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Abstract

Objective:

To examine functional connectivity within the basal ganglia network (BGN) in a group of cognitively normal patients with early Parkinson disease (PD) on and off medication compared to age- and sex-matched healthy controls (HC), and to validate the findings in a separate cohort of participants with PD.

Methods:

Participants were scanned with resting-state fMRI (RS-fMRI) at 3T field strength. Resting-state networks were isolated using independent component analysis. A BGN template was derived from 80 elderly HC participants. BGN maps were compared between 19 patients with PD on and off medication in the discovery group and 19 age- and sex-matched controls to identify a threshold for optimal group separation. The threshold was applied to 13 patients with PD (including 5 drug-naive) in the validation group to establish reproducibility of findings.

Results:

Participants with PD showed reduced functional connectivity with the BGN in a wide range of areas. Administration of medication significantly improved connectivity. Average BGN connectivity differentiated participants with PD from controls with 100% sensitivity and 89.5% specificity. The connectivity threshold was tested on the validation cohort and achieved 85% accuracy.

Conclusions:

We demonstrate that resting functional connectivity, measured with MRI using an observer-independent method, is reproducibly reduced in the BGN in cognitively intact patients with PD, and increases upon administration of dopaminergic medication. Our results hold promise for RS-fMRI connectivity as a biomarker in early PD.

Classification of evidence:

This study provides Class III evidence that average connectivity in the BGN as measured by RS-fMRI distinguishes patients with PD from age- and sex-matched controls.

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Supplementary Material

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Letters to the Editor
11 August 2014
Response: 'first step' of biomarker development
Clare E Mackay, Associate Professor
Konrad Szewczyk-Krolikowski, Oxford, UK; Yoav Ben-Shlomo, Bristol, UK; Michele Hu, Oxford, UK

We thank Dr. Montgomery for his interest in our paper [1] and his insightful comments. We agree that any biomarker should be interpreted in the context of pre-test probabilities and the test's positive and negative likelihood ratios. We also agree that our validation sample was not representative of the population in which our method would ultimately be used.

Our study represents the first step of biomarker development in attempting to simultaneously characterize a new marker and establish its reproducibility. As such, our 'validation' demonstrated that similar results can be obtained in two independent patient groups, rather than testing the biomarker in a real life situation. The next step is to test BGN connectivity in populations enriched for PD (for example, by screening participants for hyposmia [2] or rapid-eye movement sleep behavior disorder [3]) where the prior probability is much higher (e.g. 40-60%) than in a random population-based sample with low risk. In this case, the post-test probability, given a positive MRI, would be much higher, although there would inevitably still be false positives.

1. Szewczyk-Krolikowski K, Menke RA, Rolinski M, et al. Functional connectivity in the basal ganglia network differentiates PD patients from controls. Neurology 2014;83:202-203.

2. Ponsen MM, Stoffers D, Booij J, et al. Idiopathic hyposmia as a preclinical sign of Parkinson's disease. Ann Neurol 2004;56:173-181.

3. Iranzo A, Tolosa E, Gelpi E, et al. Neurodegenerative disease status and post mortem pathology in idiopathic rapid eye-movement sleep behavior disorder: an observational cohort study. Lancet Neurol 2013;12:443-453.

For disclosures, contact the editorial office.

23 July 2014
Functional connectivity in the basal ganglia network differentiates PD patients from controls
Erwin B. Montgomery Jr., Medical Director

In their article, Szewczyk-Krolikowski et al. suggested there may be a potential for resting state MRI (RS-MRI) as a biomarker for early Parkinson disease (PD). [1] However, the term "potential" connotes a range from "possible" to "probable" and the study did not support "probable". The sample was not representative of the population of concern- patients with early and uncertain diagnosis of PD. Therefore, it cannot be taken a priori that the PD sample was representative of subjects to which the RS-MRI analysis would be relevant. The specificity and sensitivity rates for the discovery group are not the critical issues, [2] rather it is the specificity and sensitivity when the logistic regression model is applied prospectively. In that case, the actual sensitivity is 85% but no prospectively derived specificity was provided.

