Brain γ-aminobutyric acid (GABA) detection in vivo with the J-editing 1H MRS technique: a comprehensive methodological evaluation of sensitivity enhancement, macromolecule contamination and test–retest reliability

NMR in Biomedicine

Volumn 29, Issue 7, 2016, Pages 932-942

  Shungu, Dikoma C ^a   Mao, Xiangling ^a   Gonzales, Robyn ^b   Soones, Tacara N ^b   Dyke, Jonathan P ^a   van der Veen, Jan Willem ^c   Kegeles, Lawrence S ^b  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

Author keywords

1H MRS; GABA; Glutamate; Glx; J editing; mobile macromolecules; phased array coil; test retest reliability

Indexed keywords

AMINO ACIDS; BRAIN; COPYRIGHTS; CORRELATION METHODS; MACROMOLECULES; POLLUTION DETECTION; RELIABILITY; TESTING;

1H MRS; GABA; GLUTAMATE; J-EDITING; PHASED ARRAY COILS;

SENSITIVITY ANALYSIS;

4 AMINOBUTYRIC ACID; CREATINE; GLUTAMIC ACID; GLUTAMINE;

4 AMINOBUTYRIC ACID BRAIN LEVEL; ADULT; ANATOMICAL VARIATION; ARTICLE; ARTIFACT; CONTROLLED STUDY; DORSOLATERAL PREFRONTAL CORTEX; FEMALE; HUMAN; HUMAN EXPERIMENT; IMAGE PROCESSING; IMAGE QUALITY; IN VIVO STUDY; J EDITING; MACROMOLECULE; MALE; MEDIAL PREFRONTAL CORTEX; MOBILE MACROMOLECULE; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE SCANNER; OCCIPITAL CORTEX; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; SENSITIVITY ANALYSIS; SIGNAL NOISE RATIO; TEST RETEST RELIABILITY; TISSUE WATER;

EID: 85027922420     PISSN: 09523480     EISSN: 10991492     Source Type: Journal    
DOI: 10.1002/nbm.3539     Document Type: Article

References (44)

