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May 07, 2019; 92 (19) Article

Higher probability of prodromal Parkinson disease is related to lower cognitive performance

View ORCID ProfileAnastasia Bougea, Maria I. Maraki, View ORCID ProfileMary Yannakoulia, Maria Stamelou, Georgia Xiromerisiou, Mary H. Kosmidis, Eva Ntanasi, Efthimios Dardiotis, View ORCID ProfileGeorgios M. Hadjigeorgiou, Paraskevi Sakka, Costas A. Anastasiou, Leonidas Stefanis, Nikolaos Scarmeas
First published April 3, 2019, DOI: https://doi.org/10.1212/WNL.0000000000007453
Anastasia Bougea
From the 1st Department of Neurology (A.B., E.N., C.A.A., L.S., N.S.), Aiginition Hospital, National and Kapodistrian, University of Athens Medical School; Department of Nutrition and Dietetics (M.I.M., M.Y., E.N., C.A.A.), Harokopio University; Parkinson's Disease and Movement Disorders Department (M.S.), Hygeia Hospital, Athens, Greece; Department of Neurology (M.S.), Philipps University, Marburg, Germany; School of Medicine (G.X., E.D., G.M.H.), University of Thessaly, Larissa; Laboratory of Cognitive Neuroscience, School of Psychology (M.H.K.), Aristotle University of Thessaloniki, Greece; Department of Neurology (G.M.H.), Medical School, University of Cyprus; Athens Association of Alzheimer's Disease and Related Disorders (E.N., P.S.), Maroussi; Center of Clinical, Experimental Surgery and Translational Research (L.S.), Biomedical Research Foundation of the Academy of Athens, Greece; and Taub Institute for Research in Alzheimer's Disease and the Aging Brain (N.S.), The Gertrude H. Sergievsky Center, Department of Neurology, Columbia University, New York, NY.
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Maria I. Maraki
From the 1st Department of Neurology (A.B., E.N., C.A.A., L.S., N.S.), Aiginition Hospital, National and Kapodistrian, University of Athens Medical School; Department of Nutrition and Dietetics (M.I.M., M.Y., E.N., C.A.A.), Harokopio University; Parkinson's Disease and Movement Disorders Department (M.S.), Hygeia Hospital, Athens, Greece; Department of Neurology (M.S.), Philipps University, Marburg, Germany; School of Medicine (G.X., E.D., G.M.H.), University of Thessaly, Larissa; Laboratory of Cognitive Neuroscience, School of Psychology (M.H.K.), Aristotle University of Thessaloniki, Greece; Department of Neurology (G.M.H.), Medical School, University of Cyprus; Athens Association of Alzheimer's Disease and Related Disorders (E.N., P.S.), Maroussi; Center of Clinical, Experimental Surgery and Translational Research (L.S.), Biomedical Research Foundation of the Academy of Athens, Greece; and Taub Institute for Research in Alzheimer's Disease and the Aging Brain (N.S.), The Gertrude H. Sergievsky Center, Department of Neurology, Columbia University, New York, NY.
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Mary Yannakoulia
From the 1st Department of Neurology (A.B., E.N., C.A.A., L.S., N.S.), Aiginition Hospital, National and Kapodistrian, University of Athens Medical School; Department of Nutrition and Dietetics (M.I.M., M.Y., E.N., C.A.A.), Harokopio University; Parkinson's Disease and Movement Disorders Department (M.S.), Hygeia Hospital, Athens, Greece; Department of Neurology (M.S.), Philipps University, Marburg, Germany; School of Medicine (G.X., E.D., G.M.H.), University of Thessaly, Larissa; Laboratory of Cognitive Neuroscience, School of Psychology (M.H.K.), Aristotle University of Thessaloniki, Greece; Department of Neurology (G.M.H.), Medical School, University of Cyprus; Athens Association of Alzheimer's Disease and Related Disorders (E.N., P.S.), Maroussi; Center of Clinical, Experimental Surgery and Translational Research (L.S.), Biomedical Research Foundation of the Academy of Athens, Greece; and Taub Institute for Research in Alzheimer's Disease and the Aging Brain (N.S.), The Gertrude H. Sergievsky Center, Department of Neurology, Columbia University, New York, NY.
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  • ORCID record for Mary Yannakoulia
Maria Stamelou
From the 1st Department of Neurology (A.B., E.N., C.A.A., L.S., N.S.), Aiginition Hospital, National and Kapodistrian, University of Athens Medical School; Department of Nutrition and Dietetics (M.I.M., M.Y., E.N., C.A.A.), Harokopio University; Parkinson's Disease and Movement Disorders Department (M.S.), Hygeia Hospital, Athens, Greece; Department of Neurology (M.S.), Philipps University, Marburg, Germany; School of Medicine (G.X., E.D., G.M.H.), University of Thessaly, Larissa; Laboratory of Cognitive Neuroscience, School of Psychology (M.H.K.), Aristotle University of Thessaloniki, Greece; Department of Neurology (G.M.H.), Medical School, University of Cyprus; Athens Association of Alzheimer's Disease and Related Disorders (E.N., P.S.), Maroussi; Center of Clinical, Experimental Surgery and Translational Research (L.S.), Biomedical Research Foundation of the Academy of Athens, Greece; and Taub Institute for Research in Alzheimer's Disease and the Aging Brain (N.S.), The Gertrude H. Sergievsky Center, Department of Neurology, Columbia University, New York, NY.
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Georgia Xiromerisiou
