Abstract
Hepatic encephalopathy (HE) is a common complication after implantation of a transjugular intrahepatic portosystemic shunt (TIPS). Neuroimaging offers a variety of techniques for non-invasive evaluation of alterations in metabolism, as well as structural and functional changes of the brain in patients after TIPS implantation. In this article, we review the epidemiology and pathophysiology of post-TIPS HE. The potential of neuroimaging including positron emission tomography and multimodality magnetic resonance imaging to investigate the pathophysiology of post-TIPS HE is presented. We also give a perspective on the role of neuroimaging in this field.
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Abbreviations
- ADC:
-
Apparent diffusion coefficient
- ALFF:
-
Amplitude of low frequency fluctuation
- ASL:
-
Arterial spin labeling
- BOLD:
-
Blood oxygenation level-dependent
- CBF:
-
Cerebral blood flow
- CMRA:
-
Cerebral metabolism rate of ammonia
- CMRO2 :
-
Metabolic rate of oxygen
- DTI:
-
Diffusion tensor imaging
- DWI:
-
Diffusion weighted imaging
- FA:
-
Fractional anisotropy
- fMRI:
-
Functional magnetic resonance imaging
- HE:
-
Hepatic encephalopathy
- MD:
-
Mean diffusivity
- PET:
-
Positron emission tomography
- ReHo:
-
Regional homogeneity
- SPECT:
-
Single photon emission computed tomography
- TIPS:
-
Transjugular intrahepatic portosystemic shunt
References
Babington JR, Stahl JH, Coy DL (2009) Reversible cytotoxic edema in a cirrhotic patient following TIPS. J Neuroimaging 19(4):391–393
Bai M, Qi X, Yang Z, Yin Z, Nie Y, Yuan S, Wu K, Han G, Fan D (2011) Predictors of hepatic encephalopathy after transjugular intrahepatic portosystemic shunt in cirrhotic patients: a systematic review. J Gastroenterol Hepatol 26(6):943–951
Balata S, Olde Damink SW, Ferguson K, Marshall I, Hayes PC, Deutz NE, Williams R, Wardlaw J, Jalan R (2003) Induced hyperammonemia alters neuropsychology, brain MR spectroscopy and magnetization transfer in cirrhosis. Hepatology 37(4):931–939
Bianchi Porro G, Maiolo AT, Della Porta P (1969) Cerebral blood flow and metabolism in hepatic cirrhosis before and after portacaval shunt operation. Gut 10(11):894–897
Butterworth RF (2003) Pathogenesis of hepatic encephalopathy: new insights from neuroimaging and molecular studies. J Hepatol 39(2):278–285
Chen HJ, Zhu XQ, Yang M, Liu B, Zhang Y, Wang Y, Teng GJ (2012) Changes in the regional homogeneity of resting-state brain activity in minimal hepatic encephalopathy. Neurosci Lett 507(1):5–9
Chen HJ, Qi R, Kong X, Wen J, Liang X, Zhang Z, Li X, Lu GM, Zhang LJ (2015) The impact of hemodialysis on cognitive dysfunction in patients with end-stage renal disease: a resting-state functional MRI study. Metab Brain Dis 30(5):1247–1256
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):979–988
Colombato L (2007) The role of transjugular intrahepatic portosystemic shunt (TIPS) in the management of portal hypertension. J Clin Gastroenterol 41(Suppl 3):S344–S351
Cordoba J, Alonso J, Rovira A, Jacas C, Sanpedro F, Castells L, Vargas V, Margarit C, Kulisewsky J, Esteban R, Guardia J (2001) The development of low-grade cerebral edema in cirrhosis is supported by the evolution of (1)H-magnetic resonance abnormalities after liver transplantation. J Hepatol 35(5):598–604
Cordoba J, Sanpedro F, Alonso J, Rovira A (2002) 1H magnetic resonance in the study of hepatic encephalopathy in humans. Metab Brain Dis 17(4):415–429
Dam G, Keiding S, Munk OL, Ott P, Vilstrup H, Bak LK, Waagepetersen HS, Schousboe A, Sorensen M (2013) Hepatic encephalopathy is associated with decreased cerebral oxygen metabolism and blood flow, not increased ammonia uptake. Hepatology 57(1):258–265
