Effects of Hyperbaric Oxygen Therapy in Children with Severe Atopic Dermatitis

Judyta Mews, Agata Tomaszewska, Jacek Siewiera, Sławomir Lewicki, Karolina Kuczborska, Agnieszka Lipińska-Opałka, Bolesław Kalicki, Judyta Mews, Agata Tomaszewska, Jacek Siewiera, Sławomir Lewicki, Karolina Kuczborska, Agnieszka Lipińska-Opałka, Bolesław Kalicki

Abstract

In the course of atopic dermatitis (AD), the overactivity of the immune system, associated with predominant Th2 lymphocyte responses, is observed, which leads to an increased inflammatory reaction. Cases of a severe course of atopic dermatitis lead to the search for new therapeutic options. The aim of this study was to assess the effects of hyperbaric oxygen therapy (HBOT) treatment for severe cases of AD in children. A total of 15 children with severe AD underwent therapy. The influence of HBOT on the clinical course of AD and immunomodulatory effect of the therapy was analyzed by the SCORAD and objective SCORAD (oSCORAD) scales and by determining the serum concentration of immunological parameters (blood: nTreg lymphocytes, CD4+CD25highCD127-FOXP3+, NKT lymphocytes CD3+, CD16/56+, and serum: total IgE, cytokines IL-4, IL-6, and IL-10, before and after the 30-day treatment cycle). The study showed a significant effect of the therapy on the improvement of the skin condition. In all children, a reduction in the extent and intensity of skin lesions, reduction of redness, swelling, oozing/crusting, scratch marks and skin lichenification after HBOT was observed. Patients also reported a reduction in the intensity of pruritus and an improvement in sleep quality after therapy. In all children, a statistically significant decrease in the serum level of IgE was observed. However, no statistically significant changes in the blood levels of IL-4, IL-6 and IL-10, as well as the percentage of CD4+CD25highCD127-FOXP3+ Treg and NKT lymphocytes, were found. In conclusion, the use of hyperbaric therapy has a positive impact on treatment results in children with a severe course of atopic dermatitis.

Keywords: SCORAD; atopic dermatitis; children; hyperbaric chamber; immune system.

Conflict of interest statement

The authors of the manuscript declare no conflict of interest in relation to this article.

Figures

Figure 1
Figure 1
Treatment profile in a hyperbaric chamber: (A–C) time during which the patient was breathing pure oxygen under hyperbaric conditions with the use of a mask or helmet; (D,E) air brakes aimed at breathing air contained in a hyperbaric chamber without the use of individual oxygen devices. Z—time to full compression. Y—decompression time.
Figure 2
Figure 2
Assessment of the disease activity before and after hyperbaric oxygen therapy (HBOT) with the use of the SCORAD method (p < 0.05).
Figure 3
Figure 3
Assessment of the disease activity before and after HBOT with the use of the objective SCORAD (oSCORAD) method (p < 0.05).
Figure 4
Figure 4
Extent of skin lesions before and after HBOT (p < 0.05).

