Top

Published in:

01-02-2015 | Review Article

PET and MR imaging of neuroinflammation in hepatic encephalopathy

Authors: Yun Yan Su, Gui Fen Yang, Guang Ming Lu, Shawn Wu, Long Jiang Zhang

Published in: Metabolic Brain Disease | Issue 1/2015

Abstract

Neurological or psychiatric abnormalities associated with hepatic encephalopathy (HE) range from subclinical findings to coma. HE is commonly accompanied with the accumulation of toxic substances in bloodstream. The toxicity effect of hyperammonemia on astrocyte, such as the alteration in neurotransmission, oxidative stress, astrocyte swelling, is considered as an important factor in the pathogenesis of HE. Besides, neuroinflammation has captured more attention in the process of HE, but the mechanism of neuroinflammation leading to HE remains unclear. Molecular imaging techniques such as positron emission tomography (PET) and magnetic resonance imaging (MRI) targeting activated microglia and/ or other mediators appear to be promising noninvasive approaches to assess HE. This review focuses on novel imaging and therapy strategies of neuroinflammation in HE.

Abourbeh G, Thézé B, Maroy R, Dubois A, Brulon V, Fontyn Y, Dollé F, Tavitian B, Boisgard R (2012) Imaging microglial/macrophage activation in spinal cords of experimental autoimmune encephalomyelitis rats by positron emission tomography using the mitochondrial 18 kDa translocator protein radioligand [(1)(8)F]DPA-714. J Neurosci 32(17):5728–5736PubMed

Agusti A, Dziedzic JL, Hernandez-Rabaza V, Guilarte TR, Felipo V (2014) Rats with minimal hepatic encephalopathy due to portacaval shunt show differential increase of translocator protein (18 kDa) binding in different brain areas, which is not affected by chronic MAP-kinase p38 inhibition. Metab Brain Dis 29(4):955–963

Amor S, Peferoen LA, Vogel DY, Breur M, van der Valk P, Baker D, van Noort JM (2014) Inflammation in neurodegenerative diseases—an update. Immunology 142(2):151–166PubMed

Antunes IF, Doorduin J, Haisma HJ, Elsinga PH, van Waarde A, Willemsen AT, Dierckx RA, de Vries EF (2012) 18 F-FEAnGA for PET of beta-glucuronidase activity in neuroinflammation. J Nucl Med 53(3):451–458PubMed

Arlicot N, Vercouillie J, Ribeiro MJ, Tauber C, Venel Y, Baulieu JL, Maia S, Corcia P, Stabin MG, Reynolds A, Kassiou M, Guilloteau D (2012) Initial evaluation in healthy humans of [18 F]DPA-714, a potential PET biomarker for neuroinflammation. Nucl Med Biol 39(4):570–578PubMed

Awde AR, Boisgard R, Thézé B, Dubois A, Zheng J, Dollé F, Jacobs AH, Tavitian B, Winkeler A (2013) The translocator protein radioligand 18 F-DPA-714 monitors antitumor effect of erufosine in a rat 9 L intracranial glioma model. J Nucl Med 54(12):2125–2131PubMed

Bajaj JS (2014) The role of microbiota in hepatic encephalopathy. Gut Microbes 5(3):397–403PubMed

Bartels AL, Willemsen AT, Doorduin J, de Vries EF, Dierckx RA, Leenders KL (2010) [11C]-PK11195 PET: quantification of neuroinflammation and a monitor of anti-inflammatory treatment in Parkinson’s disease? Parkinsonism Relat Disord 16(1):57–59PubMed

Bemeur C, Butterworth RF (2013) Liver-brain proinflammatory signalling in acute liver failure: role in the pathogenesis of hepatic encephalopathy and brain edema. Metab Brain Dis 28(2):145–150PubMed

Berding GBR, Buchert R, Chierichetti F, Grover VP, Kato A, Keiding S, Taylor-Robinson SD (2009) International Society for hepatic encephalopathy and nitrogen metabolism (ISHEN). Radiotracer imaging studies in hepatic encephalopathy: ISHEN practice guidelines. Liver Int 29(5):621–628PubMed

