Rapid reduction in Staphylococcus aureus in atopic dermatitis subjects following dupilumab treatment.


Journal

The Journal of allergy and clinical immunology
ISSN: 1097-6825
Titre abrégé: J Allergy Clin Immunol
Pays: United States
ID NLM: 1275002

Informations de publication

Date de publication:
11 2023
Historique:
received: 07 11 2022
revised: 05 05 2023
accepted: 11 05 2023
pmc-release: 13 12 2024
medline: 7 11 2023
pubmed: 15 6 2023
entrez: 14 6 2023
Statut: ppublish

Résumé

Atopic dermatitis (AD) is an inflammatory disorder characterized by dominant type 2 inflammation leading to chronic pruritic skin lesions, allergic comorbidities, and Staphylococcus aureus skin colonization and infections. S aureus is thought to play a role in AD severity. This study characterized the changes in the host-microbial interface in subjects with AD following type 2 blockade with dupilumab. Participants (n = 71) with moderate-severe AD were enrolled in a randomized (dupilumab vs placebo; 2:1), double-blind study at Atopic Dermatitis Research Network centers. Bioassays were performed at multiple time points: S aureus and virulence factor quantification, 16s ribosomal RNA microbiome, serum biomarkers, skin transcriptomic analyses, and peripheral blood T-cell phenotyping. At baseline, 100% of participants were S aureus colonized on the skin surface. Dupilumab treatment resulted in significant reductions in S aureus after only 3 days (compared to placebo), which was 11 days before clinical improvement. Participants with the greatest S aureus reductions had the best clinical outcomes, and these reductions correlated with reductions in serum CCL17 and disease severity. Reductions (10-fold) in S aureus cytotoxins (day 7), perturbations in T Blockade of IL-4 and IL-13 signaling, very rapidly (day 3) reduces S aureus abundance in subjects with AD, and this reduction correlates with reductions in the type 2 biomarker, CCL17, and measures of AD severity (excluding itch). Immunoprofiling and/or transcriptomics suggest a role for T

Sections du résumé

BACKGROUND
Atopic dermatitis (AD) is an inflammatory disorder characterized by dominant type 2 inflammation leading to chronic pruritic skin lesions, allergic comorbidities, and Staphylococcus aureus skin colonization and infections. S aureus is thought to play a role in AD severity.
OBJECTIVES
This study characterized the changes in the host-microbial interface in subjects with AD following type 2 blockade with dupilumab.
METHODS
Participants (n = 71) with moderate-severe AD were enrolled in a randomized (dupilumab vs placebo; 2:1), double-blind study at Atopic Dermatitis Research Network centers. Bioassays were performed at multiple time points: S aureus and virulence factor quantification, 16s ribosomal RNA microbiome, serum biomarkers, skin transcriptomic analyses, and peripheral blood T-cell phenotyping.
RESULTS
At baseline, 100% of participants were S aureus colonized on the skin surface. Dupilumab treatment resulted in significant reductions in S aureus after only 3 days (compared to placebo), which was 11 days before clinical improvement. Participants with the greatest S aureus reductions had the best clinical outcomes, and these reductions correlated with reductions in serum CCL17 and disease severity. Reductions (10-fold) in S aureus cytotoxins (day 7), perturbations in T
CONCLUSIONS
Blockade of IL-4 and IL-13 signaling, very rapidly (day 3) reduces S aureus abundance in subjects with AD, and this reduction correlates with reductions in the type 2 biomarker, CCL17, and measures of AD severity (excluding itch). Immunoprofiling and/or transcriptomics suggest a role for T

Identifiants

pubmed: 37315812
pii: S0091-6749(23)00754-6
doi: 10.1016/j.jaci.2023.05.026
pmc: PMC10716365
mid: NIHMS1920179
pii:
doi:

Substances chimiques

dupilumab 420K487FSG
Antibodies, Monoclonal, Humanized 0

Types de publication

Randomized Controlled Trial Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

1179-1195

Subventions

Organisme : NIAID NIH HHS
ID : UM2 AI117870
Pays : United States
Organisme : NIAID NIH HHS
ID : U01 AI152011
Pays : United States
Organisme : NIAID NIH HHS
ID : UM1 AI151958
Pays : United States
Organisme : NIAID NIH HHS
ID : U19 AI117673
Pays : United States
Organisme : NCATS NIH HHS
ID : UL1 TR002535
Pays : United States

Informations de copyright

Copyright © 2023 The Authors. Published by Elsevier Inc. All rights reserved.