From the 1st Department of Neurology (A.B., E.N., C.A.A., L.S., N.S.), Aiginition Hospital, National and Kapodistrian, University of Athens Medical School; Department of Nutrition and Dietetics (M.I.M., M.Y., E.N., C.A.A.), Harokopio University; Parkinson's Disease and Movement Disorders Department (M.S.), Hygeia Hospital, Athens, Greece; Department of Neurology (M.S.), Philipps University, Marburg, Germany; School of Medicine (G.X., E.D., G.M.H.), University of Thessaly, Larissa; Laboratory of Cognitive Neuroscience, School of Psychology (M.H.K.), Aristotle University of Thessaloniki, Greece; Department of Neurology (G.M.H.), Medical School, University of Cyprus; Athens Association of Alzheimer's Disease and Related Disorders (E.N., P.S.), Maroussi; Center of Clinical, Experimental Surgery and Translational Research (L.S.), Biomedical Research Foundation of the Academy of Athens, Greece; and Taub Institute for Research in Alzheimer's Disease and the Aging Brain (N.S.), The Gertrude H. Sergievsky Center, Department of Neurology, Columbia University, New York, NY.
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Mary H. Kosmidis
From the 1st Department of Neurology (A.B., E.N., C.A.A., L.S., N.S.), Aiginition Hospital, National and Kapodistrian, University of Athens Medical School; Department of Nutrition and Dietetics (M.I.M., M.Y., E.N., C.A.A.), Harokopio University; Parkinson's Disease and Movement Disorders Department (M.S.), Hygeia Hospital, Athens, Greece; Department of Neurology (M.S.), Philipps University, Marburg, Germany; School of Medicine (G.X., E.D., G.M.H.), University of Thessaly, Larissa; Laboratory of Cognitive Neuroscience, School of Psychology (M.H.K.), Aristotle University of Thessaloniki, Greece; Department of Neurology (G.M.H.), Medical School, University of Cyprus; Athens Association of Alzheimer's Disease and Related Disorders (E.N., P.S.), Maroussi; Center of Clinical, Experimental Surgery and Translational Research (L.S.), Biomedical Research Foundation of the Academy of Athens, Greece; and Taub Institute for Research in Alzheimer's Disease and the Aging Brain (N.S.), The Gertrude H. Sergievsky Center, Department of Neurology, Columbia University, New York, NY.
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Eva Ntanasi
From the 1st Department of Neurology (A.B., E.N., C.A.A., L.S., N.S.), Aiginition Hospital, National and Kapodistrian, University of Athens Medical School; Department of Nutrition and Dietetics (M.I.M., M.Y., E.N., C.A.A.), Harokopio University; Parkinson's Disease and Movement Disorders Department (M.S.), Hygeia Hospital, Athens, Greece; Department of Neurology (M.S.), Philipps University, Marburg, Germany; School of Medicine (G.X., E.D., G.M.H.), University of Thessaly, Larissa; Laboratory of Cognitive Neuroscience, School of Psychology (M.H.K.), Aristotle University of Thessaloniki, Greece; Department of Neurology (G.M.H.), Medical School, University of Cyprus; Athens Association of Alzheimer's Disease and Related Disorders (E.N., P.S.), Maroussi; Center of Clinical, Experimental Surgery and Translational Research (L.S.), Biomedical Research Foundation of the Academy of Athens, Greece; and Taub Institute for Research in Alzheimer's Disease and the Aging Brain (N.S.), The Gertrude H. Sergievsky Center, Department of Neurology, Columbia University, New York, NY.
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Efthimios Dardiotis
From the 1st Department of Neurology (A.B., E.N., C.A.A., L.S., N.S.), Aiginition Hospital, National and Kapodistrian, University of Athens Medical School; Department of Nutrition and Dietetics (M.I.M., M.Y., E.N., C.A.A.), Harokopio University; Parkinson's Disease and Movement Disorders Department (M.S.), Hygeia Hospital, Athens, Greece; Department of Neurology (M.S.), Philipps University, Marburg, Germany; School of Medicine (G.X., E.D., G.M.H.), University of Thessaly, Larissa; Laboratory of Cognitive Neuroscience, School of Psychology (M.H.K.), Aristotle University of Thessaloniki, Greece; Department of Neurology (G.M.H.), Medical School, University of Cyprus; Athens Association of Alzheimer's Disease and Related Disorders (E.N., P.S.), Maroussi; Center of Clinical, Experimental Surgery and Translational Research (L.S.), Biomedical Research Foundation of the Academy of Athens, Greece; and Taub Institute for Research in Alzheimer's Disease and the Aging Brain (N.S.), The Gertrude H. Sergievsky Center, Department of Neurology, Columbia University, New York, NY.
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Georgios M. Hadjigeorgiou
From the 1st Department of Neurology (A.B., E.N., C.A.A., L.S., N.S.), Aiginition Hospital, National and Kapodistrian, University of Athens Medical School; Department of Nutrition and Dietetics (M.I.M., M.Y., E.N., C.A.A.), Harokopio University; Parkinson's Disease and Movement Disorders Department (M.S.), Hygeia Hospital, Athens, Greece; Department of Neurology (M.S.), Philipps University, Marburg, Germany; School of Medicine (G.X., E.D., G.M.H.), University of Thessaly, Larissa; Laboratory of Cognitive Neuroscience, School of Psychology (M.H.K.), Aristotle University of Thessaloniki, Greece; Department of Neurology (G.M.H.), Medical School, University of Cyprus; Athens Association of Alzheimer's Disease and Related Disorders (E.N., P.S.), Maroussi; Center of Clinical, Experimental Surgery and Translational Research (L.S.), Biomedical Research Foundation of the Academy of Athens, Greece; and Taub Institute for Research in Alzheimer's Disease and the Aging Brain (N.S.), The Gertrude H. Sergievsky Center, Department of Neurology, Columbia University, New York, NY.
