Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-10T15:20:09.045Z Has data issue: false hasContentIssue false
  • English
  • Français

Relationship between symptom dimensions and white matter alterations in obsessive-compulsive disorder

Published online by Cambridge University Press:  13 September 2016

Michiyo Yagi ,
Yoshiyuki Hirano Open the ORCID record for Yoshiyuki Hirano [Opens in a new window] ,
Michiko Nakazato ,
Kiyotaka Nemoto Open the ORCID record for Kiyotaka Nemoto [Opens in a new window] ,
Kazuhiro Ishikawa ,
Chihiro Sutoh Open the ORCID record for Chihiro Sutoh [Opens in a new window] ,
Haruko Miyata ,
Junko Matsumoto ,
Koji Matsumoto  and
Yoshitada Masuda
...Show all authors
Michiyo Yagi
Affiliation:
Research Center for Child Mental Development, Chiba University, Chiba, Japan United Graduate School of Child Development, Osaka University, Kanazawa University, Hamamatsu University School of Medicine, Chiba University and University of Fukui, Suita, Osaka, Japan
Yoshiyuki Hirano*
Affiliation:
Research Center for Child Mental Development, Chiba University, Chiba, Japan United Graduate School of Child Development, Osaka University, Kanazawa University, Hamamatsu University School of Medicine, Chiba University and University of Fukui, Suita, Osaka, Japan Department of Molecular Imaging and Theranostics, National Institute of Radiological Sciences, National Institutes for Quantum and Radiological Science and Technology, Chiba, Japan
Michiko Nakazato
Affiliation:
Research Center for Child Mental Development, Chiba University, Chiba, Japan United Graduate School of Child Development, Osaka University, Kanazawa University, Hamamatsu University School of Medicine, Chiba University and University of Fukui, Suita, Osaka, Japan
Kiyotaka Nemoto
Affiliation:
Department of Psychiatry, Division of Clinical Medicine, Faculty of Medicine, University of Tsukuba, Tsukuba, Japan
Kazuhiro Ishikawa
Affiliation:
Ibaraki Prefectural Medical Center of Psychiatry, Kasama, Japan
Chihiro Sutoh
Affiliation:
Department of Molecular Imaging and Theranostics, National Institute of Radiological Sciences, National Institutes for Quantum and Radiological Science and Technology, Chiba, Japan Department of Cognitive Behavioral Physiology, Graduate School of Medicine, Chiba University, Chiba, Japan
Haruko Miyata
Affiliation:
Research Center for Child Mental Development, Chiba University, Chiba, Japan
Junko Matsumoto
Affiliation:
Department of Regional Disaster Medicine, Graduate School of Medicine, Chiba University, Chiba, Japan
Koji Matsumoto
Affiliation:
Department of Radiology, Chiba University Hospital, Chiba, Japan
Yoshitada Masuda
Affiliation:
Department of Radiology, Chiba University Hospital, Chiba, Japan
Takayuki Obata
Affiliation:
Research Center for Child Mental Development, Chiba University, Chiba, Japan Department of Molecular Imaging and Theranostics, National Institute of Radiological Sciences, National Institutes for Quantum and Radiological Science and Technology, Chiba, Japan
Masaomi Iyo
Affiliation:
Department of Psychiatry, Graduate School of Medicine, Chiba University, Chiba, Japan
Eiji Shimizu
Affiliation:
Research Center for Child Mental Development, Chiba University, Chiba, Japan United Graduate School of Child Development, Osaka University, Kanazawa University, Hamamatsu University School of Medicine, Chiba University and University of Fukui, Suita, Osaka, Japan Department of Molecular Imaging and Theranostics, National Institute of Radiological Sciences, National Institutes for Quantum and Radiological Science and Technology, Chiba, Japan Department of Cognitive Behavioral Physiology, Graduate School of Medicine, Chiba University, Chiba, Japan
Akiko Nakagawa
Affiliation:
Research Center for Child Mental Development, Chiba University, Chiba, Japan United Graduate School of Child Development, Osaka University, Kanazawa University, Hamamatsu University School of Medicine, Chiba University and University of Fukui, Suita, Osaka, Japan
*
Yoshiyuki Hirano, Research Center for Child Mental Development, Chiba University, 1-8-1 Inohana, Chuo-ku, Chiba 260-8670, Japan. Tel: +81-43-226-2975; Fax: +81-43-226-8588; E-mail: hirano@chiba-u.jp
Get access Rights & Permissions [Opens in a new window]

Abstract

Objective

To investigate the relationship between the severities of symptom dimensions in obsessive-compulsive disorder (OCD) and white matter alterations.

