Gut Microbiota Differs Between Parkinson's Disease Patients and Healthy Controls in Northeast China

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Needs review
study design
Citation
PMID PubMed identifier for scientific articles.
DOI Digital object identifier for electronic documents.
URI Uniform resource identifier for web resources.
Authors
Li C, Cui L, Yang Y, Miao J, Zhao X, Zhang J, Cui G, Zhang Y
Journal
Frontiers in molecular neuroscience
Year
2019
Background: There is accumulating evidence suggesting a connection between the gut and Parkinson's disease (PD). Gut microbiota may play an important role in the intestinal lesions in PD patients. Objective: This study aims to determine whether gut microbiota differs between PD patients and healthy controls in Northeast of China, and to identify the factors that influence the changes in the gut microbiota. Methods: We enrolled 51 PD patients and 48 healthy controls in this study. Microbial species in stool samples were determined through 16S-rRNA gene sequencing. Dietary intakes were collected from a subset of 42 patients and 23 controls using a food frequency questionnaire (FFQ). Gut microbiota species richness, diversity, differential abundance of individual taxa between PD patients and controls, and the relationship between the gut microbiota abundance and the dietary and clinical factors were analyzed. Results: PD patients showed decreased species richness, phylogenetic diversity, β- diversity, and altered relative abundance in several taxa compared to the controls. PD- associated clinical scores appeared to be the most influential factors that correlated with the abundance of a variety of taxa. The most consistent findings suggested by multiple analyses used in this study were the increase of Akkermansia and the decrease of Lactobacillus in PD patients in Northeast China. Conclusion: Gut microbiota significantly differed between a group of PD patients and healthy controls in Northeast China, with decreased species richness, phylogenetic diversity, β-diversity, and altered relative abundance in several taxa compared to the controls.

Experiment 1


Needs review

Curated date: 2021/10/18

Curator: Fcuevas3

Revision editor(s): Fcuevas3, Aiyshaaaa, WikiWorks

Subjects

Location of subjects
China
Host species Species from which microbiome was sampled (if applicable)
Homo sapiens
Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology
Feces Cow dung,Cow pat,Droppings,Dung,Excrement,Excreta,Faeces,Fecal material,Fecal matter,Fewmet,Frass,Guano,Matières fécales@fr,Merde@fr,Ordure,Partie de la merde@fr,Piece of shit,Porción de mierda@es,Portion of dung,Portion of excrement,Portion of faeces,Portion of fecal material,Portion of fecal matter,Portion of feces,Portion of guano,Portion of scat,Portionem cacas,Scat,Spoor,Spraint,Stool,Teil der fäkalien@de,Feces
Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
Parkinson's disease IDIOPATHIC PARKINSON DIS,Idiopathic Parkinson Disease,Idiopathic Parkinson's Disease,IDIOPATHIC PARKINSONS DIS,Idiopathic PD,LEWY BODY PARKINSON DIS,Lewy Body Parkinson Disease,Lewy Body Parkinson's Disease,Paralysis agitans,paralysis agitans,PARKINSON DIS,PARKINSON DIS IDIOPATHIC,Parkinson disease,Parkinson Disease, Idiopathic,Parkinson syndrome,Parkinson's,Parkinson's disease,Parkinson's disease (disorder),Parkinson's disease NOS,Parkinson's disease NOS (disorder),Parkinson's Disease, Idiopathic,Parkinson's Disease, Lewy Body,Parkinson's syndrome,Parkinsonian disorder,Parkinsonism, Primary,Parkinsons,PARKINSONS DIS,PARKINSONS DIS IDIOPATHIC,PARKINSONS DIS LEWY BODY,Parkinsons disease,Primary Parkinsonism
Group 0 name Corresponds to the control (unexposed) group for case-control studies
healthy controls without any form of Parkinson's Disease
Group 1 name Corresponds to the case (exposed) group for case-control studies
patients with parkinson's disease
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Diagnosed with PD according to the diagnostic criteria proposed by the International Parkinson Disease and Movement Disorder Society in 2015 (Postuma et al., 2015) in the First Hospital of Jilin University.
Group 0 sample size Number of subjects in the control (unexposed) group
48
Group 1 sample size Number of subjects in the case (exposed) group
51
Antibiotics exclusion Number of days without antibiotics usage (if applicable) and other antibiotics-related criteria used to exclude participants (if any)
No antibiotic use for at least 3 months prior to the study.

