Residual nasal polyp tissue following dupilumab therapy is associated with periostin-associated fibrosis.
Asthma
Collagen
Dupilumab
Eosinophilic chronic rhinosinusitis
Nasal polyp
Periostin
Journal
European archives of oto-rhino-laryngology : official journal of the European Federation of Oto-Rhino-Laryngological Societies (EUFOS) : affiliated with the German Society for Oto-Rhino-Laryngology - Head and Neck Surgery
ISSN: 1434-4726
Titre abrégé: Eur Arch Otorhinolaryngol
Pays: Germany
ID NLM: 9002937
Informations de publication
Date de publication:
Apr 2024
Apr 2024
Historique:
received:
24
06
2023
accepted:
03
11
2023
medline:
18
3
2024
pubmed:
18
11
2023
entrez:
18
11
2023
Statut:
ppublish
Résumé
Dupilumab, an anti-interleukin-4 receptor alpha monoclonal antibody, is a new treatment for severe uncontrolled chronic rhinosinusitis with nasal polyps. However, data on the effect of dupilumab on histological changes in nasal polyp tissue are lacking. We aimed to investigate the effect of dupilumab on real-life clinical conditions and nasal polyp tissues from patients with eosinophilic chronic rhinosinusitis (ECRS), which is a refractory subtype. We conducted an open-label, prospective, observational, single-centre study on 63 patients with refractory ECRS on the basis of the criteria of the Japanese Epidemiological Survey of Refractory Eosinophilic Chronic Rhinosinusitis Study. These patients had a history of surgery and received dupilumab for 24 weeks. Patient-reported sinonasal symptoms, T&T olfactometry and nasal polyp scores were prospectively evaluated. In 23 patients with residual nasal polyps following dupilumab treatment, changes in systemic and local periostin expression, and total collagen deposition in nasal polyp tissues were investigated before and after dupilumab administration. Dupilumab rapidly improved sinonasal symptoms and reduced the nasal polyp score 24 weeks after initiation. 40 (63.5%) patients had resolution of nasal polyps, but the reduction was limited in the remaining 23 (36.5%) patients. Periostin expression in serum and nasal lavage fluid was decreased, whereas periostin and the total collagen deposition area in subepithelial tissues in residual nasal polyps were enhanced after dupilumab administration. Dupilumab improves sinonasal symptoms and reduces the nasal polyp score in refractory ECRS. Periostin-associated tissue fibrosis may be involved in the differential effect of dupilumab on nasal polyp reduction.
Identifiants
pubmed: 37979011
doi: 10.1007/s00405-023-08336-8
pii: 10.1007/s00405-023-08336-8
doi:
Substances chimiques
dupilumab
420K487FSG
Periostin
0
Collagen
9007-34-5
Antibodies, Monoclonal, Humanized
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1807-1817Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Fokkens WJ, Lund VJ, Hopkins C et al (2020) European position paper on rhinosinusitis and nasal polyps 2020. Rhinology 58:1–464. https://doi.org/10.4193/Rhin20.600
doi: 10.4193/Rhin20.600
pubmed: 32078669
Grayson JW, Hopkins C, Mori E, Senior B, Harvey RJ (2020) Contemporary classification of chronic rhinosinusitis beyond polyps vs no polyps: a review. JAMA Otolaryngology-Head & Neck Surgery 146:831–838. https://doi.org/10.1001/jamaoto.2020.1453
