Profiling the oral microbiomes in patients with Alzheimer's disease

Study information

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study design

case-control

Citation

PMID PubMed identifier for scientific articles.

34931394

DOI Digital object identifier for electronic documents.

10.1111/odi.14110

URI

Authors

Guo H, Li B, Yao H, Liu D, Chen R, Zhou S, Ji Y, Zeng L, Du M

Journal

Oral diseases

Year

2023

Keywords:

Alzheimer's disease, oral microbiomes, periodontal bacteria, periodontal disease

OBJECTIVES: To analyse the characteristics of the oral microbiomes and expected to find biomarkers about Alzheimer's disease (AD). SUBJECTS AND METHODS: AD patients (n = 26) and cognitive intact people (n = 26) were examined for cognition, depression, oral health and collected saliva and gingival crevicular fluid (GCF) in the morning. Full-length 16S rRNA gene was amplified and sequencing was performed using the PacBio platform. RESULTS: The predominant bacterium of salivary microbiome and periodontal microbiome from AD patients was Streptococcus oralis and Porphyromonas gingivalis, respectively. With respect to β diversity analysis, there was a significance difference in periodontal microbiome between AD patients and cognitively intact subjects. The relative abundance of Veillonella parvula significantly increased in oral microbiomes from AD patients. Interestingly, the dominant species were different between early-onset AD and late-onset AD patients. Moreover, the predominant species were changed as the clinical severity of AD. Furthermore, the correlation analysis revealed that V. parvula was associated with AD in both saliva and GCF and that P. gingivalis was associated with AD only in GCF. CONCLUSIONS: In this study, the microbiome community of oral microbes was altered in AD patients and periodontal microbiome was sensitive to cognition changes. Moreover, V. parvula and P. gingivalis were associated with AD.

Experiment 1

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Subjects

Location of subjects

China

Host species Species from which microbiome was sampled. Contact us to have more species added.

Homo sapiens

Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology

Saliva Sailva normalis,Saliva atomaris,Saliva molecularis,Salivary gland secretion,Saliva,saliva

Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology

Alzheimer's disease [X]Dementia in Alzheimer's disease,[X]Dementia in Alzheimer's disease (disorder),AD,AD - Alzheimer's disease,Alzheimer Dementia,Alzheimer dementia,Alzheimer Dementia, Presenile,ALZHEIMER DIS,Alzheimer Disease,Alzheimer disease,Alzheimer disease, familial,Alzheimer Type Dementia,Alzheimer's,Alzheimer's Dementia,Alzheimer's dementia,Alzheimer's disease,Alzheimer's disease (disorder),Alzheimer's disease, NOS,Alzheimers,Alzheimers Dementia,Alzheimers dementia,ALZHEIMERS DIS,Alzheimers disease,DAT - Dementia Alzheimer's type,Dementia in Alzheimer's disease,Dementia in Alzheimer's disease (disorder),Dementia in Alzheimer's disease, unspecified (disorder),Dementia of the Alzheimer's type,Dementia, Alzheimer Type,Dementia, Presenile,Dementia, Presenile Alzheimer,Disease, Alzheimer,Disease, Alzheimer's,Presenile Alzheimer Dementia,sporadic Alzheimer's disease,alzheimer's disease

Group 0 name Corresponds to the control (unexposed) group for case-control studies

Cognitive intact subjects

Group 1 name Corresponds to the case (exposed) group for case-control studies

Alzheimer's Disease (AD) patients

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

Patients with Alzheimer's Disease

Group 0 sample size Number of subjects in the control (unexposed) group

26

Group 1 sample size Number of subjects in the case (exposed) group

26

Antibiotics exclusion Number of days without antibiotics usage (if applicable) and other antibiotics-related criteria used to exclude participants (if any)

3 months

Lab analysis

Sequencing type

16S

16S variable region One or more hypervariable region(s) of the bacterial 16S gene

Not specified

Sequencing platform Manufacturer and experimental platform used for quantifying microbial abundance

PacBio RS

Statistical Analysis

Data transformation Data transformation applied to microbial abundance measurements prior to differential abundance testing (if any).

relative abundances

Statistical test

Metastats

Significance threshold p-value or FDR threshold used for differential abundance testing (if any)

0.05

MHT correction Have statistical tests be corrected for multiple hypothesis testing (MHT)?

