A preliminary study of resting brain metabolism in treatment-resistant depression before and after treatment with olanzapine-fluoxetine combination


Autoři: José V. Pardo aff001;  Sohail A. Sheikh aff001;  Graeme Schwindt aff001;  Joel T. Lee aff001;  David E. Adson aff002;  Barry Rittberg aff002;  Faruk S. Abuzzahab, Sr. aff002
Působiště autorů: Cognitive Neuroimaging Unit, Mental Health PSL, Minneapolis VA Health Care System, Minneapolis, Minnesota, United States of America aff001;  Department of Psychiatry, University of Minnesota, Minneapolis, Minnesota, United States of America aff002
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226486

Souhrn

Treatment-resistant depression (TRD) occurs in many patients and causes high morbidity and mortality. Because TRD subjects are particularly difficult to study especially longitudinally, biological data remain very limited. In a preliminary study to judge feasibility and power, 25 TRD patients were referred from specialty psychiatric practices. All were severely and chronically depressed and mostly had comorbid psychiatric disorders as is typical in TRD. Nine patients were able to complete all required components of the protocol that included diagnostic interview; rating scales; clinical magnetic resonance imaging; medication washout; treatment with maximally tolerated olanzapine-fluoxetine combination for 8 weeks; and pre- and post-treatment fluorodeoxyglucose positron emission tomography. This drug combination is an accepted standard of treatment for TRD. Dropouts arose from worsening depression, insomnia, and anxiety. One patient remitted; three responded. A priori regions of interest included the amygdala and subgenual cingulate cortex (sgACC; Brodmann area BA25). Responders showed decreased metabolism with treatment in the right amygdala that correlated with clinical response; no significant changes in BA25; better response to treatment the higher the baseline BA25 metabolism; and decreased right ventromedial prefrontal metabolism (VMPFC; broader than BA25) with treatment which did not correlate with depression scores. The baseline metabolism of all individuals showed heterogeneous patterns when compared to a normative metabolic database. Although preliminary given the sample size, this study highlights several issues important for future work: marked dropout rate in this study design; need for large sample size for adequate power; baseline metabolic heterogeneity of TRD requiring careful subject characterization for future studies of interventions; relationship of amygdala activity decreases with response; and the relationship between baseline sgACC and VMPFC activity with response. Successful treatment of TRD with olanzapine-fluoxetine combination shows changes in cerebral metabolism like those seen in treatment-responsive major depression.

Klíčová slova:

Amygdala – Antidepressants – Antipsychotics – Depression – Drug metabolism – Drug therapy – Glucose metabolism – Hippocampus


Zdroje

1. Thase ME, Rush AJ. When at first you don't succeed: Sequential strategies for antidepressant nonresponders. J Clin Psychiatry. 1997;58 Suppl 13:23–9.

2. Nemeroff CB. Prevalence and management of treatment-resistant depression. J Clin Psychiatry. 2007;68 Suppl 8:17–25.

3. Fagiolini A, Kupfer DJ. Is treatment-resistant depression a unique subtype of depression? Biol Psychiatry. 2003;53(8):640–8. doi: 10.1016/s0006-3223(02)01670-0 12706950

4. Rush AJ, Trivedi MH, Wisniewski SR, Nierenberg AA, Stewart JW, Warden D, et al. Acute and longer-term outcomes in depressed outpatients requiring one or several treatment steps: A STAR*D report. Am J Psychiatry. 2006;163(11):1905–17. doi: 10.1176/ajp.2006.163.11.1905 17074942

5. Rizvi SJ, Grima E, Tan M, Rotzinger S, Lin P, McIntyre RS, et al. Treatment-resistant depression in primary care across Canada. Can J Psychiatry. 2014;59(7):349–57. doi: 10.1177/070674371405900702 25007419

6. De Carlo V, Calati R, Serretti A. Socio-demographic and clinical predictors of non-response/non-remission in treatment resistant depressed patients: A systematic review. Psychiatry Res. 2016;240:421–30. doi: 10.1016/j.psychres.2016.04.034 27155594

7. Papakostas GI, Petersen TJ, Farabaugh AH, Murakami JL, Pava JA, Alpert JE, et al. Psychiatric comorbidity as a predictor of clinical response to nortriptyline in treatment-resistant major depressive disorder. J Clin Psychiatry. 2003;64(11):1357–61. doi: 10.4088/jcp.v64n1112 14658951

