8993(96)00633-6 CrossRefPubMed

Garcia-Martinez R et al (2011) Hepatic encephalopathy is associated with posttransplant cognitive function and brain volume. Liver Transpl 17:38–46. https://doi.org/10.1002/lt.22197 CrossRefPubMed

Garcia-Tsao G, Lim JK, Members of Veterans Affairs Hepatitis CRCP (2009) Management and treatment of patients with cirrhosis and portal hypertension: recommendations from the Department of Veterans Affairs Hepatitis C Resource Center Program and the National Hepatitis C Program. Am J Gastroenterol 104(7):1802–1829. https://doi.org/10.1038/ajg.2009.191 CrossRefPubMed

Hahn B, Ross TJ, Stein EA (2006) Neuroanatomical dissociation between bottom-up and top-down processes of visuospatial selective attention. NeuroImage 32(2):842–853. https://doi.org/10.1016/j.neuroimage.2006.04.177 CrossRefPubMedPubMedCentral

Hampson M, Driesen NR, Skudlarski P, Gore JC, Constable RT (2006) Brain connectivity related to working memory performance. J Neurosci Off J Soc Neurosci 26(51):13338–13343. https://doi.org/10.1523/JNEUROSCI.3408-06.2006 CrossRef

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. https://doi.org/10.1093/cercor/bhl149 CrossRefPubMed

Jenkinson M, Bannister P, Brady M, Smith S (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage 17(2):825–841. https://doi.org/10.1006/nimg.2002.1132 CrossRefPubMed

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(3):273–280. https://doi.org/10.1016/S0168-8278(02)00423-3 CrossRefPubMed

Lee HW, Hong SB, Seo DW, Tae WS, Hong SC (2000) Mapping of functional organization in human visual cortex: electrical cortical stimulation. Neurology 54(4):849–854. https://doi.org/10.1212/WNL.54.4.849 CrossRefPubMed

Lim SH et al (1994) Functional anatomy of the human supplementary sensorimotor area: results of extraoperative electrical stimulation. Electroencephalogr Clin Neurophysiol 91(3):179–193. https://doi.org/10.1016/0013-4694(94)90068-X CrossRefPubMed

Lin WC et al (2014a) Longitudinal brain white matter alterations in minimal hepatic encephalopathy before and after liver transplantation. PLoS One 9(8):e105887. https://doi.org/10.1371/journal.pone.0105887 CrossRefPubMedPubMedCentral

Lin WC, Hsu TW, Chen CL, CH L, Chen HL, Cheng YF, Lin CP (2014b) Reestablishing brain networks in patients without overt hepatic encephalopathy after liver transplantation. J Cereb Blood Flow Metab 34(12):1877–1886. https://doi.org/10.1038/jcbfm.2014.143 CrossRefPubMedPubMedCentral

Liu F et al (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(3):401–406. https://doi.org/10.1016/j.jad.2012.10.001 CrossRefPubMed

Liu F et al (2015a) Multivariate classification of social anxiety disorder using whole brain functional connectivity. Brain Struct Funct 220(1):101–115. https://doi.org/10.1007/s00429-013-0641-4 CrossRefPubMed

Liu F et al (2015b) Disrupted cortical hubs in functional brain networks in social anxiety disorder. Clin Neurophysiol 126(9):1711–1716. https://doi.org/10.1016/j.clinph.2014.11.014 CrossRefPubMed

Lv XF et al (2013) 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. https://doi.org/10.1007/s11011-013-9420-4 CrossRefPubMed

Mattarozzi K, Stracciari A, Vignatelli L, D'Alessandro R, Morelli MC, Guarino M (2004) Minimal hepatic encephalopathy: longitudinal effects of liver transplantation. Arch Neurol 61(2):242–247. https://doi.org/10.1001/archneur.61.2.242 CrossRefPubMed

Mattarozzi K, Cretella L, Guarino M, Stracciari A (2012) Minimal hepatic encephalopathy: follow-up 10 years after successful liver transplantation. Transplantation 93:639–643. https://doi.org/10.1097/TP.0b013e318244f734 PubMed

Mechtcheriakov S et al (2004) Incomplete improvement of visuo-motor deficits in patients with minimal hepatic encephalopathy after liver transplantation. Liver Transpl 10:77–83. https://doi.org/10.1002/lt.20009 CrossRefPubMed

Moore KA, Mc LJR, Burrows GD (2000) Quality of life and cognitive function of liver transplant patients: a prospective study. Liver Transpl 6:633–642. https://doi.org/10.1053/jlts.2000.9743 CrossRefPubMed

O'Carroll RE, Couston M, Cossar J, Masterton G, Hayes PC (2003) Psychological outcome and quality of life following liver transplantation: a prospective, national, single-center study. Liver Transpl 9:712–720. https://doi.org/10.1053/jlts.2003.50138 CrossRefPubMed

Qi R et al (2012) Altered resting-state brain activity at functional MR imaging during the progression of hepatic encephalopathy. Radiology 264(1):187–195. https://doi.org/10.1148/radiol.12111429 CrossRefPubMed

