Gut Microbial Ecosystem in Parkinson Disease: New Clinicobiological Insights from Multi‐Omics

Objective Gut microbiome alterations in Parkinson disease (PD) have been reported repeatedly, but their functional relevance remains unclear. Fecal metabolomics, which provide a functional readout of microbial activity, have scarcely been investigated. We investigated fecal microbiome and metabolome...

Full description

Saved in:
Bibliographic Details
Published inAnnals of neurology Vol. 89; no. 3; pp. 546 - 559
Main Authors Tan, Ai Huey, Chong, Chun Wie, Lim, Shen‐Yang, Yap, Ivan Kok Seng, Teh, Cindy Shuan Ju, Loke, Mun Fai, Song, Sze‐Looi, Tan, Jiun Yan, Ang, Ban Hong, Tan, Yong Qi, Kho, Mee Teck, Bowman, Jeff, Mahadeva, Sanjiv, Yong, Hoi Sen, Lang, Anthony E.
Format Journal Article
LanguageEnglish
Published Hoboken, USA John Wiley & Sons, Inc 01.03.2021
Wiley Subscription Services, Inc
Subjects
Online AccessGet full text

Cover

Loading…
Abstract Objective Gut microbiome alterations in Parkinson disease (PD) have been reported repeatedly, but their functional relevance remains unclear. Fecal metabolomics, which provide a functional readout of microbial activity, have scarcely been investigated. We investigated fecal microbiome and metabolome alterations in PD, and their clinical relevance. Methods Two hundred subjects (104 patients, 96 controls) underwent extensive clinical phenotyping. Stool samples were analyzed using 16S rRNA gene sequencing. Fecal metabolomics were performed using two platforms, nuclear magnetic resonance (NMR) spectroscopy and liquid chromatography–mass spectrometry. Results Fecal microbiome and metabolome composition in PD was significantly different from controls, with the largest effect size seen in NMR‐based metabolome. Microbiome and NMR‐based metabolome compositional differences remained significant after comprehensive confounder analyses. Differentially abundant fecal metabolite features and predicted functional changes in PD versus controls included bioactive molecules with putative neuroprotective effects (eg, short chain fatty acids [SCFAs], ubiquinones, and salicylate) and other compounds increasingly implicated in neurodegeneration (eg, ceramides, sphingosine, and trimethylamine N‐oxide). In the PD group, cognitive impairment, low body mass index (BMI), frailty, constipation, and low physical activity were associated with fecal metabolome compositional differences. Notably, low SCFAs in PD were significantly associated with poorer cognition and low BMI. Lower butyrate levels correlated with worse postural instability–gait disorder scores. Interpretation Gut microbial function is altered in PD, characterized by differentially abundant metabolic features that provide important biological insights into gut–brain pathophysiology. Their clinical relevance further supports a role for microbial metabolites as potential targets for the development of new biomarkers and therapies in PD. ANN NEUROL 2021;89:546–559
AbstractList ObjectiveGut microbiome alterations in Parkinson disease (PD) have been reported repeatedly, but their functional relevance remains unclear. Fecal metabolomics, which provide a functional readout of microbial activity, have scarcely been investigated. We investigated fecal microbiome and metabolome alterations in PD, and their clinical relevance.MethodsTwo hundred subjects (104 patients, 96 controls) underwent extensive clinical phenotyping. Stool samples were analyzed using 16S rRNA gene sequencing. Fecal metabolomics were performed using two platforms, nuclear magnetic resonance (NMR) spectroscopy and liquid chromatography–mass spectrometry.ResultsFecal microbiome and metabolome composition in PD was significantly different from controls, with the largest effect size seen in NMR‐based metabolome. Microbiome and NMR‐based metabolome compositional differences remained significant after comprehensive confounder analyses. Differentially abundant fecal metabolite features and predicted functional changes in PD versus controls included bioactive molecules with putative neuroprotective effects (eg, short chain fatty acids [SCFAs], ubiquinones, and salicylate) and other compounds increasingly implicated in neurodegeneration (eg, ceramides, sphingosine, and trimethylamine N‐oxide). In the PD group, cognitive impairment, low body mass index (BMI), frailty, constipation, and low physical activity were associated with fecal metabolome compositional differences. Notably, low SCFAs in PD were significantly associated with poorer cognition and low BMI. Lower butyrate levels correlated with worse postural instability–gait disorder scores.InterpretationGut microbial function is altered in PD, characterized by differentially abundant metabolic features that provide important biological insights into gut–brain pathophysiology. Their clinical relevance further supports a role for microbial metabolites as potential targets for the development of new biomarkers and therapies in PD. ANN NEUROL 2021;89:546–559
Gut microbiome alterations in Parkinson disease (PD) have been reported repeatedly, but their functional relevance remains unclear. Fecal metabolomics, which provide a functional readout of microbial activity, have scarcely been investigated. We investigated fecal microbiome and metabolome alterations in PD, and their clinical relevance. Two hundred subjects (104 patients, 96 controls) underwent extensive clinical phenotyping. Stool samples were analyzed using 16S rRNA gene sequencing. Fecal metabolomics were performed using two platforms, nuclear magnetic resonance (NMR) spectroscopy and liquid chromatography-mass spectrometry. Fecal microbiome and metabolome composition in PD was significantly different from controls, with the largest effect size seen in NMR-based metabolome. Microbiome and NMR-based metabolome compositional differences remained significant after comprehensive confounder analyses. Differentially abundant fecal metabolite features and predicted functional changes in PD versus controls included bioactive molecules with putative neuroprotective effects (eg, short chain fatty acids [SCFAs], ubiquinones, and salicylate) and other compounds increasingly implicated in neurodegeneration (eg, ceramides, sphingosine, and trimethylamine N-oxide). In the PD group, cognitive impairment, low body mass index (BMI), frailty, constipation, and low physical activity were associated with fecal metabolome compositional differences. Notably, low SCFAs in PD were significantly associated with poorer cognition and low BMI. Lower butyrate levels correlated with worse postural instability-gait disorder scores. Gut microbial function is altered in PD, characterized by differentially abundant metabolic features that provide important biological insights into gut-brain pathophysiology. Their clinical relevance further supports a role for microbial metabolites as potential targets for the development of new biomarkers and therapies in PD. ANN NEUROL 2021;89:546-559.
