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Articles
October 8, 2014
Letter to the Editor

Imaging prodromal Parkinson disease
The Parkinson Associated Risk Syndrome Study

November 4, 2014 issue
83 (19) 1739-1746

Abstract

Objectives:

The purpose of this study is to evaluate the relative risk of abnormal dopamine transporter (DAT) imaging for subjects with and without hyposmia and the feasibility of acquiring a large, community-based, 2-tiered biomarker assessment strategy to detect prodromal Parkinson disease (PD).

Methods:

In this observational study, individuals without a diagnosis of PD, recruited through 16 movement disorder clinics, underwent tier 1 assessments (olfactory testing, questionnaires). Tier 2 assessments (neurologic examination, DAT imaging, and other biomarker assessments) were completed by 303 subjects. The main outcome of the study is to compare age-expected [123I]β-CIT striatal binding ratio in hyposmic and normosmic subjects.

Results:

Tier 1 assessments were mailed to 9,398 eligible subjects and returned by 4,999; 669 were hyposmic. Three hundred three subjects (203 hyposmic, 100 normosmic) completed baseline evaluations. DAT deficit was present in 11% of hyposmic subjects compared with 1% of normosmic subjects. Multiple logistic regression demonstrates hyposmia (odds ratio [OR] 12.4; 95% confidence interval [CI] 1.6, 96.1), male sex (OR 5.5; 95% CI 1.7, 17.2), and constipation (OR 4.3; 95% CI 1.6, 11.6) as factors predictive of DAT deficit. Combining multiple factors (hyposmia, male sex, and constipation) increased the percentage of subjects with a DAT deficit to >40%.

Conclusion:

Subjects with DAT deficit who do not meet criteria for a diagnosis of PD can be identified by olfactory testing. Sequential biomarker assessment may identify those at risk of PD. Selecting hyposmic individuals enriches the population for DAT deficit, and combining hyposmia with other potential risk factors (male sex, constipation) increases the percentage of subjects with a DAT deficit compatible with prodromal PD.

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Supplementary Material

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Letters to the Editor
18 November 2014
Hyposmia as a sensitive but non-specific marker for early neurodegeneration
Martijn L.T.M. Muller, Research Assistant Professor
Roger L. Albin, University of Michigan & VAAAHS, Ann Arbor, MI; Nicolaas I. Bohnen, University of Michigan & VAAAHS Ann Arbor, MI

Jennings et al. reported striatal dopamine transporter SPECT (DAT) findings in hyposmic, but otherwise healthy subjects, compared to subjects without hyposmia. [1] These findings suggest that hyposmia, especially in combination with other Parkinson disease (PD) risk factors, may serve as a screening tool to identify subjects with prodromal PD. It should be noted, however, that abnormal DAT findings were found in 11% of hyposmic subjects only, and the inclusion of other PD risk factors increased this percentage to only ~40%. A possible explanation may be the presence of Alzheimer-type pathology in the olfactory bulb and its projection areas rather than ??-synucleinopathy. [2] Olfactory loss is also an early sign of Alzheimer disease. [3]

We suggest that hyposmia is a sensitive marker of early neurodegeneration. Given the relatively high frequency of ??-synucleinopathy and amyloidopathy in relatively healthy cognitively normal older adults, [4, 5] present definitions of hyposmia in the elderly, such as the 15th percentile cut-off used in this paper, may exclude individuals with mild hyposmia secondary to neurodegeneration. Further studies are required to redefine normative data for hyposmia in older subjects, which should be defined in the absence of prodromal Lewy or Alzheimer-type pathologies.

1. Jennings D, Siderowf A, Stern M, et al. Imaging prodromal Parkinson disease: The Parkinson Associated Risk Syndrome Study. Neurology 2014;83:1739-1746.

2. Braak H, Braak E. Staging of Alzheimer's disease-related neurofibrillary changes. Neurobiol Aging 1995;16:271-278; discussion 278-284.

