Abstract
Skin harbors an important microbial ecosystem — the skin microbiota that is in homeostasis with its host and is beneficial for human health. Cosmetic products have the potential to interfere with this microbial community; therefore their impact should be assessed. The aim of this review is to highlight the importance of skin microbiota in the cosmetic industry. Several studies determined that cosmetic ingredients have the potential to disrupt the skin microbiota equilibrium leading to the development of skin diseases and dysregulation of immune response. These studies led their investigation by using different methodologies and models, concluding that methods must be chosen according to the aim of the study, the skin site to be evaluated, and the target population of the cosmetics. Overall, it is crucial to test the impact of cosmetics in the skin microbiota and to stablish standard procedures, as well as specific criteria that allow to classify a cosmetic product as skin microbiota friendly.
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Kim BS, Gao G, Kim JY, Cho DW (2019) 3D cell printing of perfusable vascularized human skin equivalent composed of epidermis, dermis, and hypodermis for better structural recapitulation of native skin. Adv Healthc Mater 8:1–11. https://doi.org/10.1002/adhm.201801019
Byrd AL, Belkaid Y, Segre JA (2018) The human skin microbiome. Nat Rev Microbiol 16:143–155. https://doi.org/10.1038/nrmicro.2017.157
Harvey CJ, LeBouf RF, Stefaniak AB (2010) Formulation and stability of a novel artificial human sweat under conditions of storage and use. Toxicol Vitr 24:1790–1796. https://doi.org/10.1016/j.tiv.2010.06.016
Brohem CA, Da Silva Cardeal LB, Tiago M et al (2011) Artificial skin in perspective: concepts and applications. Pigment Cell Melanoma Res 24:35–50. https://doi.org/10.1111/j.1755-148X.2010.00786.x
Cundell AM (2018) Microbial ecology of the human skin. Microb Ecol 76:113–120. https://doi.org/10.1007/s00248-016-0789-6
Manus MB, Kuthyar S, Perroni-Marañón AG et al (2021) Comparing different sample collection and storage methods for field-based skin microbiome research Am J Hum Biol 1–14. https://doi.org/10.1002/ajhb.23584
Lee B, Kim, (2019) Potential role of the microbiome in acne: a comprehensive review. J Clin Med 8:987. https://doi.org/10.3390/jcm8070987
Fricker AM, Podlesny D, Fricke WF (2019) What is new and relevant for sequencing-based microbiome research? A mini-review. J Adv Res 19:105–112. https://doi.org/10.1016/j.jare.2019.03.006
Naik S, Bouladoux N, Wilhelm C, et al (2012) Compartmentalized control of skin immunity by resident commensals. Science (80- ). https://doi.org/10.1126/science.1225152
Dreno B, Martin R, Moyal D et al (2017) Skin microbiome and acne vulgaris : Staphylococcus, a new actor in acne. Exp Dermatol 26:798–803. https://doi.org/10.1111/exd.13296
Stehlikova Z, Kostovcik M, Kostovcikova K et al (2019) Dysbiosis of skin microbiota in psoriatic patients: co-occurrence of Fungal and Bacterial Communities. Front Microbiol 10:1–13. https://doi.org/10.3389/fmicb.2019.00438
Nakatsuji T, Chen TH, Narala S et al (2017) Antimicrobials from human skin commensal bacteria protect against Staphylococcus aureus and are deficient in atopic dermatitis. Sci Transl Med 9:1–12. https://doi.org/10.1126/scitranslmed.aah4680
Belkaid Y, Segre JA (2014) Dialogue between skin microbiota and immunity. Science (80) 346:954–959. https://doi.org/10.1126/science.1260144
Chen YE, Fischbach MA, Belkaid Y (2018) Skin microbiota–host interactions. Nature 553:427–436. https://doi.org/10.1038/nature25177
Schommer NN, Gallo RL (2013) Structure and function of the human skin microbiome. Trends Microbiol 21:660–668. https://doi.org/10.1016/j.tim.2013.10.001
