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Discriminating schizophrenia and schizo-obsessive disorder: a structural MRI study combining VBM and machine learning methods

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Abstract

Schizo-obsessive disorder is characterized by the clinical syndrome in which comorbid obsessive–compulsive disorder accompanies schizophrenia. A substantial number of studies have investigated the neuropsychological and clinical differences between schizophrenia and schizo-obsessive disorder. However, the neurostructural differences between these two groups have not been adequately investigated. The aim of this study was to explore gray matter differences between schizophrenia and schizo-obsessive patients using voxel-based morphometry and support vector machines combined with feature selection algorithm. Twenty-three schizophrenia and 23 schizo-obsessive patients matched by age, gender and handedness were recruited. Clinical assessments were completed in addition to high-resolution structural MRI scanning. Group differences were investigated using contrast maps, and significant regions were subjected to a feature selection and support vector machine hybrid model. In addition, voxel-of-interest values for the commonly shared brain areas between schizophrenia and OCD reported in previous meta-analyses were also used as inputs in this step. The results showed that schizo-obsessive patients had greater gray matter densities in paracentral areas (including supplementary motor area) and middle cingulate gyrus than schizophrenia patients. These brain areas together with the fronto-subcortical areas could successfully discriminate two groups with an accuracy of 78.26 %. Our results provide the first neuroanatomical evidence that schizo-obsessive disorder and schizophrenia may be two distinct clinical entities. Based on these findings, considering schizo-obsessive disorder as a subtype of schizophrenia is discernible.

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References

  1. Poyurovsky M, Hramenkov S, Isakov V, Rauchverger B, Modai I, Schneidman M, Fuchs C, Weizman A (2001) Obsessive–compulsive disorder in hospitalized patients with chronic schizophrenia. Psychiatry Res 102:49–57

    Article  Google Scholar 

  2. Bottas A, Cooke RG, Richter MA (2005) Comorbidity and pathophysiology of obsessive–compulsive disorder in schizophrenia: Is there evidence for a schizo-obsessive subtype of schizophrenia? J Psychiatry Neurosci 30:187–193

    Google Scholar 

  3. Braff DL, Ryan J, Rissling AJ, Carpenter WT (2013) Lack of use in the literature from the last 20 years supports dropping traditional schizophrenia subtypes from DSM-5 and ICD-11. Schizophr Bull 39:751–753

    Article  Google Scholar 

  4. Berman I, Sapers BL, Chang HH, Losonczy MF, Schmildler J, Green AI (1995) Treatment of obsessive–compulsive symptoms in schizophrenic patients with clomipramine. J Clin Psychopharmacol 15:206–210

    Article  Google Scholar 

  5. Sevincok L, Akoglu A, Topaloglu B, Aslantas H (2004) Neurological soft signs in schizophrenic patients with obsessive–compulsive disorder. Psychiatry Clin Neurosci 58:274–279

    Article  Google Scholar 

  6. Nechmad A, Ratzoni G, Poyurovsk M, Meged S, Avidan G, Fuchs C, Bloch Y, Weizman R (2003) Obsessive–compulsive disorder in adolescent schizophrenia patients. Am J Psychiatry 160:1002–1004

    Article  Google Scholar 

  7. Michalopoulou PG, Konstantakopoulos G, Typaldou M, Papageorgiou C, Christodoulou GN, Lykouras L, Oulis P (2014) Can cognitive deficits differentiate between schizophrenia with and without obsessive–compulsive symptoms? Compr Psychiatry 55:1015–1021

    Article  Google Scholar 

  8. Cunill R, Huerta Ramos E, Castells X (2013) The effect of obsessive–compulsive symptomatology on executive functions in schizophrenia: a systematic review and meta-analysis. Psychiatry Res 210:21–28

    Article  Google Scholar 

  9. Tibbo P, Kroetsch M, Chue P, Warneke L (2000) Obsessive–compulsive disorder in schizophrenia. J Psychiatr Res 34:139–146

    Article  Google Scholar 

  10. Cunill R, Castells X, Simeon D (2009) Relationships between obsessive–compulsive symptomatology and severity of psychosis in schizophrenia: a systematic review and meta-analysis. J Clin Psychiatry 70:70–82

    Article  Google Scholar 

  11. Üçok A, Ceylan ME, Tihan AK, Lapçin S, Ger C, Tükel R (2010) Obsessive compulsive disorder and symptoms may have different effects on schizophrenia. Prog Neuro-Psychopharmacol 35:429–433