3. Barresi M, Ciurleo R, Giacoppo S, et al. Evaluation of olfactory dysfunction in neurodegenerative diseases. J Neurol Sci 2012;323:16-24.

4. Aizenstein HJ, Nebes RD, Saxton JA, et al. Frequent amyloid deposition without significant cognitive impairment among the elderly. Arch Neurol 2008;65:1509-1517.

5. Adler CH, Connor DJ, Hentz JG, et al. Incidental Lewy body disease: clinical comparison to a control cohort. Mov Disord 2010;25:642-646.

For disclosures, please contact the editorial office at [email protected].

11 March 2015
Response to Mullen et al.
Danna Jennings, Senior Clinical Research Director
Andrew Siderowf, MD; Matthew Stern, MD; John Seibyl, MD; Shirley Eberly, MS; David Oakes, PhD; Kenneth Marek, MD

As Muller et al. noted, it has been shown that hyposmia is a sensitive, but non-specific marker for Parkinson disease (PD), Alzheimer disease (AD) and potentially other neurodegenerative disorders. Nearly all patients with PD and AD are hyposmic, however a small percentage of individuals with hyposmia have a neurologic etiology with the most common causes being post-infection and post- traumatic disease (70%) .[1] While the PARS study was designed to examine hyposmia in combination with DAT imaging as a strategy to identify individuals with prodromal PD, we recognize that the PARS cohort is also enriched for prodromal AD based on their hyposmic status. We have therefore expanded the PARS study to include extensive cognitive evaluations and amyloid imaging of hyposmic subjects to identify individuals with prodromal AD. In addition, we acknowledge that utilizing the less than 15th percentile cut-off for the UPSIT may have eliminated healthy adults with amyloidopathy or a-synucleinopathy, however this is of lesser concern as the goal of PARS was to identify individuals with the greatest probability of having a DAT deficit (those with the most severe hyposmia) and ultimately highest likelihood of phenoconversion to PD.

1. Fonteyn S, Huart C, Deggouj N, Collet S, Eloy P, Rombaux P. Non-sinonasal-related olfactory dysfunction: a cohort of 496 patients. Eur Ann Ototrhin 2014;131:87-91.

For disclosures, contact the editorial office at [email protected].

Information & Authors

Information

Published In

Neurology®
Volume 83Number 19November 4, 2014
Pages: 1739-1746
PubMed: 25298306

Publication History

Received: April 9, 2014
Accepted: August 7, 2014
Published online: October 8, 2014
Published in print: November 4, 2014

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Disclosure

D. Jennings is an employee of Molecular NeuroImaging, LLC. A. Siderowf is an employee of Avid Radiopharmaceuticals, a wholly owned subsidiary of Eli Lilly and Co. M. Stern is a member of the scientific advisory board for Adamas and Civitas. He is a paid consultant to Adamas, Civitas, Ipsen, Merz, NuPathe, and Teva. He has received payment for participating in the educational videos “Parkinson's in the Crossfire” and “Parkinson's Update” funded by Teva and for a lecture series in Australia funded by Novartis. J. Seibyl is a paid consultant for GE Healthcare and has received payment for developing educational presentations for Bayer Healthcare. He holds an equity interest in Molecular NeuroImaging, LLC, and has current grants with the Department of Defense. S. Eberly and D. Oakes report no disclosures relevant to the manuscript. K. Marek has served as a consultant for Pfizer, GE Healthcare, Merck, Eli Lilly, Bristol-Myers Squibb, Piramal, Prothena, NeuroPhage, nLife, and Roche. He holds grants with the Department of Defense and The Michael J. Fox Foundation for Parkinson's Research. Dr. Marek has ownership interest in Molecular NeuroImaging, LLC. Go to Neurology.org for full disclosures.

Study Funding

Support for this study is provided by the Department of Defense award number W81XWH-06-067.

