The Follicular Skin Microbiome in Patients With Hidradenitis Suppurativa and Healthy Controls

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Reviewed Marked as Reviewed by Peace Sandy on 2024-1-29
study design
Citation
PMID PubMed identifier for scientific articles.
DOI Digital object identifier for electronic documents.
Authors
Ring HC, Thorsen J, Saunte DM, Lilje B, Bay L, Riis PT, Larsen N, Andersen LO, Nielsen HV, Miller IM, Bjarnsholt T, Fuursted K, Jemec GB
Journal
JAMA dermatology
Year
2017
IMPORTANCE: Although the pathogenesis of hidradenitis suppurativa (HS) remains enigmatic, several factors point to potential involvement of the cutaneous microbiome. Insight into the cutaneous microbiome in HS using next-generation sequencing may provide novel data on the microbiological diversity of the skin. OBJECTIVE: To investigate the follicular skin microbiome in patients with HS and in healthy controls. DESIGN, SETTING, AND PARTICIPANTS: This case-control study obtained punch biopsy specimens from patients with HS (lesional and nonlesional) and healthy controls between October 1, 2014, and August 1, 2016. Data were analyzed from March to November 2016. Patients with HS were recruited from the Department of Dermatology, Zealand University Hospital, Roskilde, Denmark. Biopsy specimens were analyzed at the Department of Microbiology and Infection Control, Statens Serum Institut, Copenhagen, Denmark. None of the participants received any antibiotics (systemic or topical therapy) within 1 month before the study. In patients with HS, biopsy specimens were obtained from lesional skin (axilla or groin) and nonlesional skin. Only nodules containing at least 1 visible hair follicle were biopsied. Biopsy specimens from healthy controls were obtained from the axilla only. MAIN OUTCOMES AND MEASURES: The different microbiomes were investigated using next-generation sequencing targeting 16S and 18S ribosomal RNA. RESULTS: The skin microbiome was characterized in 30 patients with HS (mean [SD] age, 46.9 [14.0] years; 19 [63% female]) and 24 healthy controls (mean [SD] age, 32.2 [12.0] years; 13 [54% female]). The next-generation sequencing data provided a previously unreported (to our knowledge) characterization of the skin microbiome in HS. The study demonstrated that the microbiome in HS differs significantly from that in healthy controls in lesional and nonlesional skin. Overall, the following 5 microbiome types were identified: Corynebacterium species (type I), Acinetobacter and Moraxella species (type II), Staphylococcus epidermidis (type III), Porphyromonas and Peptoniphilus species (type IV), and Propionibacterium acnes (type V). In lesional skin, microbiome types consisted predominantly of type I or type IV. Microbiome type IV was not detected in healthy controls. Several taxa, including Propionibacterium, showed a significantly higher relative abundance in healthy controls vs HS skin, indicating that Propionibacterium may be part of the pathogenesis in HS. CONCLUSIONS AND RELEVANCE: The study findings suggest a link between a dysbiotic cutaneous microbiome and HS.

Experiment 1


Reviewed Marked as Reviewed by Peace Sandy on 2024-1-29

Curated date: 2024/01/17

Curator: Andre

Revision editor(s): Andre, Victoria

Subjects

Location of subjects
Denmark
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
Axilla skin Axillary skin,Skin of axilla,Axilla skin,axilla skin
Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
Hidradenitis suppurativa acne inversa,Acne inversa, familial,acne inversa, familial,hidradenitis,hidradenitis suppurativa,Hidradenitis suppurativa
Group 0 name Corresponds to the control (unexposed) group for case-control studies
Healthy controls
Group 1 name Corresponds to the case (exposed) group for case-control studies
Hidradenitis suppurativa patients
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Lesional skin of biopsy confirmed hidradenitis suppurativa
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)
1 month

Lab analysis

Sequencing type
16S
16S variable region One or more hypervariable region(s) of the bacterial 16S gene
V3-V4
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).
raw counts
Statistical test
Linear Regression
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)?
Yes

Alpha Diversity

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

Signature 1

Reviewed Marked as Reviewed by Peace Sandy on 2024-1-29

Curated date: 2024/01/18

Curator: Andre

Revision editor(s): Andre, Peace Sandy

Source: Fig4A and B

Description: A, Differential abundance at genus level between hidradenitis suppurativa (HS) lesional skin and healthy controls. Note significantly higher relative abundance of Propionibacterium in healthy controls and significantly higher relative abundance of Porphyromonas and Peptoniphilus. B, Differential abundance at species level between HS lesional skin and healthy controls. Note higher relative abundance of Propionibacterium acnes in healthy controls than in lesional samples.