References

    1. Lyons J., Milner J., Stone K. Atopic dermatitis in children: Clinical features, pathophysiology and treatment. Immunol. Allergy Clin. 2015;35:161–183. doi: 10.1016/j.iac.2014.09.008.
    1. Hanifin J.M., Rajka G. Diagnostic features of atopic dermatitis. Acta Derm. Venereol. 1980;92:44–47.
    1. Bieber T. Atopic dermatitis. Ann. Dermatol. 2010;22:125–137. doi: 10.5021/ad.2010.22.2.125.
    1. Samochocki Z., Alifier M., Bodera P., Jeziorkowska R., Rosiak E., Jurkiewicz B., Glińska O., Gliński W., Stankiewicz W. T-regulatory cells in severe atopic dermatitis: Alterations related to cytokines and other lymphocyte subpopulations. Arch. Dermatol. Res. 2012;304:795–801. doi: 10.1007/s00403-012-1290-9.
    1. Lipińska-Opałka A., Wawrzyniak A., Lewicki S., Zdanowski R., Kalicki B. Evaluation of Immune Indices and Serum Vitamin D Content in Chil-dren with Atopic Dermatitis. Adv. Exp. Med. Biol. 2017;42:101–106.
    1. Chiarelli F., Canfora G., Verrotti A., Amerio P., Morgese G. Humoral and cellular immunity in children with active and quiescent atopic dermati-tis. Br. J. Dermatol. 1980;116:651–660. doi: 10.1111/j.1365-2133.1987.tb05898.x.
    1. Bacchetta R., Gambineri E., Roncarolo M.-G. Role of regulatory T cells and FOXP3 in human diseases. J. Allergy Clin. Immunol. 2007;120:227–235. doi: 10.1016/j.jaci.2007.06.023.
    1. Zhang Y., Zhou B. Functions of Thymic Stromal Lymphopoietin in Immunity and Disease. Immunol. Res. 2012;52:211–223. doi: 10.1007/s12026-012-8264-z.
    1. Wong L.-S., Wu T., Lee C.-H. Inflammatory and Noninflammatory Itch: Implications in Pathophysiology-Directed Treatments. Int. J. Mol. Sci. 2017;18:1485. doi: 10.3390/ijms18071485.
    1. Paprocki J., Gackowska M., Pawłowska M., Woźniak A. The current use of hyperbaric oxygen treatment. Med. Rodz. 2016;19:217–222.
    1. Roekevisch E., Spuls P.I., Kuester D., Limpens J., Schmitt J. Efficacy and safety of systemic treatments for moderate to severe atopic dermatitis: A systematic review. J. Allergy Clin. Immunol. 2014;133:429–437. doi: 10.1016/j.jaci.2013.07.049.
    1. Nowicki R., Trzeciak M., Wilkowska A., Sokołowska-Wojdyło M., Ługowska-Umer H., Barańska-Rybak W., Kaczmarski M., Kowalewski C., Kruszewski J., Maj J., et al. Special paper Atopic dermatitis: Current treatment guidelines. Statement of the experts of the Dermatological Section, Polish Society of Allergology, and the Allergology Section, Polish Society of Dermatology. Adv. Dermatol. Allergol. 2015;4:239–249. doi: 10.5114/pdia.2015.53319.
    1. Wawrzyniak A., Lipińska-Opałka A., Zdanowski R., Lewicki S., Murawski P., Kalicki B. Evaluation of selected immunological parameters and the concentra-tion of vitamin D in children with asthma. Case-control study. Cent Eur. J. Immunol. 2017;42:101–106. doi: 10.5114/ceji.2017.67323.
    1. Bartlet L.B., Westbroek R., White E.J. Sleep patterns in children with atopic eczema. Acta Derm. Venereol. 1997;77:446–448.
    1. Ben-Gashir M.A., Seed P.T., Hay R.J. Are quality of family life and disease severity related in childhood atopic dermatitis? J. Eur. Acad. Dermatol. Venereol. 2002;16:455–462. doi: 10.1046/j.1468-3083.2002.00495.x.
    1. Siewiera J., Mews J., Królikowska K., Kalicki B., Jobs K. Hyperbaric oxygenation in pediatrics: Indications in the light of evidence—Based medicine. Dev. Period Med. 2019;23:142–148.
    1. Mews J., Królikowska K., Siewiera J., Wawrzyniak A., Kalicki B. Assessment of hyperbaric oxygen efficacy in children with carbon monoxide poison-ing. Pediatr. Med. Rodz. 2019;15:157–163. doi: 10.15557/PiMR.2019.0027.
    1. Mathieu D., Marroni A., Kot J. Tenth European Consensus Conference on Hyperbaric Medicine: Recommendations for accept-ed and nonaccepted clinical indications and practice of hyperbaric oxygen treatment. Diving Hyperb. Med. 2017;47:24–32. doi: 10.28920/dhm47.2.131-132.
    1. Edwards M.L. Hyperbaric oxygen therapy. Part 1: History and principles. J. Veter. Emerg. Crit. Care. 2010;20:284–288. doi: 10.1111/j.1476-4431.2010.00535.x.