Das K, Singh P, Chawla Y, Duseja A, Dhiman RK, Suri S (2008) Magnetic resonance imaging of brain in patients with cirrhotic and non-cirrhotic portal hypertension. Dig Dis Sci 53(10):2793–2798
Freedman AM, Sanyal AJ, Tisnado J, Cole PE, Shiffman ML, Luketic VA, Purdum PP, Darcy MD, Posner MP (1993) Complications of transjugular intrahepatic portosystemic shunt: a comprehensive review. Radiographics 13(6):1185–1210
Hassoun Z, Deschenes M, Lafortune M, Dufresne MP, Perreault P, Lepanto L, Gianfelice D, Bui B, Pomier-Layrargues G (2001) Relationship between pre-TIPS liver perfusion by the portal vein and the incidence of post-TIPS chronic hepatic encephalopathy. Am J Gastroenterol 96(4):1205–1209
Haussinger D, Laubenberger J, vom Dahl S, Ernst T, Bayer S, Langer M, Gerok W, Hennig J (1994) Proton magnetic resonance spectroscopy studies on human brain myo-inositol in hypo-osmolarity and hepatic encephalopathy. Gastroenterology 107(5):1475–1480
Haussinger D, Kircheis G, Fischer R, Schliess F, vom Dahl S (2000) Hepatic encephalopathy in chronic liver disease: a clinical manifestation of astrocyte swelling and low-grade cerebral edema? J Hepatol 32(6):1035–1038
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(2):488–500
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(2):551–555
Iversen P, Sorensen M, Bak LK, Waagepetersen HS, Vafaee MS, Borghammer P, Mouridsen K, Jensen SB, Vilstrup H, Schousboe A, Ott P, Gjedde A, Keiding S (2009) Low cerebral oxygen consumption and blood flow in patients with cirrhosis and an acute episode of hepatic encephalopathy. Gastroenterology 136(3):863–871
Iversen P, Keiding S, Mouridsen K, Ott P, Vilstrup H (2011) Transjugular intrahepatic portosystemic shunt does not alter cerebral blood flow. Clin Gastroenterol Hepatol 9(11):1001–1003
Jalan R, Olde Damink SW, Ter Steege JC, Redhead DN, Lee A, Hayes PC, Deutz NE (2011) Acute endotoxemia following transjugular intrahepatic stent-shunt insertion is associated with systemic and cerebral vasodilatation with increased whole body nitric oxide production in critically ill cirrhotic patients. J Hepatol 54(2):265–271
Kavitt RT, Yang VL, Jensen DM (2008) Cerebral edema and hyperammonemia after transjugular intrahepatic portosystemic shunt placement in a cirrhotic patient. Clin Gastroenterol Hepatol 6(9):1054–1056
Keiding S, Sorensen M, Bender D, Munk OL, Ott P, Vilstrup H (2006) Brain metabolism of 13N-ammonia during acute hepatic encephalopathy in cirrhosis measured by positron emission tomography. Hepatology 43(1):42–50
Kochar N, Tripathi D, Ireland H, Redhead DN, Hayes PC (2006) Transjugular intrahepatic portosystemic stent shunt (TIPSS) modification in the management of post-TIPSS refractory hepatic encephalopathy. Gut 55(11):1617–1623
Krieger S, Jauss M, Jansen O, Stiehl A, Sauer P, Geissler M, Theilmann L, Krieger D (1997) MRI findings in chronic hepatic encephalopathy depend on portosystemic shunt: results of a controlled prospective clinical investigation. J Hepatol 27(1):121–126
Le Bihan D, Mangin JF, Poupon C, Clark CA, Pappata S, Molko N, Chabriat H (2001) Diffusion tensor imaging: concepts and applications. J Magn Reson Imaging 13(4):534–546
Masson S, Mardini HA, Rose JD, Record CO (2008) Hepatic encephalopathy after transjugular intrahepatic portosystemic shunt insertion: a decade of experience. QJM 101(6):493–501
Mechtcheriakov S, Schocke M, Kugener A, Graziadei IW, Mattedi M, Hinterhuber H, Vogel W, Marksteiner J (2005) Chemical shift magnetic resonance spectroscopy of cingulate grey matter in patients with minimal hepatic encephalopathy. Neuroradiology 47(1):27–34
