Evidence of altered membrane phospholipid metabolism in the anterior cingulate cortex and striatum of patients with bipolar disorder I: A multi-voxel 1H MRS study

Journal of Psychiatric Research

Volumn 81, Issue , 2016, Pages 48-55

  Cao, Bo ^a   Stanley, Jeffrey A ^b   Selvaraj, Sudhakar ^a   Mwangi, Benson ^a   Passos, Ives Cavalcante ^a   Zunta Soares, Giovana B ^a   Soares, Jair C ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

1H MRS; Anterior cingulate cortex; Basal ganglia; Bipolar disorder; Caudate; Choline; Proton magnetic resonance spectroscopy; Putamen; Striatum

Indexed keywords

GLUTAMIC ACID; GLYCEROPHOSPHORYLCHOLINE; INOSITOL; MEMBRANE PHOSPHOLIPID; PHOSPHORYLCHOLINE; CREATINE; PHOSPHOLIPID;

ADULT; ANTERIOR CINGULATE; ARTICLE; BASAL GANGLION; BIPOLAR I DISORDER; BRAIN METABOLISM; CAUDATE NUCLEUS; CLINICAL ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DIAGNOSTIC AND STATISTICAL MANUAL OF MENTAL DISORDERS; DORSAL STRIATUM; FEMALE; HUMAN; IN VIVO STUDY; MALE; MIDDLE AGED; MULTI VOXEL PROTON NUCLEAR MAGNETIC RESONANCE; NEUTRON ACTIVATION ANALYSIS; PHOSPHOLIPID METABOLISM; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; PUTAMEN; YOUNG ADULT; YOUNG MANIA RATING SCALE; AGED; BIPOLAR DISORDER; CINGULATE GYRUS; DIAGNOSTIC IMAGING; METABOLISM; PATHOLOGY; PSYCHOLOGICAL RATING SCALE;

ADULT; AGED; BIPOLAR DISORDER; CORPUS STRIATUM; CREATINE; FEMALE; GLUTAMIC ACID; GYRUS CINGULI; HUMANS; MALE; MIDDLE AGED; PHOSPHOLIPIDS; PROTON MAGNETIC RESONANCE SPECTROSCOPY; PSYCHIATRIC STATUS RATING SCALES; YOUNG ADULT;

EID: 84976869143     PISSN: 00223956     EISSN: 18791379     Source Type: Journal    
DOI: 10.1016/j.jpsychires.2016.06.006     Document Type: Article

References (60)

