In vivo magnetic resonance spectroscopy: basic methodology and clinical applications

Ardenkjaer-Larsen JH, Fridlund B, Gram A, Hansson G, Hansson L, Lerche MH, Servin R, Thaning M, Golman K (2003) Increase in signal-to-noise ratio of >10,000 times in liquid-state NMR. Proc Natl Acad Sci USA 100:10158–10163

Argov Z, Löfberg M, Arnold DL (2000) Insights into muscle diseases gained by phosphorus magnetic resonance spectroscopy. Muscle Nerve 23:1316–1334

Baslow MH (2002) Evidence supporting a role for N-acetyl-L-aspartate as a molecular water pump in myelinated neurons in the central nervous system. An analytical review. Neurochem Int 40:295–300

Blüml S, Moreno A, Hwang JH, Ross BD (2001) 1-(13)C glucose magnetic resonance spectroscopy of pediatric and adult brain disorders. NMR Biomed 14:19–32

Bolan PJ, Nelson MT, Yee D, Garwood M (2005) Imaging in breast cancer: magnetic resonance spectroscopy. Breast Cancer Res 7:149–152

Bottomley PA (1987) Spatial localization in NMR-spectroscopy in vivo. Ann N Y Acad Sci 508:333–348

Brockmann K, Bjornstad A, Dechent P, Korenke CG, Smeitink J, Trijbels JM, Athanassopoulos S, Villagran R, Skjeldal OH, Wilichowski E, Frahm J, Hanefeld F (2002) Succinate in dystrophic white matter: a proton magnetic resonance spectroscopy finding characteristic for complex II deficiency. Ann Neurol 52:38–46

Brown TR (1992) Practical applications of chemical shift imaging. NMR Biomed 5:238–243

Brown TR, Kincaid BM, Ugurbil K (1982) NMR chemical shift imaging in three dimensions. Proc Natl Acad Sci USA 79:3523–3526

Cavassila S, Deval S, Huegen C, van Ormondt D, Graveron-Demilly D (2001) Cramér-Rao bounds: an evaluation tool for quantitation. NMR Biomed 14:278–283

Cecil KM (2006) MR spectroscopy of metabolic disorders. Neuroimaging Clin N Am 16:87–116

Cecil KM, Salomons GS, Ball WS, Wong B, Chuck G, Verhoeven NM, Jakobs C, DeGrauw TJ (2001) Irreversible brain creatine deficiency with elevated serum and urine creatine: a creatine transporter defect? Ann Neurol 49:401–404

Duyn JH, Moonen CT (1993) Fast proton spectroscopic imaging of human brain using multiple spin-echoes. Magn Reson Med 30:409–414

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

Dydak U, Weiger M, Pruesmann KP, Meier D, Boesiger P (2001) Sensitivity-encoded spectroscopic imaging. Magn Reson Med 46:713–722

Engelke UF, Kremer B, Kluijtmans LA, van der Graaf M, Morava E, Loupatty FJ, Wanders RJ, Moskau D, Loss S, van den Bergh E, Wevers RA (2006) NMR spectroscopic studies on the late onset form of 3-methylglutaconic aciduria type I and other defects in leucine metabolism. NMR Biomed 19:271–278

Engelke UFH, Moolenaar SH, Hoenderop SMGC, Morava E, van der Graaf M, Heerschap A, Wevers RA (2007) Handbook of 1H-NMR spectroscopy in inborn errors of metabolism: body fluid NMR spectroscopy and in vivo MR spectroscopy. Fully revised 2nd edn. SPS Publications, Heilbronn

Frahm J, Bruhn H, Gyngell ML, Merboldt KD, Hänicke W, Sauter R (1989) Localized high-resolution proton NMR spectroscopy using stimulated echoes: initial applications to human brain in vivo. Magn Reson Med 9:79–93

Fujita H (2007) New horizons in MR technology: RF coil designs and trends. Magn Reson Med Sci 6:29–42

Galanaud D, Chinot O, Nicoli F, Confort-Gouny S, Le Fur Y, Barrie-Attarian M, Ranjeva JP, Fuentès S, Viout P, Figarella-Branger D, Cozzone PJ (2003) Use of proton magnetic resonance spectroscopy of the brain to differentiate gliomatosis cerebri from low-grade glioma. J Neurosurg 98:269–276

Gruber S, Pinker K, Riederer F, Chmelík M, Stadlbauer A, Bittsanský M, Mlynárik V, Frey R, Serles W, Bodamer O, Moser E (2008) Metabolic changes in the normal ageing brain: consistent findings from short and long echo time proton spectroscopy. Eur J Radiol 68:320–327

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

Heerschap A, Jager GJ, van der Graaf M, Barentsz JO, de la Rosette JJ, Oosterhof GO, Ruijter ET, Ruijs SH (1997) In vivo proton MR spectroscopy reveals altered metabolite content in malignant prostate tissue. Anticancer Res 17:1455–1460

Heindel W, Kugel H, Roth B (1993) Noninvasive detection of increased glycine content by proton MR spectroscopy in the brains of two infants with nonketotic hyperglycinemia. Am J Neuroradiol 14:629–635