Methods

We applied tract-based spatial statistics for diffusion tensor imaging (DTI) acquired by 3T magnetic resonance imaging. First, we compared fractional anisotropy (FA) between 20 OCD patients and 30 healthy controls (HC). Then, applying whole brain analysis, we searched the brain regions showing correlations between the severities of symptom dimensions assessed by Obsessive-Compulsive Inventory-Revised and FA in all participants. Finally, we calculated the correlations between the six symptom dimensions and multiple DTI measures [FA, axial diffusivity (AD), radial diffusivity (RD), mean diffusivity (MD)] in a region-of-interest (ROI) analysis and explored the differences between OCD patients and HC.

Results

There were no between-group differences in FA or brain region correlations between the severities of symptom dimensions and FA in any of the participants. ROI analysis revealed negative correlations between checking severity and left inferior frontal gyrus white matter and left middle temporal gyrus white matter and a positive correlation between ordering severity and right precuneus in FA in OCD compared with HC. We also found negative correlations between ordering severity and right precuneus in RD, between obsessing severities and right supramarginal gyrus in AD and MD, and between hoarding severity and right insular gyrus in AD.

Conclusion

Our study supported the hypothesis that the severities of respective symptom dimensions are associated with different patterns of white matter alterations.

Keywords

diffusion tensor imagingfractional anisotropyobsessive-compulsive disorderobsessive-compulsive inventory-revisedsymptom dimensions
Type
Original Articles
Information
Acta Neuropsychiatrica , Volume 29 , Issue 3 , June 2017 , pp. 153 - 163
Check for updates
Copyright
© Scandinavian College of Neuropsychopharmacology 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1. Fullana, MA, Mataix-Cols, D, Caspi, A et al. Obsessions and compulsions in the community: prevalence, interference, help-seeking, developmental stability, and co-occurring psychiatric conditions. Am J Psychiatry 2009;166:329–336.CrossRefGoogle ScholarPubMed
2. Leonard, HL, Ale, CM, Freeman, JB, Garcia, AM, Ng, JS. Obsessive-compulsive disorder. Child Adolesc Psychiatr Clin N Am 2005;14:727–743.CrossRefGoogle ScholarPubMed
3. Michaud, CM, McKenna, MT, Begg, S et al. The burden of disease and injury in the United States 1996. Popul Health Metr 2006;4:11.CrossRefGoogle ScholarPubMed
4. Saxena, S. Neuroimaging and psychopathology of obsessive-compulsive disorder (OCD). In: Fu CHY, Senior C, Russell T, Weinberger DR, Murray R, editors. Neuroimaging in psychiatry. London, New York and Independence, KY: CRC Press, 2003, p. 191–224.Google Scholar
5. Del Casale, A, Kotzalidis, GD, Rapinesi, C et al. Functional neuroimaging in obsessive-compulsive disorder. Neuropsychobiology 2011;64:61–85.Google Scholar
6. Menzies, L, Chamberlain, SR, Laird, AR, Thelen, SM, Sahakian, BJ, Bullmore, ET. Integrating evidence from neuroimaging and neuropsychological studies of obsessive-compulsive disorder: the orbitofronto-striatal model revisited. Neurosci Biobehav Rev 2008;32:525–549.Google Scholar
7. Nishida, S, Narumoto, J, Sakai, Y et al. Anterior insular volume is larger in patients with obsessive-compulsive disorder. Prog Neuropsychopharmacol Biol Psychiatry 2011;35:997–1001.Google Scholar
8. Piras, F, Piras, F, Chiapponi, C, Girardi, P, Caltagirone, C, Spalletta, G. Widespread structural brain changes in OCD: a systematic review of voxel-based morphometry studies. Cortex J Devoted Study Nerv Syst Behav 2015;62C:89–108.Google Scholar
9. Song, A, Jung, WH, Jang, JH et al. Disproportionate alterations in the anterior and posterior insular cortices in obsessive-compulsive disorder. PLoS One 2011;6:e22361.CrossRefGoogle ScholarPubMed