Références

Int J Mol Sci. 2020 Feb 13;21(4):
pubmed: 32070069
Am J Clin Dermatol. 2019 Jun;20(3):443-456
pubmed: 31066001
J Allergy Clin Immunol. 2021 Jan;147(1):213-223
pubmed: 32615169
PLoS One. 2016 Jul 14;11(7):e0158969
pubmed: 27414801
Pediatr Dermatol. 2021 Nov;38(6):1500-1505
pubmed: 34647354
J Invest Dermatol. 2022 Oct;142(10):2660-2667
pubmed: 35395222
J Invest Dermatol. 2018 Oct;138(10):2224-2233
pubmed: 29604251
Br J Dermatol. 2010 Jul;163(1):12-26
pubmed: 20222931
J Allergy Clin Immunol. 2010 Jan;125(1):4-13; quiz 14-5
pubmed: 20109729
Clin Infect Dis. 2008 May 15;46(10):1562-7
pubmed: 18419342
Genes (Basel). 2019 Dec 12;10(12):
pubmed: 31842331
mSphere. 2021 Aug 25;6(4):e0060821
pubmed: 34319127
Am J Obstet Gynecol. 2003 Dec;189(6):1785-91
pubmed: 14710116
J Clin Invest. 2010 May;120(5):1762-73
pubmed: 20364087
J Invest Dermatol. 2005 Nov;125(5):977-82
pubmed: 16297199
J Allergy Clin Immunol. 1999 Jan;103(1 Pt 1):119-24
pubmed: 9893195
J Allergy Clin Immunol Pract. 2022 Jun;10(6):1515-1526
pubmed: 35259535
mBio. 2022 Jun 28;13(3):e0093022
pubmed: 35608301
Int J Mol Sci. 2013 Mar 26;14(4):6720-45
pubmed: 23531535
J Allergy Clin Immunol. 2019 Jul;144(1):267-279.e4
pubmed: 30768990
Nat Immunol. 2007 Sep;8(9):950-7
pubmed: 17676044
Int Arch Allergy Immunol. 2011;156(4):412-5
pubmed: 21832830
J Allergy Clin Immunol. 2014 Oct;134(4):848-55
pubmed: 25159465
Curr Opin Immunol. 2018 Oct;54:115-122
pubmed: 30015087
Pediatr Dermatol. 2003 Nov-Dec;20(6):465-9
pubmed: 14651561
JID Innov. 2022 Apr 26;2(5):100131
pubmed: 36059592
mSphere. 2019 Dec 11;4(6):
pubmed: 31826969
Cells. 2022 Apr 14;11(8):
pubmed: 35456017
Cell Host Microbe. 2011 Aug 18;10(2):158-64
pubmed: 21843872
Am J Clin Dermatol. 2006;7(5):273-9
pubmed: 17007538
Front Immunol. 2019 Oct 24;10:2507
pubmed: 31708926
Br J Dermatol. 2016 Oct;175(4):687-95
pubmed: 26994362
J Cutan Med Surg. 2018 Nov/Dec;22(1_suppl):10S-16S
pubmed: 30439297
Br J Dermatol. 2013 Sep;169(3):700-3
pubmed: 23600999
Allergy Asthma Immunol Res. 2019 Sep;11(5):593-603
pubmed: 31332972
J Allergy Clin Immunol. 2019 Jan;143(1):155-172
pubmed: 30194992
Microorganisms. 2021 Jul 13;9(7):
pubmed: 34361924
Sci Transl Med. 2017 Jul 5;9(397):
pubmed: 28679656
J Allergy Clin Immunol. 2015 Dec;136(6):1591-1600
pubmed: 26343451
Allergy. 2022 Nov;77(11):3388-3397
pubmed: 35815904
Br J Dermatol. 2000 Feb;142(2):288-97
pubmed: 10730763
N Engl J Med. 2014 Jul 10;371(2):130-9
pubmed: 25006719
Clin Microbiol Rev. 2013 Jul;26(3):422-47
pubmed: 23824366
J Leukoc Biol. 2003 Sep;74(3):448-55
pubmed: 12949249
Nucleic Acids Res. 2021 Jan 8;49(D1):D545-D551
pubmed: 33125081
J Invest Dermatol. 2020 Jan;140(1):191-202.e7
pubmed: 31252032
J Leukoc Biol. 2021 Jan;109(1):67-72
pubmed: 32869342
Arthritis Res Ther. 2020 May 6;22(1):105
pubmed: 32375861
Toxins (Basel). 2017 Jun 28;9(7):
pubmed: 28657583
JID Innov. 2021 Apr 28;1(2):100018
pubmed: 34909717
Ann Allergy Asthma Immunol. 2021 Jan;126(1):3-12
pubmed: 32771354
Front Microbiol. 2021 Oct 18;12:757215
pubmed: 34733265
Cytometry A. 2014 May;85(5):408-21
pubmed: 24677621
Br J Dermatol. 2021 Aug;185(2):432-434
pubmed: 33730377
J Allergy Clin Immunol. 2009 Aug;124(2):260-9, 269.e1-7
pubmed: 19541356
J Allergy Clin Immunol. 2011 Jan;127(1):186-93, 193.e1-11
pubmed: 21211653
J Invest Dermatol. 2010 May;130(5):1355-64
pubmed: 20107483
Nat Immunol. 2015 Sep;16(9):970-9
pubmed: 26168081
J Allergy Clin Immunol. 2012 Sep;130(3):683-691.e2
pubmed: 22840852
Protein Sci. 2019 Nov;28(11):1947-1951
pubmed: 31441146
J Allergy Clin Immunol Pract. 2022 Jan;10(1):349-351.e1
pubmed: 34536614
J Infect Dis. 2014 Mar;209(6):865-75
pubmed: 24072844
mSphere. 2016 Dec 7;1(6):
pubmed: 27981233
Sci Transl Med. 2017 Feb 22;9(378):
pubmed: 28228596
Nucleic Acids Res. 2000 Jan 1;28(1):27-30
pubmed: 10592173
Ann Intern Med. 1982 Jun;96(6 Pt 2):937-40
pubmed: 7091971
Immunity. 2016 Jul 19;45(1):172-84
pubmed: 27438770
PLoS One. 2013;8(4):e60463
pubmed: 23565251
Immunobiology. 2012 Apr;217(4):436-45
pubmed: 22137028
Cytometry A. 2014 May;85(5):422-33
pubmed: 24532172
Arch Dermatol. 1996 Jan;132(1):27-33
pubmed: 8546480
Pediatr Dermatol. 2022 Mar;39(2):187-196
pubmed: 35083774
J Allergy Clin Immunol. 2010 Dec;126(6):1176-83.e4
pubmed: 20864149
Ann N Y Acad Sci. 2017 Oct;1405(1):53-70
pubmed: 28753223
J Allergy Clin Immunol. 2011 Apr;127(4):965-73.e1-5
pubmed: 21458658
Clin Sci (Lond). 2018 May 8;132(9):909-923
pubmed: 29739822
Atherosclerosis. 2012 Feb;220(2):552-6
pubmed: 22169111
Allergy Asthma Immunol Res. 2021 Sep;13(5):762-775
pubmed: 34486260
Clin Exp Dermatol. 2012 Apr;37(3):296-9
pubmed: 22300286
Nat Med. 2021 Apr;27(4):700-709
pubmed: 33619370

