Evidence map›Paper›PMID 26511451›Full record

ArticleNeurology2015

Increased CSF biomarkers of angiogenesis in Parkinson disease.

Shorena Janelidze, Daniel Lindqvist, Veronica Francardo, Sara Hall, Henrik Zetterberg, Kaj Blennow, Charles H Adler, Thomas G Beach, Geidy E Serrano, Danielle van Westen and 3 more

Open access · hybridAbstract read
In one paragraph

Article in Neurology, 2015. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 90 papers, 2 of them syntheses that pooled it.

0numbers the graph read from it
0cells of the map it votes in
90citing papers in PubMed, 2 pooled it
7.2field-weighted citation impact, top 2% of its field
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

90 citing papers in PubMed, 2 syntheses or guidelines pooled it, 147 citations in OpenAlex.

  1. Pooled it
  2. Pooled it
  3. Review
  4. Review
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  6. Observational
  7. Review
  8. Plasma Metabolomics Profiles in Prodromal and Clinical Parkinson's Disease.Movement disorders : official journal of the Movement Disorder Society · 2025
    Article
  9. Review
  10. Article
  11. Article
  12. Review
  13. Article
  14. Review
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  16. Biomarkers of blood-brain barrier and neurovascular unit integrity in human cognitive impairment and dementia.Alzheimer's & dementia : the journal of the Alzheimer's Association · 2025
    Review
  17. Review
  18. Article
  19. Review
  20. Article

30 more citing papers are in PubMed but not listed here.

4 · The record

Corrections and comments

5 · Who and what money

Authors and funding

13 authors at 3 institutions in 2 countries.

