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April 13, 2021; 96 (15) Article

Olfactory Testing in Parkinson Disease and REM Behavior Disorder

A Machine Learning Approach

View ORCID ProfileChristine Lo, Siddharth Arora, View ORCID ProfileYoav Ben-Shlomo, View ORCID ProfileThomas R. Barber, View ORCID ProfileMichael Lawton, View ORCID ProfileJohannes C. Klein, Sofia Kanavou, Annette Janzen, Elisabeth Sittig, View ORCID ProfileWolfgang H. Oertel, Donald G. Grosset, View ORCID ProfileMichele T. Hu
First published February 24, 2021, DOI: https://doi.org/10.1212/WNL.0000000000011743
Christine Lo
From the Oxford Parkinson's Disease Centre (C.L., S.A., T.R.B., J.C.K., M.T.H.), Nuffield Department of Clinical Neurosciences (C.L., T.R.B., J.C.K., M.T.H.), and Saïd Business School (S.A.), University of Oxford; Population Health Sciences (Y.B.-S., M.L., S.K.), University of Bristol, UK; Department of Neurology (A.J., E.S., W.H.O.), Philipps University Marburg; Institute for Neurogenomics (W.H.O.), München Helmholtz Center for Health and Environment, Neuherberg München, Germany; and Institute of Neurological Sciences (D.G.G.), Queen Elizabeth University Hospital, Glasgow, UK.
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Siddharth Arora
From the Oxford Parkinson's Disease Centre (C.L., S.A., T.R.B., J.C.K., M.T.H.), Nuffield Department of Clinical Neurosciences (C.L., T.R.B., J.C.K., M.T.H.), and Saïd Business School (S.A.), University of Oxford; Population Health Sciences (Y.B.-S., M.L., S.K.), University of Bristol, UK; Department of Neurology (A.J., E.S., W.H.O.), Philipps University Marburg; Institute for Neurogenomics (W.H.O.), München Helmholtz Center for Health and Environment, Neuherberg München, Germany; and Institute of Neurological Sciences (D.G.G.), Queen Elizabeth University Hospital, Glasgow, UK.
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Yoav Ben-Shlomo
From the Oxford Parkinson's Disease Centre (C.L., S.A., T.R.B., J.C.K., M.T.H.), Nuffield Department of Clinical Neurosciences (C.L., T.R.B., J.C.K., M.T.H.), and Saïd Business School (S.A.), University of Oxford; Population Health Sciences (Y.B.-S., M.L., S.K.), University of Bristol, UK; Department of Neurology (A.J., E.S., W.H.O.), Philipps University Marburg; Institute for Neurogenomics (W.H.O.), München Helmholtz Center for Health and Environment, Neuherberg München, Germany; and Institute of Neurological Sciences (D.G.G.), Queen Elizabeth University Hospital, Glasgow, UK.
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Thomas R. Barber
From the Oxford Parkinson's Disease Centre (C.L., S.A., T.R.B., J.C.K., M.T.H.), Nuffield Department of Clinical Neurosciences (C.L., T.R.B., J.C.K., M.T.H.), and Saïd Business School (S.A.), University of Oxford; Population Health Sciences (Y.B.-S., M.L., S.K.), University of Bristol, UK; Department of Neurology (A.J., E.S., W.H.O.), Philipps University Marburg; Institute for Neurogenomics (W.H.O.), München Helmholtz Center for Health and Environment, Neuherberg München, Germany; and Institute of Neurological Sciences (D.G.G.), Queen Elizabeth University Hospital, Glasgow, UK.
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Michael Lawton
From the Oxford Parkinson's Disease Centre (C.L., S.A., T.R.B., J.C.K., M.T.H.), Nuffield Department of Clinical Neurosciences (C.L., T.R.B., J.C.K., M.T.H.), and Saïd Business School (S.A.), University of Oxford; Population Health Sciences (Y.B.-S., M.L., S.K.), University of Bristol, UK; Department of Neurology (A.J., E.S., W.H.O.), Philipps University Marburg; Institute for Neurogenomics (W.H.O.), München Helmholtz Center for Health and Environment, Neuherberg München, Germany; and Institute of Neurological Sciences (D.G.G.), Queen Elizabeth University Hospital, Glasgow, UK.
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Johannes C. Klein
From the Oxford Parkinson's Disease Centre (C.L., S.A., T.R.B., J.C.K., M.T.H.), Nuffield Department of Clinical Neurosciences (C.L., T.R.B., J.C.K., M.T.H.), and Saïd Business School (S.A.), University of Oxford; Population Health Sciences (Y.B.-S., M.L., S.K.), University of Bristol, UK; Department of Neurology (A.J., E.S., W.H.O.), Philipps University Marburg; Institute for Neurogenomics (W.H.O.), München Helmholtz Center for Health and Environment, Neuherberg München, Germany; and Institute of Neurological Sciences (D.G.G.), Queen Elizabeth University Hospital, Glasgow, UK.