    Article  Google Scholar 

  12. Patel DD, Laws KR, Padhi A, Farrow JM, Mukhopadhaya K, Krishnaiah R, Fineberg NA (2010) The neuropsychology of the schizo-obsessive subtype of schizophrenia: a new analysis. Psychol Med 40:921–933

    Article  Google Scholar 

  13. Iida J, Matumura K, Aoyama F, Iwasaka H, Hirao F, Sakiyama S (1998) Cerebral MRI findings in childhood-onset schizophrenia, comparison of patients with prodromal obsessive–compulsive symptoms and those without symptoms. Recent Prog Child Adolesc Psychiatry 2:75–83

    Google Scholar 

  14. Aoyama F, Iida J, Inoue M, Iwasaka H, Sakiyam S, Hata K, Kishimoto T (2000) Brain imaging in childhood- and adolescence-onset schizophrenia associated with obsessive–compulsive symptoms. Acta Psychiatr Scand 102:32–37

    Article  Google Scholar 

  15. Gross Isseroff R, Hermesh H, Zohar J, Weizman A (2003) Neuroimaging communality between schizophrenia and obsessive compulsive disorder: A putative basis for schizo-obsessive disorder? World J Biol 4:129–134

    Google Scholar 

  16. Menzies L, Chamberlain SR, Laird AR, Thelen SM, Sahakian BJ, Bullmore ET (2008) Integrating evidence from neuroimaging and neuropsychological studies of obsessive–compulsive disorder: the orbitofronto-striatal model revisited. Neurosci Biobehav R 32:525–549

    Article  Google Scholar 

  17. Rotge JY, Guehl D, Dilharreguy B, Tignol J, Bioulac B, Allard M, Burbaud P, Aouizerate B (2009) Meta-analysis of brain volume changes in obsessive–compulsive disorder. Biol Psychiatry 65:75–83

    Article  Google Scholar 

  18. Rotge JY, Langbour N, Guehl D, Bioulac B, Jaafar N, Allard M, Aouizerate B, Burbaud P (2010) Gray matter alterations in obsessive–compulsive disorder: an anatomic likelihood estimation meta-analysis. Neuropsychopharmacology 35:686–691

    Article  Google Scholar 

  19. Bor E, Fornito A, Radu J, Walterfang M, Seal M, Wood SJ, Yücel M, Velakoulis D, Pantelis C (2011) Neuroanatomical abnormalities in schizophrenia: a multimodal voxelwise meta-analysis and meta-regression analysis. Schizophr Res 127:46–57

    Article  Google Scholar 

  20. Fusar-Poli P, Radua J, McGuire P, Borgwardt S (2011) Neuroanatomical maps ofpsychosis onset: voxel-wise meta-analysis of antipsychotic-naive VBM studies. Schizophr Bull 38:1297–1307

    Article  Google Scholar 

  21. Glahn DC, Laird AR, Ellison-Wright I, Thelen SM, Robinson JL, Lancaster JL, Bullmore E, Fox PT (2008) Meta-analysis of gray matter anomalies in schizophrenia: application of anatomic likelihood estimation and network analysis. Biol Psychiatry 64:774–781

    Article  Google Scholar 

  22. McIntosh AM, Job DE, Moorhead TW, Harrison LK, Forrester K, Lawrie SM, Johnstone EC (2004) Voxel-based morphometry of patients with schizophrenia or bipolar disorder and their unaffected relatives. Biol Psychiatry 56:544–552

    Article  Google Scholar 

  23. Orrù G, Pettersson-Yeo W, Marquand AF, Sartori G, Mechelli A (2012) Using support vector machine to identify imaging biomarkers of neurological and psychiatric disease: a critical review. Neurosci Biobehav R 36:1140–1152

    Article  Google Scholar 

  24. Lemm S, Blankertz B, Dickhaus T, Müller KR (2011) Introduction to machine learning for brain imaging. Neuroimage 56:387–399

    Article  Google Scholar 

  25. Liu Y, Teverovskiy L, Carmichael O, Kikinis R, Shenton M, Carter CS, Stenger VA, Davis S, Aizenstein H, Becker J, Lopez O, Meltzer C (2004) Discriminative MR image feature analysis for automatic schizophrenia and Alzheimer’s disease classification. In: Barillot C, David H, Hellier R, Pierre (eds) Medical image computing and computer-assisted intervention—MICCAI2004 7th international conference. Springer, Saint-Malo, pp 393–401

