Effects of Probiotics on Acne Vulgaris

Abstract

Acne vulgaris is a common chronic inflammatory disease of the pilosebaceous unit. Its pathophysiology includes increased colonization of Cutibacterium acnes in hair follicles, follicular hyperkeratinization, excessive sebum production, and immunological and inflammatory processes. It has been reported that several strains of C. acnes may play role in acne. However, acne is commonly associated with microbial dysbiosis. Studies show that probiotics can have effects on treating acne by providing microbial diversity, controlling the growth of C. acnes strains, and reducing the production of sebum and inflammatory cytokines. Probiotics have also been reported to have potential effects on systemic inflammation, oxidative-stress, tissue lipid content, and even mood. However, since the majority of studies in this area are in vitro, further studies are needed to prove the true efficacy and safety of probiotics. In this study, current literature information is thought to address the effects of probiotics on the development of acne vulgaris.

Keywords

• Acne vulgaris
• probiotics
• microbiota

Probiyotiklerin Akne Vulgaris’e Etkisi

Abstract

Akne vulgaris, pilosebase ünitenin yaygın bir kronik inflamatuar hastalığıdır. Patofizyolojisi, kıl köklerinde Cutibacterium acnes kolonizasyonunun artmasını, foliküler hiperkeratinizasyonu, aşırı sebum üretimini ve immünolojik ve inflamatuar süreçleri içermektedir. C. acnes’in birkaç suşunun aknede rol oynayabileceği bildirilmiştir. Bununla birlikte akne yaygın olarak mikrobiyal disbiyozisle ilişkilidir. Çalışmalar; probiyotiklerin, mikrobiyal çeşitliliği sağlayarak, C. acnes suşlarının büyümesini kontrol ederek ve sebum ve inflamatuar sitokinlerin üretimini azaltarak akne tedavisinde etkileri olabileceğini göstermektedir. Probiyotiklerin ayrıca, sistemik inflamasyonu, oksidatif stresi, doku lipit içeriğini ve hatta ruh halini etkileme potansiyelinin de, aknede etkileri olabileceği bildirilmiştir. Ancak bu alanda yapılan çalışmaların çoğunluğu in vitro olduğundan, probiyotiklerin gerçek etkinlik ve güvenliğini kanıtlamak için daha ileri çalışmalara ihtiyaç duyulmaktadır. Bu çalışmada, güncel literatür bilgileriyle probiyotiklerin akne vulgaris gelişimi üzerine etkilerine değinilmesi düşünülmektedir.

Keywords

• Akne vulgaris
• probiyotikler
• Mikrobiota

References

1. Agamia, N., Abdallah, D., Sorour, O., Mourad, B., & Younan, D. (2016). Skin expression of mammalian target of rapamycin and forkhead box transcription factor O1, and serum insulin‐like growth factor‐1 in patients with acne vulgaris and their relationship with diet.
2. British Journal of Dermatology, 174(6), 1299-1307.
3. Akaza, N., Akamatsu, H., Numata, S., Yamada, S., Yagami, A., Nakata, S., & Matsunaga, K. (2016). Microorganisms inhabiting follicular contents of facial acne are not only Propionibacterium but also Malassezia spp.
4. The Journal of Dermatology, 43(8), 906-911.
5. Al‐Ghazzewi, F. H., & Tester, R. F. (2010). Effect of konjac glucomannan hydrolysates and probiotics on the growth of the skin bacterium Propionibacterium acnes in vitro. International Journal of Cosmetic Science, 32(2), 139-142.
6. Awan, S., & Lu, J. (2017). Management of severe acne during pregnancy: A case report and review of the literature. International Journal of Women's Dermatology, 3(3), 145-150.
7. Barnard, E., Shi, B., Kang, D., Craft, N., & Li, H. (2016). The balance of metagenomic elements shapes the skin microbiome in acne and health. Scientific Reports, 6, 39491.
8. Barrett, K., Ghishan, F., Merchant, J., Said, H., & Wood, J. (2013). Physiology of the gastrointestinal tract, vol. 1‐2. In: Elsevier, Cambridge, MA.

9. Bateni, E., Tester, R., Al-Ghazzewi, F., Bateni, S., Alvani, K., & Piggott, J. (2013). The use of konjac glucomannan hydrolysates (GMH) to improve the health of the skin and reduce acne vulgaris.
10. American Journal of Dermatology Venereology, 2(2), 10-14.
11. Belkaid, Y., & Tamoutounour, S. (2016). The influence of skin microorganisms on cutaneous immunity. Nature Reviews Immunology, 16(6), 353-366.