doi: 10.1001/jamaoto.2020.1453
Tokunaga T, Sakashita M, Haruna T et al (2015) Novel scoring system and algorithm for classifying chronic rhinosinusitis: the JESREC Study. Allergy 70:995–1003. https://doi.org/10.1111/all.12644
doi: 10.1111/all.12644
pubmed: 25945591
Fujieda S, Imoto Y, Kato Y et al (2019) Eosinophilic chronic rhinosinusitis. Allergol Int 68:403–412. https://doi.org/10.1016/j.alit.2019.07.002
doi: 10.1016/j.alit.2019.07.002
pubmed: 31402319
Takabayashi T, Schleimer RP (2020) Formation of nasal polyps: The roles of innate type 2 inflammation and deposition of fibrin. J Allergy Clin Immunol 145:740–750. https://doi.org/10.1016/j.jaci.2020.01.027
doi: 10.1016/j.jaci.2020.01.027
pubmed: 32145873
pmcid: 7263055
Bachert C, Han JK, Desrosiers M et al (2019) Efficacy and safety of dupilumab in patients with severe chronic rhinosinusitis with nasal polyps (LIBERTY NP SINUS-24 and LIBERTY NP SINUS-52): results from two multicentre, randomised, double-blind, placebo-controlled, parallel-group phase 3 trials. Lancet 394:1638–1650. https://doi.org/10.1016/s0140-6736(19)31881-1
doi: 10.1016/s0140-6736(19)31881-1
pubmed: 31543428
Fujieda S, Matsune S, Takeno S et al (2022) Dupilumab efficacy in chronic rhinosinusitis with nasal polyps from SINUS-52 is unaffected by eosinophilic status. Allergy 77:186–196. https://doi.org/10.1111/all.14906
doi: 10.1111/all.14906
pubmed: 33993501
(GINA) GIfA Global Strategy for Asthma Management and Prevention. GINA Updated Report 2022. Accessed 01 June 2023***
Kowalski ML, Agache I, Bavbek S et al (2019) Diagnosis and management of NSAID-exacerbated respiratory disease (N-ERD)-a EAACI position paper. Allergy 74:28–39. https://doi.org/10.1111/all.13599
doi: 10.1111/all.13599
pubmed: 30216468
Miwa T, Ikeda K, Ishibashi T et al (2019) Clinical practice guidelines for the management of olfactory dysfunction—secondary publication. Auris Nasus Larynx 46:653–662. https://doi.org/10.1016/j.anl.2019.04.002
doi: 10.1016/j.anl.2019.04.002
pubmed: 31076272
Gevaert P, Calus L, Van Zele T et al (2013) Omalizumab is effective in allergic and nonallergic patients with nasal polyps and asthma. J Allergy Clin Immunol 131:110-116.e111. https://doi.org/10.1016/j.jaci.2012.07.047
doi: 10.1016/j.jaci.2012.07.047
pubmed: 23021878
Takayama G, Arima K, Kanaji T et al (2006) Periostin: a novel component of subepithelial fibrosis of bronchial asthma downstream of IL-4 and IL-13 signals. J Allergy Clin Immunol 118:98–104. https://doi.org/10.1016/j.jaci.2006.02.046
doi: 10.1016/j.jaci.2006.02.046
pubmed: 16815144
Ninomiya T, Noguchi E, Haruna T et al (2018) Periostin as a novel biomarker for postoperative recurrence of chronic rhinosinitis with nasal polyps. Sci Rep 8:11450. https://doi.org/10.1038/s41598-018-29612-2
doi: 10.1038/s41598-018-29612-2
pubmed: 30061580
pmcid: 6065353
Kato A, Peters AT, Stevens WW, Schleimer RP, Tan BK, Kern RC (2022) Endotypes of chronic rhinosinusitis: Relationships to disease phenotypes, pathogenesis, clinical findings, and treatment approaches. Allergy 77:812–826. https://doi.org/10.1111/all.15074
doi: 10.1111/all.15074
pubmed: 34473358
