Regional gray matter abnormality in hepatic myelopathy patients after transjugular intrahepatic portosystemic shunt: a voxel-based morphometry study
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摘要
Hepatic myelopathy is a complication seen in patients with chronic liver failure with physiologic or iatrogenic portosystemic shunting. The main symptom is progressive lower limb dyskinesia. The role of the brain motor control center in hepatic myelopathy is unknown. This study aimed to investigate the gray matter changes in patients with hepatic myelopathy secondary to transjugular intrahepatic portosystemic shunt and to examine their clinical relevance. This was a cross-sectional study. Twenty-three liver failure patients with hepatic myelopathy(hepatic myelopathy group), 23 liver failure patients without hepatic myelopathy(non-hepatic myelopathy group) after transjugular intrahepatic portosystemic shunt, and 23 demographically matched healthy volunteers were enrolled from March 2014 to November 2016 at Xijing Hospital, Air Force Military Medical University(Fourth Military Medical University), China. High-resolution magnetization-prepared rapid gradient-echo brain imaging was acquired. Group differences in regional gray matter were assessed using voxel-based morphometry analysis. The relationship between aberrant gray matter and motor characteristics was investigated. Results demonstrated that compared with the non-hepatic myelopathy group, gray matter volume abnormalities were asymmetric, with decreased volume in the left insula(P = 0.003), left thalamus(P = 0.029), left superior frontal gyrus(P = 0.006), and right middle cingulate cortex(P = 0.021), and increased volume in the right caudate nucleus(P = 0.017), corrected with open-source software. The volume of the right caudate nucleus in the hepatic myelopathy group negatively correlated with the lower limb clinical rating of the Fugl-Meyer Assessment(r = –0.53, P = 0.01). Compared with healthy controls, patients with and without hepatic myelopathy exhibited overall increased gray matter volume in both thalami, and decreased gray matter volume in both putamen, as well as in the globus pallidus, cerebellum, and vermis. The gray matter abnormalities we found predominantly involved motor-related regions, and may be associated with motor dysfunction. An enlarged right caudate nucleus might help to predict weak lower limb motor performance in patients with preclinical hepatic myelopathy after transjugular intrahepatic portosystemic shunt. This study was approved by the Ethics Committee of Xijing Hospital, Air Force Military Medical University(Fourth Military Medical University), China(approval No. 20140227-6) on February 27, 2014.
Hepatic myelopathy is a complication seen in patients with chronic liver failure with physiologic or iatrogenic portosystemic shunting. The main symptom is progressive lower limb dyskinesia. The role of the brain motor control center in hepatic myelopathy is unknown. This study aimed to investigate the gray matter changes in patients with hepatic myelopathy secondary to transjugular intrahepatic portosystemic shunt and to examine their clinical relevance. This was a cross-sectional study. Twenty-three liver failure patients with hepatic myelopathy(hepatic myelopathy group), 23 liver failure patients without hepatic myelopathy(non-hepatic myelopathy group) after transjugular intrahepatic portosystemic shunt, and 23 demographically matched healthy volunteers were enrolled from March 2014 to November 2016 at Xijing Hospital, Air Force Military Medical University(Fourth Military Medical University), China. High-resolution magnetization-prepared rapid gradient-echo brain imaging was acquired. Group differences in regional gray matter were assessed using voxel-based morphometry analysis. The relationship between aberrant gray matter and motor characteristics was investigated. Results demonstrated that compared with the non-hepatic myelopathy group, gray matter volume abnormalities were asymmetric, with decreased volume in the left insula(P = 0.003), left thalamus(P = 0.029), left superior frontal gyrus(P = 0.006), and right middle cingulate cortex(P = 0.021), and increased volume in the right caudate nucleus(P = 0.017), corrected with open-source software. The volume of the right caudate nucleus in the hepatic myelopathy group negatively correlated with the lower limb clinical rating of the Fugl-Meyer Assessment(r = –0.53, P = 0.01). Compared with healthy controls, patients with and without hepatic myelopathy exhibited overall increased gray matter volume in both thalami, and decreased gray matter volume in both putamen, as well as in the globus pallidus, cerebellum, and vermis. The gray matter abnormalities we found predominantly involved motor-related regions, and may be associated with motor dysfunction. An enlarged right caudate nucleus might help to predict weak lower limb motor performance in patients with preclinical hepatic myelopathy after transjugular intrahepatic portosystemic shunt. This study was approved by the Ethics Committee of Xijing Hospital, Air Force Military Medical University(Fourth Military Medical University), China(approval No. 20140227-6) on February 27, 2014.
