Characterization of the forehead skin microbiome in the early phase of acne.


Journal

Journal of the European Academy of Dermatology and Venereology : JEADV
ISSN: 1468-3083
Titre abrégé: J Eur Acad Dermatol Venereol
Pays: England
ID NLM: 9216037

Informations de publication

Date de publication:
Aug 2024
Historique:
received: 12 12 2023
accepted: 27 05 2024
medline: 26 7 2024
pubmed: 26 7 2024
entrez: 25 7 2024
Statut: ppublish

Résumé

The skin microbiota is known to be imbalanced in acne vulgaris, but the changes occurring during the early stages of acne onset remain poorly described. To characterize the skin microbiome of subclinical stages of acne in adults and adolescents. The composition and diversity of the microbiota from non-lesional skin on the forehead of subjects with mild-to-moderate acne were compared to the ones from non-acne subjects. Analyses of skin swab samples were performed using high-throughput sequencing of the V1-V3 regions of the bacterial 16S ribosomal RNA gene, the tuf gene fragment of Staphylococcus species and the internal transcribed spacer (ITS1) region of the fungal rRNA gene to determine the relative abundance, alpha-diversity and beta-diversity of bacteria and fungi. Compared with non-acne subjects, acne subjects had a higher abundance of Cutibacterium (72.4% vs. 57.8%) and lower abundances of Corynebacterium (2.8% vs. 4.8%) and Streptococcus (1.4% vs. 3.2%). Bacterial alpha- and beta-diversity indices also differed significantly between the two groups, reflecting differences in richness, evenness, abundance and phylogenetic distance between bacterial populations. Differences were also observed at the level of Staphylococcus species: S. capitis was predominant in skin samples from non-acne subjects (46.7%), whereas S. epidermidis was the most abundant Staphylococcus species in non-lesional forehead skin areas of acne subjects (44.2%). Conversely, no significant between-group differences were found for fungi, with Malasseziales being the predominant order in both subject groups. Dysbiosis was observed very early in subclinical acne stages of the forehead skin, with the overall abundance, richness and evenness of the bacterial population being lower in acne than in non-acne skin samples. Dysbiosis was also found at the level of Staphylococcus species. The development of acne lesions could therefore be prevented by using a skin care product that rebalances facial skin microbiota at very early stages.

Sections du résumé

BACKGROUND BACKGROUND
The skin microbiota is known to be imbalanced in acne vulgaris, but the changes occurring during the early stages of acne onset remain poorly described.
OBJECTIVES OBJECTIVE
To characterize the skin microbiome of subclinical stages of acne in adults and adolescents.
METHODS METHODS
The composition and diversity of the microbiota from non-lesional skin on the forehead of subjects with mild-to-moderate acne were compared to the ones from non-acne subjects. Analyses of skin swab samples were performed using high-throughput sequencing of the V1-V3 regions of the bacterial 16S ribosomal RNA gene, the tuf gene fragment of Staphylococcus species and the internal transcribed spacer (ITS1) region of the fungal rRNA gene to determine the relative abundance, alpha-diversity and beta-diversity of bacteria and fungi.
RESULTS RESULTS
Compared with non-acne subjects, acne subjects had a higher abundance of Cutibacterium (72.4% vs. 57.8%) and lower abundances of Corynebacterium (2.8% vs. 4.8%) and Streptococcus (1.4% vs. 3.2%). Bacterial alpha- and beta-diversity indices also differed significantly between the two groups, reflecting differences in richness, evenness, abundance and phylogenetic distance between bacterial populations. Differences were also observed at the level of Staphylococcus species: S. capitis was predominant in skin samples from non-acne subjects (46.7%), whereas S. epidermidis was the most abundant Staphylococcus species in non-lesional forehead skin areas of acne subjects (44.2%). Conversely, no significant between-group differences were found for fungi, with Malasseziales being the predominant order in both subject groups.
CONCLUSION CONCLUSIONS
Dysbiosis was observed very early in subclinical acne stages of the forehead skin, with the overall abundance, richness and evenness of the bacterial population being lower in acne than in non-acne skin samples. Dysbiosis was also found at the level of Staphylococcus species. The development of acne lesions could therefore be prevented by using a skin care product that rebalances facial skin microbiota at very early stages.

Identifiants

pubmed: 39051132
doi: 10.1111/jdv.20203
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

3-11

Subventions

Organisme : Pierre Fabre Dermo-Cosmétique

Informations de copyright

© 2024 European Academy of Dermatology and Venereology.

