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Published in: European Radiology 1/2018

01-01-2018 | Magnetic Resonance

Disrupted topological organization of brain structural network associated with prior overt hepatic encephalopathy in cirrhotic patients

Authors: Hua-Jun Chen, Hai-Bin Shi, Long-Feng Jiang, Lan Li, Rong Chen

Published in: European Radiology | Issue 1/2018

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Abstract

Objectives

To investigate structural brain connectome alterations in cirrhotic patients with prior overt hepatic encephalopathy (OHE).

Methods

Seventeen cirrhotic patients with prior OHE (prior-OHE), 18 cirrhotic patients without prior OHE (non-prior-OHE) and 18 healthy controls (HC) underwent diffusion tensor imaging. Neurocognitive functioning was assessed with Psychometric Hepatic Encephalopathy Score (PHES). Using a probabilistic fibre tracking approach, we depicted the whole-brain structural network as a connectivity matrix of 90 regions (derived from the Automated Anatomic Labeling atlas). Graph theory-based analyses were performed to analyse topological properties of the brain network.

Results

The analysis of variance showed significant group effects on several topological properties, including network strength, global efficiency and local efficiency. A progressive decrease trend for these metrics was found from non-prior-OHE to prior-OHE, compared with HC. Among the three groups, the regions with altered nodal efficiency were mainly distributed in the frontal and occipital cortices, paralimbic system and subcortical regions. The topological metrics, such as network strength and global efficiency, were correlated with PHES among cirrhotic patients.

Conclusions

The cirrhotic patients developed structural brain connectome alterations; this is aggravated by prior OHE episode. Disrupted topological organization of the brain structural network may account for cognitive impairments related to prior OHE.

