Stool Immune Profiles Evince Gastrointestinal Inflammation in Parkinson's Disease

Background: Gastrointestinal symptoms are common in Parkinson's disease and frequently precede the development of motor impairments. Intestinal inflammation has been proposed as a driver of disease pathology, and evaluation of inflammatory mediators in stool could possibly identify valuable ear...

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Published inMovement disorders Vol. 33; no. 5; pp. 793 - 804
Main Authors Houser, Madelyn C., Chang, Jianjun, Factor, Stewart A., Molho, Eric S., Zabetian, Cyrus P., Hill‐Burns, Erin M., Payami, Haydeh, Hertzberg, Vicki S., Tansey, Malú G.
Format Journal Article
LanguageEnglish
Published United States Wiley Subscription Services, Inc 01.05.2018
Subjects
Online AccessGet full text
ISSN0885-3185
1531-8257
1531-8257
DOI10.1002/mds.27326

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Abstract Background: Gastrointestinal symptoms are common in Parkinson's disease and frequently precede the development of motor impairments. Intestinal inflammation has been proposed as a driver of disease pathology, and evaluation of inflammatory mediators in stool could possibly identify valuable early‐stage biomarkers. We measured immune‐ and angiogenesis‐related proteins in human stool to examine inflammatory profiles associated with Parkinson's disease. Methods: Stool samples and subjects' self‐reported metadata were obtained from 156 individuals with Parkinson's disease and 110 without, including spouse and nonhousehold controls. Metadata were probed for disease‐associated differences, and levels of 37 immune and angiogenesis factors in stool homogenates were measured by multiplexed immunoassay and compared across experimental groups. Results: Parkinson's disease patients reported greater incidence of intestinal disease and digestive problems than controls. Direct comparison of levels of stool analytes in patients and controls revealed elevated vascular endothelial growth factor receptor 1, interleukin‐1α, and CXCL8 in patients' stool. Paired comparison of patients and spouses suggested higher levels of multiple factors in patients, but this was complicated by sex differences. Sex, body mass index, a history of smoking, and use of probiotics were found to strongly influence levels of stool analytes. Multivariate analysis accounting for these and other potential confounders confirmed elevated levels of interleukin‐1α and CXCL8 and also revealed increased interleukin‐1β and C‐reactive protein in stool in Parkinson's disease. These differences were not dependent on subject age or disease duration. Conclusions: Levels of stool immune factors indicate that intestinal inflammation is present in patients with Parkinson's disease. © 2018 International Parkinson and Movement Disorder Society
AbstractList Gastrointestinal symptoms are common in Parkinson's disease and frequently precede the development of motor impairments. Intestinal inflammation has been proposed as a driver of disease pathology, and evaluation of inflammatory mediators in stool could possibly identify valuable early-stage biomarkers. We measured immune- and angiogenesis-related proteins in human stool to examine inflammatory profiles associated with Parkinson's disease. Stool samples and subjects' self-reported metadata were obtained from 156 individuals with Parkinson's disease and 110 without, including spouse and nonhousehold controls. Metadata were probed for disease-associated differences, and levels of 37 immune and angiogenesis factors in stool homogenates were measured by multiplexed immunoassay and compared across experimental groups. Parkinson's disease patients reported greater incidence of intestinal disease and digestive problems than controls. Direct comparison of levels of stool analytes in patients and controls revealed elevated vascular endothelial growth factor receptor 1, interleukin-1α, and CXCL8 in patients' stool. Paired comparison of patients and spouses suggested higher levels of multiple factors in patients, but this was complicated by sex differences. Sex, body mass index, a history of smoking, and use of probiotics were found to strongly influence levels of stool analytes. Multivariate analysis accounting for these and other potential confounders confirmed elevated levels of interleukin-1α and CXCL8 and also revealed increased interleukin-1β and C-reactive protein in stool in Parkinson's disease. These differences were not dependent on subject age or disease duration. Levels of stool immune factors indicate that intestinal inflammation is present in patients with Parkinson's disease. © 2018 International Parkinson and Movement Disorder Society.
Background: Gastrointestinal symptoms are common in Parkinson's disease and frequently precede the development of motor impairments. Intestinal inflammation has been proposed as a driver of disease pathology, and evaluation of inflammatory mediators in stool could possibly identify valuable early‐stage biomarkers. We measured immune‐ and angiogenesis‐related proteins in human stool to examine inflammatory profiles associated with Parkinson's disease. Methods: Stool samples and subjects' self‐reported metadata were obtained from 156 individuals with Parkinson's disease and 110 without, including spouse and nonhousehold controls. Metadata were probed for disease‐associated differences, and levels of 37 immune and angiogenesis factors in stool homogenates were measured by multiplexed immunoassay and compared across experimental groups. Results: Parkinson's disease patients reported greater incidence of intestinal disease and digestive problems than controls. Direct comparison of levels of stool analytes in patients and controls revealed elevated vascular endothelial growth factor receptor 1, interleukin‐1α, and CXCL8 in patients' stool. Paired comparison of patients and spouses suggested higher levels of multiple factors in patients, but this was complicated by sex differences. Sex, body mass index, a history of smoking, and use of probiotics were found to strongly influence levels of stool analytes. Multivariate analysis accounting for these and other potential confounders confirmed elevated levels of interleukin‐1α and CXCL8 and also revealed increased interleukin‐1β and C‐reactive protein in stool in Parkinson's disease. These differences were not dependent on subject age or disease duration. Conclusions: Levels of stool immune factors indicate that intestinal inflammation is present in patients with Parkinson's disease. © 2018 International Parkinson and Movement Disorder Society
