Cortical folding defects as markers of poor treatment response in first-episode psychosis

JAMA Psychiatry

Volumn 70, Issue 10, 2013, Pages 1031-1040

  Palaniyappan, Lena ^a   Marques, Tiago Reis ^b   Taylor, Heather ^b   Handley, Rowena ^d   Mondelli, Valeria ^b   Bonaccorso, Stefania ^b   Giordano, Annalisa ^b,c   McQueen, Grant ^b   DiForti, Marta ^b   Simmons, Andrew ^b   David, Anthony S ^b   Pariante, Carmine M ^b   Murray, Robin M ^b   Dazzan, Paola ^b,c  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c SOUTH LONDON AND MAUDSLEY NHS FOUNDATION TRUST   (United Kingdom)

^d BRISTOL MYERS SQUIBB   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMISULPRIDE; ARIPIPRAZOLE; FLUPENTIXOL; HALOPERIDOL; OLANZAPINE; QUETIAPINE; RISPERIDONE; NEUROLEPTIC AGENT;

ADULT; AFFECTIVE PSYCHOSIS; ANGULAR GYRUS; ARTICLE; BIPOLAR DISORDER; BRAIN CORTEX LESION; BRAIN SIZE; CASE CONTROL STUDY; CLINICAL ASSESSMENT; CONTROLLED STUDY; CORTICAL GYRIFICATION; DEPRESSION; DRUG TREATMENT FAILURE; FEMALE; FOLLOW UP; GRAY MATTER; HANDEDNESS; HUMAN; INFERIOR FRONTAL GYRUS; INTELLIGENCE QUOTIENT; LEFT HEMISPHERE; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MALE; MENTAL HEALTH SERVICE; MIDDLE FRONTAL GYRUS; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; OUTCOME ASSESSMENT; POSITIVE AND NEGATIVE SYNDROME SCALE; PRECUNEUS; PRIMARY MOTOR CORTEX; PSYCHOSIS; RIGHT HEMISPHERE; SCHIZOAFFECTIVE PSYCHOSIS; SCHIZOPHRENIA; TREATMENT DURATION; TREATMENT RESPONSE; WHITE MATTER; BRAIN CORTEX; PATHOLOGY; PSYCHOTIC DISORDERS; TREATMENT FAILURE;

ADULT; ANTIPSYCHOTIC AGENTS; CASE-CONTROL STUDIES; CEREBRAL CORTEX; FEMALE; HUMANS; MALE; NEUROIMAGING; PSYCHOTIC DISORDERS; TREATMENT FAILURE;

EID: 84885209280     PISSN: 2168622X     EISSN: None     Source Type: Journal    
DOI: 10.1001/jamapsychiatry.2013.203     Document Type: Article

References (75)