1. Lewis DA, Volk DW, Hashimoto T. Selective alterations in prefrontal cortical GABA neurotransmission in schizophrenia: a novel target for the treatment of working memory dysfunction. Psychopharmacology 2004; 174(1): 143–150.
2. Sanacora G, Mason GF, Rothman DL, Behar KL, Hyder F, Petroff OA, Berman RM, Charney DS, Krystal JH. Reduced cortical gamma-aminobutyric acid levels in depressed patients determined by proton magnetic resonance spectroscopy. Arch. Gen. Psychiatry 1999; 56(11): 1043–1047.
3. Goddard AW, Mason GF, Almai A, Rothman DL, Behar KL, Petroff OA, Charney DS, Krystal JH. Reductions in occipital cortex GABA levels in panic disorder detected with 1 h-magnetic resonance spectroscopy. Arch. Gen. Psychiatry 2001; 58(6): 556–561.
4. Simpson HB, Shungu DC, Bender J, Jr, Mao X, Xu X, Slifstein M, Kegeles LS. Investigation of cortical glutamate–glutamine and gamma-aminobutyric acid in obsessive–compulsive disorder by proton magnetic resonance spectroscopy. Neuropsychopharmacology 2012; 37(12): 2684–2692.
5. Petroff OA, Rothman DL. Measuring human brain GABA in vivo: effects of GABA-transaminase inhibition with vigabatrin. Mol. Neurobiol. 1998; 16(1): 97–121.
6. 1H NMR measurements of gamma-aminobutyric acid in human brain in vivo. Proc. Natl. Acad. Sci. U. S. A. 1993; 90(12): 5662–5666.
7. Mullins PG, McGonigle DJ, O'Gorman RL, Puts NA, Vidyasagar R, Evans CJ. Cardiff Symposium on MRSoG, Edden RA. Current practice in the use of MEGA-PRESS spectroscopy for the detection of GABA. NeuroImage, 2014; 86: 43–52.
8. Puts NA, Edden RA. In vivo magnetic resonance spectroscopy of GABA: a methodological review. Prog. Nucl. Magn. Reson. Spectrosc. 2012; 60: 29–41.
9. Veen van derJW, Shen J. Multi-channel GABA editing on a clinical 3 T scanner. Proceedings of the 13th Annual Meeting ISMRM, Miami Beach, Florida, USA, 2005; 13: 214 (http://cds.ismrm.org/ismrm-2005/Files/00214.pdf).
10. Mescher M, Merkle H, Kirsch J, Garwood M, Gruetter R. Simultaneous in vivo spectral editing and water suppression. NMR Biomed. 1998; 11(6): 266–272.
11. Sailasuta N, LeRoux P, Hurd R, Wang P, Sachs N, Ketter T. Detection of cerebral gamma-aminobutyric acid (GABA) in bipolar disorder patients and healthy volunteers at 3 T. Proceedings of the 9th Annual Meeting ISMRM, Glasgow, Scotland, UK, 2001; 9: 1011.
12. 1H NMR spectrum of rat brain. Magn. Reson. Med. 1993; 30(1): 38–44.
13. 1H NMR spectra of human brain. Magn. Reson. Med. 1994; 32(3): 294–302.
14. Mader I, Seeger U, Weissert R, Klose U, Naegele T, Melms A, Grodd W. Proton MR spectroscopy with metabolite-nulling reveals elevated macromolecules in acute multiple sclerosis. Brain 2001; 124(Pt 5): 953–961.
15. Brown MA. Time-domain combination of MR spectroscopy data acquired using phased-array coils. Magn. Reson. Med. 2004; 52(5): 1207–1213.
16. Markwardt C. Non-linear least squares fitting in IDL with MPFIT. Proceedings of Astronomical Data Analysis Software and Systems XVIII, Québec City, QC, Canada, 2009; 411: 251–254.
17. Marshall I, Bruce SD, Higinbotham J, MacLullich A, Wardlaw JM, Ferguson KJ, Seckl J. Choice of spectroscopic lineshape model affects metabolite peak areas and area ratios. Magn. Reson. Med. 2000; 44(4): 646–649.
18. Kirk RE. Experimental Design: Procedures for the Behavioral Sciences. Brooks/Cole Publishing Company: Pacific Grove, CA, 1982.
19. Albrecht J, Burke M, Haegler K, Schopf V, Kleemann AM, Paolini M, Wiesmann M, Linn J. Potential impact of a 32-channel receiving head coil technology on the results of a functional MRI paradigm. Clin. Neuroradiol. 2010; 20(4): 223–229.
20. Mader I, Seeger U, Karitzky J, Erb M, Schick F, Klose U. Proton magnetic resonance spectroscopy with metabolite nulling reveals regional differences of macromolecules in normal human brain. J. Magn. Reson. Imaging 2002; 16(5): 538–546.
21. Shen J, Rothman DL, Brown P. In vivo GABA editing using a novel doubly selective multiple quantum filter. Magn. Reson. Med. 2002; 47(3): 447–454.
22. Near J, Simpson R, Cowen P, Jezzard P. Efficient gamma-aminobutyric acid editing at 3 T without macromolecule contamination: MEGA-SPECIAL. NMR Biomed. 2011; 24(10): 1277–1285.
23. Aufhaus E, Weber-Fahr W, Sack M, Tunc-Skarka N, Oberthuer G, Hoerst M, Meyer-Lindenberg A, Boettcher U, Ende G. Absence of changes in GABA concentrations with age and gender in the human anterior cingulate cortex: a MEGA-PRESS study with symmetric editing pulse frequencies for macromolecule suppression. Magn. Reson. Med. 2013; 69(2): 317–320.
