Advertisement

European Archives of Oto-Rhino-Laryngology

, Volume 275, Issue 9, pp 2193–2202 | Cite as

Temporary olfactory improvement in chronic rhinosinusitis with nasal polyps after treatment

  • Dawei Wu
  • Benjamin S. Bleier
  • Yongxiang WeiEmail author
Review Article

Abstract

Purpose

Olfactory dysfunction in chronic rhinosinusitis with nasal polyps (CRSwNP) is a severe type of inflammatory olfactory disorders which greatly impair quality of life. The aim of this review is to summarize the current literature and to provide a comprehensive guide to the key metrics of the olfactory dysfunction, evaluations, treatment responses, and pathophysiological mechanisms in CRSwNP patients with olfactory dysfunction.

Methods

A review of the literature for olfaction in CRSwNP was conducted. The key terms (“chronic rhinosinusitis”, “nasal polyps”, and “olfaction”) were used to search relevant articles in Pubmed.

Results

Inflammation within the olfactory cleft is a well-recognized cause of the olfactory loss in patients with CRSwNP. Although the current treatment could significantly improve the olfactory function, olfaction in patients with CRSwNP tends to deteriorate after temporary improvement. Recent research has focused on the change of olfactory cleft and its association with the olfactory function which shed light on the mechanisms of both conductive and sensorineural olfactory dysfunctions in patients with CRSwNP. The state of the olfaction in patients with CRSwNP is directly associated with the degree of inflammation control and disturbed normal turnover of the olfactory sensory neurons induced by chronic inflammation, especially the eosinophilic inflammation contributes to the olfactory dysfunction. Refractory factors contributing to the olfactory deterioration are the promising therapeutic target to maintain the olfactory function in patients with CRSwNP.

Conclusions

The current evidence supports temporary olfactory improvement in CRSwNP patients which accords with the refractory nature of CRSwNP. Future treatment should aim to the continuous elimination of inflammation and promote the normal turnover of the olfactory epithelium.

Keywords

Olfaction Chronic rhinosinusitis Nasal polyps Evaluation Improvement Treatment Mechanism Neurogenesis 

Notes

Author contributions

All authors have contributed to the preparation and reviewing the final version of the manuscript.