Bladowska JZA, Knysz B, Małyszczak K, Kołtowska A, Szewczyk P, Gąsiorowski J, Furdal M, Sąsiadek MJ (2013) Evaluation of early cerebral metabolic, perfusion and microstructural changes in HCV-positive patients: a pilot study. J Hepatol 59(4):651–657PubMed

Bladowska J, Knysz B, Zimny A, Małyszczak K, Kołtowska A, Szewczyk P, Gąsiorowski J, Furdal M, Sąsiadek MJ (2014) Value of perfusion-weighted MR imaging in the assessment of early cerebral alterations in neurologically asymptomatic HIV-1-positive and HCV-positive patients. PLoS ONE 9(7):e102214PubMedCentralPubMed

Bokemeyer M, Ding XQ, Goldbecker A, Raab P, Heeren M, Arvanitis D, Tillmann HL, Lanfermann H, Weissenborn K (2011) Evidence for neuroinflammation and neuroprotection in HCV infection-associated encephalopathy. Gut 60(3):370–377PubMed

Boutin H, Prenant C, Maroy R, Galea J, Greenhalgh AD, Smigova A, Cawthorne C, Julyan P, Wilkinson SM, Banister SD, Brown G, Herholz K, Kassiou M, Rothwell NJ (2013) [18F]DPA-714: direct comparison with [11C]PK11195 in a model of cerebral ischemia in rats. PLoS ONE 8(2):e56441PubMedCentralPubMed

Butterworth RF (2011a) Hepatic encephalopathy: a central neuroinflammatory disorder? Hepatology 53(4):1372–1376PubMed

Butterworth RF (2011b) Neuroinflammation in acute liver failure: mechanisms and novel therapeutic targets. Neurochem Int 59(6):830–836PubMed

Butterworth RF (2013) The liver-brain axis in liver failure: neuroinflammation and encephalopathy. Nat Rev Gastroenterol Hepatol 10(9):522–528PubMed

Cagnin A, Taylor-Robinson SD, Forton DM, Banati RB (2006) In vivo imaging of cerebral “peripheral benzodiazepine binding sites” in patients with hepatic encephalopathy. Gut 55(4):547–553PubMedCentralPubMed

Cai W, Chen X (2006) Anti-angiogenic cancer therapy based on integrin alphavbeta3 antagonism. Anticancer Agents Med Chem 6(5):407–428PubMed

Candelario-Jalil E, Yang Y, Rosenberg GA (2009) Diverse roles of matrix metalloproteinases and tissue inhibitors of metalloproteinases in neuroinflammation and cerebral ischemia. Neuroscience 158(3):983–994PubMedCentralPubMed

Cao Q, Cai W, Li ZB, Chen K, He L, Li HC, Hui M, Chen X (2007) PET imaging of acute and chronic inflammation in living mice. Eur J Nucl Med Mol Imaging 34(11):1832–1842PubMed

Cauli O, Rodrigo R, Piedrafita B, Llansola M, Mansouri MT, Felipo V (2009) Neuroinflammation contributes to hypokinesia in rats with hepatic encephalopathy: ibuprofen restores its motor activity. J Neurosci Res 87(6):1369–1374PubMed

Chang L, Munsaka SM, Kraft-Terry S, Ernst T (2013) Magnetic resonance spectroscopy to assess neuroinflammation and neuropathic pain. J Neuroimmune Pharm 8(3):576–593

Chauveau F, Van Camp N, Dollé F, Kuhnast B, Hinnen F, Damont A, Boutin H, James M, Kassiou M, Tavitian B (2009) Comparative evaluation of the translocator protein radioligands 11C-DPA-713, 18 F-DPA-714, and 11C-PK11195 in a rat model of acute neuroinflammation. J Nucl Med 50(3):468–476PubMed

Chavarria L, Cordoba J (2014) Magnetic resonance of the brain in chronic and acute liver failure. Metab Brain Dis 29(4):937–944

Chavarria L, Oria M, Romero-Giménez J, Alonso J, Lope-Piedrafita S, Cordoba J (2013) Brain magnetic resonance in experimental acute-on-chronic liver failure. Liver Int 33(2):294–300PubMed