Objective Gut microbiome alterations in Parkinson disease (PD) have been reported repeatedly, but their functional relevance remains unclear. Fecal metabolomics, which provide a functional readout of microbial activity, have scarcely been investigated. We investigated fecal microbiome and metabolome alterations in PD, and their clinical relevance. Methods Two hundred subjects (104 patients, 96 controls) underwent extensive clinical phenotyping. Stool samples were analyzed using 16S rRNA gene sequencing. Fecal metabolomics were performed using two platforms, nuclear magnetic resonance (NMR) spectroscopy and liquid chromatography–mass spectrometry. Results Fecal microbiome and metabolome composition in PD was significantly different from controls, with the largest effect size seen in NMR‐based metabolome. Microbiome and NMR‐based metabolome compositional differences remained significant after comprehensive confounder analyses. Differentially abundant fecal metabolite features and predicted functional changes in PD versus controls included bioactive molecules with putative neuroprotective effects (eg, short chain fatty acids [SCFAs], ubiquinones, and salicylate) and other compounds increasingly implicated in neurodegeneration (eg, ceramides, sphingosine, and trimethylamine N‐oxide). In the PD group, cognitive impairment, low body mass index (BMI), frailty, constipation, and low physical activity were associated with fecal metabolome compositional differences. Notably, low SCFAs in PD were significantly associated with poorer cognition and low BMI. Lower butyrate levels correlated with worse postural instability–gait disorder scores. Interpretation Gut microbial function is altered in PD, characterized by differentially abundant metabolic features that provide important biological insights into gut–brain pathophysiology. Their clinical relevance further supports a role for microbial metabolites as potential targets for the development of new biomarkers and therapies in PD. ANN NEUROL 2021;89:546–559
Gut microbiome alterations in Parkinson disease (PD) have been reported repeatedly, but their functional relevance remains unclear. Fecal metabolomics, which provide a functional readout of microbial activity, have scarcely been investigated. We investigated fecal microbiome and metabolome alterations in PD, and their clinical relevance.OBJECTIVEGut microbiome alterations in Parkinson disease (PD) have been reported repeatedly, but their functional relevance remains unclear. Fecal metabolomics, which provide a functional readout of microbial activity, have scarcely been investigated. We investigated fecal microbiome and metabolome alterations in PD, and their clinical relevance.Two hundred subjects (104 patients, 96 controls) underwent extensive clinical phenotyping. Stool samples were analyzed using 16S rRNA gene sequencing. Fecal metabolomics were performed using two platforms, nuclear magnetic resonance (NMR) spectroscopy and liquid chromatography-mass spectrometry.METHODSTwo hundred subjects (104 patients, 96 controls) underwent extensive clinical phenotyping. Stool samples were analyzed using 16S rRNA gene sequencing. Fecal metabolomics were performed using two platforms, nuclear magnetic resonance (NMR) spectroscopy and liquid chromatography-mass spectrometry.Fecal microbiome and metabolome composition in PD was significantly different from controls, with the largest effect size seen in NMR-based metabolome. Microbiome and NMR-based metabolome compositional differences remained significant after comprehensive confounder analyses. Differentially abundant fecal metabolite features and predicted functional changes in PD versus controls included bioactive molecules with putative neuroprotective effects (eg, short chain fatty acids [SCFAs], ubiquinones, and salicylate) and other compounds increasingly implicated in neurodegeneration (eg, ceramides, sphingosine, and trimethylamine N-oxide). In the PD group, cognitive impairment, low body mass index (BMI), frailty, constipation, and low physical activity were associated with fecal metabolome compositional differences. Notably, low SCFAs in PD were significantly associated with poorer cognition and low BMI. Lower butyrate levels correlated with worse postural instability-gait disorder scores.RESULTSFecal microbiome and metabolome composition in PD was significantly different from controls, with the largest effect size seen in NMR-based metabolome. Microbiome and NMR-based metabolome compositional differences remained significant after comprehensive confounder analyses. Differentially abundant fecal metabolite features and predicted functional changes in PD versus controls included bioactive molecules with putative neuroprotective effects (eg, short chain fatty acids [SCFAs], ubiquinones, and salicylate) and other compounds increasingly implicated in neurodegeneration (eg, ceramides, sphingosine, and trimethylamine N-oxide). In the PD group, cognitive impairment, low body mass index (BMI), frailty, constipation, and low physical activity were associated with fecal metabolome compositional differences. Notably, low SCFAs in PD were significantly associated with poorer cognition and low BMI. Lower butyrate levels correlated with worse postural instability-gait disorder scores.Gut microbial function is altered in PD, characterized by differentially abundant metabolic features that provide important biological insights into gut-brain pathophysiology. Their clinical relevance further supports a role for microbial metabolites as potential targets for the development of new biomarkers and therapies in PD. ANN NEUROL 2021;89:546-559.INTERPRETATIONGut microbial function is altered in PD, characterized by differentially abundant metabolic features that provide important biological insights into gut-brain pathophysiology. Their clinical relevance further supports a role for microbial metabolites as potential targets for the development of new biomarkers and therapies in PD. ANN NEUROL 2021;89:546-559.
Author Teh, Cindy Shuan Ju
Bowman, Jeff
Lim, Shen‐Yang
Loke, Mun Fai
Kho, Mee Teck
Yap, Ivan Kok Seng
Yong, Hoi Sen
Tan, Yong Qi
Chong, Chun Wie
Ang, Ban Hong
Lang, Anthony E.
Tan, Ai Huey
Mahadeva, Sanjiv
Tan, Jiun Yan
Song, Sze‐Looi
Author_xml – sequence: 1
  givenname: Ai Huey
  orcidid: 0000-0002-2979-3839
  surname: Tan
  fullname: Tan, Ai Huey
  email: aihuey.tan@gmail.com
  organization: University of Malaya
– sequence: 2
  givenname: Chun Wie
  surname: Chong
  fullname: Chong, Chun Wie
  email: chong.chunwie@monash.edu
  organization: International Medical University
– sequence: 3
  givenname: Shen‐Yang
  surname: Lim
  fullname: Lim, Shen‐Yang
  organization: University of Malaya
– sequence: 4
  givenname: Ivan Kok Seng
  surname: Yap
  fullname: Yap, Ivan Kok Seng
  organization: Sarawak Research and Development Council
– sequence: 5
  givenname: Cindy Shuan Ju
  surname: Teh
  fullname: Teh, Cindy Shuan Ju
  organization: University of Malaya
– sequence: 6
  givenname: Mun Fai
  surname: Loke
  fullname: Loke, Mun Fai
  organization: University of Malaya
– sequence: 7
  givenname: Sze‐Looi
  surname: Song
  fullname: Song, Sze‐Looi
  organization: Xiamen University Malaysia
– sequence: 8
  givenname: Jiun Yan
  surname: Tan
  fullname: Tan, Jiun Yan
  organization: University of Malaya
– sequence: 9
  givenname: Ban Hong
  surname: Ang
  fullname: Ang, Ban Hong
  organization: University of Malaya
– sequence: 10
  givenname: Yong Qi
  surname: Tan
  fullname: Tan, Yong Qi
  organization: University of Malaya
– sequence: 11
  givenname: Mee Teck
  surname: Kho
  fullname: Kho, Mee Teck
  organization: International Medical University
– sequence: 12
  givenname: Jeff
  surname: Bowman
  fullname: Bowman, Jeff
  organization: University of California, San Diego
– sequence: 13
  givenname: Sanjiv
  surname: Mahadeva
  fullname: Mahadeva, Sanjiv
  organization: University Malaya
– sequence: 14
  givenname: Hoi Sen
  surname: Yong
  fullname: Yong, Hoi Sen
  organization: University of Malaya
– sequence: 15
  givenname: Anthony E.
  surname: Lang
  fullname: Lang, Anthony E.
