Skin microbiome and modern treatment options for complicated forms of atopic dermatitis
- Authors: Chernushevich D.D.1, Elisyutina O.G.1,2, Fedenko E.S.1
-
Affiliations:
- National Research Center ― Institute of Immunology
- Peoples’ Friendship University of Russia
- Issue: Vol 20, No 1 (2023)
- Pages: 63-73
- Section: Reviews
- Submitted: 22.02.2023
- Accepted: 10.03.2023
- Published: 06.04.2023
- URL: https://rusalljournal.ru/raj/article/view/6221
- DOI: https://doi.org/10.36691/RJA6221
- ID: 6221
Cite item
Abstract
Currently, atopic dermatitis is considered a systemic multifactorial disease, and its development involves various factors, mainly genetic disorders, epidermal barrier impairment, microbiome changes, allergen sensitization, and nonspecific environmental factors.
The microbial skin barrier in patients with atopic dermatitis has its characteristics due to changes in the species composition of the microflora toward contamination by conditionally pathogenic microorganisms, which have a significant effect on the disease course, leading to secondary skin infection and exacerbations. Microbes and allergens percutaneously penetrate the disrupted epidermal barrier, leading to sensitization to various proteins, including bacterial and fungal proteins, characterizing the t2 immune response.
The treatment of atopic dermatitis aims at achieving long-term control over the disease through an integrated approach, including external and systemic therapy.
Keywords
Full Text
About the authors
Daria D. Chernushevich
National Research Center ― Institute of Immunology
Author for correspondence.
Email: chernushevitchdasha@yandex.ru
ORCID iD: 0000-0003-0006-2773
SPIN-code: 2497-5608
Россия, Moscow
Olga G. Elisyutina
National Research Center ― Institute of Immunology; Peoples’ Friendship University of Russia
Email: el-olga@yandex.ru
ORCID iD: 0000-0002-4609-2591
SPIN-code: 9567-1894
MD, Dr. Sci. (Med)
Россия, Moscow; MoscowElena S. Fedenko
National Research Center ― Institute of Immunology
Email: efedks@gmail.com
ORCID iD: 0000-0003-3358-5087
SPIN-code: 5012-7242
MD, Dr. Sci. (Med)
Россия, MoscowReferences
- Atopic dermatitis. Draft clinical guidelines. The Russian Association of Allergology and Clinical Immunology; 2023. (In Russ). Available from: https://raaci.ru/dat/pdf/project_AtD.pdf. Accessed: 16.01.2023
- Coates M, Lee MJ, Norton D, MacLeod AS. The skin and intestinal microbiota and their specific innate immune systems. Front Immunol. 2019;10:2950. doi: 10.3389/fimmu.2019.02950
- Ali SM, Yosipovitch G. Skin pH: From basic science to basic skin care. Acta Derm Venereol. 2013;93(3):261–267. doi: 10.2340/00015555-1531
- Fluhr JW, Kao J, Jain M, et al. Generation of free fatty acids from phospholipids regulates stratum corneum acidification and integrity. J Invest Dermatol. 2001;117(1):44–51. doi: 10.1046/j.0022-202x.2001.01399.x
- Khaitov RM. Immunologiya: uchebnik. 4th revised and updated. Moscow: GEOTAR-Media; 2021. 520 р. (In Russ).