Shorena JanelidzeFrom the Clinical Memory Research Unit, Department of Clinical Sciences (S.J., E.L., O.H.), Lund University, Malmö; the Department of Clinical Sciences (D.L., S.H.), Division of Psychiatry (D.L.), Department of Experimental Medical Science (V.F., M.A.C.), and Clinical Sciences, Diagnostic Radiology (D.v.W.), Lund University, Lund; Psychiatry Skåne (D.L.), Lund; the Department of Neurology (S.H.) and Memory Clinic (E.L., O.H.), Skåne University Hospital, Lund; Institute of Neuroscience and Physiology (H.Z., K.B.), Department of Psychiatry and Neurochemistry, the Sahlgrenska Academy at the University of Gothenburg, Mölndal, Sweden; UCL Institute of Neurology (H.Z.), London, UK; The Torsten Söderberg Professorship in Medicine at the Royal Swedish Academy of Sciences (K.B.), Stockholm, Sweden; Department of Neurology (C.H.A.), Mayo Clinic, Scottsdale; Banner Sun Health Research Institute (T.G.B., G.E.S.), Sun City, AZ; and Imaging and Function (D.v.W.), Skåne University Health Care, Lund, Sweden.
Daniel LindqvistFrom the Clinical Memory Research Unit, Department of Clinical Sciences (S.J., E.L., O.H.), Lund University, Malmö; the Department of Clinical Sciences (D.L., S.H.), Division of Psychiatry (D.L.), Department of Experimental Medical Science (V.F., M.A.C.), and Clinical Sciences, Diagnostic Radiology (D.v.W.), Lund University, Lund; Psychiatry Skåne (D.L.), Lund; the Department of Neurology (S.H.) and Memory Clinic (E.L., O.H.), Skåne University Hospital, Lund; Institute of Neuroscience and Physiology (H.Z., K.B.), Department of Psychiatry and Neurochemistry, the Sahlgrenska Academy at the University of Gothenburg, Mölndal, Sweden; UCL Institute of Neurology (H.Z.), London, UK; The Torsten Söderberg Professorship in Medicine at the Royal Swedish Academy of Sciences (K.B.), Stockholm, Sweden; Department of Neurology (C.H.A.), Mayo Clinic, Scottsdale; Banner Sun Health Research Institute (T.G.B., G.E.S.), Sun City, AZ; and Imaging and Function (D.v.W.), Skåne University Health Care, Lund, Sweden. Daniel.Lindqvist@med.lu.se.
Veronica FrancardoFrom the Clinical Memory Research Unit, Department of Clinical Sciences (S.J., E.L., O.H.), Lund University, Malmö; the Department of Clinical Sciences (D.L., S.H.), Division of Psychiatry (D.L.), Department of Experimental Medical Science (V.F., M.A.C.), and Clinical Sciences, Diagnostic Radiology (D.v.W.), Lund University, Lund; Psychiatry Skåne (D.L.), Lund; the Department of Neurology (S.H.) and Memory Clinic (E.L., O.H.), Skåne University Hospital, Lund; Institute of Neuroscience and Physiology (H.Z., K.B.), Department of Psychiatry and Neurochemistry, the Sahlgrenska Academy at the University of Gothenburg, Mölndal, Sweden; UCL Institute of Neurology (H.Z.), London, UK; The Torsten Söderberg Professorship in Medicine at the Royal Swedish Academy of Sciences (K.B.), Stockholm, Sweden; Department of Neurology (C.H.A.), Mayo Clinic, Scottsdale; Banner Sun Health Research Institute (T.G.B., G.E.S.), Sun City, AZ; and Imaging and Function (D.v.W.), Skåne University Health Care, Lund, Sweden.
Sara HallFrom the Clinical Memory Research Unit, Department of Clinical Sciences (S.J., E.L., O.H.), Lund University, Malmö; the Department of Clinical Sciences (D.L., S.H.), Division of Psychiatry (D.L.), Department of Experimental Medical Science (V.F., M.A.C.), and Clinical Sciences, Diagnostic Radiology (D.v.W.), Lund University, Lund; Psychiatry Skåne (D.L.), Lund; the Department of Neurology (S.H.) and Memory Clinic (E.L., O.H.), Skåne University Hospital, Lund; Institute of Neuroscience and Physiology (H.Z., K.B.), Department of Psychiatry and Neurochemistry, the Sahlgrenska Academy at the University of Gothenburg, Mölndal, Sweden; UCL Institute of Neurology (H.Z.), London, UK; The Torsten Söderberg Professorship in Medicine at the Royal Swedish Academy of Sciences (K.B.), Stockholm, Sweden; Department of Neurology (C.H.A.), Mayo Clinic, Scottsdale; Banner Sun Health Research Institute (T.G.B., G.E.S.), Sun City, AZ; and Imaging and Function (D.v.W.), Skåne University Health Care, Lund, Sweden.
