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Unified Airway—Cystic Fibrosis

  • Do-Yeon Cho
    Affiliations
    Department of Otolaryngology - Head & Neck Surgery, University of Alabama at Birmingham, 1155 Faculty Office Tower 510 20th Street South, Birmingham, AL 35233, USA

    Gregory Fleming James Cystic Fibrosis Research Center, University of Alabama at Birmingham, Birmingham, AL, USA

    Department of Surgery, Division of Otolaryngology, Veteran Affairs Medical Center, Birmingham, AL, USA
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  • Jessica W. Grayson
    Affiliations
    Department of Otolaryngology - Head & Neck Surgery, University of Alabama at Birmingham, 1155 Faculty Office Tower 510 20th Street South, Birmingham, AL 35233, USA
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  • Bradford A. Woodworth
    Correspondence
    Corresponding author.
    Affiliations
    Department of Otolaryngology - Head & Neck Surgery, University of Alabama at Birmingham, 1155 Faculty Office Tower 510 20th Street South, Birmingham, AL 35233, USA

    Gregory Fleming James Cystic Fibrosis Research Center, University of Alabama at Birmingham, Birmingham, AL, USA
    Search for articles by this author
Published:October 17, 2022DOI:https://doi.org/10.1016/j.otc.2022.09.009

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      References

        • Moller W.
        • Haussinger K.
        • Ziegler-Heitbrock L.
        • et al.
        Mucociliary and long-term particle clearance in airways of patients with immotile cilia.
        Respir Res. 2006; 7: 10
        • Tipirneni K.E.
        • Woodworth B.A.
        Medical and surgical advancements in the management of cystic fibrosis chronic rhinosinusitis.
        Curr Otorhinolaryngol Rep. 2017; 5: 24-34
        • Chaaban M.R.
        • Kejner A.
        • Rowe S.M.
        • et al.
        Cystic fibrosis chronic rhinosinusitis: a comprehensive review.
        Am J Rhinol Allergy. 2013; 27: 387-395
        • Birket S.E.
        • Chu K.K.
        • Liu L.
        • et al.
        A functional anatomic defect of the cystic fibrosis airway.
        Am J Respir Crit Care Med. 2014; 190: 421-432
        • Knowles M.R.
        • Durie P.R.
        What is cystic fibrosis?.
        N Engl J Med. 2002; 347: 439-442
        • Wang X.
        • Moylan B.
        • Leopold D.A.
        • et al.
        Mutation in the gene responsible for cystic fibrosis and predisposition to chronic rhinosinusitis in the general population.
        JAMA. 2000; 284: 1814-1819
        • Raman V.
        • Clary R.
        • Siegrist K.L.
        • et al.
        Increased prevalence of mutations in the cystic fibrosis transmembrane conductance regulator in children with chronic rhinosinusitis.
        Pediatrics. 2002; 109: E13
        • Cho D.Y.
        • Hwang P.H.
        • Illek B.
        Effect of L-ascorbate on chloride transport in freshly excised sinonasal epithelia.
        Am J Rhinol Allergy. 2009; 23: 294-299
        • McCormick J.
        • Hoffman K.
        • Thompson H.
        • et al.
        Differential chloride secretory capacity in transepithelial ion transport properties in chronic rhinosinusitis.
        Am J Rhinol Allergy. 2020; 34: 830-837
        • Tipirneni K.E.
        • Zhang S.
        • Cho D.Y.
        • et al.
        Submucosal gland mucus strand velocity is decreased in chronic rhinosinusitis.
        Int Forum Allergy Rhinology. 2018; 8: 509-512
        • Courville C.A.
        • Tidwell S.
        • Liu B.
        • et al.
        Acquired defects in CFTR-dependent beta-adrenergic sweat secretion in chronic obstructive pulmonary disease.
        Respir Res. 2014; 15: 25
        • Dransfield M.T.
        • Wilhelm A.M.
        • Flanagan B.
        • et al.
        Acquired cystic fibrosis transmembrane conductance regulator dysfunction in the lower airways in COPD.
        Chest. 2013; 144: 498-506
        • Rab A.
        • Rowe S.M.
        • Raju S.V.
        • et al.
        Cigarette smoke and CFTR: implications in the pathogenesis of COPD.
        Am J Physiol Lung Cell Mol Physiol. 2013; 305: L530-L541
        • Raju S.V.
        • Jackson P.L.
        • Courville C.A.
        • et al.
