Diagnostic and prognostic value of biomarkers in atopic dermatitis for assessing its endotypes, phenotypes, and treatment efficacy

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Abstract

Atopic dermatitis is a highly heterogeneous disease that usually requires a tailored approach to therapy. Recent studies have described a variety of biomarkers linked to diverse pathophysiological aspects of atopic dermatitis. Furthermore, they have provided encouraging evidence supporting high clinical importance of these biomarkers as promising tools for personalized diagnosis, assessment of disease severity, and monitoring of treatment efficacy. This review aims to provide a comprehensive summary of research progress on atopic dermatitis biomarkers, their diagnostic and prognostic value, as well as the benefits they might potentially offer not only for determining the disease endotype, but also for developing novel management strategies. The implementation of easily accessible and simple methods to measure atopic dermatitis biomarkers into clinical practice is an ambitious task for allergologists and dermatologists. A detailed overview of currently available data will allow us to identify the most important trajectories for future research in this area that will promote the concept of personalized atopic dermatitis therapy, reduce the disease burden, and improve the quality of life of patients.

About the authors

Olga G. Elisyutina

National Research Center ― Institute of Immunology Federal Medical-Biological Agency of Russia

Email: el-olga@yandex.ru
ORCID iD: 0000-0002-4609-2591
SPIN-code: 9567-1894

MD, Dr. Sci.(Med.)

Russian Federation, Moscow

Elena S. Fedenko

National Research Center ― Institute of Immunology Federal Medical-Biological Agency of Russia

Email: efedks@gmail.com
ORCID iD: 0000-0003-3358-5087
SPIN-code: 5012-7242

MD, Dr. Sci.(Med.), Professor

Russian Federation, Moscow

Eugeniy V. Smolnikov

National Research Center ― Institute of Immunology Federal Medical-Biological Agency of Russia; Peoples' Friendship University of Russia

Email: qwertil2010@yandex.ru
ORCID iD: 0000-0003-1302-4178
SPIN-code: 4874-8100
Russian Federation, Moscow; Moscow

Olga A. Ignatyeva

Peoples' Friendship University of Russia

Email: ignatyevaolga@rambler.ru
ORCID iD: 0000-0003-2020-4206
SPIN-code: 1817-9028

Cand. Sci. (Biol.)

Russian Federation, Moscow

Musa R. Khaitov

National Research Center ― Institute of Immunology Federal Medical-Biological Agency of Russia; Peoples' Friendship University of Russia; The Russian National Research Medical University named after N.I. Pirogov

Author for correspondence.
Email: mr.khaitov@nrcii.ru
ORCID iD: 0000-0003-4961-9640
SPIN-code: 3199-9803

MD, Dr. Sci. (Med.), Professor, Corresponding member of the Russian Academy of Sciences