Bay L, Barnes CJ, Fritz BG et al (2020) Universal dermal microbiome in human skin. MBio 11:1–13. https://doi.org/10.1128/mBio.02945-19
Ganju P, Nagpal S, Mohammed MH et al (2016) Microbial community profiling shows dysbiosis in the lesional skin of Vitiligo subjects. Sci Rep 6:1–10. https://doi.org/10.1038/srep18761
Gilbert JA, Blaser MJ, Caporaso JG et al (2018) Current understanding of the human microbiome. Nat Med 24:392–400. https://doi.org/10.1038/nm.4517
Wallen-Russell C, Wallen-Russell S (2017) Meta analysis of skin microbiome: new link between skin microbiota diversity and skin health with proposal to use this as a future mechanism to determine whether cosmetic products damage the skin. Cosmetics 4:1–19. https://doi.org/10.3390/cosmetics4020014
Grice EA, Kong HH, Renaud G et al (2008) A diversity profile of the human skin microbiota. Genome Res 18:1043–1050. https://doi.org/10.1101/gr.075549.107
Kong HH, Segre JA (2012) Skin microbiome: looking back to move forward. J Invest Dermatol 132:933–939. https://doi.org/10.1038/jid.2011.417
Olesen SW, Alm EJ (2016) Dysbiosis is not an answer. Nat Microbiol 1:16228. https://doi.org/10.1038/nmicrobiol.2016.228
Yamazaki Y, Nakamura Y, Núñez G (2017) Role of the microbiota in skin immunity and atopic dermatitis. Allergol Int 66:539–544. https://doi.org/10.1016/j.alit.2017.08.004
Filaire E, Vialleix C, Cadoret J-P et al (2019) Characterization of reactive and sensitive skin microbiota: effect of Halymenia durvillei (HD) extract treatment. Cosmetics 6:69. https://doi.org/10.3390/cosmetics6040069
O’Sullivan JN, Rea MC, O’Connor PM et al (2019) Human skin microbiota is a rich source of bacteriocin-producing staphylococci that kill human pathogens. FEMS Microbiol Ecol. https://doi.org/10.1093/femsec/fiy241
Grice EA, Dawson TL (2017) Host–microbe interactions: Malassezia and human skin. Curr Opin Microbiol 40:81–87. https://doi.org/10.1016/j.mib.2017.10.024
Findley K, Oh J, Yang J et al (2013) Topographic diversity of fungal and bacterial communities in human skin. Nature 498:367–370. https://doi.org/10.1038/nature12171
Dréno B, Araviiskaia E, Berardesca E et al (2016) Microbiome in healthy skin, update for dermatologists. J Eur Acad Dermatology Venereol 30:2038–2047. https://doi.org/10.1111/jdv.13965
Foulongne V, Sauvage V, Hebert C et al (2012) Human skin microbiota: high diversity of DNA viruses identified on the human skin by high throughput sequencing PLoS ONE 7. https://doi.org/10.1371/journal.pone.0038499
Cosseau C, Romano-Bertrand S, Duplan H et al (2016) Proteobacteria from the human skin microbiota: species-level diversity and hypotheses. One Heal 2:33–41. https://doi.org/10.1016/j.onehlt.2016.02.002
Kong HH (2011) Skin microbiome: genomics-based insights into the diversity and role of skin microbes. Trends Mol Med 17:320–328. https://doi.org/10.1016/j.molmed.2011.01.013
Christie S, Lubis SR, Yosi A, Wahyuni DD (2020) Differences of skin normal microbiota in adult men and elderly Int J Sci Res Publ 10 p9785 10.01.2020.p9785
Fournière M, Latire T, Souak D et al (2020) Staphylococcus epidermidis and Cutibacterium acnes: two major sentinels of skin microbiota and the influence of cosmetics. Microorganisms 8:1–31. https://doi.org/10.3390/microorganisms8111752
Gimblet C, Meisel JS, Loesche MA et al (2017) Cutaneous leishmaniasis induces a transmissible dysbiotic skin microbiota that promotes skin inflammation. Cell Host Microbe 22:13-24.e4. https://doi.org/10.1016/j.chom.2017.06.006
Abdallah F, Mijouin L, Pichon C (2017) Skin immune landscape: inside and outside the organism Mediators Inflamm 2017. https://doi.org/10.1155/2017/5095293
