Skip to main content

Advertisement

SpringerLink
Log in

Multi-dimensional MR spectroscopy: towards a better understanding of hepatic encephalopathy

  • Original Paper
  • Published:
Metabolic Brain Disease Aims and scope Submit manuscript

Abstract

Hepatic encephalopathy (HE) is normally diagnosed by neuropsychological (NP) tests. The goals of this study were to quantify cerebral metabolites, separate glutamate (Glu) from glutamine (Gln) in patients with minimal hepatic encephalopathy (MHE) as well as healthy subjects using the prior-knowledge fitting (ProFit) algorithm on data acquired by two-dimensional (2D) localized correlated spectroscopy (L-COSY) on two different MR scanners, and to correlate the metabolite changes with neuropsychological (NP) tests. We studied 14 MHE patients and 18 healthy controls using a GE 1.5 T Signa MR scanner. Another group of 16 MHE patients and 18 healthy controls were studied using a Siemens 1.5 T Avanto MR scanner. The following parameters were used for L-COSY: TR/TE = 2 s/30 ms, 3 × 3 × 3 cm3 voxel size, 96 Δt1 increments with 8 averages per Δt1. Using the ProFit algorithm, we were able to differentiate Gln from Glu on the GE 1.5 T data in the medial frontal white/gray matter. The ratios of myo-inositol (mI), Glu, total choline, scyllo-inositol (sI), phosphoethanolamine (PE), and total N-acetyl aspartate (NAA) showed statistically significant decline in HE patients compared to healthy controls, while the ratio of Gln was significantly increased. Similar trend was seen in the ProFit quantified Siemens 1.5 T data in the frontal and occipito-parietal white/gray regions. Among the NP domain scores, motor function, cognitive speed, executive function and the global scores showed significant differences. Excellent correlations between various NP domains and metabolite ratios were also observed. ProFit based cerebral metabolite quantitation enhances the understanding and basis of the current hypothesis of MHE.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Amodio P, Del Piccolo F, Marchetti P, Angeli P, Iemmolo R, Caregaro L, Merkel C, Gerunda G, Gatta A (1999) Clinical features and survivial of cirrhotic patients with subclinical cognitive alterations detected by the number connection test and computerized psychometric tests. Hepatology 29:1662–1667

    Article  PubMed  CAS  Google Scholar 

  • Amodio P, Del Piccolo F, Pettenò E, Mapelli D, Angeli P, Iemmolo R, Muraca M, Musto C, Gerunda G, Rizzo C, Merkel C, Gatta A (2001) Prevalence and prognostic value of quantified electroencephalogram (EEG) alterations in cirrhotic patients. J Hepatol 35:37–45

    Article  PubMed  CAS  Google Scholar 

  • Amodio P, Montagnese S, Gatta A, Morgan MY (2004) Characteristics of minimal hepatic encephalopathy. Metab Brain Dis 19:253–267

    Article  PubMed  Google Scholar 

  • Amodio P, Ridola L, Schiff S, Montagnese S, Pasquale C, Nardelli S, Pentassuglio I, Trezza M, Marzano C, Flaiban C, Angeli P, Cona G, Bisiacchi P, Gatta A, Riggio O (2010) Improving detection of minimal hepatic encephalopathy using the inhibitory control task. Gastroenterology 139:510–518

    Article  PubMed  Google Scholar 

  • Berl S, Tokagaki G, Clarke DD, Waelsch H (1962) Metabolic compartments in vivo. Ammonia and glutamic acid metabolism in brain and liver. J Biol Chem 237:2562–2569

    PubMed  CAS  Google Scholar 

  • Bernthal P, Hayes A, Tarter RE, Van Thiel D, Lecky J, Hegedus A (1987) Cerebral CT scan abnormalities in cholestatic and hepatocellular disease and their relationship to neuropsychologic test performance. Hepatology 7:107–114

    Article  PubMed  CAS  Google Scholar 

  • Bhujwalla ZM, Aboagye EO, Gillies RJ, Chacko VP, Mendola CE, Backer JM (1999) Nm23-transfected MDA-MB-435 human breast carcinoma cells form tumors with altered phospholipid metabolism and pH: a 31P nuclear magnetic resonance study in vivo and in vitro. Magn Reson Med 41:897–903

