Biological Therapy of Severe Asthma and Nasal Polyps

asthma; benralizumab; chronic rhinosinusitis with nasal polyps (CRSwNP); dupilumab; mepolizumab; monoclonal antibodies; cyclooxygenase 1; interleukin 13; interleukin 25; interleukin 33; interleukin 4; interleukin 5; omalizumab; peptidoleukotriene; prostaglandin D2; prostaglandin F2 alpha; thymic stromal lymphopoietin; anosmia; aspirin exacerbated respiratory disease; bronchiectasis; cell adhesion; chronic rhinosinusitis; computer assisted tomography; disease severity; eosinophil; eosinophil count; eosinophilic asthma; follow up; group 2 innate lymphoid cell; human; immune response; lung lavage; mast cell; nose polyp; nose surgery; phenotype; Review; severe asthma; sino-nasal outcome test-22; Staphylococcus aureus; tight junction; visual analog scale

Abstract :

[en] Chronic rhinosinusitis is a common disease worldwide and can be categorized into chronic rhinosinusitis with nasal polyps and chronic rhinosinusitis without nasal polyps. Chronic rhinosinusitis with nasal polyps is common in patients with asthma and, particularly, severe asthma. Severe asthma is effectively treated with biologics and the coexistence of severe asthma with chronic rhinosinusitis with nasal polyps presents a phenotype that is more likely to respond to such treatment. In this review, we focus on the link between asthma and nasal polyps, and we review the treatment effect of various monoclonal antibodies in patients with severe asthma and nasal polyps as well as in patients with nasal polyps without asthma or with mild-to-moderate asthma. With the enhancement of our armamentarium with new monoclonal antibodies the right choice of biologic becomes an important target and one that is difficult to achieve due to the lack of comparative head-to-head studies. © 2022 by the authors. Licensee MDPI, Basel, Switzerland.

Disciplines :

Cardiovascular & respiratory systems

Author, co-author :

Bakakos, A.; Department of Respiratory Medicine, National and Kapodistrian University of Athens, Athens, 157 72, Greece

Schleich, FLorence ; Centre Hospitalier Universitaire de Liège - CHU > > Service de pneumologie - allergologie

Bakakos, P.; Department of Respiratory Medicine, National and Kapodistrian University of Athens, Athens, 157 72, Greece

Language :

English

Title :

Biological Therapy of Severe Asthma and Nasal Polyps

Publication date :

2022

Journal title :

Journal of Personalized Medicine

eISSN :

2075-4426

Publisher :

MDPI

Volume :

Issue :

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 25 November 2022

Statistics

Number of views

30 (0 by ULiège)