8. Souery D, Oswald P, Massat I, Bailer U, Bollen J, Demyttenaere K, et al. Clinical factors associated with treatment resistance in major depressive disorder: Results from a European multicenter study. J Clin Psychiatry. 2007;68(7):1062–70. doi: 10.4088/jcp.v68n0713 17685743

9. GBD 2015 Disease and Injury Incidence and Prevalence Collaborators ( Vos T, Allen C, Arora M, Barber RM, Bhutta ZA, Brown A, et al.). Global, regional, and national incidence, prevalence, and years lived with disability for 310 diseases and injuries, 1990–2015: A systematic analysis for the global burden of disease study 2015. Lancet. 2016;388(10053):1545–602. doi: 10.1016/S0140-6736(16)31678-6 27733282

10. Mayberg HS, Lozano AM, Voon V, McNeely HE, Seminowicz D, Hamani C, et al. Deep brain stimulation for treatment-resistant depression. Neuron. 2005;45(5):651–60. doi: 10.1016/j.neuron.2005.02.014 15748841

11. Dougherty DD, Weiss AP, Cosgrove GR, Alpert NM, Cassem EH, Nierenberg AA, et al. Cerebral metabolic correlates as potential predictors of response to anterior cingulotomy for treatment of major depression. J Neurosurg. 2003;99(6):1010–7. doi: 10.3171/jns.2003.99.6.1010 14705729

12. Seminowicz DA, Mayberg HS, McIntosh AR, Goldapple K, Kennedy S, Segal Z, et al. Limbic-frontal circuitry in major depression: A path modeling metanalysis. Neuroimage. 2004;22(1):409–18. doi: 10.1016/j.neuroimage.2004.01.015 15110034

13. Li CT, Wang SJ, Hirvonen J, Hsieh JC, Bai YM, Hong CJ, et al. Antidepressant mechanism of add-on repetitive transcranial magnetic stimulation in medication-resistant depression using cerebral glucose metabolism. J Affect Disord. 2010;127(1–3):219–29. doi: 10.1016/j.jad.2010.05.028 20598753

14. Li CT, Su TP, Wang SJ, Tu PC, Hsieh JC. Prefrontal glucose metabolism in medication-resistant major depression. Br J Psychiatry. 2015;206(4):316–23. doi: 10.1192/bjp.bp.113.140434 25657357

15. Li CT, Chen MH, Lin WC, Hong CJ, Yang BH, Liu RS, et al. The effects of low-dose ketamine on the prefrontal cortex and amygdala in treatment-resistant depression: A randomized controlled study. Hum Brain Mapp. 2016;37(3):1080–90. doi: 10.1002/hbm.23085 26821769

16. Conway CR, Chibnall JT, Gebara MA, Price JL, Snyder AZ, Mintun MA, et al. Association of cerebral metabolic activity changes with vagus nerve stimulation antidepressant response in treatment-resistant depression. Brain Stimul. 2013;6(5):788–97. doi: 10.1016/j.brs.2012.11.006 23485649

17. Pardo JV, Sheikh SA, Schwindt GC, Lee JT, Surerus-Johnson C, Pardo PJ, et al. Functional neuroimaging in treatment-resistant depression. Depression: Mind and Body. 2007;3(2):57–70 https://pdfs.semanticscholar.org/f975/b867629c541e404216caa92980707beb28c8.pdf.

18. Pardo JV, Sheikh SA, Schwindt GC, Lee JT, Kuskowski MA, Surerus C, et al. Chronic vagus nerve stimulation for treatment-resistant depression decreases resting ventromedial prefrontal glucose metabolism. Neuroimage. 2008;42(2):879–89. doi: 10.1016/j.neuroimage.2008.04.267 18595737

19. Mayberg HS. Targeted electrode-based modulation of neural circuits for depression. J Clin Invest. 2009;119(4):717–25. doi: 10.1172/JCI38454 19339763

20. Drevets WC. Neuroimaging abnormalities in the amygdala in mood disorders. Ann N Y Acad of Sci. 2006;985:420–44.

21. Drevets WC, Savitz J, Trimble M. The subgenual anterior cingulate cortex in mood disorders. CNS Spectr. 2008;13(8):663–81. doi: 10.1017/s1092852900013754 18704022

22. Kennedy SH, Evans KR, Kruger S, Mayberg HS, Meyer JH, McCann S, et al. Changes in regional brain glucose metabolism measured with positron emission tomography after paroxetine treatment of major depression. Am J Psychiatry. 2001;158(6):899–905. doi: 10.1176/appi.ajp.158.6.899 11384897