Henrik ZetterbergFrom the Clinical Memory Research Unit, Department of Clinical Sciences (S.J., E.L., O.H.), Lund University, Malmö; the Department of Clinical Sciences (D.L., S.H.), Division of Psychiatry (D.L.), Department of Experimental Medical Science (V.F., M.A.C.), and Clinical Sciences, Diagnostic Radiology (D.v.W.), Lund University, Lund; Psychiatry Skåne (D.L.), Lund; the Department of Neurology (S.H.) and Memory Clinic (E.L., O.H.), Skåne University Hospital, Lund; Institute of Neuroscience and Physiology (H.Z., K.B.), Department of Psychiatry and Neurochemistry, the Sahlgrenska Academy at the University of Gothenburg, Mölndal, Sweden; UCL Institute of Neurology (H.Z.), London, UK; The Torsten Söderberg Professorship in Medicine at the Royal Swedish Academy of Sciences (K.B.), Stockholm, Sweden; Department of Neurology (C.H.A.), Mayo Clinic, Scottsdale; Banner Sun Health Research Institute (T.G.B., G.E.S.), Sun City, AZ; and Imaging and Function (D.v.W.), Skåne University Health Care, Lund, Sweden.
Kaj BlennowFrom the Clinical Memory Research Unit, Department of Clinical Sciences (S.J., E.L., O.H.), Lund University, Malmö; the Department of Clinical Sciences (D.L., S.H.), Division of Psychiatry (D.L.), Department of Experimental Medical Science (V.F., M.A.C.), and Clinical Sciences, Diagnostic Radiology (D.v.W.), Lund University, Lund; Psychiatry Skåne (D.L.), Lund; the Department of Neurology (S.H.) and Memory Clinic (E.L., O.H.), Skåne University Hospital, Lund; Institute of Neuroscience and Physiology (H.Z., K.B.), Department of Psychiatry and Neurochemistry, the Sahlgrenska Academy at the University of Gothenburg, Mölndal, Sweden; UCL Institute of Neurology (H.Z.), London, UK; The Torsten Söderberg Professorship in Medicine at the Royal Swedish Academy of Sciences (K.B.), Stockholm, Sweden; Department of Neurology (C.H.A.), Mayo Clinic, Scottsdale; Banner Sun Health Research Institute (T.G.B., G.E.S.), Sun City, AZ; and Imaging and Function (D.v.W.), Skåne University Health Care, Lund, Sweden.
Charles H AdlerFrom the Clinical Memory Research Unit, Department of Clinical Sciences (S.J., E.L., O.H.), Lund University, Malmö; the Department of Clinical Sciences (D.L., S.H.), Division of Psychiatry (D.L.), Department of Experimental Medical Science (V.F., M.A.C.), and Clinical Sciences, Diagnostic Radiology (D.v.W.), Lund University, Lund; Psychiatry Skåne (D.L.), Lund; the Department of Neurology (S.H.) and Memory Clinic (E.L., O.H.), Skåne University Hospital, Lund; Institute of Neuroscience and Physiology (H.Z., K.B.), Department of Psychiatry and Neurochemistry, the Sahlgrenska Academy at the University of Gothenburg, Mölndal, Sweden; UCL Institute of Neurology (H.Z.), London, UK; The Torsten Söderberg Professorship in Medicine at the Royal Swedish Academy of Sciences (K.B.), Stockholm, Sweden; Department of Neurology (C.H.A.), Mayo Clinic, Scottsdale; Banner Sun Health Research Institute (T.G.B., G.E.S.), Sun City, AZ; and Imaging and Function (D.v.W.), Skåne University Health Care, Lund, Sweden.
Thomas G BeachFrom the Clinical Memory Research Unit, Department of Clinical Sciences (S.J., E.L., O.H.), Lund University, Malmö; the Department of Clinical Sciences (D.L., S.H.), Division of Psychiatry (D.L.), Department of Experimental Medical Science (V.F., M.A.C.), and Clinical Sciences, Diagnostic Radiology (D.v.W.), Lund University, Lund; Psychiatry Skåne (D.L.), Lund; the Department of Neurology (S.H.) and Memory Clinic (E.L., O.H.), Skåne University Hospital, Lund; Institute of Neuroscience and Physiology (H.Z., K.B.), Department of Psychiatry and Neurochemistry, the Sahlgrenska Academy at the University of Gothenburg, Mölndal, Sweden; UCL Institute of Neurology (H.Z.), London, UK; The Torsten Söderberg Professorship in Medicine at the Royal Swedish Academy of Sciences (K.B.), Stockholm, Sweden; Department of Neurology (C.H.A.), Mayo Clinic, Scottsdale; Banner Sun Health Research Institute (T.G.B., G.E.S.), Sun City, AZ; and Imaging and Function (D.v.W.), Skåne University Health Care, Lund, Sweden.
Geidy E SerranoFrom the Clinical Memory Research Unit, Department of Clinical Sciences (S.J., E.L., O.H.), Lund University, Malmö; the Department of Clinical Sciences (D.L., S.H.), Division of Psychiatry (D.L.), Department of Experimental Medical Science (V.F., M.A.C.), and Clinical Sciences, Diagnostic Radiology (D.v.W.), Lund University, Lund; Psychiatry Skåne (D.L.), Lund; the Department of Neurology (S.H.) and Memory Clinic (E.L., O.H.), Skåne University Hospital, Lund; Institute of Neuroscience and Physiology (H.Z., K.B.), Department of Psychiatry and Neurochemistry, the Sahlgrenska Academy at the University of Gothenburg, Mölndal, Sweden; UCL Institute of Neurology (H.Z.), London, UK; The Torsten Söderberg Professorship in Medicine at the Royal Swedish Academy of Sciences (K.B.), Stockholm, Sweden; Department of Neurology (C.H.A.), Mayo Clinic, Scottsdale; Banner Sun Health Research Institute (T.G.B., G.E.S.), Sun City, AZ; and Imaging and Function (D.v.W.), Skåne University Health Care, Lund, Sweden.