Hepatic myelopathy is a complication seen in patients with chronic liver failure with physiologic or iatrogenic portosystemic shunting. The main symptom is progressive lower limb dyskinesia. The role of the brain motor control center in hepatic myelopathy is unknown. This study aimed to investigate the gray matter changes in patients with hepatic myelopathy secondary to transjugular intrahepatic portosystemic shunt and to examine their clinical relevance. This was a cross-sectional study. Twenty-three liver failure patients with hepatic myelopathy(hepatic myelopathy group), 23 liver failure patients without hepatic myelopathy(non-hepatic myelopathy group) after transjugular intrahepatic portosystemic shunt, and 23 demographically matched healthy volunteers were enrolled from March 2014 to November 2016 at Xijing Hospital, Air Force Military Medical University(Fourth Military Medical University), China. High-resolution magnetization-prepared rapid gradient-echo brain imaging was acquired. Group differences in regional gray matter were assessed using voxel-based morphometry analysis. The relationship between aberrant gray matter and motor characteristics was investigated. Results demonstrated that compared with the non-hepatic myelopathy group, gray matter volume abnormalities were asymmetric, with decreased volume in the left insula(P = 0.003), left thalamus(P = 0.029), left superior frontal gyrus(P = 0.006), and right middle cingulate cortex(P = 0.021), and increased volume in the right caudate nucleus(P = 0.017), corrected with open-source software. The volume of the right caudate nucleus in the hepatic myelopathy group negatively correlated with the lower limb clinical rating of the Fugl-Meyer Assessment(r = –0.53, P = 0.01). Compared with healthy controls, patients with and without hepatic myelopathy exhibited overall increased gray matter volume in both thalami, and decreased gray matter volume in both putamen, as well as in the globus pallidus, cerebellum, and vermis. The gray matter abnormalities we found predominantly involved motor-related regions, and may be associated with motor dysfunction. An enlarged right caudate nucleus might help to predict weak lower limb motor performance in patients with preclinical hepatic myelopathy after transjugular intrahepatic portosystemic shunt. This study was approved by the Ethics Committee of Xijing Hospital, Air Force Military Medical University(Fourth Military Medical University), China(approval No. 20140227-6) on February 27, 2014.
引文
Adams RD,Foley JM(1953)The neurological disorder associated with liver disease.Res Publ Assoc Res Nerv Ment Dis 32:198-237.
Ahl B,Weissenborn K,van den Hoff J,Fischer-Wasels D,Kastler H,Hecker H,Burchert W(2004)Regional differences in cerebral blood flow and cerebral ammonia metabolism in patients with cirrhosis.Hepatology 40:73-79.
Alexander GE.,Crutcher MD(1990)Functional architecture of basal ganglia circuits:neural substrates of parallel processing.Trends Neurosci 13:266-271.
Amiez C,Petrides M(2014)Neuroimaging evidence of the anatomo-functional organization of the human cingulate motor areas.Cereb Cortex 24:563-578.
Amiez C,Wutte MG,Faillenot I,Petrides M,Burle B,Procyk E(2016)Single subject analyses reveal consistent recruitment of frontal operculum in performance monitoring.Neuroimage 133:266-278.
Ashburner J(2007)A fast diffeomorphic image registration algorithm.Neuroimage 38:95-113.
Berglund K,Fugl-Meyer AR(1986)Upper extremity function in hemiplegia.A cross-validation study of two assessment methods.Scand JRehabil Med 18:155-157.
Caldwell C,Werdiger N,Jakab S,Schilsky M,Arvelakis A,Kulkarni S,Emre S(2010)Use of model for end-stage liver disease exception points for early liver transplantation and successful reversal of hepatic myelopathy with a review of the literature.Liver Transpl 16:818-826.
Campellone JV,Lacomis D,Giuliani MJ,Kroboth FJ(1996)Hepatic myelopathy.Case report with review of the literature.Clin Neurol Neurosurg 98:242-246.
