Methods for Correcting the Skin Microbiome and Preventing Bacterial Diseases Using Cosmetic Products Based on Probiotics (Systematic Scoping Review)

Introduction. Solving the problem of maintaining balance, ensuring the protection and restoration of the skin microbiome is an urgent need due to the fact that diseases of the skin and subcutaneous tissue occupy the 4th place in primary morbidity among all diseases in the Russian Federation. An analysis of Russian and foreign publications devoted to the use of probiotics for the prevention and treatment of various skin diseases has revealed a problematic field of research – an insufficient degree of knowledge and systematization of information related to the use of probiotics in the composition of therapeutic and preventive cosmetics. 

Purpose. The authors set a goal to critically evaluate the prospects of using cosmetics based on probiotic microorganisms in bacterial skin diseases. To write this review, we used peer-reviewed articles, reviews and books, patents published between 2010 and 2022, in Russian and English. The studied collection of sources includes 126 publications published in domestic and foreign databases such as Scopus, Web of Science, SciHub, PubMed, Google scholar, eLlibrary and Cyberlinica. During the initial analysis of publications (annotation analysis), 76 sources were selected for relevance to the topic, which were further investigated in detail. 

Results. The analysis of the sources allowed us to study and systematize information about the nature and causes of atopic dermatitis, seborrheic dermatitis, acne and rosacea, to come to the following conclusions: mainly foreign cosmetics using metabolites or lysates of probiotic microorganisms are on the market, which does not allow achieving the desired sustainable effect. In this industry, import-substituting technologies for the production of active components of cosmetics are required. The use of probiotic microorganisms as part of local cosmetic therapy is a promising direction, as the positive effect of S.thermophilus, V.filiformis, E.faecalis, L.plantarum, B.longum, S.hominis and L.johnsonii has been proven. A correlation has been shown between the improvement of the course of diseases from the dose and the regimens of probiotic drugs. 

Conclusion. Further research areas include screening of probiotic microorganisms that are most suitable for the treatment and prevention of the above-described diseases, developing the basis of a cosmetic product that allows you to keep probiotic microorganisms in a viable state, developing technological solutions for the production and storage of innovative cosmetics.

1. Human Microbiome Project Consortium. (2012). Structure, function and diversity of the healthy human microbiome. Nature, 486(7402), 207-214.

2. Doré, J., Blottière, H. (2015) The influence of diet on the gut microbiota and its consequences for health. Curr Opin Biotechnol., (32),195–9.

3. Oh, J. (2014) Biogeography and individuality shape function in the human skin metagenome. Nature, (514), 59–64.

4. Oh, J., Byrd, A.L., Park, M., Kong, H.H., Segre, J.A. (2016) Temporal stability of the human skin microbiome. Cell, 165(4),66.

5. Flores, G.E. (2014) Temporal variability is a personalized feature of the human microbiome. Genome Biol, (15), 541.

6. Perez Perez, G.I. (2016) Body site is a more determinant factor than human population diversity in the healthy skin microbiome. PloS One, 11(4).

7. Troccaz, M. (2015) Mapping axillary microbiota responsible for body odours using a culture-independent approach. Microbiome, 3(1).

8. Grice, E.A., Segre, J.A. (2011) The skin microbiome. Nat Rev Microbiol., 9(4), 244–253.

9. Kong, H.H. (2012) Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. Genome Res.,22(5).

10. Lomholt, H.B. (2010) Population genetic analysis of Propionibacterium acnes identifies a subpopulation and epidemic clones associated with acne. PloS One, 5(8).

11. Kobayashi, T. (2015) Dysbiosis and Staphyloccus aureus colonization drives inflammation in atopic dermatitis. Immunity, 42 (4), 756–766.

12. Chng, K.R. (2016) Whole metagenome profiling reveals skin microbiome-dependent susceptibility to atopic dermatitis flare. Nat Microbiol., 1(9).

13. Myles, I.A. (2016) Transplantation of human skin microbiota in models of atopic dermatitis. JCI Insight, 1(10), 2016.

14. Alekseyenko, A.V. (2013) Community differentiation of the cutaneous microbiota in psoriasis. Microbiome 1(31).

15. Wang, L. (2015) Characterization of the major bacterial-fungal populations colonizing dandruff scalps in Shanghai, China, shows microbial disequilibrium. Exp Dermatol., 24(5) ,398–400.

