Assessment of heterogeneity and disease onset in the Parkinson’s Progression Markers Initiative (PPMI) cohort using the α-synuclein seed amplification assay: a cross-sectional study

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Published March 1, 2023

Background Recent research demonstrates that α-synuclein seed amplification assays (αSyn-SAA) accurately differentiate Parkinson’s disease (PD) patients from healthy controls (HC). We used the well-characterized, multicenter Parkinson’s Progression Markers Initiative (PPMI) cohort to further assess the diagnostic performance of αSyn-SAA and to examine whether the assay identifies heterogeneity among patients and enables early identification in at-risk groups. Methods αSyn-SAA analysis of cerebrospinal fluid (CSF) was performed using previously described methods. We assessed sensitivity and specificity in PD and HC, including subgroups based on genetic and clinical features. We determined the frequency of positive αSyn-SAA results in prodromal participants (REM sleep behavior disorder and hyposmia) and non-manifesting carriers (NMCs) of genetic variants associated with PD and compared αSyn-SAA to clinical measures and other biomarkers. Findings 1,123 participants were included: 545 PD, 163 HCs, 54 participants with scans without evidence of dopaminergic deficit (SWEDDs), 51 prodromal participants, and 310 NMCs. Sensitivity and specificity for PD versus HC were 88% and 96%, respectively. Sensitivity in sporadic PD with the typical olfactory deficit was 99%. The proportion of positive αSyn-SAA was lower in subgroups including LRRK2 PD (68%) and sporadic PD patients without olfactory deficit (78%). Participants with LRRK2 variant and normal olfaction had an even lower αSyn-SAA positivity rate (35%). Among prodromal and at-risk groups, 86% of RBD and hyposmic cases had positive αSyn-SAA. 8% of NMC (either LRRK2 or GBA) were positive. Interpretation This study represents the largest analysis of αSyn-SAA for biochemical diagnosis of PD. Our results demonstrate that the assay classifies PD patients with high sensitivity and specificity, provides information about molecular heterogeneity, and detects prodromal individuals prior to diagnosis. These findings suggest a crucial role for αSyn-SAA in therapeutic development, both to identify pathologically defined subgroups of PD patients and to establish biomarker-defined at-risk cohorts. (Initial Preprint DOI: 10.1101/2023.02.27.23286156 )
Tags
  • Alpha-synuclein
  • Biomarkers
  • CSF (Cerebral Spinal Fluid)
  • Original Research
  • PD subtypes

Meet the Authors

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    Andrew Siderowf

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    Luis Concha-Marambio

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    David-Erick Lafontant

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    Carly M. Farris

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    Yihua Ma

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    Paula A. Urenia

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    Hieu Nguyen

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    Roy N. Alcalay

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    Lana M. Chahine

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    Tatiana Foroud

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    Douglas Galasko

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    Karl Kieburtz

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    Kalpana Merchant, PhD

    Northwestern University

  • Brit Mollenhauer , MD

    Co-PI (Core Leadership): Team Schlossmacher

    University of Goettingen

  • Kathleen Poston, MD

    Stanford University

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    John Seibyl

  • Tanya Simuni, MD

    Northwestern University

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    Caroline M. Tanner

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    Daniel Weintraub

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    Aleksandar Videnovic

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    Seung Ho Choi

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    Ryan Kurth

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    Chelsea Caspell-Garcia

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    Christopher S. Coffey

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    Mark Frasier

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    Luis M. A. Oliveira

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    Samantha J. Hutten

  • Todd Sherer, PhD

    Michael J. Fox Foundation

  • Ken Marek, MD

    University of California, San Diego

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    Claudio Soto

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    Parkinson's Progression Markers Initiative