Cauda F,D’Agata F,Sacco K,Duca S,Geminiani G,Vercelli A(2011)Functional connectivity of the insula in the resting brain.Neuroimage 55:8-23.
Chang Y,Jin SU,Kim Y,Kim Y,Kyung MS,Lee HJ,Kim SH,Ahn JH,Park SJ,Jeong KS,Weon YC,Lee H(2013)Decreased brain volumes in manganese-exposed welders.Neurotoxicology 37:182-189.
Chen HJ,Zhu XQ,Shu H(2012)Structural and functional cerebral impairments in cirrhotic patients with a history of overt hepatic encephalopathy.Eur J Radiol 81:2463-2469.
Conn HO,R?ssle M,Levy L,Glocker FX(2006)Portosystemic myelopathy:spastic paraparesis after portosystemic shunting.Scand JGastroenterol 41:619-625.
Demirci M,Tan E,Elibol B,Gediko?lu G,Sariba?O(1992)Spastic paraparesis associated with portal-systemic venous shunting due to congenital hepatic fibrosis.Neurology 42:983-985.
Dumurgier J,Crivello F,Mazoyer B,Ahmed,Tavernier B,Grabli D,Fran?ois C,Tzourio-Mazoyer N,Tzourio C,Elbaz A(2012)MRIatrophy of the caudate nucleus and slower walking speed in the elderly.Neuroimage 60:871-878.
Eriksson H,Magiste K,Plantin LO,Fonnum F,Hedstr?m KG,Theodorsson-Norheim E,Kristensson K,Stalberg E,Heilbronn E(1987)Effects of manganese oxide on monkeys as revealed by a combined neurochemical,histological and neurophysiological evaluation.Arch Toxicol 61:46-52.
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.Hepatology35:716-721.
Ferreira CR,Gahl WA(2017)Disorders of metal metabolism.Transl Sci Rare Dis 2:101-139.
Finelli PF,Gupta F,Zeevi N(2007)Neuroimaging of bilateral caudate infarction manifesting as Parkinsonian gait disorder.Conn Med71:149-150.
García-Lezana T,Oria M,Romero-Giménez J,BovéJ,Vila M,GenescàJ,Chavarria L,Cordoba J(2017)Cerebellar neurodegeneration in a new rat model of episodic hepatic encephalopathy.J Cereb Blood Flow Metab 37:927-937.
Goto M,Abe O,Aoki S,Hayashi N,Miyati T,Takao H,Iwatsubo T,Yamashita F,Matsuda H,Mori H,Kunimatsu A,Ino K,Yano K,Ohtomo K(2013)Diffeomorphic anatomical registration through exponentiated lie algebra provides reduced effect of scanner for cortex volumetry with atlas-based method in healthy subjects.Neuroradiology 55:869-875.
Guevara M,Baccaro ME,Gomez-Anson B(2011)Cerebral magnetic resonance imaging reveals marked abnormalities of brain tissue density in patients with cirrhosis without overt hepatic encephalopathy.J Hepatol 55:564-573.
Haber SN(2016)Corticostriatal circuitry.Dialogues Clin Neurosci18:7-21.
Kulisevsky J,Pujol J,BalanzóJ,JunquéC,Deus J,Capdevilla A,Villanueva C(1992)Pallidal hyperintensity on magnetic resonance imaging in cirrhotic patients:clinical correlations.Hepatology 16:1382-1388.
Layrargues GP,Rose C,Spahr L,Zayed J,Normandin L,Butterworth RF(1998)Role of manganese in the pathogenesis of portal-systemic encephalopathy.Metab Brain Dis 13:311-317.
Lefer LG,Vogel FS(1972)Encephalomyelopathy with hepatic cirrhosis following portosystemic venous shunts.Arch Pathol 93:91-97.
Leigh AD,Card WI(1949)Hepatolenticular degeneration:a case associated with postero-lateral column degeneration.J Neuropathol Exp Neurol 8:338-346.
Liversedge LA,Rawson MD(1966)Myelopathy in hepatic disease and portosystemic venous anastomosis.Lancet 1:277-279.
Maeda H,Sato M,Yoshikawa A,Kimura M,Sonomura T,Terada M,Kishi K(1997)Brain MR imaging in patients with hepatic cirrhosis:relationship between high intensity signal in basal ganglia on T1-weighted images and elemental concentrations in brain.Neuroradiology 39:546-550.