Number of downloads

0 (0 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Hastan, D.; Fokkens, W.J.; Bachert, C.; Newson, R.B.; Bislimovska, J.; Bockelbrink, A.; Bousquet, P.J.; Brozek, G.; Bruno, A.; Dahlen, S.E.; et al. Chronic rhinosinusitis in Europe—An underestimated disease. A GA2LEN study. Allergy 2011, 66, 1216–1223. [CrossRef]
Bachert, C.; Zhang, L.; Gevaert, P. Current and future treatment options for adult chronic rhinosinusitis: Focus on nasal polyposis. J. Allergy Clin. Immunol. 2015, 136, 1431–1440. [CrossRef]
Fokkens, W.J.; Lund, V.J.; Mullol, J.; Bachert, C.; Alobid, I.; Baroody, F.; Cohen, N.; Cervin, A.; Douglas, R.; Gevaert, P.; et al. EPOS 2012: European position paper on rhinosinusitis and nasal polyps 2012. A summary for otorhinolaryngologists. Rhinology 2012, 50, 1–12. [CrossRef]
Alobid, I.; Benitez, P.; Bernal-Sprekelsen, M.; Roca, J.; Alonso, J.; Picado, C.; Mullol, J. Nasal polyposis and its impact on quality of life: Comparison between the effects of medical and surgical treatments. Allergy 2005, 60, 452–458. [CrossRef]
Hakansson, K.; Bachert, C.; Konge, L.; Thomsen, S.F.; Pedersen, A.E.; Poulsen, S.S.; Martin-Bertelsen, T.; Winther, O.; Backer, V.; von Buchwald, C. Airway Inflammation in Chronic Rhinosinusitis with Nasal Polyps and Asthma: The United Airways Concept Further Supported. PLoS ONE 2015, 10, e0127228. [CrossRef]
Van Zele, T.; Gevaert, P.; Holtappels, G.; Beule, A.; Wormald, P.J.; Mayr, S.; Hens, G.; Hellings, P.; Ebbens, F.A.; Fokkens, W.; et al. Oral steroids and doxycycline: Two different approaches to treat nasal polyps. J. Allergy Clin. Immunol. 2010, 125, 1069–1076.e4. [CrossRef]
Sharma, R.; Lakhani, R.; Rimmer, J.; Hopkins, C. Surgical interventions for chronic rhinosinusitis with nasal polyps. Cochrane Database Syst. Rev. 2014, 11, CD006990. [CrossRef]
Hellings, P.W.; Verhoeven, E.; Fokkens, W.J. State-of-the-art overview on biological treatment for CRSwNP. Rhinology 2021, 59, 151–163. [CrossRef]
Van Zele, T.; Claeys, S.; Gevaert, P.; Van Maele, G.; Holtappels, G.; Van Cauwenberge, P.; Bachert, C. Differentiation of chronic sinus diseases by measurement of inflammatory mediators. Allergy 2006, 61, 1280–1289. [CrossRef]
Van Bruaene, N.; Perez-Novo, C.A.; Basinski, T.M.; Van Zele, T.; Holtappels, G.; De Ruyck, N.; Schmidt-Weber, C.; Akdis, C.; Van Cauwenberge, P.; Bachert, C.; et al. T-cell regulation in chronic paranasal sinus disease. J. Allergy Clin. Immunol. 2008, 121, 1435–1441.e3. [CrossRef]
Chipps, B.E.; Newbold, P.; Hirsch, I.; Trudo, F.; Goldman, M. Benralizumab efficacy by atopy status and serum immunoglobulin E for patients with severe, uncontrolled asthma. Ann. Allergy Asthma Immunol. Off. Publ. Am. Coll. Allergy Asthma Immunol. 2018, 120, 504–511.e4. [CrossRef]
Ortega, H.G.; Liu, M.C.; Pavord, I.D.; Brusselle, G.G.; FitzGerald, J.M.; Chetta, A.; Humbert, M.; Katz, L.E.; Keene, O.N.; Yancey, S.W.; et al. Mepolizumab treatment in patients with severe eosinophilic asthma. N. Engl. J. Med. 2014, 371, 1198–1207. [CrossRef]
Papi, A.; Brightling, C.; Pedersen, S.E.; Reddel, H.K. Asthma. Lancet 2018, 391, 783–800. [CrossRef]
Chung, K.F.; Wenzel, S.E.; Brozek, J.L.; Bush, A.; Castro, M.; Sterk, P.J.; Adcock, I.M.; Bateman, E.D.; Bel, E.H.; Bleecker, E.R.; et al. International ERS/ATS guidelines on definition, evaluation and treatment of severe asthma. Eur. Respir. J. 2014, 43, 343–373. [CrossRef]
Bakakos, A.; Loukides, S.; Bakakos, P. Severe Eosinophilic Asthma. J. Clin. Med. 2019, 8, 1375. [CrossRef]