Subjects with a history of using medications that have been shown to affect gut microbiota, including COMT inhibitors, anticholinergics, anti-secretory drugs, or cardiological drugs within the 3 months before the start of the study were excluded.

Lab analysis

Sequencing type
16S
16S variable region One or more hypervariable region(s) of the bacterial 16S gene
V4
Sequencing platform Manufacturer and experimental platform used for quantifying microbial abundance
Illumina

Statistical Analysis

Statistical test
T-Test
Significance threshold p-value or FDR threshold used for differential abundance testing (if any)
.05
LDA Score above Threshold for the linear discriminant analysis (LDA) score for studies using the popular LEfSe tool
4
Matched on Factors on which subjects have been matched on in a case-control study
age, body mass index

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
increased
Chao1 Abundance-based estimator of species richness
increased
Simpson Estimator of species richness and species evenness: more weight on species evenness
increased
Richness Number of species
decreased

Signature 1

Needs review

Curated date: 2021/10/18

Curator: Fcuevas3

Revision editor(s): Fcuevas3

Source: Figure 2A: Phylum

Description: Gut microbiota differences between PD patients and controls detected by t-tests. Gut microbiota is compared between PD patients and healthy control subjects at phylum (A), class (B), order (C), family (D), genus (E), and species (F) levels.

Abundance in Group 1: increased abundance in patients with parkinson's disease

NCBI Links
Verrucomicrobiota

Revision editor(s): Fcuevas3

Signature 2

Needs review

Curated date: 2021/10/18

Curator: Fcuevas3

Revision editor(s): Fcuevas3

Source: Figure 2B: Class

Description: Gut microbiota differences between PD patients and controls detected by t-tests. Gut microbiota is compared between PD patients and healthy control subjects at phylum (A), class (B), order (C), family (D), genus (E), and species (F) levels.

Abundance in Group 1: increased abundance in patients with parkinson's disease

NCBI Links
Clostridia
Negativicutes
Verrucomicrobiae

Revision editor(s): Fcuevas3

Signature 3

Needs review

Curated date: 2021/10/18

Curator: Fcuevas3

Revision editor(s): Fcuevas3

Source: Figure 2B: Class

Description: Gut microbiota differences between PD patients and controls detected by t-tests. Gut microbiota is compared between PD patients and healthy control subjects at phylum (A), class (B), order (C), family (D), genus (E), and species (F) levels

Abundance in Group 1: decreased abundance in patients with parkinson's disease

NCBI Links
Bacilli

Revision editor(s): Fcuevas3

Signature 4

Needs review

Curated date: 2021/10/19

Curator: Fcuevas3

Revision editor(s): Fcuevas3

Source: Figure 2C: Order

Description: Gut microbiota differences between PD patients and controls detected by t-tests. Gut microbiota is compared between PD patients and healthy control subjects at phylum (A), class (B), order (C), family (D), genus (E), and species (F) levels.

Abundance in Group 1: increased abundance in patients with parkinson's disease

NCBI Links
Clostridiales Family XIII bacterium
Selenomonadales
Verrucomicrobiales

Revision editor(s): Fcuevas3

Signature 5

Needs review

Curated date: 2021/10/19

Curator: Fcuevas3

Revision editor(s): Fcuevas3

Source: Figure 2C: Order

Description: Gut microbiota differences between PD patients and controls detected by t-tests. Gut microbiota is compared between PD patients and healthy control subjects at phylum (A), class (B), order (C), family (D), genus (E), and species (F) levels.

Abundance in Group 1: decreased abundance in patients with parkinson's disease

NCBI Links
Lactobacillales

Revision editor(s): Fcuevas3

Signature 6

Needs review

Curated date: 2021/10/19

Curator: Fcuevas3

Revision editor(s): Fcuevas3

Source: Figure 2D: Family

Description: Gut microbiota differences between PD patients and controls detected by t-tests. Gut microbiota is compared between PD patients and healthy control subjects at phylum (A), class (B), order (C), family (D), genus (E), and species (F) levels.

Abundance in Group 1: increased abundance in patients with parkinson's disease

NCBI Links
Oscillospiraceae
Veillonellaceae
Verrucomicrobiaceae
Porphyromonadaceae
Rikenellaceae
Acidaminococcaceae

Revision editor(s): Fcuevas3

Signature 7

Needs review

Curated date: 2021/10/19

Curator: Fcuevas3

Revision editor(s): Fcuevas3

Source: Figure 2D: Family

Description: Gut microbiota differences between PD patients and controls detected by t-tests. Gut microbiota is compared between PD patients and healthy control subjects at phylum (A), class (B), order (C), family (D), genus (E), and species (F) levels.