10. Benedetti, F, Giacosa, C, Radaelli, D et al. Widespread changes of white matter microstructure in obsessive-compulsive disorder: effect of drug status. Eur Neuropsychopharmacol J Eur Coll Neuropsychopharmacol 2013;23:581–593.Google Scholar
11. Cannistraro, PA, Makris, N, Howard, JD et al. A diffusion tensor imaging study of white matter in obsessive-compulsive disorder. Depress Anxiety 2007;24:440–446.Google Scholar
12. Garibotto, V, Scifo, P, Gorini, A et al. Disorganization of anatomical connectivity in obsessive compulsive disorder: a multi-parameter diffusion tensor imaging study in a subpopulation of patients. Neurobiol Dis 2010;37:468–476.CrossRefGoogle Scholar
13. Ha, TH, Kang, D-H, Park, JS et al. White matter alterations in male patients with obsessive-compulsive disorder. Neuroreport 2009;20:735–739.Google Scholar
14. Nakamae, T, Narumoto, J, Shibata, K et al. Alteration of fractional anisotropy and apparent diffusion coefficient in obsessive-compulsive disorder: a diffusion tensor imaging study. Prog Neuropsychopharmacol Biol Psychiatry 2008;32:1221–1226.Google Scholar
15. Saito, Y, Nobuhara, K, Okugawa, G et al. Corpus callosum in patients with obsessive-compulsive disorder: diffusion-tensor imaging study. Radiology 2008;246:536–542.CrossRefGoogle ScholarPubMed
16. Szeszko, PR, Christian, C, Macmaster, F et al. Gray matter structural alterations in psychotropic drug-naive pediatric obsessive-compulsive disorder: an optimized voxel-based morphometry study. Am J Psychiatry 2008;165:1299–1307.Google Scholar
17. Yoo, SY, Jang, JH, Shin, Y-W et al. White matter abnormalities in drug-naïve patients with obsessive-compulsive disorder: a diffusion tensor study before and after citalopram treatment. Acta Psychiatr Scand 2007;116:211–219.CrossRefGoogle ScholarPubMed
18. Smith, SM, Jenkinson, M, Johansen-Berg, H et al. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 2006;31:1487–1505.CrossRefGoogle ScholarPubMed
19. Koch, K, Reess, TJ, Rus, OG, Zimmer, C, Zaudig, M. Diffusion tensor imaging (DTI) studies in patients with obsessive-compulsive disorder (OCD): a review. J Psychiatr Res 2014;54:26–35.CrossRefGoogle ScholarPubMed
20. Koch, K, Wagner, G, Schachtzabel, C et al. White matter structure and symptom dimensions in obsessive-compulsive disorder. J Psychiatr Res 2012;46:264–270.Google Scholar
21. Glahn, A, Prell, T, Grosskreutz, J, Peschel, T, Müller-Vahl, KR. Obsessive-compulsive disorder is a heterogeneous disorder: evidence from diffusion tensor imaging and magnetization transfer imaging. BMC Psychiatry 2015;15:135.Google Scholar
22. Foa, EB, Huppert, JD, Leiberg, S et al. The Obsessive-Compulsive Inventory: development and validation of a short version. Psychol Assess 2002;14:485–496.CrossRefGoogle ScholarPubMed
23. Hajcak, G, Huppert, JD, Simons, RF, Foa, EB. Psychometric properties of the OCI-R in a college sample. Behav Res Ther 2004;42:115–123.Google Scholar
24. Zermatten, A, Van der Linden, M, Larøi, F, Ceschi, G. Reality monitoring and motor memory in checking-prone individuals. J Anxiety Disord 2006;20:580–596.Google Scholar
25. Huppert, JD, Walther, MR, Hajcak, G et al. The OCI-R: validation of the subscales in a clinical sample. J Anxiety Disord 2007;21:394–406.Google Scholar
26. First, MB, Spitzer, RM, Gibbon, M, Williams, JBW. Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Patient Edition. (SCID-I/P). New York: Biometrics Research, New York State Psychiatric Institute, 2002.Google Scholar
27. Goodman, WK, Price, LH, Rasmussen, SA et al. The Yale-Brown Obsessive Compulsive Scale. I. Development, use, and reliability. Arch Gen Psychiatry 1989;46:1006–1011.CrossRefGoogle ScholarPubMed
28. Wechsler, D. WAIS-III: administration and scoring manual. New York: Harcourt Brace & Company, 1997.Google Scholar
29. Oldfield, RC. The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia 1971;9:97–113.Google Scholar