23. Mayberg HS, Brannan SK, Tekell JL, Silva JA, Mahurin RK, McGinnis S, et al. Regional metabolic effects of fluoxetine in major depression: Serial changes and relationship to clinical response. Biol Psychiatry. 2000;48(8):830–43. doi: 10.1016/s0006-3223(00)01036-2 11063978

24. Li CT, Chen LF, Tu PC, Wang SJ, Chen MH, Su TP, et al. Impaired prefronto-thalamic functional connectivity as a key feature of treatment-resistant depression: A combined MEG, PET and rTMS study. PLoS One. 2013;8(8):e70089. doi: 10.1371/journal.pone.0070089 23936378

25. Cao B, Luo Q, Fu Y, Du L, Qiu T, Yang X, et al. Predicting individual responses to the electroconvulsive therapy with hippocampal subfield volumes in major depression disorder. Sci Rep. 2018;8(1):5434. doi: 10.1038/s41598-018-23685-9 29615675

26. Gosnell SN, Curtis KN, Velasquez K, Fowler JC, Madan A, Goodman W, et al. Habenular connectivity may predict treatment response in depressed psychiatric inpatients. J Affect Disord. 2019;242:211–9. doi: 10.1016/j.jad.2018.08.026 30195174

27. Hamilton JP, Siemer M, Gotlib IH. Amygdala volume in major depressive disorder: a meta-analysis of magnetic resonance imaging studies. Mol Psychiatry. 2008;13(11):993–1000. doi: 10.1038/mp.2008.57 18504424

28. Brown SSG, Rutland JW, Verma G, Feldman RE, Alper J, Schneider M, et al. Structural MRI at 7T reveals amygdala nuclei and hippocampal subfield volumetric association with major depressive disorder symptom severity. Sci Rep. 2019;9(1):10166. doi: 10.1038/s41598-019-46687-7 31308432

29. Sheline YI, Barch DM, Donnelly JM, Ollinger JM, Snyder AZ, Mintun MA. Increased amygdala response to masked emotional faces in depressed subjects resolves with antidepressant treatment: an fMRI study. Biol Psychiatry. 2001;50(9):651–8. doi: 10.1016/s0006-3223(01)01263-x 11704071

30. Victor TA, Furey ML, Fromm SJ, Ohman A, Drevets WC. Relationship between amygdala responses to masked faces and mood state and treatment in major depressive disorder. Arch Gen Psychiatry. 2010;67(11):1128–38. doi: 10.1001/archgenpsychiatry.2010.144 21041614

31. Siegle GJ, Carter CS, Thase ME. Use of FMRI to predict recovery from unipolar depression with cognitive behavior therapy. Am J Psychiatry. 2006;163(4):735–8. doi: 10.1176/appi.ajp.163.4.735 16585452

32. Siegle GJ, Steinhauer SR, Thase ME, Stenger VA, Carter CS. Can't shake that feeling: event-related fMRI assessment of sustained amygdala activity in response to emotional information in depressed individuals. Biol Psychiatry. 2002;51(9):693–707. doi: 10.1016/s0006-3223(02)01314-8 11983183

33. Cullen KR, Westlund MK, Klimes-Dougan B, Mueller BA, Houri A, Eberly LE, et al. Abnormal amygdala resting-state functional connectivity in adolescent depression. JAMA Psychiatry. 2014;71(10):1138–47. doi: 10.1001/jamapsychiatry.2014.1087 25133665

34. Ramasubbu R, Konduru N, Cortese F, Bray S, Gaxiola-Valdez I, Goodyear B. Reduced intrinsic connectivity of amygdala in adults with major depressive disorder. Front Psychiatry. 2014;5:17. doi: 10.3389/fpsyt.2014.00017 24600410

35. Ambrosi E, Arciniegas DB, Madan A, Curtis KN, Patriquin MA, Jorge RE, et al. Insula and amygdala resting-state functional connectivity differentiate bipolar from unipolar depression. Acta Psychiatr Scand. 2017;136(1):129–39. doi: 10.1111/acps.12724 28369737

36. Tang Y, Kong L, Wu F, Womer F, Jiang W, Cao Y, et al. Decreased functional connectivity between the amygdala and the left ventral prefrontal cortex in treatment-naive patients with major depressive disorder: a resting-state functional magnetic resonance imaging study. Psychol Med. 2013;43(9):1921–7. doi: 10.1017/S0033291712002759 23194671