  organization: Toronto Western Hospital
BackLink https://www.ncbi.nlm.nih.gov/pubmed/33274480$$D View this record in MEDLINE/PubMed
BookMark eNp10c9OFTEUBvDGYOQCLnwB08SNLAbaTmfauru5IpLwx4Wum3amgwc7LbYzIXfnI_CMPgnFe9kQWXVxft9Jc749tBNicAi9o-SIEsKOTTBHrFGSvUIL2tS0koyrHbQgdcurhtZ8F-3lfEMIUS0lb9BuXTPBuSQLpE_nCV9Al6IF4_FJF_M6T27EEPA3k35ByDHgz5Cdye4TvnR3eOUhQFd89PEaupI6Cxmuf04ZDymO-GL2E_z9c381QpcP0OvB-Ozebt999OPLyffV1-r86vRstTyvOk4Vq6gU0jTSWdGb1lopCbG0V0Pf8H5QxDJjG2V6IwbRijLjtRhUz1vG29o6yet99HGz9zbF37PLkx4hd857E1ycsy5QtLSRLSv0wzN6E-cUyu-KUoRzJkhT1Putmu3oen2bYDRprZ9OV8DxBpTb5ZzcoDuYzAQxTMmA15Tox3J0KUf_K6ckDp8lnpb-z26334F365ehXl4uN4kHySidww
CitedBy_id crossref_primary_10_1007_s00253_023_12410_w
crossref_primary_10_1038_s43856_024_00630_8
crossref_primary_10_1080_1028415X_2022_2110189
crossref_primary_10_1038_s41420_022_01175_2
crossref_primary_10_3389_fnagi_2023_1185671
crossref_primary_10_3389_fnagi_2022_875261
crossref_primary_10_1038_s41531_024_00732_z
crossref_primary_10_1007_s10072_023_07204_x
crossref_primary_10_1002_mdc3_70029
crossref_primary_10_1039_D4FO00462K
crossref_primary_10_1038_s41531_022_00327_6
crossref_primary_10_3390_nu15204365
crossref_primary_10_3390_ijms252212125
crossref_primary_10_1080_19490976_2022_2125739
crossref_primary_10_1038_s41531_022_00300_3
crossref_primary_10_20517_mrr_2024_35
crossref_primary_10_1080_15548627_2024_2323785
crossref_primary_10_4103_1673_5374_391304
crossref_primary_10_1039_D2FO03825K
crossref_primary_10_3389_fmed_2021_777961
crossref_primary_10_1152_jn_00363_2023
crossref_primary_10_3389_fnagi_2024_1479343
crossref_primary_10_1002_msp2_15
crossref_primary_10_1002_adfm_202206670
crossref_primary_10_3390_ijms22115576
crossref_primary_10_1080_20002297_2024_2331264
crossref_primary_10_1016_j_jns_2024_122889
crossref_primary_10_14802_jmd_22220
crossref_primary_10_3389_fnagi_2021_636545
crossref_primary_10_3233_JPD_230021
crossref_primary_10_1007_s12015_021_10222_x
crossref_primary_10_1038_s41392_023_01399_3
crossref_primary_10_3390_metabo12121222
crossref_primary_10_1016_j_arr_2021_101347
crossref_primary_10_1007_s10072_022_06347_7
crossref_primary_10_1021_acs_jafc_1c06998
crossref_primary_10_3389_fphar_2024_1459655
crossref_primary_10_3390_molecules27113402
crossref_primary_10_3389_fcimb_2023_1296713
crossref_primary_10_4103_1673_5374_373673
crossref_primary_10_1007_s12264_021_00730_8
crossref_primary_10_1016_j_nbd_2022_105780
crossref_primary_10_1038_s42003_023_05548_w
crossref_primary_10_1212_WNL_0000000000013225
crossref_primary_10_4103_NRR_NRR_D_24_00994
crossref_primary_10_1111_jgh_16619
crossref_primary_10_3389_fnagi_2022_955919
crossref_primary_10_1002_jnr_70016
crossref_primary_10_3390_nu16132041
crossref_primary_10_52667_2712_9179_2024_4_2_3_12
crossref_primary_10_3389_fnagi_2022_927625
crossref_primary_10_1002_mco2_315
crossref_primary_10_1002_ctm2_1152
crossref_primary_10_3748_wjg_v30_i3_225
crossref_primary_10_1016_j_jare_2024_03_023
crossref_primary_10_3389_fphar_2024_1388401
crossref_primary_10_3390_applbiosci2010005
crossref_primary_10_3389_fneur_2021_792227
crossref_primary_10_1002_mds_28561
crossref_primary_10_1038_s41531_023_00535_8
crossref_primary_10_1007_s11011_024_01369_w
crossref_primary_10_14802_jmd_21074
crossref_primary_10_3390_diagnostics13142394
crossref_primary_10_1177_1721727X221083763
crossref_primary_10_1007_s00253_023_12789_6
crossref_primary_10_1007_s12035_024_04151_2
crossref_primary_10_1016_j_parkreldis_2022_01_005
crossref_primary_10_3390_microorganisms11061527
crossref_primary_10_1016_j_brainresbull_2022_02_015
crossref_primary_10_1016_j_tifs_2021_07_004
crossref_primary_10_3390_pathophysiology31020019
crossref_primary_10_1007_s12035_021_02625_1
crossref_primary_10_1111_cns_13990
crossref_primary_10_1016_j_parkreldis_2023_105775
crossref_primary_10_3389_fnagi_2022_881872
crossref_primary_10_1016_j_parkreldis_2021_11_017
crossref_primary_10_1155_2023_1566684
crossref_primary_10_3390_ijms232012289
crossref_primary_10_3389_fneur_2023_1185375
crossref_primary_10_14802_jmd_21085
crossref_primary_10_1016_j_jep_2023_116893
crossref_primary_10_1007_s10048_024_00779_3
crossref_primary_10_1101_cshperspect_a041618
crossref_primary_10_1016_j_arr_2022_101759
crossref_primary_10_1016_j_neuroscience_2023_06_010
crossref_primary_10_1016_j_ymeth_2024_10_009
crossref_primary_10_1038_s41531_023_00511_2
crossref_primary_10_1007_s12035_024_04584_9
crossref_primary_10_1016_j_fcr_2022_108521
crossref_primary_10_3233_JPD_240172
crossref_primary_10_3389_fnagi_2022_993615
crossref_primary_10_2174_1871527322666230203140805
crossref_primary_10_1002_2211_5463_13651
crossref_primary_10_1186_s40168_023_01475_4
crossref_primary_10_1080_19490976_2025_2454937
crossref_primary_10_1186_s40035_023_00392_8
crossref_primary_10_3389_fnagi_2022_1026688
crossref_primary_10_3390_nu15071737
crossref_primary_10_1016_j_nbd_2022_105614
crossref_primary_10_1016_j_neuropharm_2021_108839
crossref_primary_10_1021_acsomega_3c08184
crossref_primary_10_1016_j_nbd_2022_105695
crossref_primary_10_3390_biomedicines10092057
crossref_primary_10_1016_j_jad_2025_02_091
crossref_primary_10_3389_fphar_2022_893567
crossref_primary_10_3389_fmicb_2022_801587
crossref_primary_10_3389_fimmu_2022_937555
crossref_primary_10_3389_fnins_2024_1488820
crossref_primary_10_3389_fmicb_2022_869931
crossref_primary_10_3390_ijms25179489
crossref_primary_10_1038_s41582_022_00681_2
crossref_primary_10_1002_ajmg_b_32959
crossref_primary_10_3389_fnint_2022_1054627
crossref_primary_10_1016_j_parkreldis_2024_105989
crossref_primary_10_1186_s12929_022_00839_6
crossref_primary_10_5582_bst_2024_01352
crossref_primary_10_4103_NRR_NRR_D_23_01776
crossref_primary_10_1002_mds_28922
crossref_primary_10_3390_biomedicines11082089
crossref_primary_10_1016_j_arr_2024_102466
crossref_primary_10_1007_s12264_023_01123_9
crossref_primary_10_1016_j_drudis_2022_08_002
crossref_primary_10_1155_ijcp_5511146
crossref_primary_10_3390_nu14193967
crossref_primary_10_3389_fendo_2021_748254
Cites_doi 10.3390/nu10101398
10.1038/s41591-019-0439-x
10.1016/j.pnmrs.2017.01.001
10.3389/fnins.2019.00330
10.1016/j.parkreldis.2018.06.020
10.1038/nature11708
10.3233/JPD-171103
10.1002/mds.28248
10.1002/mds.25522
10.1016/bs.pbr.2020.01.004
10.1002/mds.26069
10.1016/j.bbr.2015.05.052
10.1038/s41575-019-0173-3
10.1001/jamaneurol.2019.4611
10.1038/npjbiofilms.2016.4
10.1002/mds.27203
10.1016/j.cca.2019.10.038
10.1002/mds.23566
10.1007/BF02260943
10.1186/1471-2105-11-538
10.1172/JCI129987
10.1016/B978-0-323-07447-6.00012-0
10.3390/ijms20061482
10.1002/mds.27581
10.1128/CMR.00053-08
10.3389/fimmu.2019.00277
10.1002/ana.24901
10.1016/j.parkreldis.2018.06.027
10.1186/s12866-019-1602-8
10.1038/s41531-017-0014-4
10.1021/pr901188e
10.1016/j.neuropharm.2012.01.026
10.1016/j.celrep.2019.12.078
10.1016/j.aca.2018.05.031
10.1016/j.parkreldis.2016.08.019
10.3389/fmicb.2017.00536
10.1111/nure.12027
10.1001/jamaneurol.2014.131
10.1016/j.ebiom.2019.05.064
10.1038/s41575-019-0157-3
10.1186/s12915-020-00775-7
10.1371/journal.pone.0135868
10.1038/s41586-020-2269-x
10.1002/mds.28052
10.1002/ana.25788
10.1212/WNL.0000000000010998
10.1038/nrendo.2015.128
10.1016/j.parkreldis.2014.02.019
10.1016/j.parkreldis.2014.12.009
10.1002/mds.26942
10.1038/s41564-018-0306-4
10.1016/S0140-6736(14)61393-3
10.1016/j.jand.2018.01.014
10.1128/mSystems.00561-20
10.1073/pnas.1000097107
10.1016/S0140-6736(09)60492-X
10.1002/syn.21658
10.1016/S1474-4422(19)30024-9
10.3748/wjg.v21.i37.10609
10.1038/nature11319
10.1038/s41583-020-00381-0
10.1136/gutjnl-2018-316723
10.1038/nature06882
10.1371/journal.pone.0028032
10.3390/nu11071633
10.3390/nu7010045
10.1038/s41598-017-13601-y
10.1038/nature11053
10.3233/JPD-191711
10.1016/j.jnutbio.2019.03.021
10.1007/s00415-019-09320-1
10.3390/microorganisms6030075
10.1136/gutjnl-2018-316844
10.1128/mSystems.00321-18
10.1056/NEJMra1600266
10.3390/cells8010027
ContentType Journal Article
Copyright 2020 American Neurological Association
2020 American Neurological Association.
2021 American Neurological Association
Copyright_xml – notice: 2020 American Neurological Association
– notice: 2020 American Neurological Association.