12. Bhate, K., & Williams, H. (2013). Epidemiology of acne vulgaris. British Journal of Dermatology, 168(3), 474-485.
13. Bienenstock, J., Kunze, W., & Forsythe, P. (2015). Microbiota and the gut–brain axis. Nutrition Reviews, 73(suppl_1), 28-31.
14. Bowe, W., Patel, N., & Logan, A. (2014). Acne vulgaris, probiotics and the gut-brain-skin axis: from anecdote to translational medicine. Beneficial Microbes, 5(2), 185-199.
15. Bowe, W. P., Filip, J. C., DiRienzo, J. M., Volgina, A., & Margolis, D. J. (2006). Inhibition of Propionibacterium acnes by bacteriocin-like inhibitory substances (BLIS) produced by Streptococcus salivarius.
16. Journal of drugs in dermatology: JDD, 5(9), 868.
17. Bowe, W. P., & Logan, A. C. (2010). Clinical implications of lipid peroxidation in acne vulgaris: old wine in new bottles. Lipids in Health Disease, 9(1), 141.
18. Bowe, W. P., & Logan, A. C. (2011). Acne vulgaris, probiotics and the gut-brain-skin axis-back to the future? Gut pathogens, 3(1), 1-11.
19. Brial, F., Le Lay, A., Dumas, M.-E., & Gauguier, D. (2018). Implication of gut microbiota metabolites in cardiovascular and metabolic diseases. Cellular Molecular Life Sciences, 75(21), 3977-3990.
20. Burris, J., Shikany, J. M., Rietkerk, W., & Woolf, K. (2018). A low glycemic index and glycemic load diet decreases insulin-like growth factor-1 among adults with moderate and severe acne: A short-duration, 2-week randomized controlled trial.
21. Journal of the Academy of Nutrition Dietetics, 118(10), 1874-1885.
22. Byrd, A. L., Belkaid, Y., & Segre, J. A. (2018). The human skin microbiome. Nat Rev Microbiol, 16(3), 143-155.
23. Caputi, V., & Giron, M. C. (2018). Microbiome-gut-brain axis and toll-like receptors in Parkinson’s disease. International Journal of Molecular Sciences, 19(6), 1689.
24. Chernyshov, P. V., Zouboulis, C. C., Tomas‐Aragones, L., Jemec, G. B., Manolache, L., Tzellos, T., Sampogna, F., Evers, A. W. M., Dessinioti, C., Marron, S. E., Bettoli, V., van Cranenburgh, O. D., Svensson, A., Liakou, A. I., Poot, F., Szepietowski, J. C., Salek, M. S., & Finlay, A. Y. (2018).
25. Quality of life measurement in acne. Position paper of the European Academy of Dermatology and Venereology Task Forces on quality of life and patient oriented outcomes and acne, rosacea and hidradenitis suppurativa. Journal of the European Academy of Dermatology, 32(2), 194-208.
26. Christensen, G. J., Scholz, C. F. P., Enghild, J., Rohde, H., Kilian, M., Thürmer, A., Brzuszkiewicz, E., Lomholt, H. B., & Brüggemann, H. (2016). Antagonism between Staphylococcus epidermidis and Propionibacterium acnes and its genomic basis. BMC genomics, 17(1), 1-14.
27. Christensen, G. J. M., & Brüggemann, H. (2014). Bacterial skin commensals and their role as host guardians. Beneficial Microbes, 5(2), 201-215.
28. Claudel, J.-P., Auffret, N., Leccia, M.-T., Poli, F., Corvec, S., & Dréno, B. (2019). Staphylococcus epidermidis: A Potential New Player in the Physiopathology of Acne? Dermatology, 235(4), 287-294.
29. Clemente, J. C., Manasson, J., & Scher, J. U. (2018). The role of the gut microbiome in systemic inflammatory disease. Bmj, 360.
30. Coates, R., Moran, J., & Horsburgh, M. J. (2014). Staphylococci: colonizers and pathogens of human skin. Future Microbiology, 9(1), 75-91.
31. Collins, S., & Reid, G. (2016). Distant site effects of ingested prebiotics. Nutrients, 8(9), 523.
32. Cong, T.-X., Hao, D., Wen, X., Li, X.-H., He, G., & Jiang, X. (2019). From pathogenesis of acne vulgaris to anti-acne agents. Archives of Dermatological Research, 1-13.
33. Cosseau, C., Devine, D. A., Dullaghan, E., Gardy, J. L., Chikatamarla, A., Gellatly, S., Lorraine, L. Y., Pistolic, J., Falsafi, R., & Tagg, J. (2008). The commensal Streptococcus salivarius K12 downregulates the innate immune responses of human epithelial cells and promotes host-microbe homeostasis. Infection Immunity, 76(9), 4163-4175.