Auteurs

Eric L Simpson (EL)

Department of Dermatology, Oregon Health and Science University, Portland, Ore.

Patrick M Schlievert (PM)

Department of Microbiology and Immunology, University of Iowa, Iowa City, Iowa.

Takeshi Yoshida (T)

Department of Dermatology, University of Rochester School of Medicine and Dentistry, Rochester, NY.

Stephanie Lussier (S)

Rho, Inc, Durham, NC.

Mark Boguniewicz (M)

Division of Allergy-Immunology, Department of Pediatrics, National Jewish Health and University of Colorado School of Medicine, Denver, Colo.

Tissa Hata (T)

Department of Dermatology, University of California, San Diego, Calif.

Zelma Fuxench (Z)

Department of Dermatology, University of Pennsylvania, Philadelphia, Pa.

Anna De Benedetto (A)

Department of Dermatology, University of Rochester School of Medicine and Dentistry, Rochester, NY.

Peck Y Ong (PY)

Department of Pediatrics, University Southern California, Los Angeles, Calif.

Justin Ko (J)

Department of Dermatology, Stanford University, Stanford, Calif.

Agustin Calatroni (A)

Rho, Inc, Durham, NC.

Amanda K Rudman Spergel (AK)

Division of Allergy, Immunology, and Transplantation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Md.

Marshall Plaut (M)

Division of Allergy, Immunology, and Transplantation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Md.

Sally A Quataert (SA)

Center for Vaccine Biology and Immunology, University of Rochester Medical Center, Rochester, NY.

Samuel H Kilgore (SH)

Department of Microbiology and Immunology, University of Iowa, Iowa City, Iowa.

Liam Peterson (L)

Department of Dermatology, University of Rochester School of Medicine and Dentistry, Rochester, NY.

Ann L Gill (AL)

Department of Microbiology and Immunology, University of Rochester Medical Center, Rochester, NY.

Gloria David (G)

Rho, Inc, Durham, NC.

Tim Mosmann (T)

Center for Vaccine Biology and Immunology, University of Rochester Medical Center, Rochester, NY.

Steven R Gill (SR)

Department of Microbiology and Immunology, University of Rochester Medical Center, Rochester, NY.

Donald Y M Leung (DYM)

Division of Allergy-Immunology, Department of Pediatrics, National Jewish Health and University of Colorado School of Medicine, Denver, Colo. Electronic address: LeungD@NJHealth.org.

Lisa A Beck (LA)

Department of Dermatology, University of Rochester School of Medicine and Dentistry, Rochester, NY. Electronic address: Lisa_Beck@urmc.rochester.edu.

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