– notice: 2021 American Neurological Association
DBID AAYXX
CITATION
CGR
CUY
CVF
ECM
EIF
NPM
7TK
7U7
C1K
K9.
7X8
DOI 10.1002/ana.25982
DatabaseName CrossRef
Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
Neurosciences Abstracts
Toxicology Abstracts
Environmental Sciences and Pollution Management
ProQuest Health & Medical Complete (Alumni)
MEDLINE - Academic
DatabaseTitle CrossRef
MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
ProQuest Health & Medical Complete (Alumni)
Toxicology Abstracts
Neurosciences Abstracts
Environmental Sciences and Pollution Management
MEDLINE - Academic
DatabaseTitleList ProQuest Health & Medical Complete (Alumni)
MEDLINE

MEDLINE - Academic
Database_xml – sequence: 1
  dbid: NPM
  name: PubMed
  url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 2
  dbid: EIF
  name: MEDLINE
  url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search
  sourceTypes: Index Database
DeliveryMethod fulltext_linktorsrc
Discipline Medicine
EISSN 1531-8249
EndPage 559
ExternalDocumentID 33274480
10_1002_ana_25982
ANA25982
Genre article
Research Support, Non-U.S. Gov't
Journal Article
GrantInformation_xml – fundername: University of Malaya‐Ministry of Higher Education High Impact Research Grant
  funderid: UM.0000017/HIR.C3
– fundername: University of Malaya Parkinson and Movement Disorders Research Program
  funderid: PV035‐2017
GroupedDBID ---
.3N
.55
.GA
.GJ
.Y3
05W
0R~
10A
1CY
1L6
1OB
1OC
1ZS
23M
2QL
31~
33P
3O-
3SF
3WU
4.4
4ZD
50Y
50Z
51W
51X
52M
52N
52O
52P
52R
52S
52T
52U
52V
52W
52X
53G
5GY
5VS
66C
6J9
6P2
6PF
702
7PT
8-0
8-1
8-3
8-4
8-5
8UM
930
A01
A03
AAEJM
AAESR
AAEVG
AAHHS
AAHQN
AAIPD
AAMNL
AANHP
AANLZ
AAONW
AAQQT
AASGY
AAWTL
AAXRX
AAYCA
AAZKR
ABCQN
ABCUV
ABEML
ABIJN
ABIVO
ABJNI
ABLJU
ABOCM
ABPVW
ABQWH
ABXGK
ACAHQ
ACBMB
ACBWZ
ACCFJ
ACCZN
ACGFO
ACGFS
ACGOF
ACMXC
ACPOU
ACPRK
ACRPL
ACRZS
ACSCC
ACXBN
ACXQS
ACYXJ
ADBBV
ADBTR
ADEOM
ADIZJ
ADKYN
ADMGS
ADNMO
ADOZA
ADXAS
ADZMN
ADZOD
AEEZP
AEGXH
AEIGN
AEIMD
AENEX
AEQDE
AEUQT
AEUYR
AFAZI
AFBPY
AFFNX
AFFPM
AFGKR
AFPWT
AFRAH
AFWVQ
AFZJQ
AHBTC
AHMBA
AI.
AIACR
AIAGR
AITYG
AIURR
AIWBW
AJBDE
AJJEV
ALAGY
ALMA_UNASSIGNED_HOLDINGS
ALUQN
ALVPJ
AMBMR
AMYDB
ASPBG
ATUGU
AVWKF
AZBYB
AZFZN
AZVAB
BAFTC
BDRZF
BFHJK
BHBCM
BMXJE
BROTX
BRXPI
BY8
C45
CS3
D-6
D-7
D-E
D-F
DCZOG
DPXWK
DR1
DR2
DRFUL
DRMAN
DRSTM
EBS
EJD
EMOBN
F00
F01
F04
F5P
F8P
FEDTE
FUBAC
FYBCS
G-S
G.N
GNP
GODZA
GOZPB
GRPMH
H.X
HBH
HF~
HGLYW
HHY
HHZ
HVGLF
HZ~
IX1
J0M
J5H
JPC
KBYEO
KD1
KQQ
L7B
LATKE
LAW
LC2
LC3
LEEKS
LH4
LITHE
LOXES
LP6
LP7
LUTES
LW6
LXL
LXN
LXY
LYRES
M6M
MEWTI
MK4
MRFUL
MRMAN
MRSTM
MSFUL
MSMAN
MSSTM
MXFUL
MXMAN
MXSTM
N04
N05
N4W
N9A
NF~
NNB
O66
O9-
OHT
OIG
OVD
P2P
P2W
P2X
P2Z
P4B
P4D
PALCI
PQQKQ
Q.-
Q.N
Q11
QB0
QRW
R.K
RIWAO
RJQFR
ROL
RWD
RWI
RX1
SAMSI
SJN
SUPJJ
TEORI
UB1
V2E
V8K
V9Y
VH1
W8V
W99
WBKPD
WH7
WHWMO
WIB
WIH
WIJ
WIK
WJL
WOHZO
WQJ
WRC
WUP
WVDHM
WXI
WXSBR
X7M
XG1
XJT
XPP
XSW
XV2
YOC
YQJ
ZGI
ZRF
ZRR
ZXP
ZZTAW
~IA
~WT
~X8
AAYXX
AEYWJ
AGHNM
AGQPQ
AGYGG
CITATION
CGR
CUY
CVF
ECM
EIF
NPM
7TK
7U7
AAMMB
AEFGJ
AGXDD
AIDQK
AIDYY
C1K
K9.