Danielle van WestenFrom the Clinical Memory Research Unit, Department of Clinical Sciences (S.J., E.L., O.H.), Lund University, Malmö; the Department of Clinical Sciences (D.L., S.H.), Division of Psychiatry (D.L.), Department of Experimental Medical Science (V.F., M.A.C.), and Clinical Sciences, Diagnostic Radiology (D.v.W.), Lund University, Lund; Psychiatry Skåne (D.L.), Lund; the Department of Neurology (S.H.) and Memory Clinic (E.L., O.H.), Skåne University Hospital, Lund; Institute of Neuroscience and Physiology (H.Z., K.B.), Department of Psychiatry and Neurochemistry, the Sahlgrenska Academy at the University of Gothenburg, Mölndal, Sweden; UCL Institute of Neurology (H.Z.), London, UK; The Torsten Söderberg Professorship in Medicine at the Royal Swedish Academy of Sciences (K.B.), Stockholm, Sweden; Department of Neurology (C.H.A.), Mayo Clinic, Scottsdale; Banner Sun Health Research Institute (T.G.B., G.E.S.), Sun City, AZ; and Imaging and Function (D.v.W.), Skåne University Health Care, Lund, Sweden.
Elisabet LondosFrom the Clinical Memory Research Unit, Department of Clinical Sciences (S.J., E.L., O.H.), Lund University, Malmö; the Department of Clinical Sciences (D.L., S.H.), Division of Psychiatry (D.L.), Department of Experimental Medical Science (V.F., M.A.C.), and Clinical Sciences, Diagnostic Radiology (D.v.W.), Lund University, Lund; Psychiatry Skåne (D.L.), Lund; the Department of Neurology (S.H.) and Memory Clinic (E.L., O.H.), Skåne University Hospital, Lund; Institute of Neuroscience and Physiology (H.Z., K.B.), Department of Psychiatry and Neurochemistry, the Sahlgrenska Academy at the University of Gothenburg, Mölndal, Sweden; UCL Institute of Neurology (H.Z.), London, UK; The Torsten Söderberg Professorship in Medicine at the Royal Swedish Academy of Sciences (K.B.), Stockholm, Sweden; Department of Neurology (C.H.A.), Mayo Clinic, Scottsdale; Banner Sun Health Research Institute (T.G.B., G.E.S.), Sun City, AZ; and Imaging and Function (D.v.W.), Skåne University Health Care, Lund, Sweden.
M Angela CenciFrom the Clinical Memory Research Unit, Department of Clinical Sciences (S.J., E.L., O.H.), Lund University, Malmö; the Department of Clinical Sciences (D.L., S.H.), Division of Psychiatry (D.L.), Department of Experimental Medical Science (V.F., M.A.C.), and Clinical Sciences, Diagnostic Radiology (D.v.W.), Lund University, Lund; Psychiatry Skåne (D.L.), Lund; the Department of Neurology (S.H.) and Memory Clinic (E.L., O.H.), Skåne University Hospital, Lund; Institute of Neuroscience and Physiology (H.Z., K.B.), Department of Psychiatry and Neurochemistry, the Sahlgrenska Academy at the University of Gothenburg, Mölndal, Sweden; UCL Institute of Neurology (H.Z.), London, UK; The Torsten Söderberg Professorship in Medicine at the Royal Swedish Academy of Sciences (K.B.), Stockholm, Sweden; Department of Neurology (C.H.A.), Mayo Clinic, Scottsdale; Banner Sun Health Research Institute (T.G.B., G.E.S.), Sun City, AZ; and Imaging and Function (D.v.W.), Skåne University Health Care, Lund, Sweden.
Oskar HanssonFrom the Clinical Memory Research Unit, Department of Clinical Sciences (S.J., E.L., O.H.), Lund University, Malmö; the Department of Clinical Sciences (D.L., S.H.), Division of Psychiatry (D.L.), Department of Experimental Medical Science (V.F., M.A.C.), and Clinical Sciences, Diagnostic Radiology (D.v.W.), Lund University, Lund; Psychiatry Skåne (D.L.), Lund; the Department of Neurology (S.H.) and Memory Clinic (E.L., O.H.), Skåne University Hospital, Lund; Institute of Neuroscience and Physiology (H.Z., K.B.), Department of Psychiatry and Neurochemistry, the Sahlgrenska Academy at the University of Gothenburg, Mölndal, Sweden; UCL Institute of Neurology (H.Z.), London, UK; The Torsten Söderberg Professorship in Medicine at the Royal Swedish Academy of Sciences (K.B.), Stockholm, Sweden; Department of Neurology (C.H.A.), Mayo Clinic, Scottsdale; Banner Sun Health Research Institute (T.G.B., G.E.S.), Sun City, AZ; and Imaging and Function (D.v.W.), Skåne University Health Care, Lund, Sweden.
University College London · GBBanner Sun Health Research Institute · USMayo Clinic in Arizona · US