    Article  PubMed  CAS  Google Scholar 

  • Binesh N, Huda A, Bugbee M, Gupta R, Rasgon N, Kumar A, Green M, Han S, Thomas MA (2005) Adding another spectral dimension to 1H magnetic resonance spectroscopy of hepatic encephalopathy. J Magn Reson Imaging 21:398–405

    Article  PubMed  Google Scholar 

  • Binesh N, Huda A, Thomas MA, Wyckoff N, Bugbee M, Han S, Rasgon N, Davanzo P, Sayre J, Guze B, Martin P, Fawzy F (2006) Hepatic encephalopathy: a neurochemical, neuroanatomical, and neuropsychological study. J Appl Clin Med Phys 7:86–96

    Article  PubMed  Google Scholar 

  • Blei AT, Cordoba J (1996) Subclinical encephalopathy. Digest Dis 14:2–11

    Article  Google Scholar 

  • Bosman DK, Deutz NE, De Graaf AA, vd Hulst RW, Van Eijk HM, Bovée WM, Maas MA, Jörning GG, Chamuleau RA (1990) Changes in brain metabolism during hyperammonemia and acute liver failure: results of a comparative 1H-NMR spectroscopy and biochemical investigation. Hepatology 12:281–290

    Google Scholar 

  • Butterworth RF (1995) Hepatic encephalopathy. Neurologist 1:95–104

    Google Scholar 

  • Butterworth RF (1996) Taurine in hepatic encephalopathy. Adv Exp Med Biol 403:601–606

    PubMed  CAS  Google Scholar 

  • Butterworth RF (2000) Complication of cirrhosis. III. Hepatic encephalopathy. J Hepatol 32:171–180

    Article  PubMed  CAS  Google Scholar 

  • Chalasani N, Gitlin N (1997) Subclinical hepatic encephalopathy: How best to diagnose? Am J Gastroent 92:905–906

    PubMed  CAS  Google Scholar 

  • Chih CP, Roberts EL Jr (2003) Energy substrates for neurons during neural activity: a critical review of the astrocyte-neuron lactate shuttle hypothesis. J Cereb Blood Flow Metab 23:1263–1281

    Article  PubMed  CAS  Google Scholar 

  • Clarke DD, Sokoloff L (1999) Circulation and energy metabolism of the brain. In: Siegel GJ, Agranoff BW et al (eds) Basic neurochemistry. Lippincott-Raven, Philadelphia, pp 637–669

    Google Scholar 

  • Dhiman RK, Chawla YK (2009) Minimal hepatic encephalopathy. Indian J Gastroenterol 28:5–16

    Article  PubMed  Google Scholar 

  • Duyn JH, Gillen J, Sobering G, van Zijl PC, Moonen CTW (1993) Multisection proton MR spectrosocopic imaging of the brain. Radiology 188:277–282

    PubMed  CAS  Google Scholar 

  • Evanochko WT, Sakal TT, Ng TC, Krishnaa NR, Kimc HD, Zeidlerc RB, Ghantad VK, Brockmane RW, Schifferf LM, Braunschweigerf PG, Glicksona JD (1984) NMR study of in vivo RIF-1 tumors. Analysis of perchloric acid extracts and identification of 1H, 31P and 13C resonances. Biochim Biophys Acta 805:104–116

    Article  PubMed  CAS  Google Scholar 

  • 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 35:716–721

    Article  PubMed  Google Scholar 

  • Foerster BR, Conklin LS, Petrou M, Barker PB, Schwarz KB (2009) Minimal hepatic encephalopathy in children: evaluation with proton MR spectroscopy. AJNR Am J Neuroradiol 30:1610–1613