Russian Federation, Moscow; Moscow; Moscow

References

  1. Weidinger S, Novak N. Atopic dermatitis. Lancet. 2016;387(10023):1109–1122. doi: 10.1016/S0140-6736(15)00149-X
  2. Kubanov AA, Namazova-Baranova LS, Khaitov RM, et al. Atopic dermatitis. Russ Allergol J. 2021;18(3):44–92. doi: 10.36691/RJA1474
  3. Barbarot S, Auziere S, Gadkari A, et al. Epidemiology of atopic dermatitis in adults: Results from an international survey. Allergy. 2018;73(6):1284–1293. doi: 10.1111/all.13401
  4. Megna M, Patruno C, Balato A, et al. An Italian multicentre study on adult atopic dermatitis: Persistent versus adult-onset disease. Arch Dermatol Res. 2017;309(6):443–452. doi: 10.1007/s00403-017-1739-y
  5. Oliveira C, Torres T. More than skin deep: The systemic nature of atopic dermatitis. Eur J Dermatol. 2019;29(3):250–258. doi: 10.1684/ejd.2019.3557
  6. Renert-Yuval Y, Guttman-Yassky E. What's new in atopic dermatitis. Dermatol Clin. 2019;37(2):205–213. doi: 10.1016/j.det.2018.12.007
  7. Hammad H, Lambrecht BN. Barrier epithelial cells and the control of type 2 immunity. Immunity. 2015;43(1):29–40. doi: 10.1016/j.immuni.2015.07.007
  8. Gittler JK, Shemer A, Suárez-Fariñas M, et al. Progressive activation of T(h)2/T(h)22 cytokines and selective epidermal proteins characterizes acute and chronic atopic dermatitis. J Allergy Clin Immunol. 2012;130(6):1344–1354. doi: 10.1016/j.jaci.2012.07.012
  9. Gandhi NA, Bennett BL, Graham NM, et al. Targeting key proximal drivers of type 2 inflammation in disease. Nat Rev Drug Discov. 2016;15(1):35–50. doi: 10.1038/nrd4624
  10. Sims JT, Chang CY, Higgs RE, et al. Insights into adult atopic dermatitis heterogeneity derived from circulating biomarker profiling in patients with moderate-to-severe disease. Exp Dermatol. 2021;30(11):1650–1661. doi: 10.1111/exd.14389
  11. Gewiss C, Augustin M. Recent insights into comorbidities in atopic dermatitis. Expert Rev Clin Immunol. 2023;19(4):393–404. doi: 10.1080/1744666X.2023.2181790
  12. Beck LA, Cork MJ, Amagai M, et al. Type 2 inflammation contributes to skin barrier dysfunction in atopic dermatitis. JID Innov. 2022;2(5):100131. doi: 10.1016/j.xjidi.2022.100131
  13. Itamura MY. Involvement of atopic dermatitis in the development of systemic inflammatory diseases. Int J Mol Sci. 2022;23(21):13445. doi: 10.3390/ijms232113445
  14. Wollenberg A, Kinberger M, Arents B, et al. European guideline (EuroGuiDerm) on atopic eczema, part I. Systemic therapy. J Eur Acad Dermatol Venereol. 2022;36(9):1409–1431. doi: 10.1111/jdv.18345
  15. Wollenberg A, Kinberger M, Arents B, et al. European guideline (EuroGuiDerm) on atopic eczema, part II: Non-systemic treatments and treatment recommendations for special AE patient populations. J Eur Acad Dermatol Venereol. 2022;36(11):1904–1926. doi: 10.1111/jdv.18429
  16. Simpson EL, Bieber T, Guttman-Yassky E, et al. Two Phase 3 Trials of dupilumab versus placebo in atopic dermatitis. New Engl J Med. 2016;375(24):2335–2348. doi: 10.1056/NEJMoa1610020
  17. Blauvelt A, de Bruin-Weller M, Gooderham M, et al. Long-term management of moderate-to-severe atopic dermatitis with dupilumab and concomitant topical corticosteroids (LIBERTY AD CHRONOS): A 1-year, randomised, double-blinded, placebo-controlled, phase 3 trial. Lancet. 2017;389(10086):2287–2303. doi: 10.1016/S0140-6736(17)31191-1
  18. De Bruin-Weller M, Thaçi D, Smith CH, et al. Dupilumab with concomitant topical corticosteroid treatment in adults with atopic dermatitis with an inadequate response or intolerance to ciclosporin A or when this treatment is medically inadvisable: A placebo-controlled, randomized phase III clinical trial (LIBERTY AD CAFÉ). Brit J Dermatol. 2018;178(5):1083–1101. doi: 10.1111/bjd.16156
  19. Thaçi D, Simpson LE, Deleuran M, et al. Efficacy and safety of dupilumab monotherapy in adults with moderate-to-severe atopic dermatitis: A pooled analysis of two phase 3 randomized trials (LIBERTY AD SOLO 1 and LIBERTY AD SOLO 2). J Dermatol Sci. 2019;94(2):266–275. doi: 10.1016/j.jdermsci.2019.02.002
  20. Cork MJ, Eckert L, Simpson EL, et al. Dupilumab improves patient-reported symptoms of atopic dermatitis, symptoms of anxiety and depression, and health-related quality of life in moderate-to-severe atopic dermatitis: Analysis of pooled data from the randomized trials SOLO 1 and SOLO 2. J Dermatol Treat. 2020;31(6):606–614. doi: 10.1080/09546634.2019.1612836