Heffler, E.; Blasi, F.; Latorre, M.; Menzella, F.; Paggiaro, P.; Pelaia, G.; Senna, G.; Canonica, G.W.; Network, S. The Severe Asthma Network in Italy: Findings and Perspectives. J. Allergy Clin. Immunol. Pract. 2019, 7, 1462–1468. [CrossRef]
John Staniorski, C.; Price, C.P.E.; Weibman, A.R.; Welch, K.C.; Conley, D.B.; Shintani-Smith, S.; Stevens, W.W.; Peters, A.T.; Grammer, L.; Lidder, A.K.; et al. Asthma onset pattern and patient outcomes in a chronic rhinosinusitis population. Int. Forum Allergy Rhinol. 2018, 8, 495–503. [CrossRef]
Denlinger, L.C.; Phillips, B.R.; Ramratnam, S.; Ross, K.; Bhakta, N.R.; Cardet, J.C.; Castro, M.; Peters, S.P.; Phipatanakul, W.; Aujla, S.; et al. Inflammatory and Comorbid Features of Patients with Severe Asthma and Frequent Exacerbations. Am. J. Respir. Crit. Care Med. 2017, 195, 302–313. [CrossRef]
Canonica, G.W.; Malvezzi, L.; Blasi, F.; Paggiaro, P.; Mantero, M.; Senna, G.; Heffler, E.; Severe Asthma Network, I. Chronic rhinosinusitis with nasal polyps impact in severe asthma patients: Evidences from the Severe Asthma Network Italy (SANI) registry. Respir. Med. 2020, 166, 105947. [CrossRef]
Laidlaw, T.M.; Mullol, J.; Woessner, K.M.; Amin, N.; Mannent, L.P. Chronic Rhinosinusitis with Nasal Polyps and Asthma. J. Allergy Clin. Immunol. Pract. 2021, 9, 1133–1141. [CrossRef]
Castillo, J.A.; Plaza, V.; Rodrigo, G.; Julia, B.; Mullol, J. Chronic rhinosinusitis with and without nasal polyps and rhinitis in adult asthma. Frequency distribution and relationship with asthma control and severity (the IRIS-ASMA study). Eur. Respir. J. 2013, 42, P3448.
Tan, W.C. Viruses in asthma exacerbations. Curr. Opin. Pulm. Med. 2005, 11, 21–26. [CrossRef]
Larsen, K. The clinical relationship of nasal polyps to asthma. Allergy Asthma Proc. 1996, 17, 243–249. [CrossRef]
Barretto, K.T.; Brockman-Schneider, R.A.; Kuipers, I.; Basnet, S.; Bochkov, Y.A.; Altman, M.C.; Jarjour, N.N.; Gern, J.E.; Esnault, S. Human airway epithelial cells express a functional IL-5 receptor. Allergy 2020, 75, 2127–2130. [CrossRef]
Bachert, C.; Pawankar, R.; Zhang, L.; Bunnag, C.; Fokkens, W.J.; Hamilos, D.L.; Jirapongsananuruk, O.; Kern, R.; Meltzer, E.O.; Mullol, J.; et al. ICON: Chronic rhinosinusitis. World Allergy Organ. J. 2014, 7, 25. [CrossRef]
Kim, D.W.; Cho, S.H. Emerging Endotypes of Chronic Rhinosinusitis and Its Application to Precision Medicine. Allergy Asthma Immunol. Res. 2017, 9, 299–306. [CrossRef]
Jackson, D.J.; Makrinioti, H.; Rana, B.M.; Shamji, B.W.; Trujillo-Torralbo, M.B.; Footitt, J.; Jerico, D.-R.; Telcian, A.G.; Nikonova, A.; Zhu, J.; et al. IL-33-dependent type 2 inflammation during rhinovirus-induced asthma exacerbations in vivo. Am. J. Respir. Crit. Care Med. 2014, 190, 1373–1382. [CrossRef]
Duerr, C.U.; McCarthy, C.D.; Mindt, B.C.; Rubio, M.; Meli, A.P.; Pothlichet, J.; Eva, M.M.; Gauchat, J.F.; Qureshi, S.T.; Mazer, B.D.; et al. Type I interferon restricts type 2 immunopathology through the regulation of group 2 innate lymphoid cells. Nat. Immunol. 2016, 17, 65–75. [CrossRef]
Peters, A.T.; Bose, S.; Guo, A.; Li, N.; Benjamin, M.; Prickett, M.; Villareal, R.S.; Yang, A.; Kato, A.; Kern, R.C.; et al. Prevalence of Bronchiectasis in Patients with Chronic Rhinosinusitis in a Tertiary Care Center. J. Allergy Clin. Immunol. Pract. 2021, 9, 3188–3195.e2. [CrossRef]
Crimi, C.; Ferri, S.; Crimi, N. Bronchiectasis and asthma: A dangerous liaison? Curr. Opin. Allergy Clin. Immunol. 2019, 19, 46–52. [CrossRef]