Chin CL, Pai M, Bousquet PF, Schwartz AJ, O’Connor EM, Nelson CM, Hradil VP, Cox BF, McRae BL, Fox GB (2009) Distinct spatiotemporal pattern of CNS lesions revealed by USPIO-enhanced MRI in MOG-induced EAE rats implicates the involvement of spino-olivocerebellar pathways. J Neuroimmunol 211(1–2):49–55PubMed

Ching AS, Kuhnast B, Damont A, Roeda D, Tavitian B, Dollé F (2012) Current paradigm of the 18-kDa translocator protein (TSPO) as a molecular target for PET imaging in neuroinflammation and neurodegenerative diseases. Insights Imaging 3(1):111–119PubMedCentralPubMed

Ciarmiello A (2011) Imaging of neuroinflammation. Eur J Nucl Med Mol Imaging 38(12):2198–2201PubMed

Ciecko-Michalska I, Szczepanek M, Slowik A, Mach T (2012) Pathogenesis of hepatic encephalopathy. Gastroenterol Res Pract 2012:642108PubMedCentralPubMed

Colombo M, Carregal-Romero S, Casula MF, Gutiérrez L, Morales MP, Böhm IB, Heverhagen JT, Prosperi D, Parak WJ (2012) Biological applications of magnetic nanoparticles. Chem Soc Rev 41(11):4306–4334PubMed

Corcia P, Tauber C, Vercoullie J, Arlicot N, Prunier C, Praline J, Nicolas G, Venel Y, Hommet C, Baulieu JL, Cottier JP, Roussel C, Kassiou M, Guilloteau D, Ribeiro MJ (2012) Molecular imaging of microglial activation in amyotrophic lateral sclerosis. PLoS ONE 7(12):e52941PubMedCentralPubMed

Cordoba J (2014) Hepatic encephalopathy: from the pathogenesis to the new treatments. ISRN Hepatol 2014:236268. doi:10.1155/2014/236268

Cui Y, Takashima T, Takashima-Hirano M, Wada Y, Shukuri M, Tamura Y, Doi H, Onoe H, Kataoka Y, Watanabe Y (2009) 11C-PK11195 PET for the in vivo evaluation of neuroinflammation in the rat brain after cortical spreading depression. J Nucl Med 50(11):1904–1911PubMed

Czeh M, Gressens P, Kaindl AM (2011) The yin and yang of microglia. Dev Neurosci 33(3–4):199–209PubMed

David S, Kroner A (2011) Repertoire of microglial and macrophage responses after spinal cord injury. Nat Rev Neurosci 12(7):388–399PubMed

Deddens LH, Van Tilborg GA, Mulder WJ, De Vries HE, Dijkhuizen RM (2012) Imaging neuroinflammation after stroke: current status of cellular and molecular MRI strategies. Cerebrovasc Dis 33(4):392–402PubMed

Dennis CV, Sheahan PJ, Graeber MB, Sheedy DL, Kril JJ, Sutherland GT (2014) Microglial proliferation in the brain of chronic alcoholics with hepatic encephalopathy. Metab Brain Dis 29(4):1027–1039

Dhiman RK (2013) Gut microbiota and hepatic encephalopathy. Metab Brain Dis 28(2):321–326PubMed

Doorduin J, Klein HC, Dierckx RA, James M, Kassiou M, de Vries EF (2009) [11C]-DPA-713 and [18 F]-DPA-714 as new PET tracers for TSPO: a comparison with [11C]-(R)-PK11195 in a rat model of herpes encephalitis. Mol Imaging Biol 11(6):386–398PubMedCentralPubMed

Dou Y, Wu HJ, Li HQ, Qin S, Wang YE, Li J, Lou HF, Chen Z, Li XM, Luo QM, Duan S (2012) Microglial migration mediated by ATP-induced ATP release from lysosomes. Cell Res 22(6):1022–1033PubMedCentralPubMed

Eckelman WC, Reba RC, Kelloff GJ (2008) Targeted imaging: an important biomarker for understanding disease progression in the era of personalized medicine. Drug Discov Today 13(17–18):748–759PubMed