Funding

Research Education ComponentP30AG019610 · NIA · SUN HEALTH RESEARCH INSTITUTE · PI REIMAN, ERIC MICHAEL · 2001 to 2020
$32.5M
National Brain and Tissue Resource for Parkinson's Disease and Related DisordersU24NS072026 · NINDS · BANNER SUN HEALTH RESEARCH INSTITUTE · PI BEACH, THOMAS G · 2011 to 2015
$7.8M
NIA NIH HHS P30 AG019610NIA NIH HHS P30 AG19610NINDS NIH HHS U24 NS072026
6 · The paper itself

Abstract

objectiveTo study biomarkers of angiogenesis in Parkinson disease (PD), and how these are associated with clinical characteristics, blood-brain barrier (BBB) permeability, and cerebrovascular disease.

methodsIn this cross-sectional analysis, 38 elderly controls and 100 patients with PD (82 without dementia and 18 with dementia) were included from the prospective Swedish BioFinder study. CSF samples were analyzed for the angiogenesis biomarkers vascular endothelial growth factor (VEGF); its receptors, VEGFR-1 and VEGFR-2; placental growth factor (PlGF); angiopoietin 2 (Ang2); and interleukin-8. BBB permeability, white matter lesions (WMLs), and cerebral microbleeds (CMB) were assessed. CSF angiogenesis biomarkers were also measured in 2 validation cohorts: (1) 64 controls and 87 patients with PD with dementia; and (2) 35 controls and 93 patients with neuropathologically confirmed diagnosis of PD with and without dementia.

resultsPatients with PD without dementia displayed higher CSF levels of VEGF, PlGF, and sVEGFR-2, and lower levels of Ang2, compared to controls. Similar alterations in VEGF, PlGF, and Ang2 levels were observed in patients with PD with dementia. Angiogenesis markers were associated with gait difficulties and orthostatic hypotension as well as with more pronounced BBB permeability, WMLs, and CMB. Moreover, higher levels of VEGF and PlGF levels were associated with increased CSF levels of neurofilament light (a marker of neurodegeneration) and monocyte chemotactic protein-1 (a marker of glial activation). The main results were validated in the 2 additional cohorts.

conclusionsCSF biomarkers of angiogenesis are increased in PD, and they are associated with gait difficulties, BBB dysfunction, WMLs, and CMB. Abnormal angiogenesis may be important in PD pathogenesis and contribute to dopa-resistant symptoms.

Indexed as

AgedAngiogenesis Inducing AgentsBiomarkersCohort StudiesCross-Sectional StudiesFemaleHumansMaleMiddle AgedNeovascularization, PathologicParkinson DiseaseProspective StudiesReproducibility of ResultsAngiogenesis Inducing AgentsBiomarkers

Identifiers

PMID26511451
PMCPMC4662706
OpenAlexW2173706022

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