Marshall RS,Zarahn E,Alon L,Minzer B,Lazar RM,Krakauer JW(2009)Early imaging correlates of subsequent motor recovery after stroke.Ann Neurol 65:596-602.
McFarland NR.,Haber SN(2002)Thalamic relay nuclei of the basal ganglia form both reciprocal and nonreciprocal cortical connections,linking multiple frontal cortical areas.J Neurosci 22:8117-8132.
Mendoza G,Marti-Fàbregas J,Kulisevsky J,Escartín A(1994)Hepatic myelopathy:a rare complication of portacaval shunt.Eur Neurol34:209-212.
Moreno-Alcázar A,Ramos-Quiroga JA,Radua J,Salavert J,Palomar G,Bosch R,Salvador R,Blanch J,Casas M,McKenna PJ,Pomarol-Clotet E(2016)Brain abnormalities in adults with attention deficit hyperactivity disorder revealed by voxel-based morphometry.Psychiatry Res Neuroimaging 254:41-47.
Mutschler I,Wieckhorst B,Kowalevski S,Derix J,Wentlandt J,Schulze-Bonhage A,Ball T(2009)Functional organization of the human anterior insular cortex.Neurosci Lett 457:66-70.
Nardone R,Buratti T,Oliviero A,Lochmann A,Tezzon F(2006)Corticospinal involvement in patients with a portosystemic shunt due to liver cirrhosis:a MEP study.J Neurol 253:81-85.
Navarro-Cebrian A,Knight RT,Kayser AS(2013)Error-monitoring and post-error compensations:dissociation between perceptual failures and motor errors with and without awareness.J Neurosci33:12375-12383.
Obeso JA,Rodriguez-Oroz MC,Stamelou M,Bhatia KP,Burn DJ(2014)The expanding universe of disorders of the basal ganglia.Lancet 384:523-531.
Pomier-Layrargues G,Spahr L,Butterworth RF(1995)Increased manganese concentration in pallidum of cirrhotic patients.Lancet345:735.
Procyk E,Wilson CR,Stoll FM,Faraut MC,Petrides M,Amiez C(2016)Midcingulate motor map and feedback detection:converging data from humans and monkeys.Cereb Cortex 26:467-476.
Pugh RN,Murray-Lyon IM,Dawson JL,Pietroni MC,Williams R(1973)Transection of the oesophagus for bleeding oesophageal varices.Br J Surg 60:646-649.
Rao AK,Muratori L,Louis ED,Moskowitz CB,Marder KS(2008)Spectrum of gait impairments in presymptomatic and symptomatic Huntington’s disease.Mov Disord 23:1100-1107.
Rose C,Butterworth RF,Zayed J,Normandin L,Todd K,Michalak A,Spahr L,Huet PM,Pomier-Layrargues G(1999)Manganese deposition in basal ganglia structures results from both portal-systemic shunting and liver dysfunction.Gastroenterology 117:640-644.
Rudebeck PH,Behrens TE,Kennerley SW,Baxter MG,Buckley MJ,Walton ME,Rushworth MF(2008)Frontal cortex subregions play distinct roles in choices between actions and stimuli.J Neurosci28:13775-13785.
Stein JL,Hibar DP,Madsen SK,Khamis M,McMahon KL,de Zubicaray GI,Hansell NK,Montgomery GW,Martin NG,Wright MJ,Saykin AJ,Jack CR Jr,Weiner MW,Toga AW,Thompson PM(2011)Discovery and replication of dopaminerelated gene effects on caudate volume in young and elderly populations(N=1198)using genome-wide search.Mol Psychiatry 16:927-937.
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 densitytric MRI study.Eur J Radiol 82:e715-720.
Tian Q,Chastan N,Bair WN,Resnick SM,Ferrucci L,Studenski SA(2017)The brain map of gait variability in aging,cognitive impairment and dementia.A systematic review.Neurosci Biobehav Rev74:149-162.
Troisi R,Debruyne J,de Hemptinne B(1999)Improvement of hepatic myelopathy after liver transplantation.N Engl J Med 340:151.