Ellrichmann G, Reick C, Saft C, Linker RA (2013) The role of the immune system in Huntington’s disease. Clin Dev Immunol 2013:541259PubMedCentralPubMed

Felipo V, Urios A, Montesinos E, Molina I, Garcia-Torres ML, Civera M, Olmo JA, Ortega J, Martinez-Valls J, Serra MA, Cassinello N, Wassel A, Jordá E, Montoliu C (2012) Contribution of hyperammonemia and inflammatory factors to cognitive impairment in minimal hepatic encephalopathy. Metab Brain Dis 27(1):51–58PubMed

Floch MH (2014) Intestinal microbiota metabolism of a prebiotic to treat hepatic encephalopathy. Clin Gastroenterol Hepatol doi:10.1016/j.cgh.2014.06.008

Fries AW, Dadsetan S, Keiding S, Bak LK, Schousboe A, Waagepetersen HS, Simonsen M, Ott P, Vilstrup H, Sørensen M (2014) Effect of glutamine synthetase inhibition on brain and interorgan ammonia metabolism in bile duct ligated rats. J Cereb Blood Flow Metab 34(3):460–466PubMed

Garcia-Martinez R, Cordoba J (2011) Acute-on-chronic liver failure: the brain. Curr Opin Crit Care 17(2):177–183PubMed

Gonzalez-Usano A, Cauli O, Agusti A, Felipo V (2014) Pregnenolone sulfate restores the glutamate-nitric-oxide-cGMP pathway and extracellular GABA in cerebellum and learning and motor coordination in hyperammonemic rats. ACS Chem Neurosci 5(2):100–105PubMed

Grover VP, Pavese N, Koh SB, Wylezinska M, Saxby BK, Gerhard A, Forton DM, Brooks DJ, Thomas HC, Taylor-Robinson SD (2012) Cerebral microglial activation in patients with hepatitis C: in vivo evidence of neuroinflammation. J Viral Hepat 19(2):e89–e96PubMed

Gulyas B, Toth M, Vas A, Shchukin E, Kostulas K, Hillert J, Halldin C (2012) Visualising neuroinflammation in post-stroke patients: a comparative PET study with the TSPO molecular imaging biomarkers [11C]PK11195 and [11C]vinpocetine. Curr Radiopharm 5(1):19–28PubMed

Herranz F, Almarza E, Rodríguez I, Salinas B, Rosell Y, Desco M, Bulte JW, Ruiz-Cabello J (2011) The application of nanoparticles in gene therapy and magnetic resonance imaging. Microsc Res Tech 74(7):577–591PubMedCentralPubMed

Holland JP, Liang SH, Rotstein BH, Collier TL, Stephenson NA, Greguric I, Vasdev N (2014) Alternative approaches for PET radiotracer development in Alzheimer’s disease: imaging beyond plaque. J Label Compd Radiopharm 57(4):323–331

Hu W, Metselaar J, Ben LH, Cravens PD, Singh MP, Frohman EM, Eagar TN, Racke MK, Kieseier BC, Stüve O (2009) PEG minocycline-liposomes ameliorate CNS autoimmune disease. PLoS ONE 4(1):e4151PubMedCentralPubMed

Iversen P, Hansen DA, Bender D, Rodell A, Munk OL, Cumming P, Keiding S (2006) Peripheral benzodiazepine receptors in the brain of cirrhosis patients with manifest hepatic encephalopathy. Eur J Nucl Med Mol Imaging 33(7):810–816PubMed

Jacobs AH, Tavitian B, Consortium IN (2012) Noninvasive molecular imaging of neuroinflammation. J Cereb Blood Flow Metab 32(7):1393–1415PubMedCentralPubMed

Ji RR, Xu ZZ, Gao YJ (2014) Emerging targets in neuroinflammation-driven chronic pain. Nat Rev Drug Discov 13(7):533–548PubMedCentralPubMed

Jin AYTU, Rushforth D, Filfil R, Kaur J, Ni F, Tomanek B, Barber PA (2009) Magnetic resonance molecular imaging of post-stroke neuroinflammation with a P-selectin targeted iron oxide nanoparticle. Contrast Media Mol Imaging 4(6):305–311PubMed