    Article  PubMed  CAS  Google Scholar 

  • Fraser CL, Arieff AI (1985) Hepatic encephalopathy. New Eng J Med 313:865–873

    Article  PubMed  CAS  Google Scholar 

  • Frias-Martinez E, Rajakumar N, Liu X, Singhal A, Banakar S, Lipnick S, Verma G, Ramadan S, Kumar A, Thomas MA (2008) ProFit-based Quantitation of Cerebral Metabolites using 2D L-COSY at 3 T Magnetic Resonance. Proc Intl Soc Mag Reson Med 16: 691, Toronto, Canada

  • Gilberstadt SJ, Gilberstadt H, Zieve L, Buegel B, Collier RO Jr, McClain CJ (1980) Psychomotor performance defects in cirrhotic patients without overt encephalopathy. Arch Intern Med 140:519–521

    Article  PubMed  CAS  Google Scholar 

  • Gitlin N (1996) Hepatic encephalopathy. In: Zorkin D, Boyer TD (eds) Hepatology. Saunders, Philadelphia, pp 605–617

    Google Scholar 

  • Govindaraju V, Young K, Maudsley AA (2000) Proton NMR chemical shifts and coupling constants for brain metabolites. NMR Biomed 13:129–153

    Article  PubMed  CAS  Google Scholar 

  • Griffiths JR, Cady E, Edwards RHT, McCready VR, Wilkie DR, Wiltshaw E (1983) 31P-NMR studies of a human tumour in situ. Lancet 1:1435–1436

    Article  PubMed  CAS  Google Scholar 

  • Gruetter R, Novotny EJ, Boulware SD, Mason GF, Rothman DL, Shulman GI, Prichard JW, Shulman RG (1994) Localized 13C NMR spectroscopy in the human brain of amino acid labeling from D-[1-13C]glucose. J Neurochem 63:1377–1385

    Article  PubMed  CAS  Google Scholar 

  • Haase A, Frahm J, Haenicke W, Matthaei D (1985) 1H NMR chemical-shift selective (CHESS) imaging. Phys Med Biol 30:341–344

    Article  PubMed  CAS  Google Scholar 

  • Heaton RK, Grant I, Matthews CG (1991) Comprehensive norms for an expanded Halstead-Reitan battery: demographic corrections, research findings, and clinical applications. Psychological Assessment Resources, Odessa

    Google Scholar 

  • Hilbe JM (2009) Logistic regression models. Chapman & Hall/CRC Press

  • Hilgier W, Law RO, Zielinska M (2000) Taurine, glutamine, glutamate, and aspartate content and efflux, cell volume of cerebrocortical minislices of rats with hepatic encephalopathy. Adv Exp Med Biol 483:305–312

    Article  PubMed  CAS  Google Scholar 

  • Hosmer DW, Lemeshow S (1995) Applied Logistic Regression. John Wiley and Sons, Inc Menard, Scott

  • Kaibara T, Tyson RL, Sutherland GR (1998) Human cerebral neoplasms studied using MR spectroscopy: a review. Biochem Cell Biol 76:477–486

    Article  PubMed  CAS  Google Scholar 

  • Klein J, Gonzalez R, Koppen A, Loffelholz K (1993) Free choline and choline metabolites in rat brain and body fluids: sensitive determination and implications for choline supply to the brain. Neurochem Int 22:293–300

    Article  PubMed  CAS  Google Scholar 

  • Koc H, Mar M, Ranasinghe A, Swenberg JA, Zeisel SH (2002) Quantitation of Choline and its Metabolites in Tissues and Foods by Liquid Chromatography/Electrospray Ionization-Isotope Dilution Mass Spectrometry. Analytical Chemistry 74:4734–4740

    Article  PubMed  CAS  Google Scholar 

  • Kreis R, Ross BD, Farrow NA, Ackerman Z (1992) Metabolic disorders of the brain in chronic hepatic encephalopathy detected with H-1 MR spectroscopy. Radiology 182:19–27

    PubMed  CAS  Google Scholar 

  • Larzelere RE, Mulak SA (1977) Single-sample tests for many correlations. Psychol Bull 84:557–569

    Article  Google Scholar 

  • Lavoie J, Giguere JF, Layrargues GP, Butterworth RF (1987) Amino acid changes in autopsied brain tissue from cirrhotic patients with hepatic encephalopathy. J Neurochem 49:692–697