16. Clavaud, C. (2013) Dandruff is associated with disequilibrium in the proportion of the major bacterial and fungal populations colonizing the scalp. PloS One, 8(3).

17. Fitz-Gibbon, S. (2013) Propionibacterium acnes strain populations in the human skin microbiome associated with acne. J Invest Dermatol., 133(9).

18. Lomholt, H. B., Scholz, C. F. P., Brüggemann, H., Tettelin, H. & Kilian, M. A. (2017) Comparative study of Cutibacterium (Propionibacterium) acnes clones from acne patients and healthy controls. Anaerobe 47, 57–63.

19. Barnard, E, Shi B, Kang D, Craft N, Li H. (2016) The balance of metagenomic elements shapes the skin microbiome in acne and health. Sci Rep., 6 (39491).

20. Allhorn, M, Arve S, Brüggemann H, Lood R. (2016) A novel enzyme with antioxidant capacity produced by the ubiquitous skin colonizer Propionibacterium acnes. Nat Publ Gr., 6 (36412).

21. Nood, E. (2013) Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med.,368 (5), 407–415.

22. Olle B. (2013) Medicines from microbiota. Nat Biotechnol., 31 (4), 309–315.

23. Belkaid, Y, Segre J.A. (2014) Dialogue between skin microbiota and immunity. Science, 346(6212).

24. McDowell, A. (2012) An expanded multilocus sequence typing scheme for Propionibacterium acnes: investigation of ‘pathogenic’, ‘commensal’ and antibiotic resistant strains. PloS One, 7(7).

25. Grice, E.A., Kong, H.H., Renaud, G., Young, A.C., Bouffard, G.G., Blakesley, R.W., Wolfsberg, T.G., Turner, M.L., Segre, J.A. (2008) A diversity profile of the human skin microbiota. Genome Res 18, 1043–1050.

26. Ngo, M.A., Sinitsyna, N.N., Qin, Q., Rice, R.H. (2007) Oxygen-Dependent Differentiation of Human Keratinocytes. J. Investig. Dermatol 127, 354–361.

27. Grice, E.A., Segre, J.A. (2011) The skin microbiome. Nat. Rev. Microbiol., 9, 244–253.

28. Kong, H.H., Segre, J.A. (2012) Skin microbiome: Looking back to move forward. J. Investig. Dermatol, 132, 933–939.

29. Capone, K.A., Dowd, S.E., Stamatas, G.N., Nikolovski, J. (2012) Diversity of the human skin microbiome early in life. J. Investig. Dermatol. 131, 2026–2032

30. Grice, E.A., Kong, H.H., Conlan, S., Deming, C.B., Davis, J., Young, A.C., Bouffard, G.G., Blakesley, R.W., Murray, P.R., Green, E.D. (2009) Topographical and temporal diversity of the human skin microbiome. Science, 324, 1190–1192.

31. Racine, P., Janvier, X., Clabaut, M., Catovic, C., Souak, D., Boukerb, A.M., Groboillot, A., Konto-Ghiorghi, Y., Duclairoir-Poc, C., Lesouhaitier, O., (2020) Dialog between skin and its microbiota: Emergence of “Cutaneous Bacterial Endocrinology”. Exp. Dermatol. 29, 790–800.

32. Takahashi, T., Gallo, R.L. (2017) The critical and multifunctional roles of antimicrobial peptides in dermatology. Dermatol. Clin., 35, 39–50.

33. Sanford, J.A., Gallo, R.L.n(2013) Functions of the skin microbiota in health and disease. Semin. Immunol., 25, 370–377.

34. Musthaq, S., Mazuy, A., Jakus, J. (2018) The microbiome in dermatology. Clin. Dermatol., 36, 390–398.

35. Paller, A.S., Kong, H.H., Seed, P., Naik, S., Scharschmidt, T.C., Gallo, R.L., Luger, T., Irvine, A.D. (2019) The microbiome in patients with atopic dermatitis. J. Allergy Clin. Immunol., 143, 26–35.

36. Nakatsuji, T., Gallo, R.L. (2019) The role of the skin microbiome in atopic dermatitis. Ann. Allergy Asthma Immunol., 122, 263–269.

37. Williams, M.R., Nakatsuji, T., Gallo, R.L. (2017) Staphylococcus aureus: Master Manipulator of the Skin. Cell Host Microbe, 22, 579–581.

38. Schommer, N.N., Gallo, R.L. (2013) Structure and function of the human skin microbiome. Trends Microbiol., 21, 660–668.