Background: Gastrointestinal symptoms are common in Parkinson's disease and frequently precede the development of motor impairments. Intestinal inflammation has been proposed as a driver of disease pathology, and evaluation of inflammatory mediators in stool could possibly identify valuable early‐stage biomarkers. We measured immune‐ and angiogenesis‐related proteins in human stool to examine inflammatory profiles associated with Parkinson's disease. Methods: Stool samples and subjects' self‐reported metadata were obtained from 156 individuals with Parkinson's disease and 110 without, including spouse and nonhousehold controls. Metadata were probed for disease‐associated differences, and levels of 37 immune and angiogenesis factors in stool homogenates were measured by multiplexed immunoassay and compared across experimental groups. Results: Parkinson's disease patients reported greater incidence of intestinal disease and digestive problems than controls. Direct comparison of levels of stool analytes in patients and controls revealed elevated vascular endothelial growth factor receptor 1, interleukin‐1α, and CXCL8 in patients' stool. Paired comparison of patients and spouses suggested higher levels of multiple factors in patients, but this was complicated by sex differences. Sex, body mass index, a history of smoking, and use of probiotics were found to strongly influence levels of stool analytes. Multivariate analysis accounting for these and other potential confounders confirmed elevated levels of interleukin‐1α and CXCL8 and also revealed increased interleukin‐1β and C‐reactive protein in stool in Parkinson's disease. These differences were not dependent on subject age or disease duration. Conclusions: Levels of stool immune factors indicate that intestinal inflammation is present in patients with Parkinson's disease. © 2018 International Parkinson and Movement Disorder Society
Background: Gastrointestinal symptoms are common in Parkinson's disease and frequently precede the development of motor impairments. Intestinal inflammation has been proposed as a driver of disease pathology, and evaluation of inflammatory mediators in stool could possibly identify valuable early‐stage biomarkers. We measured immune‐ and angiogenesis‐related proteins in human stool to examine inflammatory profiles associated with Parkinson's disease.Methods: Stool samples and subjects' self‐reported metadata were obtained from 156 individuals with Parkinson's disease and 110 without, including spouse and nonhousehold controls. Metadata were probed for disease‐associated differences, and levels of 37 immune and angiogenesis factors in stool homogenates were measured by multiplexed immunoassay and compared across experimental groups.Results: Parkinson's disease patients reported greater incidence of intestinal disease and digestive problems than controls. Direct comparison of levels of stool analytes in patients and controls revealed elevated vascular endothelial growth factor receptor 1, interleukin‐1α, and CXCL8 in patients' stool. Paired comparison of patients and spouses suggested higher levels of multiple factors in patients, but this was complicated by sex differences. Sex, body mass index, a history of smoking, and use of probiotics were found to strongly influence levels of stool analytes. Multivariate analysis accounting for these and other potential confounders confirmed elevated levels of interleukin‐1α and CXCL8 and also revealed increased interleukin‐1β and C‐reactive protein in stool in Parkinson's disease. These differences were not dependent on subject age or disease duration.Conclusions: Levels of stool immune factors indicate that intestinal inflammation is present in patients with Parkinson's disease. © 2018 International Parkinson and Movement Disorder Society
Gastrointestinal symptoms are common in Parkinson's disease and frequently precede the development of motor impairments. Intestinal inflammation has been proposed as a driver of disease pathology, and evaluation of inflammatory mediators in stool could possibly identify valuable early-stage biomarkers. We measured immune- and angiogenesis-related proteins in human stool to examine inflammatory profiles associated with Parkinson's disease.BACKGROUNDGastrointestinal symptoms are common in Parkinson's disease and frequently precede the development of motor impairments. Intestinal inflammation has been proposed as a driver of disease pathology, and evaluation of inflammatory mediators in stool could possibly identify valuable early-stage biomarkers. We measured immune- and angiogenesis-related proteins in human stool to examine inflammatory profiles associated with Parkinson's disease.Stool samples and subjects' self-reported metadata were obtained from 156 individuals with Parkinson's disease and 110 without, including spouse and nonhousehold controls. Metadata were probed for disease-associated differences, and levels of 37 immune and angiogenesis factors in stool homogenates were measured by multiplexed immunoassay and compared across experimental groups.METHODSStool samples and subjects' self-reported metadata were obtained from 156 individuals with Parkinson's disease and 110 without, including spouse and nonhousehold controls. Metadata were probed for disease-associated differences, and levels of 37 immune and angiogenesis factors in stool homogenates were measured by multiplexed immunoassay and compared across experimental groups.Parkinson's disease patients reported greater incidence of intestinal disease and digestive problems than controls. Direct comparison of levels of stool analytes in patients and controls revealed elevated vascular endothelial growth factor receptor 1, interleukin-1α, and CXCL8 in patients' stool. Paired comparison of patients and spouses suggested higher levels of multiple factors in patients, but this was complicated by sex differences. Sex, body mass index, a history of smoking, and use of probiotics were found to strongly influence levels of stool analytes. Multivariate analysis accounting for these and other potential confounders confirmed elevated levels of interleukin-1α and CXCL8 and also revealed increased interleukin-1β and C-reactive protein in stool in Parkinson's disease. These differences were not dependent on subject age or disease duration.RESULTSParkinson's disease patients reported greater incidence of intestinal disease and digestive problems than controls. Direct comparison of levels of stool analytes in patients and controls revealed elevated vascular endothelial growth factor receptor 1, interleukin-1α, and CXCL8 in patients' stool. Paired comparison of patients and spouses suggested higher levels of multiple factors in patients, but this was complicated by sex differences. Sex, body mass index, a history of smoking, and use of probiotics were found to strongly influence levels of stool analytes. Multivariate analysis accounting for these and other potential confounders confirmed elevated levels of interleukin-1α and CXCL8 and also revealed increased interleukin-1β and C-reactive protein in stool in Parkinson's disease. These differences were not dependent on subject age or disease duration.Levels of stool immune factors indicate that intestinal inflammation is present in patients with Parkinson's disease. © 2018 International Parkinson and Movement Disorder Society.CONCLUSIONSLevels of stool immune factors indicate that intestinal inflammation is present in patients with Parkinson's disease. © 2018 International Parkinson and Movement Disorder Society.
