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October 15, 2019; 93 (16) Article

Pediatric postoperative cerebellar cognitive affective syndrome follows outflow pathway lesions

View ORCID ProfileFatimah M. Albazron, View ORCID ProfileJoel Bruss, Robin M. Jones, View ORCID ProfileTorunn I. Yock, View ORCID ProfileMargaret B. Pulsifer, View ORCID ProfileAlexander L. Cohen, View ORCID ProfilePeg C. Nopoulos, Annah N. Abrams, Mariko Sato, View ORCID ProfileAaron D. Boes
First published September 16, 2019, DOI: https://doi.org/10.1212/WNL.0000000000008326
Fatimah M. Albazron
From the Neuroimaging and Noninvasive Brain Stimulation Laboratory (F.M.A., J.B., A.D.B.), Departments of Pediatrics, Neurology, and Psychiatry, University of Iowa Hospitals and Clinics, Iowa City; Department of Pediatric Neurology (R.M.J.), Department of Radiation Oncology (T.I.Y.), Department of Psychiatry (M.B.P.), and Department of Child and Adolescent Psychiatry and Pediatric Hematology Oncology (A.N.A.), Massachusetts General Hospital; Department of Neurology (A.L.C.), Boston Children's Hospital, MA; Department of Psychiatry (P.C.N.), University of Iowa Hospitals and Clinics, Iowa City; and Department of Pediatric Hematology Oncology (M.S.), Stead Family Children's Hospital, Iowa City, IA.
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Joel Bruss
From the Neuroimaging and Noninvasive Brain Stimulation Laboratory (F.M.A., J.B., A.D.B.), Departments of Pediatrics, Neurology, and Psychiatry, University of Iowa Hospitals and Clinics, Iowa City; Department of Pediatric Neurology (R.M.J.), Department of Radiation Oncology (T.I.Y.), Department of Psychiatry (M.B.P.), and Department of Child and Adolescent Psychiatry and Pediatric Hematology Oncology (A.N.A.), Massachusetts General Hospital; Department of Neurology (A.L.C.), Boston Children's Hospital, MA; Department of Psychiatry (P.C.N.), University of Iowa Hospitals and Clinics, Iowa City; and Department of Pediatric Hematology Oncology (M.S.), Stead Family Children's Hospital, Iowa City, IA.
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Robin M. Jones
From the Neuroimaging and Noninvasive Brain Stimulation Laboratory (F.M.A., J.B., A.D.B.), Departments of Pediatrics, Neurology, and Psychiatry, University of Iowa Hospitals and Clinics, Iowa City; Department of Pediatric Neurology (R.M.J.), Department of Radiation Oncology (T.I.Y.), Department of Psychiatry (M.B.P.), and Department of Child and Adolescent Psychiatry and Pediatric Hematology Oncology (A.N.A.), Massachusetts General Hospital; Department of Neurology (A.L.C.), Boston Children's Hospital, MA; Department of Psychiatry (P.C.N.), University of Iowa Hospitals and Clinics, Iowa City; and Department of Pediatric Hematology Oncology (M.S.), Stead Family Children's Hospital, Iowa City, IA.
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Torunn I. Yock
From the Neuroimaging and Noninvasive Brain Stimulation Laboratory (F.M.A., J.B., A.D.B.), Departments of Pediatrics, Neurology, and Psychiatry, University of Iowa Hospitals and Clinics, Iowa City; Department of Pediatric Neurology (R.M.J.), Department of Radiation Oncology (T.I.Y.), Department of Psychiatry (M.B.P.), and Department of Child and Adolescent Psychiatry and Pediatric Hematology Oncology (A.N.A.), Massachusetts General Hospital; Department of Neurology (A.L.C.), Boston Children's Hospital, MA; Department of Psychiatry (P.C.N.), University of Iowa Hospitals and Clinics, Iowa City; and Department of Pediatric Hematology Oncology (M.S.), Stead Family Children's Hospital, Iowa City, IA.
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Margaret B. Pulsifer
From the Neuroimaging and Noninvasive Brain Stimulation Laboratory (F.M.A., J.B., A.D.B.), Departments of Pediatrics, Neurology, and Psychiatry, University of Iowa Hospitals and Clinics, Iowa City; Department of Pediatric Neurology (R.M.J.), Department of Radiation Oncology (T.I.Y.), Department of Psychiatry (M.B.P.), and Department of Child and Adolescent Psychiatry and Pediatric Hematology Oncology (A.N.A.), Massachusetts General Hospital; Department of Neurology (A.L.C.), Boston Children's Hospital, MA; Department of Psychiatry (P.C.N.), University of Iowa Hospitals and Clinics, Iowa City; and Department of Pediatric Hematology Oncology (M.S.), Stead Family Children's Hospital, Iowa City, IA.
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Alexander L. Cohen
From the Neuroimaging and Noninvasive Brain Stimulation Laboratory (F.M.A., J.B., A.D.B.), Departments of Pediatrics, Neurology, and Psychiatry, University of Iowa Hospitals and Clinics, Iowa City; Department of Pediatric Neurology (R.M.J.), Department of Radiation Oncology (T.I.Y.), Department of Psychiatry (M.B.P.), and Department of Child and Adolescent Psychiatry and Pediatric Hematology Oncology (A.N.A.), Massachusetts General Hospital; Department of Neurology (A.L.C.), Boston Children's Hospital, MA; Department of Psychiatry (P.C.N.), University of Iowa Hospitals and Clinics, Iowa City; and Department of Pediatric Hematology Oncology (M.S.), Stead Family Children's Hospital, Iowa City, IA.
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Peg C. Nopoulos
From the Neuroimaging and Noninvasive Brain Stimulation Laboratory (F.M.A., J.B., A.D.B.), Departments of Pediatrics, Neurology, and Psychiatry, University of Iowa Hospitals and Clinics, Iowa City; Department of Pediatric Neurology (R.M.J.), Department of Radiation Oncology (T.I.Y.), Department of Psychiatry (M.B.P.), and Department of Child and Adolescent Psychiatry and Pediatric Hematology Oncology (A.N.A.), Massachusetts General Hospital; Department of Neurology (A.L.C.), Boston Children's Hospital, MA; Department of Psychiatry (P.C.N.), University of Iowa Hospitals and Clinics, Iowa City; and Department of Pediatric Hematology Oncology (M.S.), Stead Family Children's Hospital, Iowa City, IA.
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Annah N. Abrams
From the Neuroimaging and Noninvasive Brain Stimulation Laboratory (F.M.A., J.B., A.D.B.), Departments of Pediatrics, Neurology, and Psychiatry, University of Iowa Hospitals and Clinics, Iowa City; Department of Pediatric Neurology (R.M.J.), Department of Radiation Oncology (T.I.Y.), Department of Psychiatry (M.B.P.), and Department of Child and Adolescent Psychiatry and Pediatric Hematology Oncology (A.N.A.), Massachusetts General Hospital; Department of Neurology (A.L.C.), Boston Children's Hospital, MA; Department of Psychiatry (P.C.N.), University of Iowa Hospitals and Clinics, Iowa City; and Department of Pediatric Hematology Oncology (M.S.), Stead Family Children's Hospital, Iowa City, IA.
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Mariko Sato
From the Neuroimaging and Noninvasive Brain Stimulation Laboratory (F.M.A., J.B., A.D.B.), Departments of Pediatrics, Neurology, and Psychiatry, University of Iowa Hospitals and Clinics, Iowa City; Department of Pediatric Neurology (R.M.J.), Department of Radiation Oncology (T.I.Y.), Department of Psychiatry (M.B.P.), and Department of Child and Adolescent Psychiatry and Pediatric Hematology Oncology (A.N.A.), Massachusetts General Hospital; Department of Neurology (A.L.C.), Boston Children's Hospital, MA; Department of Psychiatry (P.C.N.), University of Iowa Hospitals and Clinics, Iowa City; and Department of Pediatric Hematology Oncology (M.S.), Stead Family Children's Hospital, Iowa City, IA.
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Aaron D. Boes
From the Neuroimaging and Noninvasive Brain Stimulation Laboratory (F.M.A., J.B., A.D.B.), Departments of Pediatrics, Neurology, and Psychiatry, University of Iowa Hospitals and Clinics, Iowa City; Department of Pediatric Neurology (R.M.J.), Department of Radiation Oncology (T.I.Y.), Department of Psychiatry (M.B.P.), and Department of Child and Adolescent Psychiatry and Pediatric Hematology Oncology (A.N.A.), Massachusetts General Hospital; Department of Neurology (A.L.C.), Boston Children's Hospital, MA; Department of Psychiatry (P.C.N.), University of Iowa Hospitals and Clinics, Iowa City; and Department of Pediatric Hematology Oncology (M.S.), Stead Family Children's Hospital, Iowa City, IA.
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Citation
Pediatric postoperative cerebellar cognitive affective syndrome follows outflow pathway lesions
Fatimah M. Albazron, Joel Bruss, Robin M. Jones, Torunn I. Yock, Margaret B. Pulsifer, Alexander L. Cohen, Peg C. Nopoulos, Annah N. Abrams, Mariko Sato, Aaron D. Boes
Neurology Oct 2019, 93 (16) e1561-e1571; DOI: 10.1212/WNL.0000000000008326