    1. Edwards M.L. Hyperbaric oxygen therapy. Part 2: Application in disease. J. Veter. Emerg. Crit. Care. 2010;20:289–297. doi: 10.1111/j.1476-4431.2010.00535_1.x.
    1. Dulai P.S., Buckey J.C., Jr., Raffals L.E. Hyperbaric oxygen therapy is well tolerated and effective for ulcerative colitis patients hospitalized for moderate–severe flares: A phase 2A pilot multi-center, randomized, double-blind, sham-controlled trial. Am. J. Gastroenterol. 2018;10:1516–1523. doi: 10.1038/s41395-018-0005-z.
    1. Jeter J.P., Wong E.B. Hyperbaric oxygen therapy in dermatology. Cutis. 2020;105:24–27.
    1. Bennardop L., Del Duca E., Dastoli S., Schipani G., Scali E., Silvestri M., Nisticò S.P., Bennardo L. Potential applications of topical oxygen therapy in dermatology. Dermatol. Pract. Concept. 2018;8:272–276. doi: 10.5826/dpc.0804a04.
    1. Hao Y., Zhang L., Chen Y. Hyperbaric oxygen for the treatment of skin diseases. Chin. J. Dermatol. 2016;49:672–675.
    1. Olszański R., Konarski M., Siermontowski P. Leczenie tlenoterapią hiperbaryczną (HBOT) jako opcja terapeutyczna dla cho-rych na atopowe zapalenie skóry (AZS)—Doświadczenia własne i przegląd piśmiennictwa. Pol. Hyperb. Res. 2017;60:3.
    1. Noval Rivas M., Chatila T. Regulatory T cells in Allergic Diseases. J. Allergy Clin. Immunol. 2016;138:639–652. doi: 10.1016/j.jaci.2016.06.003.
    1. Ulewicz K., Zannini D. On the possibility of hyperbaric oxygen therapy in some pathological reactions of immunological hy-persensitivity. Bull. Inst. Mar. Trop. Med. Gdynia. 1986;37:71–79.
    1. Matsuda J., Mallevaey T., Scott-Browne J., Gapin L. CD1d-restricted iNKT cells, the “Swiss-Army knife” of the immune system. Curr. Opin. Immunol. 2008;20:358–368. doi: 10.1016/j.coi.2008.03.018.
    1. Scordamaglia F., Balsamo M., Scordamaglia A., Moretta A., Mingari M.C., Canonica G.W., Moretta L., Vitale M. Perturbations of natural killer cell regulatory functions in respiratory aller-gic diseases. J. Allergy Clin. Immunol. 2008;121:479–485. doi: 10.1016/j.jaci.2007.09.047.
    1. Stelmaszczyk-Emmel A., Zawadzka-Krajewska A., Szypowska A., Kulus M., Demkow U. Frequency and activation of CD4+CD25 FoxP3+ regu-latory T cells in peripheral blood from children with atopic allergy. Int. Arch. Allergy Immunol. 2013;162:16–24. doi: 10.1159/000350769.
    1. Lee J.-H., Yu H.-H., Wang L.-C., Yang Y.-H., Lin Y.-T., Chiang B.-L. The levels of CD4+CD25+ regulatory T cells in paediatric patients with allergic rhinitis and bronchial asthma. Clin. Exp. Immunol. 2007;148:53–63. doi: 10.1111/j.1365-2249.2007.03329.x.
    1. Xu G., Mou Z., Jiang H., Cheng L., Shi J., Xu R., Oh Y., Li H. A Possible Role of CD4+CD25+ T Cells as Well as Transcription Factor Foxp3 in the Dysregulation of Allergic Rhinitis. Laryngoscope. 2007;117:876–880. doi: 10.1097/MLG.0b013e318033f99a.
    1. De Vries J.E. Immunosuppressive and anti-inflammatory properties of IL-10. Ann. Med. 1995;27:537–541. doi: 10.3109/07853899509002465.
    1. Nedoszytko B., Lange M., Sokołowska-Wojdyło M., Renke J., Trzonkowski P., Sobjanek M., Szczerkowska-Dobosz A., Niedoszytko M., Górska A., Romantowski J., et al. The role of regulatory T cells and genes involved in their differentia-tion in pathogenesis of selected inflammatory and neoplastic skin diseases. Part II: The Treg role in skin diseases pathogenesis. Adv. Dermatol. Allergol. 2017;34:405–417. doi: 10.5114/ada.2017.71105.
    1. Schnopp C., Rad R., Weidinger A., Weidinger S., Ring J., Eberlein B., Ollert M., Mempel M. Fox-P3-positive regulatory T cells are present in the skin of generalized atopic eczema patients and are not particulary affected by medium-dose UVA1 therapy. Photodermatol. Photoimmunol. Photomed. 2007;23:81–85. doi: 10.1111/j.1600-0781.2007.00284.x.
    1. Verhagen J., Akdis M., Traidl-Hoffmann C., Schmid-Grendelmeier P., Hijnen D., Knol E.F., Behrendt H., Blaser K., Akdis C.A. Absence of T-regulatory cell expression and function in atopic dermatitis skin. J. Allergy Clin. Immunol. 2006;117:176–183. doi: 10.1016/j.jaci.2005.10.040.
    1. Di Cesare A., Di Meglio P., Nestle F.O. A role for Th17 cells in the immunopathogenesis of atopic dermatitis? J. Investig. Dermatol. 2008;128:2569–2571. doi: 10.1038/jid.2008.283.