Jover R, Rodrigo R, Felipo V, Insausti R, Sáez-Valero J, García-Ayllón MS, Suárez I, Candela A, Compañ A, Esteban A, Cauli O, Ausó E, Rodríguez E, Gutiérrez A, Girona E, Erceg S, Berbel P, Pérez-Mateo M (2006) Brain edema and inflammatory activation in bile duct ligated rats with diet-induced hyperammonemia: A model of hepatic encephalopathy in cirrhosis. Hepatology 43(6):1257–1266PubMed

Kale RA, Gupta RK, Saraswat VA, Hasan KM, Trivedi R, Mishra AM, Ranjan P, Pandey CM, Narayana PA (2006) Demonstration of interstitial cerebral edema with diffusion tensor MR imaging in type C hepatic encephalopathy. Hepatology 43(4):698–706PubMed

Kannan S, Balakrishnan B, Muzik O, Romero R, Chugani D (2009) Positron emission tomography imaging of neuroinflammation. J Child Neurol 24(9):1190–1199PubMed

Kimer NKA, Møller S, Bendtsen F, Gluud LL (2014) Systematic review with meta-analysis: the effects of rifaximin in hepatic encephalopathy. Aliment Pharmacol Ther 40(2):123–132PubMed

Kircheis G, Hilger N, Haussinger D (2014) Value of critical flicker frequency and psychometric hepatic encephalopathy score in diagnosis of low-grade hepatic encephalopathy. Gastroenterology 146(4):961–969PubMed

Kreisl WC, Jenko KJ, Hines CS, Lyoo CH, Corona W, Morse CL, Zoghbi SS, Hyde T, Kleinman JE, Pike VW, McMahon FJ, Innis RB, Biomarkers Consortium PET Radioligand Project Team (2013) A genetic polymorphism for translocator protein 18 kDa affects both in vitro and in vivo radioligand binding in human brain to this putative biomarker of neuroinflammation. J Cereb Blood Flow Metab 33(1):53–58PubMedCentralPubMed

Lavisse SGM, Hérard AS, Petit F, Delahaye M, Van Camp N, Ben Haim L, Lebon V, Remy P, Dollé F, Delzescaux T, Bonvento G, Hantraye P, Escartin C (2012) Reactive astrocytes overexpress TSPO and are detected by TSPO positron emission tomography imaging. J Neurosci 32(32):10809–10818PubMed

Linnman C, Becerra L, Borsook D (2013) Inflaming the brain: CRPS a model disease to understand neuroimmune interactions in chronic pain. J Neuroimmune Pharm 8(3):547–563

Lodi R, Tonon C, Stracciari A, Weiger M, Camaggi V, Iotti S, Donati G, Guarino M, Bolondi L, Barbiroli B (2004) Diffusion MRI shows increased water apparent diffusion coefficient in the brains of cirrhotics. Neurology 62(5):762–766PubMed

Martin A, Boisgard R, Kassiou M, Dolle F, Tavitian B (2011) Reduced PBR/TSPO expression after minocycline treatment in a rat model of focal cerebral ischemia: a PET study using [(18)F]DPA-714. Mol Imaging Biol 13(1):10–15PubMed

Mattner F, Katsifis A, Staykova M, Ballantyne P, Willenborg DO (2005) Evaluation of a radiolabelled peripheral benzodiazepine receptor ligand in the central nervous system inflammation of experimental autoimmune encephalomyelitis: a possible probe for imaging multiple sclerosis. Eur J Nucl Med Mol Imaging 32(5):557–563PubMed

McCarthy JR, Weissleder R (2008) Multifunctional magnetic nanoparticles for targeted imaging and therapy. Adv Drug Deliv Rev 60(11):1241–1251PubMedCentralPubMed

McMillin M, Frampton G, Thompson M, Galindo C, Standeford H, Whittington E, Alpini G, DeMorrow S (2014) Neuronal CCL2 is upregulated during hepatic encephalopathy and contributes to microglia activation and neurological decline. J Neuroinflammation 11(1):121PubMedCentralPubMed