Hennig J (2008) Ultra high field MR: useful instruments or toys for the boys? MAGMA 21:1–3

Herminghaus S, Pilatus U, Möller-Hartmann W, Raab P, Lanfermann H, Schlote W, Zanella FE (2002) Increased choline levels coincide with enhanced proliferative activity of human neuroepithelial brain tumors. NMR Biomed 15:385–392

Hoult DI, Richards RE (1976) The signal-to-noise ratio of the nuclear magnetic resonance experiment. J Magn Reson 24:71–85

Howe FA, Barton SJ, Cudlip SA, Stubbs M, Saunders DE, Murphy M, Wilkins P, Opstad KS, Doyle VL, McLean MA, Bell BA, Griffiths JR (2003) Metabolic profiles of human brain tumors using quantitative in vivo 1H magnetic resonance spectroscopy. Magn Reson Med 49:223–232

in ‘t Zandt H, van der Graaf M, Heerschap A (2001) Common processing of in vivo MR spectra. NMR Biomed 14:224–232

Item CB, Stöckler-Ipsiroglu S, Stromberger C, Mühl A, Alessandrì MG, Bianchi MC, Tosetti M, Fornai F, Cioni G (2001) Arginine:glycine amidinotransferase deficiency: the third inborn error of creatine metabolism in humans. Am J Hum Genet 69:1127–1133

Janson CG, McPhee SW, Francis J, Shera D, Assadi M, Freese A, Hurh P, Haselgrove J, Wang DJ, Bilaniuk L, Leone P (2006) Natural history of Canavan disease revealed by proton magnetic resonance spectroscopy (1H-MRS) and diffusion-weighted MRI. Neuropediatrics 37:209–221

Klomp DW, Kentgens AP, Heerschap A (2008a) Polarization transfer for sensitivity-enhanced MRS using a single radio frequency transmit channel. NMR Biomed 21:444–452

Klomp DW, Wijnen JP, Scheenen TW, Heerschap A (2008b) Efficient 1H to 31P polarization transfer on a clinical 3T MR system. Magn Reson Med 60:1298–1305

Klose U (1990) In vivo proton spectroscopy in presence of eddy currents. Magn Reson Med 14:26–30

Kreis R, Ernst T, Ross BD (1993) Development of the human brain: in vivo quantification of metabolite and water content with proton magnetic resonance spectroscopy. Magn Reson Med 30:424–437

Kugel H, Heindel W, Ernestus RI, Bunke J, du Mesnil R, Friedmann G (1992) Human brain tumors: spectral patterns detected with localized H-1 MR spectroscopy. Radiology 183:701–709

Li BS, Wang H, Gonen O (2003) Metabolite ratios to assumed stable creatine level may confound the quantification of proton brain MR spectroscopy. Magn Reson Imaging 21:923–928

Maintz D, Heindel W, Kugel H, Jaeger R, Lackner KJ (2002) Phosphorus-31 MR spectroscopy of normal adult human brain and brain tumors. NMR Biomed 15:18–27

Martin E, Capone A, Schneider J, Hennig J, Thiel T (2001) Absence of N-acetylaspartate in the human brain: impact on neurospectroscopy? Ann Neurol 49:518–521

Maudsley AA, Matson GB, Hugg JW, Weiner MW (1994) Reduced phase encoding in spectroscopic imaging. Magn Reson Med 31:645–651

Michaelis T, Merboldt KD, Bruhn H, Hänicke W, Frahm J (1993) Absolute concentrations of metabolites in the adult human brain in vivo: quantification of localized proton MR spectra. Radiology 187:219–227

Moolenaar SH, Engelke UF, Wevers RA (2003) Proton nuclear magnetic resonance spectroscopy of body fluids in the field of inborn errors of metabolism. Ann Clin Biochem 40:16–24

Nelson SJ, Graves E, Pirzkall A, Li X, Antiniw Chan A, Vigneron DB, McKnight TR (2002) In vivo molecular imaging for planning radiation therapy of gliomas: an application of 1H MRSI. J Magn Reson Imaging 16:464–476

Novotny EJ Jr, Fulbright RK, Pearl PL, Gibson KM, Rothman DL (2003) Magnetic resonance spectroscopy of neurotransmitters in human brain. Ann Neurol 54(Suppl 6):S25–S31

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

Opstad KS, Murphy MM, Wilkins PR, Bell BA, Griffiths JR, Howe FA (2004) Differentiation of metastases from high-grade gliomas using short echo time 1H spectroscopy. J Magn Reson Imaging 20:187–192

Ordidge RJ, Bendall MR, Gordon RE, Connelly A (1985) Volume selection for in vivo biological spectroscopy. In: Govil G, Khetrapal CL, Saran A (eds) Magnetic resonance in biology and medicine. Tata McGraw-Hill, New Delhi, pp 387–397

Pietz J, Lutz T, Zwygart K, Hoffmann GF, Ebinger F, Boesch C, Kreis R (2003) Phenylalanine can be detected in brain tissue of healthy subjects by 1H magnetic resonance spectroscopy. J Inherit Metab Dis 26:683–692

