Blood-brain barrier breakdown, neuroinflammation, and cognitive decline in older adults

Blood-brain barrier (BBB) breakdown is observed in older versus younger adults and in late-onset Alzheimer's disease versus age-matched controls, but its causes and consequences in aging are unclear. We tested the hypothesis that BBB breakdown is associated with cognitive decline and inflammati...

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Published inAlzheimer's & dementia Vol. 14; no. 12; pp. 1640 - 1650
Main Authors Bowman, Gene L., Dayon, Loïc, Kirkland, Richard, Wojcik, Jérôme, Peyratout, Gwendoline, Severin, India C., Henry, Hugues, Oikonomidi, Aikaterini, Migliavacca, Eugenia, Bacher, Michael, Popp, Julius
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 01.12.2018
Subjects
Aged
Angiogenesis
Apolipoprotein E4 - genetics
Biomarkers
Biomarkers - blood
Biomarkers - cerebrospinal fluid
Blood-Brain Barrier - metabolism
Cerebrovascular Disorders - blood
Cerebrovascular Disorders - cerebrospinal fluid
Cerebrovascular Disorders - immunology
Chemokines
Cognitive Dysfunction - blood
Cognitive Dysfunction - cerebrospinal fluid
Cognitive Dysfunction - immunology
Cohort Studies
CSF
Cytokines
Disease Progression
Elderly
Female
HDL metabolism
Humans
IL-16
IL-8
Inflammation - blood
Inflammation - cerebrospinal fluid
Inflammation - immunology
Male
MDC
Mild cognitive impairment
Neuropsychological Tests
Neurovascular unit
Serum
Serum amyloid A
sICAM-1
VEGF
Cytokines
Mild cognitive impairment
VEGF
IL-16
IL-8
HDL metabolism
MDC
sICAM-1
Serum amyloid A
Angiogenesis
CSF
Biomarkers
Serum
Neurovascular unit
Elderly
Chemokines
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Abstract Blood-brain barrier (BBB) breakdown is observed in older versus younger adults and in late-onset Alzheimer's disease versus age-matched controls, but its causes and consequences in aging are unclear. We tested the hypothesis that BBB breakdown is associated with cognitive decline and inflammation in nondemented elders. Cerebrospinal fluid and serum inflammatory markers were measured using sandwich immunoassays in 120 subjects. Least Absolute Shrinkage and Selection Operator-logistic regression selected cerebrospinal fluid and serum signatures that best classified BBB impairment defined by the cerebrospinal fluid albumin index ≥9. Linear regression examined changes in Clinical Dementia Rating sum of boxes as a function of BBB integrity at baseline. Mean age was 70 years, mean Mini–Mental State Examination was 27, and BBB impairment was recorded in 13.5%. BBB breakdown was associated with cognitive decline (P = .015). Cerebrospinal fluid intercellular adhesion molecule-1, vascular endothelial growth factor, interleukin-8, serum amyloid A, macrophage derived chemokine, and gender generated an area under the curve of 0.95 for BBB impairment, and serum IL-16, VEGF-D, IL-15, and other variables generated an AUC of 0.92 for BBB impairment. BBB breakdown is associated with more rapid cognitive decline. Inflammatory mechanisms, including cell adhesion, neutrophil migration, lipid metabolism, and angiogenesis may be implicated.
AbstractList Blood-brain barrier (BBB) breakdown is observed in older versus younger adults and in late-onset Alzheimer's disease versus age-matched controls, but its causes and consequences in aging are unclear. We tested the hypothesis that BBB breakdown is associated with cognitive decline and inflammation in nondemented elders. Cerebrospinal fluid and serum inflammatory markers were measured using sandwich immunoassays in 120 subjects. Least Absolute Shrinkage and Selection Operator-logistic regression selected cerebrospinal fluid and serum signatures that best classified BBB impairment defined by the cerebrospinal fluid albumin index ≥9. Linear regression examined changes in Clinical Dementia Rating sum of boxes as a function of BBB integrity at baseline. Mean age was 70 years, mean Mini–Mental State Examination was 27, and BBB impairment was recorded in 13.5%. BBB breakdown was associated with cognitive decline (P = .015). Cerebrospinal fluid intercellular adhesion molecule-1, vascular endothelial growth factor, interleukin-8, serum amyloid A, macrophage derived chemokine, and gender generated an area under the curve of 0.95 for BBB impairment, and serum IL-16, VEGF-D, IL-15, and other variables generated an AUC of 0.92 for BBB impairment. BBB breakdown is associated with more rapid cognitive decline. Inflammatory mechanisms, including cell adhesion, neutrophil migration, lipid metabolism, and angiogenesis may be implicated.