    1. Butler G., Michaels J.C., Al-Waili N., Finkelstein M., Allen M., Petrillo R., Carrey Z., Kolanuvada B., Lee B.Y., Riera A.G., et al. Therapeutic effect of hyperbaric oxygen in psoriasis vulgaris: Two case reports and a review of the literature. J. Med. Case Rep. 2009;3:7023. doi: 10.1186/1752-1947-0003-0000007023.
    1. Kindwall E.P., Whelan H.T. Hiperbaric Medicine Practice. Best Publishing Company; North Palm Beach, FL, USA: 2008.
    1. Kranke P., Bennett M.H., Martyn-St James M., Schnabel A., Debus S.E., Weibel S. Hyperbaric oxygen therapy for chronic wounds. Ochr. Database Syst. Rev. 2015;6:CD004123. doi: 10.1002/14651858.CD004123.pub4.
    1. Kraaij M.D., Savage N.D.L., Van Der Kooij S.W., Koekkoek K., Wang J., Berg J.M.V.D., Ottenhoff T.H.M., Kuijpers T.W., Holmdahl R., Van Kooten C., et al. Induction of regulatory T cells by macrophages is dependent on production of reactive oxygen species. Proc. Natl. Acad. Sci. USA. 2010;107:17686–17691. doi: 10.1073/pnas.1012016107.
    1. Dang E.V., Barbi J., Yang H.Y., Jinasena D., Yu H., Zheng Y., Bordman Z., Fu J., Kim Y., Yen H.R., et al. Control of T(H)17/T(reg) balance by hypoxia-inducible factor 1. Cell. 2011;146:772–784. doi: 10.1016/j.cell.2011.07.033.
    1. Dennog C., Radermacher P., Barnett A.Y., Speit G. Antioxidant status in humans after exposure to hyperbaric oxygen. Mutat. Res. Mol. Mech. Mutagen. 1999;428:83–89. doi: 10.1016/S1383-5742(99)00034-4.
    1. Saito K., Tanaka Y., Ota T., Eto S., Yamashita U. Suppressive effect of hyperbaric oxygenation on immune responses of normal and autoim-mune mice. Clin. Exp. Immunol. 1991;86:322–327. doi: 10.1111/j.1365-2249.1991.tb05817.x.
    1. Hultqvist M., Olsson L.M., Gelderman K.A., Holmdahl R. The protective role of ROS in autoimmune disease. Trends Immunol. 2009;30:201–208. doi: 10.1016/j.it.2009.03.004.
    1. Thom S.R. Hyperbaric oxygen: Its mechanisms and efficacy. Plast. Reconstr. Surg. 2011;127:131–141. doi: 10.1097/PRS.0b013e3181fbe2bf.
    1. Munn D.H., Mellor A.L. Indoleamine 2,3 dioxygenase and metabolic control of immune responses. Trends Immunol. 2013;34:137–143. doi: 10.1016/j.it.2012.10.001.
    1. Won H.Y., Sohn J.H., Min H.J., Lee K., Woo H.A., Ho Y.-S., Park J.W., Rhee S., Hwang E.S. Glutathione Peroxidase 1 Deficiency Attenuates Allergen-Induced Airway Inflammation by Suppressing Th2 and Th17 Cell Development. Antioxid. Redox Signal. 2010;13:575–587. doi: 10.1089/ars.2009.2989.
    1. Faleo G., Fotino C., Bocca N., Molano R.D., Zahr-Akrawi E., Molina J., Villate S., Umland O., Skyler J.S., Bayer A.L., et al. Prevention of autoimmune diabetes and induction of beta-cell proliferation in NOD mice by hyperbaric oxygen therapy. Diabetes. 2012;61:1769–1778. doi: 10.2337/db11-0516.
    1. Kim H.-R., Kim J.-H., Choi E.-J., Lee Y.K., Kie J.-H., Jang M.H., Seoh J.-Y. Hyperoxygenation Attenuated a Murine Model of Atopic Dermatitis through Raising Skin Level of ROS. PLoS ONE. 2014;9:e109297. doi: 10.1371/journal.pone.0109297.
    1. Bouaziz J.D., Yanaba K., Venturi G.M., Wang Y., Tisch R.M., Poe J.C., Tedder T.F. Therapeutic B cell depletion impairs adaptive and autoreactive CD4+ T cell activa-tion in mice. Proc. Natl. Acad. Sci. USA. 2007;104:20882–20887. doi: 10.1073/pnas.0709205105.
    1. Simon D., Hösli S., Kostylina G., Yawalkar N., Simon H.-U. Anti-CD20 (rituximab) treatment improves atopic eczema. J. Allergy Clin. Immunol. 2008;121:122–128. doi: 10.1016/j.jaci.2007.11.016.
    1. Kasperkiewicz M., Schmidt E., Ludwig R.J., Zillikens D. Targeting IgE Antibodies by Immuno-adsorption in Atopic Dermatitis. Front. Immunol. 2018;9:254. doi: 10.3389/fimmu.2018.00254.
    1. Thom S.R. Oxidative stress is fundamental to hyperbaric oxygen therapy. J. Appl. Physiol. 2009;106:988–995. doi: 10.1152/japplphysiol.91004.2008.
    1. Narożny W., Siebert J. Możliwości i ograniczenia stosowania tlenu hiperbarycznego w medycynie. Forum Med. Rodz. 2007;4:368–375.

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