    Article  PubMed  CAS  Google Scholar 

  • Leybaert L (2005) Neurobarrier coupling in the brain: a partner of neurovascular and neurometabolic coupling? J Cereb Blood Flow Metab 25:2–16

    PubMed  CAS  Google Scholar 

  • Lezak MD (1995) Neuropsychological assessment. Oxford University Press, New York, pp 333–685

    Google Scholar 

  • Lockwood AH (2000) “What’s in a name?” Improving the care of cirrhotics. J Hepatol 32:859–861

    Article  PubMed  CAS  Google Scholar 

  • Lockwood AH, Yap EWH, Wong WH (1991a) Cerebral ammonia metabolism in patients with severe liver disease and minimal hepatic encephalopathy. J Cerebral Blood Flow Metabol 11:337–341

    Article  CAS  Google Scholar 

  • Lockwood AH, Yap EWH, Rhodes HM, Wong WH (1991b) Altered cerebral blood flow and glucose metabolism in patients with liver disease and minimal encephalopathy. J Cerebral Blood Flow Metabol 11:331–336

    Article  CAS  Google Scholar 

  • Loening NM, Chamberlin AM, Zepeda AG, Gonzalez RG, Cheng LL (2005) Quantification of phosphocholine and glycerophosphocholine with 31P edited 1H NMR spectroscopy. NMR in Biomedicine 18:413–420

    Article  PubMed  CAS  Google Scholar 

  • Magistretti PJ, Pellerin L, Rothman DL, Shulman RG (1999) Energy on demand. Science 283:496–497

    Article  PubMed  CAS  Google Scholar 

  • McCrea M, Cordoba I, Vessey G, Blei AT, Randolph C (1996) Neuropsychological characterization and detection of subclinical hepatic encephalopathy. Arch Neurol 53:758–763

    PubMed  CAS  Google Scholar 

  • McPhail MJ, Taylor-Robinson SD (2010) The role of magnetic resonance imaging and spectroscopy in hepatic encephalopathy. Metab Brain Dis 25:65–72

    Article  PubMed  Google Scholar 

  • Miller BL, Chang L, Booth R, Ernst T, Cornford M, Nikas D, McBride D, Jenden DJ (1996) In Vivo 1H MRS Choline: Correlation with In Vitro Chemistry/Histology. Life Sciences 58:1929–1935

    Article  PubMed  CAS  Google Scholar 

  • Mullen KD (2007) Review of the final report of the 1998 Working Party on definition, nomenclature and diagnosis of hepatic encephalopathy. Aliment Pharmacol Ther 25:11–16

    Article  PubMed  Google Scholar 

  • Ogg RJ, Kingsley PB, Taylor JS (1994) WET, a T1- and B1-insensitive water-suppression method for in vivo localized 1H NMR spectroscopy. J Magn Reson B 104:1–10

    Article  PubMed  CAS  Google Scholar 

  • Patel N, Forton DM, Coutts GA, Thomas HC, Taylor-Robinson SD (2000) Intracellular pH measurements of the whole head and the basal ganglia in chronic liver disease: a phosphorus-31 MR spectroscopy study. Metab Brain Dis 15:223–240

    PubMed  CAS  Google Scholar 

  • Pardridge WM, Cornford EM, Braun LD, Oldendorf WH (1979) Transport of choline and choline analogues through the blood-brain barrier. In: Barbeau A, Growdon JH, Wurtman RJ (eds) Nutrition and the Brain. Raven, New York, pp 25–33

    Google Scholar 

  • Pellerin L, Magistretti PJ (1997) Glutamate uptake stimulates Na+, K+-ATPase activity in astrocytes via activation of a distinct subunit highly sensitive to ouabian. J Neurochem 69:2132–2137

    Article  PubMed  CAS  Google Scholar 

  • Provencher SW (1993) Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn Reson Med 30:672–679

    Article  PubMed  CAS  Google Scholar 

  • Romero-Gómez M (2007) Critical flicker frequency: it is time to break down barriers surrounding minimal hepatic encephalopathy. J Hepatol 47:10–11