Reeber SL, Otis TS, Sillitoe RV (2013) New roles for the cerebellum in health and disease. Front Syst Neurosci 7:83. https://doi.org/10.3389/fnsys.2013.00083 CrossRefPubMedPubMedCentral

Saalmann YB, Kastner S (2015) The cognitive thalamus. Front Syst Neurosci 9:39. https://doi.org/10.3389/fnsys.2015.00039 CrossRefPubMedPubMedCentral

Schmahmann JD, Caplan D (2006) Cognition, emotion and the cerebellum. Brain J Neurol 129(2):290–292. https://doi.org/10.1093/brain/awh729 CrossRef

Sotil EU, Gottstein J, Ayala E, Randolph C, Blei AT (2009) Impact of preoperative overt hepatic encephalopathy on neurocognitive function after liver transplantation. Liver Transpl 15(2):184–192. https://doi.org/10.1002/lt.21593 CrossRefPubMed

Squire LR, Stark CE, Clark RE (2004) The medial temporal lobe. Annu Rev Neurosci 27(1):279–306. https://doi.org/10.1146/annurev.neuro.27.070203.144130 CrossRefPubMed

Tao H, Guo S, Ge T, Kendrick KM, Xue Z, Liu Z, Feng J (2013) Depression uncouples brain hate circuit. Mol Psychiatry 18(1):101–111. https://doi.org/10.1038/mp.2011.127 CrossRefPubMed

Wandell BA, Dumoulin SO, Brewer AA (2007) Visual field maps in human cortex. Neuron 56(2):366–383. https://doi.org/10.1016/j.neuron.2007.10.012 CrossRefPubMed

Wang X et al (2014) Disrupted resting-state functional connectivity in minimally treated chronic schizophrenia. Schizophr Res 156(2-3):150–156. https://doi.org/10.1016/j.schres.2014.03.033 CrossRefPubMed

Wang L et al (2015) The effects of antidepressant treatment on resting-state functional brain networks in patients with major depressive disorder. Hum Brain Mapp 36(2):768–778. https://doi.org/10.1002/hbm.22663 CrossRefPubMed

Weissenborn K, Ennen JC, Schomerus H, Ruckert N, Hecker H (2001) Neuropsychological characterization of hepatic encephalopathy. J Hepatol 34(5):768–773. https://doi.org/10.1016/S0168-8278(01)00026-5 CrossRefPubMed

Zeneroli ML, Cioni G, Vezzelli C, Grandi S, Crisi G, Luzietti R, Ventura E (1987) Prevalence of brain atrophy in liver cirrhosis patients with chronic persistent encephalopathy. Evaluation by computed tomography. J Hepatol 4(3):283–292. https://doi.org/10.1016/S0168-8278(87)80536-6 CrossRefPubMed

Zhang L et al (2012a) Brain default-mode network abnormalities in hepatic encephalopathy: a resting-state functional MRI study. Hum Brain Mapp 33(6):1384–1392. https://doi.org/10.1002/hbm.21295 CrossRefPubMed

Zhang LJ, Qi R, Zhong J, Xu Q, Zheng G, GM L (2012b) 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. https://doi.org/10.1371/journal.pone.0042824 CrossRefPubMedPubMedCentral

Zhang XD et al (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. https://doi.org/10.1016/j.brainres.2015.04.046 CrossRefPubMed

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. https://doi.org/10.1007/s11682-016-9553-2 CrossRefPubMed

Zuo XN, Ehmke R, Mennes M, Imperati D, Castellanos FX, Sporns O, Milham MP (2012) Network centrality in the human functional connectome. Cereb Cortex 22(8):1862–1875. https://doi.org/10.1093/cercor/bhr269 CrossRefPubMed

Title: Impact of previous episodes of hepatic encephalopathy on short-term brain function recovery after liver transplantation: a functional connectivity strength study
Authors: Yue Cheng
Gaoyan Zhang
Wen Shen
Li-Xiang Huang
Li Zhang
Shuang-Shuang Xie
Xiao-Dong Zhang
Baolin Liu
Publication date: 01-02-2018
Publisher: Springer US
Published in: Metabolic Brain Disease / Issue 1/2018
Print ISSN: 0885-7490
Electronic ISSN: 1573-7365
DOI: https://doi.org/10.1007/s11011-017-0155-5

At a glance: The STEP trials

Springer Medicine

Impact of previous episodes of hepatic encephalopathy on short-term brain function recovery after liver transplantation: a functional connectivity strength study

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2018

The cerebellum is a common site of affection in Leigh syndrome

An effort toward molecular neuroeconomics of food deprivation induced food hoarding in mice: focus on xanthine oxidoreductase gene expression and xanthine oxidase activity

Risperidone-induced metabolic dysfunction is attenuated by Curcuma longa extract administration in mice

Acquired hepatocerebral degeneration (AHD): a peculiar neurological impairment in advanced chronic liver disease

Pyridoxine-dependent epilepsies: an observational study on clinical, diagnostic, therapeutic and prognostic features in a pediatric cohort

Neuroprotective effects of nootkatone from Alpiniae oxyphyllae Fructus against amyloid-β-induced cognitive impairment