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Paraskevi Sakka
From the 1st Department of Neurology (A.B., E.N., C.A.A., L.S., N.S.), Aiginition Hospital, National and Kapodistrian, University of Athens Medical School; Department of Nutrition and Dietetics (M.I.M., M.Y., E.N., C.A.A.), Harokopio University; Parkinson's Disease and Movement Disorders Department (M.S.), Hygeia Hospital, Athens, Greece; Department of Neurology (M.S.), Philipps University, Marburg, Germany; School of Medicine (G.X., E.D., G.M.H.), University of Thessaly, Larissa; Laboratory of Cognitive Neuroscience, School of Psychology (M.H.K.), Aristotle University of Thessaloniki, Greece; Department of Neurology (G.M.H.), Medical School, University of Cyprus; Athens Association of Alzheimer's Disease and Related Disorders (E.N., P.S.), Maroussi; Center of Clinical, Experimental Surgery and Translational Research (L.S.), Biomedical Research Foundation of the Academy of Athens, Greece; and Taub Institute for Research in Alzheimer's Disease and the Aging Brain (N.S.), The Gertrude H. Sergievsky Center, Department of Neurology, Columbia University, New York, NY.
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Costas A. Anastasiou
From the 1st Department of Neurology (A.B., E.N., C.A.A., L.S., N.S.), Aiginition Hospital, National and Kapodistrian, University of Athens Medical School; Department of Nutrition and Dietetics (M.I.M., M.Y., E.N., C.A.A.), Harokopio University; Parkinson's Disease and Movement Disorders Department (M.S.), Hygeia Hospital, Athens, Greece; Department of Neurology (M.S.), Philipps University, Marburg, Germany; School of Medicine (G.X., E.D., G.M.H.), University of Thessaly, Larissa; Laboratory of Cognitive Neuroscience, School of Psychology (M.H.K.), Aristotle University of Thessaloniki, Greece; Department of Neurology (G.M.H.), Medical School, University of Cyprus; Athens Association of Alzheimer's Disease and Related Disorders (E.N., P.S.), Maroussi; Center of Clinical, Experimental Surgery and Translational Research (L.S.), Biomedical Research Foundation of the Academy of Athens, Greece; and Taub Institute for Research in Alzheimer's Disease and the Aging Brain (N.S.), The Gertrude H. Sergievsky Center, Department of Neurology, Columbia University, New York, NY.
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Leonidas Stefanis
From the 1st Department of Neurology (A.B., E.N., C.A.A., L.S., N.S.), Aiginition Hospital, National and Kapodistrian, University of Athens Medical School; Department of Nutrition and Dietetics (M.I.M., M.Y., E.N., C.A.A.), Harokopio University; Parkinson's Disease and Movement Disorders Department (M.S.), Hygeia Hospital, Athens, Greece; Department of Neurology (M.S.), Philipps University, Marburg, Germany; School of Medicine (G.X., E.D., G.M.H.), University of Thessaly, Larissa; Laboratory of Cognitive Neuroscience, School of Psychology (M.H.K.), Aristotle University of Thessaloniki, Greece; Department of Neurology (G.M.H.), Medical School, University of Cyprus; Athens Association of Alzheimer's Disease and Related Disorders (E.N., P.S.), Maroussi; Center of Clinical, Experimental Surgery and Translational Research (L.S.), Biomedical Research Foundation of the Academy of Athens, Greece; and Taub Institute for Research in Alzheimer's Disease and the Aging Brain (N.S.), The Gertrude H. Sergievsky Center, Department of Neurology, Columbia University, New York, NY.
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Nikolaos Scarmeas
From the 1st Department of Neurology (A.B., E.N., C.A.A., L.S., N.S.), Aiginition Hospital, National and Kapodistrian, University of Athens Medical School; Department of Nutrition and Dietetics (M.I.M., M.Y., E.N., C.A.A.), Harokopio University; Parkinson's Disease and Movement Disorders Department (M.S.), Hygeia Hospital, Athens, Greece; Department of Neurology (M.S.), Philipps University, Marburg, Germany; School of Medicine (G.X., E.D., G.M.H.), University of Thessaly, Larissa; Laboratory of Cognitive Neuroscience, School of Psychology (M.H.K.), Aristotle University of Thessaloniki, Greece; Department of Neurology (G.M.H.), Medical School, University of Cyprus; Athens Association of Alzheimer's Disease and Related Disorders (E.N., P.S.), Maroussi; Center of Clinical, Experimental Surgery and Translational Research (L.S.), Biomedical Research Foundation of the Academy of Athens, Greece; and Taub Institute for Research in Alzheimer's Disease and the Aging Brain (N.S.), The Gertrude H. Sergievsky Center, Department of Neurology, Columbia University, New York, NY.
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Higher probability of prodromal Parkinson disease is related to lower cognitive performance
Anastasia Bougea, Maria I. Maraki, Mary Yannakoulia, Maria Stamelou, Georgia Xiromerisiou, Mary H. Kosmidis, Eva Ntanasi, Efthimios Dardiotis, Georgios M. Hadjigeorgiou, Paraskevi Sakka, Costas A. Anastasiou, Leonidas Stefanis, Nikolaos Scarmeas
Neurology May 2019, 92 (19) e2261-e2272; DOI: 10.1212/WNL.0000000000007453