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Sofia Kanavou
From the Oxford Parkinson's Disease Centre (C.L., S.A., T.R.B., J.C.K., M.T.H.), Nuffield Department of Clinical Neurosciences (C.L., T.R.B., J.C.K., M.T.H.), and Saïd Business School (S.A.), University of Oxford; Population Health Sciences (Y.B.-S., M.L., S.K.), University of Bristol, UK; Department of Neurology (A.J., E.S., W.H.O.), Philipps University Marburg; Institute for Neurogenomics (W.H.O.), München Helmholtz Center for Health and Environment, Neuherberg München, Germany; and Institute of Neurological Sciences (D.G.G.), Queen Elizabeth University Hospital, Glasgow, UK.
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Annette Janzen
From the Oxford Parkinson's Disease Centre (C.L., S.A., T.R.B., J.C.K., M.T.H.), Nuffield Department of Clinical Neurosciences (C.L., T.R.B., J.C.K., M.T.H.), and Saïd Business School (S.A.), University of Oxford; Population Health Sciences (Y.B.-S., M.L., S.K.), University of Bristol, UK; Department of Neurology (A.J., E.S., W.H.O.), Philipps University Marburg; Institute for Neurogenomics (W.H.O.), München Helmholtz Center for Health and Environment, Neuherberg München, Germany; and Institute of Neurological Sciences (D.G.G.), Queen Elizabeth University Hospital, Glasgow, UK.
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Elisabeth Sittig
From the Oxford Parkinson's Disease Centre (C.L., S.A., T.R.B., J.C.K., M.T.H.), Nuffield Department of Clinical Neurosciences (C.L., T.R.B., J.C.K., M.T.H.), and Saïd Business School (S.A.), University of Oxford; Population Health Sciences (Y.B.-S., M.L., S.K.), University of Bristol, UK; Department of Neurology (A.J., E.S., W.H.O.), Philipps University Marburg; Institute for Neurogenomics (W.H.O.), München Helmholtz Center for Health and Environment, Neuherberg München, Germany; and Institute of Neurological Sciences (D.G.G.), Queen Elizabeth University Hospital, Glasgow, UK.
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Wolfgang H. Oertel
From the Oxford Parkinson's Disease Centre (C.L., S.A., T.R.B., J.C.K., M.T.H.), Nuffield Department of Clinical Neurosciences (C.L., T.R.B., J.C.K., M.T.H.), and Saïd Business School (S.A.), University of Oxford; Population Health Sciences (Y.B.-S., M.L., S.K.), University of Bristol, UK; Department of Neurology (A.J., E.S., W.H.O.), Philipps University Marburg; Institute for Neurogenomics (W.H.O.), München Helmholtz Center for Health and Environment, Neuherberg München, Germany; and Institute of Neurological Sciences (D.G.G.), Queen Elizabeth University Hospital, Glasgow, UK.
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Donald G. Grosset
From the Oxford Parkinson's Disease Centre (C.L., S.A., T.R.B., J.C.K., M.T.H.), Nuffield Department of Clinical Neurosciences (C.L., T.R.B., J.C.K., M.T.H.), and Saïd Business School (S.A.), University of Oxford; Population Health Sciences (Y.B.-S., M.L., S.K.), University of Bristol, UK; Department of Neurology (A.J., E.S., W.H.O.), Philipps University Marburg; Institute for Neurogenomics (W.H.O.), München Helmholtz Center for Health and Environment, Neuherberg München, Germany; and Institute of Neurological Sciences (D.G.G.), Queen Elizabeth University Hospital, Glasgow, UK.
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Michele T. Hu
From the Oxford Parkinson's Disease Centre (C.L., S.A., T.R.B., J.C.K., M.T.H.), Nuffield Department of Clinical Neurosciences (C.L., T.R.B., J.C.K., M.T.H.), and Saïd Business School (S.A.), University of Oxford; Population Health Sciences (Y.B.-S., M.L., S.K.), University of Bristol, UK; Department of Neurology (A.J., E.S., W.H.O.), Philipps University Marburg; Institute for Neurogenomics (W.H.O.), München Helmholtz Center for Health and Environment, Neuherberg München, Germany; and Institute of Neurological Sciences (D.G.G.), Queen Elizabeth University Hospital, Glasgow, UK.
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Citation
Olfactory Testing in Parkinson Disease and REM Behavior Disorder
A Machine Learning Approach
Christine Lo, Siddharth Arora, Yoav Ben-Shlomo, Thomas R. Barber, Michael Lawton, Johannes C. Klein, Sofia Kanavou, Annette Janzen, Elisabeth Sittig, Wolfgang H. Oertel, Donald G. Grosset, Michele T. Hu
Neurology Apr 2021, 96 (15) e2016-e2027; DOI: 10.1212/WNL.0000000000011743