Kato A, Schleimer RP, Bleier BS (2022) Mechanisms and pathogenesis of chronic rhinosinusitis. J Allergy Clin Immunol 149:1491–1503. https://doi.org/10.1016/j.jaci.2022.02.016
doi: 10.1016/j.jaci.2022.02.016
pubmed: 35245537
pmcid: 9081253
Nakayama T, Sugimoto N, Okada N et al (2019) JESREC score and mucosal eosinophilia can predict endotypes of chronic rhinosinusitis with nasal polyps. Auris Nasus Larynx 46:374–383. https://doi.org/10.1016/j.anl.2018.09.004
doi: 10.1016/j.anl.2018.09.004
pubmed: 30243753
Kim DK, Kang SI, Kong IG et al (2018) Two-track medical treatment strategy according to the clinical scoring system for chronic rhinosinusitis. Allergy Asthma Immunol Res 10:490–502. https://doi.org/10.4168/aair.2018.10.5.490
doi: 10.4168/aair.2018.10.5.490
pubmed: 30088369
pmcid: 6082823
Jansen F, Becker B, Eden JK et al (2023) Dupilumab (Dupixent(®)) tends to be an effective therapy for uncontrolled severe chronic rhinosinusitis with nasal polyps: real data of a single-centered, retrospective single-arm longitudinal study from a university hospital in Germany. Eur Arch Otorhinolaryngol 280:1741–1755. https://doi.org/10.1007/s00405-022-07679-y
doi: 10.1007/s00405-022-07679-y
pubmed: 36242612
De Corso E, Settimi S, Montuori C et al (2022) Effectiveness of dupilumab in the treatment of patients with severe uncontrolled CRSwNP: a “real-life” observational study in the first year of treatment. J Clin Med 11:2684. https://doi.org/10.3390/jcm11102684
doi: 10.3390/jcm11102684
pubmed: 35628815
pmcid: 9146210
Kashiwagi T, Tsunemi Y, Akutsu M, Nakajima I, Haruna S (2019) Postoperative evaluation of olfactory dysfunction in eosinophilic chronic rhinosinusitis—comparison of histopathological and clinical findings. Acta Otolaryngol 139:881–889. https://doi.org/10.1080/00016489.2019.1654131
doi: 10.1080/00016489.2019.1654131
pubmed: 31438745
Van Zele T, Gevaert P, Holtappels G et al (2010) Oral steroids and doxycycline: two different approaches to treat nasal polyps. J Allergy Clin Immunol 125:1069-1076.e1064. https://doi.org/10.1016/j.jaci.2010.02.020
doi: 10.1016/j.jaci.2010.02.020
pubmed: 20451040
Ecevit MC, Erdag TK, Dogan E, Sutay S (2015) Effect of steroids for nasal polyposis surgery: a placebo-controlled, randomized, double-blind study. Laryngoscope 125:2041–2045. https://doi.org/10.1002/lary.25352
doi: 10.1002/lary.25352
pubmed: 25945691
Hissaria P, Smith W, Wormald PJ et al (2006) Short course of systemic corticosteroids in sinonasal polyposis: a double-blind, randomized, placebo-controlled trial with evaluation of outcome measures. J Allergy Clin Immunol 118:128–133. https://doi.org/10.1016/j.jaci.2006.03.012
doi: 10.1016/j.jaci.2006.03.012
pubmed: 16815148
Mullol J, Mariño-Sánchez F, Valls M, Alobid I, Marin C (2020) The sense of smell in chronic rhinosinusitis. J Allergy Clin Immunol 145:773–776. https://doi.org/10.1016/j.jaci.2020.01.024
doi: 10.1016/j.jaci.2020.01.024
pubmed: 32145875
Stevens WW, Peters AT, Tan BK et al (2019) Associations between inflammatory endotypes and clinical presentations in chronic rhinosinusitis. J Allergy Clin Immunol Pract 7:2812-2820.e2813. https://doi.org/10.1016/j.jaip.2019.05.009
doi: 10.1016/j.jaip.2019.05.009