1. Adler, C.M., DelBello, M.P., Weber, W. a., Jarvis, K.B., Welge, J., Chu, W.-J., Rummelhoff, E., Kim, M.-J., Lee, J.-H., Strakowski, S.M., Neurochemical effects of quetiapine in patients with bipolar mania. J. Clin. Psychopharmacol. 33 (2013), 528–532, 10.1097/JCP.0b013e3182905b77.
2. Amaral, J.A.D.M.S., Tamada, R.S., Issler, C.K., Caetano, S.C., Cerri, G.G., de Castro, C.C., Lafer, B., A 1HMRS study of the anterior cingulate gyrus in euthymic bipolar patients. Hum. Psychopharmacol. 21 (2006), 215–220, 10.1002/hup.761.
3. Bitsch, A., Bruhn, H., Vougioukas, V., Stringaris, A., Lassmann, H., Frahm, J., Brück, W., Inflammatory CNS demyelination: histopathologic correlation with in vivo quantitative proton MR spectroscopy. AJNR. Am. J. Neuroradiol. 20 (1999), 1619–1627 doi:Cliff-grant -Converted #28; ERN-Converted #103; Master_Reference_List-Converted #269; Used to be #1841 and #2119.
4. Bokemeyer, M., Ding, X.-Q., Goldbecker, a, Raab, P., Heeren, M., Arvanitis, D., Tillmann, H.L., Lanfermann, H., Weissenborn, K., Evidence for neuroinflammation and neuroprotection in HCV infection-associated encephalopathy. Gut 60 (2011), 370–377, 10.1136/gut.2010.217976.
5. Bush, G., Luu, P., Posner, M., Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn. Sci. 4 (2000), 215–222, 10.1016/S1364-6613(00)01483-2.
6. Bustillo, J.R., Rowland, L.M., Lauriello, J., Petropoulos, H., Hammond, R., Hart, B., Brooks, W.M., High choline concentrations in the caudate nucleus in antipsychotic-naive patients with schizophrenia. Am. J. Psychiatry 159 (2002), 130–133, 10.1176/appi.ajp.159.1.130.
7. Chang, L., Munsaka, S.M., Kraft-Terry, S., Ernst, T., Magnetic resonance spectroscopy to assess neuroinflammation and neuropathic pain. J. Neuroimmune Pharmacol. 8 (2013), 576–593, 10.1007/s11481-013-9460-x.
8. Dager, S.R., Friedman, S.D., Parow, A., Demopulos, C., Stoll, A.L., Lyoo, I.K., Dunner, D.L., Renshaw, P.F., Brain metabolic alterations in medication-free patients with bipolar disorder. Arch. Gen. Psychiatry 61 (2004), 450–458, 10.1001/archpsyc.61.5.450.
9. Dale, A.M., Fischl, B., Sereno, M.I., Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 9 (1999), 179–194, 10.1006/nimg.1998.0395.
10. De Stefano, N., Filippi, M., Miller, D., Pouwels, P., Rovira, a, Gass, a, Enzinger, C., Matthews, P., Arnold, D., Guidelines for Using Proton MR Spectroscopy in Multicenter Clinical MS Studies. 2007.
11. Ehrlich, A., Schubert, F., Pehrs, C., Gallinat, J., Alterations of cerebral glutamate in the euthymic state of patients with bipolar disorder. Psychiatry Res. Neuroimaging, 2015, 1–8, 10.1016/j.pscychresns.2015.05.010.
12. Fillman, S.G., Sinclair, D., Fung, S.J., Webster, M.J., Shannon Weickert, C., Markers of inflammation and stress distinguish subsets of individuals with schizophrenia and bipolar disorder. Transl. Psychiatry, 4, 2014, e365, 10.1038/tp.2014.8.
13. Frederick, B. deB., Satlin, A., Wald, L.L., Hennen, J., Bodick, N., Renshaw, P.F., Brain proton magnetic resonance spectroscopy in alzheimer disease. Am. J. Geriatr. Psychiatry 10 (2002), 81–88, 10.1097/00019442-200201000-00010.
14. Frye, M.A., Thomas, M.A., Yue, K., Binesh, N., Davanzo, P., Ventura, J., O'Neill, J., Guze, B., Curran, J.G., Mintz, J., Reduced concentrations of N-acetylaspartate (NAA) and the NAA-creatine ratio in the basal ganglia in bipolar disorder: a study using 3-Tesla proton magnetic resonance spectroscopy. Psychiatry Res. - Neuroimaging 154 (2007), 259–265, 10.1016/j.pscychresns.2006.11.003.