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Abstract

Objective To evaluate lesion location after pediatric cerebellar tumor resection in relation to the development of severe cognitive and affective disturbances, or cerebellar cognitive affective syndrome (CCAS).

Methods The postsurgical lesion location of 195 pediatric patients with cerebellar tumors was mapped onto a template brain. Individuals with CCAS were matched to 2 participants without CCAS by sex, age, and lesion volume. Lesion analyses included both a hypothesis-driven evaluation of the cerebellar outflow pathway (deep nuclei and superior cerebellar peduncles) and data-driven multivariate lesion symptom mapping. Lesion-associated networks were evaluated by comparing connectivity patterns between the lesion location of cases with and those without CCAS with resting-state functional connectivity MRI data from large normative adult and pediatric cohorts.

Results CCAS was present in 48 of 195 participants (24.6%) and was strongly associated with cerebellar outflow tract lesions (p < 0.0001). Lesion symptom mapping also highlighted the cerebellar outflow pathway, with peak findings in the fastigial nuclei extending into the inferior vermis. Lesion network mapping revealed that the cerebellar region most associated with CCAS was functionally connected to the thalamic mediodorsal nucleus, among other sites, and that higher connectivity between lesion location and the mediodorsal nucleus predicts CCAS occurrence (p < 0.01). A secondary analysis of 27 participants with mutism revealed similar localization of lesions and lesion-associated networks.

Conclusion Lesions of the cerebellar outflow pathway and inferior vermis are associated with major cognitive and affective disturbances after pediatric cerebellar tumor resection, and disrupted communication between the cerebellum and the thalamic mediodorsal nucleus may be important.

Glossary

CCAS=
cerebellar cognitive affective syndrome;
CMS=
cerebellar mutism syndrome;
MNI=
Montreal Neurological Institute;
ROI=
region of interest;
rs-fcMRI=
resting-state functional connectivity MRI

Footnotes

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Editorial, page 693

  • Received December 28, 2018.
  • Accepted in final form June 17, 2019.
  • © 2019 American Academy of Neurology
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