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Abstract

Objective We sought to identify an abbreviated test of impaired olfaction amenable for use in busy clinical environments in prodromal (isolated REM sleep behavior disorder [iRBD]) and manifest Parkinson disease (PD).

Methods Eight hundred ninety individuals with PD and 313 controls in the Discovery cohort study underwent Sniffin’ Stick odor identification assessment. Random forests were initially trained to distinguish individuals with poor (functional anosmia/hyposmia) and good (normosmia/super-smeller) smell ability using all 16 Sniffin’ Sticks. Models were retrained using the top 3 sticks ranked by order of predictor importance. One randomly selected 3-stick model was tested in a second independent PD dataset (n = 452) and in 2 iRBD datasets (Discovery n = 241, Marburg n = 37) before being compared to previously described abbreviated Sniffin’ Stick combinations.

Results In differentiating poor from good smell ability, the overall area under the curve (AUC) value associated with the top 3 sticks (anise/licorice/banana) was 0.95 in the Development dataset (sensitivity 90%, specificity 92%, positive predictive value 92%, negative predictive value 90%). Internal and external validation confirmed AUCs ≥0.90. The combination of the 3-stick model determined poor smell, and an RBD screening questionnaire score of ≥5 separated those with iRBD from controls with a sensitivity, specificity, positive predictive value, and negative predictive value of 65%, 100%, 100%, and 30%.

Conclusions Our 3-Sniffin’-Stick model holds potential utility as a brief screening test in the stratification of individuals with PD and iRBD according to olfactory dysfunction.

Classification of Evidence This study provides Class III evidence that a 3-Sniffin’-Stick model distinguishes individuals with poor and good smell ability and can be used to screen for individuals with iRBD.

Glossary

AUC=
area under the curve;
iRBD=
isolated REM sleep behavior disorder;
MLA=
machine learning algorithm;
NPV=
negative predictive value;
PD=
Parkinson disease;
PPV=
positive predictive value;
RBDSQ=
REM Sleep Behavior Disorder Screening Questionnaire

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.

  • Class of Evidence: NPub.org/coe

  • Received April 15, 2020.
  • Accepted in final form January 15, 2021.
  • © 2021 American Academy of Neurology
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