Volkow ND,Gur RC,Wang GJ,Fowler JS,Moberg PJ,Ding YS,Hitzemann R,Smith G,Logan J(1998)Association between decline in brain dopamine activity with age and cognitive and motor impairment in healthy individuals.Am J Psychiatry 155:344-349.
Weiller C,Chollet F,Friston KJ,Wise RJ,Frackowiak RS(1992)Functional reorganization of the brain in recovery from striatocapsular infarction in man.Ann Neurol 31:463-472.
Wennberg AMV,Savica R,Mielke MM(2017)Association between various brain pathologies and gait disturbance.Dement Geriatr Cogn Disord 43:128-143.
Yengue P,Adler M,Bouhdid H,Mavroudakis N,Gelin M,Bourgeois N(2001)Hepatic myelopathy after splenorenal shunting:report of one case and review of the literature.Acta Gastroenterol Belg 64:231-233.
Zhang LJ,Qi R,Zhong J,Xu Q,Zheng G,Lu GM(2012)The effect of hepatic encephalopathy,hepatic failure,and portosystemic shunt on brain density of cirrhotic patients:a voxel-based morphometry study.PLoS One 7:e42824.
Zhao H,Liu F,Yue Z,Wang L,Fan Z(2016)Evaluation of mid-and long-term efficacy of shunt limiting for hepatic myelopathy after transjugular intrahepatic portosystemic shunt.Clin Res Hepatol Gastroenterol 40:440-446.
Ahl B,Weissenborn K,van den Hoff J,Fischer-Wasels D,Kastler H,Hecker H,Burchert W(2004)Regional differences in cerebral blood flow and cerebral ammonia metabolism in patients with cirrhosis.Hepatology 40:73-79.
Alexander GE.,Crutcher MD(1990)Functional architecture of basal ganglia circuits:neural substrates of parallel processing.Trends Neurosci 13:266-271.
Amiez C,Petrides M(2014)Neuroimaging evidence of the anatomo-functional organization of the human cingulate motor areas.Cereb Cortex 24:563-578.
Amiez C,Wutte MG,Faillenot I,Petrides M,Burle B,Procyk E(2016)Single subject analyses reveal consistent recruitment of frontal operculum in performance monitoring.Neuroimage 133:266-278.
Ashburner J(2007)A fast diffeomorphic image registration algorithm.Neuroimage 38:95-113.
Berglund K,Fugl-Meyer AR(1986)Upper extremity function in hemiplegia.A cross-validation study of two assessment methods.Scand JRehabil Med 18:155-157.
Caldwell C,Werdiger N,Jakab S,Schilsky M,Arvelakis A,Kulkarni S,Emre S(2010)Use of model for end-stage liver disease exception points for early liver transplantation and successful reversal of hepatic myelopathy with a review of the literature.Liver Transpl 16:818-826.
Campellone JV,Lacomis D,Giuliani MJ,Kroboth FJ(1996)Hepatic myelopathy.Case report with review of the literature.Clin Neurol Neurosurg 98:242-246.
Cauda F,D’Agata F,Sacco K,Duca S,Geminiani G,Vercelli A(2011)Functional connectivity of the insula in the resting brain.Neuroimage 55:8-23.
Chang Y,Jin SU,Kim Y,Kim Y,Kyung MS,Lee HJ,Kim SH,Ahn JH,Park SJ,Jeong KS,Weon YC,Lee H(2013)Decreased brain volumes in manganese-exposed welders.Neurotoxicology 37:182-189.
Chen HJ,Zhu XQ,Shu H(2012)Structural and functional cerebral impairments in cirrhotic patients with a history of overt hepatic encephalopathy.Eur J Radiol 81:2463-2469.
Conn HO,R?ssle M,Levy L,Glocker FX(2006)Portosystemic myelopathy:spastic paraparesis after portosystemic shunting.Scand JGastroenterol 41:619-625.
Demirci M,Tan E,Elibol B,Gediko?lu G,Sariba?O(1992)Spastic paraparesis associated with portal-systemic venous shunting due to congenital hepatic fibrosis.Neurology 42:983-985.
Dumurgier J,Crivello F,Mazoyer B,Ahmed,Tavernier B,Grabli D,Fran?ois C,Tzourio-Mazoyer N,Tzourio C,Elbaz A(2012)MRIatrophy of the caudate nucleus and slower walking speed in the elderly.Neuroimage 60:871-878.