Author Hertzberg, Vicki S.
Payami, Haydeh
Molho, Eric S.
Factor, Stewart A.
Zabetian, Cyrus P.
Chang, Jianjun
Houser, Madelyn C.
Hill‐Burns, Erin M.
Tansey, Malú G.
AuthorAffiliation 3 Department of Neurology, Albany Medical College, Albany, NY
2 Department of Neurology, Emory University School of Medicine
7 Center for Nursing Data Science, Nell Hodgson Woodruff School of Nursing, Emory University
6 HudsonAlpha Institute for Biotechnology, Huntsville, AL
1 Department of Physiology, Emory University School of Medicine
5 Department of Neurology, University of Alabama at Birmingham, AL
4 Veterans Affairs Puget Sound Health Care System and Department of Neurology, University of Washington School of Medicine, Seattle, WA
AuthorAffiliation_xml – name: 3 Department of Neurology, Albany Medical College, Albany, NY
– name: 5 Department of Neurology, University of Alabama at Birmingham, AL
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– name: 2 Department of Neurology, Emory University School of Medicine
– name: 4 Veterans Affairs Puget Sound Health Care System and Department of Neurology, University of Washington School of Medicine, Seattle, WA
– name: 6 HudsonAlpha Institute for Biotechnology, Huntsville, AL
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/29572994$$D View this record in MEDLINE/PubMed
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Cites_doi 10.1111/j.1471-4159.2010.06879.x
10.1371/journal.pone.0142164
10.1002/mds.26307
10.1159/000087940
10.3945/ajcn.113.071506
10.1016/j.ajog.2014.03.020
10.1038/ng.175
10.1073/pnas.1610099113
10.1210/jc.2007-2630
10.3233/JPD-140491
10.1016/j.parkreldis.2014.02.019
10.1615/CritRevImmunol.v32.i1.30
10.1002/mds.25863
10.1186/s13073-017-0428-y
10.1016/j.bbamem.2008.08.027
10.1212/WNL.0000000000003127
10.1371/journal.pone.0151841
10.3233/JPD-161050
10.1016/j.cger.2016.02.007
10.11613/BM.2011.036
10.1186/2047-9158-4-1
10.1016/j.parkreldis.2015.02.004
10.1371/journal.pgen.1002237
10.1038/labinvest.2011.74
10.1016/j.neures.2006.11.012
10.1038/35079107
10.1093/hmg/dds135
10.5114/aoms.2016.63599
10.1016/j.jcmgh.2015.12.008
10.1136/jnnp.74.2.268
10.1002/mds.25020
10.1046/j.1365-2567.2003.01608.x
10.1007/s12307-015-0177-7
10.1007/s10620-013-2694-x
10.1159/000477990
10.1007/s00018-016-2175-4
10.1016/j.neuron.2004.11.005
10.1016/j.nbd.2012.09.007
10.1016/j.jogn.2016.05.002
10.1097/SHK.0b013e31822f36b0
10.2105/AJPH.2016.303324
10.1002/mds.25445
10.1002/mds.25882
10.1074/jbc.M208231200
10.1038/sj.ijo.0802987
10.1158/1055-9965.EPI-03-0160
10.1002/mds.25736
10.1007/s00401-013-1214-6
10.1016/j.parkreldis.2016.08.019
10.1111/bpa.12371
10.1038/s41531-016-0002-0
10.1038/sj.onc.1203239
10.1007/s10654-014-9878-3
10.1007/s00702-015-1442-0
10.1371/journal.pone.0028032
10.1097/MIB.0000000000000735
10.1212/WNL.0000000000002151
10.1111/nmo.12797
10.1002/mds.26069
10.1038/sj.ijo.0802408
10.1186/1824-7288-36-66
10.1038/jcbfm.2015.32
10.1016/j.parkreldis.2017.06.007
10.3748/wjg.v18.i18.2180
10.1097/NNR.0000000000000068
10.1002/mds.26942
10.3233/JPD-160982
10.1016/j.brainres.2017.04.019
10.1038/35079114
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Copyright 2018 International Parkinson and Movement Disorder Society
2018 International Parkinson and Movement Disorder Society.
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ID FETCH-LOGICAL-c5096-aa2a00bb217af3d793590c010076f4a74a7e73e8e16f6c676856134fde6314293
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Issue 5
Keywords stool
Parkinson's disease
intestine
biomarker
inflammation
Language English
License 2018 International Parkinson and Movement Disorder Society.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c5096-aa2a00bb217af3d793590c010076f4a74a7e73e8e16f6c676856134fde6314293
Notes M.G.T. is a member of the Executive Scientific Advisory Board for the Michael J. Fox Foundation for Parkinson's Research, a member of the Scientific Review Board for the Alzheimer's Drug Discovery Foundation, and a consultant for Celgene Corporation. E.S.M. is supported by the Riley Family Chair in Parkinson's Disease.
Relevant conflicts of interest/financial disclosures
Funding agencies
Subject recruitment and characterization, stool and metadata collection, and multiplexed immunoassays were funded by NIH grants NS036960 (to H.P.), NS067469 (to H.P.), and P50 NS062684 (to C.P.Z.).