Abundance in Group 1: decreased abundance in patients with parkinson's disease

NCBI Links
Lactobacillaceae
Bacteroidales

Revision editor(s): Fcuevas3

Signature 8

Needs review

Curated date: 2021/10/19

Curator: Fcuevas3

Revision editor(s): Fcuevas3

Source: Figure 2E: Genus

Description: Gut microbiota differences between PD patients and controls detected by t-tests. Gut microbiota is compared between PD patients and healthy control subjects at phylum (A), class (B), order (C), family (D), genus (E), and species (F) levels.

Abundance in Group 1: increased abundance in patients with parkinson's disease

NCBI Links
Ruminococcus
Akkermansia
Eubacterium
Parabacteroides
Coprococcus
Phascolarctobacterium
Methanobrevibacter
Alistipes
Roseburia
Lachnospiraceae
Eubacterium ventriosum
Lachnospira

Revision editor(s): Fcuevas3

Signature 9

incomplete

Curated date: 2021/10/20

Curator: Fcuevas3

Revision editor(s): Fcuevas3

Source: Figure 2E: Genus

Description: Gut microbiota differences between PD patients and controls detected by t-tests. Gut microbiota is compared between PD patients and healthy control subjects at phylum (A), class (B), order (C), family (D), genus (E), and species (F) levels.

Abundance in Group 1: decreased abundance in patients with parkinson's disease

NCBI Links
Lactobacillus
Streptococcus
Anaerobutyricum hallii

Revision editor(s): Fcuevas3

Experiment 2


Needs review

Curated date: 2021/10/18

Curator: Fcuevas3

Revision editor(s): Fcuevas3, WikiWorks

Subjects

Location of subjects
China
Host species Species from which microbiome was sampled (if applicable)
Homo sapiens
Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology
Feces Cow dung,Cow pat,Droppings,Dung,Excrement,Excreta,Faeces,Fecal material,Fecal matter,Fewmet,Frass,Guano,Matières fécales@fr,Merde@fr,Ordure,Partie de la merde@fr,Piece of shit,Porción de mierda@es,Portion of dung,Portion of excrement,Portion of faeces,Portion of fecal material,Portion of fecal matter,Portion of feces,Portion of guano,Portion of scat,Portionem cacas,Scat,Spoor,Spraint,Stool,Teil der fäkalien@de,Feces
Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
Parkinson's disease IDIOPATHIC PARKINSON DIS,Idiopathic Parkinson Disease,Idiopathic Parkinson's Disease,IDIOPATHIC PARKINSONS DIS,Idiopathic PD,LEWY BODY PARKINSON DIS,Lewy Body Parkinson Disease,Lewy Body Parkinson's Disease,Paralysis agitans,paralysis agitans,PARKINSON DIS,PARKINSON DIS IDIOPATHIC,Parkinson disease,Parkinson Disease, Idiopathic,Parkinson syndrome,Parkinson's,Parkinson's disease,Parkinson's disease (disorder),Parkinson's disease NOS,Parkinson's disease NOS (disorder),Parkinson's Disease, Idiopathic,Parkinson's Disease, Lewy Body,Parkinson's syndrome,Parkinsonian disorder,Parkinsonism, Primary,Parkinsons,PARKINSONS DIS,PARKINSONS DIS IDIOPATHIC,PARKINSONS DIS LEWY BODY,Parkinsons disease,Primary Parkinsonism
Group 0 name Corresponds to the control (unexposed) group for case-control studies
healthy controls without any form of Parkinson's Disease, with Wexner scores < 3 using Wilcoxon rank sum test.
Group 1 name Corresponds to the case (exposed) group for case-control studies
patients with Parkinson's disease with Wexner scores < 3
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Patients with Parkinson's disease with Wexner scores < 3.
Group 0 sample size Number of subjects in the control (unexposed) group
25
Group 1 sample size Number of subjects in the case (exposed) group
13
Antibiotics exclusion Number of days without antibiotics usage (if applicable) and other antibiotics-related criteria used to exclude participants (if any)
No antibiotic use for at least 3 months prior to the study.

Subjects with a history of using medications that have been shown to affect gut microbiota, including COMT inhibitors, anticholinergics, anti-secretory drugs, or cardiological drugs within the 3 months before the start of the study were excluded.