        Cigarette smoke induces systemic defects in cystic fibrosis transmembrane conductance regulator function.
        Am J Respir Crit Care Med. 2013; 188: 1321-1330
        • Raju S.V.
        • Tate J.H.
        • Peacock S.K.
        • et al.
        Impact of heterozygote CFTR mutations in COPD patients with chronic bronchitis.
        Respir Res. 2014; 15: 18
        • Sloane P.A.
        • Shastry S.
        • Wilhelm A.
        • et al.
        A pharmacologic approach to acquired cystic fibrosis transmembrane conductance regulator dysfunction in smoking related lung disease.
        PLoS One. 2012; 7: e39809
        • Alexander N.S.
        • Blount A.
        • Zhang S.
        • et al.
        Cystic fibrosis transmembrane conductance regulator modulation by the tobacco smoke toxin acrolein.
        Laryngoscope. 2012; 122: 1193-1197
        • Virgin F.W.
        • Azbell C.
        • Schuster D.
        • et al.
        Exposure to cigarette smoke condensate reduces calcium activated chloride channel transport in primary sinonasal epithelial cultures.
        Laryngoscope. 2010; 120: 1465-1469
        • Cohen N.A.
        • Zhang S.
        • Sharp D.B.
        • et al.
        Cigarette smoke condensate inhibits transepithelial chloride transport and ciliary beat frequency.
        Laryngoscope. 2009; 119: 2269-2274
        • Woodworth B.A.
        Resveratrol ameliorates abnormalities of fluid and electrolyte secretion in a hypoxia-Induced model of acquired CFTR deficiency.
        Laryngoscope. 2015; 125: S1-S13
        • Tipirneni K.E.
        • Grayson J.W.
        • Zhang S.
        • et al.
        Assessment of acquired mucociliary clearance defects using micro-optical coherence tomography.
        Int Forum Allergy Rhinology. 2017; 7: 920-925
        • Banks C.
        • Freeman L.
        • Cho D.Y.
        • et al.
        Acquired cystic fibrosis transmembrane conductance regulator dysfunction.
        World J Otorhinolaryngol Head Neck Surg. 2018; 4: 193-199
        • Guimbellot J.S.
        • Fortenberry J.A.
        • Siegal G.P.
        • et al.
        Role of oxygen availability in CFTR expression and function.
        Am J Respir Cell Mol Biol. 2008; 39: 514-521
        • Zhang S.
        • Skinner D.
        • Hicks S.B.
        • et al.
        Sinupret activates CFTR and TMEM16A-dependent transepithelial chloride transport and improves indicators of mucociliary clearance.
        PLoS One. 2014; 9: e104090
        • Lim D.J.
        • McCormick J.
        • Skinner D.
        • et al.
        Controlled delivery of ciprofloxacin and ivacaftor via sinus stent in a preclinical model of Pseudomonas sinusitis.
        Int Forum Allergy Rhinology. 2020; 10: 481-488
        • Cho D.Y.
        • Skinner D.
        • Mackey C.
        • et al.
        Herbal dry extract BNO 1011 improves clinical and mucociliary parameters in a rabbit model of chronic rhinosinusitis.
        Int Forum Allergy Rhinology. 2019; 9: 629-637
        • Cho D.-Y.
        • Mackey C.
        • Van Der Pol W.J.
        • et al.
        Sinus microanatomy and microbiota in a rabbit model of rhinosinusitis.
        Front Cell Infect Microbiol. 2018; 7: 540
        • Cho D.Y.
        • Lim D.J.
        • Mackey C.
        • et al.
        Preclinical therapeutic efficacy of the ciprofloxacin-eluting sinus stent for Pseudomonas aeruginosa sinusitis.
        Int Forum Allergy Rhinology. 2018; 8: 482-489
        • Lim D.J.
        • Skinner D.
        • West J.M.
        • et al.
        In vitro evaluation of a novel oxygen-generating biomaterial for chronic rhinosinusitis therapy.
        Int Forum Allergy Rhinology. 2022; 12: 181-190
        • Blount A.
        • Zhang S.
        • Chestnut M.
        • et al.
        Transepithelial ion transport is suppressed in hypoxic sinonasal epithelium.
        Laryngoscope. 2011; 121: 1929-1934
        • Chiu A.G.
        • Palmer J.N.
        • Woodworth B.A.
        • et al.
        Baby shampoo nasal irrigations for the symptomatic post-functional endoscopic sinus surgery patient.
        Am J Rhinol. 2008; 22: 34-37
        • Cho D.Y.