  21. Reich K, Teixeira HD, de Bruin-Weller M, et al. Safety and efficacy of upadacitinib in combination with topical corticosteroids in adolescents and adults with moderate-to-severe atopic dermatitis (AD Up): Results from a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet. 2021;397(10290):2169–2181. doi: 10.1016/S0140-6736(21)00589-4
  22. Reich K, Teixeira HD, de Bruin-Weller M, et al. Upadacitinib plus topical corticosteroids in atopic dermatitis: Week 52 AD Up study results. J Allergy Clin Immunol. 2022;149(3):977–987.e14. doi: 10.1016/j.jaci.2021.07.036
  23. Simpson EL, Sinclair R, Forman S, et al. Efficacy and safety of abrocitinib in adults and adolescents with moderate-to-severe atopic dermatitis (JADE MONO-1): A multicentre, double-blind, randomised, placebo-controlled, phase 3 trial. Lancet. 2020;396(10246):255–266. doi: 10.1016/S0140-6736(20)30732-7
  24. Silverberg JI, Simpson EL, Thyssen JP, et al. Efficacy and safety of abrocitinib in patients with moderate-to-severe atopic dermatitis: A randomized clinical trial. JAMA Dermatol. 2020;156(8):863–873. doi: 10.1001/jamadermatol.2020.1406
  25. Bieber T, Simpson EL, Silverberg JI, et al. Abrocitinib versus placebo or dupilumab for atopic dermatitis. New Engl J Med. 2021;384(12):1101–1112. doi: 10.1056/NEJMoa2019380
  26. Eczemacouncil.org [Internet]. Chicago: International Eczema Council, Inc. Available from: https://www.eczemacouncil.org/. Accessed: 15.11.2023.
  27. Hanifin JM, Rajka G. Diagnostic features of atopic dermatitis. Acta Derm Venereol. 1980;60(Suppl 92):44–47. doi: 10.2340/00015555924447
  28. Ferreira MA, Vonk JM, Baurecht H, et al. Shared genetic origin of asthma, hay fever and eczema elucidates allergic disease biology. Nat Genet. 2017;49(12):1752–1757. doi: 10.1038/ng.3985
  29. Palmer CN, Irvine AD, Terron-Kwiatkowski A, et al. Common loss-of-function variants of the epidermal barrier protein filaggrin are a major predisposing factor for atopic dermatitis. Nat Genet. 2006;38(4):441–446. doi: 10.1038/ng1767
  30. Ruether A, Stoll M, Schwarz T, et al. Filaggrin loss-of-function variant contributes to atopic dermatitis risk in the population of Northern Germany. Brit J Dermatol. 2006;155(5):1093–1094. doi: 10.1111/j.1365-2133.2006.07500.x
  31. Irvine AD, McLean WH, Leung DY, et al. Filaggrin mutations associated with skin and allergic diseases. New Engl J Med. 2011;365(14):1315–1327. doi: 10.1056/NEJMra1011040
  32. Stefansson K, Brattsand M, Roosterman D, et al. Activation of proteinase-activated receptor-2 by human kallikrein-related peptidases. J Invest Dermatol. 2008;128(1):18–25. doi: 10.1038/sj.jid.5700965
  33. Vasilopoulos Y, Cork MJ, Teare D, et al. A nonsynonymous substitution of cystatin A, a cysteine protease inhibitor of house dust mite protease, leads to decreased mRNA stability and shows a significant association with atopic dermatitis. Allergy. 2007;62(5):514–519. doi: 10.1111/j.1398-9995.2007.01350.x
  34. Elias PM, Eichenfield LF, Fowler JF, et al. Update on the structure and function of the skin barrier: Atopic dermatitis as an exemplar of clinical implications. Semin Cutan Med Surg. 2013;32(Suppl 2):S21–24. doi: 10.12788/j.sder.0022
  35. Hershey GK, Friedrich MF, Esswein LA, et al. The association of atopy with a gain-of-function mutation in the alpha subunit of the interleukin-4 receptor. New Engl J Med. 1997;337(24):1720–1725. doi: 10.1056/NEJM199712113372403
  36. Novak N, Kruse S, Potreck J, et al. Single nucleotide polymorphisms of the IL-18 gene are associated with atopic eczema. J Allergy Clin Immunol. 2005;115(4):828–833. doi: 10.1016/j.jaci.2005.01.030
  37. Stephan W, Christian G, Elke R, et al. Genome-wide scan on total serum IgE levels identifies FCER1A as novel susceptibility locus. PLoS Genet. 2008;4(8):e1000166. doi: 10.1371/journal.pgeN1000166
  38. Zhou J, Zhou Y, Lin LH, et al. Association of polymorphisms in the promoter region of FCER1A gene with atopic dermatitis, chronic urticaria, asthma, and serum immunoglobulin E levels in a Han Chinese population. Hum Immunol. 2012;73(3):301–305. doi: 10.1016/j.humimm.2011.12.001