Crimi, C.; Campisi, R.; Nolasco, S.; Ferri, S.; Cacopardo, G.; Impellizzeri, P.; Pistorio, M.P.; Fagone, E.; Pelaia, C.; Heffler, E.; et al. Type 2-High Severe Asthma with and without Bronchiectasis: A Prospective Observational Multicentre Study. J. Asthma Allergy 2021, 14, 1441–1452. [CrossRef] [PubMed]
Bhattacharyya, N. Assessing the additional disease burden of polyps in chronic rhinosinusitis. Ann. Otol. Rhinol. Laryngol. 2009, 118, 185–189. [CrossRef] [PubMed]
Cahill, K.N.; Bensko, J.C.; Boyce, J.A.; Laidlaw, T.M. Prostaglandin D2: A dominant mediator of aspirin-exacerbated respiratory disease. J. Allergy Clin. Immunol. 2015, 135, 245–252. [CrossRef] [PubMed]
Kowalski, M.L.; Sliwinska-Kowalska, M.; Igarashi, Y.; White, M.V.; Wojciechowska, B.; Brayton, P.; Kaulbach, H.; Rozniecki, J.; Kaliner, M.A. Nasal secretions in response to acetylsalicylic acid. J. Allergy Clin. Immunol. 1993, 91, 580–598. [CrossRef]
Buchheit, K.M.; Lewis, E.; Gakpo, D.; Hacker, J.; Sohail, A.; Taliaferro, F.; Berreondo Giron, E.; Asare, C.; Vukovic, M.; Bensko, J.C.; et al. Mepolizumab targets multiple immune cells in aspirin-exacerbated respiratory disease. J. Allergy Clin. Immunol. 2021, 148, 574–584. [CrossRef]
Mathe, A.A.; Hedqvist, P.; Holmgren, A.; Svanborg, N. Bronchial hyperreactivity to prostaglandin F2α and histamine in patients with asthma. Br. Med. J. 1973, 1, 193–196. [CrossRef]
Hsieh, F.H.; Lam, B.K.; Penrose, J.F.; Austen, K.F.; Boyce, J.A. T helper cell type 2 cytokines coordinately regulate immunoglobulin E-dependent cysteinyl leukotriene production by human cord blood-derived mast cells: Profound induction of leukotriene C4 synthase expression by interleukin 4. J. Exp. Med. 2001, 193, 123–133. [CrossRef]
Mesquita-Santos, F.P.; Vieira-de-Abreu, A.; Calheiros, A.S.; Figueiredo, I.H.; Castro-Faria-Neto, H.C.; Weller, P.F.; Bozza, P.T.; Diaz, B.L.; Bandeira-Melo, C. Cutting edge: Prostaglandin D2 enhances leukotriene C4 synthesis by eosinophils during allergic inflammation: Synergistic in vivo role of endogenous eotaxin. J. Immunol. 2006, 176, 1326–1330. [CrossRef]
Buchheit, K.M.; Dwyer, D.F.; Ordovas-Montanes, J.; Katz, H.R.; Lewis, E.; Vukovic, M.; Lai, J.; Bankova, L.G.; Bhattacharyya, N.; Shalek, A.K.; et al. IL-5Ralpha marks nasal polyp IgG4-and IgE-expressing cells in aspirin-exacerbated respiratory disease. J. Allergy Clin. Immunol. 2020, 145, 1574–1584. [CrossRef]
Boehme, S.A.; Franz-Bacon, K.; Chen, E.P.; Ly, T.W.; Kawakami, Y.; Bacon, K.B. Murine bone marrow-derived mast cells express chemoattractant receptor-homologous molecule expressed on T-helper class 2 cells (CRTh2). Int. Immunol. 2009, 21, 621–632. [CrossRef]
Moon, T.C.; Campos-Alberto, E.; Yoshimura, T.; Bredo, G.; Rieger, A.M.; Puttagunta, L.; Barreda, D.R.; Befus, A.D.; Cameron, L. Expression of DP2 (CRTh2), a prostaglandin D2 receptor, in human mast cells. PLoS ONE 2014, 9, e108595. [CrossRef] [PubMed]
Zhang, N.; Holtappels, G.; Gevaert, P.; Patou, J.; Dhaliwal, B.; Gould, H.; Bachert, C. Mucosal tissue polyclonal IgE is functional in response to allergen and SEB. Allergy 2011, 66, 141–148. [CrossRef] [PubMed]
Aldinger, J.P.; Dobyns, T.; Lam, K.; Han, J.K. The role of omalizumab in the treatment of chronic rhinosinusitis with nasal polyposis. Expert Opin. Biol. Ther. 2021, 21, 1143–1149. [CrossRef] [PubMed]
