Metagenomic gut microbiome analysis of Japanese patients with multiple chemical sensitivity/idiopathic environmental intolerance

Study information

Needs review

study design

case-control

Citation

PMID PubMed identifier for scientific articles.

38468206

DOI Digital object identifier for electronic documents.

10.1186/s12866-024-03239-y

URI

Authors

Watai K, Suda W, Kurokawa R, Sekiya K, Hayashi H, Iwata M, Nagayama K, Nakamura Y, Hamada Y, Kamide Y, Fukutomi Y, Nakabayashi T, Tanaka K, Kamita M, Taniguchi M, Hattori M

Journal

BMC microbiology

Year

2024

Keywords:

Central nervous system, Gut microbiome, Multiple chemical sensitivity, Shotgun metagenomic sequencing

BACKGROUND: Although the pathology of multiple chemical sensitivity (MCS) is unknown, the central nervous system is reportedly involved. The gut microbiota is important in modifying central nervous system diseases. However, the relationship　between the gut microbiota and MCS remains unclear. This study aimed to identify gut microbiota variations associated with MCS using shotgun metagenomic sequencing of fecal samples. METHODS: We prospectively recruited 30 consecutive Japanese female patients with MCS and analyzed their gut microbiomes using shotgun metagenomic sequencing. The data were compared with metagenomic data obtained from 24 age- and sex-matched Japanese healthy controls (HC). RESULTS: We observed no significant difference in alpha and beta diversity of the gut microbiota between the MCS patients and HC. Focusing on the important changes in the literatures, at the genus level, Streptococcus, Veillonella, and Akkermansia were significantly more abundant in MCS patients than in HC (p < 0.01, p < 0.01, p = 0.01, respectively, fold change = 4.03, 1.53, 2.86, respectively). At the species level, Akkermansia muciniphila was significantly more abundant (p = 0.02, fold change = 3.3) and Faecalibacterium prausnitzii significantly less abundant in MCS patients than in HC (p = 0.03, fold change = 0.53). Functional analysis revealed that xylene and dioxin degradation pathways were significantly enriched (p < 0.01, p = 0.01, respectively, fold change = 1.54, 1.46, respectively), whereas pathways involved in amino acid metabolism and synthesis were significantly depleted in MCS (p < 0.01, fold change = 0.96). Pathways related to antimicrobial resistance, including the two-component system and cationic antimicrobial peptide resistance, were also significantly enriched in MCS (p < 0.01, p < 0.01, respectively, fold change = 1.1, 1.2, respectively). CONCLUSIONS: The gut microbiota of patients with MCS shows dysbiosis and alterations in bacterial functions related to exogenous chemicals and amino acid metabolism and synthesis. These findings may contribute to the further development of treatment for MCS. TRIAL REGISTRATION: This study was registered with the University Hospital Medical Information Clinical Trials Registry as UMIN000031031. The date of first trial registration: 28/01/2018.

Experiment 1

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Subjects

Location of subjects: Japan

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: 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,feces

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

Group 0 name Corresponds to the control (unexposed) group for case-control studies: Healthy Control (HC)

Group 1 name Corresponds to the case (exposed) group for case-control studies: Multiple Chemical Sensitivity (MCS)

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group: Japanese female patients with Multiple Chemical Sensitivity (MCS)

Group 0 sample size Number of subjects in the control (unexposed) group: 24

Group 1 sample size Number of subjects in the case (exposed) group: 30

Antibiotics exclusion Number of days without antibiotics usage (if applicable) and other antibiotics-related criteria used to exclude participants (if any): 6 months

Lab analysis

Sequencing type: WMS

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: Illumina

Statistical Analysis

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

Statistical test: Mann-Whitney (Wilcoxon); T-Test

Significance threshold p-value or FDR threshold used for differential abundance testing (if any): 0.05

Matched on Factors on which subjects have been matched on in a case-control study: age, sex

Confounders controlled for Confounding factors that have been accounted for by stratification or model adjustment: age, sex, health

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness: unchanged

Signature 1

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Source: Fig. 2b, Fig. 3a, Fig. 4a, Additional File Fig. S1a

Description: Relative abundances of species that differed significantly between multiple chemical sensitivity (MCS, n = 30) patients and healthy controls (HC, n = 24).

Abundance in Group 1: increased abundance in

NCBI	Quality Control	Links
Actinomyces
Akkermansia
Akkermansia muciniphila
Akkermansia sp. CAG:344
Bacteroides fragilis str. 3976T8
Bifidobacterium animalis subsp. animalis
Blautia obeum A2-162
Clostridium sp. CAG:217
Clostridium sp. CAG:264
Clostridium sp. CAG:273
Clostridium sp. CAG:352
Dialister
Dialister invisus DSM 15470
Dialister sp. CAG:357
Enterococcus durans ATCC 6056
Eubacterium sp. CAG:192
Eubacterium sp. CAG:202
Eubacterium sp. CAG:251
Lactobacillus
Lactobacillus delbrueckii subsp. jakobsenii ZN7a-9 = DSM 26046
Phocaeicola dorei CL02T12C06
Roseburia intestinalis M50/1
Ruminococcus bromii L2-63
Ruminococcus sp. CAG:177
Ruminococcus sp. CAG:254
Ruminococcus sp. CAG:57
Ruminococcus sp. JC304
Streptococcus
Streptococcus lutetiensis 033
Streptococcus parasanguinis
Streptococcus salivarius
Streptococcus sp. C150
Streptococcus sp. HSISS1
Streptococcus thermophilus TH985
Streptococcus vestibularis ATCC 49124
Thomasclavelia
Thomasclavelia ramosa DSM 1402
Veillonella
Veillonella sp. CAG:933
Verrucomicrobiia

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Signature 2

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Source: Fig. 2a, Fig. 3b, Fig. 4b, Additional File Fig. S1b

Description: Relative abundances of species that differed significantly between multiple chemical sensitivity (MCS, n = 30) patients and healthy controls (HC, n = 24).

Abundance in Group 1: decreased abundance in

NCBI	Quality Control	Links
Actinomycetota
Blautia sp. CAG:37
Clostridium sp. CAG:127
Clostridium sp. CAG:138
Dialister sp. CAG:486
Faecalibacterium duncaniae
Hungatella hathewayi 12489931
Megamonas
Megamonas hypermegale ART12/1
Megamonas rupellensis DSM 19944
Roseburia hominis A2-183
Clostridiales bacterium VE202-27
Mitsuokella multacida DSM 20544
unclassified Erysipelotrichaceae
Phascolarctobacterium succinatutens YIT 12067

Revision editor(s): Taofeecoh, WikiWorks