Références

Harris‐Tryon TA, Grice EA. Microbiota and maintenance of skin barrier function. Science. 2022;376:940–945. https://doi.org/10.1126/science.abo0693
Carmona‐Cruz S, Orozco‐Covarrubias L, Saez‐de‐Ocariz M. The human skin microbiome in selected cutaneous diseases. Front Cell Infect Microbiol. 2022;12:834135. https://doi.org/10.3389/fcimb.2022.834135
Dréno B, Dagnelie MA, Khammari A, et al. The skin microbiome: a new actor in inflammatory acne. Am J Clin Dermatol. 2020;21:18–24. https://doi.org/10.1007/s40257‐020‐00531‐1
Lee YB, Byun EJ, Kim HS. Potential role of the microbiome in acne: a comprehensive review. J Clin Med. 2019;8:987. https://doi.org/10.3390/jcm8070987
Ramasamy S, Barnard E, Dawson TL Jr, Li H. The role of the skin microbiota in acne pathophysiology. Br J Dermatol. 2019;181:691–699. https://doi.org/10.1111/bjd.18230
Akaza N, Takasaki K, Nishiyama E, Usui A, Miura S, Yokoi A, et al. The microbiome in comedonal contents of inflammatory acne vulgaris is composed of an overgrowth of Cutibacterium spp. and other cutaneous microorganisms. Clin Cosmet Investig Dermatol. 2022;15:2003–2012. https://doi.org/10.2147/CCID.S379609
Xu X, Ran X, Tang J, Pradhan S, Dai Y, Zhuang K, et al. Skin microbiota in non‐inflammatory and inflammatory lesions of acne vulgaris: the underlying changes within the pilosebaceous unit. Mycopathologia. 2021;186:863–869. https://doi.org/10.1007/s11046‐021‐00586‐6
Dréno B, Bettoli V, Araviiskaia E, Sanchez Viera M, Bouloc A. The influence of exposome on acne. J Eur Acad Dermatol Venereol. 2018;32:812–819. https://doi.org/10.1111/jdv.14820
Kistowska M, Meier B, Proust T, Feldmeyer L, Cozzio A, Kuendig T, et al. Propionibacterium acnes promotes Th17 and Th17/Th1 responses in acne patients. J Invest Dermatol. 2015;135:110–118. https://doi.org/10.1038/jid.2014.290
Schneider AM, Nolan ZT, Banerjee K, Paine AR, Cong Z, Gettle SL, et al. Evolution of the facial skin microbiome during puberty in normal and acne skin. J Eur Acad Dermatol Venereol. 2023;37:166–175. https://doi.org/10.1111/jdv.18616
Eliasse Y, Leveque E, Garidou L, Battut L, McKenzie B, Nocera T, et al. IL‐17(+) mast cell/T helper cell axis in the early stages of acne. Front Immunol. 2021;12:740540. https://doi.org/10.3389/fimmu.2021.740540
Mias C, Mengeaud V, Bessou‐Touya S, Duplan H. Recent advances in understanding inflammatory acne: deciphering the relationship between Cutibacterium acnes and Th17 inflammatory pathway. J Eur Acad Dermatol Venereol. 2023a;37(Suppl 2):3–11. https://doi.org/10.1111/jdv.18794
Dreno B, Martin R, Moyal D, Henley JB, Khammari A, Seite S. Skin microbiome and acne vulgaris: Staphylococcus, a new actor in acne. Exp Dermatol. 2017;26:798–803. https://doi.org/10.1111/exd.13296
Guo Z, Yang Y, Wu Q, Liu M, Zhou L, Zhang L, et al. New insights into the characteristic skin microorganisms in different grades of acne and different acne sites. Front Microbiol. 2023;14:1167923. https://doi.org/10.3389/fmicb.2023.1167923
Li CX, You ZX, Lin YX, Liu HY, Su J. Skin microbiome differences relate to the grade of acne vulgaris. J Dermatol. 2019;46:787–790. https://doi.org/10.1111/1346‐8138.14952
Ahluwalia J, Borok J, Haddock ES, Ahluwalia RS, Schwartz EW, Hosseini D, et al. The microbiome in preadolescent acne: assessment and prospective analysis of the influence of benzoyl peroxide. Pediatr Dermatol. 2019;36:200–206. https://doi.org/10.1111/pde.13741
Coughlin CC, Swink SM, Horwinski J, Sfyroera G, Bugayev J, Grice EA, et al. The preadolescent acne microbiome: a prospective, randomized, pilot study investigating characterization and effects of acne therapy. Pediatr Dermatol. 2017;34:661–664. https://doi.org/10.1111/pde.13261
Kim J, Park T, Kim HJ, An S, Sul WJ. Inferences in microbial structural signatures of acne microbiome and mycobiome. J Microbiol. 2021;59:369–375. https://doi.org/10.1007/s12275‐021‐0647‐1
Huang C, Zhuo F, Han B, Li W, Jiang B, Zhang K, et al. The updates and implications of cutaneous microbiota in acne. Cell Biosci. 2023;13:113. https://doi.org/10.1186/s13578‐023‐01072‐w
Fourniere M, Latire T, Souak D, Feuilloley MGJ, Bedoux G. Staphylococcus epidermidis and Cutibacterium acnes: two major sentinels of skin microbiota and the influence of cosmetics. Microorganisms. 2020;8:1752. https://doi.org/10.3390/microorganisms8111752
Chien AL, Tsai J, Leung S, Mongodin EF, Nelson AM, Kang S, et al. Association of systemic antibiotic treatment of acne with skin microbiota characteristics. JAMA Dermatol. 2019;155:425–434. https://doi.org/10.1001/jamadermatol.2018.5221
Lam M, Hu A, Fleming P, Lynde CW. The impact of acne treatment on skin bacterial microbiota: a systematic review. J Cutan Med Surg. 2022;26:93–97. https://doi.org/10.1177/12034754211037994
Dréno B, Poli F, Pawin H, Beylot C, Faure M, Chivot M, et al. Development and evaluation of a Global Acne Severity Scale (GEA Scale) suitable for France and Europe. J Eur Acad Dermatol Venereol. 2011;25:43–48. https://doi.org/10.1111/j.1468‐3083.2010.03685.x
Bergeron M, Dauwalder O, Gouy M, Freydiere AM, Bes M, Meugnier H, et al. Species identification of staphylococci by amplification and sequencing of the tuf gene compared to the gap gene and by matrix‐assisted laser desorption ionization time‐of‐flight mass spectrometry. Eur J Clin Microbiol Infect Dis. 2011;30:343–354. https://doi.org/10.1007/s10096‐010‐1091‐z