Lab analysis

Sequencing type
16S
Sequencing platform Manufacturer and experimental platform used for quantifying microbial abundance
Illumina

Statistical Analysis

Statistical test
Mann-Whitney (Wilcoxon)
Significance threshold p-value or FDR threshold used for differential abundance testing (if any)
.01
LDA Score above Threshold for the linear discriminant analysis (LDA) score for studies using the popular LEfSe tool
4
Matched on Factors on which subjects have been matched on in a case-control study
age, Matched on: "bmi" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.bmi

Alpha Diversity

Chao1 Abundance-based estimator of species richness
decreased

Signature 1

incomplete

Curated date: 2021/10/18

Curator: Fcuevas3

Revision editor(s): Fcuevas3

Source: Supplemental Figure 5

Description: Comparison of microbiota abundances between PD and controls with constipation Wexner score less than or equal to 3.

Abundance in Group 1: decreased abundance in patients with Parkinson's disease with Wexner scores < 3

NCBI Links
Bacilli
Lactobacillales
Bacteroidales
Lactobacillaceae
Lactobacillus

Revision editor(s): Fcuevas3

Experiment 3


Needs review

Curated date: 2021/10/18

Curator: Fcuevas3

Revision editor(s): Fcuevas3, WikiWorks

Subjects

Location of subjects
China
Host species Species from which microbiome was sampled (if applicable)
Homo sapiens
Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology
Feces Cow dung,Cow pat,Droppings,Dung,Excrement,Excreta,Faeces,Fecal material,Fecal matter,Fewmet,Frass,Guano,Matières fécales@fr,Merde@fr,Ordure,Partie de la merde@fr,Piece of shit,Porción de mierda@es,Portion of dung,Portion of excrement,Portion of faeces,Portion of fecal material,Portion of fecal matter,Portion of feces,Portion of guano,Portion of scat,Portionem cacas,Scat,Spoor,Spraint,Stool,Teil der fäkalien@de,Feces
Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
Parkinson's disease IDIOPATHIC PARKINSON DIS,Idiopathic Parkinson Disease,Idiopathic Parkinson's Disease,IDIOPATHIC PARKINSONS DIS,Idiopathic PD,LEWY BODY PARKINSON DIS,Lewy Body Parkinson Disease,Lewy Body Parkinson's Disease,Paralysis agitans,paralysis agitans,PARKINSON DIS,PARKINSON DIS IDIOPATHIC,Parkinson disease,Parkinson Disease, Idiopathic,Parkinson syndrome,Parkinson's,Parkinson's disease,Parkinson's disease (disorder),Parkinson's disease NOS,Parkinson's disease NOS (disorder),Parkinson's Disease, Idiopathic,Parkinson's Disease, Lewy Body,Parkinson's syndrome,Parkinsonian disorder,Parkinsonism, Primary,Parkinsons,PARKINSONS DIS,PARKINSONS DIS IDIOPATHIC,PARKINSONS DIS LEWY BODY,Parkinsons disease,Primary Parkinsonism
Group 0 name Corresponds to the control (unexposed) group for case-control studies
controls without any form of Parkinson's
Group 1 name Corresponds to the case (exposed) group for case-control studies
patients with Parkinson's disease
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Patients who had been diagnosed with PD according to the diagnostic criteria proposed by the International Parkinson Disease and Movement Disorder Society in 2015 (Postuma et al., 2015) in the First Hospital of Jilin University.
Group 0 sample size Number of subjects in the control (unexposed) group
48
Group 1 sample size Number of subjects in the case (exposed) group
51
Antibiotics exclusion Number of days without antibiotics usage (if applicable) and other antibiotics-related criteria used to exclude participants (if any)
No antibiotic use for at least 3 months prior to the study.

Subjects with a history of using medications that have been shown to affect gut microbiota, including COMT inhibitors, anticholinergics, anti-secretory drugs, or cardiological drugs within the 3 months before the start of the study were excluded.

Lab analysis

Sequencing type
16S
Sequencing platform Manufacturer and experimental platform used for quantifying microbial abundance
Illumina

Statistical Analysis

Statistical test
ANOVA
Significance threshold p-value or FDR threshold used for differential abundance testing (if any)
.05
LDA Score above Threshold for the linear discriminant analysis (LDA) score for studies using the popular LEfSe tool
4
Matched on Factors on which subjects have been matched on in a case-control study
age, Matched on: "bmi" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.bmi


Signature 1

incomplete

Curated date: 2021/10/18

Curator: Fcuevas3

Revision editor(s): Fcuevas3

Source: Supplemental Figure 7

Description: Two-way ANOVA analysis to assess the impact of gender and PD on gut microbiota taxa identified by LDA scores>4 in LEfSe analysis.