Funding

This study was supported by the International Science & Technology Cooperation Program of China (2015DFA30160); the Natural Science Foundation of China (81670903).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Stevens WW, Schleimer RP, Kern RC (2016) Chronic rhinosinusitis with nasal polyps. J Allergy Clin Immunol Pract 4:565–572CrossRefPubMedCentralPubMedGoogle Scholar
  2. 2.
    Schleimer RP (2017) Immunopathogenesis of chronic rhinosinusitis and nasal polyposis. Annu Rev Pathol 12:331–357CrossRefPubMedGoogle Scholar
  3. 3.
    Kato A (2015) Immunopathology of chronic rhinosinusitis. Allergol Int 64:121–130CrossRefPubMedCentralPubMedGoogle Scholar
  4. 4.
    Fokkens WJ, Lund VJ, Mullol J, Bachert C, Alobid I, Baroody F, Cohen N, Cervin A, Douglas R, Gevaert P et al (2012) European position paper on rhinosinusitis and nasal polyps 2012. Rhinol Suppl 23:1–298 (3 p preceding table of contents) Google Scholar
  5. 5.
    Kohli P, Naik AN, Harruff EE, Nguyen SA, Schlosser RJ, Soler ZM (2017) The prevalence of olfactory dysfunction in chronic rhinosinusitis. Laryngoscope 127:309–320CrossRefPubMedGoogle Scholar
  6. 6.
    Litvack JR, Fong K, Mace J, James KE, Smith TL (2008) Predictors of olfactory dysfunction in patients with chronic rhinosinusitis. Laryngoscope 118:2225–2230CrossRefPubMedCentralPubMedGoogle Scholar
  7. 7.
    Croy I, Nordin S, Hummel T (2014) Olfactory disorders and quality of life—an updated review. Chem Senses 39:185–194CrossRefPubMedGoogle Scholar
  8. 8.
    Brämerson A, Johansson L, Ek L, Nordin S, Bende M (2004) Prevalence of olfactory dysfunction: the Skövde population-based study. Laryngoscope 114:733–737CrossRefPubMedGoogle Scholar
  9. 9.
    Katotomichelakis M, Simopoulos E, Zhang N, Tripsianis G, Danielides G, Livaditis M, Bachert C, Danielides V (2013) Olfactory dysfunction and asthma as risk factors for poor quality of life in upper airway diseases. Am J Rhinol Allergy 27:293–298CrossRefPubMedGoogle Scholar
  10. 10.
    Mattos JL, Schlosser RJ, Storck KA, Soler ZM (2017) Understanding the relationship between olfactory-specific quality of life, objective olfactory loss, and patient factors in chronic rhinosinusitis. In: International forum of allergy and rhinology. Wiley Online Library, Hoboken, pp 734–740Google Scholar
  11. 11.
    Schlosser RJ, Storck KA, Rudmik L, Smith TL, Mace JC, Mattos J, Soler ZM (2017) Association of olfactory dysfunction in chronic rhinosinusitis with economic productivity and medication usage. In: International forum of allergy and rhinology. Wiley Online Library, Hoboken, pp 50–55Google Scholar
  12. 12.
    Poletti SC, Murta G, Hähner A, Hummel T (2018) Olfactory cleft evaluation: a predictor for olfactory function in smell-impaired patients? Eur Arch Oto-Rhino-Laryngol 2018:1–9Google Scholar
  13. 13.
    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.  https://doi.org/10.1002/lary.27112 CrossRefPubMedGoogle Scholar
  14. 14.
    Lavin J, Min JY, Lidder AK, Huang JH, Kato A, Lam K, Meen E, Chmiel JS, Norton J, Suh L (2017) Superior turbinate eosinophilia correlates with olfactory deficit in chronic rhinosinusitis patients. Laryngoscope 127:2210–2218CrossRefPubMedGoogle Scholar
  15. 15.
    Kohli P, Naik AN, Farhood Z, Ong AA, Nguyen SA, Soler ZM, Schlosser RJ (2016) Olfactory outcomes after endoscopic sinus surgery for chronic rhinosinusitis: a meta-analysis. Otolaryngol Head Neck Surg 155:936–948CrossRefPubMedGoogle Scholar
  16. 16.
    Banglawala SM, Oyer SL, Lohia S, Psaltis AJ, Soler ZM, Schlosser RJ (2014) Olfactory outcomes in chronic rhinosinusitis with nasal polyposis after medical treatments: a systematic review and meta-analysis. In: International forum of allergy and rhinology. Wiley Online Library, Hoboken, pp 986–994Google Scholar
  17. 17.
    Levy JM, Mace JC, Sansoni ER, Soler ZM, Smith TL (2016) Longitudinal improvement and stability of olfactory function in the evaluation of surgical management for chronic rhinosinusitis. In: International forum of allergy and rhinology. Wiley Online Library, Hoboken, pp 1188–1195Google Scholar
  18. 18.
    Poetker DM, Jakubowski LA, Lal D, Hwang PH, Wright ED, Smith TL (2013) Oral corticosteroids in the management of adult chronic rhinosinusitis with and without nasal polyps: an evidence-based review with recommendations. Int Forum Allergy Rhinol 3:104–120CrossRefPubMedGoogle Scholar
  19. 19.
    Schwob JE, Jang W, Holbrook EH, Lin B, Herrick DB, Peterson JN, Hewitt Coleman J (2017) Stem and progenitor cells of the mammalian olfactory epithelium: taking poietic license. J Comp Neurol 525:1034–1054CrossRefPubMedGoogle Scholar
  20. 20.
    Yu CR, Wu Y (2017) Regeneration and rewiring of rodent olfactory sensory neurons. Exp Neurol 287:395–408CrossRefPubMedGoogle Scholar
  21. 21.