39. Burns, E.M., Ahmed, H., Isedeh, P.N., Kohli, I., Van Der Pol, W., Shaheen, A., Muzaffar, A.F., Al-Sadek, C., Foy, T.M., Abdelgawwad, M.S. (2019) Ultraviolet radiation, both UVA and UVB, influences the composition of the skin microbiome. Exp. Dermatol., 28, 136–141.

40. Zhai, W., Huang, Y., Zhang, X., Fei, W., Chang, Y., Cheng, S., Zhou, Y., Gao, J., Tang, X., Zhang, X. (2018) Profile of the skin microbiota in a healthy Chinese population. J. Dermatol., 45, 1289–1300.

41. Fournière, M., Latire, T., Souak, D., Feuilloley, M., Bedoux, G. (2020) Staphylococcus epidermidis and Cutibacterium acnes: Two major sentinels of skin microbiota and the influence of cosmetics. Microorganisms, 8, 1752.

42. Lawrence, K.P., Long, P.F., Young, A.R. (2019) Mycosporine-like amino acids for skin photoprotection. Curr. Med. Chem., 25, 5512–5527.

43. Byrd, A.L., Belkaid, Y., Segre, J.A. (2018) The human skin microbiome. Nat. Rev. Microbiol, 16, 143–155.

44. Percival, S.L., Emanuel, C., Cutting, K.F., Williams, D.W. (2012) Microbiology of the skin and the role of biofilms in infection. Int. Wound J., 9, 14–32.

45. Feuilloley, M.G.J. (2018) Antidromic neurogenic activity and cutaneous bacterial flora. Semin. Immunopathol, 40, 281–289.

46. Lange-Asschenfeldt, B., Marenbach, D., Lang, C., Patzelt, A., Ulrich, M., Maltusch, A., Terhorst, D., Stockfleth, E., Sterry, W., Lademann, J. (2011) Distribution of bacteria in the epidermal layers and hair follicles of the human skin. Ski. Pharmacol. Physiol., 24, 305–311.

47. Findley, K., Oh, J., Yang, J., Conlan, S., Deming, C., Meyer, J.A., Schoenfeld, D., Nomicos, E., Park, M., Kong, H.H. (2013) Topographic diversity of fungal and bacterial communities in human skin. Nature, 498, 367–370.

48. Probst, A.J., Auerbach, A.K., Moissl-Eichinger, C. (2013) Archaea on human skin. PLoS One 8.

49. Moissl-Eichinger, C., Pausan, M., Taffner, J., Berg, G., Bang, C., Schmitz, R.A. (2018) Archaea are interactive components of complex microbiomes. Trends Microbiol, 26, 70–85.

50. Hannigan, G.D., Meisel, J.S., Tyldsley, A.S., Zheng, Q., Hodkinson, B.P., SanMiguel, A.J., Minot, S., Bushman, F.D., Grice, E.A. (2015) The human skin double-stranded DNA virome: Topographical and temporal diversity, genetic enrichment, and dynamic associations with the host microbiome. mBio, 6, e01578-15.

51. Foulongne, V., Sauvage, V., Hebert, C., Dereure, O., Cheval, J., Gouilh, M.A., Pariente, K., Segondy, M., Burguière, A. (2012) Human skin microbiota: High diversity of DNA viruses identified on the human skin by high throughput sequencing. PLoS One, 7, e38499.

52. Wylie, K.M., Mihindukulasuriya, K.A., Zhou, Y., Sodergren, E., Storch, A.G., Weinstock, G.M. (2014) Metagenomic analysis of double-stranded DNA viruses in healthy adults. BMC Biol., 12, 71.

53. Mayba, J. N., Gooderham, M. J., Cutan, J. (2017) Review of Atopic Dermatitis and Topical Therapies. Med. Surg.,21, 227.

54. Loden, M, Clin, Am. J. (2003) Role of Topical Emollients and Moisturizers in the Treatment of Dry Skin Barrier Disorders. Dermatol.,4, 771.

55. Eyerich, K., Novak, N. (2013) Clinical Characteristics, Treatments, and Prognosis of Atopic Eczema in the Elderly. Allergy 68, 974.

56. Mallbris, L. Carlén, T. Wei, J. Heilborn, M. F. Nilsson, F. Granath, M. (2010) Vitamin D, the Cutaneous Barrier, Antimicrobial Peptides and Allergies: Is There a Link? Dermatol., 19, 442.

