Neuroanatomical characteristics associated with response to dorsal anterior cingulotomy for obsessive-compulsive disorder

Garrett P. Banks, Charles B. Mikell, Brett E. Youngerman, Bryan Henriques, Kathleen M. Kelly, Andrew K. Chan, Diana Herrera, Darin D. Dougherty, Emad N. Eskandar, Sameer A. Sheth

Research output: Contribution to journalArticle

22 Citations (Scopus)

Abstract

IMPORTANCE Approximately 10% of patients with obsessive-compulsive disorder (OCD) have symptoms that are refractory to pharmacologic and cognitive-behavioral therapies. Neurosurgical interventions can be effective therapeutic options in these patients, but not all individuals respond. The mechanisms underlying this response variability are poorly understood. OBJECTIVE To identify neuroanatomical characteristics on preoperative imaging that differentiate responders from nonresponders to dorsal anterior cingulotomy, a neurosurgical lesion procedure used to treat refractory OCD. DESIGN, SETTING, AND PARTICIPANTS We retrospectively analyzed preoperative T1 and diffusion magnetic resonance imaging sequences from 15 patients (9 men and 6 women) who underwent dorsal anterior cingulotomy. Eight of the 15 patients (53%) responded to the procedure. MAIN OUTCOMES AND MEASURES We used voxel-based morphometry (VBM) and diffusion tensor imaging to identify structural and connectivity variations that could differentiate eventual responders from nonresponders. The VBM and probabilistic tractographymetrics were correlated with clinical response to the cingulotomy procedure as measured by changes in the Yale-Brown Obsessive Compulsive Scale score. RESULTS Voxel-based morphometry analysis revealed a gray matter cluster in the right anterior cingulate cortex, anterior to the eventual lesion, for which signal strength correlated with poor response (P = .017). Decreased gray matter in this region of the dorsal anterior cingulate cortex predicted improved response (mean [SD] gray matter partial volume for responders vs nonresponders, 0.47 [0.03] vs 0.66 [0.03]; corresponding to mean Yale-Brown Obsessive Compulsive Scale score change, -60%[19] vs -11% [9], respectively). Hemispheric asymmetry in connectivity between the eventual lesion and the caudate (for responders vs nonresponders, mean [SD] group laterality for individual lesion seeds, -0.79 [0.18] vs -0.08 [0.65]; P = .04), putamen (-0.55 [0.35] vs 0.50 [0.33]; P = .001), thalamus (-0.82 [0.19] vs 0.41 [0.24]; P = .001), pallidum (-0.78 [0.18] vs 0.43 [0.48]; P = .001), and hippocampus (-0.66 [0.33] vs 0.33 [0.18]; P = .001) also correlated significantly with clinical response, with increased right-sided connectivity predicting greater response. CONCLUSIONS AND RELEVANCE We identified features of anterior cingulate cortex structure and connectivity that predict clinical response to dorsal anterior cingulotomy for refractory OCD. These results suggest that the variability seen in individual responses to a highly consistent, stereotyped procedure may be due to neuroanatomical variation in the patients. Furthermore, these variations may allow us to predict which patients are most likely to respond to cingulotomy, thereby refining our ability to individualize this treatment for refractory psychiatric disorders.

Original languageEnglish (US)
Pages (from-to)127-135
Number of pages9
JournalJAMA Psychiatry
Volume72
Issue number2
DOIs
StatePublished - Jan 1 2015
Externally publishedYes

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Obsessive-Compulsive Disorder
Gyrus Cinguli
Neurosurgical Procedures
Diffusion Magnetic Resonance Imaging
Globus Pallidus
Diffusion Tensor Imaging
Aptitude
Putamen
Cognitive Therapy
Thalamus
Psychiatry
Hippocampus
Seeds
Therapeutics
Gray Matter