1. Emsley R, Rabinowitz J, Medori R; Early Psychosis GlobalWorking Group. Remission in early psychosis: rates, predictors, and clinical and functional outcome correlates. Schizophr Res. 2007;89(1-3):129-139.
2. LambertM, Naber D, Schacht A, et al. Rates and predictors of remission and recovery during 3 years in 392 never-treated patients with schizophrenia. Acta Psychiatr Scand. 2008;118(3):220-229.
3. Alvarez-Jimenez M, Gleeson JF, Henry LP, et al. Prediction of a single psychotic episode: a 7.5-year, prospective study in first-episode psychosis. Schizophr Res. 2011;125(2-3):236-246.
4. Mourao-Miranda J, Reinders AATS, Rocha-Rego V, et al. Individualized prediction of illness course at the first psychotic episode: a support vector machine MRI study. Psychol Med. 2012;42(5):1037-1047.
5. Friedman L, Lys C, Schulz SC. The relationship of structural brain imaging parameters to antipsychotic treatment response: a review. J Psychiatry Neurosci. 1992;17(2):42-54.
6. Zipursky RB, Zhang-Wong J, Lambe EK, Bean G, Beiser M. MRI correlates of treatment response in first episode psychosis. Schizophr Res. 1998;30(1):81-90.
7. Arango C, Breier A, McMahon R, CarpenterWT Jr, Buchanan RW. The relationship of clozapine and haloperidol treatment response to prefrontal, hippocampal, and caudate brain volumes. Am J Psychiatry. 2003;160(8):1421-1427.
8. Molina V, Reig S, Sarramea F, et al. Anatomical and functional brain variables associated with clozapine response in treatment-resistant schizophrenia. Psychiatry Res. 2003;124(3):153-161.
9. Molina V, Martín C, Ballesteros A, de Herrera AG, Hernández-Tamames JA. Optimized voxel brain morphometry: association between brain volumes and the response to atypical antipsychotics. Eur Arch Psychiatry Clin Neurosci. 2011;261(6):407-416.
10. Csernansky JG, Gillespie SK, Dierker DL, et al. Symmetric abnormalities in sulcal patterning in schizophrenia. Neuroimage. 2008;43(3):440-446.
11. Palaniyappan L, Liddle PF. Differential effects of surface area, gyrification and cortical thickness on voxel based morphometric deficits in schizophrenia. Neuroimage. 2012;60(1):693-699.
12. Mangin JF, Jouvent E, Cachia A. In-vivo measurement of cortical morphology: means and meanings. Curr Opin Neurol. 2010;23(4):359-367.
13. Stanfield AC, Moorhead TW, Harris JM, Owens DG, Lawrie SM, Johnstone EC. Increased right prefrontal cortical folding in adolescents at risk of schizophrenia for cognitive reasons. Biol Psychiatry. 2008;63(1):80-85.
14. van Haren NE, Schnack HG, CahnW, et al. Changes in cortical thickness during the course of illness in schizophrenia. Arch Gen Psychiatry. 2011;68(9):871-880.
15. Palaniyappan L, Mallikarjun P, Joseph V, White TP, Liddle PF. Regional contraction of brain surface area involves three large-scale networks in schizophrenia. Schizophr Res. 2011;129(2-3): 163-168.
16. Palaniyappan L, Liddle PF. Aberrant cortical gyrification in schizophrenia: a surface-based morphometry study. J Psychiatry Neurosci. 2012;37(6):399-406.
17. Harris JM, Yates S, Miller P, Best JJ, Johnstone EC, Lawrie SM. Gyrification in first-episode schizophrenia: a morphometric study. Biol Psychiatry. 2004;55(2):141-147.
18. White T, Hilgetag CC. Gyrification and neural connectivity in schizophrenia. Dev Psychopathol. 2011;23(1):339-352.
19. Giménez M, Junqué C, Vendrell P, et al. Abnormal orbitofrontal development due to prematurity. Neurology. 2006;67(10):1818-1822.
20. Kesler SR, Vohr B, Schneider KC, et al. Increased temporal lobe gyrification in preterm children. Neuropsychologia. 2006;44(3):445-453.
21. Haukvik UK, Schaer M, Nesvåg R, et al. Cortical folding in Broca's area relates to obstetric complications in schizophrenia patients and healthy controls. Psychol Med. 2012;42(6):1329-1337.
22. Dubois J, BendersM, Borradori-Tolsa C, et al. Primary cortical folding in the human newborn: an early marker of later functional development. Brain. 2008;131(pt 8):2028-2041.
23. Palaniyappan L, Liddle PF. Dissociable morphometric differences of the inferior parietal lobule in schizophrenia. Eur Arch Psychiatry Clin Neurosci. 2012;262(7):579-587.
24. Cachia A, Paillère-Martinot ML, Galinowski A, et al. Cortical folding abnormalities in schizophrenia patients with resistant auditory hallucinations. Neuroimage. 2008;39(3):927-935.
25. Demjaha A, MacCabe JH, Murray RM. How genes and environmental factors determine the different neurodevelopmental trajectories of schizophrenia and bipolar disorder. Schizophr Bull. 2012;38(2):209-214.