  26. Ecker C, Rocha-Rego V, Johnston P, Mourao-Miranda J, Marquand A, Daly EM, Brammer MJ, Murphy C, Murphy DG (2010) Investigating the predictive value of whole-brain structural MR scans in autism: a pattern classification approach. NeuroImage 49:44–56

    Article  Google Scholar 

  27. Magnin B, Mesrob L, Kinkingnéhun S, Pélégrini-Issac M, Colliot O, Sarazin M, Dubois B, Lehéricy S, Benali H (2009) Support vector machine-based classification of Alzheimer’s disease from whole-brain anatomical MRI. Neuroradiology 51:73–83

    Article  Google Scholar 

  28. Erguzel TT, Ozekes S, Tan O, Gultekin S (2014) Feature selection and classification of electroencephalographic signals an artificial neural network and genetic algorithm based approach. Clin EEG Neurosci. doi:10.1177/1550059414523764

    Google Scholar 

  29. Huang CL (2009) ACO-based hybrid classification system with feature subset selection and model parameters optimization. Neurocomputing 73:438–448

    Article  Google Scholar 

  30. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

    Article  Google Scholar 

  31. Rijcken CA, Monster TB, Brouwers JR (2003) Chlorpromazine equivalents versus defined daily doses: How to compare antipsychotic drug doses? J Clin Psychopharmacol 23:657–659

    Article  Google Scholar 

  32. Kroken RA, Johnsen E, Ruud T, Wentzel-Larsen T, Jørgensen HA (2009) Treatment of schizophrenia with antipsychotics in Norwegian emergency wards, a cross-sectional national study. BMC Psychiatry 9:24

    Article  Google Scholar 

  33. Doyle M, Chorcorain AN, Griffith E, Trimble T, O’Callaghan E (2014) Obsessive compulsive symptoms in patients with Schizophrenia on clozapine and with obsessive compulsive disorder: a comparison study. Compr Psychiatry 55:130–136

    Article  Google Scholar 

  34. Overall JE, Gorham DR (1962) The brief psychiatric rating scale. Psychol Rep 10:799–812

    Article  Google Scholar 

  35. Kay SR, Flszbein A, Opfer LA (1987) The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull 13:261

    Article  Google Scholar 

  36. Goodman WK, Price LH, Rasmussen SA, Mazure C, Fleischmann RL, Hill CL, Heninger GR, Charney DS (1989) The Yale-Brown obsessive compulsive scale: I. Development, use, and reliability. Arch Gen Psychiatry 46:1006–1011

    Article  Google Scholar 

  37. Ashburner J, Friston KJ (2000) Voxel-based morphometry—the methods. NeuroImage 11:805–821

    Article  Google Scholar 

  38. Ashburner J (2007) A fast diffeomorphic image registration algorithm. NeuroImage 38:95–113

    Article  Google Scholar 

  39. Lao Z, Shen D, Xue Z, Karacali B, Resnick SM, Davatzikos C (2004) Morphological classification of brains via high-dimensional shape transformations and machine learning methods. Neuroimage 21:46–57

    Article  Google Scholar 

  40. Fung G, Stoeckel J (2007) SVM feature selection for classification of SPECT images of Alzheimer’s disease using spatial information. Knowl Inf Syst 11:243–258

    Article  Google Scholar 

  41. Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. NeuroImage 19:1233–1239

    Article  Google Scholar 

  42. Kohavi R, John GH (1997) Wrappers for feature subset selection. Artif Intell 97:273–324

    Article  MATH  Google Scholar 

  43. Li Y, Wang G, Chen H, Shi L, Qin L (2013) An ant colony optimization based dimension reduction method for high-dimensional datasets. J Bionic Eng 10:231–241

    Article  Google Scholar 

  44. Dorigo M, Gambardella LM (1997) Ant colony system: a cooperative learning approach to the traveling salesman problem. IEEE Trans Evol Comput 1:53–66

    Article  Google Scholar 

  45. Song S, Zhan Z, Long Z, Zhang J, Yao L (2011) Comparative study of SVM methods combined with voxel selection for object category classification on fMRI data. PLoS One 6(2):e17191

    Article  Google Scholar 

  46. Norman KA, Polyn SM, Detre GJ, Haxby JV (2006) Beyond mind-reading: multi-voxel pattern analysis of fMRI data. Trends Cognit Sci 10:424–430

