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The Cerebellar Cognitive Affective/Schmahmann Syndrome Scale in Spinocerebellar Ataxias

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Abstract

The Cerebellar Cognitive Affective/Schmahmann Syndrome (CCAS) manifests as impaired executive control, linguistic processing, visual spatial function, and affect regulation. The CCAS has been described in the spinocerebellar ataxias (SCAs), but its prevalence is unknown. We analyzed results of the CCAS/Schmahmann Scale (CCAS-S), developed to detect and quantify CCAS, in two natural history studies of 309 individuals Symptomatic for SCA1, SCA2, SCA3, SCA6, SCA7, or SCA8, 26 individuals Pre-symptomatic for SCA1 or SCA3, and 37 Controls. We compared total raw scores, domain scores, and total fail scores between Symptomatic, Pre-symptomatic, and Control cohorts, and between SCA types. We calculated scale sensitivity and selectivity based on CCAS category designation among Symptomatic individuals and Controls, and correlated CCAS-S performance against age and education, and in Symptomatic patients, against genetic repeat length, onset age, disease duration, motor ataxia, depression, and fatigue. Definite CCAS was identified in 46% of the Symptomatic group. False positive rate among Controls was 5.4%. Symptomatic individuals had poorer global CCAS-S performance than Controls, accounting for age and education. The domains of semantic fluency, phonemic fluency, and category switching that tap executive function and linguistic processing consistently separated Symptomatic individuals from Controls. CCAS-S scores correlated most closely with motor ataxia. Controls were similar to Pre-symptomatic individuals whose nearness to symptom onset was unknown. The use of the CCAS-S identifies a high CCAS prevalence in a large cohort of SCA patients, underscoring the utility of the scale and the notion that the CCAS is the third cornerstone of clinical ataxiology.

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Data Availability

Primary data from the natural history studies (CRC-SCA and READISCA) are housed and curated at the Heath Informatics Institute (HII) at the University of South Florida. Data that serve as the basis for this analysis were downloaded to secure, password-protected Massachusetts General Hospital servers maintained in the Schmahmann Laboratory for Neuroanatomy and Cerebellar Neurobiology. Data are de-identified and available from the senior author upon reasonable request.

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Acknowledgements

We are grateful to the patients and families who participate in the natural history studies and the coordinators at the participating sites who administer these studies together with their site principal investigators. The assistance of Jason MacMore in this project is gratefully acknowledged.

Funding

Supported in part by the National Ataxia Foundation, the Gordon and Marilyn Macklin Foundation, the MINDlink Foundation, and the National Institute of Neurological Disorders and Stroke (NINDS) grant U01 NS104326 for the READISCA project (NCT03487367). L.P.S. was funded by an Australian-US Fulbright Commission scholarship.

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Authors and Affiliations

  1. Department of Neurology, Ataxia Center, Cognitive Behavioral Neurology Unit, Laboratory for Neuroanatomy and Cerebellar Neurobiology, Massachusetts General Hospital and Harvard Medical School, 100 Cambridge Street, Suite 2000, Boston, MA, 02114, USA