- Schauber J, Gallo RL. Antimicrobial peptides and the skin immune defense system. J Allergy Clin Immunol. 2008;122(2): 261–266. doi: 10.1016/j.jaci.2008.03.027
- Pflughoeft KJ, Versalovic J. Human microbiome in health and disease. Annu Rev Pathol. 2012;7:99–122. doi: 10.1146/annurev-pathol-011811-132421
- Boxberger M, Cenizo V, Cassir N, La Scola B. Challenges in exploring and manipulating the human skin microbiome. Microbiome. 2021;9(1):125. doi: 10.1186/s40168-021-01062-5
- Byrd AL, Belkaid Y, Segre JA. The human skin microbiome. Nat Rev Microbiol. 2018;16(3):143–155. doi: 10.1038/nrmicro.2017.157
- Pennisi E. Body’s hardworking microbes get some overdue respect. Science. 2010;330(6011):1619. doi: 10.1126/science.330.6011.1619
- Kong HH, Segre JA. Skin microbiome: Looking back to move forward. J Invest Dermatol. 2012;132(3 Pt 2):933–939. doi: 10.1038/jid.2011.417
- Arumugam M, Raes J, Pelletier E, et al. Enterotypes of the human gut microbiome. Nature. 2011;473(7346):174–180. doi: 10.1038/nature09944
- Schmid-Wendtner MH, Korting HC. The pH of the skin surface and its impact on the barrier function. Skin Pharmacol Physiol. 2006;19(6):296–302. doi: 10.1159/000094670
- Myles IA, Reckhow JD, Williams KW, et al. A method for culturing Gram-negative skin microbiota. BMC Microbiol. 2016;16:60. doi: 10.1186/s12866-016-0684-9
- Cassir N, Thomas G, Hraiech S, et al. Chlorhexidine daily bathing: Impact on health care-associated infections caused by gram-negative bacteria. Am J Infect Control. 2015;43(6):640–643. doi: 10.1016/j.ajic.2015.02.010
- Oh J, Byrd AL, Park M; NISC Comparative Sequencing Program. Temporal stability of the human skin microbiome. Cell. 2016;165(4):854–866. doi: 10.1016/j.cell.2016.04.008
- Gupta AK, Kohli Y, Summerbell RC. Molecular differentiation of seven Malassezia species. J Clin Microbiol. 2000;38(5):1869–1875. doi: 10.1128/JCM.38.5.1869-1875.2000
- Oh J, Byrd AL, Deming C, et al. Biogeography and individuality shape function in the human skin metagenome. Nature. 2014;514(7520):59–64. doi: 10.1038/nature13786
- Nakatsuji T, Chen TH, Narala S, et al. Antimicrobials from human skin commensal bacteria protect against Staphylococcus aureus and are deficient in atopic dermatitis. Sci Transl Med. 2017;9(378):eaah4680. doi: 10.1126/scitranslmed.aah4680
- Gaitanis G, Tsiouri G, Spyridonos P, et al. Variation of cultured skin microbiota in mothers and their infants during the first year postpartum. Pediatr Dermatol. 2019;36(4):460–465. doi: 10.1111/pde.13829
- Kim BE, Leung DY. Significance of skin barrier dysfunction in atopic dermatitis. Allergy Asthma Immunol Res. 2018;10(3):207–215. doi: 10.4168/aair.2018.10.3.207
- Yoshida T, Beck LA, de Benedetto A. Skin barrier defects in atopic dermatitis: From old idea to new opportunity. Allergol Int. 2022;71(1):3–13. doi: 10.1016/j.alit.2021.11.006
- Leung DI. Staphylococcus aureus in atopic dermatitis. In: Reitamo S, Luger TA, Steinhoff M, eds. Textbook of atopic dermatitis. London: Informa Healthcare; 2008. Р. 59–68.
- Lin YT, Wang CT, Chiang BL. Role of bacterial pathogens in atopic dermatitis. Clin Rev Allergy Immunol. 2007;33(3):167–177. doi: 10.1007/s12016-007-0044-5
- Byrd AL, Deming C, Cassidy SK, et al. Staphylococcus aureus and Staphylococcus epidermidis strain diversity underlying pediatric atopic dermatitis. Sci Transl Med. 2017;9(397):eaal4651. doi: 10.1126/scitranslmed.aal4651
- Chng KR, Tay AS, Li C, et al. Whole metagenome profiling reveals skin microbiome-dependent susceptibility to atopic dermatitis flare. Nat Microbiol. 2016;1(9):16106. doi: 10.1038/nmicrobiol.2016.106
- Hanski I, von Hertzen L, Fyhrquist N, et al. Environmental biodiversity, human microbiota, and allergy are interrelated. Proc Natl Acad Sci USA. 2012;109(21):8334–8339. doi: 10.1073/pnas.1205624109
- Nakamura Y, Oscherwitz J, Cease KB, et al. Staphylococcus δ-toxin induces allergic skin disease by activating mast cells. Nature. 2013;503(7476):397–401. doi: 10.1038/nature12655
- Niebuhr M, Gathmann M, Scharonow H, et al. Staphylococcal alpha-toxin is a strong inducer of interleukin-17 in humans. Infect Immun. 2011;79(4):1615–1622. doi: 10.1128/IAI.00958-10