Key points

Altered structural brain connectome is found in cirrhotic patients.
Structural brain connectome alterations could be aggravated by prior-OHE episode.
Altered structural brain connectome may account for cognitive impairments associated with prior OHE.
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Literature
2.
go back to reference Stepanova M, Mishra A, Venkatesan C, Younossi ZM (2012) In-hospital mortality and economic burden associated with hepatic encephalopathy in the United States from 2005 to 2009. Clin Gastroenterol Hepatol 10(1034-1041), e1031 Stepanova M, Mishra A, Venkatesan C, Younossi ZM (2012) In-hospital mortality and economic burden associated with hepatic encephalopathy in the United States from 2005 to 2009. Clin Gastroenterol Hepatol 10(1034-1041), e1031
3.
go back to reference Bustamante J, Rimola A, Ventura PJ et al (1999) Prognostic significance of hepatic encephalopathy in patients with cirrhosis. J Hepatol 30:890–895CrossRefPubMed Bustamante J, Rimola A, Ventura PJ et al (1999) Prognostic significance of hepatic encephalopathy in patients with cirrhosis. J Hepatol 30:890–895CrossRefPubMed
4.
go back to reference Bajaj JS, Schubert CM, Heuman DM et al (2010) Persistence of cognitive impairment after resolution of overt hepatic encephalopathy. Gastroenterology 138:2332–2340CrossRefPubMedPubMedCentral Bajaj JS, Schubert CM, Heuman DM et al (2010) Persistence of cognitive impairment after resolution of overt hepatic encephalopathy. Gastroenterology 138:2332–2340CrossRefPubMedPubMedCentral
5.
go back to reference Umapathy S, Dhiman RK, Grover S, Duseja A, Chawla YK (2014) Persistence of cognitive impairment after resolution of overt hepatic encephalopathy. Am J Gastroenterol 109:1011–1019CrossRefPubMed Umapathy S, Dhiman RK, Grover S, Duseja A, Chawla YK (2014) Persistence of cognitive impairment after resolution of overt hepatic encephalopathy. Am J Gastroenterol 109:1011–1019CrossRefPubMed
6.
go back to reference Riggio O, Ridola L, Pasquale C et al (2011) Evidence of persistent cognitive impairment after resolution of overt hepatic encephalopathy. Clin Gastroenterol Hepatol 9:181–183CrossRefPubMed Riggio O, Ridola L, Pasquale C et al (2011) Evidence of persistent cognitive impairment after resolution of overt hepatic encephalopathy. Clin Gastroenterol Hepatol 9:181–183CrossRefPubMed
7.
go back to reference Bajaj JS, Heuman DM, Sterling RK et al (2015) Validation of EncephalApp, smartphone-based Stroop test, for the diagnosis of covert hepatic encephalopathy. Clin Gastroenterol Hepatol 13(1828-1835), e1821 Bajaj JS, Heuman DM, Sterling RK et al (2015) Validation of EncephalApp, smartphone-based Stroop test, for the diagnosis of covert hepatic encephalopathy. Clin Gastroenterol Hepatol 13(1828-1835), e1821
8.
go back to reference Bajaj JS, Thacker LR, Heuman DM et al (2013) The Stroop smartphone application is a short and valid method to screen for minimal hepatic encephalopathy. Hepatology 58:1122–1132CrossRefPubMedPubMedCentral Bajaj JS, Thacker LR, Heuman DM et al (2013) The Stroop smartphone application is a short and valid method to screen for minimal hepatic encephalopathy. Hepatology 58:1122–1132CrossRefPubMedPubMedCentral
9.
go back to reference Allampati S, Mullen KD (2014) Does overt hepatic encephalopathy cause persistent cognitive defects even after successful liver transplantation? Liver Transpl 20:874–875CrossRefPubMed Allampati S, Mullen KD (2014) Does overt hepatic encephalopathy cause persistent cognitive defects even after successful liver transplantation? Liver Transpl 20:874–875CrossRefPubMed
10.
go back to reference Campagna F, Montagnese S, Schiff S et al (2014) Cognitive impairment and electroencephalographic alterations before and after liver transplantation: what is reversible? Liver Transpl 20:977–986CrossRefPubMed Campagna F, Montagnese S, Schiff S et al (2014) Cognitive impairment and electroencephalographic alterations before and after liver transplantation: what is reversible? Liver Transpl 20:977–986CrossRefPubMed
11.
go back to reference 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 15:184–192CrossRefPubMed 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 15:184–192CrossRefPubMed
12.
go back to reference Frederick RT (2012) Extent of reversibility of hepatic encephalopathy following liver transplantation. Clin Liver Dis 16:147–158CrossRefPubMed Frederick RT (2012) Extent of reversibility of hepatic encephalopathy following liver transplantation. Clin Liver Dis 16:147–158CrossRefPubMed
13.
go back to reference Guevara M, Baccaro ME, Gomez-Anson B et al (2011) Cerebral magnetic resonance imaging reveals marked abnormalities of brain tissue density in patients with cirrhosis without overt hepatic encephalopathy. J Hepatol 55:564–573CrossRefPubMed Guevara M, Baccaro ME, Gomez-Anson B et al (2011) Cerebral magnetic resonance imaging reveals marked abnormalities of brain tissue density in patients with cirrhosis without overt hepatic encephalopathy. J Hepatol 55:564–573CrossRefPubMed
14.
go back to reference Chen HJ, Wang Y, Zhu XQ, Cui Y, Chen YC, Teng GJ (2012) White matter abnormalities correlate with neurocognitive performance in patients with HBV-related cirrhosis. J Neurol Sci 321:65–72CrossRefPubMed Chen HJ, Wang Y, Zhu XQ, Cui Y, Chen YC, Teng GJ (2012) White matter abnormalities correlate with neurocognitive performance in patients with HBV-related cirrhosis. J Neurol Sci 321:65–72CrossRefPubMed