34. Cresce, N. D., Davis, S. A., Huang, W. W., & Feldman, S. R. (2014). The quality of life impact of acne and rosacea compared to other major medical conditions. Journal of Drugs in Dermatology: JDD, 13(6), 692.
35. Dagnelie, M.-A., Corvec, S., Saint-Jean, M., Bourdès, V., Nguyen, J.-M., Khammari, A., & Dréno, B. (2018). Decrease in diversity of Propionibacterium acnes phylotypes in patients with severe acne on the back. Acta dermato-venereologica, 98(1-2), 262-267.
36. Dagnelie, M. A., Corvec, S., Saint‐Jean, M., Nguyen, J. M., Khammari, A., & Dréno, B. (2019a). Cutibacterium acnes phylotypes diversity loss: a trigger for skin inflammatory process. Journal of the European Academy of Dermatology Venereology, 33(12), 2340-2348.
37. Dagnelie, M. A., Montassier, E., Khammari, A., Mounier, C., Corvec, S., & Dréno, B. (2019b). Inflammatory skin is associated with changes in the skin microbiota composition on the back of severe acne patients. Experimental Dermatology, 28(8), 961-967.
38. Danby, F. W. (2010). Nutrition and acne. Clinics in Dermatology, 28(6), 598-604.
39. de Gunzburg, J., Ghozlane, A., Ducher, A., Le Chatelier, E., Duval, X., Ruppé, E., Armand-Lefevre, L., Sablier-Gallis, F., Burdet, C., & Alavoine, L. (2018). Protection of the human gut microbiome from antibiotics. The Journal of Infectious Diseases, 217(4), 628-636.
40. Deng, Y., Wang, H., Zhou, J., Mou, Y., Wang, G., & Xiong, X. (2018). Patients with acne vulgaris have a distinct gut microbiota in comparison with healthy controls. Acta dermato-venereologica, 98(7-8), 783-790.
41. Derwa, Y., Gracie, D., Hamlin, P., & Ford, A. (2017). Systematic review with meta‐analysis: the efficacy of probiotics in inflammatory bowel disease. Alimentary Pharmacology Therapeutics, 46(4), 389-400.
42. Dimarzio, L., Cinque, B., Cupelli, F., De Simone, C., Cifone, M., & Giuliani, M. (2008). Increase of skin-ceramide levels in aged subjects following a short-term topical application of bacterial sphingomyelinase from Streptococcus thermophilus. International Journal of Immunopathology Pharmacology, 21(1), 137-143.
43. Dréno, B. (2017). What is new in the pathophysiology of acne, an overview. Journal of the European Academy of Dermatology Venereology, 31, 8-12.
44. Dreno, B., Martin, R., Moyal, D., Henley, J. B., Khammari, A., & Seité, S. (2017). Skin microbiome and acne vulgaris: Staphylococcus, a new actor in acne. Experimental Dermatology, 26(9), 798-803.
45. Dréno, B., Pécastaings, S., Corvec, S., Veraldi, S., Khammari, A., & Roques, C. (2018). Cutibacterium acnes (Propionibacterium acnes) and acne vulgaris: a brief look at the latest updates. Journal of the European Academy of Dermatology Venereology, 32, 5-14.
46. Fabbrocini, G., Bertona, M., Picazo, O., Pareja-Galeano, H., Monfrecola, G., & Emanuele, E. (2016). Supplementation with Lactobacillus rhamnosus SP1 normalises skin expression of genes implicated in insulin signalling and improves adult acne. Beneficial Microbes, 7(5), 625-630.
47. FAO/WHO. (2001). Evaluation of health and nutritional properties of powder milk and live lactic acid bacteria. In (pp. 1-4). Report from FAO/WHO Expert Consultation.
48. Feng, Y., Ralls, M. W., Xiao, W., Miyasaka, E., Herman, R. S., & Teitelbaum, D. H. (2012). Loss of enteral nutrition in a mouse model results in intestinal epithelial barrier dysfunction. Annals of the New York Academy of Sciences, 1258, 71.
49. Fitz-Gibbon, S., Tomida, S., Chiu, B.-H., Nguyen, L., Du, C., Liu, M., Elashoff, D., Erfe, M. C., Loncaric, A., & Kim, J. (2013). Propionibacterium acnes strain populations in the human skin microbiome associated with acne. Journal of Investigative Dermatology, 133(9), 2152-2160.