No

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Source: Figure 3a

Description: Differential salivary microbes in AD patients and cognitive-intact subjects

Abundance in Group 1: increased abundance in Alzheimer's Disease (AD) patients

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Deinococcota

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Source: Figure 3a

Description: Differential salivary microbes in AD patients and cognitive-intact subjects

Abundance in Group 1: decreased abundance in Alzheimer's Disease (AD) patients

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Fusobacteriia
Pseudomonadota

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Experiment 2

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Subjects

Lab analysis

Statistical Analysis

Statistical test

LEfSe

LDA Score above Threshold for the linear discriminant analysis (LDA) score for studies using the popular LEfSe tool

2.0

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Source: Figure 3b

Description: Differential salivary microbes in AD patients and cognitive-intact subjects

Abundance in Group 1: increased abundance in Alzheimer's Disease (AD) patients

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Prevotella denticola
Lactobacillus gasseri
Ligilactobacillus salivarius
Streptococcus gordonii
Lactobacillales
Bacilli
Stomatobaculum longum
Stomatobaculum
Lachnospiraceae
Eubacteriales
Clostridia
Megasphaera micronuciformis
Megasphaera
Veillonella dispar
Veillonella parvula
Veillonella
Veillonellaceae
Veillonellales
Negativicutes

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Source: Figure 3b

Description: Differential salivary microbes in AD patients and cognitive-intact subjects

Abundance in Group 1: decreased abundance in Alzheimer's Disease (AD) patients

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Arachnia
Propionibacteriaceae
Propionibacteriales
Metaprevotella massiliensis
Metaprevotella
Tannerella forsythia
Tannerella
Lactobacillus helveticus
Weissella
Lactobacillaceae
Fusobacterium periodonticum
Fusobacterium
Fusobacteriaceae
Leptotrichia buccalis
Pseudoleptotrichia goodfellowii
Leptotrichia wadei
Leptotrichia
Leptotrichiaceae
Fusobacteriales
Fusobacteriia
Lautropia mirabilis
Lautropia
Burkholderiaceae
Neisseria oralis
Cardiobacterium hominis
Cardiobacterium valvarum
Cardiobacterium
Cardiobacteriaceae
Cardiobacteriales
Aggregatibacter aphrophilus
Aggregatibacter
Haemophilus haemolyticus
Haemophilus parahaemolyticus
Haemophilus parainfluenzae
Haemophilus
Pasteurellaceae
Pasteurellales
Gammaproteobacteria
Acholeplasma
Acholeplasmataceae

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Experiment 3

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Subjects

Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology

Gingival groove Gingival sulcus,Sulcus gingivalis,Tooth-gingiva interface,Gingival groove,gingival groove

Lab analysis

Statistical Analysis

Statistical test

Metastats

LDA Score above Threshold for the linear discriminant analysis (LDA) score for studies using the popular LEfSe tool

Not specified

Signature 1

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Source: Figure 4a

Description: Differential gingival crevicular fluid (GCF) microbes in AD patients and cognitive-intact subjects

Abundance in Group 1: increased abundance in Alzheimer's Disease (AD) patients

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Actinomycetota

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Source: Figure 4a

Description: Differential gingival crevicular fluid (GCF) microbes in AD patients and cognitive-intact subjects

Abundance in Group 1: decreased abundance in Alzheimer's Disease (AD) patients

NCBI	Quality Control	Links
Pseudomonadota
Fusobacteriia
Mycoplasmatota
Chloroflexia

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Experiment 4

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Subjects

Lab analysis

Statistical Analysis

Statistical test

LEfSe

LDA Score above Threshold for the linear discriminant analysis (LDA) score for studies using the popular LEfSe tool

2.0

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Source: Figure 4b

Description: Differential gingival crevicular fluid (GCF) microbes in AD patients and cognitive-intact subjects

Abundance in Group 1: increased abundance in Alzheimer's Disease (AD) patients

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Bifidobacterium dentium
Bifidobacterium
Bifidobacteriaceae
Bifidobacteriales
Lancefieldella parvula
Lancefieldella rimae
Atopobium
Olsenella uli
Olsenella
Atopobiaceae
Coriobacteriales
Coriobacteriia
Lactobacillus gasseri
Streptococcus anginosus
Streptococcus sanguinis
Lactobacillales
Bacilli
Oribacterium parvum
Oribacterium
Stomatobaculum longum
Stomatobaculum
Lachnospiraceae
Selenomonas flueggei
Veillonella parvula
Veillonella
Veillonellaceae
Veillonellales
Negativicutes