        • Skinner D.
        • Hunter R.C.
        • et al.
        Contribution of short chain fatty acids to the growth of pseudomonas aeruginosa in rhinosinusitis.
        Front Cell Infect Microbiol. 2020; 10: 412
        • Cho D.Y.
        • Zhang S.
        • Lazrak A.
        • et al.
        LPS decreases CFTR open probability and mucociliary transport through generation of reactive oxygen species.
        Redox Biol. 2021; 43: 101998
        • Cho D.Y.
        • Zhang S.
        • Skinner D.F.
        • et al.
        Ivacaftor restores delayed mucociliary transport caused by Pseudomonas aeruginosa-induced acquired cystic fibrosis transmembrane conductance regulator dysfunction in rabbit nasal epithelia.
        Int Forum Allergy Rhinology. 2022; 12: 690-698
        • Londino J.D.
        • Lazrak A.
        • Noah J.W.
        • et al.
        Influenza virus M2 targets cystic fibrosis transmembrane conductance regulator for lysosomal degradation during viral infection.
        FASEB J. 2015; 29: 2712-2725
        • Kern R.C.
        • Conley D.B.
        • Walsh W.
        • et al.
        Perspectives on the etiology of chronic rhinosinusitis: an immune barrier hypothesis.
        Am J Rhinol. 2008; 22: 549-559
        • Schleimer R.P.
        • Kato A.
        • Peters A.
        • et al.
        Epithelium, inflammation, and immunity in the upper airways of humans: studies in chronic rhinosinusitis.
        Proc Am Thorac Soc. 2009; 6: 288-294
        • Bernstein J.M.
        • Ballow M.
        • Schlievert P.M.
        • et al.
        A superantigen hypothesis for the pathogenesis of chronic hyperplastic sinusitis with massive nasal polyposis.
        Am J Rhinol. 2003; 17: 321-326
        • Perloff J.R.
        • Palmer J.N.
        Evidence of bacterial biofilms in a rabbit model of sinusitis.
        Am J Rhinol. 2005; 19: 1-6
        • Khalid A.N.
        • Woodworth B.A.
        • Prince A.
        • et al.
        Physiologic alterations in the murine model after nasal fungal antigenic exposure.
        Otolaryngology--Head Neck Surg. 2008; 139: 695-701
        • Krouse J.H.
        • Brown R.W.
        • Fineman S.M.
        • et al.
        Asthma and the unified airway.
        Otolaryngol Head Neck Surg. 2007; 136: S75-S106
        • Illing E.A.
        • Woodworth B.A.
        Management of the upper airway in cystic fibrosis.
        Curr Opin Pulm Med. 2014; 20: 623-631
        • Senior B.A.
        • Kennedy D.W.
        • Tanabodee J.
        • et al.
        Long-term impact of functional endoscopic sinus surgery on asthma.
        Otolaryngol Head Neck Surg. 1999; 121: 66-68
        • Hamilos D.L.
        Chronic sinusitis.
        J Allergy Clin Immunol. 2000; 106: 213-227
        • Batra P.S.
        • Kern R.C.
        • Tripathi A.
        • et al.
        Outcome analysis of endoscopic sinus surgery in patients with nasal polyps and asthma.
        Laryngoscope. 2003; 113: 1703-1706
        • Munck A.
        • Bonacorsi S.
        • Mariani-Kurkdjian P.
        • et al.
        Genotypic characterization of Pseudomonas aeruginosa strains recovered from patients with cystic fibrosis after initial and subsequent colonization.
        Pediatr Pulmonol. 2001; 32: 288-292
        • Koch C.
        Early infection and progression of cystic fibrosis lung disease.
        Pediatr Pulmonol. 2002; 34: 232-236
        • Johansen H.K.
        • Aanaes K.
        • Pressler T.
        • et al.
        Colonisation and infection of the paranasal sinuses in cystic fibrosis patients is accompanied by a reduced PMN response.
        J Cyst Fibros. 2012; 11: 525-531
        • Aanaes K.
        • von Buchwald C.
        • Hjuler T.
        • et al.
        The effect of sinus surgery with intensive follow-up on pathogenic sinus bacteria in patients with cystic fibrosis.
        Am J Rhinol Allergy. 2013; 27: e1-e4
        • Lavin J.
        • Bhushan B.
        • Schroeder Jr., J.W.
        Correlation between respiratory cultures and sinus cultures in children with cystic fibrosis.