pubmed: 31128376
pmcid: 6842686
Mullol J, Bachert C, Amin N et al (2022) Olfactory outcomes with dupilumab in chronic rhinosinusitis with nasal polyps. J Allergy Clin Immunol Pract 10:1086-1095.e1085. https://doi.org/10.1016/j.jaip.2021.09.037
doi: 10.1016/j.jaip.2021.09.037
pubmed: 34628065
Saraswathula A, Liu MM, Kulaga H, Lane AP (2023) Chronic interleukin-13 expression in mouse olfactory mucosa results in regional aneuronal epithelium. Int Forum Allergy Rhinol 13:230–241. https://doi.org/10.1002/alr.23073
doi: 10.1002/alr.23073
pubmed: 35950767
Wu J, Chandra RK, Li P, Hull BP, Turner JH (2018) Olfactory and middle meatal cytokine levels correlate with olfactory function in chronic rhinosinusitis. Laryngoscope 128:E304-e310. https://doi.org/10.1002/lary.27112
doi: 10.1002/lary.27112
pubmed: 29417576
pmcid: 6082743
Soler ZM, Yoo F, Schlosser RJ et al (2020) Correlation of mucus inflammatory proteins and olfaction in chronic rhinosinusitis. Int Forum Allergy Rhinol 10:343–355. https://doi.org/10.1002/alr.22499
doi: 10.1002/alr.22499
pubmed: 31856395
Izuhara K, Nunomura S, Nanri Y, Ono J, Takai M, Kawaguchi A (2019) Periostin: an emerging biomarker for allergic diseases. Allergy 74:2116–2128. https://doi.org/10.1111/all.13814
doi: 10.1111/all.13814
pubmed: 30964557
Suzaki I, Kawano S, Komiya K et al (2017) Inhibition of IL-13-induced periostin in airway epithelium attenuates cellular protein expression of MUC5AC. Respirology 22:93–100. https://doi.org/10.1111/resp.12873
doi: 10.1111/resp.12873
pubmed: 27553766
Izuhara K, Conway SJ, Moore BB et al (2016) Roles of periostin in respiratory disorders. Am J Respir Crit Care Med 193:949–956. https://doi.org/10.1164/rccm.201510-2032PP
doi: 10.1164/rccm.201510-2032PP
pubmed: 26756066
pmcid: 4872656
Ebenezer JA, Christensen JM, Oliver BG et al (2017) Periostin as a marker of mucosal remodelling in chronic rhinosinusitis. Rhinology 55:234–241. https://doi.org/10.4193/Rhino16.215
doi: 10.4193/Rhino16.215
pubmed: 28667737
Ishida A, Ohta N, Suzuki Y et al (2012) Expression of pendrin and periostin in allergic rhinitis and chronic rhinosinusitis. Allergol Int 61:589–595. https://doi.org/10.2332/allergolint.11-OA-0370
doi: 10.2332/allergolint.11-OA-0370
pubmed: 22918213
Izuhara K, Fujieda S, Ohta N (2023) The functional role and the clinical application of periostin in chronic rhinosinusitis. Expert Rev Clin Immunol:1–10. https://doi.org/10.1080/1744666x.2023.2192928
Zhang Z, Liu J, Xie L, Cao W, Ma F, Zhang Y (2022) Tissue eosinophils and mucous inflammatory cytokines for the evaluation of olfactory recovery after endoscopic sinus surgery in patients with nasal polyposis. Am J Otolaryngol 43:103561. https://doi.org/10.1016/j.amjoto.2022.103561
doi: 10.1016/j.amjoto.2022.103561
pubmed: 35952528
Mueller SK, Wendler O, Nocera A et al (2019) Escalation in mucus cystatin 2, pappalysin-A, and periostin levels over time predict need for recurrent surgery in chronic rhinosinusitis with nasal polyps. Int Forum Allergy Rhinol 9:1212–1219. https://doi.org/10.1002/alr.22407
doi: 10.1002/alr.22407
pubmed: 31430426