Zheng D, Liwinski T, Elinav E (2020) Interaction between microbiota and immunity in health and disease. Cell Res 30:492–506. https://doi.org/10.1038/s41422-020-0332-7
Bouslimani A, Da Silva R, Kosciolek T et al (2019) The impact of skin care products on skin chemistry and microbiome dynamics. BMC Biol 17:1–20. https://doi.org/10.1186/s12915-019-0660-6
Mukherjee PK, Maity N, Nema NK, Sarkar BK (2011) Bioactive compounds from natural resources against skin aging. Phytomedicine 19:64–73. https://doi.org/10.1016/j.phymed.2011.10.003
Kumar S (2005) Exploratory analysis of global cosmetic industry: major players, technology and market trends. Technovation 25:1263–1272. https://doi.org/10.1016/j.technovation.2004.07.003
Chouhan N, Vig H, Deshmukh R (2021) Cosmetics market by category (skin and sun care products, hair care products, deodorants & fragrances, and makeup & color cosmetics), gender (men, women, and unisex), and distribution channel (hypermarkets/supermarkets, specialty stores, pharmacies, onlin. https://www.alliedmarketresearch.com/cosmetics-market. Accessed 6 Feb 2021
Wallen-Russell C (2019) The role of every-day cosmetics in altering the skin microbiome: A study using biodiversity Cosmetics https://doi.org/10.3390/cosmetics6010020
Collado MC, Vinderola G, Salminen S (2019) Postbiotics: facts and open questions. A position paper on the need for a consensus definition. Benef Microbes 10:711–719. https://doi.org/10.3920/BM2019.0015
Meisel JS, Hannigan GD, Tyldsley AS et al (2016) Skin microbiome surveys are strongly influenced by experimental design. J Invest Dermatol 136:947–956. https://doi.org/10.1016/j.jid.2016.01.016
Fraher MH, O’Toole PW, Quigley EMM (2012) Techniques used to characterize the gut microbiota: a guide for the clinician. Nat Rev Gastroenterol Hepatol 9:312–322. https://doi.org/10.1038/nrgastro.2012.44
Grogan MD, Bartow-McKenney C, Flowers L et al (2019) Research techniques made simple: profiling the skin microbiota. J Invest Dermatol 139:747-752.e1. https://doi.org/10.1016/j.jid.2019.01.024
Ogai K, Nagase S, Mukai K et al (2018) A comparison of techniques for collecting skin microbiome samples: swabbing versus tape-stripping. Front Microbiol 9:1–10. https://doi.org/10.3389/fmicb.2018.02362
Prast-Nielsen S, Tobin AM, Adamzik K et al (2019) Investigation of the skin microbiome: swabs vs. biopsies. Br J Dermatol 181:572–579. https://doi.org/10.1111/bjd.17691
Schneider AM, Nelson AM (2019) Skin microbiota: friend or foe in pediatric skin health and skin disease. Pediatr Dermatol 36:815–822. https://doi.org/10.1111/pde.13955
Kong HH, Segre JA (2017) The molecular revolution in cutaneous biology: investigating the skin microbiome. J Invest Dermatol 137:e119–e122. https://doi.org/10.1016/j.jid.2016.07.045
Bjerre RD, Hugerth LW, Boulund F et al (2019) Effects of sampling strategy and DNA extraction on human skin microbiome investigations. Sci Rep 9:1–11. https://doi.org/10.1038/s41598-019-53599-z
Kong HH, Andersson B, Clavel T et al (2017) Performing skin microbiome research: a method to the madness. J Invest Dermatol 137:561–568. https://doi.org/10.1016/j.jid.2016.10.033
Myles IA, Williams KW, Reckhow JD et al (2016) Transplantation of human skin microbiota in models of atopic dermatitis. JCI Insight 1:1–10. https://doi.org/10.1172/jci.insight.86955
Gaitanis G, Tsiouri G, Spyridonos P et al (2019) Variation of cultured skin microbiota in mothers and their infants during the first year postpartum. Pediatr Dermatol 36:460–465. https://doi.org/10.1111/pde.13829
Hou TY, Chiang-Ni C, Teng SH (2019) Current status of MALDI-TOF mass spectrometry in clinical microbiology. J Food Drug Anal 27:404–414. https://doi.org/10.1016/j.jfda.2019.01.001