Médran-Navarrete V, Bernards N, Kuhnast B, Damont A, Pottier G, Peyronneau MA, Kassiou M, Marguet F, Puech F, Boisgard R, Dollé F (2014) [18 F]DPA-C5yne, a novel fluorine-18-labelled analogue of DPA-714: radiosynthesis and preliminary evaluation as a radiotracer for imaging neuroinflammation with PET. J Label Compd Radiopharm 57(6):410–418

Monfort P, Cauli O, Montoliu C, Rodrigo R, Llansola M, Piedrafita B, El Mlili N, Boix J, Agustí A, Felipo V (2009) Mechanisms of cognitive alterations in hyperammonemia and hepatic encephalopathy: therapeutical implications. Neurochem Int 55(1–3):106–112PubMed

Mulder WJ, Jaffer FA, Fayad ZA, Nahrendorf M (2014) Imaging and nanomedicine in inflammatory atherosclerosis. Sci Transl Med 6(239):239sr1PubMed

Niu G, Chen X (2011) Why integrin as a primary target for imaging and therapy. Theranostics 1:30–47PubMedCentralPubMed

Ott P, Vilstrup H (2014) Cerebral effects of ammonia in liver disease: current hypotheses. Metab Brain Dis 29(4):901–911

Ouchi Y, Yagi S, Yokokura M, Sakamoto M (2009) Neuroinflammation in the living brain of Parkinson’s disease. Parkinsonism Relat Disord 15(Suppl 3):S200–S204PubMed

Pichika R, Taha AY, Gao F, Kotta K, Cheon Y, Chang L, Kiesewetter D, Rapoport SI, Eckelman WC (2012) The synthesis and in vivo pharmacokinetics of fluorinated arachidonic acid: implications for imaging neuroinflammation. J Nucl Med 53(9):1383–1391PubMedCentralPubMed

Pichler BJ, Kneilling M, Haubner R, Braumüller H, Schwaiger M, Röcken M, Weber WA (2005) Imaging of delayed-type hypersensitivity reaction by PET and 18 F-galacto-RGD. J Nucl Med 46(1):184–189PubMed

Prakash R, Mullen KD (2010) Mechanisms, diagnosis and management of hepatic encephalopathy. Nat Rev Gastroenterol Hepatol 7(9):515–525PubMed

Qi R, Xu Q, Zhang LJ, Zhong J, Zheng G, Wu S, Zhang Z, Liao W, Zhong Y, Ni L, Jiao Q, Zhang Z, Liu Y, Lu G (2012) Structural and functional abnormalities of default mode network in minimal hepatic encephalopathy: a study combining DTI and fMRI. PLoS ONE 7(7):e41376PubMedCentralPubMed

Quigley EM, Monsour HP (2013) The gut microbiota and the liver: implications for clinical practice. Expert Rev Gastroenterol Hepatol 7(8):723–732PubMed

Rahmim A, Zaidi H (2008) PET versus SPECT: strengths, limitations and challenges. Nucl Med Commun 29(3):193–207PubMed

Rami L, Gómez-Ansón B, Bosch B, Sánchez-Valle R, Monte GC, Villar A, Molinuevo JL (2007) Cortical brain metabolism as measured by proton spectroscopy is related to memory performance in patients with amnestic mild cognitive impairment and Alzheimer’s disease. Dement Geriatr Cogn Disord 24(4):274–279PubMed

Rapic S, Backes H, Viel T, Kummer MP, Monfared P, Neumaier B, Vollmar S, Hoehn M, Van der Linden A, Heneka MT, Jacobs AH (2013) Imaging microglial activation and glucose consumption in a mouse model of Alzheimer’s disease. Neurobiol Aging 34(1):351–354PubMed

Razek AA, Abdalla A, Ezzat A, Megahed A, Barakat T (2014) Minimal hepatic encephalopathy in children with liver cirrhosis: diffusion-weighted MR imaging and proton MR spectroscopy of the brain. Neuroradiology 56(10):885–891PubMed

Ribeiro MJ, Vercouillie J, Debiais S, Cottier JP, Bonnaud I, Camus V, Banister S, Kassiou M, Arlicot N, Guilloteau D (2014) Could (18) F-DPA-714 PET imaging be interesting to use in the early post-stroke period? EJNMMI Res 4:28PubMedCentralPubMed