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References 2015; 35
2017; 7
2017; 42
2013; 28
2017; 3
2013; 1
2017; 1667
2015; 30
2016; 32
2016; 73
2016; 2016
2016; 106
2012; 18
2011; 57
2014; 29
2003; 278
2005; 29
2017; 9
2014; 211
2014; 20
2014; 127
2013; 58
2005; 101
1999; 18
2010; 114
2017; 32
2013; 50
2015; 85
2016; 113
2016; 87
2011; 21
2012; 27
2012; 21
2001; 411
2016; 45
2004; 44
2009; 1788
2015; 5
2015; 4
2010; 36
2015; 122
2015; 10
2011; 36
2011; 6
2015; 8
2003; 74
2008; 93
2012; 32
2007; 57
2011; 7
2016; 11
2003; 108
2016; 2
2011; 91
2015; 64
2017; 13
2015; 21
2004; 13
2003; 27
2016; 28
2014; 100
2008; 40
2016; 26
2016; 22
e_1_2_7_5_1
e_1_2_7_3_1
e_1_2_7_9_1
Kovacs M (e_1_2_7_49_1) 2016; 2016
e_1_2_7_7_1
e_1_2_7_19_1
e_1_2_7_60_1
e_1_2_7_17_1
e_1_2_7_62_1
e_1_2_7_15_1
e_1_2_7_41_1
e_1_2_7_64_1
e_1_2_7_13_1
e_1_2_7_43_1
e_1_2_7_66_1
e_1_2_7_11_1
e_1_2_7_45_1
e_1_2_7_68_1
e_1_2_7_47_1
e_1_2_7_28_1
e_1_2_7_73_1
e_1_2_7_50_1
e_1_2_7_71_1
e_1_2_7_25_1
Chen Y (e_1_2_7_27_1) 2015; 8
e_1_2_7_31_1
e_1_2_7_52_1
e_1_2_7_23_1
e_1_2_7_33_1
e_1_2_7_54_1
e_1_2_7_75_1
Haep L (e_1_2_7_44_1) 2015; 21
e_1_2_7_21_1
e_1_2_7_35_1
e_1_2_7_56_1
e_1_2_7_37_1
e_1_2_7_58_1
e_1_2_7_39_1
e_1_2_7_6_1
e_1_2_7_4_1
e_1_2_7_8_1
Mushref MA (e_1_2_7_26_1) 2013; 1
Cassani E (e_1_2_7_70_1) 2011; 57
e_1_2_7_18_1
e_1_2_7_16_1
e_1_2_7_40_1
e_1_2_7_61_1
e_1_2_7_2_1
e_1_2_7_14_1
e_1_2_7_42_1
e_1_2_7_63_1
e_1_2_7_12_1
e_1_2_7_65_1
e_1_2_7_10_1
e_1_2_7_46_1
e_1_2_7_67_1
e_1_2_7_48_1
e_1_2_7_69_1
e_1_2_7_29_1
e_1_2_7_72_1
e_1_2_7_51_1
e_1_2_7_30_1
e_1_2_7_53_1
e_1_2_7_24_1
e_1_2_7_32_1
e_1_2_7_55_1
e_1_2_7_74_1
e_1_2_7_22_1
e_1_2_7_34_1
e_1_2_7_57_1
e_1_2_7_20_1
e_1_2_7_36_1
e_1_2_7_59_1
e_1_2_7_38_1
References_xml – volume: 13
  start-page: 279
  issue: 2
  year: 2004
  end-page: 284
  article-title: Bowel inflammation as measured by fecal calprotectin: a link between lifestyle factors and colorectal cancer risk
  publication-title: Cancer Epidemiol Biomarkers Prev
– volume: 21
  start-page: 2360
  issue: 10
  year: 2015
  end-page: 2371
  article-title: Interferon gamma counteracts the angiogenic switch and induces vascular permeability in dextran sulfate sodium colitis in mice
  publication-title: Inflamm Bowel Dis
– volume: 58
  start-page: 2594
  issue: 9
  year: 2013
  end-page: 2598
  article-title: Small intestinal bacterial overgrowth and orocecal transit time in patients of inflammatory bowel disease
  publication-title: Dig Dis Sci
– volume: 27
  start-page: 716
  issue: 6
  year: 2012
  end-page: 719
  article-title: Is alpha‐synuclein in the colon a biomarker for premotor Parkinson's disease? Evidence from 3 cases
  publication-title: Mov Disord
– volume: 36
  start-page: 66
  year: 2010
  article-title: Relationship between severe obesity and gut inflammation in children: What's next?
  publication-title: Ital J Pediatr
– volume: 106
  start-page: 1650
  issue: 9
  year: 2016
  end-page: 1655
  article-title: Epidemiology of major neurodegenerative diseases in women: contribution of the nurses' health study
  publication-title: Am J Public Health
– volume: 7
  start-page: e1002237
  issue: 8
  year: 2011
  article-title: Genome‐wide gene‐environment study identifies glutamate receptor gene GRIN2A as a Parkinson's disease modifier gene via interaction with coffee
  publication-title: PLoS Genet
– volume: 28
  start-page: 966
  issue: 7
  year: 2016
  end-page: 974
  article-title: What a gastrointestinal biopsy can tell us about Parkinson's disease?