ASJC Scopus subject areas

  • Psychiatry and Mental health

Cite this

Banks, G. P., Mikell, C. B., Youngerman, B. E., Henriques, B., Kelly, K. M., Chan, A. K., ... Sheth, S. A. (2015). Neuroanatomical characteristics associated with response to dorsal anterior cingulotomy for obsessive-compulsive disorder. JAMA Psychiatry, 72(2), 127-135. https://doi.org/10.1001/jamapsychiatry.2014.2216

Neuroanatomical characteristics associated with response to dorsal anterior cingulotomy for obsessive-compulsive disorder. / Banks, Garrett P.; Mikell, Charles B.; Youngerman, Brett E.; Henriques, Bryan; Kelly, Kathleen M.; Chan, Andrew K.; Herrera, Diana; Dougherty, Darin D.; Eskandar, Emad N.; Sheth, Sameer A.

In: JAMA Psychiatry, Vol. 72, No. 2, 01.01.2015, p. 127-135.

Research output: Contribution to journalArticle

Banks, GP, Mikell, CB, Youngerman, BE, Henriques, B, Kelly, KM, Chan, AK, Herrera, D, Dougherty, DD, Eskandar, EN & Sheth, SA 2015, 'Neuroanatomical characteristics associated with response to dorsal anterior cingulotomy for obsessive-compulsive disorder', JAMA Psychiatry, vol. 72, no. 2, pp. 127-135. https://doi.org/10.1001/jamapsychiatry.2014.2216
Banks, Garrett P. ; Mikell, Charles B. ; Youngerman, Brett E. ; Henriques, Bryan ; Kelly, Kathleen M. ; Chan, Andrew K. ; Herrera, Diana ; Dougherty, Darin D. ; Eskandar, Emad N. ; Sheth, Sameer A. / Neuroanatomical characteristics associated with response to dorsal anterior cingulotomy for obsessive-compulsive disorder. In: JAMA Psychiatry. 2015 ; Vol. 72, No. 2. pp. 127-135.
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T1 - Neuroanatomical characteristics associated with response to dorsal anterior cingulotomy for obsessive-compulsive disorder

AU - Banks, Garrett P.

AU - Mikell, Charles B.

AU - Youngerman, Brett E.

AU - Henriques, Bryan

AU - Kelly, Kathleen M.

AU - Chan, Andrew K.

AU - Herrera, Diana

AU - Dougherty, Darin D.

AU - Eskandar, Emad N.

AU - Sheth, Sameer A.

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N2 - IMPORTANCE Approximately 10% of patients with obsessive-compulsive disorder (OCD) have symptoms that are refractory to pharmacologic and cognitive-behavioral therapies. Neurosurgical interventions can be effective therapeutic options in these patients, but not all individuals respond. The mechanisms underlying this response variability are poorly understood. OBJECTIVE To identify neuroanatomical characteristics on preoperative imaging that differentiate responders from nonresponders to dorsal anterior cingulotomy, a neurosurgical lesion procedure used to treat refractory OCD. DESIGN, SETTING, AND PARTICIPANTS We retrospectively analyzed preoperative T1 and diffusion magnetic resonance imaging sequences from 15 patients (9 men and 6 women) who underwent dorsal anterior cingulotomy. Eight of the 15 patients (53%) responded to the procedure. MAIN OUTCOMES AND MEASURES We used voxel-based morphometry (VBM) and diffusion tensor imaging to identify structural and connectivity variations that could differentiate eventual responders from nonresponders. The VBM and probabilistic tractographymetrics were correlated with clinical response to the cingulotomy procedure as measured by changes in the Yale-Brown Obsessive Compulsive Scale score. RESULTS Voxel-based morphometry analysis revealed a gray matter cluster in the right anterior cingulate cortex, anterior to the eventual lesion, for which signal strength correlated with poor response (P = .017). Decreased gray matter in this region of the dorsal anterior cingulate cortex predicted improved response (mean [SD] gray matter partial volume for responders vs nonresponders, 0.47 [0.03] vs 0.66 [0.03]; corresponding to mean Yale-Brown Obsessive Compulsive Scale score change, -60%[19] vs -11% [9], respectively). Hemispheric asymmetry in connectivity between the eventual lesion and the caudate (for responders vs nonresponders, mean [SD] group laterality for individual lesion seeds, -0.79 [0.18] vs -0.08 [0.65]; P = .04), putamen (-0.55 [0.35] vs 0.50 [0.33]; P = .001), thalamus (-0.82 [0.19] vs 0.41 [0.24]; P = .001), pallidum (-0.78 [0.18] vs 0.43 [0.48]; P = .001), and hippocampus (-0.66 [0.33] vs 0.33 [0.18]; P = .001) also correlated significantly with clinical response, with increased right-sided connectivity predicting greater response. CONCLUSIONS AND RELEVANCE We identified features of anterior cingulate cortex structure and connectivity that predict clinical response to dorsal anterior cingulotomy for refractory OCD. These results suggest that the variability seen in individual responses to a highly consistent, stereotyped procedure may be due to neuroanatomical variation in the patients. Furthermore, these variations may allow us to predict which patients are most likely to respond to cingulotomy, thereby refining our ability to individualize this treatment for refractory psychiatric disorders.