15.
16.
go back to reference Bressler SL, Menon V (2010) Large-scale brain networks in cognition: emerging methods and principles. Trends Cogn Sci 14:277–290CrossRefPubMed Bressler SL, Menon V (2010) Large-scale brain networks in cognition: emerging methods and principles. Trends Cogn Sci 14:277–290CrossRefPubMed
17.
go back to reference Barkhof F, Haller S, Rombouts SA (2014) Resting-state functional MR imaging: a new window to the brain. Radiology 272:29–49CrossRefPubMed Barkhof F, Haller S, Rombouts SA (2014) Resting-state functional MR imaging: a new window to the brain. Radiology 272:29–49CrossRefPubMed
18.
go back to reference Bullmore E, Sporns O (2009) Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10:186–198CrossRefPubMed Bullmore E, Sporns O (2009) Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10:186–198CrossRefPubMed
19.
go back to reference Zhang L, Qi R, Wu S et al (2012) Brain default-mode network abnormalities in hepatic encephalopathy: a resting-state functional MRI study. Hum Brain Mapp 33:1384–1392CrossRefPubMed Zhang L, Qi R, Wu S et al (2012) Brain default-mode network abnormalities in hepatic encephalopathy: a resting-state functional MRI study. Hum Brain Mapp 33:1384–1392CrossRefPubMed
20.
go back to reference Jao T, Schroter M, Chen CL et al (2015) Functional brain network changes associated with clinical and biochemical measures of the severity of hepatic encephalopathy. Neuroimage 122:332–344CrossRefPubMed Jao T, Schroter M, Chen CL et al (2015) Functional brain network changes associated with clinical and biochemical measures of the severity of hepatic encephalopathy. Neuroimage 122:332–344CrossRefPubMed
21.
go back to reference Chen HJ, Jiao Y, Zhu XQ et al (2013) Brain dysfunction primarily related to previous overt hepatic encephalopathy compared with minimal hepatic encephalopathy: resting-state functional MR imaging demonstration. Radiology 266:261–270CrossRefPubMed Chen HJ, Jiao Y, Zhu XQ et al (2013) Brain dysfunction primarily related to previous overt hepatic encephalopathy compared with minimal hepatic encephalopathy: resting-state functional MR imaging demonstration. Radiology 266:261–270CrossRefPubMed
22.
go back to reference Griffa A, Baumann PS, Thiran JP, Hagmann P (2013) Structural connectomics in brain diseases. Neuroimage 80:515–526CrossRefPubMed Griffa A, Baumann PS, Thiran JP, Hagmann P (2013) Structural connectomics in brain diseases. Neuroimage 80:515–526CrossRefPubMed
23.
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 35:716–721CrossRefPubMed 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 35:716–721CrossRefPubMed
24.
go back to reference Chen HJ, Jiang LF, Sun T, Liu J, Chen QF, Shi HB (2015) Resting-state functional connectivity abnormalities correlate with psychometric hepatic encephalopathy score in cirrhosis. Eur J Radiol 84:2287–2295CrossRefPubMed Chen HJ, Jiang LF, Sun T, Liu J, Chen QF, Shi HB (2015) Resting-state functional connectivity abnormalities correlate with psychometric hepatic encephalopathy score in cirrhosis. Eur J Radiol 84:2287–2295CrossRefPubMed
25.
go back to reference Herskovits EH, Hong LE, Kochunov P, Sampath H, Chen R (2015) Edge-centered DTI connectivity analysis: application to schizophrenia. Neuroinformatics 13:501–509CrossRefPubMedPubMedCentral Herskovits EH, Hong LE, Kochunov P, Sampath H, Chen R (2015) Edge-centered DTI connectivity analysis: application to schizophrenia. Neuroinformatics 13:501–509CrossRefPubMedPubMedCentral
26.
go back to reference Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52:1059–1069CrossRefPubMed Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52:1059–1069CrossRefPubMed
27.
go back to reference Bai F, Shu N, Yuan Y et al (2012) Topologically convergent and divergent structural connectivity patterns between patients with remitted geriatric depression and amnestic mild cognitive impairment. J Neurosci 32:4307–4318CrossRefPubMed Bai F, Shu N, Yuan Y et al (2012) Topologically convergent and divergent structural connectivity patterns between patients with remitted geriatric depression and amnestic mild cognitive impairment. J Neurosci 32:4307–4318CrossRefPubMed
28.
go back to reference Korgaonkar MS, Fornito A, Williams LM, Grieve SM (2014) Abnormal structural networks characterize major depressive disorder: a connectome analysis. Biol Psychiatry 76:567–574CrossRefPubMed Korgaonkar MS, Fornito A, Williams LM, Grieve SM (2014) Abnormal structural networks characterize major depressive disorder: a connectome analysis. Biol Psychiatry 76:567–574CrossRefPubMed
29.
go back to reference Hahn A, Kranz GS, Kublbock M et al (2015) Structural connectivity networks of transgender people. Cereb Cortex 25:3527–3534CrossRefPubMed Hahn A, Kranz GS, Kublbock M et al (2015) Structural connectivity networks of transgender people. Cereb Cortex 25:3527–3534CrossRefPubMed
30.
go back to reference Lei D, Li K, Li L et al (2015) Disrupted functional brain connectome in patients with posttraumatic stress disorder. Radiology 276:818–827CrossRefPubMed Lei D, Li K, Li L et al (2015) Disrupted functional brain connectome in patients with posttraumatic stress disorder. Radiology 276:818–827CrossRefPubMed
31.