Abundance in Group 1: increased abundance in patients with Parkinson's disease

NCBI Links

Revision editor(s): Fcuevas3

Signature 2

Needs review

Curated date: 2021/10/18

Curator: Fcuevas3

Revision editor(s): Fcuevas3

Source: Supplemental Figure 7

Description: Two-way ANOVA analysis to assess the impact of gender and PD on gut microbiota taxa identified by LDA scores>4 in LEfSe analysis.

Abundance in Group 1: decreased abundance in patients with Parkinson's disease

NCBI Links
Bacteroidales
Lactobacillaceae
Lactobacillales
Lactobacillus
Bacilli

Revision editor(s): Fcuevas3

Experiment 4


incomplete

Curated date: 2021/10/20

Curator: Fcuevas3

Revision editor(s): Fcuevas3, WikiWorks

Subjects

Location of subjects
China
Host species Species from which microbiome was sampled (if applicable)
Homo sapiens
Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology
Feces Cow dung,Cow pat,Droppings,Dung,Excrement,Excreta,Faeces,Fecal material,Fecal matter,Fewmet,Frass,Guano,Matières fécales@fr,Merde@fr,Ordure,Partie de la merde@fr,Piece of shit,Porción de mierda@es,Portion of dung,Portion of excrement,Portion of faeces,Portion of fecal material,Portion of fecal matter,Portion of feces,Portion of guano,Portion of scat,Portionem cacas,Scat,Spoor,Spraint,Stool,Teil der fäkalien@de,Feces
Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
Parkinson's disease IDIOPATHIC PARKINSON DIS,Idiopathic Parkinson Disease,Idiopathic Parkinson's Disease,IDIOPATHIC PARKINSONS DIS,Idiopathic PD,LEWY BODY PARKINSON DIS,Lewy Body Parkinson Disease,Lewy Body Parkinson's Disease,Paralysis agitans,paralysis agitans,PARKINSON DIS,PARKINSON DIS IDIOPATHIC,Parkinson disease,Parkinson Disease, Idiopathic,Parkinson syndrome,Parkinson's,Parkinson's disease,Parkinson's disease (disorder),Parkinson's disease NOS,Parkinson's disease NOS (disorder),Parkinson's Disease, Idiopathic,Parkinson's Disease, Lewy Body,Parkinson's syndrome,Parkinsonian disorder,Parkinsonism, Primary,Parkinsons,PARKINSONS DIS,PARKINSONS DIS IDIOPATHIC,PARKINSONS DIS LEWY BODY,Parkinsons disease,Primary Parkinsonism
Group 0 name Corresponds to the control (unexposed) group for case-control studies
controls without any form of Parkinson's disease
Group 1 name Corresponds to the case (exposed) group for case-control studies
patients with Parkinson's disease
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Patients who had been diagnosed with PD according to the diagnostic criteria proposed by the International Parkinson Disease and Movement Disorder Society in 2015 (Postuma et al., 2015) in the First Hospital of Jilin University.
Group 0 sample size Number of subjects in the control (unexposed) group
48
Group 1 sample size Number of subjects in the case (exposed) group
51
Antibiotics exclusion Number of days without antibiotics usage (if applicable) and other antibiotics-related criteria used to exclude participants (if any)
No antibiotic use for at least 3 months prior to the study.

Subjects with a history of using medications that have been shown to affect gut microbiota, including COMT inhibitors, anticholinergics, anti-secretory drugs, or cardiological drugs within the 3 months before the start of the study were excluded.

Lab analysis

Sequencing type
16S
Sequencing platform Manufacturer and experimental platform used for quantifying microbial abundance
Illumina

Statistical Analysis

Statistical test
LEfSe
LDA Score above Threshold for the linear discriminant analysis (LDA) score for studies using the popular LEfSe tool
4
Matched on Factors on which subjects have been matched on in a case-control study
age, Matched on: "bmi" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.bmi


Signature 1

incomplete

Curated date: 2021/10/20

Curator: Fcuevas3

Revision editor(s): Fcuevas3

Source: Figure 3

Description: Gut microbiota differences between PD patients and controls detected by LEfSe analysis.

Abundance in Group 1: increased abundance in patients with Parkinson's disease

NCBI Links

Revision editor(s): Fcuevas3