Eriksson H,Magiste K,Plantin LO,Fonnum F,Hedstr?m KG,Theodorsson-Norheim E,Kristensson K,Stalberg E,Heilbronn E(1987)Effects of manganese oxide on monkeys as revealed by a combined neurochemical,histological and neurophysiological evaluation.Arch Toxicol 61:46-52.
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.Hepatology35:716-721.
Ferreira CR,Gahl WA(2017)Disorders of metal metabolism.Transl Sci Rare Dis 2:101-139.
Finelli PF,Gupta F,Zeevi N(2007)Neuroimaging of bilateral caudate infarction manifesting as Parkinsonian gait disorder.Conn Med71:149-150.
García-Lezana T,Oria M,Romero-Giménez J,BovéJ,Vila M,GenescàJ,Chavarria L,Cordoba J(2017)Cerebellar neurodegeneration in a new rat model of episodic hepatic encephalopathy.J Cereb Blood Flow Metab 37:927-937.
Goto M,Abe O,Aoki S,Hayashi N,Miyati T,Takao H,Iwatsubo T,Yamashita F,Matsuda H,Mori H,Kunimatsu A,Ino K,Yano K,Ohtomo K(2013)Diffeomorphic anatomical registration through exponentiated lie algebra provides reduced effect of scanner for cortex volumetry with atlas-based method in healthy subjects.Neuroradiology 55:869-875.
Guevara M,Baccaro ME,Gomez-Anson B(2011)Cerebral magnetic resonance imaging reveals marked abnormalities of brain tissue density in patients with cirrhosis without overt hepatic encephalopathy.J Hepatol 55:564-573.
Haber SN(2016)Corticostriatal circuitry.Dialogues Clin Neurosci18:7-21.
Kulisevsky J,Pujol J,BalanzóJ,JunquéC,Deus J,Capdevilla A,Villanueva C(1992)Pallidal hyperintensity on magnetic resonance imaging in cirrhotic patients:clinical correlations.Hepatology 16:1382-1388.
Layrargues GP,Rose C,Spahr L,Zayed J,Normandin L,Butterworth RF(1998)Role of manganese in the pathogenesis of portal-systemic encephalopathy.Metab Brain Dis 13:311-317.
Lefer LG,Vogel FS(1972)Encephalomyelopathy with hepatic cirrhosis following portosystemic venous shunts.Arch Pathol 93:91-97.
Leigh AD,Card WI(1949)Hepatolenticular degeneration:a case associated with postero-lateral column degeneration.J Neuropathol Exp Neurol 8:338-346.
Liversedge LA,Rawson MD(1966)Myelopathy in hepatic disease and portosystemic venous anastomosis.Lancet 1:277-279.
Maeda H,Sato M,Yoshikawa A,Kimura M,Sonomura T,Terada M,Kishi K(1997)Brain MR imaging in patients with hepatic cirrhosis:relationship between high intensity signal in basal ganglia on T1-weighted images and elemental concentrations in brain.Neuroradiology 39:546-550.
Marshall RS,Zarahn E,Alon L,Minzer B,Lazar RM,Krakauer JW(2009)Early imaging correlates of subsequent motor recovery after stroke.Ann Neurol 65:596-602.
McFarland NR.,Haber SN(2002)Thalamic relay nuclei of the basal ganglia form both reciprocal and nonreciprocal cortical connections,linking multiple frontal cortical areas.J Neurosci 22:8117-8132.
Mendoza G,Marti-Fàbregas J,Kulisevsky J,Escartín A(1994)Hepatic myelopathy:a rare complication of portacaval shunt.Eur Neurol34:209-212.
Moreno-Alcázar A,Ramos-Quiroga JA,Radua J,Salavert J,Palomar G,Bosch R,Salvador R,Blanch J,Casas M,McKenna PJ,Pomarol-Clotet E(2016)Brain abnormalities in adults with attention deficit hyperactivity disorder revealed by voxel-based morphometry.Psychiatry Res Neuroimaging 254:41-47.
Mutschler I,Wieckhorst B,Kowalevski S,Derix J,Wentlandt J,Schulze-Bonhage A,Ball T(2009)Functional organization of the human anterior insular cortex.Neurosci Lett 457:66-70.