37. Price JL. Comparative aspects of amygdala connectivity. Ann N Y Acad Sci. 2003;985:50–8. doi: 10.1111/j.1749-6632.2003.tb07070.x 12724147

38. Senn V, Wolff Steffen BE, Herry C, Grenier F, Ehrlich I, Gründemann J, et al. Long-range connectivity defines behavioral specificity of amygdala neurons. Neuron. 2014;81(2):428–37. doi: 10.1016/j.neuron.2013.11.006 24462103

39. Sharma KK, Kelly EA, Pfeifer CW, Fudge JL. Translating fear circuitry: Amygdala projections to subgenual and perigenual anterior cingulate in the macaque. Cereb Cortex. 2019. doi: 10.1093/cercor/bhz106 31219571

40. Drevets WC, Price JL, Simpson JR Jr., Todd RD, Reich T, Vannier M, et al. Subgenual prefrontal cortex abnormalities in mood disorders. Nature. 1997;386(6627):824–7. doi: 10.1038/386824a0 9126739

41. Rajkowska G, Miguel-Hidalgo JJ, Wei J, Dilley G, Pittman SD, Meltzer HY, et al. Morphometric evidence for neuronal and glial prefrontal cell pathology in major depression. Biol Psychiatry. 1999;45(9):1085–98. doi: 10.1016/s0006-3223(99)00041-4 10331101

42. Botteron KN, Raichle ME, Drevets WC, Heath AC, Todd RD. Volumetric reduction in left subgenual prefrontal cortex in early onset depression. Biol Psychiatry. 2002;51(4):342–4. doi: 10.1016/s0006-3223(01)01280-x 11958786

43. Mayberg HS, Silva JA, Brannan SK, Tekell JL, Mahurin RK, McGinnis S, et al. The functional neuroanatomy of the placebo effect. Am J Psychiatry. 2002;159(5):728–37. doi: 10.1176/appi.ajp.159.5.728 11986125

44. Nobler MS, Oquendo MA, Kegeles LS, Malone KM, Campbell C, Sackeim HA, et al. Decreased regional brain metabolism after ECT. Am J Psychiatry. 2001;158(2):305–8. doi: 10.1176/appi.ajp.158.2.305 11156816

45. Riva-Posse P, Choi KS, Holtzheimer PE, McIntyre CC, Gross RE, Chaturvedi A, et al. Defining critical white matter pathways mediating successful subcallosal cingulate deep brain stimulation for treatment-resistant depression. Biol Psychiatry. 2014. 76(12):963–9. doi: 10.1016/j.biopsych.2014.03.029 24832866

46. Fox MD, Buckner RL, White MP, Greicius MD, Pascual-Leone A. Efficacy of transcranial magnetic stimulation targets for depression is related to intrinsic functional connectivity with the subgenual cingulate. Biol Psychiatry. 2012;72(7):595–603. doi: 10.1016/j.biopsych.2012.04.028 22658708

47. Zald DH, Mattson DL, Pardo JV. Brain activity in ventromedial prefrontal cortex correlates with individual differences in negative affect. Proc Natl Acad Sci U S A. 2002;99(4):2450–4. doi: 10.1073/pnas.042457199 11842195

48. Epstein LR. Symbyax: The first medication approved for treatment-resistant depression. Pharmanote. 2009;24(11):1–6.

49. Shelton RC, Williamson DJ, Corya SA, Sanger TM, Van Campen LE, Case M, et al. Olanzapine/fluoxetine combination for treatment-resistant depression: A controlled study of SSRI and nortriptyline resistance. J Clin Psychiatry. 2005;66(10):1289–97. doi: 10.4088/jcp.v66n1012 16259543

50. Shelton RC, Tollefson GD, Tohen M, Stahl S, Gannon KS, Jacobs TG, et al. A novel augmentation strategy for treating resistant major depression. Am J Psychiatry. 2001;158(1):131–4. doi: 10.1176/appi.ajp.158.1.131 11136647

51. Haridas RM, Parkar SR, Ghulam R, Amin G, Thombre KG, Srivastava A, et al. Olanzapine and fluoxetine combination in severe or resistant depression. Indian J Psychiatry. 2003;45(4):234–8. 21206864

52. Bobo WV, Shelton RC. Efficacy, safety and tolerability of Symbyax for acute-phase management of treatment-resistant depression. Expert Rev Neurother. 2010;10(5):651–70. doi: 10.1586/ern.10.44 20420487