26. Friedman L, Knutson L, ShurellM, Meltzer HY. Prefrontal sulcal prominence is inversely related to response to clozapine in schizophrenia. Biol Psychiatry. 1991;29(9):865-877.
27. HonerWG, Smith GN, Lapointe JS, MacEwan GW, Kopala L, Altman S. Regional cortical anatomy and clozapine response in refractory schizophrenia. Neuropsychopharmacology. 1995;13(1):85-87.
28. Konicki PE, Kwon KY, Steele V, et al. Prefrontal cortical sulcal widening associated with poor treatment response to clozapine. Schizophr Res. 2001;48(2-3):173-176.
29. Singh SP, Cooper JE, Fisher HL, et al. Determining the chronology and components of psychosis onset: the Nottingham Onset Schedule (NOS). Schizophr Res. 2005;80(1):117-130.
30. Bebbington P, Nayani T. The Psychosis Screening Questionnaire. Int JMethods Psychiatr Res. 1995;5(1):11-19.
31. McGuffin P, Farmer A, Harvey I. A polydiagnostic application of operational criteria in studies of psychotic illness: development and reliability of the OPCRIT system. Arch Gen Psychiatry. 1991;48(8):764-770.
32. Kay SR, Fiszbein A, Opler LA. The Positive and Negative Syndrome Scale (PANSS) for schizophrenia. Schizophr Bull. 1987;13(2):261-276.
33. Handley R, Zelaya FO, Reinders AA, et al. Acute effects of single-dose aripiprazole and haloperidol on resting cerebral blood flow (rCBF) in the human brain. Hum Brain Mapp. 2013;34(2):272-282.
34. AtkinsM, Burgess A, Bottomley C, RiccioM. Chlorpromazine equivalents: a consensus of opinion for both clinical and research applications. Psychiatr Bull. 1997;21(4):224-226. doi:10.1192/pb.21.4.224.
35. Woods SW. Chlorpromazine equivalent doses for the newer atypical antipsychotics. J Clin Psychiatry. 2003;64(6):663-667.
36. Nelson HE, O'Connell A. Dementia: the estimation of premorbid intelligence levels using the New Adult Reading Test. Cortex. 1978;14(2):234-244.
37. Annett M. A classification of hand preference by association analysis. Br J Psychol. 1970;61(3):303-321.
38. Taylor D, Paton C, Kerwin R. The Maudsley Prescribing Guidelines. Boca Raton, FL: CRC Press; 2007.
39. Jablensky A, Sartorius N, Ernberg G, et al. Schizophrenia: manifestations, incidence and course in different cultures: aWorld Health Organization ten-country study. Psychol Med Monogr Suppl. 1992;20:1-97.
40. Andreasen NC, CarpenterWT Jr, Kane JM, Lasser RA, Marder SR,Weinberger DR. Remission in schizophrenia: proposed criteria and rationale for consensus. Am J Psychiatry. 2005;162(3):441-449.
41. Leucht S, Davis JM, Engel RR, Kane JM, Wagenpfeil S. Defining "response" in antipsychotic drug trials: recommendations for the use of scale-derived cutoffs. Neuropsychopharmacology. 2007;32(9):1903-1910.
42. Simmons A,Westman E, Muehlboeck S, et al. The AddNeuroMed framework for multi-centre MRI assessment of Alzheimer's disease: experience from the first 24 months. Int J Geriatr Psychiatry. 2011;26(1):75-82.
43. Dale AM, Fischl B, Sereno MI. Cortical surface-based analysis, I: segmentation and surface reconstruction. Neuroimage. 1999;9(2):179-194.
44. Fischl B, Sereno MI, Dale AM. Cortical surface-based analysis, II: inflation, flattening, and a surface-based coordinate system. Neuroimage. 1999;9(2):195-207.
45. Schaer M, Cuadra MB, Tamarit L, Lazeyras F, Eliez S, Thiran J-P. A surface-based approach to quantify local cortical gyrification. IEEE Trans Med Imaging. 2008;27(2):161-170.
46. Palaniyappan L, Mallikarjun P, Joseph V, White TP, Liddle PF. Folding of the prefrontal cortex in schizophrenia: regional differences in gyrification. Biol Psychiatry. 2011;69(10):974-979.
47. Zilles K, Armstrong E, Schleicher A, Kretschmann H-J. The human pattern of gyrification in the cerebral cortex. Anat Embryol (Berl). 1988;179(2):173-179.
48. Schaer M, Cuadra MB, Schmansky N, Fischl B, Thiran J-P, Eliez S. How to measure cortical folding fromMR images: a step-by-step tutorial to compute local gyrification index. J Vis Exp. 2012;(59):e3417.
49. Hagler DJ Jr, Saygin AP, Sereno MI. Smoothing and cluster thresholding for cortical surface-based group analysis of fMRI data. Neuroimage. 2006;33(4):1093-1103.
50. Szeszko PR, Narr KL, Phillips OR, et al. Magnetic resonance imaging predictors of treatment response in first-episode schizophrenia. Schizophr Bull. 2012;38(3):569-578.
51. Mechelli A, Price CJ, Friston KJ, Ashburner J. Voxel-based morphometry of the human brain: methods and applications. Curr Med Imaging Rev. 2005;1(2):105-113. doi:10.2174/1573405054038726.