Kostrzewa M, Nagy E, Schröttner P, Pranada AB (2019) How MALDI-TOF mass spectrometry can aid the diagnosis of hard-to-identify pathogenic bacteria–the rare and the unknown. Expert Rev Mol Diagn 19:667–682. https://doi.org/10.1080/14737159.2019.1643238
Myles IA, Reckhow JD, Williams KW et al (2016) A method for culturing gram-negative skin microbiota. BMC Microbiol 16:1–6. https://doi.org/10.1186/s12866-016-0684-9
Cassir N, Papazian L, Fournier PE et al (2015) Insights into bacterial colonization of intensive care patients’ skin: the effect of chlorhexidine daily bathing. Eur J Clin Microbiol Infect Dis 34:999–1004. https://doi.org/10.1007/s10096-015-2316-y
Ramasamy S, Barnard E, Dawson TL, Li H (2019) The role of the skin microbiota in acne pathophysiology. Br J Dermatol 181:691–699. https://doi.org/10.1111/bjd.18230
Arnold JW, Roach J, Azcarate-Peril MA (2016) Emerging technologies for gut microbiome research. Trends Microbiol 24:887–901. https://doi.org/10.1016/j.tim.2016.06.008
The human microbiome project consortium (2012) Structure, function and diversity of the healthy human microbiome. Nature 486:207–214. https://doi.org/10.1038/nature11234
Tsuji R, Yazawa K, Kokubo T et al (2021) The effects of dietary supplementation of Lactococcus lactis strain plasma on skin microbiome and skin conditions in healthy subjects—a randomized, double-blind, placebo-controlled trial. Microorganisms 9:563. https://doi.org/10.3390/microorganisms9030563
Tanaka A, Cho O, Saito C et al (2016) Comprehensive pyrosequencing analysis of the bacterial microbiota of the skin of patients with seborrheic dermatitis. Microbiol Immunol 60:521–526. https://doi.org/10.1111/1348-0421.12398
Kralik P, Ricchi M (2017) A basic guide to real time PCR in microbial diagnostics: definitions, parameters, and everything. Front Microbiol 8:1–9. https://doi.org/10.3389/fmicb.2017.00108
Arastehfar A, Boekhout T, Butler G et al (2019) Recent trends in molecular diagnostics of yeast infections: from PCR to NGS. FEMS Microbiol Rev 43:517–547. https://doi.org/10.1093/femsre/fuz015
Bonk F, Popp D, Harms H, Centler F (2018) PCR-based quantification of taxa-specific abundances in microbial communities: quantifying and avoiding common pitfalls. J Microbiol Methods 153:139–147. https://doi.org/10.1016/j.mimet.2018.09.015
Slatko BE, Gardner AF, Ausubel FM (2018) Overview of next-generation sequencing technologies CurrProtoc Mol Biol 122. https://doi.org/10.1002/cpmb.59
Raimondi S, Amaretti A, Gozzoli C et al (2019) Longitudinal survey of fungi in the human gut: ITS profiling, phenotyping, and colonization. Front Microbiol 10:1–12. https://doi.org/10.3389/fmicb.2019.01575
Mukherjee S, Mitra R, Maitra A et al (2016) Sebum and hydration levels in specific regions of human face significantly predict the nature and diversity of facial skin microbiome. Sci Rep 6:36062. https://doi.org/10.1038/srep36062
Kuczynski J, Lauber CL, Walters WA et al (2012) Experimental and analytical tools for studying the human microbiome. Nat Rev Genet 13:47–58. https://doi.org/10.1038/nrg3129
Knight R, Vrbanac A, Taylor BC et al (2018) Best practices for analysing microbiomes. Nat Rev Microbiol 16:410–422. https://doi.org/10.1038/s41579-018-0029-9
Oh J, Byrd AL, Deming C et al (2014) Biogeography and individuality shape function in the human skin metagenome. Nature 514:59–64. https://doi.org/10.1038/nature13786
Byrd AL, Deming C, Cassidy SKB et al (2017) Staphylococcus aureus and Staphylococcus epidermidis strain diversity underlying pediatric atopic dermatitis SciTransl Med 9. https://doi.org/10.1126/scitranslmed.aal4651
Quince C, Walker AW, Simpson JT et al (2017) Shotgun metagenomics, from sampling to analysis. Nat Biotechnol 35:833–844. https://doi.org/10.1038/nbt.3935