15. Frye, M.A., Watzl, J., Banakar, S., O'Neill, J., Mintz, J., Davanzo, P., Fischer, J., Chirichigno, J.W., Ventura, J., Elman, S., Tsuang, J., Walot, I., Thomas, M.A., Increased anterior cingulate/medial prefrontal cortical glutamate and creatine in bipolar depression. Neuropsychopharmacology 32 (2007), 2490–2499, 10.1038/sj.npp.1301387.
16. Gabbay, V., Hess, D. a., Liu, S., Babb, J.S., Klein, R.G., Gonen, O., Lateralized caudate metabolic abnormalities in adolescent major depressive disorder: a proton MR spectroscopy study. Am. J. Psychiatry 164 (2007), 1881–1889, 10.1176/appi.ajp.2007.06122032.
17. Gasparovic, C., Song, T., Devier, D., Bockholt, H.J., Caprihan, A., Mullins, P.G., Posse, S., Jung, R.E., Morrison, L.A., Use of tissue water as a concentration reference for proton spectroscopic imaging. Magn. Reson. Med. 55 (2006), 1219–1226, 10.1002/mrm.20901.
18. Govindaraju, V., Young, K., Maudsley, A.A., Proton NMR chemical shifts and coupling constants for brain metabolites. NMR Biomed. 13 (2000), 129–153, 10.1002/1099-1492(200005)13:3<129::AID-NBM619>3.0.CO;2-V.
19. Haldane, M., Frangou, S., New insights help define the pathophysiology of bipolar affective disorder: neuroimaging and neuropathology findings. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 28 (2004), 943–960, 10.1016/j.pnpbp.2004.05.040.
20. Hamakawa, H., Kato, T., Murashita, J., Kato, N., Quantitative proton magnetic resonance spectroscopy of the basal ganglia in patients with affective disorders. Eur. Arch. Psychiatry Clin. Neurosci. 248 (1998), 53–58, 10.1007/s004060050017.
21. Hamilton, M., Rating depressive patients. J. Clin. Psychiatry 41 (1980), 21–24.
22. Janowsky, D., Davis, J., El-Yousef, M.K., Sekerke, H.J., A cholinergic-adrenergic hypothesis of mania and depression. Lancet 300 (1972), 632–635, 10.1016/S0140-6736(72)93021-8.
23. Kato, T., Hamakawa, H., Shioiri, T., Murashita, J., Takahashi, Y., Takahashi, S., Inubushi, T., Choline-containing compounds detected by proton magnetic resonance spectroscopy in the basal ganglia in bipolar disorder. J. Psychiatry Neurosci. 21 (1996), 248–254.
24. Mader, I., Roser, W., Kappos, L., Hagberg, G., Seelig, J., Radue, E.W., Steinbrich, W., Serial proton MR spectroscopy of contrast-enhancing multiple sclerosis plaques: absolute metabolic values over 2 years during a clinical pharmacological study. Am. J. Neuroradiol. 21 (2000), 1220–1227.
25. Mcclure, R.J., Kanfer, J.N., Pettegreiwmf, J.W., Alzheimer ’ s Disease: membrane-associated metabolic changes. Ann. N. Y. Acad. Sci., 1994, 110–124.
26. McClure, R.J., Kanfer, J.N., Panchalingam, K., Klunk, W.E., Pettegrew, J.W., Alzheimer's disease: membrane-associated metabolic changes. Ann. N. Y. Acad. Sci. 747 (1994), 110–124, 10.1111/j.1749-6632.1994.tb44404.x.
27. Merikangas, K.R., Akiskal, H.S., Angst, J., Greenberg, P.E., Hirschfeld, R.M.A., Petukhova, M., Kessler, R.C., Lifetime and 12-month prevalence of bipolar spectrum disorder in the National Comorbidity Survey replication. Arch. Gen. Psychiatry 64 (2007), 543–552, 10.1001/archpsyc.64.5.543.
28. Michaelis, T., Merboldt, K.D., Bruhn, H., Hänicke, W., Frahm, J., Absolute concentrations of metabolites in the adult human brain in vivo: quantification of localized proton MR spectra. Radiology 187 (1993), 219–227, 10.1148/radiology.187.1.8451417.
29. Miller, D., Albert, P., Barkhof, F., Guidelines for the use of magnetic resonance techniques in monitoring the treatment of multiple sclerosis. Ann. Neurol. 39 (1996), 6–16.