  39. Ahmad-Nejad P, Mrabet-Dahbi S, Breuer K, et al. The toll-like receptor 2 R753Q polymorphism defines a subgroup of patients with atopic dermatitis having severe phenotype. J Allergy Clin Immunol. 2004;113(3):565–567. doi: 10.1016/j.jaci.2003.12.583
  40. Novak N, Yu CF, Bussmann C, et al. Putative association of a TLR9 promoter polymorphism with atopic eczema. Allergy. 2007;62(7):766–772. doi: 10.1111/j.1398-9995.2007.01358.x
  41. He H, Bissonnette R, Wu J, et al. Tape strips detect distinct immune and barrier profiles in atopic dermatitis and psoriasis. J Allergy Clin Immunol. 2021;147(1):199–212. doi: 10.1016/j.jaci.2020.05.048
  42. 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
  43. Reginald K, Westritschnig K, Werfel T, et al. The Malassezia genus in skin and systemic diseases. Clin Microbiol Rev. 2012;25(1):106–141. doi: 10.1128/CMR.00021-11
  44. Benet M, Albang R, Pinart M, et al. Integrating clinical and epidemiologic data on allergic diseases across birth cohorts: A harmonization study in the mechanisms of the development of allergy project. Am J Epidemiol. 2019;188(2):408–417. doi: 10.1093/aje/kwy242
  45. Kjaer HF, Eller E, Andersen KE, et al. The association between early sensitization patterns and subsequent allergic disease. The DARC birth cohort study. Pediatr Allergy Immunol. 2009;20(8):726–734. doi: 10.1111/j.1399-3038.2009.00862.x
  46. Eller E, Kjaer HF, Høst A, et al. Food allergy and food sensitization in early childhood: Results from the DARC cohort. Allergy. 2009;64(7):1023–1029. doi: 10.1111/j.1398-9995.2009.01952.x
  47. González-Pérez R, Poza-Guedes P, Pineda F, et al. House dust mite Precision Allergy Molecular Diagnosis (PAMD) in the Th2-prone atopic dermatitis endotype. Life (Basel, Switzerland). 2021;11(12):1418. doi: 10.3390/life11121418
  48. Broeks SA, Brand PL. Atopic dermatitis is associated with a fivefold increased risk of polysensitisation in children. Acta Paediat. 2017;106(3):485–488. doi: 10.1111/apa.13729
  49. Shtyrbul OV. Significance of molecular allergodiagnostics in personalised management of patients with atopic dermatitis: 14.03.09: 14.01.10; place of defence: State Scientific Centre "Institute of Immunology" [dissertation abstract]. Moscow; 2020. 24 р. (In Russ).
  50. Elisyutina OG, Fedenko ES, Smolnikov EV, et al. Significance of component allergodiagnostics in determining indications for allergen-specific immunotherapy in patients with atopic dermatitis. Russ J Allergol. 2022;19(4):519–533. doi: 10.36691/RJA1588
  51. Roesner LM, Werfel T. Autoimmunity (or Not) in Atopic Dermatitis. Fron Immunol. 2019;10:2128. doi: 10.3389/fimmu.2019.02128
  52. Futamura K, Matsumoto K. Epicutaneous sensitization in patients with atopic dermatitis. Pediatr Allergy Immunol Pulmonol. 2016;29(4):170–173. doi: 10.1089/ped.2016.0716
  53. Kubo A, Nagao K, Amagai M, et al. Epidermal barrier dysfunction and cutaneous sensitization in atopic diseases. J Clin Invest. 2012;122(2):440–447. doi: 10.1172/JCI57416
  54. Wassmann-Otto A, Heratizadeh A, Wichmann K, et al. Birch pollen-related foods can cause late eczematous reactions in patients with atopic dermatitis. Allergy. 2018;73(10):2046–2054. doi: 10.1111/all.13454
  55. Fölster-Holst R, Galecka J, Weißmantel S, et al. Birch pollen influence the severity of atopic eczema: Prospective clinical cohort pilot study and ex vivo penetration study. Clin Cosmet Investig Dermatol. 2015;29(8):539–548. doi: 10.2147/CCID.S81700
  56. Shershakova N, Bashkatova E, Babakhin A, et al. Allergen-specific immunotherapy with monomeric allergoid in a mouse model of atopic dermatitis. PLoS One. 2015;10(8):e0135070. doi: 10.1371/journal.pone.0135070
  57. Werfel T, Allam JP, Biedermann T, et al. Cellular and molecular immunologic mechanisms in patients with atopic dermatitis. J Allergy Clin Immunol. 2016;138(2):336–349. doi: 10.1016/j.jaci.2016.06.010
  58. Heratizadeh A. Atopic dermatitis: New evidence on the role of allergic inflammation. Curr Opin Allergy Clin Immunol. 2016;16(5):458–464. doi: 10.1097/ACI.0000000000000308
  59. Fadadu RP, Abuabara K, Balmes JR, et al. Air pollution and atopic dermatitis, from molecular mechanisms to population-level evidence: A review. Int J Environ Res Public Health. 2023;20(3):2526. doi: 10.3390/ijerph20032526