Nardone R,Buratti T,Oliviero A,Lochmann A,Tezzon F(2006)Corticospinal involvement in patients with a portosystemic shunt due to liver cirrhosis:a MEP study.J Neurol 253:81-85.
Navarro-Cebrian A,Knight RT,Kayser AS(2013)Error-monitoring and post-error compensations:dissociation between perceptual failures and motor errors with and without awareness.J Neurosci33:12375-12383.
Obeso JA,Rodriguez-Oroz MC,Stamelou M,Bhatia KP,Burn DJ(2014)The expanding universe of disorders of the basal ganglia.Lancet 384:523-531.
Pomier-Layrargues G,Spahr L,Butterworth RF(1995)Increased manganese concentration in pallidum of cirrhotic patients.Lancet345:735.
Procyk E,Wilson CR,Stoll FM,Faraut MC,Petrides M,Amiez C(2016)Midcingulate motor map and feedback detection:converging data from humans and monkeys.Cereb Cortex 26:467-476.
Pugh RN,Murray-Lyon IM,Dawson JL,Pietroni MC,Williams R(1973)Transection of the oesophagus for bleeding oesophageal varices.Br J Surg 60:646-649.
Rao AK,Muratori L,Louis ED,Moskowitz CB,Marder KS(2008)Spectrum of gait impairments in presymptomatic and symptomatic Huntington’s disease.Mov Disord 23:1100-1107.
Rose C,Butterworth RF,Zayed J,Normandin L,Todd K,Michalak A,Spahr L,Huet PM,Pomier-Layrargues G(1999)Manganese deposition in basal ganglia structures results from both portal-systemic shunting and liver dysfunction.Gastroenterology 117:640-644.
Rudebeck PH,Behrens TE,Kennerley SW,Baxter MG,Buckley MJ,Walton ME,Rushworth MF(2008)Frontal cortex subregions play distinct roles in choices between actions and stimuli.J Neurosci28:13775-13785.
Stein JL,Hibar DP,Madsen SK,Khamis M,McMahon KL,de Zubicaray GI,Hansell NK,Montgomery GW,Martin NG,Wright MJ,Saykin AJ,Jack CR Jr,Weiner MW,Toga AW,Thompson PM(2011)Discovery and replication of dopaminerelated gene effects on caudate volume in young and elderly populations(N=1198)using genome-wide search.Mol Psychiatry 16:927-937.
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 densitytric MRI study.Eur J Radiol 82:e715-720.
Tian Q,Chastan N,Bair WN,Resnick SM,Ferrucci L,Studenski SA(2017)The brain map of gait variability in aging,cognitive impairment and dementia.A systematic review.Neurosci Biobehav Rev74:149-162.
Troisi R,Debruyne J,de Hemptinne B(1999)Improvement of hepatic myelopathy after liver transplantation.N Engl J Med 340:151.
Volkow ND,Gur RC,Wang GJ,Fowler JS,Moberg PJ,Ding YS,Hitzemann R,Smith G,Logan J(1998)Association between decline in brain dopamine activity with age and cognitive and motor impairment in healthy individuals.Am J Psychiatry 155:344-349.
Weiller C,Chollet F,Friston KJ,Wise RJ,Frackowiak RS(1992)Functional reorganization of the brain in recovery from striatocapsular infarction in man.Ann Neurol 31:463-472.
Wennberg AMV,Savica R,Mielke MM(2017)Association between various brain pathologies and gait disturbance.Dement Geriatr Cogn Disord 43:128-143.
Yengue P,Adler M,Bouhdid H,Mavroudakis N,Gelin M,Bourgeois N(2001)Hepatic myelopathy after splenorenal shunting:report of one case and review of the literature.Acta Gastroenterol Belg 64:231-233.
Zhang LJ,Qi R,Zhong J,Xu Q,Zheng G,Lu GM(2012)The effect of hepatic encephalopathy,hepatic failure,and portosystemic shunt on brain density of cirrhotic patients:a voxel-based morphometry study.PLoS One 7:e42824.
Zhao H,Liu F,Yue Z,Wang L,Fan Z(2016)Evaluation of mid-and long-term efficacy of shunt limiting for hepatic myelopathy after transjugular intrahepatic portosystemic shunt.Clin Res Hepatol Gastroenterol 40:440-446.