- Kaesler S, Skabytska Y, Chen KM, et al. Staphylococcus aureus-derived lipoteichoic acid induces temporary T-cell paralysis independent of Toll-like receptor 2. J Allergy Clin Immunol. 2016;138(3):780–790.e6. doi: 10.1016/j.jaci.2015.11.043
- Nakatsuji T, Chen TH, Two AM, et al. Staphylococcus aureus exploits epidermal barrier defects in atopic dermatitis to trigger cytokine expression. J Invest Dermatol. 2016;136(11):2192–2200. doi: 10.1016/j.jid.2016.05.127
- Miajlovic H, Fallon PG, Irvine AD, Foster TJ. Effect of filaggrin breakdown products on growth of and protein expression by Staphylococcus aureus. J Allergy Clin Immunol. 2010;126(6): 1184–90.e3. doi: 10.1016/j.jaci.2010.09.015
- Leung DY, Harbeck R, Bina P, et al. Presence of IgE antibodies to Staphylococcal exotoxins on the skin of patients with atopic dermatitis. Evidence for a new group of allergens. J Clin Invest. 1993;92(3):1374–1380. doi: 10.1172/JCI116711
- Reginald K, Westritschnig K, Werfel T, et al. Immunoglobulin E antibody reactivity to bacterial antigens in atopic dermatitis patients. Clin Exp Allergy. 2011;41(3):357–369. doi: 10.1111/j.1365-2222.2010.03655.x
- Geoghegan JA, Irvine AD, Foster TJ. Staphylococcus aureus and atopic dermatitis: A complex and evolving relationship. Trends Microbiol. 2018;26(6):484–497. doi: 10.1016/j.tim.2017.11.008
- Simpson EL. Comorbidity in atopic dermatitis. Curr Dermatol Rep. 2012;1(1):29–38. doi: 10.1007/s13671-011-0003-5
- Glatz M, Bosshard PP, Hoetzenecker W, Schmid-Grendelmeier P. The role of Malassezia spp. in atopic dermatitis. J Clin Med. 2015; 4(6):1217–1228. doi: 10.3390/jcm4061217
- Roesner LM, Werfel T. Autoimmunity (or not) in atopic dermatitis. Front Immunol. 2019;10:2128. doi: 10.3389/fimmu.2019.02128
- Badloe FM, de Vriese S, Coolens K, et al. IgE autoantibodies and autoreactive T cells and their role in children and adults with atopic dermatitis. Clin Transl Allergy. 2020;10:34. doi: 10.1186/s13601-020-00338-7
- Pellefigues C. IgE autoreactivity in atopic dermatitis: Paving the road for autoimmune diseases? Antibodies (Basel). 2020;9(3):47. doi: 10.3390/antib9030047
- Sircar G, Bhowmik M, Sarkar RK, et al. Molecular characterization of a fungal cyclophilin allergen Rhi o 2 and elucidation of antigenic determinants responsible for IgE-cross-reactivity. J Biol Chem. 2020;295(9):2736–2748. doi: 10.1074/jbc.RA119.011659
- Agaphonova EE, Dvoryankova NV, Dobriyan ZF, Korsunskaya IM. Therapy of chronic dermatoses, complicated by Candida infection. Terra Medica. 2006;(1):34–35. (In Russ).
- Wong IT, Tsuyuki RT, Cresswell-Melville A, et al. Guidelines for the management of atopic dermatitis (eczema) for pharmacists. Can Pharm J (Ott). 2017;150(5):285–297. doi: 10.1177/1715163517710958
- Silina LV, Shvarts NE. Skin microbiome in case of microbial eczema. Russ J Clin Dermatol Venereol. 2019;18(1):49–54. (In Russ.). doi: 10.17116/klinderma20191801149
- Khaldin AA, Zhukova OV. Open randomized controlled trial to study the effectiveness and safety of domestic (Russian) versus foreign multicomponent topical preparations for the treatment of eczema. Russ J Clin Dermatol Venereol. 2019;18(3):327–337. (In Russ.). doi: 10.17116/klinderma201918031327
- Kong HH, Oh J, Deming C, et al. Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. Genome Res. 2012;22(5):850–859. doi: 10.1101/gr.131029.111
- Roberts JK, Moore CD, Ward RM, et al. Metabolism of beclomethasone dipropionate by cytochrome P450 3A enzymes. J Pharmacol Exp Ther. 2013;345(2):308–316. doi: 10.1124/jpet.112.202556
- Guidance on Prescribing. In: British National Formulary No 60. London: British Medical Association and Royal Pharmaceutical Society of Great Britain; 2010.
- Samtsov AV, Khairutdinov VR, Belousova IE. Etiopathogenetic therapy of inflammatory dermatoses. Bulletin of Dermatology and Venereology. 2018;94(2):78–83. (In Russ). doi: 10.25208/0042-4609-2018-94-2-78-83
- Kozlov SN, Kozlov RS. Modern antimicrobial chemotherapy: A guide for physicians. Moscow: Meditsinskoe informatsionnoe agentstvo; 2017. 397 р. (In Russ).
- Filimonkova NN, Bahlykova EA. Combined topical therapy of chronic dermatoses. Vestnik Dermatologii i Venerologii. 2015;(3): 147–152. (In Russ).