Introduction Blood‐brain barrier (BBB) breakdown is observed in older versus younger adults and in late‐onset Alzheimer's disease versus age‐matched controls, but its causes and consequences in aging are unclear. We tested the hypothesis that BBB breakdown is associated with cognitive decline and inflammation in nondemented elders. Methods Cerebrospinal fluid and serum inflammatory markers were measured using sandwich immunoassays in 120 subjects. Least Absolute Shrinkage and Selection Operator‐logistic regression selected cerebrospinal fluid and serum signatures that best classified BBB impairment defined by the cerebrospinal fluid albumin index ≥9. Linear regression examined changes in Clinical Dementia Rating sum of boxes as a function of BBB integrity at baseline. Results Mean age was 70 years, mean Mini–Mental State Examination was 27, and BBB impairment was recorded in 13.5%. BBB breakdown was associated with cognitive decline (P = .015). Cerebrospinal fluid intercellular adhesion molecule‐1, vascular endothelial growth factor, interleukin‐8, serum amyloid A, macrophage derived chemokine, and gender generated an area under the curve of 0.95 for BBB impairment, and serum IL‐16, VEGF‐D, IL‐15, and other variables generated an AUC of 0.92 for BBB impairment. Discussion BBB breakdown is associated with more rapid cognitive decline. Inflammatory mechanisms, including cell adhesion, neutrophil migration, lipid metabolism, and angiogenesis may be implicated.
Blood-brain barrier (BBB) breakdown is observed in older versus younger adults and in late-onset Alzheimer's disease versus age-matched controls, but its causes and consequences in aging are unclear. We tested the hypothesis that BBB breakdown is associated with cognitive decline and inflammation in nondemented elders.INTRODUCTIONBlood-brain barrier (BBB) breakdown is observed in older versus younger adults and in late-onset Alzheimer's disease versus age-matched controls, but its causes and consequences in aging are unclear. We tested the hypothesis that BBB breakdown is associated with cognitive decline and inflammation in nondemented elders.Cerebrospinal fluid and serum inflammatory markers were measured using sandwich immunoassays in 120 subjects. Least Absolute Shrinkage and Selection Operator-logistic regression selected cerebrospinal fluid and serum signatures that best classified BBB impairment defined by the cerebrospinal fluid albumin index ≥9. Linear regression examined changes in Clinical Dementia Rating sum of boxes as a function of BBB integrity at baseline.METHODSCerebrospinal fluid and serum inflammatory markers were measured using sandwich immunoassays in 120 subjects. Least Absolute Shrinkage and Selection Operator-logistic regression selected cerebrospinal fluid and serum signatures that best classified BBB impairment defined by the cerebrospinal fluid albumin index ≥9. Linear regression examined changes in Clinical Dementia Rating sum of boxes as a function of BBB integrity at baseline.Mean age was 70 years, mean Mini–Mental State Examination was 27, and BBB impairment was recorded in 13.5%. BBB breakdown was associated with cognitive decline (P = .015). Cerebrospinal fluid intercellular adhesion molecule-1, vascular endothelial growth factor, interleukin-8, serum amyloid A, macrophage derived chemokine, and gender generated an area under the curve of 0.95 for BBB impairment, and serum IL-16, VEGF-D, IL-15, and other variables generated an AUC of 0.92 for BBB impairment.RESULTSMean age was 70 years, mean Mini–Mental State Examination was 27, and BBB impairment was recorded in 13.5%. BBB breakdown was associated with cognitive decline (P = .015). Cerebrospinal fluid intercellular adhesion molecule-1, vascular endothelial growth factor, interleukin-8, serum amyloid A, macrophage derived chemokine, and gender generated an area under the curve of 0.95 for BBB impairment, and serum IL-16, VEGF-D, IL-15, and other variables generated an AUC of 0.92 for BBB impairment.BBB breakdown is associated with more rapid cognitive decline. Inflammatory mechanisms, including cell adhesion, neutrophil migration, lipid metabolism, and angiogenesis may be implicated.DISCUSSIONBBB breakdown is associated with more rapid cognitive decline. Inflammatory mechanisms, including cell adhesion, neutrophil migration, lipid metabolism, and angiogenesis may be implicated.
Blood-brain barrier (BBB) breakdown is observed in older versus younger adults and in late-onset Alzheimer's disease versus age-matched controls, but its causes and consequences in aging are unclear. We tested the hypothesis that BBB breakdown is associated with cognitive decline and inflammation in nondemented elders. Cerebrospinal fluid and serum inflammatory markers were measured using sandwich immunoassays in 120 subjects. Least Absolute Shrinkage and Selection Operator-logistic regression selected cerebrospinal fluid and serum signatures that best classified BBB impairment defined by the cerebrospinal fluid albumin index ≥9. Linear regression examined changes in Clinical Dementia Rating sum of boxes as a function of BBB integrity at baseline. Mean age was 70 years, mean Mini–Mental State Examination was 27, and BBB impairment was recorded in 13.5%. BBB breakdown was associated with cognitive decline (P = .015). Cerebrospinal fluid intercellular adhesion molecule-1, vascular endothelial growth factor, interleukin-8, serum amyloid A, macrophage derived chemokine, and gender generated an area under the curve of 0.95 for BBB impairment, and serum IL-16, VEGF-D, IL-15, and other variables generated an AUC of 0.92 for BBB impairment. BBB breakdown is associated with more rapid cognitive decline. Inflammatory mechanisms, including cell adhesion, neutrophil migration, lipid metabolism, and angiogenesis may be implicated.