57. Ong, P. Y., Ohtake, T., Brandt, C., Strickland, I., Boguniewicz, M., Ganz, T., R. L. Gallo, D. Y. Leung, N. Engl. J. (2002) Antimicrobial Peptides, Skin Infections and Atopic Dermatitis. Med, 347, 1151.

58. Hata, P. Kotol, M. Boguniewicz, P. Taylor, A. Paik, M. Jackson, M. Nguyen, F. Kabigting, J. Miller, M. Gerber, D. Zaccaro, B. Armstrong, R. Dorschner, D. Y. Leung, R. L. Gallo, Br. J. (2010) Antimicrobials from human skin commensal bacteria protect against Staphylococcus aureus and are deficient in atopic dermatitis. Dermatol., 163, 659.

59. Howell, M.D., Boguniewicz, M., Pastore, S., Novak, N., Bieber,T. (2006) Skin Barrier Defects in Atopic Dermatitis. Clin. Immunol.,121, 332.

60. Ballardini, N., Johansson, C., Lilja, G., Lindh, M., Linde, Y., Scheynius, A., Agerberth, B. (2009) Epidermal Permeability Barrier Defects and Barrier Repair Therapy in Atopic Dermatitis. Dermatol., 161, 40.

61. Clausen, M. L., Slotved, H. C., Krogfelt, K. A. (2018) Advancement through epidermis using tape stripping technique and Reflectance Confocal Microscopy. Sci. Rep., 8, 1666.

62. J. Harder, S. Dressel, M. Wittersheim, J. Cordes, U. Meyer‐Hoffert, U. Mrowietz, R. Fölster‐Holst, E. Proksch, J. M. Schröder, T. Schwarz, R. Gläser, J. Invest. (2010) Expression of antimicrobial peptides in atopic dermatitis and possible immunoregulatory functions. Dermatol., 130, 1355.

63. H. H. Kong, J. Oh, C. Deming, S. Conlan, E.A. Grice, M. A. Beatson, E. Nomicos, E. C. Polley, H. D. Komarow (2012) Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. Genome Res., 22, 850.

64. Leyden, J. J., Marples, J. J., Kligman, A. M. (1974) Staphylococcus aureus in the lesions of atopic dermatitis. Dermatol., 90, 525.

65. Allakhverdi, Z., Comeau, M. R., Jessup, H. K., (2007) Thymic stromal lymphopoietin is released by human epithelial cells in response to microbes, trauma, or inflammation and potently activates mast cells. J. Exp. Med., 204, 253.

66. Sieprawska‐Lupa, M. (2004). he Oligo-Acyl Lysyl Antimicrobial Peptide C12K-2β12 Exhibits a Dual Mechanism of Action and Demonstrates Strong In Vivo Efficacy against Helicobacter pylori. Antimicrob. Agents Chemother., 48, 4673.

67. Datta, A., Alexander, R., Sulikowski, M.G., Nicholson, A.G. (2013) Evidence for a functional thymic stromal lymphopoietin signaling axis in fibrotic lung disease. J Immunol.,191(9).

68. Miller, L.S., Cho, J.S. (2011) Immunity against Staphylococcus aureus cutaneous infections. Nat Rev Immunol., 11(8), 505-518.

69. Nakatsuji, T. H. Chen, A. M. Two, K. A. Chun, S. Narala, R. S. Geha, T. R. Hata, R. L. Gallo, (2016) Staphylococcus aureus Exploits Epidermal Barrier Defects in Atopic Dermatitis to Trigger Cytokine Expression. J. Invest. Dermatol., 136(11), 2192.

70. Fitz‐Gibbon, S. Tomida, B. H. Chiu, L. Nguyen, C. Du, M. Liu, D. Elashoff, M. C. Erfe, A. Loncaric, J. Kim, R. L. Modlin, J. F. Miller, E. Sodergren, N. Craft, G. M. Weinstock, H. Li, (2013) Propionibacterium acnes Strain Populations in the Human Skin Microbiome Associated with Acne J. Invest. Dermatol., 133, 2152.