  60. Kim YM, Kim J, Han Y, et al. Short-term effects of weather and air pollution on atopic dermatitis symptoms in children: A panel study in Korea. PLoS One. 2017;12(4):e0175229. doi: 10.1371/journal.pone.0175229
  61. Sargen MR, Hoffstad O, Margolis DJ. Warm, humid, and high sun exposure climates are associated with poorly controlled eczema: PEER (Pediatric Eczema Elective Registry) cohort, 2004–2012. J Invest Dermatol. 2014;134(1):51–57. doi: 10.1038/jid.2013.274
  62. Silverberg JI, Hanifin J, Simpson EL. Climatic factors are associated with childhood eczema prevalence in the United States. J Invest Dermatol. 2013;133(7):1752–1759. doi: 10.1038/jid.2013.19
  63. Hankinson O. The aryl hydrocarbon receptor complex. Ann Rev Pharmacol Toxicol. 1995;(35):307–340. doi: 10.1146/annurev.pa.35.040195.001515
  64. Murota H, Izumi M, Abd El-Latif MI, et al. Artemin causes hypersensitivity to warm sensation, mimicking warmth-provoked pruritus in atopic dermatitis. J Allergy Clin Immunol. 2012;130(3):671–682. doi: 10.1016/j.jaci.2012.05.027
  65. Hidaka T, Ogawa E, Kobayashi EH, et al. The aryl hydrocarbon receptor AhR links atopic dermatitis and air pollution via induction of the neurotrophic factor artemin. Nat Immunol. 2017;18(1):64–73. doi: 10.1038/ni.3614
  66. Afaq F, Zaid MA, Pelle E, et al. Aryl hydrocarbon receptor is an ozone sensor in human skin. J Invest Dermatol. 2009;129(10):2396–2403. doi: 10.1038/jid.2009.85
  67. Vogeley C, Kress S, Lang D, et al. A gene variant of AKR1C3 contributes to interindividual susceptibilities to atopic dermatitis triggered by particulate air pollution. Allergy. 2023;78(5):1372–1375. doi: 10.1111/all.15622
  68. Niwa Y, Sumi H, Kawahira K, et al. Protein oxidative damage in the stratum corneum: Evidence for a link between environmental oxidants and the changing prevalence and nature of atopic dermatitis in Japan. Brit J Dermatol. 2003;149(2):248–254. doi: 10.1046/j.1365-2133.2003.05417.x
  69. Schnass W, Hüls A, Vierkötter A, et al. Traffic-related air pollution and eczema in the elderly: Findings from the SALIA cohort. Int J Hygiene Environ Health. 2018;221(6):861–867. doi: 10.1016/j.ijheh.2018.06.002
  70. Krämer U, Sugiri D, Ranft U, et al. Eczema, respiratory allergies, and traffic-related air pollution in birth cohorts from small-town areas. J Dermatol Sci. 2009;56(2):99–105. doi: 10.1016/j.jdermsci.2009.07.014
  71. Aguilera I, Pedersen M, Garcia-Esteban R, et al. Early-life exposure to outdoor air pollution and respiratory health, ear infections, and eczema in infants from the INMA study. Environ Health Perspect. 2013;121(3):387–392. doi: 10.1289/ehp.1205281
  72. Asher MI, Stewart AW, Mallol J, et al. Which population level environmental factors are associated with asthma, rhinoconjunctivitis and eczema? Review of the ecological analyses of ISAAC Phase One. Respirat Res. 2010;11(1):8. doi: 10.1186/1465-9921-11-8
  73. Lehmann I, Rehwagen M, Diez U, et al. Enhanced in vivo IgE production and T cell polarization toward the type 2 phenotype in association with indoor exposure to VOC: Results of the LARS study. Int J Hyg Environ Health. 2001;204(4):211–221. doi: 10.1078/1438-4639-00100
  74. Lehmann I, Thoelke A, Rehwagen M, et al. The influence of maternal exposure to volatile organic compounds on the cytokine secretion profile of neonatal T cells. Environ Toxicol. 2002;17(3):203–210. doi: 10.1002/tox.10055
  75. Aslam I, Roeffaers MB. Carbonaceous nanoparticle air pollution: Toxicity and detection in biological samples. Nanomaterials. 2022;12(22):3948. doi: 10.3390/nano12223948
  76. Busch W, Kühnel D, Schirmer K, et al. Tungsten carbide cobalt nanoparticles exert hypoxia-like effects on the gene expression level in human keratinocytes. BMC Genom. 2010;11:65. doi: 10.1186/1471-2164-11-65
  77. Wollenberg A, Christen-Zäch S, Taieb A, et al. ETFAD/EADV Eczema task force 2020 position paper on diagnosis and treatment of atopic dermatitis in adults and children. J Eur Acad Dermatol Venereol. 2020;34(12):2717–2744. doi: 10.1111/jdv.16892
  78. Hijnen D, Knol EF, Gent YY, et al. CD8(+) T cells in the lesional skin of atopic dermatitis and psoriasis patients are an important source of IFN-γ, IL-13, IL-17, and IL-22. J Invest Dermatol. 2013;133(4):973–979. doi: 10.1038/jid.2012.456