Baroody, F.M.; Suh, S.H.; Naclerio, R.M. Total IgE serum levels correlate with sinus mucosal thickness on computerized tomography scans. J. Allergy Clin. Immunol. 1997, 100, 563–568. [CrossRef]
Bachert, C.; Zhang, N.; Patou, J.; van Zele, T.; Gevaert, P. Role of staphylococcal superantigens in upper airway disease. Curr. Opin. Allergy Clin. Immunol. 2008, 8, 34–38. [CrossRef]
Takaku, Y.; Soma, T.; Nishihara, F.; Nakagome, K.; Kobayashi, T.; Hagiwara, K.; Kanazawa, M.; Nagata, M. Omalizumab attenuates airway inflammation and interleukin-5 production by mononuclear cells in patients with severe allergic asthma. Int. Arch. Allergy Immunol. 2013, 161 (Suppl. 2), 107–117. [CrossRef]
Pavord, I.D.; Korn, S.; Howarth, P.; Bleecker, E.R.; Buhl, R.; Keene, O.N.; Ortega, H.; Chanez, P. Mepolizumab for severe eosinophilic asthma (DREAM): A multicentre, double-blind, placebo-controlled trial. Lancet 2012, 380, 651–659. [CrossRef]
Khatri, S.; Moore, W.; Gibson, P.G.; Leigh, R.; Bourdin, A.; Maspero, J.; Barros, M.; Buhl, R.; Howarth, P.; Albers, F.C.; et al. Assessment of the long-term safety of mepolizumab and durability of clinical response in patients with severe eosinophilic asthma. J. Allergy Clin. Immunol. 2019, 143, 1742–1751.e7. [CrossRef]
Chapman, K.R.; Albers, F.C.; Chipps, B.; Munoz, X.; Devouassoux, G.; Bergna, M.; Galkin, D.; Azmi, J.; Mouneimne, D.; Price, R.G.; et al. The clinical benefit of mepolizumab replacing omalizumab in uncontrolled severe eosinophilic asthma. Allergy 2019, 74, 1716–1726. [CrossRef]
Chupp, G.L.; Bradford, E.S.; Albers, F.C.; Bratton, D.J.; Wang-Jairaj, J.; Nelsen, L.M.; Trevor, J.L.; Magnan, A.; Ten Brinke, A. Efficacy of mepolizumab add-on therapy on health-related quality of life and markers of asthma control in severe eosinophilic asthma (MUSCA): A randomised, double-blind, placebo-controlled, parallel-group, multicentre, phase 3b trial. Lancet Respir. Med. 2017, 5, 390–400. [CrossRef]
Howarth, P.; Chupp, G.; Nelsen, L.M.; Bradford, E.S.; Bratton, D.J.; Smith, S.G.; Albers, F.C.; Brusselle, G.; Bachert, C. Severe eosinophilic asthma with nasal polyposis: A phenotype for improved sinonasal and asthma outcomes with mepolizumab therapy. J. Allergy Clin. Immunol. 2020, 145, 1713–1715. [CrossRef] [PubMed]
Han, J.K.; Bachert, C.; Fokkens, W.; Desrosiers, M.; Wagenmann, M.; Lee, S.E.; Smith, S.G.; Martin, N.; Mayer, B.; Yancey, S.W.; et al. Mepolizumab for chronic rhinosinusitis with nasal polyps (SYNAPSE): A randomised, double-blind, placebo-controlled, phase 3 trial. Lancet Respir. Med. 2021, 9, 1141–1153. [CrossRef]
Bagnasco, D.; Caminati, M.; Menzella, F.; Milanese, M.; Rolla, G.; Lombardi, C.; Bucca, C.; Heffler, E.; Paoletti, G.; Testino, E.; et al. One year of mepolizumab. Efficacy and safety in real-life in Italy. Pulm. Pharmacol. Ther. 2019, 58, 101836. [CrossRef] [PubMed]
Harvey, E.S.; Langton, D.; Katelaris, C.; Stevens, S.; Farah, C.S.; Gillman, A.; Harrington, J.; Hew, M.; Kritikos, V.; Radhakrishna, N.; et al. Mepolizumab effectiveness and identification of super-responders in severe asthma. Eur. Respir. J. 2020, 55, 1902420. [CrossRef] [PubMed]
Kavanagh, J.E.; d’Ancona, G.; Elstad, M.; Green, L.; Fernandes, M.; Thomson, L.; Roxas, C.; Dhariwal, J.; Nanzer, A.M.; Kent, B.D.; et al. Real-World Effectiveness and the Characteristics of a “Super-Responder” to Mepolizumab in Severe Eosinophilic Asthma. Chest 2020, 158, 491–500. [CrossRef]