    Article  Google Scholar 

  47. Misaki M, Kim Y, Bandettini P, Kriegeskorte N (2010) Comparison of multivariate classifiers and response normalizations for pattern-information fMRI. NeuroImage 53:103–118

    Article  Google Scholar 

  48. Douglas PK, Lau E, Anderson A, Head A, Kerr W, Wollner M, Cohen MS (2013) Single trial decoding of belief decision making from EEG and fMRI data using independent components features. Front Hum Neurosci 7:392

    Article  Google Scholar 

  49. Krstajic D, Buturovic LJ, Leahy DE, Thomas S (2014) Cross-validation pitfalls when selecting and assessing regression and classification models. J Cheminform 6:1–15

    Article  Google Scholar 

  50. Japkowicz N, Shah M (2011) Evaluating learning algorithms: a classification perspective. Cambridge University Press, Cambridge

    Book  MATH  Google Scholar 

  51. Varma S, Simon R (2006) Bias in error estimation when using cross-validation for model selection. BMC Bioinform 7:91

    Article  Google Scholar 

  52. Exner C, Weniger G, Schmidt-Samoa C, Irle E (2006) Reduced size of the pre-supplementary motor cortex and impaired motor sequence learning in first-episode schizophrenia. Schizophr Res 84:386–396

    Article  Google Scholar 

  53. Voets NL, Hough MG, Douaud G, Matthews PM, James A, Winmill L, Webster P, Smith S (2008) Evidence for abnormalities of cortical development in adolescent-onset schizophrenia. NeuroImage 43:665–675

    Article  Google Scholar 

  54. Stegmayer K, Horn H, Federspiel A, Razav N, Bracht T, Laimböck K, Strik W, Dierks T, Wiest R, Müller TJ (2014) Supplementary motor area (SMA) volume is associated with psychotic aberrant motor behaviour of patients with schizophrenia. Psychiatry Res Neuroimaging 223:49–51

    Article  Google Scholar 

  55. Goldberg G (1985) Supplementary motor area structure and function: review and hypotheses. Behav Brain Sci 8:567–588

    Article  Google Scholar 

  56. Jürgens U (1984) The efferent and afferent connections of the supplementary motor area. Brain Res 300:63–81

    Article  Google Scholar 

  57. Hoffstaedter F, Grefkes C, Caspers S, Roski C, Palomero-Gallagher N, Laird AN, Fox PT, Eickhoff SB (2013) The role of anterior midcingulate cortex in cognitive motor control. Hum Brain Mapp 35:2741–2753

    Article  Google Scholar 

  58. Vogt BA, Berger GR, Derbyshire SW (2003) Structural and functional dichotomy of human midcingulate cortex. Eur J Neurosci 18:3134–3144

    Article  Google Scholar 

  59. Iacoboni M, Molnar-Szakacs I, Gallese V, Buccino G, Mazziotta JC, Rizzolatti G (2005) Grasping the intentions of others with one’s own mirror neuron system. PLoS Biol 3:79

    Article  Google Scholar 

  60. Gould IC, Shepherd AM, Laurens KR, Cairns MJ, Carr VJ, Green MJ (2014) Multivariate neuroanatomical classification of cognitive subtypes in schizophrenia: a support vector machine learning approach. Neuroimage Clin 18:229–236

    Article  Google Scholar 

  61. Riffkin J, Yücel M, Maruff P, Wood SJ, Soulsby B, Olver J, Pantelis C (2005) A manual and automated MRI study of anterior cingulate and orbito-frontal cortices, and caudate nucleus in obsessive–compulsive disorder: comparison with healthy controls and patients with schizophrenia. Psychiatry Res Neuroimaging 138:99–113

    Article  Google Scholar 

  62. Rajkumar RP, Reddy Y, Kandavel T (2008) Clinical profile of “schizo-obsessive” disorder: a comparative study. Compr Psychiatry 49:262–268

    Article  Google Scholar 

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Acknowledgments

Uskudar University Research Council and NPIstanbul Neuropsychiatry Hospital funded the sample collection and MRI scans (No. NPI-120814).

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Correspondence to Cumhur Tas.

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Tas, C., Mogulkoc, H., Eryilmaz, G. et al. Discriminating schizophrenia and schizo-obsessive disorder: a structural MRI study combining VBM and machine learning methods. Neural Comput & Applic 29, 377–387 (2018). https://doi.org/10.1007/s00521-016-2451-0

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