        Int J Pediatr Otorhinolaryngol. 2013; 77: 686-689
        • Ciofu O.
        • Johansen H.K.
        • Aanaes K.
        • et al.
        P. aeruginosa in the paranasal sinuses and transplanted lungs have similar adaptive mutations as isolates from chronically infected CF lungs.
        J Cyst Fibros. 2013; 12: 729-736
        • Mainz J.G.
        • Naehrlich L.
        • Schien M.
        • et al.
        Concordant genotype of upper and lower airways P aeruginosa and S aureus isolates in cystic fibrosis.
        Thorax. 2009; 64: 535-540
        • Chang E.H.
        New insights into the pathogenesis of cystic fibrosis sinusitis.
        Int Forum Allergy Rhinol. 2014; 4: 132-137
        • Spielman D.B.
        • Beswick D.M.
        • Kimple A.J.
        • et al.
        The management of cystic fibrosis chronic rhinosinusitis: An evidenced-based review with recommendations.
        Int Forum Allergy Rhinology. 2022; 12: 1148-1183
        • Kimple A.J.
        • Senior B.A.
        • Naureckas E.T.
        • et al.
        Cystic Fibrosis foundation otolaryngology care multidisciplinary consensus recommendations.
        Int Forum Allergy Rhinology. 2022; 12: 1089-1103
        • Georgalas C.
        • Cornet M.
        • Adriaensen G.
        • et al.
        Evidence-based surgery for chronic rhinosinusitis with and without nasal polyps.
        Curr Allergy Asthma Rep. 2014; 14: 427
        • Vlastarakos P.V.
        • Fetta M.
        • Segas J.V.
        • et al.
        Functional endoscopic sinus surgery improves sinus-related symptoms and quality of life in children with chronic rhinosinusitis: a systematic analysis and meta-analysis of published interventional studies.
        Clin Pediatr. 2013; 52: 1091-1097
        • Virgin F.W.
        • Rowe S.M.
        • Wade M.B.
        • et al.
        Extensive surgical and comprehensive postoperative medical management for cystic fibrosis chronic rhinosinusitis.
        Am J Rhinol Allergy. 2012; 26: 70-75
        • Woodworth B.A.
        • Parker R.O.
        • Schlosser R.J.
        Modified endoscopic medial maxillectomy for chronic maxillary sinusitis.
        Am J Rhinol. 2006; 20: 317-319
        • McCormick J.P.
        • Hicks M.D.
        • Grayson J.W.
        • et al.
        Endoscopic management of maxillary sinus diseases of dentoalveolar origin.
        Oral Maxillofacial Surg Clin N Am. 2020; 32: 639-648
        • Cho D.Y.
        • Hwang P.H.
        Results of endoscopic maxillary mega-antrostomy in recalcitrant maxillary sinusitis.
        Am J Rhinol. 2008; 22: 658-662
        • Ramsey B.W.
        • Davies J.
        • McElvaney N.G.
        • et al.
        A CFTR potentiator in patients with cystic fibrosis and the G551D mutation.
        N Engl J Med. 2011; 365: 1663-1672
        • Chang E.H.
        • Tang X.X.
        • Shah V.S.
        • et al.
        Medical reversal of chronic sinusitis in a cystic fibrosis patient with ivacaftor.
        Int Forum Allergy Rhinol. 2015; 5: 178-181
        • Hayes Jr., D.
        • McCoy K.S.
        • Sheikh S.I.
        Improvement of sinus disease in cystic fibrosis with ivacaftor therapy.
        Am J Respir Crit Care Med. 2014; 190: 468
        • Lee S.E.
        • Farzal Z.
        • Daniels M.L.A.
        • et al.
        Cystic Fibrosis Transmembrane Conductance Regulator Modulator Therapy: A Review for the Otolaryngologist.
        Am J Rhinol Allergy. 2020; 34: 573-580
        • Beswick D.M.
        • Humphries S.M.
        • Balkissoon C.D.
        • et al.
        Machine learning evaluates improvement in sinus computed tomography opacification with CFTR modulator therapy.
        Int Forum Allergy Rhinol. 2021; 11: 953-954
        • DiMango E.
        • Overdevest J.
        • Keating C.
        • et al.
        Effect of highly effective modulator treatment on sinonasal symptoms in cystic fibrosis.
        J Cyst Fibros. 2021; 20: 460-463
        • Douglas J.E.
        • Civantos A.M.
        • Locke T.B.
        • et al.
        Impact of novel CFTR modulator on sinonasal quality of life in adult patients with cystic fibrosis.