7X8
ID FETCH-LOGICAL-c4192-1878a58eb7da6bb8800b1d9fd54df90b2ab59ada7f76700b437f9d462463be843
IEDL.DBID DR2
ISSN 0364-5134
1531-8249
IngestDate Fri Jul 11 06:04:02 EDT 2025
Fri Jul 25 12:21:28 EDT 2025
Wed Feb 19 02:28:20 EST 2025
Tue Jul 01 02:24:13 EDT 2025
Thu Apr 24 22:53:06 EDT 2025
Wed Jan 22 16:29:58 EST 2025
IsPeerReviewed true
IsScholarly true
Issue 3
Language English
License 2020 American Neurological Association.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c4192-1878a58eb7da6bb8800b1d9fd54df90b2ab59ada7f76700b437f9d462463be843
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 14
content type line 23
ORCID 0000-0002-2979-3839
PMID 33274480
PQID 2490442705
PQPubID 946345
PageCount 14
ParticipantIDs proquest_miscellaneous_2467615862
proquest_journals_2490442705
pubmed_primary_33274480
crossref_citationtrail_10_1002_ana_25982
crossref_primary_10_1002_ana_25982
wiley_primary_10_1002_ana_25982_ANA25982
ProviderPackageCode CITATION
AAYXX
PublicationCentury 2000
PublicationDate March 2021
PublicationDateYYYYMMDD 2021-03-01
PublicationDate_xml – month: 03
  year: 2021
  text: March 2021
PublicationDecade 2020
PublicationPlace Hoboken, USA
PublicationPlace_xml – name: Hoboken, USA
– name: United States
– name: Minneapolis
PublicationTitle Annals of neurology
PublicationTitleAlternate Ann Neurol
PublicationYear 2021
Publisher John Wiley & Sons, Inc
Wiley Subscription Services, Inc
Publisher_xml – name: John Wiley & Sons, Inc
– name: Wiley Subscription Services, Inc
References 2010; 11
2017; 7
2017; 8
2013; 28
2017; 3
2012; 486
2017; 81
2019; 11
2019; 10
2013; 67
2019; 13
2015; 386
2015; 30
2018; 1030
2016; 32
2019; 16
2013; 71
2019; 19
2020; (Epub ahead of print)
2019; 18
2019; 129
2012; 488
2014; 20
2020; 18
2012; 491
2018; 6
2020; 5
2015; 291
2019; 20
2020; 252
2019; 68
2017; 32
2019; 25
2019; 69
2020; 88
2011; 26
2018; 33
2014; 7
2010; 9
2012; 62
2019; 8
2009; 22
2019; 9
2019; 4
2012
2020; 581
2019; 34
2015; 11
2015; 10
2020; 501
2020; 35
2020; 77
2020; 267
2009; 373
2018; 67
2011; 6
1994; 8
2011; 108
2016; 2
2020; 30
2019; 44
2018; 118
2015; 21
2016; 375
2014
2020; 21
2018; 56
2008; 453
2017; 100
2018; 10
2014; 71
2018; 57
e_1_2_9_75_1
e_1_2_9_31_1
e_1_2_9_52_1
e_1_2_9_50_1
e_1_2_9_73_1
e_1_2_9_10_1
e_1_2_9_35_1
e_1_2_9_56_1
e_1_2_9_12_1
e_1_2_9_33_1
e_1_2_9_54_1
e_1_2_9_71_1
e_1_2_9_14_1
e_1_2_9_39_1
e_1_2_9_16_1
e_1_2_9_37_1
e_1_2_9_58_1
e_1_2_9_18_1
e_1_2_9_41_1
e_1_2_9_64_1
e_1_2_9_20_1
e_1_2_9_62_1
e_1_2_9_22_1
e_1_2_9_45_1
e_1_2_9_68_1
e_1_2_9_24_1
e_1_2_9_43_1
e_1_2_9_66_1
e_1_2_9_8_1
e_1_2_9_6_1
e_1_2_9_4_1
e_1_2_9_60_1
e_1_2_9_2_1
Clavel T (e_1_2_9_42_1) 2014
e_1_2_9_26_1
e_1_2_9_49_1
e_1_2_9_28_1
e_1_2_9_47_1
e_1_2_9_30_1
e_1_2_9_53_1
e_1_2_9_74_1
e_1_2_9_51_1
e_1_2_9_72_1
e_1_2_9_11_1
e_1_2_9_34_1
e_1_2_9_57_1
e_1_2_9_78_1
e_1_2_9_13_1
e_1_2_9_32_1
e_1_2_9_55_1
e_1_2_9_76_1
e_1_2_9_70_1
e_1_2_9_15_1
e_1_2_9_38_1
e_1_2_9_17_1
e_1_2_9_36_1
e_1_2_9_59_1
e_1_2_9_19_1
e_1_2_9_63_1
e_1_2_9_40_1
e_1_2_9_61_1
e_1_2_9_21_1
e_1_2_9_46_1
e_1_2_9_67_1
Tan AH (e_1_2_9_77_1) 2020
e_1_2_9_23_1
e_1_2_9_44_1
e_1_2_9_65_1
e_1_2_9_7_1
e_1_2_9_5_1
e_1_2_9_3_1
e_1_2_9_9_1
e_1_2_9_25_1
e_1_2_9_27_1
e_1_2_9_48_1
e_1_2_9_69_1
e_1_2_9_29_1
References_xml – volume: 291
  start-page: 306
  year: 2015
  end-page: 314
  article-title: Beneficial effects of sodium butyrate in 6‐OHDA induced neurotoxicity and behavioral abnormalities: modulation of histone deacetylase activity
  publication-title: Behav Brain Res
– volume: 81
  start-page: 369
  year: 2017
  end-page: 382
  article-title: The gut microbiome in human neurological disease: a review
  publication-title: Ann Neurol
– volume: 8
  start-page: 27
  year: 2019
  article-title: The role of lipids in Parkinson's disease
  publication-title: Cells
– volume: 26
  start-page: 889
  year: 2011
  end-page: 892
  article-title: Prevalence of small intestinal bacterial overgrowth in Parkinson's disease
  publication-title: Mov Disord
– volume: 88
  start-page: 320
  year: 2020
  end-page: 331
  article-title: Gut microbiome signatures of risk and prodromal markers of Parkinson's disease
  publication-title: Ann Neurol
– volume: 33
  start-page: 174
  year: 2018
  end-page: 176
  article-title: Altered gut microbiome and metabolome in patients with multiple system atrophy
  publication-title: Mov Disord
– volume: 62
  start-page: 2409
  year: 2012
  end-page: 2412
  article-title: The histone deacetylase inhibitor, sodium butyrate, alleviates cognitive deficits in pre‐motor stage PD
  publication-title: Neuropharmacology
– volume: 6
  start-page: 75
  year: 2018
  article-title: Akkermansia muciniphila in the human gastrointestinal tract: when, where, and how?
  publication-title: Microorganisms
– volume: 267
  start-page: 2507
  year: 2020
  end-page: 2523
  article-title: Parkinson's disease and the gastrointestinal microbiome
  publication-title: J Neurol
– volume: 11
  start-page: 577
  year: 2015
  end-page: 591
  article-title: Short‐chain fatty acids in control of body weight and insulin sensitivity
  publication-title: Nat Rev Endocrinol
– volume: 7
  start-page: 433
  year: 2017
  end-page: 450
  article-title: The role of lipids interacting with alpha‐synuclein in the pathogenesis of Parkinson's disease
  publication-title: J Parkinsons Dis
– volume: 100
  start-page: 1
  year: 2017
  end-page: 16
  article-title: Beyond the paradigm: combining mass spectrometry and nuclear magnetic resonance for metabolomics
  publication-title: Prog Nucl Magn Reson Spectrosc
– volume: 35
  start-page: 1208
  year: 2020
  end-page: 1217
  article-title: Microbiota composition and metabolism are associated with gut function in Parkinson's disease
  publication-title: Mov Disord
– volume: 44
  start-page: 691
  year: 2019
  end-page: 707
  article-title: Gut microbiota in Parkinson's disease: temporal stability and relations to disease progression
  publication-title: EBioMedicine
– volume: 252
  start-page: 357
  year: 2020
  end-page: 450
  article-title: The gut microbiome in Parkinson's disease: a culprit or a bystander?
  publication-title: Prog Brain Res
– volume: 71
  start-page: 483
  year: 2013
  end-page: 499
  article-title: Ethanol metabolism and its effects on the intestinal epithelial barrier
  publication-title: Nutr Rev
– volume: 21
  start-page: 10609
  year: 2015
  end-page: 10620
  article-title: Brain‐gut‐microbiota axis in Parkinson's disease
  publication-title: World J Gastroenterol
– volume: 11
  year: 2019
  article-title: Gut microbiota, muscle mass and function in aging: a focus on physical frailty and sarcopenia
  publication-title: Nutrients
– volume: 10
  start-page: 277
  year: 2019
  article-title: Short chain fatty acids (SCFAs)‐mediated gut epithelial and immune regulation and its relevance for inflammatory bowel diseases
  publication-title: Front Immunol
– volume: 20
  start-page: 535
  year: 2014
  end-page: 540
  article-title: Small intestinal bacterial overgrowth in Parkinson's disease
  publication-title: Parkinsonism Relat Disord
– volume: 34
  start-page: 396
  year: 2019
  end-page: 405
  article-title: Unraveling gut microbiota in Parkinson's disease and atypical parkinsonism
  publication-title: Mov Disord
– volume: 22
  start-page: 349
  year: 2009
  end-page: 369
  article-title: Enterotoxigenic Bacteroides fragilis: a rogue among symbiotes
  publication-title: Clin Microbiol Rev
– volume: 3
  start-page: 13
  year: 2017
  article-title: Early‐onset parkinsonism in a pedigree with phosphoglycerate kinase deficiency and a heterozygous carrier: do PGK‐1 mutations contribute to vulnerability to parkinsonism?