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Source: Figure 4b

Description: Differential gingival crevicular fluid (GCF) microbes in AD patients and cognitive-intact subjects

Abundance in Group 1: decreased abundance in Alzheimer's Disease (AD) patients

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Paludibacter propionicigenes
Paludibacter
Paludibacteraceae
Porphyromonas endodontalis
Marinilabiliales
Lactobacillus helveticus
Syntrophomonas
Syntrophomonadaceae
Centipeda periodontii
Centipeda
Fusobacterium nucleatum
Fusobacterium
Fusobacteriaceae
Leptotrichia buccalis
Leptotrichia hofstadii
Leptotrichia
Leptotrichiaceae
Fusobacteriales
Fusobacteriia
Lautropia mirabilis
Lautropia
Burkholderiaceae
Burkholderiales
Polyangiaceae
Myxococcales
Campylobacter rectus
Campylobacter showae
Campylobacter
Campylobacteraceae
Campylobacterales
Epsilonproteobacteria
Cardiobacterium hominis
Cardiobacterium valvarum
Cardiobacterium
Cardiobacteriaceae
Cardiobacteriales
Aggregatibacter aphrophilus
Aggregatibacter segnis
Aggregatibacter
Haemophilus haemolyticus
Haemophilus parainfluenzae
Haemophilus
Pasteurellaceae
Pasteurellales
Gammaproteobacteria

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Experiment 5

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Subjects

Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology

Saliva Sailva normalis,Saliva atomaris,Saliva molecularis,Salivary gland secretion,Saliva,saliva

Group 0 name Corresponds to the control (unexposed) group for case-control studies

Early-onset Alzheimer's Disease patients (EAS)

Group 1 name Corresponds to the case (exposed) group for case-control studies

Late-onset Alzheimer's Disease patients (NAS)

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

Patients with late-onset Alzheimer's Disease

Group 0 sample size Number of subjects in the control (unexposed) group

10

Group 1 sample size Number of subjects in the case (exposed) group

16

Lab analysis

Statistical Analysis

Statistical test

Welch's T-Test

LDA Score above Threshold for the linear discriminant analysis (LDA) score for studies using the popular LEfSe tool

Not specified

Signature 1

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Source: Figure 5a

Description: Differential bacteria in AD patients with different clinical types

Abundance in Group 1: increased abundance in Late-onset Alzheimer's Disease patients (NAS)

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Parvimonas micra
Prevotella veroralis
Segatella oris
Streptococcus anginosus
Veillonella parvula
Ligilactobacillus salivarius

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Source: Figure 5a

Description: Differential bacteria in AD patients with different clinical types

Abundance in Group 1: decreased abundance in Late-onset Alzheimer's Disease patients (NAS)

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Capnocytophaga leadbetteri
Streptococcus cristatus
Capnocytophaga granulosa
Neisseria elongata
Stomatobaculum longum

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Experiment 6

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Subjects

Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology

Gingival groove Gingival sulcus,Sulcus gingivalis,Tooth-gingiva interface,Gingival groove,gingival groove

Group 0 name Corresponds to the control (unexposed) group for case-control studies

Early-onset Alzheimer's Disease patients (EAG)

Group 1 name Corresponds to the case (exposed) group for case-control studies

Late-onset Alzheimer's Disease patients (NAG)

Lab analysis

Statistical Analysis

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Source: Figure 5b

Description: Differential bacteria in AD patients with different clinical types

Abundance in Group 1: increased abundance in Late-onset Alzheimer's Disease patients (NAG)

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Streptococcus constellatus
Porphyromonas gingivalis
Mogibacterium timidum

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Experiment 7

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Subjects

Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology

Saliva Sailva normalis,Saliva atomaris,Saliva molecularis,Salivary gland secretion,Saliva,saliva

Group 0 name Corresponds to the control (unexposed) group for case-control studies

Cognitive intact subjects

Group 1 name Corresponds to the case (exposed) group for case-control studies

Alzheimer's Disease (AD) patients

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

Patients with Alzheimer's Disease

Group 0 sample size Number of subjects in the control (unexposed) group

26

Group 1 sample size Number of subjects in the case (exposed) group

26

Lab analysis

Statistical Analysis

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Source: Figure S2a

Description: Differential microbes in the saliva from AD patients and cognitive intact subjects

Abundance in Group 1: increased abundance in Alzheimer's Disease (AD) patients

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Veillonella parvula
Stomatobaculum longum
Veillonella dispar
Prevotella denticola
Ligilactobacillus salivarius
Granulicatella adiacens
Dialister invisus
Gemella sanguinis