Author Migliavacca, Eugenia
Kirkland, Richard
Wojcik, Jérôme
Peyratout, Gwendoline
Severin, India C.
Oikonomidi, Aikaterini
Bacher, Michael
Popp, Julius
Dayon, Loïc
Henry, Hugues
Bowman, Gene L.
Author_xml – sequence: 1
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  surname: Bowman
  fullname: Bowman, Gene L.
  email: genebowman@hsl.harvard.edu
  organization: Nestlé Institute of Health Sciences, EPFL Campus, Lausanne, Switzerland
– sequence: 2
  givenname: Loïc
  surname: Dayon
  fullname: Dayon, Loïc
  organization: Nestlé Institute of Health Sciences, EPFL Campus, Lausanne, Switzerland
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  givenname: Richard
  surname: Kirkland
  fullname: Kirkland, Richard
  organization: Nestlé Health Science, Prometheus Laboratories, San Diego, CA, USA
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  givenname: Jérôme
  surname: Wojcik
  fullname: Wojcik, Jérôme
  organization: Precision for Medicine, Geneva, Switzerland
– sequence: 5
  givenname: Gwendoline
  surname: Peyratout
  fullname: Peyratout, Gwendoline
  organization: Old Age Psychiatry, Department of Psychiatry, University Hospital of Lausanne, Lausanne, Switzerland
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  givenname: India C.
  surname: Severin
  fullname: Severin, India C.
  organization: Nestlé Institute of Health Sciences, EPFL Campus, Lausanne, Switzerland
– sequence: 7
  givenname: Hugues
  surname: Henry
  fullname: Henry, Hugues
  organization: CHUV Department of Laboratories, Lausanne, Switzerland
– sequence: 8
  givenname: Aikaterini
  surname: Oikonomidi
  fullname: Oikonomidi, Aikaterini
  organization: Old Age Psychiatry, Department of Psychiatry, University Hospital of Lausanne, Lausanne, Switzerland
– sequence: 9
  givenname: Eugenia
  surname: Migliavacca
  fullname: Migliavacca, Eugenia
  organization: Nestlé Institute of Health Sciences, EPFL Campus, Lausanne, Switzerland
– sequence: 10
  givenname: Michael
  surname: Bacher
  fullname: Bacher, Michael
  organization: Philipps University of Marburg, Institute of Immunology, Marburg, Germany
– sequence: 11
  givenname: Julius
  surname: Popp
  fullname: Popp, Julius
  organization: Old Age Psychiatry, Department of Psychiatry, University Hospital of Lausanne, Lausanne, Switzerland
BackLink https://www.ncbi.nlm.nih.gov/pubmed/30120040$$D View this record in MEDLINE/PubMed
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Issue 12
Keywords Cytokines
Mild cognitive impairment
VEGF
IL-16
IL-8
HDL metabolism
MDC
sICAM-1
Serum amyloid A
Angiogenesis
CSF
Biomarkers
Serum
Neurovascular unit
Elderly
Chemokines
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Snippet Blood-brain barrier (BBB) breakdown is observed in older versus younger adults and in late-onset Alzheimer's disease versus age-matched controls, but its...
Introduction Blood‐brain barrier (BBB) breakdown is observed in older versus younger adults and in late‐onset Alzheimer's disease versus age‐matched controls,...
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SubjectTerms Aged
Angiogenesis
Apolipoprotein E4 - genetics
Biomarkers
Biomarkers - blood
Biomarkers - cerebrospinal fluid
Blood-Brain Barrier - metabolism
Cerebrovascular Disorders - blood
Cerebrovascular Disorders - cerebrospinal fluid
Cerebrovascular Disorders - immunology
Chemokines
Cognitive Dysfunction - blood
Cognitive Dysfunction - cerebrospinal fluid
Cognitive Dysfunction - immunology
Cohort Studies
CSF
Cytokines
Disease Progression
Elderly
Female
HDL metabolism
Humans
IL-16
IL-8
Inflammation - blood
Inflammation - cerebrospinal fluid
Inflammation - immunology
Male
MDC
Mild cognitive impairment
Neuropsychological Tests
Neurovascular unit
Serum
Serum amyloid A
sICAM-1
VEGF
Title Blood-brain barrier breakdown, neuroinflammation, and cognitive decline in older adults
URI https://dx.doi.org/10.1016/j.jalz.2018.06.2857
https://onlinelibrary.wiley.com/doi/abs/10.1016%2Fj.jalz.2018.06.2857
https://www.ncbi.nlm.nih.gov/pubmed/30120040
https://www.proquest.com/docview/2089860506
Volume 14
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