  publication-title: NPJ Parkinsons Dis
– start-page: 105
  year: 2012
  end-page: 120
– volume: 30
  start-page: 367
  year: 2020
  end-page: 380
  article-title: Probiotic bacillus subtilis protects against alpha‐synuclein aggregation in C. elegans
  publication-title: Cell Rep
– volume: 21
  start-page: 221
  year: 2015
  end-page: 255
  article-title: Helicobacter pylori infection is associated with worse severity of Parkinson's disease
  publication-title: Parkinsonism Relat Disord
– volume: 4
  start-page: e00321
  year: 2019
  end-page: e00318
  article-title: Alterations in gut glutamate metabolism associated with changes in gut microbiota composition in children with autism spectrum disorder
  publication-title: mSystems
– volume: 108
  start-page: 4586
  year: 2011
  end-page: 4591
  article-title: Composition, variability, and temporal stability of the intestinal microbiota of the elderly
  publication-title: Proc Natl Acad Sci U S A
– 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: 57
  start-page: 78
  year: 2018
  end-page: 79
  article-title: Inflammatory bowel disease and risk of Parkinson's disease
  publication-title: Parkinsonism Relat Disord
– volume: 13
  start-page: 330
  year: 2019
  article-title: Ceramides in Parkinson's disease: from recent evidence to new hypotheses
  publication-title: Front Neurosci
– start-page: 201
  year: 2014
  end-page: 238
– volume: 10
  year: 2015
  article-title: Microbial communities can be described by metabolic structure: a general framework and application to a seasonally variable, depth‐stratified microbial community from the coastal West Antarctic peninsula
  publication-title: PLoS One
– volume: 67
  start-page: 1716
  year: 2018
  end-page: 1725
  article-title: Human gut microbiome: hopes, threats and promises
  publication-title: Gut
– volume: 501
  start-page: 165
  year: 2020
  end-page: 173
  article-title: Higher cerebrospinal fluid to plasma ratio of p‐cresol sulfate and indoxyl sulfate in patients with Parkinson's disease
  publication-title: Clin Chim Acta
– volume: 28
  start-page: 1241
  year: 2013
  end-page: 1249
  article-title: The role of small intestinal bacterial overgrowth in Parkinson's disease
  publication-title: Mov Disord
– volume: 1030
  start-page: 1
  year: 2018
  end-page: 24
  article-title: A review on human fecal metabolomics: methods, applications and the human fecal metabolome database
  publication-title: Anal Chim Acta
– volume: 21
  start-page: 717
  year: 2020
  end-page: 731
  article-title: Gut microbial molecules in behavioural and neurodegenerative conditions
  publication-title: Nat Rev Neurosci
– volume: 386
  start-page: 896
  year: 2015
  end-page: 912
  article-title: Parkinson's disease
  publication-title: Lancet
– volume: (Epub ahead of print)
  year: 2020
  article-title: Probiotics for constipation in Parkinson's disease: a randomized placebo‐controlled study
  publication-title: Neurology
– volume: 7
  start-page: 45
  year: 2014
  end-page: 73
  article-title: Understanding how commensal obligate anaerobic bacteria regulate immune functions in the large intestine
  publication-title: Nutrients
– volume: 118
  start-page: 1249
  year: 2018
  end-page: 1262
  article-title: Consistency and generalizability of dietary patterns in a multiethnic working population
  publication-title: J Acad Nutr Diet
– volume: 2
  year: 2016
  article-title: A perspective on 16S rRNA operational taxonomic unit clustering using sequence similarity
  publication-title: NPJ Biofilms Microbiomes
– volume: 32
  start-page: 739
  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: 8
  start-page: 536
  year: 2017
  article-title: Global fecal and plasma metabolic dynamics related to helicobacter pylori eradication
  publication-title: Front Microbiol
– volume: 373
  start-page: 2055
  year: 2009
  end-page: 2066
  article-title: Parkinson's disease
  publication-title: Lancet
– volume: 581
  start-page: 310
  year: 2020
  end-page: 315
  article-title: Statin therapy is associated with lower prevalence of gut microbiota dysbiosis
  publication-title: Nature
– volume: 71
  start-page: 543
  year: 2014
  end-page: 552
  article-title: A randomized clinical trial of high‐dosage coenzyme Q10 in early Parkinson disease: no evidence of benefit
  publication-title: JAMA Neurol
– volume: 20
  start-page: 1482
  year: 2019
  article-title: Glutamatergic signaling along the microbiota‐gut‐brain axis
  publication-title: Int J Mol Sci
– volume: 77
  start-page: 427
  year: 2020
  end-page: 434
  article-title: Ambroxol for the treatment of patients with Parkinson disease with and without glucocerebrosidase gene mutations: a nonrandomized, noncontrolled trial
  publication-title: JAMA Neurol
– volume: 16
  start-page: 461
  year: 2019
  end-page: 478
  article-title: The role of short‐chain fatty acids in microbiota‐gut‐brain communication
  publication-title: Nat Rev Gastroenterol Hepatol
– volume: 18
  start-page: 62
  year: 2020
  article-title: Parkinson's disease‐associated alterations of the gut microbiome predict disease‐relevant changes in metabolic functions
  publication-title: BMC Biol
– volume: 5
  start-page: e00561
  year: 2020
  end-page: e00520
  article-title: Gut microbiota and metabolome alterations associated with Parkinson's disease
  publication-title: mSystems
– volume: 9
  start-page: 2996
  year: 2010
  end-page: 3004
  article-title: Urinary metabolic phenotyping differentiates children with autism from their unaffected siblings and age‐matched controls
  publication-title: J Proteome Res
– volume: 16
  start-page: 605
  year: 2019
  end-page: 616
  article-title: Probiotics and prebiotics in intestinal health and disease: from biology to the clinic
  publication-title: Nat Rev Gastroenterol Hepatol
– volume: 10
  start-page: 1398
  year: 2018
  article-title: Implication of trimethylamine N‐oxide (TMAO) in disease: potential biomarker or new therapeutic target
  publication-title: Nutrients
– volume: 488
  start-page: 178
  year: 2012
  end-page: 184
  article-title: Gut microbiota composition correlates with diet and health in the elderly
  publication-title: Nature
– volume: 8
  start-page: 223
  year: 1994
  end-page: 228
  article-title: Impaired oxidative decarboxylation of pyruvate in fibroblasts from patients with Parkinson's disease
  publication-title: J Neural Transm
– volume: 68
  start-page: 829
  year: 2019
  end-page: 843
  article-title: Role of TLR4 in the gut‐brain axis in Parkinson's disease: a translational study from men to mice
  publication-title: Gut
– volume: 453
  start-page: 396
  year: 2008
  end-page: 400
  article-title: Human metabolic phenotype diversity and its association with diet and blood pressure
  publication-title: Nature
– volume: 11
  start-page: 538
  year: 2010
  article-title: Pplacer: linear time maximum‐likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree
  publication-title: BMC Bioinformatics
– volume: 375
  start-page: 2369
  year: 2016
  end-page: 2379
  article-title: The human intestinal microbiome in health and disease
  publication-title: N Engl J Med
– volume: 6