go back to reference Hsu TW, Wu CW, Cheng YF et al (2012) Impaired small-world network efficiency and dynamic functional distribution in patients with cirrhosis. PLoS One 7, e35266CrossRefPubMedPubMedCentral Hsu TW, Wu CW, Cheng YF et al (2012) Impaired small-world network efficiency and dynamic functional distribution in patients with cirrhosis. PLoS One 7, e35266CrossRefPubMedPubMedCentral
32.
go back to reference Chen HJ, Zhu XQ, Shu H et al (2012) Structural and functional cerebral impairments in cirrhotic patients with a history of overt hepatic encephalopathy. Eur J Radiol 81:2463–2469CrossRefPubMed Chen HJ, Zhu XQ, Shu H et al (2012) Structural and functional cerebral impairments in cirrhotic patients with a history of overt hepatic encephalopathy. Eur J Radiol 81:2463–2469CrossRefPubMed
33.
go back to reference Buckner RL, Andrews-Hanna JR, Schacter DL (2008) The brain's default network: anatomy, function, and relevance to disease. Ann N Y Acad Sci 1124:1–38CrossRefPubMed Buckner RL, Andrews-Hanna JR, Schacter DL (2008) The brain's default network: anatomy, function, and relevance to disease. Ann N Y Acad Sci 1124:1–38CrossRefPubMed
34.
go back to reference Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, Raichle ME (2005) The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci U S A 102:9673–9678CrossRefPubMedPubMedCentral Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, Raichle ME (2005) The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci U S A 102:9673–9678CrossRefPubMedPubMedCentral
35.
go back to reference Tao R, Zhang J, You Z et al (2013) The thalamus in cirrhotic patients with and without hepatic encephalopathy: a volumetric MRI study. Eur J Radiol 82:e715–720CrossRefPubMed Tao R, Zhang J, You Z et al (2013) The thalamus in cirrhotic patients with and without hepatic encephalopathy: a volumetric MRI study. Eur J Radiol 82:e715–720CrossRefPubMed
36.
go back to reference Qi R, Zhang LJ, Zhong J et al (2013) Disrupted thalamic resting-state functional connectivity in patients with minimal hepatic encephalopathy. Eur J Radiol 82:850–856CrossRefPubMed Qi R, Zhang LJ, Zhong J et al (2013) Disrupted thalamic resting-state functional connectivity in patients with minimal hepatic encephalopathy. Eur J Radiol 82:850–856CrossRefPubMed
37.
go back to reference Zhang LJ, Zheng G, Zhang L et al (2012) Altered brain functional connectivity in patients with cirrhosis and minimal hepatic encephalopathy: a functional MR imaging study. Radiology 265:528–536CrossRefPubMed Zhang LJ, Zheng G, Zhang L et al (2012) Altered brain functional connectivity in patients with cirrhosis and minimal hepatic encephalopathy: a functional MR imaging study. Radiology 265:528–536CrossRefPubMed
38.
go back to reference Haber SN, Calzavara R (2009) The cortico-basal ganglia integrative network: the role of the thalamus. Brain Res Bull 78:69–74CrossRefPubMed Haber SN, Calzavara R (2009) The cortico-basal ganglia integrative network: the role of the thalamus. Brain Res Bull 78:69–74CrossRefPubMed
39.
40.
go back to reference Hope T, Westlye LT, Bjornerud A (2012) The effect of gradient sampling schemes on diffusion metrics derived from probabilistic analysis and tract-based spatial statistics. Magn Reson Imaging 30:402–412CrossRefPubMed Hope T, Westlye LT, Bjornerud A (2012) The effect of gradient sampling schemes on diffusion metrics derived from probabilistic analysis and tract-based spatial statistics. Magn Reson Imaging 30:402–412CrossRefPubMed
41.
go back to reference Vaessen MJ, Hofman PA, Tijssen HN, Aldenkamp AP, Jansen JF, Backes WH (2010) The effect and reproducibility of different clinical DTI gradient sets on small world brain connectivity measures. Neuroimage 51:1106–1116CrossRefPubMed Vaessen MJ, Hofman PA, Tijssen HN, Aldenkamp AP, Jansen JF, Backes WH (2010) The effect and reproducibility of different clinical DTI gradient sets on small world brain connectivity measures. Neuroimage 51:1106–1116CrossRefPubMed
42.
go back to reference Zalesky A, Fornito A, Harding IH et al (2010) Whole-brain anatomical networks: does the choice of nodes matter? Neuroimage 50:970–983CrossRefPubMed Zalesky A, Fornito A, Harding IH et al (2010) Whole-brain anatomical networks: does the choice of nodes matter? Neuroimage 50:970–983CrossRefPubMed
43.
go back to reference Chavarria L, Alonso J, Garcia-Martinez R et al (2011) Biexponential analysis of diffusion-tensor imaging of the brain in patients with cirrhosis before and after liver transplantation. AJNR Am J Neuroradiol 32:1510–1517CrossRefPubMed Chavarria L, Alonso J, Garcia-Martinez R et al (2011) Biexponential analysis of diffusion-tensor imaging of the brain in patients with cirrhosis before and after liver transplantation. AJNR Am J Neuroradiol 32:1510–1517CrossRefPubMed
44.
go back to reference 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 54:1154–1160CrossRefPubMed 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 54:1154–1160CrossRefPubMed
Metadata
Title
Disrupted topological organization of brain structural network associated with prior overt hepatic encephalopathy in cirrhotic patients
Authors
Hua-Jun Chen
Hai-Bin Shi
Long-Feng Jiang
Lan Li
Rong Chen
Publication date
01-01-2018
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 1/2018
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-017-4887-8

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