50. Foster, J. A., Rinaman, L., & Cryan, J. F. (2017). Stress & the gut-brain axis: regulation by the microbiome. Neurobiology of Stress, 7, 124-136.
51. Fox, L., Csongradi, C., Aucamp, M., Du Plessis, J., & Gerber, M. (2016). Treatment modalities for acne. Molecules, 21(8), 1063.
52. Fu, Y. R., Yi, Z. J., Pei, J. l., & Guan, S. (2010). Effects of Bifidobacterium bifidum on adaptive immune senescence in aging mice. Microbiology Immunology, 54(10), 578-583.
53. Fuchs-Tarlovsky, V., Marquez-Barba, M. F., & Sriram, K. (2016). Probiotics in dermatologic practice. Nutrition Reviews, 32(3), 289-295.
54. Ganji‐Arjenaki, M., & Rafieian‐Kopaei, M. (2018). Probiotics are a good choice in remission of inflammatory bowel diseases: a meta analysis and systematic review. Journal of Cellular Physiology, 233(3), 2091-2103.
55. Gasbarrini, G., Bonvicini, F., & Gramenzi, A. (2016). Probiotics history. Journal of Clinical Gastroenterology, 50, 116-119.
56. Gollnick, H., Bettoli, V., Lambert, J., Araviiskaia, E., Binic, I., Dessinioti, C., Galadari, I., Ganceviciene, R., Ilter, N., & Kaegi, M. (2016). A consensus‐based practical and daily guide for the treatment of acne patients. Journal of the European Academy of Dermatology Venereology, 30(9), 1480-1490.
57. 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(5931), 1190-1192.
58. Grice, E. A., & Segre, J. A. (2011). The skin microbiome. Nature Reviews Microbiology, 9(4), 244-253.
59. Gueniche, A., Philippe, D., Bastien, P., Reuteler, G., Blum, S., Castiel-Higounenc, I., Breton, L., & Benyacoub, J. (2014). Randomised double-blind placebo-controlled study of the effect of Lactobacillus paracasei NCC 2461 on skin reactivity. Beneficial Microbes, 5(2), 137-145.
60. Haak, B. W., Levi, M., & Wiersinga, W. J. (2017). Microbiota-targeted therapies on the intensive care unit. Current Opinion in Critical Care, 23(2), 167-174.
61. Hay, R. J., Johns, N. E., Williams, H. C., Bolliger, I. W., Dellavalle, R. P., Margolis, D. J., Marks, R., Naldi, L., Weinstock, M. A., & Wulf, S. K. (2014). The global burden of skin disease in 2010: an analysis of the prevalence and impact of skin conditions. Journal of investigative dermatology, 134(6), 1527-1534.
62. Heijtz, R. D., Wang, S., Anuar, F., Qian, Y., Björkholm, B., Samuelsson, A., Hibberd, M. L., Forssberg, H., & Pettersson, S. (2011). Normal gut microbiota modulates brain development and behavior. Proceedings of the National Academy of Sciences, 108(7), 3047-3052.
63. Hemarajata, P., & Versalovic, J. (2013). Effects of probiotics on gut microbiota: mechanisms of intestinal immunomodulation and neuromodulation. Therapeutic Advances in Gastroenterology, 6(1), 39-51.
64. Hidalgo‐Cantabrana, C., Gomez, J., Delgado, S., Requena‐López, S., Queiro‐Silva, R., Margolles, A., Coto, E., Sanchez, B., & Coto‐Segura, P. (2019). Gut microbiota dysbiosis in a cohort of patients with psoriasis. British Journal of Dermatology, 181(6), 1287-1295.
65. Hill, C., Guarner, F., Reid, G., Gibson, G. R., Merenstein, D. J., Pot, B., Morelli, L., Canani, R. B., Flint, H. J., & Salminen, S. (2014). Expert consensus document: The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nature Reviews Gastroenterology Hepatology, 11(8), 506.
66. Hutkins, R. W., Krumbeck, J. A., Bindels, L. B., Cani, P. D., Fahey Jr, G., Goh, Y. J., Hamaker, B., Martens, E. C., Mills, D. A., & Rastal, R. A. (2016). Prebiotics: why definitions matter. Current Opinion in Biotechnology, 37, 1-7. Johnson, T., Kang, D., Barnard, E., & Li, H. (2016). Strain-level differences in porphyrin production and regulation in Propionibacterium acnes elucidate disease associations. Msphere, 1(1).
67. 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 minocycline in subjects with mild to moderate acne. Journal of Cutaneous Medicine Surgery, 17(2), 114-122.