30. Moore, C.M., Breeze, J.L., Gruber, S.A., Babb, S.M., Frederick, B.B., Villafuerte, R.A., Stoll, A.L., Hennen, J., Yurgelun-Todd, D.A., Cohen, B.M., Renshaw, P.F., Choline, myo-inositol and mood in bipolar disorder: a proton magnetic resonance spectroscopic imaging study of the anterior cingulate cortex. Bipolar Disord. 2 (2000), 207–216.
31. Najjar, S., Pearlman, D.M., Alper, K., Najjar, A., Devinsky, O., Neuroinflammation and psychiatric illness. J. Neuroinflamm., 10, 2013, 43, 10.1186/1742-2094-10-43.
32. Ohara, K., Isoda, H., Suzuki, Y., Takehara, Y., Ochiai, M., Takeda, H., Igarashi, Y., Ohara, K., Proton magnetic resonance spectroscopy of the lenticular nuclei in bipolar I affective disorder. Psychiatry Res. - Neuroimaging 84 (1998), 55–60, 10.1016/S0925-4927(98)00050-X.
33. Öngür, D., Jensen, J.E., Prescot, A.P., Stork, C., Lundy, M., Cohen, B.M., Renshaw, P.F., Abnormal glutamatergic neurotransmission and neuronal-glial interactions in acute mania. Biol. Psychiatry 64 (2008), 718–726, 10.1016/j.biopsych.2008.05.014.
34. Ongür, D., Prescot, A.P., Jensen, J.E., Cohen, B.M., Renshaw, P.F., Creatine abnormalities in schizophrenia and bipolar disorder. Psychiatry Res. 172 (2009), 44–48, 10.1016/j.pscychresns.2008.06.002.
35. Phillips, M.L., Ladouceur, C.D., Drevets, W.C., A neural model of voluntary and automatic emotion regulation: implications for understanding the pathophysiology and neurodevelopment of bipolar disorder. Mol. Psychiatry 13:829 (2008), 833–857, 10.1038/mp.2008.65.
36. Port, J.D., Unal, S.S., Mrazek, D. a., Marcus, S.M., Metabolic alterations in medication-free patients with bipolar disorder: a 3T CSF-corrected magnetic resonance spectroscopic imaging study. Psychiatry Res. - Neuroimaging 162 (2008), 113–121, 10.1016/j.pscychresns.2007.08.004.
37. Provencher, S.W., Automatic quantitation of localized in vivo 1H spectra with LCModel. NMR Biomed. 14 (2001), 260–264, 10.1002/nbm.698.
38. Ramaprasad, S., Ripp, E., Pi, J., Lyon, M., Pharmacokinetics of lithium in rat brain regions by spectroscopic imaging. Magn. Reson. Imaging 23 (2005), 859–863, 10.1016/j.mri.2005.07.007.
39. Rao, J.S., Harry, G.J., Rapoport, S.I., Kim, H.W., Increased excitotoxicity and neuroinflammatory markers in postmortem frontal cortex from bipolar disorder patients. Mol. Psychiatry 15 (2010), 384–392, 10.1038/mp.2009.47.
40. Satlin, A., Bodick, N., Offen, W.W., Renshaw, P.F., Brain proton magnetic resonance spectroscopy (1H-MRS) in Alzheimer's disease: changes after treatment with xanomeline, an M1 selective cholinergic agonist. Am. J. Psychiatry 154 (1997), 1459–1461.
41. Scherk, H., Backens, M., Schneider-Axmann, T., Kemmer, C., Usher, J., Reith, W., Falkai, P., Gruber, O., Neurochemical pathology in hippocampus in euthymic patients with bipolar I disorder. Acta Psychiatr. Scand. 117 (2008), 283–288, 10.1111/j.1600-0447.2007.01142.x.
42. Schubert, F., Gallinat, J., Seifert, F., Rinneberg, H., Glutamate concentrations in human brain using single voxel proton magnetic resonance spectroscopy at 3 Tesla. Neuroimage 21 (2004), 1762–1771, 10.1016/j.neuroimage.2003.11.014.
43. Selvaraj, S., Arnone, D., Job, D., Stanfield, A., Farrow, T.F., Nugent, A.C., Scherk, H., Gruber, O., Chen, X., Sachdev, P.S., Dickstein, D.P., Malhi, G.S., Ha, T.H., Ha, K., Phillips, M.L., McIntosh, A.M., Grey matter differences in bipolar disorder: a meta-analysis of voxel-based morphometry studies. Bipolar Disord. 14 (2012), 135–145, 10.1111/j.1399-5618.2012.01000.x.
44. Sesack, S.R., Grace, A.A., Cortico-Basal Ganglia reward network: microcircuitry. Neuropsychopharmacology 35 (2010), 27–47, 10.1038/npp.2009.93.