Authors

Affiliations & Disclosures

Danna Jennings, MD
From the Institute for Neurodegenerative Disorders (D.J., J.S., K.M.), New Haven, CT; Parkinson's Disease and Movement Disorders Center (M.S.), Department of Neurology, University of Pennsylvania, Philadelphia; Department of Biostatistics and Computational Biology (S.E., D.O.), University of Rochester, NY; and Avid Radiopharmaceuticals (A.S.), Philadelphia, PA.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
Novartis speaker honorarium
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
Employed by Molecular NeuroImaging
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
(1) UCB
Other Activities:
1.
(1) Employee of Molecular NeuroImaging, LLC
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
(1)FORUM Pharmaceuticals (2)Concert Pharmaceuticals (3)Omeros (4)Amgen (5)Abbvie (6)Merck (7)Lilly (8)Avid Radiopharmaceuticals (9)Navidea (10)Eisai, Co (11)TauRx (12)Biogen
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
(1)Michael J Fox Foundation
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Andrew Siderowf, MD
From the Institute for Neurodegenerative Disorders (D.J., J.S., K.M.), New Haven, CT; Parkinson's Disease and Movement Disorders Center (M.S.), Department of Neurology, University of Pennsylvania, Philadelphia; Department of Biostatistics and Computational Biology (S.E., D.O.), University of Rochester, NY; and Avid Radiopharmaceuticals (A.S.), Philadelphia, PA.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
I was an associate editor for Movement Disorders from Jan 2012 to Jan 2013
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
I am a full-time employee of Avid Radiopharmaceuticals, a wholly owned subsidiary of Eli Lilly and Co
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Matthew Stern, MD
From the Institute for Neurodegenerative Disorders (D.J., J.S., K.M.), New Haven, CT; Parkinson's Disease and Movement Disorders Center (M.S.), Department of Neurology, University of Pennsylvania, Philadelphia; Department of Biostatistics and Computational Biology (S.E., D.O.), University of Rochester, NY; and Avid Radiopharmaceuticals (A.S.), Philadelphia, PA.
Disclosure
Scientific Advisory Boards:
1.
1) Adamas (SAB-consultant) 2) Civitas (SAB-consultant)
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
(1) Teva Sponsored educational activities
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
1)Adamas (consultant 2)Civitas (consultant) 3) Teva (consultant) 4) Merz (consultant) 5) Accorda (consultant)
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
Officer, International Parkinson and Movement Disorder Society
Stock/stock Options/board of Directors Compensation:
1.
Adamas, Inc, hold stock options, 2008-
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
John Seibyl, MD
From the Institute for Neurodegenerative Disorders (D.J., J.S., K.M.), New Haven, CT; Parkinson's Disease and Movement Disorders Center (M.S.), Department of Neurology, University of Pennsylvania, Philadelphia; Department of Biostatistics and Computational Biology (S.E., D.O.), University of Rochester, NY; and Avid Radiopharmaceuticals (A.S.), Philadelphia, PA.
Disclosure
Scientific Advisory Boards:
1.
Roche GE Healthcare
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
Molecular Neuroimaging
Consultancies:
1.
Piramal Navidea
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
MJ Fox Foundation
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
Ownership- Molecular Neuroimaging
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Shirley Eberly, MS
From the Institute for Neurodegenerative Disorders (D.J., J.S., K.M.), New Haven, CT; Parkinson's Disease and Movement Disorders Center (M.S.), Department of Neurology, University of Pennsylvania, Philadelphia; Department of Biostatistics and Computational Biology (S.E., D.O.), University of Rochester, NY; and Avid Radiopharmaceuticals (A.S.), Philadelphia, PA.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
1) Commercial entity: Biogen Idek 2) Commercial entity: Auspex Pharmaceuticals
Research Support, Government Entities:
1.
1) Subaward from MGH, Steven Hersch: 10/1/2010-8/31/2015: Blood Level of Huntington�s: A Biomarker of Huntington�s Disease; UO1NS071789 is NIH award number. Data analysis. 2) Subaward from Harvard, Alberto Ascherio: 4/15/2009-3/31/2014: Urate as a Predictor of Parkinson�s Disease Risk and Progression; RO1NS061858 is NIH award number. Data analysis. 3) University of Rochester, Mark W. Frampton: 4/1/2009-3/31/2014: Ozone Cardiovascular Effects in Genetically Susceptible People; RO100513195 is NIH award number. Data analysis.