        Int Forum Allergy Rhinol. 2021; 11: 201-203
        • Raju S.V.
        • Lin V.Y.
        • Liu L.
        • et al.
        The Cystic fibrosis transmembrane conductance regulator potentiator ivacaftor augments mucociliary clearance abrogating cystic fibrosis transmembrane conductance regulator inhibition by cigarette smoke.
        Am J Respir Cell Mol Biol. 2017; 56: 99-108
        • Solomon G.M.
        • Fu L.
        • Rowe S.M.
        • et al.
        The therapeutic potential of CFTR modulators for COPD and other airway diseases.
        Curr Opin Pharmacol. 2017; 34: 132-139
        • Dey I.
        • Shah K.
        • Bradbury N.A.
        Natural compounds as therapeutic agents in the treatment cystic fibrosis.
        J Genet Syndr Gene Ther. 2016; 7: 284
        • Carlile G.W.
        • Keyzers R.A.
        • Teske K.A.
        • et al.
        Correction of F508del-CFTR trafficking by the sponge alkaloid latonduine is modulated by interaction with PARP.
        Chem Biol. 2012; 19: 1288-1299
        • Springsteel M.F.
        • Galietta L.J.
        • Ma T.
        • et al.
        Benzoflavone activators of the cystic fibrosis transmembrane conductance regulator: towards a pharmacophore model for the nucleotide-binding domain.
        Bioorg Med Chem. 2003; 11: 4113-4120
        • Galietta L.J.
        • Springsteel M.F.
        • Eda M.
        • et al.
        Novel CFTR chloride channel activators identified by screening of combinatorial libraries based on flavone and benzoquinolizinium lead compounds.
        J Biol Chem. 2001; 276: 19723-19728
        • Caci E.
        • Folli C.
        • Zegarra-Moran O.
        • et al.
        CFTR activation in human bronchial epithelial cells by novel benzoflavone and benzimidazolone compounds.
        Am J Physiol Lung Cell Mol Physiol. 2003; 285: L180-L188
        • Zhang S.
        • Blount A.C.
        • McNicholas C.M.
        • et al.
        Resveratrol enhances airway surface liquid depth in sinonasal epithelium by increasing cystic fibrosis transmembrane conductance regulator open probability.
        PLoS One. 2013; 8: e81589
        • Conger B.T.
        • Zhang S.
        • Skinner D.
        • et al.
        Comparison of cystic fibrosis transmembrane conductance regulator (CFTR) and ciliary beat frequency activation by the CFTR Modulators Genistein, VRT-532, and UCCF-152 in primary sinonasal epithelial cultures.
        JAMA Otolaryngol Head Neck Surg. 2013; 139: 822-827
        • Zhang S.
        • Smith N.
        • Schuster D.
        • et al.
        Quercetin increases cystic fibrosis transmembrane conductance regulator-mediated chloride transport and ciliary beat frequency: therapeutic implications for chronic rhinosinusitis.
        Am J Rhinol Allergy. 2011; 25: 307-312
        • Alexander N.S.
        • Hatch N.
        • Zhang S.
        • et al.
        Resveratrol has salutary effects on mucociliary transport and inflammation in sinonasal epithelium.
        Laryngoscope. 2011; 121: 1313-1319
        • Azbell C.
        • Zhang S.
        • Skinner D.
        • et al.
        Hesperidin stimulates cystic fibrosis transmembrane conductance regulator-mediated chloride secretion and ciliary beat frequency in sinonasal epithelium.
        Otolaryngol Head Neck Surg. 2010; 143: 397-404
        • Virgin F.
        • Zhang S.
        • Schuster D.
        • et al.
        The bioflavonoid compound, sinupret, stimulates transepithelial chloride transport in vitro and in vivo.
        Laryngoscope. 2010; 120: 1051-1056
        • Tarran R.
        • Button B.
        • Boucher R.C.
        Regulation of normal and cystic fibrosis airway surface liquid volume by phasic shear stress.
        Annu Rev Physiol. 2006; 68: 543-561
        • Mall M.A.
        • Galietta L.J.
        Targeting ion channels in cystic fibrosis.
        J Cyst Fibros. 2015; 14: 561-570
        • Cho D.Y.
        • Skinner D.
        • Zhang S.
        • et al.
        Korean Red Ginseng aqueous extract improves markers of mucociliary clearance by stimulating chloride secretion.
        J Ginseng Res. 2021; 45: 66-74