45. Shahana, N., DelBello, M., Chu, W.J., Jarvis, K., Fleck, D., Welge, J., Strakowski, S., Adler, C., Neurochemical alteration in the caudate: implications for the pathophysiology of bipolar disorder. Psychiatry Res. - Neuroimaging 193 (2011), 107–112, 10.1016/j.pscychresns.2011.01.014.
46. Smith, S.M., Jenkinson, M., Woolrich, M.W., Beckmann, C.F., Behrens, T.E.J., Johansen-Berg, H., Bannister, P.R., De Luca, M., Drobnjak, I., Flitney, D.E., Niazy, R.K., Saunders, J., Vickers, J., Zhang, Y., De Stefano, N., Brady, J.M., Matthews, P.M., Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage, 2004, 10.1016/j.neuroimage.2004.07.051.
47. Soares, J.C., Contributions from brain imaging to the elucidation of pathophysiology of bipolar disorder. Int. J. Neuropsychopharmacol. 6 (2003), 171–180, 10.1017/S1461145703003390.
48. Spirtes, M.A., Lithium levels in monkey and human brain after chronic, therapeutic, oral dosage. Pharmacol. Biochem. Behav. 5 (1976), 143–147, 10.1016/0091-3057(76)90030-7.
49. Stanley, J.A., In vivo magnetic resonance spectroscopy and its application to neuropsychiatric disorders. Can. J. Psychiatry 47 (2002), 315–326.
50. Stanley, J.A., Pettegrew, J.W., Keshavan, M.S., Magnetic resonance spectroscopy in schizophrenia: methodological issues and findings–part I. Biol. Psychiatry 48 (2000), 357–368.
51. Stertz, L., Magalhães, P.V.S., Kapczinski, F., Is bipolar disorder an inflammatory condition? the relevance of microglial activation. Curr. Opin. Psychiatry 26 (2013), 19–26, 10.1097/YCO.0b013e32835aa4b4.
52. Stork, C., Renshaw, P.F., Mitochondrial dysfunction in bipolar disorder: evidence from magnetic resonance spectroscopy research. Mol. Psychiatry 10 (2005), 900–919, 10.1038/sj.mp.4001711.
53. Strakowski, S.M., Delbello, M.P., Adler, C.M., The functional neuroanatomy of bipolar disorder: a review of neuroimaging findings. Mol. Psychiatry 10 (2005), 105–116, 10.1038/sj.mp.4001585.
54. Tartaglia, M.C., Narayanan, S., De Stefano, N., Arnaoutelis, R., Antel, S.B., Francis, S.J., Santos, a. C., Lapierre, Y., Arnold, D.L., Choline is increased in pre-lesional normal appearing white matter in multiple sclerosis. J. Neurol. 249 (2002), 1382–1390, 10.1007/s00415-002-0846-6.
55. van Enkhuizen, J., Janowsky, D.S., Olivier, B., Minassian, A., Perry, W., Young, J.W., Geyer, M. a, The catecholaminergic-cholinergic balance hypothesis of bipolar disorder revisited. Eur. J. Pharmacol. 753 (2014), 1–13, 10.1016/j.ejphar.2014.05.063.
56. Watkins, C.C., Sawa, A., Pomper, M.G., Glia and immune cell signaling in bipolar disorder: insights from neuropharmacology and molecular imaging to clinical application. Transl. Psychiatry, 4, 2014, e350, 10.1038/tp.2013.119.
57. 31P MRS study. Proc. 22nd Annu. Meet. Int. Soc. Magn. Reson. Med, 2014.
58. Young, J.W., Dulcis, D., Investigating the mechanism(s) underlying switching between states in bipolar disorder. Eur. J. Pharmacol. 759 (2015), 151–162, 10.1016/j.ejphar.2015.03.019.
59. Young, R.C., Biggs, J.T., Ziegler, V.E., Meyer, D.A., A rating scale for mania: reliability, validity and sensitivity. Br. J. Psychiatry 133 (1978), 429–435, 10.1192/bjp.133.5.429.
60. Zhong, S., Wang, Y., Zhao, G., Xiang, Q., Ling, X., Liu, S., Huang, L., Jia, Y., Similarities of biochemical abnormalities between major depressive disorder and bipolar depression: a proton magnetic resonance spectroscopy study. J. Affect. Disord. 168 (2014), 380–386, 10.1016/j.jad.2014.07.024.