Schleich, F.; Graff, S.; Nekoee, H.; Moermans, C.; Henket, M.; Sanchez, C.; Paulus, V.; Guissard, F.; Donneau, A.F.; Louis, R. Real-word experience with mepolizumab: Does it deliver what it has promised? Clin. Exp. Allergy J. Br. Soc. Allergy Clin. Immunol. 2020, 50, 687–695. [CrossRef]
Taille, C.; Chanez, P.; Devouassoux, G.; Didier, A.; Pison, C.; Garcia, G.; Charriot, J.; Bouee, S.; Gruber, A.; Pribil, C.; et al. Mepolizumab in a population with severe eosinophilic asthma and corticosteroid dependence: Results from a French early access programme. Eur. Respir. J. 2020, 55, 1902345. [CrossRef]
van Toor, J.J.; van der Mark, S.C.; Kappen, J.H.; In’t Veen, J.C.C.M.; Braunstahl, G.J. Mepolizumab add-on therapy in a real world cohort of patients with severe eosinophilic asthma: Response rate, effectiveness, and safety. J. Asthma Off. J. Assoc. Care Asthma 2021, 58, 651–658. [CrossRef]
Detoraki, A.; Tremante, E.; D’Amato, M.; Calabrese, C.; Casella, C.; Maniscalco, M.; Poto, R.; Brancaccio, R.; Boccia, M.; Martino, M.; et al. Mepolizumab improves sino-nasal symptoms and asthma control in severe eosinophilic asthma patients with chronic rhinosinusitis and nasal polyps: A 12-month real-life study. Ther. Adv. Respir. Dis. 2021, 15, 17534666211009398. [CrossRef]
Bachert, C.; Sousa, A.R.; Lund, V.J.; Scadding, G.K.; Gevaert, P.; Nasser, S.; Durham, S.R.; Cornet, M.E.; Kariyawasam, H.H.; Gilbert, J.; et al. Reduced need for surgery in severe nasal polyposis with mepolizumab: Randomized trial. J. Allergy Clin. Immunol. 2017, 140, 1024–1031.e14. [CrossRef]
Crimi, C.; Campisi, R.; Nolasco, S.; Cacopardo, G.; Intravaia, R.; Porto, M.; Impellizzeri, P.; Pelaia, C.; Crimi, N. Mepolizumab effectiveness in patients with severe eosinophilic asthma and co-presence of bronchiectasis: A real-world retrospective pilot study. Respir. Med. 2021, 185, 106491. [CrossRef] [PubMed]
Bleecker, E.R.; Wechsler, M.E.; FitzGerald, J.M.; Menzies-Gow, A.; Wu, Y.; Hirsch, I.; Goldman, M.; Newbold, P.; Zangrilli, J.G. Baseline patient factors impact on the clinical efficacy of benralizumab for severe asthma. Eur. Respir. J. 2018, 52, 1800936. [CrossRef] [PubMed]
Canonica, G.W.; Harrison, T.W.; Chanez, P.; Menzella, F.; Louis, R.; Cosio, B.G.; Lugogo, N.L.; Mohan, A.; Burden, A.; Garcia Gil, E. Benralizumab improves symptoms of patients with severe, eosinophilic asthma with a diagnosis of nasal polyposis. Allergy 2022, 77, 150–161. [CrossRef] [PubMed]
Harrison, T.W.; Chanez, P.; Menzella, F.; Canonica, G.W.; Louis, R.; Cosio, B.G.; Lugogo, N.L.; Mohan, A.; Burden, A.; McDermott, L.; et al. Onset of effect and impact on health-related quality of life, exacerbation rate, lung function, and nasal polyposis symptoms for patients with severe eosinophilic asthma treated with benralizumab (ANDHI): A randomised, controlled, phase 3b trial. Lancet Respir. Med. 2021, 9, 260–274. [CrossRef]
Bagnasco, D.; Brussino, L.; Bonavia, M.; Calzolari, E.; Caminati, M.; Caruso, C.; D’Amato, M.; De Ferrari, L.; Di Marco, F.; Imeri, G.; et al. Efficacy of Benralizumab in severe asthma in real life and focus on nasal polyposis. Respir. Med. 2020, 171, 106080. [CrossRef]
Nolasco, S.; Crimi, C.; Pelaia, C.; Benfante, A.; Caiaffa, M.F.; Calabrese, C.; Carpagnano, G.E.; Ciotta, D.; D’Amato, M.; Macchia, L.; et al. Benralizumab Effectiveness in Severe Eosinophilic Asthma with and without Chronic Rhinosinusitis with Nasal Polyps: A Real-World Multicenter Study. J. Allergy Clin. Immunol. Pract. 2021, 9, 4371–4380.e4. [CrossRef]