    Article  PubMed  Google Scholar 

  • Romero-Gómez M, Córdoba J, Jover R, del Olmo JA, Ramírez M, Rey R, de Madaria E, Montoliu C, Nuñez D, Flavia M, Compañy L, Rodrigo JM, Felipo V (2007) Value of the critical flicker frequency in patients with minimal hepatic encephalopathy. Hepatology 45:879–885

    Article  PubMed  Google Scholar 

  • Ross BD, Danielsen ER, Bluml S (1996) Proton magnetic resonance spectroscopy: The new gold standard for diagnosis of clinical and subclinical hepatic encephalopathy? Digest Dis 14:30–39

    Article  Google Scholar 

  • Ross BD, Jacobson S, Villamil F, Korula J, Kreis R, Ernst T, Shonk T, Moats RA (1994) Subclinical hepatic encephalopathy: proton MR spectroscopic abnormalities. Radiology 193:457–463

    PubMed  CAS  Google Scholar 

  • Saxena N, Bhatia M, Joshi YK, Garg PK, Dwivedi SN, Tandon RK (2002) Electrophysiological and neuropsychological tests for the diagnosis of subclinical hepatic encephalopathy and prediction of overt encephalopathy. Liver 22:190–197

    Article  PubMed  Google Scholar 

  • Schomerus H, Hamster W (1998) Neuropsychological aspects of portalsystemic encephalopathy. Metab Brain Dis 13:361–377

    Article  PubMed  CAS  Google Scholar 

  • Schomerus H, Hamster W, Blunck H, Reinhard U, Mayer K, Dolle W (1981) Latent portasystemic encephalopathy. I. Nature of cerebral functional defects and their effect on fitness to drive. Dig Dis Sci 26:622–630

    Article  PubMed  CAS  Google Scholar 

  • Schulte RF, Boesiger P (2006) ProFit: two-dimensional prior-knowledge fitting of J-resolved spectra. NMR Biomed 19:255–263

    Article  PubMed  CAS  Google Scholar 

  • Singhal A, Nagarajan R, Hinkin CH, Kumar R, Sayre J, Elderkin-Thompson V, Huda A, Gupta RK, Han SH, Thomas MA (2010) Two-dimensional MR spectroscopy of minimal hepatic encephalopathy and neuropsychological correlates in vivo. J Magn Reson Imaging 32:35–43

    Article  PubMed  Google Scholar 

  • Smith SA, Levante TO, Meier BH, Ernst RR (1994) Computer-simulations in magnetic-resonance-an object-oriented programming approach. J Magn Reson A 106:75–105

    Article  CAS  Google Scholar 

  • Solivera J, Cerdan S, Pascual JM, Barrios L, Roda JM (2009) Assessment of 31P-NMR analysis of phospholipid profiles for potential differential diagnosis of human cerebral tumors. NMR in Biomedicine 22:663–674

    Article  PubMed  CAS  Google Scholar 

  • Stewart CA, Smith GE (2007) Minimal hepatic encephalopathy. Nat Clin Pract Gastroenterol Hepatol 4:677–685

    Article  PubMed  Google Scholar 

  • Tarter RE, Hegedus AM, Van Thiel DH, Schade RR, Gavaler JS, Starzl TE (1984) Nonalcoholic cirrhosis associated with neuropsychological dysfunction in the absence of overt evidence of hepatic encephalopathy. Gastroenterology 86:1421–1427

    PubMed  CAS  Google Scholar 

  • Taylor-Robinson SD, Sargentoni J, Mallalieu RJ, Bell JD, Bryant DJ, Coutts GA, Morgan MY (1994) Cerebral phosphorus-31 magnetic resonance spectroscopy in patients with chronic hepatic encephalopathy. Hepatology 20:1173–1178

    Article  PubMed  CAS  Google Scholar 

  • Taylor-Robinson SD, Buckley C, Changani KK, Hodgson HJ, Bell JD (1999) Cerebral proton and phosphorus-31 magnetic resonance spectroscopy in patients with subclinical hepatic encephalopathy. Liver 19:389–398