    Louisa P. Selvadurai & Jeremy D. Schmahmann

  2. Department of Neurology, University of California, Los Angeles, Los Angeles, CA, USA

    Susan L. Perlman

  3. Department of Neurology, Houston Methodist Research Institute, Houston, TX, USA

    Tetsuo Ashizawa

  4. Department of Neurology, Emory University School of Medicine, Atlanta, GA, USA

    George R. Wilmot

  5. Department of Psychiatry and Behavioral Sciences, Johns Hopkins School of Medicine, Baltimore, MD, USA

    Chiadi U. Onyike

  6. Department of Neurology, Johns Hopkins School of Medicine, Baltimore, MD, USA

    Liana S. Rosenthal

  7. Department of Neurology, University of Michigan, Ann Arbor, MI, USA

    Vikram G. Shakkottai & Henry L. Paulson

  8. Department of Neurology, University of Texas Southwestern Medical Center, Dallas, TX, USA

    Vikram G. Shakkottai

  9. Department of Neurology, McKnight Brain Institute, University of Florida College of Medicine, Gainesville, FL, USA

    Sub H. Subramony

  10. Department of Neurology, University of Minnesota, Minneapolis, MN, USA

    Khalaf O. Bushara

  11. Department of Neurology, Columbia University, New York, NY, USA

    Sheng-Han Kuo

  12. Department of Neurology, University of California, San Francisco, CA, USA

    Cameron Dietiker, Michael D. Geschwind & Alexandra B. Nelson

  13. Department of Neurology, University of Chicago, Chicago, IL, USA

    Christopher M. Gomez

  14. Department of Neurology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA

    Puneet Opal

  15. Department of Neurology, University of South Florida Ataxia Research Center, Tampa, FL, USA

    Theresa A. Zesiewicz

  16. Department of Neurology, University of Colorado Denver, Anschutz Medical Campus, Aurora, CO, USA

    Trevor Hawkins

  17. Department of Neurology, University of Alabama at Birmingham, Birmingham, Alabama, USA

    Talene A. Yacoubian

  18. Department of Psychiatry, University of Iowa Carver College of Medicine, Iowa City, IA, USA

    Peggy C. Nopoulos

  19. Department of Neurology and Neurological Sciences, Stanford University School of Medicine, Stanford, CA, USA

    Sharon J. Sha

  20. Department of Neurology, University of Rochester Medical Center, Rochester, NY, USA

    Peter E. Morrison

  21. Department of Neurology, University of Utah, Salt Lake City, UT, USA

    Karla P. Figueroa & Stefan M. Pulst

Authors
  1. Louisa P. Selvadurai
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  2. Susan L. Perlman
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  3. Tetsuo Ashizawa
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  4. George R. Wilmot
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  5. Chiadi U. Onyike
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  6. Liana S. Rosenthal
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  7. Vikram G. Shakkottai
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  8. Henry L. Paulson
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  18. Trevor Hawkins
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  19. Talene A. Yacoubian
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  20. Peggy C. Nopoulos
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  25. Jeremy D. Schmahmann
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Corresponding author

Correspondence to Jeremy D. Schmahmann.

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Ethics Approval

Approval was obtained for study procedures at all sites via the local IRB at each institution, and all participants gave informed consent. The central sites (UCLA for CRC-SCA and Houston Methodist for READISCA) prepared the original IRB documents that were used by all participating sites during their local reviews.

Conflict of Interest

L.P.S. was funded by an Australian-American Fulbright Commission scholarship.

C.U.O. receives research support from Alector Inc. and Transposon Inc., and consults for Acadia Pharmaceuticals. He is also supported by the Robert and Nancy Hall for Brain Research, and the Joseph Trovato Fund.

L.S.R. is site PI for Biohaven Pharma and has consulted for Bial Biotech and Reata Pharmaceuticals. She receives research support from NINDS, Pfizer, the National Ataxia Foundation, Gordon and Marilyn Macklin Foundation, and the Daniel B and Florence E. Green Foundation.

M.D.G is site PI for Biohaven Pharma, receives funding from the NIH/NIA (R01 AG AG031189; R01AG062562; R56 AG055619) and is supported by the Michael J. Homer Family Fund.

J.D.S. is site PI for Biohaven Pharma, consults for Biohaven, and holds the copyright with the General Hospital Corporation to the Brief Ataxia Rating scale, Patient Reported outcome Measure of Ataxia, the Cerebellar Cognitive Affective / Schmahmann Syndrome Scale, and the Cerebellar Neuropsychiatric Rating Scale.

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Selvadurai, L.P., Perlman, S.L., Ashizawa, T. et al. The Cerebellar Cognitive Affective/Schmahmann Syndrome Scale in Spinocerebellar Ataxias. Cerebellum (2024). https://doi.org/10.1007/s12311-023-01651-0

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