Abundance in Group 1: increased abundance in Hidradenitis suppurativa patients

NCBI Quality ControlLinks
Actinomyces
Anaerococcus murdochii
Anaerococcus obesiensis
Anaerococcus vaginalis
Corynebacterium striatum
Dialister
Ezakiella
Finegoldia
Finegoldia magna
Mycobacteriales
Peptoniphilus
Aedoeadaptatus coxii
Peptoniphilus koenoeneniae
Peptoniphilus lacrimalis
Porphyromonas
Prevotellaceae
Sphingomonas
unclassified Porphyromonas
unclassified Peptoniphilus

Revision editor(s): Andre, Peace Sandy

Signature 2

Reviewed Marked as Reviewed by Peace Sandy on 2024-1-29

Curated date: 2024/01/18

Curator: Andre

Revision editor(s): Andre, Peace Sandy

Source: Fig4A and B

Description: A, Differential abundance at genus level between hidradenitis suppurativa (HS) lesional skin and healthy controls. Note significantly higher relative abundance of Propionibacterium in healthy controls and significantly higher relative abundance of Porphyromonas and Peptoniphilus. B, Differential abundance at species level between HS lesional skin and healthy controls. Note higher relative abundance of Propionibacterium acnes in healthy controls than in lesional samples.

Abundance in Group 1: decreased abundance in Hidradenitis suppurativa patients

NCBI Quality ControlLinks
Acinetobacter johnsonii
Comamonas
Cutibacterium acnes
Propionibacterium
unclassified Peptoniphilus

Revision editor(s): Andre, Peace Sandy

Experiment 2


Reviewed Marked as Reviewed by Peace Sandy on 2024-1-29

Curated date: 2024/01/18

Curator: Andre

Revision editor(s): Andre, Victoria

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies
Non lesional skin of Hidradenitis suppurativa patients
Group 1 name Corresponds to the case (exposed) group for case-control studies
Lesional skin of Hidradenitis suppurativa patients
Group 0 sample size Number of subjects in the control (unexposed) group
29

Lab analysis

Statistical Analysis

Alpha Diversity

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

Signature 1

Needs review

Curated date: 2024/01/18

Curator: Andre

Revision editor(s): Andre, Peace Sandy

Source: Fig4C and D

Description: C, Differential abundance at genus level between HS lesional skin and HS nonlesional skin. Note significantly higher relative abundance of Porphyromonas and Peptoniphilus in lesional skin than in nonlesional skin, Propionibacterium is more abundant in nonlesional skin. D, Differential abundance at species level between HS lesional skin and HS nonlesional skin. Note significantly reduced relative abundance of Propionibacterium acnes in HS lesional skin; higher relative abundances of Porphyromonas and Peptoniphilus are found in lesional skin. P values listed are adjusted for anatomical location. Black dots indicate the medians of each distribution.

Abundance in Group 1: increased abundance in Lesional skin of Hidradenitis suppurativa patients

NCBI Quality ControlLinks
Actinomyces
Anaerococcus obesiensis
Anaerococcus vaginalis
Campylobacter
Campylobacter ureolyticus
Dialister
Peptoniphilus
Porphyromonas
Porphyromonas bennonis
Porphyromonas somerae
unclassified Peptoniphilus
unclassified Porphyromonas
Acinetobacter baumannii

Revision editor(s): Andre, Peace Sandy

Signature 2

Reviewed Marked as Reviewed by Peace Sandy on 2024-1-29

Curated date: 2024/01/18

Curator: Andre

Revision editor(s): Andre, Peace Sandy

Source: Fig4C and D

Description: C, Differential abundance at genus level between HS lesional skin and HS nonlesional skin. Note significantly higher relative abundance of Porphyromonas and Peptoniphilus in lesional skin than in nonlesional skin, Propionibacterium is more abundant in nonlesional skin. D, Differential abundance at species level between HS lesional skin and HS nonlesional skin.

Abundance in Group 1: decreased abundance in Lesional skin of Hidradenitis suppurativa patients

NCBI Quality ControlLinks
Acinetobacter
Acinetobacter baumannii
Acinetobacter junii
Acinetobacter soli
Alicycliphilus
Aquabacterium
Cutibacterium acnes
Diaphorobacter
Diaphorobacter nitroreducens
Micrococcus
Micrococcus luteus
Moraxella
Paracoccus
Propionibacterium
Pseudomonas
Rhodoluna
unclassified Moraxella

Revision editor(s): Andre, Peace Sandy