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
Michael J Fox Foundation
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
David Oakes, PhD
From the Institute for Neurodegenerative Disorders (D.J., J.S., K.M.), New Haven, CT; Parkinson's Disease and Movement Disorders Center (M.S.), Department of Neurology, University of Pennsylvania, Philadelphia; Department of Biostatistics and Computational Biology (S.E., D.O.), University of Rochester, NY; and Avid Radiopharmaceuticals (A.S.), Philadelphia, PA.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
Editor, Lifetime Data Analysis, 2010-present
Patents:
1.
NONE
Publishing Royalties:
1.
Royalties Cox DR and Oakes D Analysis of Survival Data, Chapman and Hall, 1984
Employment, Commercial Entity:
1.
University of Rochester Professor
Consultancies:
1.
Novo Nordisk Inc Sanofi Inc Vanda Pharmaceuticals
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NINDS U01 NS050573, PI, 2005-2012
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Kenneth Marek, MD
From the Institute for Neurodegenerative Disorders (D.J., J.S., K.M.), New Haven, CT; Parkinson's Disease and Movement Disorders Center (M.S.), Department of Neurology, University of Pennsylvania, Philadelphia; Department of Biostatistics and Computational Biology (S.E., D.O.), University of Rochester, NY; and Avid Radiopharmaceuticals (A.S.), Philadelphia, PA.
Disclosure
Scientific Advisory Boards:
1.
(1) Michael J Fox Foundation (2) Shire
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
(1) Pfizer (2)GE Healthcare (3)Merck (4) Eli Lilly (5)BMS (6) Piramal (7)Prothena (8)Neurophage, (9) nLife, (10)Roche
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
(1) Ownership in Molecular NeuroImaging
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
(1) DOD �TATRC, W81XWH-06-1-0678, Principal Investigator, 10/1/06 � 09/30/15
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
(1) MJFox Foundation, Parkinson progression marker intiative, Principal Investigator, 6/15/09 � 6/14/18 (2) MJFox Foundation, DAT imaging in LRKK2 family members, Principal Investigator, 1/15/10 � 1/14/15
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
(1) Equity interest in Molecular NeuroImaging, LLC (2001-present)
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
For the PARS Investigators
From the Institute for Neurodegenerative Disorders (D.J., J.S., K.M.), New Haven, CT; Parkinson's Disease and Movement Disorders Center (M.S.), Department of Neurology, University of Pennsylvania, Philadelphia; Department of Biostatistics and Computational Biology (S.E., D.O.), University of Rochester, NY; and Avid Radiopharmaceuticals (A.S.), Philadelphia, PA.

Notes

Correspondence to Dr. Jennings: [email protected]
PARS coinvestigators are listed on the Neurology® Web site at www.neurology.org.
Go to Neurology.org for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

Author Contributions

Danna Jennings, as the primary author of the manuscript, contributed to the trial design, subject recruitment, and data collection and data analysis. Andrew Siderowf contributed to the development of the protocol, data collection and data analysis, and critical review of the manuscript. Matthew Stern contributed to the study design and data collection and data interpretation. John Seibyl was involved in the analysis and interpretation of the imaging data and review of the manuscript. Shirley Eberly contributed to data analysis and interpretation and critical revision of the manuscript. David Oakes contributed to the analysis and interpretation of data and critical review of the manuscript. Kenneth Marek was involved in the development of the protocol, data collection, data analysis, and review of and contribution to the manuscript.

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  3. Review of Physical Signs and Biochemical and Radiological Biomarkers for Detection of Prodromal Parkinson's Disease, Critical Reviews in Physical and Rehabilitation Medicine, 35, 2, (59-73), (2023).https://doi.org/10.1615/CritRevPhysRehabilMed.2023045668
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