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Source: Figure S2a

Description: Differential microbes in the saliva from AD patients and cognitive intact subjects

Abundance in Group 1: decreased abundance in Alzheimer's Disease (AD) patients

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Haemophilus parainfluenzae
Haemophilus haemolyticus
Lautropia mirabilis
Lactobacillus helveticus
Aggregatibacter aphrophilus
Cardiobacterium valvarum
Fusobacterium periodonticum
Campylobacter gracilis
Fusobacterium nucleatum

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Experiment 8

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Subjects

Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology

Gingival groove Gingival sulcus,Sulcus gingivalis,Tooth-gingiva interface,Gingival groove,gingival groove

Lab analysis

Statistical Analysis

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Source: Figure S2b

Description: Differential microbes in the gingival crevicular fluid (GCF) from AD patients and cognitive intact subjects

Abundance in Group 1: increased abundance in Alzheimer's Disease (AD) patients

NCBI	Quality Control	Links
Olsenella uli
Veillonella parvula
Oribacterium parvum
Lancefieldella rimae
Streptococcus anginosus
Stomatobaculum longum
Selenomonas artemidis
Selenomonas sputigena
Streptococcus gordonii

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Source: Figure S2b

Description: Differential microbes in the gingival crevicular fluid (GCF) from AD patients and cognitive intact subjects

Abundance in Group 1: decreased abundance in Alzheimer's Disease (AD) patients

NCBI	Quality Control	Links
Fusobacterium nucleatum
Campylobacter showae
Haemophilus parainfluenzae
Cardiobacterium valvarum
Campylobacter rectus
Prevotellamassilia timonensis
Aggregatibacter aphrophilus
Leptotrichia buccalis
Porphyromonas endodontalis
Paludibacter propionicigenes
Desulfomicrobium orale
Haemophilus haemolyticus

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Experiment 9

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Subjects

Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology

Saliva Sailva normalis,Saliva atomaris,Saliva molecularis,Salivary gland secretion,Saliva,saliva

Group 0 name Corresponds to the control (unexposed) group for case-control studies

Early-onset Alzheimer's Disease patients (EAS)

Group 1 name Corresponds to the case (exposed) group for case-control studies

Late-onset Alzheimer's Disease patients (NAS)

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

Patients with late-onset Alzheimer's Disease

Group 0 sample size Number of subjects in the control (unexposed) group

10

Group 1 sample size Number of subjects in the case (exposed) group

16

Lab analysis

Statistical Analysis

Statistical test

Metastats

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Source: Figure S3d

Description: Differential abundance of bacteria in AD patients with different clinical types

Abundance in Group 1: increased abundance in Late-onset Alzheimer's Disease patients (NAS)

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Veillonella parvula
Segatella oris

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Source: Figure S3d

Description: Differential abundance of bacteria in AD patients with different clinical types

Abundance in Group 1: decreased abundance in Late-onset Alzheimer's Disease patients (NAS)

NCBI	Quality Control	Links
Capnocytophaga granulosa
Capnocytophaga leadbetteri
Neisseria elongata
Streptococcus cristatus
Porphyromonas catoniae
Aggregatibacter segnis
Stomatobaculum longum
Aggregatibacter aphrophilus
Corynebacterium matruchotii
Corynebacterium durum
Leptotrichia hofstadii
Cardiobacterium hominis
Capnocytophaga ochracea

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Experiment 10

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Subjects

Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology

Gingival groove Gingival sulcus,Sulcus gingivalis,Tooth-gingiva interface,Gingival groove,gingival groove

Group 0 name Corresponds to the control (unexposed) group for case-control studies

Early-onset Alzheimer's Disease patients (EAG)

Group 1 name Corresponds to the case (exposed) group for case-control studies

Late-onset Alzheimer's Disease patients (NAG)

Lab analysis

Statistical Analysis

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Source: Figure S3e

Description: Differential abundance of bacteria in AD patients with different clinical types

Abundance in Group 1: increased abundance in Late-onset Alzheimer's Disease patients (NAG)

NCBI	Quality Control	Links
Porphyromonas gingivalis
Streptococcus constellatus

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Source: Figure S3e

Description: Differential abundance of bacteria in AD patients with different clinical types

Abundance in Group 1: decreased abundance in Late-onset Alzheimer's Disease patients (NAG)

NCBI	Quality Control	Links
Rothia dentocariosa

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