Chitguppi, C.; Patel, P.; Gandler, A.; Murphy, K.; Khoury Md, T.; Monostra, P.; Bork, S.; Toskala, E.; Rabinowitz, M.; Rosen, M.; et al. Effect of Benralizumab in Patients with Severe Eosinophilic Asthma and Chronic Rhinosinusitis with Nasal Polyps: A Case Series. Am. J. Rhinol. Allergy 2021, 35, 559–567. [CrossRef]
Lombardo, N.; Pelaia, C.; Ciriolo, M.; Della Corte, M.; Piazzetta, G.; Lobello, N.; Viola, P.; Pelaia, G. Real-life effects of benralizumab on allergic chronic rhinosinusitis and nasal polyposis associated with severe asthma. Int. J. Immunopathol. Pharmacol. 2020, 34, 2058738420950851. [CrossRef]
Matsuno, O.; Minamoto, S. Rapid effect of benralizumab for severe asthma with chronic rhinosinusitis with nasal polyps. Pulm. Pharmacol. Ther. 2020, 64, 101965. [CrossRef]
Tversky, J.; Lane, A.P.; Azar, A. Benralizumab effect on severe chronic rhinosinusitis with nasal polyps (CRSwNP): A randomized double-blind placebo-controlled trial. Clin. Exp. Allergy J. Br. Soc. Allergy Clin. Immunol. 2021, 51, 836–844. [CrossRef]
Gevaert, P.; Omachi, T.A.; Corren, J.; Mullol, J.; Han, J.; Lee, S.E.; Kaufman, D.; Ligueros-Saylan, M.; Howard, M.; Zhu, R.; et al. Efficacy and safety of omalizumab in nasal polyposis: 2 randomized phase 3 trials. J. Allergy Clin. Immunol. 2020, 146, 595–605. [CrossRef] [PubMed]
Damask, C.; Chen, M.; Holweg, C.T.J.; Yoo, B.; Millette, L.A.; Franzese, C. Defining the Efficacy of Omalizumab in Nasal Polyposis: A POLYP 1 and POLYP 2 Subgroup Analysis. Am. J. Rhinol. Allergy 2022, 36, 135–141. [CrossRef] [PubMed]
Gevaert, P.; Saenz, R.; Corren, J.; Han, J.K.; Mullol, J.; Lee, S.E.; Ow, R.A.; Zhao, R.; Howard, M.; Wong, K.; et al. Long-term efficacy and safety of omalizumab for nasal polyposis in an open-label extension study. J. Allergy Clin. Immunol. 2022, 149, 957–965.e3. [CrossRef] [PubMed]
Wu, Q.; Yuan, L.; Qiu, H.; Wang, X.; Huang, X.; Zheng, R.; Yang, Q. Efficacy and safety of omalizumab in chronic rhinosinusitis with nasal polyps: A systematic review and meta-analysis of randomised controlled trials. BMJ Open 2021, 11, e047344. [CrossRef]
Heffler, E.; Saccheri, F.; Bartezaghi, M.; Canonica, G.W. Effectiveness of omalizumab in patients with severe allergic asthma with and without chronic rhinosinusitis with nasal polyps: A PROXIMA study post hoc analysis. Clin. Transl. Allergy 2020, 10, 25. [CrossRef]
Tiotiu, A.; Oster, J.P.; Roux, P.R.; Nguyen Thi, P.L.; Peiffer, G.; Bonniaud, P.; Dalphin, J.C.; de Blay, F. Effectiveness of Omalizumab in Severe Allergic Asthma and Nasal Polyposis: A Real-Life Study. J. Investig. Allergol. Clin. Immunol. 2020, 30, 49–57. [CrossRef]
Bachert, C.; Han, J.K.; Desrosiers, M.; Hellings, P.W.; Amin, N.; Lee, S.E.; Mullol, J.; Greos, L.S.; Bosso, J.V.; Laidlaw, T.M.; et al. 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 2019, 394, 1638–1650. [CrossRef]
Laidlaw, T.M.; Bachert, C.; Amin, N.; Desrosiers, M.; Hellings, P.W.; Mullol, J.; Maspero, J.F.; Gevaert, P.; Zhang, M.; Mao, X.; et al. Dupilumab improves upper and lower airway disease control in chronic rhinosinusitis with nasal polyps and asthma. Ann. Allergy Asthma Immunol. Off. Publ. Am. Coll. Allergy Asthma Immunol. 2021, 126, 584–592.e1. [CrossRef]
Desrosiers, M.; Mannent, L.P.; Amin, N.; Canonica, G.W.; Hellings, P.W.; Gevaert, P.; Mullol, J.; Lee, S.E.; Fujieda, S.; Han, J.K.; et al. Dupilumab reduces systemic corticosteroid use and sinonasal surgery rate in CRSwNP. Rhinology 2021, 59, 301–311. [CrossRef]