53. Trivedi MH, Thase ME, Osuntokun O, Henley DB, Case M, Watson SB, et al. An integrated analysis of olanzapine/fluoxetine combination in clinical trials of treatment-resistant depression. J Clin Psychiatry. 2009;70(3):387–96. doi: 10.4088/jcp.08m04064 19284928

54. Brunner E, Tohen M, Osuntokun O, Landry J, Thase ME. Efficacy and safety of olanzapine/fluoxetine combination vs fluoxetine monotherapy following successful combination therapy of treatment-resistant major depressive disorder. Neuropsychopharmacology. 2014;39(11):2549–59. doi: 10.1038/npp.2014.101 24801768

55. Luan S, Wan H, Wang S, Li H, Zhang B. Efficacy and safety of olanzapine/fluoxetine combination in the treatment of treatment-resistant depression: A meta-analysis of randomized controlled trials. Neuropsychiatr Dis Treat. 2017;13:609–20. doi: 10.2147/NDT.S127453 28280343

56. Dodd S, Berk M. Olanzapine/fluoxetine combination for treatment-resistant depression: Efficacy and clinical utility. Expert Rev Neurother. 2008;8(9):1299–306. doi: 10.1586/14737175.8.9.1299 18759541

57. Zhang W, Perry KW, Wong DT, Potts BD, Bao J, Tollefson GD, et al. Synergistic effects of olanzapine and other antipsychotic agents in combination with fluoxetine on norepinephrine and dopamine release in rat prefrontal cortex. Neuropsychopharmacology. 2000;23(3):250–62. doi: 10.1016/S0893-133X(00)00119-6 10942849

58. Koch S, Perry KW, Bymaster FP. Brain region and dose effects of an olanzapine/fluoxetine combination on extracellular monoamine concentrations in the rat. Neuropharmacology. 2004;46(2):232–42. doi: 10.1016/j.neuropharm.2003.09.001 14680761

59. Horowitz JM, Goyal A, Ramdeen N, Hallas BH, Horowitz AT, Torres G. Characterization of fluoxetine plus olanzapine treatment in rats: A behavior, endocrine, and immediate-early gene expression analysis. Synapse. 2003;50(4):353–64. doi: 10.1002/syn.10276 14556240

60. Kodama M, Fujioka T, Duman RS. Chronic olanzapine or fluoxetine administration increases cell proliferation in hippocampus and prefrontal cortex of adult rat. Biol Psychiatry. 2004;56(8):570–80. doi: 10.1016/j.biopsych.2004.07.008 15476686

61. Agostinho FR, Reus GZ, Stringari RB, Ribeiro KF, Pfaffenseller B, Stertz L, et al. Olanzapine plus fluoxetine treatment increases NT-3 protein levels in the rat prefrontal cortex. Neurosci Lett. 2011;497(2):99–103. doi: 10.1016/j.neulet.2011.04.039 21545827

62. Spitzer RL, Williams JB, Gibbon M, First MB. The Structured Clinical interview for DSM-III-R (SCID). I: History, rationale, and description. Arch Gen Psychiatry. 1992;49(8):624–9. doi: 10.1001/archpsyc.1992.01820080032005 1637252

63. Pardo JV, Lee JT, Kuskowski MA, Munch KR, Carlis JV, Sheikh SA, et al. Fluorodeoxyglucose positron emission tomography of mild cognitive impairment with clinical follow-up at 3 years. Alzheimers Dement. 2010;6(4):326–33. doi: 10.1016/j.jalz.2009.09.005 20447873

64. First MB, Gibbon M, Spitzer RL, Williams JBW. Structured Clinical Interview for DSM-IV Axis I Disorders, Clinician Version (SCID-CV). Washington, D.C.: American Psychiatric Press, Inc., 1996. New York: American Psychiatric Publishing, Inc.; 1996.