  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: 129
  start-page: 4539
  year: 2019
  end-page: 4549
  article-title: Enhancing glycolysis attenuates Parkinson's disease progression in models and clinical databases
  publication-title: J Clin Invest
– volume: 486
  start-page: 222
  year: 2012
  end-page: 227
  article-title: Human gut microbiome viewed across age and geography
  publication-title: Nature
– volume: 30
  start-page: 350
  year: 2015
  end-page: 358
  article-title: Gut microbiota are related to Parkinson's disease and clinical phenotype
  publication-title: Mov Disord
– volume: 491
  start-page: 384
  year: 2012
  end-page: 392
  article-title: Metabolic phenotyping in clinical and surgical environments
  publication-title: Nature
– volume: 25
  start-page: 716
  year: 2019
  end-page: 729
  article-title: The pros, cons, and many unknowns of probiotics
  publication-title: Nat Med
– volume: 67
  start-page: 502
  year: 2013
  end-page: 514
  article-title: Sodium salicylate protects against rotenone‐induced parkinsonism in rats
  publication-title: Synapse
– volume: 4
  start-page: 293
  year: 2019
  end-page: 305
  article-title: Gut microbiome structure and metabolic activity in inflammatory bowel disease
  publication-title: Nat Microbiol
– volume: 35
  start-page: 2250
  issue: 12
  year: 2020
  end-page: 2260
  article-title: Helicobacter pylori eradication in Parkinson's disease: a randomized placebo‐controlled trial
  publication-title: Mov Disord
– volume: 56
  start-page: 58
  year: 2018
  end-page: 64
  article-title: Altered body composition, sarcopenia, frailty, and their clinico‐biological correlates, in Parkinson's disease
  publication-title: Parkinsonism Relat Disord
– volume: 18
  start-page: 573
  year: 2019
  end-page: 586
  article-title: CSF and blood biomarkers for Parkinson's disease
  publication-title: Lancet Neurol
– volume: 7
  year: 2017
  article-title: Gut microbiome alterations in Alzheimer's disease
  publication-title: Sci Rep
– volume: 9
  start-page: S297
  year: 2019
  end-page: S312
  article-title: Increasing comparability and utility of gut microbiome studies in Parkinson's disease: a systematic review
  publication-title: J Parkinsons Dis
– volume: 19
  year: 2019
  article-title: Cohabitation is associated with a greater resemblance in gut microbiota which can impact cardiometabolic and inflammatory risk
  publication-title: BMC Microbiol
– volume: 69
  start-page: 73
  year: 2019
  end-page: 86
  article-title: Probiotics mixture increases butyrate, and subsequently rescues the nigral dopaminergic neurons from MPTP and rotenone‐induced neurotoxicity
  publication-title: J Nutr Biochem
– ident: e_1_2_9_56_1
  doi: 10.3390/nu10101398
– ident: e_1_2_9_36_1
  doi: 10.1038/s41591-019-0439-x
– ident: e_1_2_9_76_1
  doi: 10.1016/j.pnmrs.2017.01.001
– ident: e_1_2_9_57_1
  doi: 10.3389/fnins.2019.00330
– ident: e_1_2_9_22_1
  doi: 10.1016/j.parkreldis.2018.06.020
– ident: e_1_2_9_18_1
  doi: 10.1038/nature11708
– ident: e_1_2_9_52_1
  doi: 10.3233/JPD-171103
– ident: e_1_2_9_78_1
  doi: 10.1002/mds.28248
– ident: e_1_2_9_4_1
  doi: 10.1002/mds.25522
– ident: e_1_2_9_15_1
  doi: 10.1016/bs.pbr.2020.01.004
– ident: e_1_2_9_12_1
  doi: 10.1002/mds.26069
– ident: e_1_2_9_46_1
  doi: 10.1016/j.bbr.2015.05.052
– ident: e_1_2_9_38_1
  doi: 10.1038/s41575-019-0173-3
– ident: e_1_2_9_59_1
  doi: 10.1001/jamaneurol.2019.4611
– ident: e_1_2_9_26_1
  doi: 10.1038/npjbiofilms.2016.4
– ident: e_1_2_9_25_1
  doi: 10.1002/mds.27203
– ident: e_1_2_9_54_1
  doi: 10.1016/j.cca.2019.10.038
– ident: e_1_2_9_65_1
  doi: 10.1002/mds.23566
– ident: e_1_2_9_61_1
  doi: 10.1007/BF02260943
– ident: e_1_2_9_27_1
  doi: 10.1186/1471-2105-11-538
– ident: e_1_2_9_60_1
  doi: 10.1172/JCI129987
– ident: e_1_2_9_41_1
  doi: 10.1016/B978-0-323-07447-6.00012-0
– ident: e_1_2_9_66_1
  doi: 10.3390/ijms20061482
– ident: e_1_2_9_8_1
  doi: 10.1002/mds.27581
– ident: e_1_2_9_40_1
  doi: 10.1128/CMR.00053-08
– ident: e_1_2_9_50_1
  doi: 10.3389/fimmu.2019.00277
– ident: e_1_2_9_7_1
  doi: 10.1002/ana.24901
– ident: e_1_2_9_69_1
  doi: 10.1016/j.parkreldis.2018.06.027
– ident: e_1_2_9_74_1
  doi: 10.1186/s12866-019-1602-8
– ident: e_1_2_9_62_1
  doi: 10.1038/s41531-017-0014-4
– ident: e_1_2_9_30_1
  doi: 10.1021/pr901188e
– start-page: 201
  volume-title: The prokaryotes
  year: 2014
  ident: e_1_2_9_42_1
– ident: e_1_2_9_47_1
  doi: 10.1016/j.neuropharm.2012.01.026
– ident: e_1_2_9_58_1
  doi: 10.1016/j.celrep.2019.12.078
– ident: e_1_2_9_20_1
  doi: 10.1016/j.aca.2018.05.031
– ident: e_1_2_9_37_1
  doi: 10.1016/j.parkreldis.2016.08.019
– ident: e_1_2_9_31_1
  doi: 10.3389/fmicb.2017.00536
– ident: e_1_2_9_64_1
  doi: 10.1111/nure.12027
– ident: e_1_2_9_63_1
  doi: 10.1001/jamaneurol.2014.131
– ident: e_1_2_9_11_1
  doi: 10.1016/j.ebiom.2019.05.064
– ident: e_1_2_9_43_1
  doi: 10.1038/s41575-019-0157-3
– ident: e_1_2_9_19_1
  doi: 10.1186/s12915-020-00775-7
– ident: e_1_2_9_28_1
  doi: 10.1371/journal.pone.0135868
– ident: e_1_2_9_73_1
  doi: 10.1038/s41586-020-2269-x
– ident: e_1_2_9_10_1
  doi: 10.1002/mds.28052
– ident: e_1_2_9_17_1
  doi: 10.1002/ana.25788
– year: 2020
  ident: e_1_2_9_77_1
  article-title: Probiotics for constipation in Parkinson's disease: a randomized placebo‐controlled study
  publication-title: Neurology
  doi: 10.1212/WNL.0000000000010998
– ident: e_1_2_9_70_1
  doi: 10.1038/nrendo.2015.128
– ident: e_1_2_9_6_1
  doi: 10.1016/j.parkreldis.2014.02.019
– ident: e_1_2_9_5_1
  doi: 10.1016/j.parkreldis.2014.12.009
– ident: e_1_2_9_9_1
  doi: 10.1002/mds.26942
– ident: e_1_2_9_72_1
  doi: 10.1038/s41564-018-0306-4
– ident: e_1_2_9_2_1
  doi: 10.1016/S0140-6736(14)61393-3
– ident: e_1_2_9_24_1
  doi: 10.1016/j.jand.2018.01.014
– ident: e_1_2_9_21_1
  doi: 10.1128/mSystems.00561-20
– ident: e_1_2_9_33_1
  doi: 10.1073/pnas.1000097107
– ident: e_1_2_9_23_1
  doi: 10.1016/S0140-6736(09)60492-X
– ident: e_1_2_9_68_1
  doi: 10.1002/syn.21658
– ident: e_1_2_9_51_1
  doi: 10.1016/S1474-4422(19)30024-9
– ident: e_1_2_9_49_1
  doi: 10.3748/wjg.v21.i37.10609
– ident: e_1_2_9_13_1
  doi: 10.1038/nature11319
– ident: e_1_2_9_32_1
  doi: 10.1038/s41583-020-00381-0
– ident: e_1_2_9_35_1
  doi: 10.1136/gutjnl-2018-316723
– ident: e_1_2_9_29_1
  doi: 10.1038/nature06882
– ident: e_1_2_9_44_1
  doi: 10.1371/journal.pone.0028032
– ident: e_1_2_9_71_1
  doi: 10.3390/nu11071633
– ident: e_1_2_9_39_1
  doi: 10.3390/nu7010045
– ident: e_1_2_9_55_1
  doi: 10.1038/s41598-017-13601-y
– ident: e_1_2_9_75_1
  doi: 10.1038/nature11053
– ident: e_1_2_9_3_1
  doi: 10.3233/JPD-191711
– ident: e_1_2_9_48_1
  doi: 10.1016/j.jnutbio.2019.03.021
– ident: e_1_2_9_14_1
  doi: 10.1007/s00415-019-09320-1
– ident: e_1_2_9_34_1
  doi: 10.3390/microorganisms6030075
– ident: e_1_2_9_45_1
  doi: 10.1136/gutjnl-2018-316844
– ident: e_1_2_9_67_1
  doi: 10.1128/mSystems.00321-18
– ident: e_1_2_9_16_1
  doi: 10.1056/NEJMra1600266
– ident: e_1_2_9_53_1
  doi: 10.3390/cells8010027
SSID ssj0009610
Score 2.6442068
Snippet Objective Gut microbiome alterations in Parkinson disease (PD) have been reported repeatedly, but their functional relevance remains unclear. Fecal...