Van Der Krieken DA, Ederveen THA, Van Hijum SAFT et al (2016) An in vitro model for bacterial growth on human stratum corneum. Acta Derm Venereol 96:873–879. https://doi.org/10.2340/00015555-2401
Rademacher F, Simanski M, Gläser R, Harder J (2018) Skin microbiota and human 3D skin models. Exp Dermatol 27:489–494. https://doi.org/10.1111/exd.13517
Cadau S (2017) Studying microbiote competition and skin interaction using organotypic 3D skin models. Adv Tissue Eng Regen Med Open Access 2:3–5. https://doi.org/10.15406/atroa.2017.02.00041
Eberlin S, da Silva MS, Facchini G et al (2020) The ex vivo skin model as an alternative tool for the efficacy and safety evaluation of topical products. Altern Lab Anim 48:10–22. https://doi.org/10.1177/0261192920914193
Strbo N, Pastar I, Romero L et al (2019) Single cell analyses reveal specific distribution of anti-bacterial molecule Perforin-2 in human skin and its modulation by wounding and Staphylococcus aureus infection. Exp Dermatol 28:225–232. https://doi.org/10.1111/exd.13870
Nishioka H, Nagahama A, Inoue Y, Hagi A (2018) Evaluation of fast-acting bactericidal activity and substantivity of an antiseptic agent, olanexidine gluconate, using an ex vivo skin model. J Med Microbiol 67:1796–1803. https://doi.org/10.1099/jmm.0.000870
Mouritzen MV, Petkovic M, Qvist K et al (2021) Improved diabetic wound healing by LFcinB is associated with relevant changes in the skin immune response and microbiota. Mol Ther - Methods Clin Dev 20:726–739. https://doi.org/10.1016/j.omtm.2021.02.008
Ciardiello T, Pinto D, Marotta L et al (2020) Effects of fermented oils on alpha-biodiversity and relative abundance of cheek resident skin microbiota Cosmetics 7. https://doi.org/10.3390/COSMETICS7020034
Hong KB, Hong YH, Jung EY et al (2020) Changes in the diversity of human skin microbiota to cosmetic serum containing prebiotics: results from a randomized controlled trial. J Pers Med 10:1–14. https://doi.org/10.3390/jpm10030091
Ring HC, Bay L, Kallenbach K et al (2017) Normal skin microbiota is altered in pre-clinical hidradenitis suppurativa. Acta Derm Venereol 97:208–213. https://doi.org/10.2340/00015555-2503
Marrs T, Flohr C (2016) The role of skin and gut microbiota in the development of atopic eczema. Br J Dermatol 175:13–18. https://doi.org/10.1111/bjd.14907
Lewis DJ, Chan WH, Hinojosa T et al (2019) Mechanisms of microbial pathogenesis and the role of the skin microbiome in psoriasis: a review. Clin Dermatol 37:160–166. https://doi.org/10.1016/j.clindermatol.2019.01.011
Griffiths CEM, Armstrong AW, Gudjonsson JE, Barker JNWN (2021) Psoriasis Lancet 397:1301–1315. https://doi.org/10.1016/S0140-6736(20)32549-6
Two AM, Nakatsuji T, Kotol PF et al (2016) The cutaneous microbiome and aspects of skin antimicrobial defense system resist acute treatment with topical skin cleansers J Invest Dermatol 136 1950 1954 https://doi.org/10.1016/j.jid.2016.06.612
Funding
This work was supported by Amyris Bio Products Portugal Unipessoal Lda and Escola Superior de Biotecnologia – Universidade Católica Portuguesa through Alchemy project- Capturing high value from industrial fermentation bio products (POCI-01 − 0247-FEDER-027578). The authors would also like to thank the scientific collaboration under the FCT project UID/Multi/50016/2019.
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Carvalho, M.J., S. Oliveira, A.L., Santos Pedrosa, S. et al. Skin Microbiota and the Cosmetic Industry. Microb Ecol 86, 86–96 (2023). https://doi.org/10.1007/s00248-022-02070-0
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DOI: https://doi.org/10.1007/s00248-022-02070-0