52. Lauriello J, Mathalon DH, Rosenbloom M, et al. Association between regional brain volumes and clozapine response in schizophrenia. Biol Psychiatry. 1998;43(12):879-886.
53. SeeleyWW, Menon V, Schatzberg AF, et al. Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci. 2007;27(9):2349-2356.
54. Habas C, Kamdar N, Nguyen D, et al. Distinct cerebellar contributions to intrinsic connectivity networks. J Neurosci. 2009;29(26):8586-8594.
55. Palaniyappan L, Liddle PF. Does the salience network play a cardinal role in psychosis? an emerging hypothesis of insular dysfunction. J Psychiatry Neurosci. 2012;37(1):17-27.
56. Palaniyappan L, Mallikarjun P, Joseph V, White TP, Liddle PF. Reality distortion is related to the structure of the salience network in schizophrenia. Psychol Med. 2011;41(8):1701-1708.
57. Kumari V, Peters ER, Fannon D, et al. Dorsolateral prefrontal cortex activity predicts responsiveness to cognitive-behavioral therapy in schizophrenia. Biol Psychiatry. 2009;66(6): 594-602.
58. Garner B, Berger GE, Nicolo JP, et al. Pituitary volume and early treatment response in drug-naïve first-episode psychosis patients. Schizophr Res. 2009;113(1):65-71.
59. Chan RC, Di X, McAlonan GM, Gong QY. Brain anatomical abnormalities in high-risk individuals, first-episode, and chronic schizophrenia: an activation likelihood estimationmeta-analysis of illness progression. Schizophr Bull. 2011;37(1):177-188.
60. LeungM, Cheung C, Yu K, et al. Gray matter in first-episode schizophrenia before and after antipsychotic drug treatment: anatomical likelihood estimationmeta-analyses with sample size weighting. Schizophr Bull. 2011;37(1):199-211.
61. Adler CM, DelBello MP, Jarvis K, Levine A, Adams J, Strakowski SM. Voxel-based study of structural changes in first-episode patients with bipolar disorder. Biol Psychiatry. 2007;61(6): 776-781.
62. Vita A, De Peri L, Sacchetti E. Gray matter, white matter, brain, and intracranial volumes in first-episode bipolar disorder: ameta-analysis of magnetic resonance imaging studies. Bipolar Disord. 2009;11(8):807-814.
63. Yatham LN, Lyoo IK, Liddle P, et al. Amagnetic resonance imaging study of mood stabilizer- and neuroleptic-naïve first-episode mania. Bipolar Disord. 2007;9(7):693-697.
64. Dazzan P, Soulsby B, Mechelli A, et al. Volumetric abnormalities predating the onset of schizophrenia and affective psychoses: an MRI study in subjects at ultrahigh risk of psychosis. Schizophr Bull. 2012;38(5):1083-1091.
65. de Castro-Manglano P, Mechelli A, Soutullo C, et al. Structural brain abnormalities in first-episode psychosis: differences between affective psychoses and schizophrenia and relationship to clinical outcome. Bipolar Disord. 2011;13(5-6):545-555.
66. Farrow TFD, Whitford TJ, Williams LM, Gomes L, Harris AWF. Diagnosis-related regional gray matter loss over two years in first episode schizophrenia and bipolar disorder. Biol Psychiatry. 2005;58(9):713-723.
67. Dazzan P, Lloyd T, Morgan KD, et al. Neurological abnormalities and cognitive ability in first-episode psychosis. Br J Psychiatry. 2008;193(3):197-202.
68. Gay O, PlazeM, Oppenheim C, et al. Cortex morphology in first-episode psychosis patients with neurological soft signs. Schizophr Bull. 2013;39(4):820-829.
69. Das M, Kumari V, SoniW, et al. Neurological soft signs and their relationship to cognitive and clinical efficacy of atypical antipsychotics in schizophrenia. Schizophr Bull. 2004;30(2):241-253.
70. Penttilä J, Paillère-Martinot ML, Martinot JL, et al. Cortical folding in patients with bipolar disorder or unipolar depression. J Psychiatry Neurosci. 2009;34(2):127-135.
71. Olabi B, Ellison-Wright I, McIntosh AM,Wood SJ, Bullmore E, Lawrie SM. Are there progressive brain changes in schizophrenia? ameta-analysis of structural magnetic resonance imaging studies. Biol Psychiatry. 2011;70(1):88-96.
72. Van Essen DC. A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature. 1997;385(6614):313-318.
73. Schultz CC, Koch K,Wagner G, et al. Increased parahippocampal and lingual gyrification in first-episode schizophrenia. Schizophr Res. 2010;123(2-3):137-144.
74. Schultz CC,Wagner G, Koch K, et al. The visual cortex in schizophrenia: alterations of gyrification rather than cortical thickness: a combined cortical shape analysis. Brain Struct Funct. 2013;218(1):51-58.
75. Orrù G, Pettersson-YeoW, Marquand AF, Sartori G, Mechelli A. Using Support Vector Machine to identify imaging biomarkers of neurological and psychiatric disease: a critical review. Neurosci Biobehav Rev. 2012;36(4):1140-1152.