Posse S, DeCarli C, Le Bihan D (1994) Three-dimensional echo-planar MR spectroscopic imaging at short echo times in the human brain. Radiology 192:733–738

Pouwels PJ, Frahm J (1998) Regional metabolite concentrations in human brain as determined by quantitative localized proton MRS. Magn Reson Med 39:53–60

Pouwels PJ, Brockmann K, Kruse B, Wilken B, Wick M, Hanefeld F, Frahm J (1999) Regional age dependence of human brain metabolites from infancy to adulthood as detected by quantitative localized proton MRS. Pediatr Res 46:474–485

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

Rijpkema M, Schuuring J, van der Meulen Y, van der Graaf M, Bernsen H, Boerman R, van der Kogel A, Heerschap A (2003) Characterization of oligodendrogliomas using short echo time 1H MR spectroscopic imaging. NMR Biomed 16:12–18

Ross B, Blüml S (2001) Magnetic resonance spectroscopy of the human brain. Anat Rec 265:54–84

Ross B, Lin A, Harris K, Bhattacharya P, Schweinsburg B (2003) Clinical experience with 13C MRS in vivo. NMR Biomed 16:358–369

Scheenen TW, Klomp DW, Wijnen JP, Heerschap A (2008) Short echo time 1H-MRSI of the human brain at 3T with minimal chemical shift displacement errors using adiabatic refocusing pulses. Magn Reson Med 59:1–6

Schmidt CW (2004) Metabolomics: what’s happening downstream of DNA. Environ Health Perspect 112:A410–A415

Schulte RF, Le Roux P, Vogel MW, Koenig H (2008) Design of phase-modulated broadband refocusing pulses. J Magn Reson 190:271–279

Skoch A, Jiru F, Bunke J (2008) Spectroscopic imaging: basic principles. Eur J Radiol 67:230–239

Soher BJ, Hurd RE, Sailasuta N, Barker PB (1996) Quantitation of automated single-voxel proton MRS using cerebral water as an internal reference. Magn Reson Med 36:335–339

Stöckler S, Holzbach U, Hanefeld F, Marquardt I, Helms G, Requart M, Hänicke W, Frahm J (1994) Creatine deficiency in the brain: a new, treatable inborn error of metabolism. Pediatr Res 36:409–413

Stöckler S, Hanefeld F, Frahm J (1996) Creatine replacement therapy in guanidinoacetate methyltransferase deficiency, a novel inborn error of metabolism. Lancet 348:789–790

Stubbs M, Veech RL, Griffiths JR (1995) Tumor metabolism: the lessons of magnetic resonance spectroscopy. Adv Enzyme Regul 35:101–115

Sylvain M, Arnold DL, Scriver CR, Schreiber R, Shevell MI (1994) Magnetic resonance spectroscopy in Niemann-Pick disease type C: correlation with diagnosis and clinical response to cholestyramine and lovastatin. Pediatr Neurol 10:228–232

Tate AR, Underwood J, Acosta DM, Julià-Sapé M, Majós C, Moreno-Torres A, Howe FA, van der Graaf M, Lefournier V, Murphy MM, Loosemore A, Ladroue C, Wesseling P, Luc Bosson J, Cabañas ME, Simonetti AW, Gajewicz W, Calvar J, Capdevila A, Wilkins PR, Bell BA, Rémy C, Heerschap A, Watson D, Griffiths JR, Arús C (2006) Development of a decision support system for diagnosis and grading of brain tumors using in vivo magnetic resonance single voxel spectra. NMR Biomed 19:411–434

Van der Knaap MS, Wevers RA, Struys EA, Verhoeven NM, Pouwels PJ, Engelke UF, Feikema W, Valk J, Jakobs C (1999) Leukoencephalopathy associated with a disturbance in the metabolism of polyols. Ann Neurol 46:925–928

Varho T, Komu M, Sonninen P, Holopainen I, Nyman S, Manner T, Sillanpää M, Aula P, Lundbom N (1999) A new metabolite contributing to N-acetyl signal in 1H MRS of the brain in Salla disease. Neurology 52:1668–1672

Wijnen JP, Klomp DW, Idema AJ, de Galan BE, Heerschap A (2008) Lactate production in human brain tumor; detection by 13C MRS at 3T. Abstract. Proc Intl Soc Mag Reson Med 16:2815

Willemsen MA, Van Der Graaf M, Van Der Knaap MS, Heerschap A, Van Domburg PH, Gabreëls FJ, Rotteveel JJ (2004) MR imaging and proton MR spectroscopic studies in Sjögren–Larsson syndrome: characterization of the leukoencephalopathy. Am J Neuroradiol 25:649–657

Wolinsky JS, Narayana PA, Fenstermacher MJ (1990) Proton magnetic resonance spectroscopy in multiple sclerosis. Neurology 40:1764–1769

Yue Q, Isobe T, Shibata Y, Anno I, Kawamura H, Yamamoto Y, Takano S, Matsumura A (2008) New observations concerning the interpretation of magnetic resonance spectroscopy of meningioma. Eur Radiol 18:2901–2911