The prior probabilities of subjects with early PD in the population of concern was also not considered. If one assumes 3% as the prevalence rate of PD in the general population over age 65 and a specificity from the discovery group of 89.5%, the RS-MRI would mistakenly identified 10 normal subjects as being positive for the biomarker and all three PD patients would be positive. Thus, there would be more false than true positives. Specificity and sensitivity can be misleading, and positive and negative predictive values, which account for the prior probabilities, are more informative. Even the positive and negative predictive values do not carry consideration of the consequence of applying the test.

It is possible that the RS-MRI may have diagnostic utility, but the population with the appropriate prior probabilities would need to be defined.

1. Szewczyk-Krolikowski K, Menke RA, Rolinski M, et al. Functional connectivity in the basal ganglia network differentiates PD patients from controls. Neurology 2014;83:202-203.

2. Wasson JH, Sox HC, Neff RK, Goldman L. Clinical prediction rules. Applications and methodological standards. N Engl J Med 1985;313:793-799.

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

Information & Authors

Information

Published In

Neurology®
Volume 83Number 3July 15, 2014
Pages: 208-214
PubMed: 24920856

Publication History

Received: July 22, 2013
Accepted: January 28, 2014
Published online: June 11, 2014
Published in print: July 15, 2014

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Disclosure

K. Szewczyk-Krolikowski has received research support from Parkinson's UK. R. Menke has received research support from Parkinson's UK. M. Rolinski has received research support from the NIHR Oxford Biomedical Centre. E. Duff, G. Salimi-Khorshidi, N. Filippini, and G. Zamboni report no disclosures relevant to the manuscript. M. Hu has received research support from Parkinson's UK. C. Mackay has received research support from Parkinson's UK and the NIHR Oxford Biomedical Research Centre. Go to Neurology.org for full disclosures.

Study Funding

The research is funded by the Monument Trust Discovery Award from Parkinson's UK to the Oxford Parkinson Disease Centre. The authors are supported by the National Institute for Health Research (NIHR) Oxford Biomedical Research Centre based at Oxford University Hospitals NHS Trust and University of Oxford and the Dementias and Neurodegenerative Diseases Research Network (DeNDRoN).