  publication-title: Neurogastroenterol Motil
– volume: 8
  start-page: 187
  issue: 3
  year: 2015
  end-page: 200
  article-title: Il‐1 in colon inflammation, colon carcinogenesis and invasiveness of colon cancer
  publication-title: Cancer Microenviron
– volume: 127
  start-page: 235
  issue: 2
  year: 2014
  end-page: 241
  article-title: Accumulation of alpha‐synuclein in the bowel of patients in the pre‐clinical phase of Parkinson's disease
  publication-title: Acta Neuropathol
– volume: 29
  start-page: 57
  issue: 1
  year: 2014
  end-page: 62
  article-title: Irritable bowel syndrome correlates with increased risk of Parkinson's disease in taiwan
  publication-title: Eur J Epidemiol
– volume: 411
  start-page: 603
  issue: 6837
  year: 2001
  end-page: 606
  article-title: A frameshift mutation in nod2 associated with susceptibility to Crohn's disease
  publication-title: Nature
– volume: 7
  start-page: 359
  issue: 2
  year: 2017
  end-page: 367
  article-title: Objective colonic dysfunction is far more prevalent than subjective constipation in Parkinson's disease: a colon transit and volume study
  publication-title: J Parkinsons Dis
– volume: 36
  start-page: 458
  issue: 5
  year: 2011
  end-page: 465
  article-title: Protective effects of a phosphatidylcholine‐enriched diet in lipopolysaccharide‐induced experimental neuroinflammation in the rat
  publication-title: Shock
– volume: 32
  start-page: 23
  issue: 1
  year: 2012
  end-page: 63
  article-title: Role of interleukin 10 transcriptional regulation in inflammation and autoimmune disease
  publication-title: Crit Rev Immunol
– volume: 101
  start-page: e165
  issue: 4
  year: 2005
  end-page: e172
  article-title: C‐reactive protein induces Nf‐kappaB activation through intracellular calcium and ROS in human mesangial cells
  publication-title: Nephron Exp Nephrol
– volume: 64
  start-page: 53
  issue: 1
  year: 2015
  end-page: 66
  article-title: Reactive oxygen and nitrogen species: impact on endothelial dysfunction
  publication-title: Nurs Res
– volume: 91
  start-page: 1056
  issue: 7
  year: 2011
  end-page: 1067
  article-title: Cigarette smoking alters epithelial apoptosis and immune composition in murine Galt
  publication-title: Lab Invest
– volume: 44
  start-page: 601
  issue: 4
  year: 2004
  end-page: 607
  article-title: Mutations in LRRK2 cause autosomal‐dominant parkinsonism with pleomorphic pathology
  publication-title: Neuron
– volume: 21
  start-page: 389
  issue: 4
  year: 2015
  end-page: 393
  article-title: Increased urinary indoxyl sulfate (indican): new insights into gut dysbiosis in Parkinson's disease
  publication-title: Parkinsonism Relat Disord
– volume: 28
  start-page: 597
  issue: 5
  year: 2013
  end-page: 604
  article-title: Prodromal autonomic symptoms and signs in Parkinson's disease and dementia with Lewy bodies
  publication-title: Mov Disord
– volume: 114
  start-page: 1687
  issue: 6
  year: 2010
  end-page: 1700
  article-title: Ulcerative colitis exacerbates lipopolysaccharide‐induced damage to the nigral dopaminergic system: Potential risk factor in Parkinson's disease
  publication-title: J Neurochem
– volume: 8
  start-page: 2495
  issue: 3
  year: 2015
  end-page: 2504
  article-title: Clinical characteristics and peripheral T cell subsets in Parkinson's disease patients with constipation
  publication-title: Int J Clin Exp Pathol
– volume: 29
  start-page: 999
  issue: 8
  year: 2014
  end-page: 1009
  article-title: Progression of intestinal permeability changes and alpha‐synuclein expression in a mouse model of Parkinson's disease
  publication-title: Mov Disord
– volume: 32
  start-page: 66
  year: 2016
  end-page: 72
  article-title: Short chain fatty acids and gut microbiota differ between patients with Parkinson's disease and age‐matched controls
  publication-title: Parkinsonism Relat Disord
– volume: 5
  start-page: 1
  issue: 1
  year: 2015
  end-page: 19
  article-title: Role of alpha‐synuclein in inducing innate and adaptive immunity in Parkinson disease
  publication-title: J Parkinsons Dis
– volume: 50
  start-page: 42
  year: 2013
  end-page: 48
  article-title: Colonic inflammation in Parkinson's disease
  publication-title: Neurobiol Dis
– volume: 1
  start-page: 14
  issue: 2
  year: 2013
  article-title: Effect of high fat‐diet and obesity on gastrointestinal motility
  publication-title: Ann Transl Med
– volume: 4
  start-page: 1
  issue: 1
  year: 2015
  article-title: Meta‐analyses on prevalence of selected Parkinson's nonmotor symptoms before and after diagnosis
  publication-title: Transl Neurodegener
– volume: 74
  start-page: 268
  issue: 2
  year: 2003
  end-page: 272
  article-title: Colonic transit time and rectoanal videomanometry in Parkinson's disease
  publication-title: J Neurol Neurosurg Psychiatry
– volume: 411
  start-page: 599
  issue: 6837
  year: 2001
  end-page: 603
  article-title: Association of nod2 leucine‐rich repeat variants with susceptibility to Crohn's disease
  publication-title: Nature
– volume: 40
  start-page: 955
  issue: 8
  year: 2008
  end-page: 962
  article-title: Genome‐wide association defines more than 30 distinct susceptibility loci for Crohn's disease
  publication-title: Nat Genet
– volume: 13
  start-page: 507
  issue: 3
  year: 2017
  end-page: 514
  article-title: Can coffee consumption lower the risk of Alzheimer's disease and Parkinson's disease? A literature review
  publication-title: Arch Med Sci
– volume: 21
  start-page: 3073
  issue: 13
  year: 2012
  end-page: 3082
  article-title: Cigarette smoking behaviors and time since quitting are associated with differential DNA methylation across the human genome
  publication-title: Hum Mol Genet
– volume: 30
  start-page: 350
  issue: 3
  year: 2015
  end-page: 358
  article-title: Gut microbiota are related to Parkinson's disease and clinical phenotype
  publication-title: Mov Disord
– volume: 9
  start-page: 39
  issue: 1
  year: 2017
  article-title: Functional implications of microbial and viral gut metagenome changes in early stage l‐dopa‐naive Parkinson's disease patients
  publication-title: Genome Med
– volume: 3
  start-page: 3
  year: 2017
  article-title: The gut‐brain axis: Is intestinal inflammation a silent driver of Parkinson's disease pathogenesis?
  publication-title: NPJ Parkinsons Dis
– volume: 113
  start-page: 9587
  issue: 34
  year: 2016
  end-page: 9592
  article-title: Caspase‐1 causes truncation and aggregation of the Parkinson's disease‐associated protein alpha‐synuclein
  publication-title: Proc Natl Acad Sci U S A
– volume: 11
  start-page: e0151841
  issue: 4
  year: 2016
  article-title: Association between Parkinson's disease and cigarette smoking, rural living, well‐water consumption, farming and pesticide use: systematic review and meta‐analysis
  publication-title: PLoS One
– volume: 10
  start-page: e0142164
  issue: 11
  year: 2015
  article-title: Intestinal dysbiosis and lowered serum lipopolysaccharide‐binding protein in Parkinson's disease
  publication-title: PLoS One
– volume: 26
  start-page: 404
  issue: 3
  year: 2016
  end-page: 409
  article-title: Neuroinflammation in synucleinopathies
  publication-title: Brain Pathol
– volume: 29
  start-page: 819
  issue: 6
  year: 2014
  end-page: 822
  article-title: Alcohol intake and risk of Parkinson's disease: a meta‐analysis of observational studies
  publication-title: Mov Disord
– volume: 278
  start-page: 8508
  issue: 10
  year: 2003
  end-page: 8515
  article-title: Angiogenic effects of interleukin 8 (CXCL8) in human intestinal microvascular endothelial cells are mediated by CXCR2
  publication-title: J Biol Chem
– volume: 18
  start-page: 2180
  issue: 18
  year: 2012
  end-page: 2187
  article-title: Side‐stream smoking reduces intestinal inflammation and increases expression of tight junction proteins
  publication-title: World J Gastroenterol
– volume: 1788
  start-page: 864
  issue: 4
  year: 2009
  end-page: 871
  article-title: Cytokine regulation of tight junctions
  publication-title: Biochim Biophys Acta
– volume: 18
  start-page: 6853
  issue: 49
  year: 1999
  end-page: 6866
  article-title: Activators and target genes of Rel/LNF‐kappaB transcription factors
  publication-title: Oncogene
– volume: 93
  start-page: 3215
  issue: 8
  year: 2008
  end-page: 3221
  article-title: Cc chemokine and cc chemokine receptor profiles in visceral and subcutaneous adipose tissue are altered in human obesity
  publication-title: J Clin Endocrinol Metab
– volume: 35
  start-page: 747
  issue: 5
  year: 2015
  end-page: 750
  article-title: Striatal blood‐brain barrier permeability in Parkinson's disease
  publication-title: J Cereb Blood Flow Metab
– volume: 100
  start-page: 347S
  issue: Suppl 1
  year: 2014
  end-page: 352S
  article-title: Cognition: the new frontier for nuts and berries
  publication-title: Am J Clin Nutr
– volume: 32
  start-page: 415
  issue: 3
  year: 2016
  end-page: 432
  article-title: Host resistance and immune aging
  publication-title: Clin Geriatr Med
– volume: 85
  start-page: 1834
  issue: 21
  year: 2015
  end-page: 1842
  article-title: Increased csf biomarkers of angiogenesis in Parkinson disease
  publication-title: Neurology
– volume: 6
  start-page: e28032
  issue: 12
  year: 2011
  article-title: Increased intestinal permeability correlates with sigmoid mucosa alpha‐synuclein staining and endotoxin exposure markers in early Parkinson's disease
  publication-title: PLoS One
– volume: 1667
  start-page: 41
  year: 2017
  end-page: 45
  article-title: Gut microbiota in Parkinson disease in a northern German cohort
  publication-title: Brain Res
– volume: 57
  start-page: 473
  issue: 3
  year: 2007
  end-page: 476
  article-title: Card15 variants in patients with sporadic Parkinson's disease
  publication-title: Neurosci Res
– volume: 30
  start-page: 1351
  issue: 10
  year: 2015
  end-page: 1360
  article-title: Colonic bacterial composition in Parkinson's disease
  publication-title: Mov Disord
– volume: 122
  start-page: 1659
  issue: 12
  year: 2015
  end-page: 1661
  article-title: Small intestine dysfunction in Parkinson's disease
  publication-title: J Neural Transm (Vienna)
– volume: 7
  start-page: 353
  issue: 2
  year: 2017
  end-page: 357
  article-title: The prevalence of constipation and irritable bowel syndrome in Parkinson's disease patients according to Rome III diagnostic criteria
  publication-title: J Parkinsons Dis
– volume: 87
  start-page: 1274
  issue: 12
  year: 2016
  end-page: 1280
  article-title: Probiotics and prebiotic fiber for constipation associated with Parkinson disease: An RCT
  publication-title: Neurology
– volume: 57
  start-page: 117
  issue: 2
  year: 2011
  end-page: 121
  article-title: Use of probiotics for the treatment of constipation in Parkinson's disease patients
  publication-title: Minerva Gastroenterol Dietol
– volume: 20
  start-page: 535
  issue: 5
  year: 2014
  end-page: 540
  article-title: Small intestinal bacterial overgrowth in Parkinson's disease
  publication-title: Parkinsonism Relat Disord
– volume: 211
  start-page: 247 e241
  issue: 3
  year: 2014
  end-page: e247
  article-title: The association of body mass index with serum angiogenic markers in normal and abnormal pregnancies
  publication-title: Am J Obstet Gynecol
– volume: 42
  start-page: 40
  year: 2017
  end-page: 46
  article-title: Dietary habits in Parkinson's disease: adherence to Mediterranean diet
  publication-title: Parkinsonism Relat Disord
– volume: 21
  start-page: 264
  issue: 3
  year: 2011
  end-page: 275
  article-title: Molecular pathways in cancer‐related inflammation
  publication-title: Biochem Med (Zagreb)
– volume: 2016
  start-page: 7951840
  year: 2016
  article-title: Impact of sex on the nonmotor symptoms and the health‐related quality of life in Parkinson's disease
  publication-title: Parkinsons Dis
– volume: 29
  start-page: 976
  issue: 8
  year: 2014
  end-page: 979
  article-title: Gut feelings about smoking and coffee in Parkinson's disease
  publication-title: Mov Disord
– volume: 73
  start-page: 2511
  issue: 13
  year: 2016
  end-page: 2530
  article-title: Modulatory effects of α7 nAChRs on the immune system and its relevance for CNS disorders
  publication-title: Cell Mol Life Sci
– volume: 9
  start-page: 456
  issue: 5
  year: 2017
  end-page: 463
  article-title: A role for neuronal alpha‐synuclein in gastrointestinal immunity
  publication-title: J Innate Immun
– volume: 32
  start-page: 739
  issue: 5
  year: 2017
  end-page: 749
  article-title: Parkinson's disease and Parkinson's disease medications have distinct signatures of the gut microbiome
  publication-title: Mov Disord
– volume: 45
  start-page: 749
  issue: 5
  year: 2016
  end-page: 756
  article-title: Sex differences in the clinical progression of Parkinson's disease
  publication-title: J Obstet Gynecol Neonatal Nurs
– volume: 29
  start-page: 1308
  issue: 11
  year: 2005
  end-page: 1314
  article-title: Angiogenic factors are elevated in overweight and obese individuals
  publication-title: Int J Obes (Lond)
– volume: 108
  start-page: 539
  issue: 4
  year: 2003
  end-page: 547
  article-title: Overexpressed nuclear factor‐kappaB can participate in endogenous c‐reactive protein induction, and enhances the effects of C/EBPbeta and signal transducer and activator of transcription‐3
  publication-title: Immunology
– volume: 2
  start-page: 328
  issue: 3
  year: 2016
  end-page: 339
  article-title: Intestinal dysbiosis contributes to the delayed gastrointestinal transit in high‐fat diet fed mice
  publication-title: Cell Mol Gastroenterol Hepatol
– volume: 27
  start-page: 1325
  issue: 11
  year: 2003
  end-page: 1331
  article-title: Serum bfgf levels are reduced in Japanese overweight men and restored by a 6‐month exercise education
  publication-title: Int J Obes Relat Metab Disord
– volume: 22
  start-page: 1049
  issue: 5
  year: 2016
  end-page: 1055
  article-title: Association between Parkinson's disease and inflammatory bowel disease: a nationwide Taiwanese retrospective cohort study
  publication-title: Inflamm Bowel Dis
– ident: e_1_2_7_20_1
  doi: 10.1111/j.1471-4159.2010.06879.x
– ident: e_1_2_7_11_1
  doi: 10.1371/journal.pone.0142164
– ident: e_1_2_7_10_1
  doi: 10.1002/mds.26307
– volume: 2016
  start-page: 7951840
  year: 2016
  ident: e_1_2_7_49_1
  article-title: Impact of sex on the nonmotor symptoms and the health‐related quality of life in Parkinson's disease
  publication-title: Parkinsons Dis
– ident: e_1_2_7_43_1
  doi: 10.1159/000087940
– ident: e_1_2_7_50_1
  doi: 10.3945/ajcn.113.071506
– volume: 21
  start-page: 2360
  issue: 10
  year: 2015
  ident: e_1_2_7_44_1
  article-title: Interferon gamma counteracts the angiogenic switch and induces vascular permeability in dextran sulfate sodium colitis in mice
  publication-title: Inflamm Bowel Dis
– ident: e_1_2_7_54_1
  doi: 10.1016/j.ajog.2014.03.020
– ident: e_1_2_7_73_1
  doi: 10.1038/ng.175
– ident: e_1_2_7_30_1
  doi: 10.1073/pnas.1610099113
– ident: e_1_2_7_53_1
  doi: 10.1210/jc.2007-2630
– ident: e_1_2_7_31_1
  doi: 10.3233/JPD-140491
– ident: e_1_2_7_13_1
  doi: 10.1016/j.parkreldis.2014.02.019
– ident: e_1_2_7_41_1
  doi: 10.1615/CritRevImmunol.v32.i1.30
– ident: e_1_2_7_59_1
  doi: 10.1002/mds.25863
– ident: e_1_2_7_16_1
  doi: 10.1186/s13073-017-0428-y
– ident: e_1_2_7_32_1
  doi: 10.1016/j.bbamem.2008.08.027
– ident: e_1_2_7_69_1
  doi: 10.1212/WNL.0000000000003127
– ident: e_1_2_7_61_1
  doi: 10.1371/journal.pone.0151841
– ident: e_1_2_7_3_1
  doi: 10.3233/JPD-161050
– ident: e_1_2_7_37_1
  doi: 10.1016/j.cger.2016.02.007
– ident: e_1_2_7_45_1
  doi: 10.11613/BM.2011.036
– ident: e_1_2_7_2_1
  doi: 10.1186/2047-9158-4-1
– volume: 1
  start-page: 14
  issue: 2
  year: 2013
  ident: e_1_2_7_26_1
  article-title: Effect of high fat‐diet and obesity on gastrointestinal motility
  publication-title: Ann Transl Med
– ident: e_1_2_7_14_1
  doi: 10.1016/j.parkreldis.2015.02.004
– ident: e_1_2_7_62_1
  doi: 10.1371/journal.pgen.1002237
– ident: e_1_2_7_65_1
  doi: 10.1038/labinvest.2011.74
– ident: e_1_2_7_72_1
  doi: 10.1016/j.neures.2006.11.012
– ident: e_1_2_7_74_1
  doi: 10.1038/35079107
– ident: e_1_2_7_68_1
  doi: 10.1093/hmg/dds135
– ident: e_1_2_7_58_1
  doi: 10.5114/aoms.2016.63599
– ident: e_1_2_7_28_1
  doi: 10.1016/j.jcmgh.2015.12.008
– ident: e_1_2_7_24_1
  doi: 10.1136/jnnp.74.2.268
– ident: e_1_2_7_6_1
  doi: 10.1002/mds.25020
– ident: e_1_2_7_42_1
  doi: 10.1046/j.1365-2567.2003.01608.x
– ident: e_1_2_7_39_1
  doi: 10.1007/s12307-015-0177-7
– ident: e_1_2_7_25_1
  doi: 10.1007/s10620-013-2694-x
– ident: e_1_2_7_29_1
  doi: 10.1159/000477990
– ident: e_1_2_7_67_1
  doi: 10.1007/s00018-016-2175-4
– ident: e_1_2_7_71_1
  doi: 10.1016/j.neuron.2004.11.005
– ident: e_1_2_7_36_1
  doi: 10.1016/j.nbd.2012.09.007
– ident: e_1_2_7_48_1
  doi: 10.1016/j.jogn.2016.05.002
– ident: e_1_2_7_21_1
  doi: 10.1097/SHK.0b013e31822f36b0
– ident: e_1_2_7_51_1
  doi: 10.2105/AJPH.2016.303324
– ident: e_1_2_7_4_1
  doi: 10.1002/mds.25445
– ident: e_1_2_7_60_1
  doi: 10.1002/mds.25882
– volume: 57
  start-page: 117
  issue: 2
  year: 2011
  ident: e_1_2_7_70_1
  article-title: Use of probiotics for the treatment of constipation in Parkinson's disease patients
  publication-title: Minerva Gastroenterol Dietol
– ident: e_1_2_7_38_1
  doi: 10.1074/jbc.M208231200
– ident: e_1_2_7_52_1
  doi: 10.1038/sj.ijo.0802987
– ident: e_1_2_7_56_1
  doi: 10.1158/1055-9965.EPI-03-0160
– ident: e_1_2_7_18_1
  doi: 10.1002/mds.25736
– volume: 8
  start-page: 2495
  issue: 3
  year: 2015
  ident: e_1_2_7_27_1
  article-title: Clinical characteristics and peripheral T cell subsets in Parkinson's disease patients with constipation
  publication-title: Int J Clin Exp Pathol
– ident: e_1_2_7_7_1
  doi: 10.1007/s00401-013-1214-6
– ident: e_1_2_7_12_1
  doi: 10.1016/j.parkreldis.2016.08.019
– ident: e_1_2_7_22_1
  doi: 10.1111/bpa.12371
– ident: e_1_2_7_8_1
  doi: 10.1038/s41531-016-0002-0
– ident: e_1_2_7_40_1
  doi: 10.1038/sj.onc.1203239
– ident: e_1_2_7_34_1
  doi: 10.1007/s10654-014-9878-3
– ident: e_1_2_7_23_1
  doi: 10.1007/s00702-015-1442-0
– ident: e_1_2_7_19_1
  doi: 10.1371/journal.pone.0028032
– ident: e_1_2_7_33_1
  doi: 10.1097/MIB.0000000000000735
– ident: e_1_2_7_46_1
  doi: 10.1212/WNL.0000000000002151
– ident: e_1_2_7_5_1
  doi: 10.1111/nmo.12797
– ident: e_1_2_7_9_1
  doi: 10.1002/mds.26069
– ident: e_1_2_7_55_1
  doi: 10.1038/sj.ijo.0802408
– ident: e_1_2_7_57_1
  doi: 10.1186/1824-7288-36-66
– ident: e_1_2_7_47_1
  doi: 10.1038/jcbfm.2015.32
– ident: e_1_2_7_63_1
  doi: 10.1016/j.parkreldis.2017.06.007
– ident: e_1_2_7_66_1
  doi: 10.3748/wjg.v18.i18.2180
– ident: e_1_2_7_64_1
  doi: 10.1097/NNR.0000000000000068
– ident: e_1_2_7_15_1
  doi: 10.1002/mds.26942
– ident: e_1_2_7_35_1
  doi: 10.3233/JPD-160982
– ident: e_1_2_7_17_1
  doi: 10.1016/j.brainres.2017.04.019
– ident: e_1_2_7_75_1
  doi: 10.1038/35079114
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Snippet Background: Gastrointestinal symptoms are common in Parkinson's disease and frequently precede the development of motor impairments. Intestinal inflammation...
Background: Gastrointestinal symptoms are common in Parkinson's disease and frequently precede the development of motor impairments. Intestinal inflammation...
Gastrointestinal symptoms are common in Parkinson's disease and frequently precede the development of motor impairments. Intestinal inflammation has been...
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SubjectTerms Adult
Aged
Aged, 80 and over
Angiogenesis
Angiogenesis Inducing Agents - metabolism
biomarker
Body mass index
C-Reactive Protein - metabolism
Cytokines
Cytokines - metabolism
Feces - chemistry
Female
Gastroenteritis - etiology
Gastroenteritis - metabolism
Humans
Inflammation
Intestine
Male
Metadata
Middle Aged
Mood Disorders - etiology
Movement disorders
Multivariate analysis
Neurodegenerative diseases
Parkinson Disease - complications
Parkinson Disease - psychology
Parkinson's disease
Probiotics
Sex Characteristics
Sex differences
Smoking
stool
Vascular endothelial growth factor
Title Stool Immune Profiles Evince Gastrointestinal Inflammation in Parkinson's Disease
URI https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fmds.27326
https://www.ncbi.nlm.nih.gov/pubmed/29572994
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https://www.proquest.com/docview/2018032894
https://pubmed.ncbi.nlm.nih.gov/PMC5992021
Volume 33
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