24. Mikkelsen M, Singh KD, Sumner P, Evans CJ. Comparison of the repeatability of GABA-edited magnetic resonance spectroscopy with and without macromolecule suppression. Magn. Reson. Med. 2016; 75(3): 946–953.
25. Henry PG, Dautry C, Hantraye P, Bloch G. Brain GABA editing without macromolecule contamination. Magn. Reson. Med. 2001; 45(3): 517–520.
26. Edden RA, Puts NA, Barker PB. Macromolecule-suppressed GABA-edited magnetic resonance spectroscopy at 3 T. Magn. Reson. Med. 2012; 68(3): 657–661.
27. Rowland LM, Krause BW, Wijtenburg SA, McMahon RP, Chiappelli J, Nugent KL, Nisonger SJ, Korenic SA, Kochunov P, Hong LE. Medial frontal GABA is lower in older schizophrenia: a MEGA-PRESS with macromolecule suppression study. Mol. Psychiatry 2016; 21(2): 198–204.
28. Deicken RF, Eliaz Y, Feiwell R, Schuff N. Increased thalamic N-acetylaspartate in male patients with familial bipolar I disorder. Psychiatry Res. 2001; 106(1): 35–45.
29. 1H-MRS at 3 Tesla. Investig. Radiol. 2003; 38(7): 403–408.
30. Ongur D, Prescot AP, Jensen JE, Cohen BM, Renshaw PF. Creatine abnormalities in schizophrenia and bipolar disorder. Psychiatry Res. 2009; 172(1): 44–48.
31. Evans CJ, McGonigle DJ, Edden RA. Diurnal stability of gamma-aminobutyric acid concentration in visual and sensorimotor cortex. J. Magn. Reson. Imaging 2010; 31(1): 204–209.
32. Bogner W, Gruber S, Doelken M, Stadlbauer A, Ganslandt O, Boettcher U, Trattnig S, Doerfler A, Stefan H, Hammen T. In vivo quantification of intracerebral GABA by single-voxel (1)H-MRS. How reproducible are the results? Eur. J. Radiol. 2010; 73(3): 526–531.
33. O'Gorman RL, Michels L, Edden RA, Murdoch JB, Martin E. In vivo detection of GABA and glutamate with MEGA-PRESS: reproducibility and gender effects. J. Magn. Reson. Imaging 2011; 33(5): 1262–1267.
34. Geramita M, van der Veen JW, Barnett AS, Savostyanova AA, Shen J, Weinberger DR, Marenco S. Reproducibility of prefrontal gamma-aminobutyric acid measurements with J-edited spectroscopy. NMR Biomed. 2011; 24(9): 1089–1098.
35. Harada M, Kubo H, Nose A, Nishitani H, Matsuda T. Measurement of variation in the human cerebral GABA level by in vivo MEGA-editing proton MR spectroscopy using a clinical 3 T instrument and its dependence on brain region and the female menstrual cycle. Hum. Brain Mapp. 2011; 32(5): 828–833.
36. Wijtenburg SA, Rowland LM, Edden RA, Barker PB. Reproducibility of brain spectroscopy at 7 T using conventional localization and spectral editing techniques. J. Magn. Reson. Imaging 2013; 38(2): 460–467.
37. Near J, Ho YC, Sandberg K, Kumaragamage C, Blicher JU. Long-term reproducibility of GABA magnetic resonance spectroscopy. NeuroImage 2014; 99: 191–196.
38. Gaetz W, Bloy L, Wang DJ, Port RG, Blaskey L, Levy SE, Roberts TP. GABA estimation in the brains of children on the autism spectrum: measurement precision and regional cortical variation. NeuroImage 2014; 86: 1–9.
39. Long Z, Dyke JP, Ma R, Huang CC, Louis ED, Dydak U. Reproducibility and effect of tissue composition on cerebellar gamma-aminobutyric acid (GABA) MRS in an elderly population. NMR Biomed. 2015; 28(10): 1315–1323.
40. Vanhamme L, van den Boogaart A, Van Huffel S. Improved method for accurate and efficient quantification of MRS data with use of prior knowledge. J. Magn. Reson. 1997; 129(1): 35–43.
41. Provencher SW. Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn. Reson. Med. 1993; 30(6): 672–679.
42. Edden RA, Puts NA, Harris AD, Barker PB, Evans CJ. Gannet: A batch-processing tool for the quantitative analysis of gamma-aminobutyric acid-edited MR spectroscopy spectra. J. Magn. Reson. Imaging 2014; 40(6): 1445–1452.
43. Milak MS, Proper CJ, Mulhern ST, Parter AL, Kegeles LS, Ogden RT, Mao X, Rodriguez CI, Oquendo MA, Suckow RF, Cooper TB, Keilp JG, Shungu DC, Mann JJ. A pilot in vivo proton magnetic resonance spectroscopy study of amino acid neurotransmitter response to ketamine treatment of major depressive disorder. Mol. Psychiatry 2016; 21(3): 320–327.
44. Rodriguez CI, Kegeles LS, Levinson A, Ogden RT, Mao X, Milak MS, Vermes D, Xie S, Hunter L, Flood P, Moore H, Shungu DC, Simpson HB. In vivo effects of ketamine on glutamate–glutamine and gamma-aminobutyric acid in obsessive–compulsive disorder: proof of concept. Psychiatry Res. 2015; 233(2): 141–147.