Merli M, Salerno F, Riggio O, de Franchis R, Fiaccadori F, Meddi P, Primignani M, Pedretti G, Maggi A, Capocaccia L, Lovaria A, Ugolotti U, Salvatori F, Bezzi M, Rossi P (1998) Transjugular intrahepatic portosystemic shunt versus endoscopic sclerotherapy for the prevention of variceal bleeding in cirrhosis: a randomized multicenter trial. Gruppo Italiano Studio TIPS (G.I.S.T.). Hepatology 27(1):48–53
Miese F, Kircheis G, Wittsack HJ, Wenserski F, Hemker J, Modder U, Haussinger D, Cohnen M (2006) 1H-MR spectroscopy, magnetization transfer, and diffusion-weighted imaging in alcoholic and nonalcoholic patients with cirrhosis with hepatic encephalopathy. AJNR Am J Neuroradiol 27(5):1019–1026
Mullen KD, Ghanta RK, Putka BS (2006) Prevention of first overt episode of hepatic encephalopathy after TIPS: no easy task. Hepatology 43(5):1155–1156
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
Nolte W, Wiltfang J, Schindler CG, Unterberg K, Finkenstaedt M, Niedmann PD, Hartmann H, Ramadori G (1998a) Bright basal ganglia in T1-weighted magnetic resonance images are frequent in patients with portal vein thrombosis without liver cirrhosis and not suggestive of hepatic encephalopathy. J Hepatol 29(3):443–449
Nolte W, Wiltfang J, Schindler C, Munke H, Unterberg K, Zumhasch U, Figulla HR, Werner G, Hartmann H, Ramadori G (1998b) Portosystemic hepatic encephalopathy after transjugular intrahepatic portosystemic shunt in patients with cirrhosis: clinical, laboratory, psychometric, and electroencephalographic investigations. Hepatology 28(5):1215–1225
Ohta S, Meyer E, Thompson CJ, Gjedde A (1992) Oxygen consumption of the living human brain measured after a single inhalation of positron emitting oxygen. J Cereb Blood Flow Metab 12(2):179–192
Pujol A, Pujol J, Graus F, Rimola A, Peri J, Mercader JM, Garcia-Pagan JC, Bosch J, Rodes J, Tolosa E (1993) Hyperintense globus pallidus on T1-weighted MRI in cirrhotic patients is associated with severity of liver failure. Neurology 43(1):65–69
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 (2012) Dynamic changes of intrinsic brain activity in cirrhotic patients after transjugular intrahepatic portosystemic shunt: a resting-state FMRI study. PLoS One 7(10):e46681
Riggio O, Merlli M, Pedretti G, Servi R, Meddi P, Lionetti R, Rossi P, Bezzi M, Salvatori F, Ugolotti U, Fiaccadori F, Capocaccia L (1996) Hepatic encephalopathy after transjugular intrahepatic portosystemic shunt. Incidence and risk factors. Dig Dis Sci 41(3):578–584
Riggio O, Angeloni S, Salvatori FM, De Santis A, Cerini F, Farcomeni A, Attili AF, Merli M (2008) Incidence, natural history, and risk factors of hepatic encephalopathy after transjugular intrahepatic portosystemic shunt with polytetrafluoroethylene-covered stent grafts. Am J Gastroenterol 103(11):2738–2746
Riggio O, Nardelli S, Moscucci F, Pasquale C, Ridola L, Merli M (2012) Hepatic encephalopathy after transjugular intrahepatic portosystemic shunt. Clin Liver Dis 16(1):133–146
Rossle M, Haag K, Ochs A, Sellinger M, Noldge G, Perarnau JM, Berger E, Blum U, Gabelmann A, Hauenstein K et al (1994) The transjugular intrahepatic portosystemic stent-shunt procedure for variceal bleeding. N Engl J Med 330(3):165–171
Rovira A, Grive E, Pedraza S, Rovira A, Alonso J (2001) Magnetization transfer ratio values and proton MR spectroscopy of normal-appearing cerebral white matter in patients with liver cirrhosis. AJNR Am J Neuroradiol 22(6):1137–1142
Rydberg JN, Hammond CA, Grimm RC, Erickson BJ, Jack CR Jr, Huston J 3rd, Riederer SJ (1994) Initial clinical experience in MR imaging of the brain with a fast fluid-attenuated inversion-recovery pulse sequence. Radiology 193(1):173–180
Schaefer PW, Grant PE, Gonzalez RG (2000) Diffusion-weighted MR imaging of the brain. Radiology 217(2):331–345