Jonstam K, Westman M, Holtappels G, Holweg CTJ, Bachert C (2017) Serum periostin, IgE, and SE-IgE can be used as biomarkers to identify moderate to severe chronic rhinosinusitis with nasal polyps. J Allergy Clin Immunol 140:1705-1708.e1703. https://doi.org/10.1016/j.jaci.2017.07.031
doi: 10.1016/j.jaci.2017.07.031
pubmed: 28870464
Bachert C, Corren J, Lee SE et al (2022) Dupilumab efficacy and biomarkers in chronic rhinosinusitis with nasal polyps: association between dupilumab treatment effect on nasal polyp score and biomarkers of type 2 inflammation in patients with chronic rhinosinusitis with nasal polyps in the phase 3 SINUS-24 and SINUS-52 trials. Int Forum Allergy Rhinol 12:1191–1195. https://doi.org/10.1002/alr.22964
doi: 10.1002/alr.22964
pubmed: 34970860
pmcid: 9544911
Feng X, Payne SC, Borish L, Steinke JW (2019) Differential expression of extracellular matrix components in nasal polyp endotypes. Am J Rhinol Allergy 33:665–670. https://doi.org/10.1177/1945892419860634
doi: 10.1177/1945892419860634
pubmed: 31237767
pmcid: 6843742
Payne SC, Early SB, Huyett P, Han JK, Borish L, Steinke JW (2011) Evidence for distinct histologic profile of nasal polyps with and without eosinophilia. Laryngoscope 121:2262–2267. https://doi.org/10.1002/lary.21969
doi: 10.1002/lary.21969
pubmed: 21898422
pmcid: 3183261
Kim JW, Hong SL, Kim YK, Lee CH, Min YG, Rhee CS (2007) Histological and immunological features of non-eosinophilic nasal polyps. Otolaryngol Head Neck Surg 137:925–930. https://doi.org/10.1016/j.otohns.2007.07.036
doi: 10.1016/j.otohns.2007.07.036
pubmed: 18036422
Shin SH, Kim YH, Ye MK, Choi SY (2017) Immunopathologic characteristics of nasal polyps in adult Koreans: a single-center study. Am J Rhinol Allergy 31:168–173. https://doi.org/10.2500/ajra.2017.31.4423
doi: 10.2500/ajra.2017.31.4423
pubmed: 28490401
Hopkins C, Wagenmann M, Bachert C et al (2021) Efficacy of dupilumab in patients with a history of prior sinus surgery for chronic rhinosinusitis with nasal polyps. Int Forum Allergy Rhinol 11:1087–1101. https://doi.org/10.1002/alr.22780
doi: 10.1002/alr.22780
pubmed: 33611847
pmcid: 8359289
Poposki JA, Klingler AI, Stevens WW et al (2022) Elevation of activated neutrophils in chronic rhinosinusitis with nasal polyps. J Allergy Clin Immunol 149:1666–1674. https://doi.org/10.1016/j.jaci.2021.11.023
doi: 10.1016/j.jaci.2021.11.023
pubmed: 34953792
Delemarre T, Bochner BS, Simon HU, Bachert C (2021) Rethinking neutrophils and eosinophils in chronic rhinosinusitis. J Allergy Clin Immunol 148:327–335. https://doi.org/10.1016/j.jaci.2021.03.024
doi: 10.1016/j.jaci.2021.03.024
pubmed: 33895002
pmcid: 8355033
Delemarre T, Holtappels G, De Ruyck N et al (2021) A substantial neutrophilic inflammation as regular part of severe type 2 chronic rhinosinusitis with nasal polyps. J Allergy Clin Immunol 147:179-188.e172. https://doi.org/10.1016/j.jaci.2020.08.036
doi: 10.1016/j.jaci.2020.08.036
pubmed: 32949587
Bachert C, Han JK, Wagenmann M et al (2021) EUFOREA expert board meeting on uncontrolled severe chronic rhinosinusitis with nasal polyps (CRSwNP) and biologics: Definitions and management. J Allergy Clin Immunol 147:29–36. https://doi.org/10.1016/j.jaci.2020.11.013
doi: 10.1016/j.jaci.2020.11.013
pubmed: 33227318