AB - IMPORTANCE Approximately 10% of patients with obsessive-compulsive disorder (OCD) have symptoms that are refractory to pharmacologic and cognitive-behavioral therapies. Neurosurgical interventions can be effective therapeutic options in these patients, but not all individuals respond. The mechanisms underlying this response variability are poorly understood. OBJECTIVE To identify neuroanatomical characteristics on preoperative imaging that differentiate responders from nonresponders to dorsal anterior cingulotomy, a neurosurgical lesion procedure used to treat refractory OCD. DESIGN, SETTING, AND PARTICIPANTS We retrospectively analyzed preoperative T1 and diffusion magnetic resonance imaging sequences from 15 patients (9 men and 6 women) who underwent dorsal anterior cingulotomy. Eight of the 15 patients (53%) responded to the procedure. MAIN OUTCOMES AND MEASURES We used voxel-based morphometry (VBM) and diffusion tensor imaging to identify structural and connectivity variations that could differentiate eventual responders from nonresponders. The VBM and probabilistic tractographymetrics were correlated with clinical response to the cingulotomy procedure as measured by changes in the Yale-Brown Obsessive Compulsive Scale score. RESULTS Voxel-based morphometry analysis revealed a gray matter cluster in the right anterior cingulate cortex, anterior to the eventual lesion, for which signal strength correlated with poor response (P = .017). Decreased gray matter in this region of the dorsal anterior cingulate cortex predicted improved response (mean [SD] gray matter partial volume for responders vs nonresponders, 0.47 [0.03] vs 0.66 [0.03]; corresponding to mean Yale-Brown Obsessive Compulsive Scale score change, -60%[19] vs -11% [9], respectively). Hemispheric asymmetry in connectivity between the eventual lesion and the caudate (for responders vs nonresponders, mean [SD] group laterality for individual lesion seeds, -0.79 [0.18] vs -0.08 [0.65]; P = .04), putamen (-0.55 [0.35] vs 0.50 [0.33]; P = .001), thalamus (-0.82 [0.19] vs 0.41 [0.24]; P = .001), pallidum (-0.78 [0.18] vs 0.43 [0.48]; P = .001), and hippocampus (-0.66 [0.33] vs 0.33 [0.18]; P = .001) also correlated significantly with clinical response, with increased right-sided connectivity predicting greater response. CONCLUSIONS AND RELEVANCE We identified features of anterior cingulate cortex structure and connectivity that predict clinical response to dorsal anterior cingulotomy for refractory OCD. These results suggest that the variability seen in individual responses to a highly consistent, stereotyped procedure may be due to neuroanatomical variation in the patients. Furthermore, these variations may allow us to predict which patients are most likely to respond to cingulotomy, thereby refining our ability to individualize this treatment for refractory psychiatric disorders.

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