Ghebremedhin B, Layer F, Konig W, Konig B. Genetic classification and distinguishing of Staphylococcus species based on different partial gap, 16S rRNA, hsp60, rpoB, sodA, and tuf gene sequences. J Clin Microbiol. 2008;46:1019–1025. https://doi.org/10.1128/JCM.02058‐07
Findley K, Oh J, Yang J, Conlan S, Deming C, Meyer JA, et al. Topographic diversity of fungal and bacterial communities in human skin. Nature. 2013;498:367–370. https://doi.org/10.1038/nature12171
R Core Team. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2022. https://www.R‐project.org
Cavallo I, Sivori F, Truglio M, De Maio F, Lucantoni F, Cardinali G, et al. Skin dysbiosis and Cutibacterium acnes biofilm in inflammatory acne lesions of adolescents. Sci Rep. 2022;12:21104. https://doi.org/10.1038/s41598‐022‐25436‐3
Zhou L, Liu X, Li X, He X, Xiong X, Lai J. Epidermal barrier integrity is associated with both skin microbiome diversity and composition in patients with acne vulgaris. Clin Cosmet Investig Dermatol. 2022;15:2065–2075. https://doi.org/10.2147/ccid.S377759
O'Neill AM, Nakatsuji T, Hayachi A, Williams MR, Mills RH, Gonzalez DJ, et al. Identification of a human skin commensal bacterium that selectively kills Cutibacterium acnes. J Invest Dermatol. 2020;140:1619–1628.e1612. https://doi.org/10.1016/j.jid.2019.12.026
Park M, Park S, Jung WH. Skin commensal fungus Malassezia and its lipases. J Microbiol Biotechnol. 2021;31:637–644. https://doi.org/10.4014/jmb.2012.12048
Fabbrocini G, Saint Aroman M. Cosmeceuticals based on Rhealba(®) Oat plantlet extract for the treatment of acne vulgaris. J Eur Acad Dermatol Venereol. 2014;28(Suppl 6):1–6. https://doi.org/10.1111/jdv.12791
Sultan OS, Kantilal HK, Khoo SP, Davamani AF, Eusufzai SZ, Rashid F, et al. The potential of α‐Mangostin from Garcinia mangostana as an effective antimicrobial agent – a systematic review and meta‐analysis. Antibiotics (Basel). 2022;11:717. https://doi.org/10.3390/antibiotics11060717
Chen LG, Yang LL, Wang CC. Anti‐inflammatory activity of mangostins from Garcinia mangostana. Food Chem Toxicol. 2008;46:688–693. https://doi.org/10.1016/j.fct.2007.09.096
Phumlek K, Itharat A, Pongcharoen P, Chakkavittumrong P, Lee HY, Moon GS, et al. Garcinia mangostana hydrogel patch: bactericidal activity and clinical safety for acne vulgaris treatment. Res Pharm Sci. 2022;17:457–467. https://doi.org/10.4103/1735‐5362.355195
Carballido F, Philippe A, Maitre M, Lauze C, Chanssard N, Garidou L, et al. A dermocosmetic product containing the sap of oat plantlets and Garcinia mangostana extract improves the clinical signs of acne. J Eur Acad Dermatol Venereol. 2024;38:12–20.
Paganelli A, Righi V, Tarentini E, Magnoni C. Current knowledge in skin metabolomics: updates from literature review. Int J Mol Sci. 2022;23:8776. https://doi.org/10.3390/ijms23158776
Jacques C, Bacqueville D, Jamin EL, Maitre M, Delsol C, Simcic‐Mori A, et al. Multi‐omics approach to understand the impact of sun exposure on an in vitro skin ecosystem and evaluate a new broad‐spectrum sunscreen. Photochem Photobiol. 2024;100:477–490. https://doi.org/10.1111/php.13841
Han HS, Shin SH, Choi BY, Koo N, Lim S, Son D, et al. A split face study on the effect of an anti‐acne product containing fermentation products of Enterococcus faecalis CBT SL‐5 on skin microbiome modification and acne improvement. J Microbiol. 2022;60:488–495. https://doi.org/10.1007/s12275‐022‐1520‐6
Mias C, Thouvenin MD, Gravier E, Dalmon S, Bouyer K, Alvarez S, et al. Change in Cutibacterium acnes phylotype abundance and improvement of clinical parameters using a new dermocosmetic product containing Myrtus communis and celastrol enriched plant cell culture extracts in patients with acne vulgaris. J Eur Acad Dermatol Venereol. 2023b;37(Suppl 2):20–25. https://doi.org/10.1111/jdv.18792
Pecastaings S, Roques C, Nocera T, Peraud C, Mengeaud V, Khammari A, et al. Characterisation of Cutibacterium acnes phylotypes in acne and in vivo exploratory evaluation of Myrtacine®. J Eur Acad Dermatol Venereol. 2018;32(Suppl 2):15–23. https://doi.org/10.1111/jdv.15042
Tollenaere M, Boira C, Chapuis E, Lapierre L, Jarrin C, Robe P, et al. Action of Mangifera indica leaf extract on acne‐prone skin through sebum harmonization and targeting C. acnes. Molecules. 2022;27:4769. https://doi.org/10.3390/molecules27154769
Ho HH, Chen CW, Yi TH, Huang YF, Kuo YW, Lin JH, et al. Novel application of a co‐fermented postbiotics of TYCA06/AP‐32/CP‐9/collagen in the improvement of acne vulgaris – a randomized clinical study of efficacy evaluation. J Cosmet Dermatol. 2022;21:6249–6260. https://doi.org/10.1111/jocd.15228
Hou JH, Shin H, Jang KH, Park CK, Koo B, Shin H, et al. Anti‐acne properties of hydrophobic fraction of red ginseng (Panax ginseng C.A. Meyer) and its active components. Phytother Res. 2019;33:584–590. https://doi.org/10.1002/ptr.6243
Karadag AS, Aslan Kayiran M, Wu CY, Chen W, Parish LC. Antibiotic resistance in acne: changes, consequences and concerns. J Eur Acad Dermatol Venereol. 2021;35:73–78. https://doi.org/10.1111/jdv.16686
Soleymani S, Zargaran A, Farzaei MH, Iranpanah A, Heydarpour F, Najafi F, et al. The effect of a hydrogel made by Nigella sativa L. on acne vulgaris: a randomized double‐blind clinical trial. Phytother Res. 2020;34:3052–3062. https://doi.org/10.1002/ptr.6739