65. Montgomery SA, Asberg M. A new depression scale designed to be sensitive to change. Br J Psychiatry. 1979;134:382–9. doi: 10.1192/bjp.134.4.382 444788

66. Corruble E, Purper D, Payan C, Guelfi J. Inter-rater reliability of two depression rating scales, MADRS and DRRS, based on videotape records of structured interviews. Eur Psychiatry. 1998;13(5):264–6. doi: 10.1016/S0924-9338(98)80032-1 19698636

67. Fantino B, Moore N. The self-reported Montgomery-Asberg Depression Rating Scale is a useful evaluative tool in Major Depressive Disorder. BMC Psychiatry. 2009;9:26. doi: 10.1186/1471-244X-9-26 19473506

68. Zimovetz EA, Wolowacz SE, Classi PM, Birt J. Methodologies used in cost-effectiveness models for evaluating treatments in major depressive disorder: a systematic review. Cost Eff Resour Alloc. 2012;10(1):1. doi: 10.1186/1478-7547-10-1 22296830

69. Hamilton M. The assessment of anxiety states by rating. Br J Med Psychol. 1959;32(1):50–5. doi: 10.1111/j.2044-8341.1959.tb00467.x 13638508

70. Guy W. ECDEU Assessment Manual For Psychopharmacology. Rockville, MD: US Department of Heath, Education, and Welfare Public Health Service Alcohol, Drug Abuse, and Mental Health Administration; 1976.

71. Folstein MF, Folstein SE, McHugh PR. "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975;12(3):189–98. doi: 10.1016/0022-3956(75)90026-6 1202204

72. Zachary RA. Shipley Institute of Living Scale Revised Manual. Los Angeles: Western Psychological Services; 1986.

73. Oldfield RC. The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia. 1971;9(1):97–113. doi: 10.1016/0028-3932(71)90067-4 5146491

74. McNair DM, Lorr M, Droppleman LF. Manual for the Profile Of Mood States. San Diego, CA: Educational and Industrial Testing Services; 1971.

75. Watson D, Clark LA. Preliminary manual for the positive affective negative affect schedule. J Pers Soc. 1999;44:644–51.

76. Minoshima S, Koeppe RA, Frey KA, Kuhl DE. Anatomic standardization: Linear scaling and nonlinear warping of functional brain images. J Nucl Med. 1994;35(9):1528–37. 8071705

77. Lee JT, Munch KR, Carlis JV, Pardo JV. Internet image viewer (iiv). BMC Med Imaging. 2008;8:10. doi: 10.1186/1471-2342-8-10 18510765

78. Talairach J, Tournoux P. Coplanar Stereotaxic Atlas of the Human Brain. New York: Thieme; 1988.

79. Drevets WC, Savitz J, Trimble M. The subgenual cingulate cortex in mood disorde. CNS Spectr. 2008;13(8): 663–681. doi: 10.1017/s1092852900013754 18704022

80. Lancaster JL, Woldorff MG, Parsons LM, Liotti M, Freitas CS, Rainey L, et al. Automated Talairach atlas labels for functional brain mapping. Hum Brain Mapp. 2000;10(3):120–31. doi: 10.1002/1097-0193(200007)10:3<120::aid-hbm30>3.0.co;2-8 10912591

81. Zald DH, Lee JT, Fluegel KW, Pardo JV. Aversive gustatory stimulation activates limbic circuits in humans. Brain. 1998;121 (Pt 6):1143–54.

82. Liotti M, Mayberg HS. The role of functional neuroimaging in the neuropsyhcology of depression. J Clin Exp Neuropsychol. 2001; 23(1):121–36. doi: 10.1076/jcen.23.1.121.1223 11320448

83. Vaccarino AL, Evans KR, Sills TL, Kalali AH. Symptoms of anxiety in depression: Assessment of item performance of the hamilton anxiety rating scale in patients with depression. Depress Anxiety. 2008;25(12):1006–13. doi: 10.1002/da.20435 18800370

84. Schmidt ME, Ernst M, Matochik JA, Maisog JM, Pan BS, Zametkin AJ, et al. Cerebral glucose metabolism during pharmacologic studies: Test-retest under placebo conditions. J Nucl Med. 1996;37(7):1142–9. 8965185

85. Schaefer SM, Abercrombie HC, Lindgren KA, Larson CL, Ward RT, Oakes TR, et al. Six-month test-retest reliability of MRI-defined PET measures of regional cerebral glucose metabolic rate in selected subcortical structures. Hum Brain Mapp. 2000;10(1):1–9. doi: 10.1002/(sici)1097-0193(200005)10:1<1::aid-hbm10>3.0.co;2-o 10843513

86. Fallmar D, Lilja J, Kilander L, Danfors T, Lubberink M, Larsson EM, et al. Validation of true low-dose 18F-FDG PET of the brain. Am J Nucl Med Mol Imaging. 2016;6(5):269–76. 27766185


Článek vyšel v časopise

PLOS One


2020 Číslo 1