68. Jung, M.-J., Lee, J., Shin, N.-R., Kim, M.-S., Hyun, D.-W., Yun, J.-H., Kim, P. S., Whon, T. W., & Bae, J.-W. (2016). Chronic repression of mTOR complex 2 induces changes in the gut microbiota of diet-induced obese mice. Scientific Reports, 6(1), 1-10.
69. Kalil, C. L. P. V., Chaves, C., De Vargas, A. S., Campos, V. B., Chagas, R. P., & de Vento, M. (2020). Use of probiotics in Dermatology-Review. Surgical Cosmetic Dermatology, 208.
70. Kang, B. S., Seo, J.-G., Lee, G.-S., Kim, J.-H., Kim, S. Y., Han, Y. W., Kang, H., Kim, H. O., Rhee, J. H., & Chung, M.-J. (2009). Antimicrobial activity of enterocins from Enterococcus faecalis SL-5 against Propionibacterium acnes, the causative agent in acne vulgaris, and its therapeutic effect. The Journal of Microbiology, 47(1), 101-109.
71. Kang, D., Shi, B., Erfe, M. C., Craft, N., & Li, H. (2015). Vitamin B12 modulates the transcriptome of the skin microbiota in acne pathogenesis. Science Translational Medicine, 7(293), 103.
72. Kang, M.-S., Oh, J.-S., Lee, S.-W., Lim, H.-S., Choi, N.-K., & Kim, S.-M. (2012). Effect of Lactobacillus reuteri on the proliferation of Propionibacterium acnes and Staphylococcus epidermidis. The Journal of Microbiology, 50(1), 137-142.
73. Kim, B.-J., Lee, S.-Y., Kim, H.-B., Lee, E., & Hong, S.-J. (2014). Environmental changes, microbiota, and allergic diseases. Allergy, Asthma Immunology Research, 6(5), 389-400.
74. Kim, J., Ko, Y., Park, Y.-K., Kim, N.-I., Ha, W.-K., & Cho, Y. (2010). Dietary effect of lactoferrin-enriched fermented milk on skin surface lipid and clinical improvement of acne vulgaris. Nutrition, 26(9), 902-909.
75. Kimura, I., Ozawa, K., Inoue, D., Imamura, T., Kimura, K., Maeda, T., Terasawa, K., Kashihara, D., Hirano, K., & Tani, T. (2013). The gut microbiota suppresses insulin-mediated fat accumulation via the short-chain fatty acid receptor GPR43. Nature Communications, 4(1), 1-12.
76. Knackstedt, R., Knackstedt, T., & Gatherwright, J. (2020). The role of topical probiotics in skin conditions: A systematic review of animal and human studies and implications for future therapies. Experimental Dermatology, 29(1), 15-21.
77. Kober, M.-M., & Bowe, W. P. (2015). The effect of probiotics on immune regulation, acne, and photoaging. International Journal of Women's Dermatology, 1(2), 85-89.
78. Kong, H. H., & Segre, J. A. (2012). Skin microbiome: looking back to move forward. Journal of Investigative Dermatology, 132(3), 933-939.
79. Laborel-Préneron, E., Bianchi, P., Boralevi, F., Lehours, P., Fraysse, F., Morice-Picard, F., Sugai, M., Sato’o, Y., Badiou, C., & Lina, G. (2015). Effects of the Staphylococcus aureus and Staphylococcus epidermidis secretomes isolated from the skin microbiota of atopic children on CD4+ T cell activation. PLoS One, 10(10), e0141067.
80. Lai, Y., Cogen, A. L., Radek, K. A., Park, H. J., MacLeod, D. T., Leichtle, A., Ryan, A. F., Di Nardo, A., & Gallo, R. L. (2010). Activation of TLR2 by a small molecule produced by Staphylococcus epidermidis increases antimicrobial defense against bacterial skin infections. Journal of Investigative Dermatology, 130(9), 2211-2221.
81. Layton, A., Eady, E. A., Peat, M., Whitehouse, H., Levell, N., Ridd, M., Cowdell, F., Patel, M., Andrews, S., & Oxnard, C. (2015). Identifying acne treatment uncertainties via a James Lind Alliance priority setting partnership. BMJ Open, 5(7).
82. Lee, G. R., Maarouf, M., Hendricks, A. K., Lee, D. E., & Shi, V. Y. (2019b). Current and emerging therapies for hand eczema. Dermatologic Therapy, 32(3), e12840.
83. Lee, Y. B., Byun, E. J., & Kim, H. S. (2019a). Potential role of the microbiome in acne: a comprehensive review. Journal of Clinical Medicine, 8(7), 987.