30. Sheehan, DV, Lecrubier, Y, Sheehan, KH et al. The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry 1998;59(Suppl. 20):22–33.Google Scholar
31. Wechsler, D.. WAIS-R manual: Wechsler Adult Intelligence Scale-revised. New York: Psychological Corporation, 1981.Google Scholar
32. Wakabayashi, A, Tojo, Y, Baron-Cohen, S, Wheelwright, S. The Autism-Spectrum Quotient (AQ) Japanese version: evidence from high-functioning clinical group and normal adults. Shinrigaku Kenkyu 2004;75:78–84.Google Scholar
33. Wakabayashi, A, Baron-Cohen, S, Wheelwright, S, Tojo, Y. The Autism-Spectrum Quotient (AQ) in Japan: a cross-cultural comparison. J Autism Dev Disord 2006;36:263–270.Google Scholar
34. Nichols, TE, Holmes, AP. Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 2002;15:1–25.Google Scholar
35. Bejerot, S, Nylander, L, Lindström, E. Autistic traits in obsessive-compulsive disorder. Nord J Psychiatry 2001;55:169–176.Google Scholar
36. Meier, SM, Petersen, L, Schendel, DE, Mattheisen, M, Mortensen, PB, Mors, O. Obsessive-compulsive disorder and autism spectrum disorders: longitudinal and offspring risk. PLoS One 2015;10:e0141703.CrossRefGoogle ScholarPubMed
37. Oishi, K, Faria, AV, van Zijl, PCM, Mori, S. MRI Atlas of human white matter, 2nd edn. Amsterdam and Boston, MA: Academic Press, 2010.Google Scholar
38. Forstmann, BU, Jahfari, S, Scholte, HS, Wolfensteller, U, van den Wildenberg, WPM, Ridderinkhof, KR. Function and structure of the right inferior frontal cortex predict individual differences in response inhibition: a model-based approach. J Neurosci 2008;28:9790–9796.CrossRefGoogle ScholarPubMed
39. van den Heuvel, OA, Remijnse, PL, Mataix-Cols, D et al. The major symptom dimensions of obsessive-compulsive disorder are mediated by partially distinct neural systems. Brain 2009;132:853–868.Google Scholar
40. Li, F, Huang, X, Tang, W et al. Multivariate pattern analysis of DTI reveals differential white matter in individuals with obsessive-compulsive disorder. Hum Brain Mapp 2014;35:2643–2651.Google Scholar
41. Isaacs, KL, Philbeck, JW, Barr, WB, Devinsky, O, Alper, K. Obsessive-compulsive symptoms in patients with temporal lobe epilepsy. Epilepsy Behav EB 2004;5:569–574.Google Scholar
42. Cavanna, AE, Trimble, MR. The precuneus: a review of its functional anatomy and behavioural correlates. Brain J Neurol 2006;129:564–583.Google Scholar
43. Song, S-K, Sun, S-W, Ramsbottom, MJ, Chang, C, Russell, J, Cross, AH. Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage 2002;17:1429–1436.Google Scholar
44. Li, F, Huang, X, Yang, Y et al. Microstructural brain abnormalities in patients with obsessive-compulsive disorder: diffusion-tensor MR imaging study at 3.0T. Radiology 2011;260:216–223.Google Scholar
45. Alexander, AL, Lee, JE, Lazar, M, Field, AS. Diffusion tensor imaging of the brain. Neurother J Am Soc Exp Neurother 2007;4:316–329.Google Scholar
46. Valente, AA, Miguel, EC, Castro, CC et al. Regional gray matter abnormalities in obsessive-compulsive disorder: a voxel-based morphometry study. Biol Psychiatry 2005;58:479–487.Google Scholar
47. Craig, ADB. How do you feel – now? The anterior insula and human awareness. Nat Rev Neurosci 2009;10:59–70.Google Scholar
48. Singer, T, Critchley, HD, Preuschoff, K. A common role of insula in feelings, empathy and uncertainty. Trends Cogn Sci 2009;13:334–340.CrossRefGoogle ScholarPubMed
49. Olatunji, BO, Ebesutani, C, Haidt, J, Sawchuk, CN. Specificity of disgust domains in the prediction of contamination anxiety and avoidance: a multimodal examination. Behav Ther 2014;45:469–481.Google Scholar
50. Williams, MT, Farris, SG, Turkheimer, EN et al. The impact of symptom dimensions on outcome for exposure and ritual prevention therapy in obsessive-compulsive disorder. J Anxiety Disord 2014;28:553–558.Google Scholar