Authors

Affiliations & Disclosures

Konrad Szewczyk-Krolikowski, MD
From the Nuffield Department of Clinical Neurosciences (K.S.-K., M.R., M.H.), Oxford Parkinson's Disease Centre (OPDC) (K.S.-K., R.A.L.M., M.R., M.T.M.H., C.E.M.), Department of Psychiatry (C.E.M.), and FMRIB Centre (R.A.L.M., E.D., G.S.-K., N.F., G.Z., C.E.M.), University of Oxford, UK.
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.
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.
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Ricarda A.L. Menke, PhD
From the Nuffield Department of Clinical Neurosciences (K.S.-K., M.R., M.H.), Oxford Parkinson's Disease Centre (OPDC) (K.S.-K., R.A.L.M., M.R., M.T.M.H., C.E.M.), Department of Psychiatry (C.E.M.), and FMRIB Centre (R.A.L.M., E.D., G.S.-K., N.F., G.Z., C.E.M.), University of Oxford, UK.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
Frontiers in Neuropsychiatric Imaging and Stimulation, Review Editor, 2013
Patents:
1.
NONE
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1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
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1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
(1) MRC (PI: Dr M Turner), senior postdoctoral research fellow, 2013-2017
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
1) Parkinson�s UK (Monument Discovery award), 2) Thames Valley DeNDRoN (Dementias and Neurodegenerative Diseases Research Network) (Research Capability Funding), 3) NIHR Research Capacity Funding
Stock/stock Options/board of Directors Compensation:
1.
NONE
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Michal Rolinski, MD
From the Nuffield Department of Clinical Neurosciences (K.S.-K., M.R., M.H.), Oxford Parkinson's Disease Centre (OPDC) (K.S.-K., R.A.L.M., M.R., M.T.M.H., C.E.M.), Department of Psychiatry (C.E.M.), and FMRIB Centre (R.A.L.M., E.D., G.S.-K., N.F., G.Z., C.E.M.), University of Oxford, UK.
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.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
(1) The National Institute for Health Research (NIHR) Oxford Biomedical Research Centre based at Oxford University Hospitals NHS Trust and University of Oxford
Research Support, Foundations and Societies:
1.
NONE
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1.
NONE
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Eugene Duff, PhD
From the Nuffield Department of Clinical Neurosciences (K.S.-K., M.R., M.H.), Oxford Parkinson's Disease Centre (OPDC) (K.S.-K., R.A.L.M., M.R., M.T.M.H., C.E.M.), Department of Psychiatry (C.E.M.), and FMRIB Centre (R.A.L.M., E.D., G.S.-K., N.F., G.Z., C.E.M.), University of Oxford, UK.
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.
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
Gholamreza Salimi-Khorshidi, PhD
From the Nuffield Department of Clinical Neurosciences (K.S.-K., M.R., M.H.), Oxford Parkinson's Disease Centre (OPDC) (K.S.-K., R.A.L.M., M.R., M.T.M.H., C.E.M.), Department of Psychiatry (C.E.M.), and FMRIB Centre (R.A.L.M., E.D., G.S.-K., N.F., G.Z., C.E.M.), University of Oxford, UK.
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.
I lead the quant team at AIG and receive salary from them
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.
I founded and am the CEO of ConnectomeX
License Fee Payments, Technology or Inventions:
1.
NONE
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NONE
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1.
NONE
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1.
NONE
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1.
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Nicola Filippini, PhD
From the Nuffield Department of Clinical Neurosciences (K.S.-K., M.R., M.H.), Oxford Parkinson's Disease Centre (OPDC) (K.S.-K., R.A.L.M., M.R., M.T.M.H., C.E.M.), Department of Psychiatry (C.E.M.), and FMRIB Centre (R.A.L.M., E.D., G.S.-K., N.F., G.Z., C.E.M.), University of Oxford, UK.
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.
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
Giovanna Zamboni, PhD
From the Nuffield Department of Clinical Neurosciences (K.S.-K., M.R., M.H.), Oxford Parkinson's Disease Centre (OPDC) (K.S.-K., R.A.L.M., M.R., M.T.M.H., C.E.M.), Department of Psychiatry (C.E.M.), and FMRIB Centre (R.A.L.M., E.D., G.S.-K., N.F., G.Z., C.E.M.), University of Oxford, UK.
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.
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
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1.
NONE
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1.
NONE
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1.
NONE
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Michele T.M. Hu, MBBS, FRCP, PhD*
From the Nuffield Department of Clinical Neurosciences (K.S.-K., M.R., M.H.), Oxford Parkinson's Disease Centre (OPDC) (K.S.-K., R.A.L.M., M.R., M.T.M.H., C.E.M.), Department of Psychiatry (C.E.M.), and FMRIB Centre (R.A.L.M., E.D., G.S.-K., N.F., G.Z., C.E.M.), University of Oxford, UK.
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.
NONE
Research Support, Government Entities:
1.
(1) Oxford Biomedical Research Centre and National Institute for Health Research CLRN, funded 50% of salary years 1-2 to support research 2010- current
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
(1) Parkinson's UK Discovery project grant award, 2010-2015 funded MRI scans and research fellow support
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
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1.
NONE
Legal Proceedings:
1.
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Clare E. Mackay, PhD*
From the Nuffield Department of Clinical Neurosciences (K.S.-K., M.R., M.H.), Oxford Parkinson's Disease Centre (OPDC) (K.S.-K., R.A.L.M., M.R., M.T.M.H., C.E.M.), Department of Psychiatry (C.E.M.), and FMRIB Centre (R.A.L.M., E.D., G.S.-K., N.F., G.Z., C.E.M.), University of Oxford, UK.
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.
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
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I hold shares in Conaptic ltd, who develop online database and facility management software for clinical research
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Notes

Correspondence to Dr. Mackay: [email protected]
*
Dr. Hu and Dr. Mackay are joint senior authors.
The views expressed are those of the authors and not necessarily those of the NHS, the NIHR, or the Department of Health.
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

Dr. Szewczyk-Krolikowski: literature review, experimental design, data acquisition, image data analysis, result interpretation, statistical analysis, manuscript drafting and revision. Dr. Menke: experimental design, data acquisition, and manuscript revision. Dr. Rolinski: data acquisition and manuscript revision. Dr. Duff: data analysis and manuscript revision. Dr. Salimi-Khorshidi: data analysis and manuscript revision. Dr. Filippini: image data analysis and manuscript revision, provision of additional imaging datasets. Dr. Zamboni: provision of additional imaging data sets. Dr. Hu: experimental design, result interpretation, and manuscript revision. Dr. Mackay: experimental design, result interpretation, and manuscript revision.

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