84. Levkovich, T., Poutahidis, T., Smillie, C., Varian, B. J., Ibrahim, Y. M., Lakritz, J. R., Alm, E. J., & Erdman, S. E. (2013). Probiotic bacteria induce a ‘glow of health’. PLoS One, 8(1), e53867.
85. Leyden, J. J., McGinley, K. J., & Foglia, A. N. (1986). Qualitative and quantitative changes in cutaneous bacteria associated with systemic isotretinoin therapy for acne conglobata. Journal of Investigative Dermatology, 86(4), 390-393.
86. Lolou, V., & Panayiotidis, M. I. (2019). Functional role of probiotics and prebiotics on skin health and disease. Fermentation, 5(2), 41.
87. Magistrelli, L., Amoruso, A., Mogna, L., Graziano, T., Cantello, R., Pane, M., & Comi, C. (2019). Probiotics May Have Beneficial Effects in Parkinson's Disease: In vitro Evidence. Frontiers in Immunology, 10, 969.
88. Marchetti, F., Capizzi, R., & Tulli, A. (1987). Efficacy of regulators of the intestinal bacterial flora in the therapy of acne vulgaris. La Clinica Terapeutica, 122(5), 339.
89. Marcinkowska, M., Zagórska, A., Fajkis, N., Kołaczkowski, M., & Paśko, P. (2018). A Review of Probiotic Supplementation and Feasibility of Topical Application for the Treatment of Pediatric Atopic Dermatitis. Current Pharmaceutical Biotechnology, 19(10), 827-838.
90. Marlicz, W., Yung, D. E., Skonieczna-Żydecka, K., Loniewski, I., van Hemert, S., Loniewska, B., & Koulaouzidis, A. (2017). From clinical uncertainties to precision medicine: The emerging role of the gut barrier and microbiome in small bowel functional diseases. Expert Review of Gastroenterology Hepatology, 11(10), 961-978.
91. Mayer, E. A., Tillisch, K., & Gupta, A. (2015). Gut/brain axis and the microbiota. The Journal of Clinical Investigation, 125(3), 926-938.
92. McDowell, A., Nagy, I., Magyari, M., Barnard, E., & Patrick, S. (2013). The opportunistic pathogen Propionibacterium acnes: insights into typing, human disease, clonal diversification and CAMP factor evolution. PLoS One, 8(9), e70897.
93. Melnik, B. (2013). Acne and diet. Der Hautarzt Zeitschrift fur Dermatologie, Venerologie, und Verwandte Gebiete, 64(4), 252, 254-258, 260.
94. Melnik, B. C. (2018). Acne vulgaris: The metabolic syndrome of the pilosebaceous follicle. Clinics in Dermatology, 36(1), 29-40.
95. Melnik, B. C., & Schmitz, G. (2009). Role of insulin, insulin‐like growth factor‐1, hyperglycaemic food and milk consumption in the pathogenesis of acne vulgaris. Experimental Dermatology, 18(10), 833-841.
96. Mohseni, S., Bayani, M., Bahmani, F., Tajabadi‐Ebrahimi, M., Bayani, M. A., Jafari, P., & Asemi, Z. (2018). The beneficial effects of probiotic administration on wound healing and metabolic status in patients with diabetic foot ulcer: A randomized, double‐blind, placebo‐controlled trial. Diabetes/Metabolism Research and Reviews, 34(3), e2970.
97. Muizzuddin, N., Maher, W., Sullivan, M., Schnittger, S., & Mammone, T. (2012). Physiological effect of a probiotic on skin. Journal of Cosmetic Science, 63(6), 385-395.
98. Naik, S., Bouladoux, N., Linehan, J. L., Han, S.-J., Harrison, O. J., Wilhelm, C., Conlan, S., Himmelfarb, S., Byrd, A. L., & Deming, C. (2015). Commensal–dendritic-cell interaction specifies a unique protective skin immune signature. Nature, 520(7545), 104-108.
99. Nam, J. H., Yun, Y., Kim, H. S., Kim, H. N., Jung, H. J., Chang, Y., Ryu, S., Shin, H., Kim, H.L., & Kim, W. S. (2018). Rosacea and its association with enteral microbiota in Korean females. Experimental Dermatology, 27(1), 37-42.
100. Nast, A., Dréno, B., Bettoli, V., Bukvic Mokos, Z., Degitz, K., Dressler, C., Finlay, A. Y., Haedersdal, M., Lambert, J., & Layton, A. (2016). European evidence‐based (S3) guideline for the treatment of acne–update 2016–short version. Journal of the European Academy of Dermatology Venereology, 30(8), 1261-1268.