  79. Czarnowicki T, Gonzalez J, Bonifacio KM, et al. Diverse activation and differentiation of multiple B-cell subsets in patients with atopic dermatitis but not in patients with psoriasis. J Allergy Clin Immunol. 2016;137(1):118–129.e5. doi: 10.1016/j.jaci.2015.08.027
  80. Hwang ST. Mechanisms of T-cell homing to skin. Adv Dermatol. 2001;(17):211–241.
  81. Bieber T. The pro- and anti-inflammatory properties of human antigen-presenting cells expressing the high affinity receptor for IgE (Fc epsilon RI). Immunobiology. 2007;212(6):499–503. doi: 10.1016/j.imbio.2007.03.001
  82. Leyva-Castillo JM, McGurk A, Geha MD. Allergic skin inflammation and S. aureus skin colonization are mutually reinforcing. Clin Immunol. 2020;(218):108511. doi: 10.1016/j.clim.2020.108511
  83. Oetjen LK, Mack MR, Feng J, et al. Sensory neurons co-opt classical immune signaling pathways to mediate chronic itch. Cell. 2017;171(1):217–228.e13. doi: 10.1016/j.cell.2017.08.006
  84. He H, Del Duca E, Diaz A, et al. Mild atopic dermatitis lacks systemic inflammation and shows reduced nonlesional skin abnormalities. J Allergy Clin Immunol. 2021;147(4):1369–1380. doi: 10.1016/j.jaci.2020.08.041
  85. Simon D, Aeberhard C, Erdemoglu Y, et al. Th17 cells and tissue remodeling in atopic and contact dermatitis. Allergy. 2014;69(1):125–131. doi: 10.1111/all.12351
  86. Noda S, Suárez-Fariñas M, Ungar B, et al. The Asian atopic dermatitis phenotype combines features of atopic dermatitis and psoriasis with increased Th17 polarization. J Allergy Clin Immunol. 2015;136(5):1254–1264. doi: 10.1016/j.jaci.2015.08.015
  87. Bratton DL, Hamid Q, Boguniewicz M, et al. Granulocyte macrophage colony-stimulating factor contributes to enhanced monocyte survival in chronic atopic dermatitis. J Clin Invest. 1995;95(1):211–218. doi: 10.1172/JCI117642
  88. Purwar R, Werfel T, Wittmann M, et al. IL-13-stimulated human keratinocytes preferentially attract CD4+CCR4+ T cells: Possible role in atopic dermatitis. J Invest Dermatol. 2006;126(5):1043–1051. doi: 10.1038/sj.jid.5700085
  89. Simon D, Von Gunten S, Borelli S, et al. The interleukin-13 production by peripheral blood T cells from atopic dermatitis patients does not require CD2 costimulation. Int Arch Allergy Immunol. 2003;132(2):148–155. doi: 10.1159/000073716
  90. He R, Oyoshi MK, Garibyan L, et al. TSLP acts on infiltrating effector T cells to drive allergic skin inflammation. Proc Natl Acad Sci USA. 2008;105(33):11875–11880. doi: 10.1073/pnas.0801532105
  91. Soumelis V, Reche PA, Kanzler H, et al. Human epithelial cells trigger dendritic cell mediated allergic inflammation by producing TSLP. Nat Immunol. 2002;3(7):673–680. doi: 10.1038/ni805
  92. Souwer Y, Szegedi K, Kapsenberg ML, et al. IL-17 and IL-22 in atopic allergic disease. Curr Opin Immunol. 2010;22(6):821–826. doi: 10.1016/j.coi.2010.10.013
  93. Janssen EM, Dy SM, Meara AS, et al. Intrinsic atopic dermatitis shows similar Th2 and higher Th17 immune activation compared with extrinsic atopic dermatitis. J Allergy Clin Immunol. 2013;132(2):361–370. doi: 10.1016/j.jaci.2013.04.046
  94. Ungar B, Garcet S, Gonzalez J, et al. An integrated model of atopic dermatitis biomarkers highlights the systemic nature of the disease. J Inves Dermatol. 2017;137(3):603–613. doi: 10.1016/j.jid.2016.09.037
  95. Bao L, Zhang H, Chan LS. The involvement of the JAK-STAT signaling pathway in chronic inflammatory skin disease atopic dermatitis. JAKSTAT. 2013;2(3):e24137. doi: 10.4161/jkst.24137
  96. 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
  97. Leyden JJ, Marples RR, Kligman AM. Staphylococcus aureus in the lesions of atopic dermatitis. Brit J Dermatol. 1974;90(5):525–530. doi: 10.1111/j.1365-2133.1974.tb06447.x
  98. Lin YT, Wang CT, Chiang BL, et al. Role of bacterial pathogens in atopic dermatitis. Clin Rev Allergy Immunol. 2007;33(3):167–177. doi: 10.1007/s12016-007-0044-5
  99. 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
  100. 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):4651. doi: 10.1126/scitranslmed.aal4651
  101. 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
  102. Miajlovic H, Fallon PG, Irvine AD, et al. Effect of filaggrin breakdown products on growth of and protein expression by Staphylococcus aureus. J Allergy Clin Immunol. 2010;126(6):1184–1190. doi: 10.1016/j.jaci.2010.09.015
  103. 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