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Abstract

Objective Given the limited information on cognitive function before Parkinson disease (PD) clinical onset in the general population, we sought to assess prodromal PD (pPD) probability and relate it to detailed cognitive performance in a community cohort.

Methods In a population-based cohort of 1,629 dementia-free and PD-free participants ≥65 years of age in Greece, we assessed probability of pPD according to the International Parkinson and Movement Disorder Society's criteria. Clinical cognitive diagnoses (cognitively unimpaired, mild cognitive impairment [MCI], dementia) considering neuropsychological testing and functional status were assigned in consensus conferences. Cognitive performance in 5 cognitive domains was assessed by a detailed neuropsychological battery and summarized in the form of z scores. We investigated associations between pPD probability (and its individual constituents) and cognitive outcomes.

Results The median probability of pPD was 1.81% (0.2%–96.7%). Participants with MCI had higher probability of pPD compared to those with normal cognition (p < 0.001). Higher probability of pPD was related to lower performance in all cognitive domains (memory, language, executive, attention, and visuospatial function) (p < 0.001). Lower cognitive performance was further associated with certain nonmotor markers of pPD, such as daytime somnolence, depression, urinary dysfunction, constipation, and subthreshold parkinsonism (p < 0.001).

Conclusions Higher probability of pPD was associated with lower cognitive performance in all domains and higher probability of MCI. This may reflect a widespread pathologic process although future studies are warranted to infer causality. These results suggest to clinicians that they should assess cognition early, and to researchers that they should further look into the possible mechanisms that may underlie this observation.

Glossary

CI=
confidence interval;
DSM-IV-TR=
Diagnostic and Statistical Manual of Mental Disorders, 4th edition, text revision;
HAAS=
Honolulu–Asia Aging Study;
HELIAD=
Hellenic Longitudinal Investigation of Aging and Diet;
LR=
likelihood ratio;
MCI=
mild cognitive impairment;
MDS=
International Parkinson and Movement Disorder Society;
OR=
odds ratio;
PD=
Parkinson disease;
pPD=
prodromal Parkinson disease;
PRIPS=
Prospective Evaluation of Risk Factors for Idiopathic Parkinson's Syndrome;
RBD=
REM sleep behavior disorder;
ROS=
Religious Orders Study;
SES=
socioeconomic status;
UPDRS=
Unified Parkinson's Disease Rating Scale

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.

  • Received September 13, 2018.
  • Accepted in final form January 11, 2019.
  • © 2019 American Academy of Neurology
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