    Article  PubMed  CAS  Google Scholar 

  • Thomas MA, Yue K, Binesh N, Davanzo P, Kumar A, Siegel B, Frye M, Curran J, Lufkin R, Martin P, Guze B (2001) Localized two-dimensional shift correlated MR spectroscopy of human brain. Magn Reson Med 46:58–67

    Article  PubMed  CAS  Google Scholar 

  • Vaquero J, Butterworth RF (2006) The brain glutamate system in liver failure. J Neurochem 98:661–669

    Article  PubMed  CAS  Google Scholar 

  • Wang YM (2004) The definition, nomenclature and diagnosis of hepatic encephalopathy. Zhonghua Gan Zang Bing Za Zhi 12:305–306

    PubMed  Google Scholar 

  • Weissenborn K, Ahl B, Fischer-Wasels D, van den Hoff J, Hecker H, Burchert W, Köstler H (2007) Correlations between magnetic resonance spectroscopy alterations and cerebral ammonia and glucose metabolism in cirrhotic patients with and without hepatic encephalopathy. Gut 56:1736–1742

    Article  PubMed  Google Scholar 

  • Weissenborn K, Ennen JC, Schomerus H, Ruckert N, Hecker H (2001) Neuropsychological characterization of hepatic encephalopathy. J Hepatol 34:768–773

    Article  PubMed  CAS  Google Scholar 

  • Zimmerman C, Winnefeld K, Streck S, Roskosb M, Haberla RL (2004) Antioxidant status in acute stroke patients and patients at stroke risk. Eur Neurol 51:157–161

    Article  Google Scholar 

  • Zwingmann C, Chaturet N, Leibiritz D, Butterworth RF (2003) Selective increase of brain lactate synthesis in experimental acute liver failure: results of a [H-C] nuclear magnetic resonance study. Hepatology 37:420–428

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by a National Institute of Mental Health (NIMH) RO1 grant (1R01MH06569501A1). Scientific support of Drs. Nader Binesh, Kenneth Yue, Shida Banakar, and Sherry Liu during the earlier phase of this project is gratefully acknowledged. Authors acknowledge the support of Dr. Rolf Schulte, Prof. Dr. Peter Boesiger and his group members at ETH-Zurich, Switzerland in sharing the earlier version of the ProFit algorithm for processing the localized 2D J-resolved spectrum.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Radiological Sciences, David Geffen School of Medicine, University of California, CHS BL 428, 10833 Le Conte Avenue, Los Angeles, CA, 90095–1721, USA

    Manoj K. Sarma, Amir Huda, Rajakumar Nagarajan, Neil Wilson, Enrique Frias-Martinez, James Sayre & M. Albert Thomas

  2. Department of Physics, California State University, Fresno, CA, USA

    Amir Huda

  3. Department of Psychiatry, David Geffen School of Medicine, University of California, Los Angeles, CA, USA

    Charles H. Hinkin, Barry Guze & M. Albert Thomas

  4. VA Greater Los Angeles Healthcare System, Los Angeles, CA, USA

    Charles H. Hinkin

  5. Department of Radiology, Sanjay Gandhi Post-Graduate Institute of Medical Sciences, Lucknow, India

    Rakesh K. Gupta

  6. Department of Hepatology, David Geffen School of Medicine, University of California, Los Angeles, CA, USA

    Steven-Huy Han

Authors
  1. Manoj K. Sarma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Amir Huda
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rajakumar Nagarajan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Charles H. Hinkin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Neil Wilson
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rakesh K. Gupta
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Enrique Frias-Martinez
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. James Sayre
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Barry Guze
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Steven-Huy Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. M. Albert Thomas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Albert Thomas.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sarma, M.K., Huda, A., Nagarajan, R. et al. Multi-dimensional MR spectroscopy: towards a better understanding of hepatic encephalopathy. Metab Brain Dis 26, 173–184 (2011). https://doi.org/10.1007/s11011-011-9250-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11011-011-9250-1

Keywords

Search

Navigation