71. Jung, G.W., Tse J.E., Guiha I., Rao J. (2013) Prospective, randomized, open-label trial comparing the safety, efficacy, and tolerability of an acne treatment regimen with and without a probiotic supplement and minocy-cline in subjects with mild to moderate acne. J Cutan Med Surg, 17, 114-122

72. Fox, L, Csongradi C, Aucamp M, du Plessis J, Gerber M. (2016) Treatment Modalities for Acne. Molecules, 21(8),1063.

73. Dréno, B. (2017) What is new in the pathophysiology of acne, an overview. J. Eur. Acad. Dermatol. Venereol., 31, 8.

74. Rendon, A.; Schäkel, K. (2019) Psoriasis Pathogenesis and Treatment. Int. J. Mol. Sci., 20, 1475.

75. Feingold, K. R., Grunfeld, S.(2012) Lipids: a key player in the battle between the host and microorganisms. J. Lipid Res., 53, 1427.

76. Weyrich, S. Dixit, A. G. Farrer, A. J. Cooper, A. J. Cooper, Australas. J. (2015) The skin microbiome: Associations between altered microbial communities and disease. Australas J Dermatol., 56, 268.

77. Okada K, Matsushima Y, Mizutani K, Yamanaka K. (2015) The Human Skin Microbiome Associates with the Outcome of and Is Influenced by Bacterial Infection.Microbiome, 1, 31.

78. Matsumoto M, Ebata T, Hirooka J, Hosoya R, Inoue N, Itami S, Tsuji K, Yaginuma T, Muramatsu K, Nakamura A, Fujita A, Nagakura T. (2014) Antipruritic effects of the probiotic strain LKM512 in adults with atopic dermatitis. Ann Allergy Asthma Immunol.,113(2), 209-216

79. Rather I.A., Bajpai V.K., Huh Y.S., Han Y.-K., Bhat E.A., Lim J., Paek W.K., Park Y.-H. (2018) Probiotic Lactobacillus sakei proBio-65 extract ameliorates the severity of imiquimod induced psoriasis-like skin inflammation in a mouse model. Front. Microbiol.,9,1021

80. van Zuuren EJ, Fedorowicz Z, Carter B, van der Linden MM, Charland L. (2015) Interventions for rosacea. Cochrane Database Syst. Rev., 28, 1.

81. Picardo, M. Ottaviani, J. (2014) Diet and rosacea: the role of dietary change in the management of rosacea. Clin. Gastroenterol, 48, S85.

82. N. N. Schommer, R. L. Gallo (2013) Structure and function of the human skin microbiome. Trends Microbiol.,21, 660.

83. E. Lazaridou, C. Giannopoulou, C. Fotiadou, E. Vakirlis, A. Trigoni, D. Ioannides, J. Dtsch. (2011) Dermatol. Ges., 9, 21.

84. Parodi, S. Paolino, A. Greco, F. Drago, C. Mansi, A. Rebora, A. Parodi, V. Savarino (2008) Clin. Gastroenterol. Hepatol., 6, 759.

85. M. C. Fortuna, V. Garelli, G. Pranteda, F. Romaniello, M. Cardone, M. Carlesimo, A. Rossi (2016) Dermatol. Ther., 29, 249.

86. Wu KG, Li TH, Peng H. (2013) Oral probiotics reduce the incidence and severity of atopic dermatitis in children: A randomized controlled trial. Allergy Asthma Proc. 34(5), 496-501.

87. Kim SO, Ah YM, Yu YM (2014) Effects of probiotics for the treatment of atopic dermatitis: a meta-analysis of randomized controlled trials. Ann Allergy Asthma Immunol.,113(2), 217-226.

88. Kuitunen M, Kukkonen K, Juntunen-Backman K. (2009) Probiotics prevent IgE-associated allergy until age 5 years in cesarean-delivered children but not in the total cohort. J Allergy Clin Immunol.,123(2), 335-341.

89. Dermatologists. (2021) The significance and composition of the skin microbiome in dermatological diseases. Medicina360.ru : portal for doctors. Received from https://medicina360.ru/article /.

90. Technical Regulations of the Customs Union TR CU 009/2011 On the safety of perfumery and cosmetic products. (as amended on March 29, 2019). Official website of the Customs Union Commission www.tsouz.ru , 2011. 257 p.

91. Tikhonova E.V., & Shlenskaya N.M. (2021). Review of the subject field as a method of synthesis of scientific data. Storage and processing of agricultural raw materials, (3), 11-25. https://doi.org/10.36107/spfp.2021.257

92. Savinova Yu.S., Belkova N.L., Semenova N.V., Rychkova L.V. History, modern trends and prospects of development of pro- and prebiotic drugs in Russia and abroad. Acta biomedica scientifica. 2022; 7(5-1): 211-227. doi: 10.29413/ABS.2022-7.5-1.23