  104. 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
  105. Totté JE, van der Feltz WT, Hennekam M, et al. Prevalence and odds of Staphylococcus aureus carriage in atopic dermatitis: A systematic review and meta-analysis. Brit J Dermatol. 2016;175(4):687–695. doi: 10.1111/bjd.14566
  106. Cabanillas B, Novak N. Atopic dermatitis and filaggrin. Curr Opin Immunol. 2016;(42):1–8. doi: 10.1016/j.coi.2016.05.002
  107. Glatz M, Bosshard PP, Hoetzenecker W, et al. The role of Malassezia spp. in atopic dermatitis. J Clin Med. 2015;4(6):1217–1228. doi: 10.3390/jcm4061217
  108. Simpson EL, Villarreal M, Jepson B, et al. Patients with atopic dermatitis colonized with Staphylococcus aureus have a distinct phenotype and endotype. J Invest Dermatol. 2018;138(10):2224–2233. doi: 10.1016/j.jid.2018.03.1517
  109. Bosma AL, Ascott A, Iskandar R, et al. Classifying atopic dermatitis: A systematic review of phenotypes and associated characteristics. J Eur Acad Dermatol Venereol. 2022;36(6):807–819. doi: 10.1111/jdv.18008
  110. Elisyutina OG, Litovkina AO, Smolnikov EV, et al. Clinical features of different phenotypes of atopic dermatitis. Russ J Allergol. 2019;16(4):30–41. doi: 10.36691/RAJ.2020.16.4.004
  111. Eichenfield LF, Tom WL, Chamlin SL, et al. Guidelines of care for the management of atopic dermatitis: section 1. Diagnosis and assessment of atopic dermatitis. J Am Acad Dermatol. 2014;70(2):338–351. doi: 10.1016/j.jaad.2013.10.010
  112. Shin YH, Hwang J, Kwon R, et al. Global, regional, and national burden of allergic disorders and their risk factors in 204 countries and territories, from 1990 to 2019: A systematic analysis for the Global Burden of Disease Study 2019. Allergy. 2023;78(8):2232–2254. doi: 10.1111/all.15807
  113. Biomarkers Definitions Working Group. Biomarkers and surrogate endpoints: Preferred definitions and conceptual framework. Clin Pharmacol Therapeut. 2001;69(3):89–95. doi: 10.1067/mcp.2001.113989
  114. Hughes AJ, Tawfik SS, Baruah KP, et al. Tape strips in dermatology research. Brit J Dermatol. 2021;185(1):26–35. doi: 10.1111/bjd.19760
  115. Renert-Yuval Y, Thyssen JP, Bissonnette R, et al. Biomarkers in atopic dermatitis: A review on behalf of the International Eczema Council. J Allergy Clin Immunol. 2021;147(4):1174–1190. doi: 10.1016/j.jaci.2021.01.013
  116. Bieber T, d'Erme AM, Akdis CA, et al. Clinical phenotypes and endophenotypes of atopic dermatitis: Where are we, and where should we go? J Allergy Clin Immunol. 2017;139(4S):S58–S64. doi: 10.1016/j.jaci.2017.01.008
  117. Rosińska-Więckowicz A, Czarnecka-Operacz M, Adamski Z. Selected immunological parameters in clinical evaluation of patients with atopic dermatitis. Postepy Dermatol Alergol. 2016;33(3):211–218. doi: 10.5114/ada.2016.60614
  118. Yoshizawa Y, Nomaguchi H, Izaki S, et al. Serum cytokine levels in atopic dermatitis. Clin Exp Dermatol. 2002;27(3):225–229. doi: 10.1046/j.1365-2230.2002.00987.x
  119. Thijs J, Krastev T, Weidinger S, et al. Biomarkers for atopic dermatitis: A systematic review and meta-analysis. Curr Opin Allergy Clin Immunol. 2015;15(5):453–460. doi: 10.1097/ACI.0000000000000198
  120. Kägi MK, Joller-Jemelka H, Wüthrich B. Correlation of eosinophils, eosinophil cationic protein and soluble interleukin-2 receptor with the clinical activity of atopic dermatitis. Dermatology. 1992;185(2):88–92. doi: 10.1159/000247419
  121. Ariëns LF, van der Schaft J, Bakker DS, et al. Dupilumab is very effective in a large cohort of difficult-to-treat adult atopic dermatitis patients: First clinical and biomarker results from the BioDay registry. Allergy. 2020;75(1):116–126. doi: 10.1111/all.14080
  122. Koning H, Neijens HJ, Baert MR, et al. T cell subsets and cytokines in allergic and non-allergic children. I. Analysis of IL-4, IFN-gamma and IL-13 mRNA expression and protein production. Cytokine. 1997;9(6):416–426. doi: 10.1006/cyto.1996.0184
  123. Szegedi K, Lutter R, Res PC, et al. Cytokine profiles in interstitial fluid from chronic atopic dermatitis skin. J Eur Acad Dermatol Venereol. 2015;29(11):2136–2144. doi: 10.1111/jdv.13160
  124. Sanyal RD, Pavel AB, Glickman J, et al. Atopic dermatitis in African American patients is Th2/Th22-skewed with Th1/Th17 attenuation. Ann Allergy Asthma Immunol. 2019;122(1):99–110. doi: 10.1016/j.anai.2018.08.024