Auteurs

M Maître (M)

Pierre Fabre Dermo-Cosmétique and Personal Care, Research & Development, Toulouse, France.

E Gravier (E)

Pierre Fabre Dermo-Cosmétique and Personal Care, Research & Development, Toulouse, France.

A Simcic-Mori (A)

Pierre Fabre Dermo-Cosmétique and Personal Care, Research & Development, Toulouse, France.

C Géniès (C)

Pierre Fabre Dermo-Cosmétique and Personal Care, Research & Development, Toulouse, France.

C Mias (C)

Pierre Fabre Dermo-Cosmétique and Personal Care, Research & Development, Toulouse, France.

S Alvarez-Georges (S)

Pierre Fabre Dermo-Cosmétique and Personal Care, Research & Development, Toulouse, France.

A Noustens (A)

Pierre Fabre Dermo-Cosmétique and Personal Care, Research & Development, Toulouse, France.

K Bouyer (K)

Pierre Fabre Dermo-Cosmétique and Personal Care, Research & Development, Toulouse, France.

S Bessou-Touya (S)

Pierre Fabre Dermo-Cosmétique and Personal Care, Research & Development, Toulouse, France.

F Carballido (F)

Laboratoires A-Derma, Pierre Fabre Dermo-Cosmétique, Lavaur, France.

H Duplan (H)

Pierre Fabre Dermo-Cosmétique and Personal Care, Research & Development, Toulouse, France.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH