{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,23]],"date-time":"2026-10-23T21:06:36Z","timestamp":1792789596456,"version":"4.5.0"},"reference-count":116,"publisher":"MDPI AG","issue":"21","license":[{"start":{"date-parts":[[2024,10,24]],"date-time":"2024-10-24T00:00:00Z","timestamp":1729728000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Xjenza Malta","award":["R&I-2022-019L"],"award-info":[{"award-number":["R&I-2022-019L"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Acne vulgaris is a widespread dermatological condition that significantly affects the quality of life of adolescents and adults. Traditionally, acne pathogenesis has been linked to factors such as excess sebum production, follicular hyperkeratinization, and the presence of Cutibacterium acnes (C. acnes). However, recent studies have highlighted the role of the skin microbiome, shifting focus from individual pathogens to microbial community dynamics. This review critically evaluates existing research on the skin microbiome and its relationship to acne, focusing on microbial diversity, C. acnes strain variability, and emerging therapies targeting the microbiome. While certain studies associate C. acnes with acne severity, others show this bacterium\u2019s presence in healthy skin, suggesting that strain-specific differences and overall microbial balance play crucial roles. Emerging therapeutic approaches, such as probiotics and bacteriophage therapy, aim to restore microbial equilibrium or selectively target pathogenic strains without disturbing the broader microbiome. However, the lack of standardized methodologies, limited longitudinal studies, and the narrow focus on bacterial communities are major limitations in current research. Future research should explore the broader skin microbiome, including fungi and viruses, use consistent methodologies, and focus on longitudinal studies to better understand microbial fluctuations over time. Addressing these gaps will enable the development of more effective microbiome-based treatments for acne. In conclusion, while microbiome-targeted therapies hold promise, further investigation is needed to validate their efficacy and safety, paving the way for innovative, personalized acne management strategies.<\/jats:p>","DOI":"10.3390\/ijms252111422","type":"journal-article","created":{"date-parts":[[2024,10,24]],"date-time":"2024-10-24T04:11:38Z","timestamp":1729743098000},"page":"11422","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":64,"title":["The Role of the Skin Microbiome in Acne: Challenges and Future Therapeutic Opportunities"],"prefix":"10.3390","volume":"25","author":[{"ORCID":"https:\/\/orcid.org\/0009-0009-2254-3931","authenticated-orcid":false,"given":"Alicja","family":"Nied\u017awiedzka","sequence":"first","affiliation":[{"name":"The BioArte Ltd., Malta Life Science Park, Triq San Giljan, SGN 3000 San Gwann, Malta"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0004-8988-5278","authenticated-orcid":false,"given":"Maria Pia","family":"Micallef","sequence":"additional","affiliation":[{"name":"The BioArte Ltd., Malta Life Science Park, Triq San Giljan, SGN 3000 San Gwann, Malta"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Manuele","family":"Biazzo","sequence":"additional","affiliation":[{"name":"The BioArte Ltd., Malta Life Science Park, Triq San Giljan, SGN 3000 San Gwann, Malta"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5391-3378","authenticated-orcid":false,"given":"Christine","family":"Podrini","sequence":"additional","affiliation":[{"name":"The BioArte Ltd., Malta Life Science Park, Triq San Giljan, SGN 3000 San Gwann, Malta"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,10,24]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1038\/nrmicro.2017.157","article-title":"The Human Skin Microbiome","volume":"16","author":"Byrd","year":"2018","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Wei, Q., Li, Z., Gu, Z., Liu, X., Krutmann, J., Wang, J., and Xia, J. (2022). Shotgun Metagenomic Sequencing Reveals Skin Microbial Variability from Different Facial Sites. Front. Microbiol., 13.","DOI":"10.3389\/fmicb.2022.933189"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1111\/jdv.15043","article-title":"Cutibacterium acnes (Propionibacterium acnes) and Acne Vulgaris: A Brief Look at the Latest Updates","volume":"32","author":"Corvec","year":"2018","journal-title":"J. Eur. Acad. Dermatol. Venereol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"2152","DOI":"10.1038\/jid.2013.21","article-title":"Propionibacterium acnes Strain Populations in the Human Skin Microbiome Associated with Acne","volume":"133","author":"Tomida","year":"2013","journal-title":"J. Investig. Dermatol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"15029","DOI":"10.1038\/nrdp.2015.29","article-title":"Acne Vulgaris","volume":"1","author":"Makrantonaki","year":"2015","journal-title":"Nat. Rev. Dis. Primers"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1261","DOI":"10.1111\/jdv.13776","article-title":"European Evidence-based (S3) Guideline for the Treatment of Acne\u2013Update 2016\u2013Short Version","volume":"30","author":"Nast","year":"2016","journal-title":"Acad. Dermatol. Venereol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1038\/nature12171","article-title":"Topographic Diversity of Fungal and Bacterial Communities in Human Skin","volume":"498","author":"Findley","year":"2013","journal-title":"Nature"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"510","DOI":"10.1016\/j.tim.2013.07.001","article-title":"The Human Virome: New Tools and Concepts","volume":"21","author":"Lecuit","year":"2013","journal-title":"Trends Microbiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"e01578-15","DOI":"10.1128\/mBio.01578-15","article-title":"The Human Skin Double-Stranded DNA Virome: Topographical and Temporal Diversity, Genetic Enrichment, and Dynamic Associations with the Host Microbiome","volume":"6","author":"Hannigan","year":"2015","journal-title":"mBio"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Natarelli, N., Gahoonia, N., and Sivamani, R.K. (2023). Bacteriophages and the Microbiome in Dermatology: The Role of the Phageome and a Potential Therapeutic Strategy. Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms24032695"},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Foulongne, V., Sauvage, V., Hebert, C., Dereure, O., Cheval, J., Gouilh, M.A., Pariente, K., Segondy, M., Burgui\u00e8re, A., and Manuguerra, J.-C. (2012). Human Skin Microbiota: High Diversity of DNA Viruses Identified on the Human Skin by High Throughput Sequencing. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0038499"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"50S","DOI":"10.1097\/PRS.0000000000007621","article-title":"Temporal Variation of the Facial Skin Microbiome: A 2-Year Longitudinal Study in Healthy Adults","volume":"147","author":"Hillebrand","year":"2021","journal-title":"Plast. Reconstr. Surg."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"854","DOI":"10.1016\/j.cell.2016.04.008","article-title":"Temporal Stability of the Human Skin Microbiome","volume":"165","author":"Oh","year":"2016","journal-title":"Cell"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"595","DOI":"10.1016\/j.marpolbul.2019.06.047","article-title":"Alterations of the Human Skin Microbiome after Ocean Water Exposure","volume":"145","author":"Nielsen","year":"2019","journal-title":"Mar. Pollut. Bull."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Lee, H.J., Jeong, S.E., Lee, S., Kim, S., Han, H., and Jeon, C.O. (2018). Effects of Cosmetics on the Skin Microbiome of Facial Cheeks with Different Hydration Levels. MicrobiologyOpen, 7.","DOI":"10.1002\/mbo3.557"},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Rozas, M., Hart De Ruijter, A., Fabrega, M.J., Zorgani, A., Guell, M., Paetzold, B., and Brillet, F. (2021). From Dysbiosis to Healthy Skin: Major Contributions of Cutibacterium acnes to Skin Homeostasis. Microorganisms, 9.","DOI":"10.3390\/microorganisms9030628"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"829","DOI":"10.1016\/j.clindermatol.2021.08.021","article-title":"The Skin Microbiome and the Gut-Skin Axis","volume":"39","author":"Sinha","year":"2021","journal-title":"Clin. Dermatol."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Lee, Y.B., Byun, E.J., and Kim, H.S. (2019). Potential Role of the Microbiome in Acne: A Comprehensive Review. J. Clin. Med., 8.","DOI":"10.3390\/jcm8070987"},{"key":"ref_19","first-page":"5","article-title":"Beyond Skincare Routines: Follow Your Gut to Healthy Skin\u2014A Review of the Interplay between Gut Microbiome and Skin","volume":"6","author":"Criton","year":"2024","journal-title":"J. Skin. Sex. Transm. Dis."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Nguyen, A.V., and Soulika, A.M. (2019). The Dynamics of the Skin\u2019s Immune System. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20081811"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"677","DOI":"10.1038\/jid.2013.438","article-title":"IL-1\u03b2 Drives Inflammatory Responses to Propionibacterium acnes In Vitro and In Vivo","volume":"134","author":"Kistowska","year":"2014","journal-title":"J. Investig. Dermatol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"54","DOI":"10.5021\/ad.2018.30.1.54","article-title":"Epidermal Growth Factor Attenuated the Expression of Inflammatory Cytokines in Human Epidermal Keratinocyte Exposed to Propionibacterium acnes","volume":"30","author":"Kim","year":"2018","journal-title":"Ann. Dermatol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"2747","DOI":"10.1038\/jid.2014.221","article-title":"Propionibacterium acnes Activates the NLRP3 Inflammasome in Human Sebocytes","volume":"134","author":"Li","year":"2014","journal-title":"J. Investig. Dermatol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1038\/jid.2013.309","article-title":"Propionibacterium acnes Induces IL-1\u03b2 Secretion via the NLRP3 Inflammasome in Human Monocytes","volume":"134","author":"Qin","year":"2014","journal-title":"J. Investig. Dermatol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"110","DOI":"10.1038\/jid.2014.290","article-title":"Propionibacterium acnes Promotes Th17 and Th17\/Th1 Responses in Acne Patients","volume":"135","author":"Kistowska","year":"2015","journal-title":"J. Investig. Dermatol."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Lheure, C., Grange, P.A., Ollagnier, G., Morand, P., D\u00e9sir\u00e9, N., Sayon, S., Corvec, S., Raingeaud, J., Marcelin, A.-G., and Calvez, V. (2016). TLR-2 Recognizes Propionibacterium acnes CAMP Factor 1 from Highly Inflammatory Strains. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0167237"},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Huang, L., Yang, S., Yu, X., Fang, F., Zhu, L., Wang, L., Zhang, X., Yang, C., Qian, Q., and Zhu, T. (2024). Association of Different Cell Types and Inflammation in Early Acne Vulgaris. Front. Immunol., 15.","DOI":"10.3389\/fimmu.2024.1275269"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"eabh1478","DOI":"10.1126\/scitranslmed.abh1478","article-title":"Antimicrobial Production by Perifollicular Dermal Preadipocytes Is Essential to the Pathophysiology of Acne","volume":"14","author":"Liggins","year":"2022","journal-title":"Sci. Transl. Med."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"e398","DOI":"10.1111\/jdv.14206","article-title":"Propionibacterium acnes Phylotypes and Acne Severity: An Observational Prospective Study","volume":"31","author":"Paugam","year":"2017","journal-title":"Acad. Dermatol. Venereol."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Scholz, C.F.P., Jensen, A., Lomholt, H.B., Br\u00fcggemann, H., and Kilian, M. (2014). A Novel High-Resolution Single Locus Sequence Typing Scheme for Mixed Populations of Propionibacterium acnes In Vivo. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0104199"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"262","DOI":"10.2340\/00015555-2847","article-title":"Decrease in Diversity of Propionibacterium acnes Phylotypes in Patients with Severe Acne on the Back","volume":"98","author":"Dagnelie","year":"2018","journal-title":"Acta Derm. Venerol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1248","DOI":"10.1111\/1346-8138.13913","article-title":"Antimicrobial Susceptibility and Phylogenetic Analysis of Propionibacterium acnes Isolated from Acne Patients in Japan between 2013 and 2015","volume":"44","author":"Nakase","year":"2017","journal-title":"J. Dermatol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1619","DOI":"10.1016\/j.jid.2019.12.026","article-title":"Identification of a Human Skin Commensal Bacterium That Selectively Kills Cutibacterium acnes","volume":"140","author":"Nakatsuji","year":"2020","journal-title":"J. Investig. Dermatol."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Jang, I.-T., Yang, M., Kim, H.-J., and Park, J.-K. (2020). Novel Cytoplasmic Bacteriocin Compounds Derived from Staphylococcus Epidermidis Selectively Kill Staphylococcus Aureus, Including Methicillin-Resistant Staphylococcus Aureus (MRSA). Pathogens, 9.","DOI":"10.3390\/pathogens9020087"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Cebri\u00e1n, R., Ar\u00e9valo, S., Rubi\u00f1o, S., Arias-Santiago, S., Rojo, M.D., Montalb\u00e1n-L\u00f3pez, M., Mart\u00ednez-Bueno, M., Valdivia, E., and Maqueda, M. (2018). Control of Propionibacterium acnes by Natural Antimicrobial Substances: Role of the Bacteriocin AS-48 and Lysozyme. Sci. Rep., 8.","DOI":"10.1038\/s41598-018-29580-7"},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"O\u2019Sullivan, J.N., Rea, M.C., O\u2019Connor, P.M., Hill, C., and Ross, R.P. (2019). Human Skin Microbiota Is a Rich Source of Bacteriocin-Producing Staphylococci That Kill Human Pathogens. FEMS Microbiol. Ecol., 95.","DOI":"10.1093\/femsec\/fiy241"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1137","DOI":"10.1016\/j.jid.2017.11.034","article-title":"Skin Commensal Malassezia Globosa Secreted Protease Attenuates Staphylococcus Aureus Biofilm Formation","volume":"138","author":"Li","year":"2018","journal-title":"J. Investig. Dermatol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1128\/CMR.15.1.21-57.2002","article-title":"Immunology of Diseases Associated with Malassezia Species","volume":"15","author":"Ashbee","year":"2002","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"5954034","DOI":"10.1155\/2018\/5954034","article-title":"Lipids and the Permeability and Antimicrobial Barriers of the Skin","volume":"2018","author":"Wertz","year":"2018","journal-title":"J. Lipids"},{"key":"ref_40","unstructured":"(2024, September 25). Genus-Wide Comparative Genomics of Malassezia Delineates Its Phylogeny, Physiology, and Niche Adaptation on Human Skin-PubMed, Available online: https:\/\/pubmed.ncbi.nlm.nih.gov\/26539826\/."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1016\/j.chom.2013.03.008","article-title":"Identification of Distinct Ligands for the C-Type Lectin Receptors Mincle and Dectin-2 in the Pathogenic Fungus Malassezia","volume":"13","author":"Ishikawa","year":"2013","journal-title":"Cell Host Microbe"},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Sparber, F., and LeibundGut-Landmann, S. (2017). Host Responses to Malassezia Spp. in the Mammalian Skin. Front. Immunol., 8.","DOI":"10.3389\/fimmu.2017.01614"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"280","DOI":"10.1007\/s00403-005-0594-4","article-title":"Toll-like Receptor 2 (TLR2) Mediates Intracellular Signalling in Human Keratinocytes in Response to Malassezia Furfur","volume":"297","author":"Baroni","year":"2006","journal-title":"Arch. Dermatol. Res."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1016\/j.chom.2019.02.002","article-title":"The Skin Commensal Yeast Malassezia Triggers a Type 17 Response That Coordinates Anti-Fungal Immunity and Exacerbates Skin Inflammation","volume":"25","author":"Sparber","year":"2019","journal-title":"Cell Host Microbe"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"885","DOI":"10.1046\/j.1365-2133.2000.03467.x","article-title":"The Cutaneous Microflora of Adolescent, Persistent Andlate-Onset Acne Patients Does Not Differ: MICROFLORA OF ACNE","volume":"142","author":"Till","year":"2000","journal-title":"Br. J. Dermatol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"906","DOI":"10.1111\/1346-8138.13245","article-title":"Microorganisms Inhabiting Follicular Contents of Facial Acne Are Not Only Propionibacterium but Also Malassezia spp.","volume":"43","author":"Akaza","year":"2016","journal-title":"J. Dermatol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1159\/000356777","article-title":"Analysis of Facial Skin-Resident Microbiota in Japanese Acne Patients","volume":"228","author":"Numata","year":"2014","journal-title":"Dermatology"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"613","DOI":"10.1111\/j.1346-8138.2011.01477.x","article-title":"Malassezia Globosa Tends to Grow Actively in Summer Conditions More than Other Cutaneous Malassezia Species","volume":"39","author":"Akaza","year":"2012","journal-title":"J. Dermatol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"628","DOI":"10.3760\/cma.j.issn.0366-6999.2010.05.022","article-title":"Malasseziainfection: Is There Any Chance or Necessity in Refractory Acne?","volume":"123","author":"Hu","year":"2010","journal-title":"Chin. Med. J."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1111\/j.1087-0024.2005.10119.x","article-title":"Three Etiologic Facets of Dandruff and Seborrheic Dermatitis: Malassezia Fungi, Sebaceous Lipids, and Individual Sensitivity","volume":"10","author":"DeAngelis","year":"2005","journal-title":"J. Investig. Dermatol. Symp. Proc."},{"key":"ref_51","first-page":"593","article-title":"Antibiotic Resistant Acne","volume":"17","author":"Leyden","year":"1976","journal-title":"Cutis"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/S0190-9622(83)70005-8","article-title":"Propionibacterium acnes Resistance to Antibiotics in Acne Patients","volume":"8","author":"Leyden","year":"1983","journal-title":"J. Am. Acad. Dermatol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"945","DOI":"10.1016\/j.jaad.2015.12.037","article-title":"Guidelines of Care for the Management of Acne Vulgaris","volume":"74","author":"Zaenglein","year":"2016","journal-title":"J. Am. Acad. Dermatol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"833","DOI":"10.1111\/j.1346-8138.2012.01626.x","article-title":"Antibiotic Resistance of Microbial Strains Isolated from Korean Acne Patients","volume":"39","author":"Moon","year":"2012","journal-title":"J. Dermatol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"21","DOI":"10.13181\/mji.v28i1.2735","article-title":"The Susceptibility of Pathogens Associated with Acne Vulgaris to Antibiotics","volume":"28","author":"Sitohang","year":"2019","journal-title":"Med. J. Indones."},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Alkhawaja, E., Hammadi, S., Abdelmalek, M., Mahasneh, N., Alkhawaja, B., and Abdelmalek, S.M. (2020). Antibiotic Resistant Cutibacterium acnes among Acne Patients in Jordan: A Cross Sectional Study. BMC Dermatol., 20.","DOI":"10.1186\/s12895-020-00108-9"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"1357","DOI":"10.1007\/s10096-020-03852-5","article-title":"Propionibacterium\/Cutibacterium Species\u2013Related Positive Samples, Identification, Clinical and Resistance Features: A 10-Year Survey in a French Hospital","volume":"39","author":"Broly","year":"2020","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"687","DOI":"10.1111\/exd.12482","article-title":"Three Dimensional Distribution of Propionibacterium acnes Biofilms in Human Skin","volume":"23","author":"Jahns","year":"2014","journal-title":"Exp. Dermatol."},{"key":"ref_59","doi-asserted-by":"crossref","unstructured":"Coenye, T., Spittaels, K.-J., and Achermann, Y. (2022). The Role Of Biofilm Formation in the Pathogenesis and Antimicrobial Susceptibility of Cutibacterium acnes. Biofilm, 4.","DOI":"10.1016\/j.bioflm.2021.100063"},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Sionov, R.V., and Steinberg, D. (2022). Targeting the Holy Triangle of Quorum Sensing, Biofilm Formation, and Antibiotic Resistance in Pathogenic Bacteria. Microorganisms, 10.","DOI":"10.3390\/microorganisms10061239"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"102580","DOI":"10.1016\/j.anaerobe.2022.102580","article-title":"Cutibacterium acnes Biofilm Forming Clinical Isolates Modify the Formation and Structure of Staphylococcus Aureus Biofilms, Increasing Their Susceptibility to Antibiotics","volume":"76","author":"Abbott","year":"2022","journal-title":"Anaerobe"},{"key":"ref_62","doi-asserted-by":"crossref","unstructured":"Bronnec, V., Eilers, H., Jahns, A.C., Omer, H., and Alexeyev, O.A. (2021). Propionibacterium (Cutibacterium) Granulosum Extracellular DNase BmdE Targeting Propionibacterium (Cutibacterium) Acnes Biofilm Matrix, a Novel Inter-Species Competition Mechanism. Front. Cell Infect. Microbiol., 11.","DOI":"10.3389\/fcimb.2021.809792"},{"key":"ref_63","first-page":"677","article-title":"Topical Treatment With an Agent Disruptive to P. Acnes Biofilm Provides Positive Therapeutic Response: Results of a Randomized Clinical Trial","volume":"15","author":"Bernhardt","year":"2016","journal-title":"J. Drugs Dermatol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"1006.e1","DOI":"10.1016\/j.jaad.2023.12.017","article-title":"Guidelines of Care for the Management of Acne Vulgaris","volume":"90","author":"Reynolds","year":"2024","journal-title":"J. Am. Acad. Dermatol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1111\/j.1610-0387.2006.05931.x","article-title":"Acne Therapy with Topical Benzoyl Peroxide, Antibiotics and Azelaic Acid","volume":"4","author":"Worret","year":"2006","journal-title":"JDDG J. Dtsch. Dermatol. Ges."},{"key":"ref_66","doi-asserted-by":"crossref","unstructured":"Eishi, Y. (2023). Potential Association of Cutibacterium acnes with Sarcoidosis as an Endogenous Hypersensitivity Infection. Microorganisms, 11.","DOI":"10.3390\/microorganisms11020289"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1186\/s13027-022-00427-1","article-title":"Multiple Pathogens and Prostate Cancer","volume":"17","author":"Lawson","year":"2022","journal-title":"Infect. Agents Cancer"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"1410","DOI":"10.1016\/j.jse.2020.11.011","article-title":"Cutibacterium acnes in Shoulder Surgery: A Scoping Review of Strategies for Prevention, Diagnosis, and Treatment","volume":"30","author":"Foster","year":"2021","journal-title":"J. Shoulder Elb. Surg."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"1539","DOI":"10.1016\/j.jse.2018.06.012","article-title":"Neer Award 2018: Benzoyl Peroxide Effectively Decreases Preoperative Cutibacterium acnes Shoulder Burden: A Prospective Randomized Controlled Trial","volume":"27","author":"Kolakowski","year":"2018","journal-title":"J. Shoulder Elb. Surg."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"eabd8077","DOI":"10.1126\/scitranslmed.abd8077","article-title":"Alterations of Human Skin Microbiome and Expansion of Antimicrobial Resistance after Systemic Antibiotics","volume":"13","author":"Jo","year":"2021","journal-title":"Sci. Transl. Med."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1001\/jamadermatol.2018.5221","article-title":"Association of Systemic Antibiotic Treatment of Acne With Skin Microbiota Characteristics","volume":"155","author":"Chien","year":"2019","journal-title":"JAMA Dermatol."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"840","DOI":"10.1046\/j.1365-2133.2002.04690.x","article-title":"Prevalence of Antibiotic-resistant Propionibacteria on the Skin of Acne Patients: 10-year Surveillance Data and Snapshot Distribution Study","volume":"146","author":"Coates","year":"2002","journal-title":"Br. J. Dermatol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1159\/000106579","article-title":"Upper Respiratory Tract Infection in Household Contacts of Acne Patients","volume":"215","author":"Bowe","year":"2007","journal-title":"Dermatology"},{"key":"ref_74","doi-asserted-by":"crossref","unstructured":"Moura, I.B., Grada, A., Spittal, W., Clark, E., Ewin, D., Altringham, J., Fumero, E., Wilcox, M.H., and Buckley, A.M. (2022). Profiling the Effects of Systemic Antibiotics for Acne, Including the Narrow-Spectrum Antibiotic Sarecycline, on the Human Gut Microbiota. Front. Microbiol., 13.","DOI":"10.3389\/fmicb.2022.901911"},{"key":"ref_75","unstructured":"Anderson, M., Panteli, D., and Mossialos, E. (2024). Strengthening the EU Response to Prevention and Control of Antimicrobial Resistance (AMR), Policy Prorities for Effective Implementation, European Observatory on Health Systems and Policies a Partnership Hosted by WHO. Policy Brief."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1016\/j.jaad.2015.09.046","article-title":"The Use of Oral Antibiotics before Isotretinoin Therapy in Patients with Acne","volume":"74","author":"Nagler","year":"2016","journal-title":"J. Am. Acad. Dermatol."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"vi17","DOI":"10.1093\/jac\/dky115","article-title":"Variation in Antibiotic Use among and within Different Settings: A Systematic Review","volume":"73","author":"Zanichelli","year":"2018","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1128\/AAC.46.1.125-131.2002","article-title":"Diversity of Ribosomal Mutations Conferring Resistance to Macrolides, Clindamycin, Streptogramin, and Telithromycin in Streptococcus Pneumoniae","volume":"46","author":"Canu","year":"2002","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"1477","DOI":"10.1038\/ncomms2470","article-title":"Mechanism of Tetracycline Resistance by Ribosomal Protection Protein Tet(O)","volume":"4","author":"Li","year":"2013","journal-title":"Nat. Commun."},{"key":"ref_80","unstructured":"(2024, September 26). Overview|Acne Vulgaris: Management|Guidance|NICE. Available online: https:\/\/www.nice.org.uk\/guidance\/ng198."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1016\/j.clindermatol.2016.10.010","article-title":"Topical Treatments for Acne","volume":"35","author":"Kosmadaki","year":"2017","journal-title":"Clin. Dermatol."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"2650","DOI":"10.1111\/jocd.15923","article-title":"A Systematic Review to Evaluate the Efficacy of Azelaic Acid in the Management of Acne, Rosacea, Melasma and Skin Aging","volume":"22","author":"King","year":"2023","journal-title":"J. Cosmet. Dermatol."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"2555","DOI":"10.1517\/14656560903277228","article-title":"Benzoyl Peroxide: A Review of Its Current Use in the Treatment of Acne Vulgaris","volume":"10","author":"Sagransky","year":"2009","journal-title":"Expert Opin. Pharmacother."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"732","DOI":"10.1016\/j.jid.2018.09.023","article-title":"Skin Ecology during Sebaceous Drought-How Skin Microbes Respond to Isotretinoin","volume":"139","author":"McCoy","year":"2019","journal-title":"J. Investig. Dermatol."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1111\/exd.13397","article-title":"Isotretinoin and Lymecycline Treatments Modify the Skin Microbiota in Acne","volume":"27","author":"Aho","year":"2018","journal-title":"Exp. Dermatol."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"661","DOI":"10.1111\/pde.13261","article-title":"The Preadolescent Acne Microbiome: A Prospective, Randomized, Pilot Study Investigating Characterization and Effects of Acne Therapy","volume":"34","author":"Coughlin","year":"2017","journal-title":"Pediatr. Dermatol."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1007\/s40257-021-00643-2","article-title":"Effects of Topical Retinoids on Acne and Post-Inflammatory Hyperpigmentation in Patients with Skin of Color: A Clinical Review and Implications for Practice","volume":"23","author":"Callender","year":"2022","journal-title":"Am. J. Clin. Dermatol."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"1027","DOI":"10.1080\/14740338.2022.2102605","article-title":"Oral Isotretinoin for Acne: A Complete Overview","volume":"21","author":"Villani","year":"2022","journal-title":"Expert Opin. Drug Saf."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"955","DOI":"10.1111\/exd.14798","article-title":"Treatment Response to Isotretinoin Correlates with Specific Shifts in Cutibacterium acnes Strain Composition within the Follicular Microbiome","volume":"32","author":"Nolan","year":"2023","journal-title":"Exp. Dermatol."},{"key":"ref_90","first-page":"4411","article-title":"Hormonal and Metabolic Aspects of Acne Vulgaris in Women with Polycystic Ovary Syndrome","volume":"22","author":"Franik","year":"2018","journal-title":"Eur. Rev. Med. Pharmacol. Sci."},{"key":"ref_91","doi-asserted-by":"crossref","unstructured":"Borzyszkowska, D., Niedzielska, M., Koz\u0142owski, M., Brodowska, A., Przepiera, A., Malczyk-Matysiak, K., Cymbaluk-P\u0142oska, A., and Sowi\u0144ska-Przepiera, E. (2022). Evaluation of Hormonal Factors in Acne Vulgaris and the Course of Acne Vulgaris Treatment with Contraceptive-Based Therapies in Young Adult Women. Cells, 11.","DOI":"10.3390\/cells11244078"},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1177\/1060028020934892","article-title":"Trifarotene for the Treatment of Facial and Truncal Acne","volume":"55","author":"Bell","year":"2021","journal-title":"Ann. Pharmacother."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"1905","DOI":"10.1007\/s40265-019-01218-6","article-title":"Trifarotene: First Approval","volume":"79","author":"Scott","year":"2019","journal-title":"Drugs"},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"806","DOI":"10.1111\/ijd.17189","article-title":"Importance of Treating Acne Sequelae in Skin of Color: 6-Month Phase IV Study of Trifarotene with an Appropriate Skincare Routine Including UV Protection in Acne-Induced Post-Inflammatory Hyperpigmentation","volume":"63","author":"Alexis","year":"2024","journal-title":"Int. J. Dermatol."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"166","DOI":"10.1111\/jdv.15794","article-title":"Long-Term Safety and Efficacy of Trifarotene 50 \u039cg\/g Cream, a First-in-Class RAR-\u03b3 Selective Topical Retinoid, in Patients with Moderate Facial and Truncal Acne","volume":"34","author":"Fowler","year":"2020","journal-title":"J. Eur. Acad. Dermatol. Venereol."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"e14609","DOI":"10.1111\/dth.14609","article-title":"Efficacy and Safety of Topical Clascoterone Cream for Treatment of Acne Vulgaris: A Systematic Review and Meta-Analysis of Randomized Placebo-Controlled Trials","volume":"34","author":"Alkhodaidi","year":"2021","journal-title":"Dermatol. Ther."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1080\/1744666X.2021.1894131","article-title":"Clascoterone Cream (1%) Topical Androgen Receptor Inhibitor for the Treatment of Acne in Patients 12 Years and Older","volume":"17","author":"Gold","year":"2021","journal-title":"Expert Rev. Clin. Immunol."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"1278","DOI":"10.36849\/JDD.7719","article-title":"Integrated Short-Term and Long-Term Efficacy of Topical Clascoterone Cream 1% in Patients Aged 12 Years or Older with Acne Vulgaris","volume":"23","author":"Eichenfield","year":"2024","journal-title":"J. Drugs Dermatol."},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1007\/s40257-016-0245-x","article-title":"Oral Spironolactone for Acne Vulgaris in Adult Females: A Hybrid Systematic Review","volume":"18","author":"Layton","year":"2017","journal-title":"Am. J. Clin. Dermatol."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"e074349","DOI":"10.1136\/bmj-2022-074349","article-title":"Effectiveness of Spironolactone for Women with Acne Vulgaris (SAFA) in England and Wales: Pragmatic, Multicentre, Phase 3, Double Blind, Randomised Controlled Trial","volume":"381","author":"Santer","year":"2023","journal-title":"BMJ"},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3310\/MYJT6804","article-title":"Clinical and Cost-Effectiveness of Spironolactone in Treating Persistent Facial Acne in Women: SAFA Double-Blinded RCT","volume":"28","author":"Santer","year":"2024","journal-title":"Health Technol. Assess."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"507","DOI":"10.1111\/bjd.21663","article-title":"Efficacy and Safety of N-Acetyl-GED-0507-34-LEVO Gel in Patients with Moderate-to Severe Facial Acne Vulgaris: A Phase IIb Randomized Double-Blind, Vehicle-Controlled Trial","volume":"187","author":"Picardo","year":"2022","journal-title":"Br. J. Dermatol."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"S161","DOI":"10.1016\/j.jval.2023.09.828","article-title":"EE563 Cost-Effectiveness of the PPAR\u03b3 Modulator N-Acetyl-Ged-0507-34-Levo (NAC-GED 5%) Versus Benzoyl Peroxide-Adapalene for Moderate to Severe Acne","volume":"26","author":"Matos","year":"2023","journal-title":"Value Health"},{"key":"ref_104","doi-asserted-by":"crossref","unstructured":"Chilicka, K., Dzie\u0144dziora-Urbi\u0144ska, I., Szygu\u0142a, R., Asanova, B., and Nowicka, D. (2022). Microbiome and Probiotics in Acne Vulgaris\u2014A Narrative Review. Life, 12.","DOI":"10.3390\/life12030422"},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"5092","DOI":"10.1111\/jocd.14971","article-title":"Efficacy of Probiotic-Derived Lotion from Lactobacillus Paracasei MSMC 39-1 in Mild to Moderate Acne Vulgaris, Randomized Controlled Trial","volume":"21","author":"Sathikulpakdee","year":"2022","journal-title":"J. Cosmet. Dermatol."},{"key":"ref_106","doi-asserted-by":"crossref","unstructured":"Podrini, C., Schramm, L., Marianantoni, G., Apolinarska, J., McGuckin, C., Forraz, N., Milet, C., Desroches, A.-L., Payen, P., and D\u2019Aguanno, M. (2023). Topical Administration of Lactiplantibacillus Plantarum (SkinDuoTM) Serum Improves Anti-Acne Properties. Microorganisms, 11.","DOI":"10.3390\/microorganisms11020417"},{"key":"ref_107","doi-asserted-by":"crossref","unstructured":"Kim, M.-J., Kim, K.-P., Choi, E., Yim, J.-H., Choi, C., Yun, H.-S., Ahn, H.-Y., Oh, J.-Y., and Cho, Y. (2021). Effects of Lactobacillus Plantarum CJLP55 on Clinical Improvement, Skin Condition and Urine Bacterial Extracellular Vesicles in Patients with Acne Vulgaris: A Randomized, Double-Blind, Placebo-Controlled Study. Nutrients, 13.","DOI":"10.3390\/nu13041368"},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"adv33206","DOI":"10.2340\/actadv.v104.33206","article-title":"A Randomized Clinical Trial to Evaluate the Efficacy of an Oral Probiotic in Acne Vulgaris","volume":"104","author":"Eguren","year":"2024","journal-title":"Acta Derm. Venereol."},{"key":"ref_109","doi-asserted-by":"crossref","unstructured":"Lolou, V., and Panayiotidis, M.I. (2019). Functional Role of Probiotics and Prebiotics on Skin Health and Disease. Fermentation, 5.","DOI":"10.3390\/fermentation5020041"},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"445","DOI":"10.2147\/CCID.S179627","article-title":"Effects of Oral Supplementation with FOS and GOS Prebiotics in Women with Adult Acne: The \u201cS.O. Sweet\u201d Study: A Proof-of-Concept Pilot Trial","volume":"11","author":"Milani","year":"2018","journal-title":"Clin. Cosmet. Investig. Dermatol."},{"key":"ref_111","doi-asserted-by":"crossref","unstructured":"Dua, K. (2024). Synbiotics for the Prevention and Treatment of Skin Disorders. Synbiotics in Human Health: Biology to Drug Delivery, Springer Nature.","DOI":"10.1007\/978-981-99-5575-6"},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"577","DOI":"10.1007\/s13555-021-00664-z","article-title":"Facial Acne: A Randomized, Double-Blind, Placebo-Controlled Study on the Clinical Efficacy of a Symbiotic Dietary Supplement","volume":"12","author":"Rinaldi","year":"2022","journal-title":"Dermatol. Ther."},{"key":"ref_113","doi-asserted-by":"crossref","first-page":"e13553","DOI":"10.7717\/peerj.13553","article-title":"The Immunomodulatory Potential of Phage Therapy to Treat Acne: A Review on Bacterial Lysis and Immunomodulation","volume":"10","author":"Gonzalez","year":"2022","journal-title":"PeerJ"},{"key":"ref_114","doi-asserted-by":"crossref","unstructured":"Barnard, E., Shi, B., Kang, D., Craft, N., and Li, H. (2016). The Balance of Metagenomic Elements Shapes the Skin Microbiome in Acne and Health. Sci. Rep., 6.","DOI":"10.1038\/srep39491"},{"key":"ref_115","doi-asserted-by":"crossref","first-page":"1005","DOI":"10.1038\/s41467-023-36694-8","article-title":"Topical Phage Therapy in a Mouse Model of Cutibacterium acnes-Induced Acne-like Lesions","volume":"14","author":"Rimon","year":"2023","journal-title":"Nat. Commun."},{"key":"ref_116","doi-asserted-by":"crossref","first-page":"e93","DOI":"10.1002\/ski2.93","article-title":"Development of a Topical Bacteriophage Gel Targeting Cutibacterium acnes for Acne Prone Skin and Results of a Phase 1 Cosmetic Randomized Clinical Trial","volume":"2","author":"Golembo","year":"2022","journal-title":"Ski. Health Dis."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/25\/21\/11422\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T16:19:18Z","timestamp":1760113158000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/25\/21\/11422"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,10,24]]},"references-count":116,"journal-issue":{"issue":"21","published-online":{"date-parts":[[2024,11]]}},"alternative-id":["ijms252111422"],"URL":"https:\/\/doi.org\/10.3390\/ijms252111422","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,10,24]]}}}