Gut microbiome alterations in Parkinson disease (PD) have been reported repeatedly, but their functional relevance remains unclear. Fecal metabolomics, which...
ObjectiveGut microbiome alterations in Parkinson disease (PD) have been reported repeatedly, but their functional relevance remains unclear. Fecal...
SourceID proquest
pubmed
crossref
wiley
SourceType Aggregation Database
Index Database
Enrichment Source
Publisher
StartPage 546
SubjectTerms Aged
Biological activity
Biomarkers
Body mass
Body mass index
Body size
Ceramides - metabolism
Chromatography, Liquid
Cognition
Cognitive ability
Cognitive Dysfunction - metabolism
Cognitive Dysfunction - microbiology
Constipation
Constipation - metabolism
Constipation - microbiology
Environmental changes
Fatty acids
Fatty Acids, Volatile - metabolism
Fecal microflora
Feces
Feces - chemistry
Female
Frailty - metabolism
Frailty - microbiology
Gait
Gastrointestinal Microbiome - genetics
Gene sequencing
Humans
Intestinal microflora
Liquid chromatography
Male
Mass Spectrometry
Mass spectroscopy
Metabolites
Metabolomics
Methylamines - metabolism
Microbial activity
Microbiomes
Microorganisms
Middle Aged
Movement disorders
Neurodegeneration
Neurodegenerative diseases
Neuroprotection
NMR
NMR spectroscopy
Nuclear magnetic resonance
Parkinson Disease - metabolism
Parkinson Disease - microbiology
Parkinson's disease
Phenotyping
Physical activity
Proton Magnetic Resonance Spectroscopy
RNA, Ribosomal, 16S - genetics
rRNA 16S
Salicylates - metabolism
Salicylic acid
Sedentary Behavior
Sphingosine - metabolism
Thinness - metabolism
Thinness - microbiology
Trimethylamine
Ubiquinone - metabolism
Title Gut Microbial Ecosystem in Parkinson Disease: New Clinicobiological Insights from Multi‐Omics
URI https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fana.25982
https://www.ncbi.nlm.nih.gov/pubmed/33274480
https://www.proquest.com/docview/2490442705
https://www.proquest.com/docview/2467615862
Volume 89
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV3NTtwwEB4hDlUv_QW6hVZuxYFLFsex47g9rVoorbQgIZA4IEV27EgrIIvI7oVTH6HP2Cepx06CKK1U9RYpE9nxeP48M58BtoVWUnizm3jbZROeFyJRlVNJpbSUSrKacux3nh7mB6f825k4W4GPfS9MxIcYDtxQMoK-RgHXpt29Aw3VjR4zhJ_z-hdrtdAhOr6DjlJ5QCLANFsi0oz3qEKU7Q5f3rdFDxzM-_5qMDj7T-G8n2qsM7kYLxdmXN3-huL4n__yDJ50jiiZxJ3zHFZc8wIeTbtU-0sovywXZDoLOE2ebq-aR9BnMmsItkqHrjHyOeZ3PhCvLEnEGO1wnZD55GvTYvDfEuxiIaHZ9-f3H0dXs6pdg9P9vZNPB0l3G0NSYaY4SQtZaFE4I63OjfFyT01qVW0Ft7WihmkjlLZa1hJbfwzPZK0szxnPM-MKnq3DajNv3CsgKTM-0rROCp1y4aR3GSyta1fTQnutUI1gp-dLWXVQ5XhjxmUZQZZZ6ResDAs2gvcD6XXE5_gT0VbP3LIT0bb0cSflnEkqRvBueO2FCzMmunHzJdLk0rt8PuobwUbcFMMoWYbgigX1kw2s_fvw5eRwEh5e_zvpJjxmWD0Tqt22YHVxs3RvvPuzMG_DPv8F1eL_dQ
linkProvider Wiley-Blackwell
linkToHtml http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMw1V3NbtQwEB6VIgEX_qFbChgEEpdsHceOYyQOK7Zll3YXCbVSb6mdONKKNluRXVVw4hF4EF6Fl-BJ8Dg_VfmRuPTALVJGsWPPr2fmM8AzoZUUzuwGznblAY8TEajMqiBTWkolWUE59jtPpvFon789EAcr8K3thanxIboDN5QMr69RwPFAevMMNVSXus8Qf64pqdyxn05dwFa9Gg_d7j5nbHtr7_UoaO4UCDLMdwZhIhMtEmtkrmNjHPdSE-aqyAXPC0UN00YonWtZSGxgMTyShcp5zHgcGZvwyH33ElzGG8QRqX_4_gysSsUe-wATe4EII97iGFG22U31vPX7zaU97yF7E7d9A763i1NXtnzoLxemn33-BTfyf1m9m3C98bXJoBaOW7Biy9twZdJUE9yB9M1yQSYzD0Xl6LayeY1rTWYlwW5w3xhHhnUK6yVx9oDUMKoNdBXyNxmXFZ5vVAQbdYjvZ_7x5eu741lW3YX9C_m9e7Bazku7BiRkxgXTuZVCh1xY6byinBaFLWiineLLevCiZYQ0a9DY8VKQo7TGkWap26DUb1APnnakJzUEyZ-INlpuShstVKUutKacM0lFD550r53-wKSQLu18iTSxdF6tC2x7cL_mwm6UKEL8yIS6yXpe-vvw6WA68A_r_076GK6O9ia76e54uvMArjEsFvLFfRuwuvi4tA-dt7cwj7yQETi8aL78Cc2zXX4
linkToPdf http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMw1V3NbtQwEB6VIlVcWv7ZUsAgkLhk6zh2HCNxWHW7dCm7IESl3lI7tqVVIVuRXSE48Qi8B6_CU_AktZ2fqvxIXHrgFimj2LHn1zPzGeAxk4IzZ3YjZ7t0RNOMRaIwIiqE5FxwYjH1_c6Tabp3QF8essMV-N72wtT4EN2Bm5eMoK-9gJ9ou30GGipL2Scefq6pqNw3nz-5eK16Ph66zX1CyGj33c5e1FwpEBU-3RnFGc8ky4ziWqZKOebFKtbCaka1FVgRqZiQWnLLff-Kogm3QtOU0DRRJqOJ--4luExTLPw9EcO3Z1hVIg3QBz6vF7E4oS2MESbb3VTPG7_fPNrzDnKwcKMN-NGuTV3YctxfLlS_-PILbOR_snhXYb3xtNGgFo1rsGLK67A2aWoJbkD-YrlAk1kAonJ0u8W8RrVGsxL5XvDQFoeGdQLrGXLWANUgqg1wleduNC4rf7pRId-mg0I388-v315_mBXVTTi4kN-7BavlvDR3AMVEuVBaG85kTJnhzifS2FpjcSad2it68LTlg7xosNj9lSDv8xpFmuRug_KwQT141JGe1AAkfyLaapkpb3RQlbvAGlNKOGY9eNi9dtrDp4RkaeZLT5Ny59O6sLYHt2sm7EZJEo8emWE32cBKfx8-H0wH4WHz30kfwNqb4Sh_NZ7u34UrxFcKhcq-LVhdfFyae87VW6j7QcQQHF00W54CQAVcLQ
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Gut+Microbial+Ecosystem+in+Parkinson+Disease%3A+New+Clinicobiological+Insights+from+Multi%E2%80%90Omics&rft.jtitle=Annals+of+neurology&rft.au=Ai+Huey+Tan&rft.au=Chun+Wie+Chong&rft.au=Shen%E2%80%90Yang+Lim&rft.au=Ivan+Kok+Seng+Yap&rft.date=2021-03-01&rft.pub=Wiley+Subscription+Services%2C+Inc&rft.issn=0364-5134&rft.eissn=1531-8249&rft.volume=89&rft.issue=3&rft.spage=546&rft.epage=559&rft_id=info:doi/10.1002%2Fana.25982&rft.externalDBID=NO_FULL_TEXT
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=0364-5134&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=0364-5134&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=0364-5134&client=summon