101. Nodake, Y., Matsumoto, S., Miura, R., Honda, H., Ishibashi, G., Matsumoto, S., Dekio, I., & Sakakibara, R. (2015). Pilot study on novel skin care method by augmentation with Staphylococcus epidermidis, an autologous skin microbe–A blinded randomized clinical trial. Journal of Dermatological Science, 79(2), 119-126.
102. O'Neill, C. A., Monteleone, G., McLaughlin, J. T., & Paus, R. (2016). The gut‐skin axis in health and disease: a paradigm with therapeutic implications. BioEssays, 38(11), 1167-1176.
103. Oh, S., Kim, S.-H., Ko, Y., Sim, J.-H., Kim, K. S., Lee, S.-H., Park, S., & Kim, Y. J. (2006). Effect of bacteriocin produced by Lactococcus sp. HY 449 on skin-inflammatory bacteria. Food Chemical Toxicology, 44(4), 552-559.
104. Pandey, K. R., Naik, S. R., & Vakil, B. V. (2015). Probiotics, prebiotics and synbiotics-a review. Journal of Food Science Technology, 52(12), 7577-7587.
105. Pavicic, T., Wollenweber, U., Farwick, M., & Korting, H. (2007). Anti‐microbial and‐inflammatory activity and efficacy of phytosphingosine: an in vitro and in vivo study addressing acne vulgaris. International Journal of Cosmetic Science, 29(3), 181-190.
106. Petersen, E., Skov, L., Thyssen, J., & Jensen, P. (2019). Role of the gut microbiota in atopic dermatitis: a systematic review. Acta Dermato-Venereologica, 99(1-2), 5-11.
107. Platsidaki, E., & Dessinioti, C. (2018). Recent advances in understanding Propionibacterium acnes (Cutibacterium acnes) in acne. FResearch, 7.
108. Quadros, E., Landzert, N. M., LeRoy, S., Gasparini, F., & Worosila, G. (1994). Colonic absorption of insulin-like growth factor I in vitro. Pharmaceutical Research, 11(2), 226-230.
109. Rajiv, P., Nitesh, K., Raj, K., & Hemant, G. K. (2013). Staphylococcus epidermidis in Human Skin Microbiome associated with Acne: A Cause of Disease or Defence? Research Journal of Biotechnology, 8(12), 78-82.
110. Rather, I. A., Bajpai, V. K., Kumar, S., Lim, J., Paek, W. K., & Park, Y.-H. (2016). Probiotics and atopic dermatitis: an overview. Frontiers in Microbiology, 7, 507.
111. Salem, I., Ramser, A., Isham, N., & Ghannoum, M. A. (2018). The gut microbiome as a major regulator of the gut-skin axis. Frontiers in Microbiology, 9, 1459.
112. Samuelson, D. R., Welsh, D. A., & Shellito, J. E. (2015). Regulation of lung immunity and host defense by the intestinal microbiota. Frontiers in Microbiology, 6, 1085.
113. Scholz-Ahrens, K. E., Adolphi, B., Rochat, F., Barclay, D. V., de Vrese, M., Açil, Y., & Schrezenmeir, J. (2016). Effects of probiotics, prebiotics, and synbiotics on mineral metabolism in ovariectomized rats-impact of bacterial mass, intestinal absorptive area and reduction of bone turn-over. NFS Journal, 3, 41-50.
114. Scholz, C. F., & Kilian, M. (2016). The natural history of cutaneous propionibacteria, and reclassification of selected species within the genus Propionibacterium to the proposed novel genera Acidipropionibacterium gen. nov., Cutibacterium gen. nov. and Pseudopropionibacterium gen. nov. International Journal of Systematic Evolutionary Microbiology, 66(11), 4422-4432.
115. Silverberg, J. I., & Silverberg, N. (2014). Epidemiology and extracutaneous comorbidities of severe acne in adolescence: a US population‐based study. British Journal of Dermatology, 170(5), 1136-1142.
116. Skabytska, Y., & Biedermann, T. (2016). Staphylococcus epidermidis sets things right again. Journal of Investigative Dermatology, 136(3), 559-560.
117. Skonieczna-Żydecka, K., Kaczmarczyk, M., Łoniewski, I., Lara, L. F., Koulaouzidis, A., Misera, A., Maciejewska, D., & Marlicz, W. (2018). A systematic review, Meta-analysis, and Meta-regression evaluating the efficacy and mechanisms of action of Probiotics and synbiotics in the prevention of surgical site infections and surgery-related complications. Journal of Clinical Medicine, 7(12), 556.