Rodrigo R, Cauli O, Gomez-Pinedo U, Agusti A, Hernandez-Rabaza V, Garcia-Verdugo JM, Felipo V (2010) Hyperammonemia induces neuroinflammation that contributes to cognitive impairment in rats with hepatic encephalopathy. Gastroenterology 139(2):675–684PubMed

Rodríguez I, Pérez-Rial S, González-Jimenez J, Pérez-Sánchez J, Herranz F, Beckmann N, Ruíz-Cabello J (2008) Magnetic resonance methods and applications in pharmaceutical research. J Pharm Sci 97(9):3637–3665PubMed

Schwartz M, Kipnis J, Rivest S, Prat A (2013) How do immune cells support and shape the brain in health, disease, and aging? J Neurosci 33(45):17587–17596PubMedCentralPubMed

Scott TR, Kronsten VT, Hughes RD, Shawcross DL (2013) Pathophysiology of cerebral oedema in acute liver failure. World J Gastroenterol 19(48):9240–9255PubMedCentralPubMed

Seale-Goldsmith MM, Leary JF (2009) Nanobiosystems. Wiley Interdiscip Rev Nanomed Nanobiotechnol 1(5):553–567PubMed

Shukuri M, Takashima-Hirano M, Tokuda K, Takashima T, Matsumura K, Inoue O, Doi H, Suzuki M, Watanabe Y, Onoe H (2011) In vivo expression of cyclooxygenase-1 in activated microglia and macrophages during neuroinflammation visualized by PET with 11C-ketoprofen methyl ester. J Nucl Med 52(7):1094–1101PubMed

Sieger D, Moritz C, Ziegenhals T, Prykhozhij S, Peri F (2012) Long-range Ca2+ waves transmit brain-damage signals to microglia. Dev Cell 22(6):1138–1148PubMed

Stinton LM, Jayakumar S (2013) Minimal hepatic encephalopathy. Can J Gastroenterol 27(10):572–574PubMedCentralPubMed

Stoll G, Bendszus M (2009) Imaging of inflammation in the peripheral and central nervous system by magnetic resonance imaging. Neuroscience 158(3):1151–1160PubMed

Stoll GB-LT, Weise G, Jakob P (2012) Visualization of inflammation using (19) F-magnetic resonance imaging and perfluorocarbons. Wiley Interdiscip Rev Nanomed Nanobiotechnol 4(4):438–447PubMed

Tang D, Hight MR, McKinley ET, Fu A, Buck JR, Smith RA, Tantawy MN, Peterson TE, Colvin DC, Ansari MS, Nickels M, Manning HC (2012) Quantitative preclinical imaging of TSPO expression in glioma using N, N-diethyl-2-(2-(4-(2–18 F-fluoroethoxy)phenyl)-5,7-dimethylpyrazolo[1,5-a]pyrimi din-3-yl)acetamide. J Nucl Med 53(2):287–294PubMedCentralPubMed

Thorek DL, Weisshaar CL, Czupryna JC, Winkelstein BA, Tsourkas A (2011) Superparamagnetic iron oxide-enhanced magnetic resonance imaging of neuroinflammation in a rat model of radicular pain. Mol Imaging 10(3):206–214PubMed

Tilleux S, Hermans E (2007) Neuroinflammation and regulation of glial glutamate uptake in neurological disorders. J Neurosci Res 85(10):2059–2070PubMed

Tiwari AK, Yui J, Fujinaga M, Kumata K, Shimoda Y, Yamasaki T, Xie L, Hatori A, Maeda J, Nengaki N, Zhang MR (2014) Characterization of a novel acetamidobenzoxazolone-based PET ligand for translocator protein (18 kDa) imaging of neuroinflammation in the brain. J Neurochem 129(4):712–720PubMed

Tourdias T, Dousset V (2013) Neuroinflammatory imaging biomarkers: relevance to multiple sclerosis and its therapy. Neurotherapeutics 10(1):111–123PubMedCentralPubMed

Vasudeva K, Andersen K, Zeyzus-Johns B, Hitchens TK, Patel SK, Balducci A, Janjic JM, Pollock JA (2014) Imaging neuroinflammation in vivo in a neuropathic pain rat model with near-infrared fluorescence and (1)(9)F magnetic resonance. PLoS ONE 9(2):e90589PubMedCentralPubMed

Venneti S, Lopresti BJ, Wiley CA (2006) The peripheral benzodiazepine receptor (Translocator protein 18 kDa) in microglia: from pathology to imaging. Prog Neurobiol 80(6):308–322PubMedCentralPubMed

Venneti S, Lopresti BJ, Wiley CA (2013) Molecular imaging of microglia/macrophages in the brain. Glia 61(1):10–23PubMedCentralPubMed

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):715–735PubMed

Wang Y, Yue X, Kiesewetter DO, Niu G, Teng G, Chen X (2014) PET imaging of neuroinflammation in a rat traumatic brain injury model with radiolabeled TSPO ligand DPA-714. Eur J Nucl Med Mol Imaging 41(7):1440–1449PubMed

Weise G, Basse-Luesebrink TC, Wessig C, Jakob PM, Stoll G (2011) In vivo imaging of inflammation in the peripheral nervous system by (19)F MRI. Exp Neurol 229(2):494–501PubMed

Weissenborn K (2013) Psychometric tests for diagnosing minimal hepatic encephalopathy. Metab Brain Dis 28(2):227–229PubMed

Wright G, Jalan R (2007) Ammonia and inflammation in the pathogenesis of hepatic encephalopathy: Pandora’s box? Hepatology 46(2):291–294PubMed

Wright G, Shawcross D, Olde Damink SW, Jalan R (2007) Brain cytokine flux in acute liver failure and its relationship with intracranial hypertension. Metab Brain Dis 22(3–4):375–388PubMed

Wu S, Zhang L, Zhong J, Zhang Z (2010) Dual contrast magnetic resonance imaging tracking of iron-labeled cells in vivo. Cytotherapy 12(7):859–869PubMed

Wunder A, Klohs J, Dirnagl U (2009) Non-invasive visualization of CNS inflammation with nuclear and optical imaging. Neuroscience 158(3):1161–1173PubMed

Zemtsova I, Görg B, Keitel V, Bidmon HJ, Schrör K, Häussinger D (2011) Microglia activation in hepatic encephalopathy in rats and humans. Hepatology 54(1):204–215PubMed

Zhang LJ, Lu GM, Yin JZ, Qi J (2010) Metabolic changes of anterior cingulate cortex in patients with hepatic cirrhosis: a magnetic resonance spectroscopy study. Hepatol Res 40(8):777–785PubMed

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(2):528–536PubMed

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):707–715PubMed

Zhang LJ, Wu S, Ren J, Lu GM (2014) Resting-state functional magnetic resonance imaging in hepatic encephalopathy: current status and perspectives. Metab Brain Dis 29(3):569–582PubMed

Title: PET and MR imaging of neuroinflammation in hepatic encephalopathy
Authors: Yun Yan Su
Gui Fen Yang
Guang Ming Lu
Shawn Wu
Long Jiang Zhang
Publication date: 01-02-2015
Publisher: Springer US
Published in: Metabolic Brain Disease / Issue 1/2015
Print ISSN: 0885-7490
Electronic ISSN: 1573-7365
DOI: https://doi.org/10.1007/s11011-014-9633-1

Keynote webinar | Spotlight on medication adherence

Springer Medicine

PET and MR imaging of neuroinflammation in hepatic encephalopathy

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2015

The characterization of neuroenergetic effects of chronic L-tyrosine administration in young rats: evidence for striatal susceptibility

Antidepressant-like effects of ferulic acid: involvement of serotonergic and norepinergic systems

Brain glycogen: emergency fuel and dynamic function in neurotransmission

In vivo Magnetic Resonance Spectroscopy of cerebral glycogen metabolism in animals and humans

Thrombin mutant W215A/E217A treatment improves neurological outcome and attenuates central nervous system damage in experimental autoimmune encephalomyelitis

Pluralistic roles for glycogen in the central and peripheral nervous systems