Chuang, C.C.; Guillemin, I.; Bachert, C.; Lee, S.E.; Hellings, P.W.; Fokkens, W.J.; Duverger, N.; Fan, C.; Daizadeh, N.; Amin, N.; et al. Dupilumab in CRSwNP: Responder Analysis Using Clinically Meaningful Efficacy Outcome Thresholds. Laryn-goscope 2022, 132, 259–264. [CrossRef]
Hopkins, C.; Wagenmann, M.; Bachert, C.; Desrosiers, M.; Han, J.K.; Hellings, P.W.; Lee, S.E.; Msihid, J.; Radwan, A.; Rowe, P.; et al. Efficacy of dupilumab in patients with a history of prior sinus surgery for chronic rhinosinusitis with nasal polyps. Int. Forum Allergy Rhinol. 2021, 11, 1087–1101. [CrossRef] [PubMed]
Bachert, C.; Mannent, L.; Naclerio, R.M.; Mullol, J.; Ferguson, B.J.; Gevaert, P.; Hellings, P.; Jiao, L.; Wang, L.; Evans, R.R.; et al. Effect of Subcutaneous Dupilumab on Nasal Polyp Burden in Patients with Chronic Sinusitis and Nasal Polyposis: A Randomized Clinical Trial. JAMA 2016, 315, 469–479. [CrossRef] [PubMed]
Bachert, C.; Hellings, P.W.; Mullol, J.; Naclerio, R.M.; Chao, J.; Amin, N.; Grabher, A.; Swanson, B.N.; Hamilton, J.D.; Guillonneau, S.; et al. Dupilumab improves patient-reported outcomes in patients with chronic rhinosinusitis with nasal polyps and comorbid asthma. J. Allergy Clin. Immunol. Pract. 2019, 7, 2447–2449.e2. [CrossRef]
Wu, Q.; Zhang, Y.; Kong, W.; Wang, X.; Yuan, L.; Zheng, R.; Qiu, H.; Huang, X.; Yang, Q. Which Is the Best Biologic for Nasal Polyps: Dupilumab, Omalizumab, or Mepolizumab? A Network Meta-Analysis. Int. Arch. Allergy Immunol. 2022, 183, 279–288. [CrossRef] [PubMed]
Chong, L.Y.; Piromchai, P.; Sharp, S.; Snidvongs, K.; Webster, K.E.; Philpott, C.; Hopkins, C.; Burton, M.J. Biologics for chronic rhinosinusitis. Cochrane Database Syst. Rev. 2021, 3, CD013513.
Agache, I.; Song, Y.; Alonso-Coello, P.; Vogel, Y.; Rocha, C.; Sola, I.; Santero, M.; Akdis, C.A.; Akdis, M.; Canonica, G.W.; et al. Efficacy and safety of treatment with biologicals for severe chronic rhinosinusitis with nasal polyps: A systematic review for the EAACI guidelines. Allergy 2021, 76, 2337–2353. [CrossRef] [PubMed]
Peters, A.T.; Han, J.K.; Hellings, P.; Heffler, E.; Gevaert, P.; Bachert, C.; Xu, Y.; Chuang, C.C.; Neupane, B.; Msihid, J.; et al. Indirect Treatment Comparison of Biologics in Chronic Rhinosinusitis with Nasal Polyps. J. Allergy Clin. Immunol. Pract. 2021, 9, 2461–2471.e5. [CrossRef]
Meier, E.C.; Schmid-Grendelmeier, P.; Steiner, U.C.; Soyka, M.B. Real-Life Experience of Monoclonal Antibody Treatments in Chronic Rhinosinusitis with Nasal Polyposis. Int. Arch. Allergy Immunol. 2021, 182, 736–743. [CrossRef]
Gevaert, P.; Van Bruaene, N.; Cattaert, T.; Van Steen, K.; Van Zele, T.; Acke, F.; De Ruyck, N.; Blomme, K.; Sousa, A.R.; Marshall, R.P.; et al. Mepolizumab, a humanized anti-IL-5 mAb, as a treatment option for severe nasal polyposis. J. Allergy Clin. Immunol. 2011, 128, 989–995.e8. [CrossRef]
Bandi, F.; Gallo, S.; Preti, A.; Mozzanica, F.; Visca, D.; Marelli, M.; Maddalone, E.; Gambarini, C.; Vaghi, A.; Spanevello, A.; et al. Effects of biological therapies on chronic rhinosinusitis in severe asthmatic patients. Acta Otorhinolaryngol. Ital. Organo Uff. Della Soc. Ital. Otorinolaringol. Chir. Cervico-Facciale 2020, 40, 435–443. [CrossRef]
Bachert, C.; Han, J.K.; Desrosiers, M.Y.; Gevaert, P.; Heffler, E.; Hopkins, C.; Tversky, J.R.; Barker, P.; Cohen, D.; Emson, C.; et al. Efficacy and safety of benralizumab in chronic rhinosinusitis with nasal polyps: A randomized, placebo-controlled trial. J. Allergy Clin. Immunol. 2021, 149, 1309–1317.e12. [CrossRef] [PubMed]