118. Sommer, F., Adam, N., Johansson, M. E., Xia, L., Hansson, G. C., & Bäckhed, F. (2014). Altered mucus glycosylation in core 1 O-glycan-deficient mice affects microbiota composition and intestinal architecture. PLoS One, 9(1), e85254.
119. Sonnenburg, J. L., & Bäckhed, F. (2016). Diet–microbiota interactions as moderators of human metabolism. Nature, 535(7610), 56-64.
120. Stokes, J. H., & Pillsbury, D. M. (1930). The effect on the skin of emotional and nervous states: iII. Theoretical and practical consideration of a gastro-intestinal mechanism. Archives of Dermatology Syphilology, 22(6), 962-993.
121. Suh, D. H., & Kwon, H. (2015). What's new in the physiopathology of acne? British Journal of Dermatology, 172, 13-19.
122. Szabó, K., & Kemény, L. (2011). Studying the genetic predisposing factors in the pathogenesis of acne vulgaris. Human Immunology, 72(9), 766-773.
123. Szántó, M., Dózsa, A., Antal, D., Szabó, K., Kemény, L., & Bai, P. (2019). Targeting the gut‐skin axis—Probiotics as new tools for skin disorder management? Experimental Dermatology, 28(11), 1210-1218.
124. Tan, L., Zhao, S., Zhu, W., Wu, L., Li, J., Shen, M., Lei, L., Chen, X., & Peng, C. (2018). The Akkermansia muciniphila is a gut microbiota signature in psoriasis. Experimental Dermatology, 27(2), 144-149.
125. Tax, G., Urbán, E., Palotás, Z., Puskás, R., Kónya, Z., Bíró, T., Kemény, L., & Szabó, K. (2016). Propionic acid produced by Propionibacterium acnes strains contributes to their pathogenicity. Acta Dermato-Venereologica, 96(1), 43-49.
126. Tejero-Sariñena, S., Barlow, J., Costabile, A., Gibson, G. R., & Rowland, I. (2012). In vitro evaluation of the antimicrobial activity of a range of probiotics against pathogens: evidence for the effects of organic acids. Anaerobe, 18(5), 530-538.
127. Therapeutics, A. (2017). AOBiome Therapeutics reports positive efficacy results from phase 2b clinical trial of ammonia oxidizing bacteria (AOB) for the treatment of acne vulgaris.
128. Tomida, S., Nguyen, L., Chiu, B.-H., Liu, J., Sodergren, E., Weinstock, G. M., & Li, H. (2013). Pan-genome and comparative genome analyses of Propionibacterium acnes reveal its genomic diversity in the healthy and diseased human skin microbiome. MBIO, 4(3).
129. Tuchayi, S. M., Makrantonaki, E., Ganceviciene, R., Dessinioti, C., Feldman, S. R., & Zouboulis, C. C. (2015). Acne vulgaris. Nature Reviews Disease Primers, 1(1), 1-20.
130. US Department of Health and Human Services. "Antibiotic resistance threats in the United States, 2013." Centers for disease control and prevention (2013): 1-113.
131. Wang, Y., Kuo, S., Shu, M., Yu, J., Huang, S., Dai, A., Two, A., Gallo, R. L., & Huang, C.-M. (2014). Staphylococcus epidermidis in the human skin microbiome mediates fermentation to inhibit the growth of Propionibacterium acnes: implications of probiotics in acne vulgaris. Applied Microbiology Biotechnology, 98(1), 411-424.
132. Williams, H. C., Dellavalle, R. P., & Garner, S. (2012). Acne vulgaris. The Lancet, 379(9813), 361-372.
133. Wu, X.-D., Liu, M.-M., Liang, X., Hu, N., & Huang, W. (2018). Effects of perioperative supplementation with pro-/synbiotics on clinical outcomes in surgical patients: a meta-analysis with trial sequential analysis of randomized controlled trials. Clinical Nutrition, 37(2), 505-515.
134. Xu, H., & Li, H. (2019). Acne, the skin microbiome, and antibiotic treatment. American Journal of Clinical Dermatology, 20(3), 335-344.
135. Yel, B. Ö., & Güneş, F. E. (2018). Akne Vulgaris ile Beslenme İlişkisi. Hacettepe Üniversitesi Sağlık Bilimleri Fakültesi Dergisi, 5(1), 46-59.
136. Zaenglein, A. L., Pathy, A. L., Schlosser, B. J., Alikhan, A., Baldwin, H. E., Berson, D. S., Bowe, W. P., Graber, E. M., Harper, J. C., & Kang, S. (2016). Guidelines of care for the management of acne vulgaris. Journal of the American Academy of Dermatology, 74(5), 945-973.