Stadlbauer V, Tauss J, Portugaller HR, Stiegler P, Iberer F, Stauber RE (2007) Hepatic encephalopathy following transjugular intrahepatic portosystemic shunt (TIPS): management with L-ornithine-L-aspartate and stent reduction. Metab Brain Dis 22(1):45–50
Stefankova J, Huleki P, Babu A, Cermakova E, Safka V, Stefanek J, Fejfar T, Krajina A (2007) Hepatic encephalopathy due to TIPS--retrospective study. Hepatogastroenterology 54(74):480–484
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
Tarasow E, Panasiuk A, Siergiejczyk L, Orzechowska-Bobkiewicz A, Lewszuk A, Walecki J, Prokopowicz D (2003) MR and 1H MR spectroscopy of the brain in patients with liver cirrhosis and early stages of hepatic encephalopathy. Hepatogastroenterology 50(54):2149–2153
Vilstrup H, Amodio P, Bajaj J, 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, Bokemeyer M, Ahl B, Fischer-Wasels D, Giewekemeyer K, van den Hoff J, Kostler H, Berding G (2004) Functional imaging of the brain in patients with liver cirrhosis. Metab Brain Dis 19(3–4):269–280
Weitzman G, Schamberg NJ, Lake-Bakaar G (2007) Synergism between hepatocellular injury and shunting in portosystemic encephalopathy (PSE): case report of acute brittle TIPS-induced PSE. Dig Dis Sci 52(11):3270–3274
Zang Y, 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 Dev 29(2):83–91
Zhang LJ, Zhong J, Lu GM (2013) Multimodality MR imaging findings of low-grade brain edema in hepatic encephalopathy. AJNR Am J Neuroradiol 34(4):707–715
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(3):569–582
Zhang XD, Zhang LJ, Wu SY, Lu GM (2014b) Multimodality magnetic resonance imaging in hepatic encephalopathy: an update. World J Gastroenterol 20(32):11262–11272
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, Lu GM (2013a) Venous blood ammonia can be associated with cerebral blood flow in hepatic encephalopathy. Hepatology 58(2):832–833
Zheng G, Zhang LJ, Cao Y, Pan Z, Qi RF, Ni L, Shi D, Fan X, Lu GM (2013b) 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
Zuo XN, Xing XX (2014) Test-retest reliabilities of resting-state FMRI measurements in human brain functional connectomics: a systems neuroscience perspective. Neurosci Biobehav Rev 45:100–118
Zuo XN, Di Martino A, Kelly C, Shehzad ZE, Gee DG, Klein DF, Castellanos FX, Biswal BB, Milham MP (2010a) The oscillating brain: complex and reliable. Neuroimage 49(2):1432–1445
Zuo XN, Kelly C, Adelstein JS, Klein DF, Castellanos FX, Milham MP (2010b) Reliable intrinsic connectivity networks: test-retest evaluation using ICA and dual regression approach. Neuroimage 49(3):2163–2177
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
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 65:374–386
Acknowledgments
Supported by Grants from National Natural Science Foundation of China, Nos. 30700194, 81322020 and 81230032 (to Zhang LJ); Grant No.81101039 (to Zheng G); Program for New Century Excellent Talents in University, No. NCET-12-0260 (to Zhang LJ)
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Zhang LJ and Lu GM designed the research; Chen HJ, Zheng G, Wichmann JL, Schoepf UJ, Lu GM and Zhang LJ wrote the paper.
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The authors declare that they have no conflict of interest.
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Chen, H.J., Zheng, G., Wichmann, J.L. et al. The brain following transjugular intrahepatic portosystemic shunt: the perspective from neuroimaging. Metab Brain Dis 30, 1331–1341 (2015). https://doi.org/10.1007/s11011-015-9735-4
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DOI: https://doi.org/10.1007/s11011-015-9735-4