  125. Leung TF, Ma KC, Hon KL, et al. Serum concentration of macrophage-derived chemokine may be a useful inflammatory marker for assessing severity of atopic dermatitis in infants and young children. Pediatr Allergy Immunol. 2003;14(4):296–301. doi: 10.1034/j.1399-3038.2003.00052.x
  126. Hijnen D, De Bruin-Weller M, Oosting B, et al. Serum thymus and activation-regulated chemokine (TARC) and cutaneous T cell-attracting chemokine (CTACK) levels in allergic diseases: TARC and CTACK are disease-specific markers for atopic dermatitis. J Allergy Clin Immunol. 2004;113(2):334–340. doi: 10.1016/j.jaci.2003.12.007
  127. Furukawa H, Takahashi M, Nakamura K, et al. Effect of an antiallergic drug (Olopatadine hydrochloride) on TARC/CCL17 and MDC/CCL22 production by PBMCs from patients with atopic dermatitis. J Dermatol Sci. 2004;36(3):165–172. doi: 10.1016/j.jdermsci.2004.09.001
  128. Yasukochi Y, Nakahara T, Abe T, et al. Reduction of serum TARC levels in atopic dermatitis by topical anti-inflammatory treatments. Asian Pac J Allergy Immunol. 2014;32(3):240–245. doi: 10.12932/AP0419.32.3.2014
  129. Kyoya M, Kawakami T, Soma Y. Serum thymus and activation-regulated chemokine (TARC) and interleukin-31 levels as biomarkers for monitoring in adult atopic dermatitis. J Dermatol Sci. 2014;75(3):204–207. doi: 10.1016/j.jdermsci.2014.06.001
  130. Gohar MK, Atta AH, Nasr MM, Hussein DN. Serum Thymus and Activation Regulated Chemokine (TARC), IL-18 and IL-18 gene polymorphism as associative factors with atopic dermatitis. Egypt J Immunol. 2017;24(2):9–22.
  131. Bogaczewicz J, Malinowska K, Sysa-Jedrzejowska A, Wozniacka A. Medium-dose ultraviolet A1 phototherapy and mRNA expression of TSLP, TARC, IL-5, and IL-13 in acute skin lesions in atopic dermatitis. Int J Dermatol. 2016;55(8):856–863. doi: 10.1111/ijd.12992
  132. Vekaria AS, Brunner PM, Aleisa AI, et al. Moderate-to-severe atopic dermatitis patients show increases in serum C-reactive protein levels, correlating with skin disease activity. F1000Research. 2017;(6):1712. doi: 10.12688/f1000research.12422.2
  133. Morishima Y, Kawashima H, Takekuma K, Hoshika A. Changes in serum lactate dehydrogenase activity in children with atopic dermatitis. Pediatr Int. 2010;52(2):171–174. doi: 10.1111/j.1442-200X.2009.02908.x
  134. Kou K, Aihara M, Matsunaga T, et al. Association of serum interleukin-18 and other biomarkers with disease severity in adults with atopic dermatitis. Arch Dermatol Res. 2012;304(4):305–312. doi: 10.1007/s00403-011-1198-9
  135. Mizawa M, Yamaguchi M, Ueda C, et al. Stress evaluation in adult patients with atopic dermatitis using salivary cortisol. BioMed Res Int. 2013;2013:138027. doi: 10.1155/2013/138027
  136. Kezic S, O'Regan GM, Lutter R, et al. Filaggrin loss-of-function mutations are associated with enhanced expression of IL-1 cytokines in the stratum corneum of patients with atopic dermatitis and in a murine model of filaggrin deficiency. J Allergy Clin Immunol. 2012;129(4):1031–1039. doi: 10.1016/j.jaci.2011.12.989
  137. Khattri S, Shemer A, Rozenblit M, et al. Cyclosporine in patients with atopic dermatitis modulates activated inflammatory pathways and reverses epidermal pathology. J Allergy Clin Immunol. 2014;133(6):1626–1634. doi: 10.1016/j.jaci.2014.03.003
  138. Brunner PM, Pavel AB, Khattri S, et al. Baseline IL-22 expression in patients with atopic dermatitis stratifies tissue responses to fezakinumab. J Allergy Clin Immunol. 2019;143(1):142–154. doi: 10.1016/j.jaci.2018.07.028
  139. Glickman JW, Han J, Garcet S, et al. Improving evaluation of drugs in atopic dermatitis by combining clinical and molecular measures. J Allergy Clin Immunol Pract. 2020;8(10):3622–3625.e19. doi: 10.1016/j.jaip.2020.07.015
  140. Dyjack N, Goleva E, Rios C, et al. Minimally invasive skin tape strip RNA sequencing identifies novel characteristics of the type 2-high atopic dermatitis disease endotype. J Allergy Clin Immunol. 2018;141(4):1298–1309. doi: 10.1016/j.jaci.2017.10.046
  141. Guttman-Yassky E, Diaz A, Pavel AB, et al. Use of tape strips to detect immune and barrier abnormalities in the skin of children with early-onset atopic dermatitis. JAMA Dermatol. 2019;155(12):1358–1370. doi: 10.1001/jamadermatol.2019.2983

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