    Pozharskaya T, Liang J, Lane AP (2013) Regulation of inflammation-associated olfactory neuronal death and regeneration by the type II tumor necrosis factor receptor. In: International forum of allergy and rhinology. Wiley Online Library, Hoboken, pp 740–747Google Scholar
  22. 22.
    Turner JH, May L, Reed RR, Lane AP (2010) Reversible loss of neuronal marker protein expression in a transgenic mouse model for sinusitis-associated olfactory dysfunction. Am J Rhinol Allergy 24:192CrossRefPubMedCentralPubMedGoogle Scholar
  23. 23.
    Turner JH, Liang KL, May L, Lane AP (2010) Tumor necrosis factor alpha inhibits olfactory regeneration in a transgenic model of chronic rhinosinusitis-associated olfactory loss. Am J Rhinol Allergy 24:336CrossRefPubMedCentralPubMedGoogle Scholar
  24. 24.
    Tsybikov NN, Egorova EV, Kuznik BI, Fefelova EV, Magen E (2016) Neuron-specific enolase in nasal secretions as a novel biomarker of olfactory dysfunction in chronic rhinosinusitis. Am J Rhinol Allergy 30:65–69CrossRefPubMedGoogle Scholar
  25. 25.
    Hummel T, Whitcroft K, Andrews P, Altundag A, Cinghi C, Costanzo R, Damm M, Frasnelli J, Gudziol H, Gupta N (2017) Position paper on olfactory dysfunction. Rhinology 54:1–30PubMedGoogle Scholar
  26. 26.
    Kobal G, Hummel T, Sekinger B, Barz S, Roscher S, Wolf S (1996) " Sniffin’sticks”: screening of olfactory performance. Rhinology 34:222–226PubMedGoogle Scholar
  27. 27.
    Whitcroft KL, Cuevas M, Haehner A, Hummel T (2017) Patterns of olfactory impairment reflect underlying disease etiology. Laryngoscope 127:291–295CrossRefPubMedGoogle Scholar
  28. 28.
    Hedner M, Larsson M, Arnold N, Zucco GM, Hummel T (2010) Cognitive factors in odor detection, odor discrimination, and odor identification tasks. J Clin Exp Neuropsychol 32:1062–1067CrossRefPubMedGoogle Scholar
  29. 29.
    Jones-Gotman M, Zatorre RJ (1988) Olfactory identification deficits in patients with focal cerebral excision. Neuropsychologia 26:387–400CrossRefPubMedGoogle Scholar
  30. 30.
    Hornung DE, Kurtz DB, Bradshaw CB, Seipel DM, Kent PF, Blair DC, Emko P (1998) The olfactory loss that accompanies an HIV infection. Physiol Behav 64:549–556CrossRefPubMedGoogle Scholar
  31. 31.
    Whitcroft KL, Cuevas M, Andrews P, Hummel T (2018) Monitoring olfactory function in chronic rhinosinusitis and the effect of disease duration on outcome. In: International forum of allergy and rhinology. Wiley Online Library, HobokenGoogle Scholar
  32. 32.
    Kohli P, Schlosser RJ, Storck K, Soler ZM (2016) Olfactory cleft computed tomography analysis and olfaction in chronic rhinosinusitis. Am J Rhinol Allergy 30:402CrossRefPubMedCentralPubMedGoogle Scholar
  33. 33.
    Soler ZM, Hyer J, Karnezis TT, Schlosser RJ (2016) The Olfactory Cleft Endoscopy Scale correlates with olfactory metrics in patients with chronic rhinosinusitis. In: International forum of allergy and rhinology. Wiley Online Library, Hoboken, pp 293–298Google Scholar
  34. 34.
    Soler ZM, Pallanch JF, Sansoni ER, Jones CS, Lawrence LA, Schlosser RJ, Mace JC, Smith TL (2015) Volumetric computed tomography analysis of the olfactory cleft in patients with chronic rhinosinusitis. In: International forum of allergy and rhinology. Wiley Online Library, Hoboken, pp 846–854Google Scholar
  35. 35.
    Hauser LJ, Chandra RK, Li P, Turner JH (2017) Role of tissue eosinophils in chronic rhinosinusitis-associated olfactory loss. In: International forum of allergy and rhinology. Wiley Online Library, Hoboken, pp 957–962Google Scholar
  36. 36.
    Hox V, Callebaut I, Bobic S, Jorissen M, Hellings PW (2010) Nasal obstruction and smell impairment in nasal polyp disease: correlation between objective and subjective parameters. Rhinology 48:426PubMedGoogle Scholar
  37. 37.
    Mori E, Matsuwaki Y, Mitsuyama C, Okushi T, Nakajima T, Moriyama H (2013) Risk factors for olfactory dysfunction in chronic rhinosinusitis. Auris Nasus Larynx 40:465–469CrossRefPubMedGoogle Scholar
  38. 38.
    Schlosser RJ, Mulligan JK, Hyer JM, Karnezis TT, Gudis DA, Soler ZM (2016) Mucous cytokine levels in chronic rhinosinusitis-associated olfactory loss. JAMA Otolaryngol Head Neck Surg 142:731–737CrossRefPubMedCentralPubMedGoogle Scholar
  39. 39.
    Durack DT, Ackerman SJ, Loegering DA, Gleich GJ (1981) Purification of human eosinophil-derived neurotoxin. Proc Natl Acad Sci 78:5165–5169CrossRefPubMedGoogle Scholar
  40. 40.
    Fredens K, Dahl R, Venge P (1982) The Gordon phenomenon induced by the eosinophil cationic protein and eosinophil protein X. J Allergy Clin Immunol 70:361–366CrossRefPubMedGoogle Scholar
  41. 41.
    Lane AP, Turner J, May L, Reed R (2010) A genetic model of chronic rhinosinusitis-associated olfactory inflammation reveals reversible functional impairment and dramatic neuroepithelial reorganization. J Neurosci 30:2324–2329CrossRefPubMedCentralPubMedGoogle Scholar
  42. 42.
    Pozharskaya T, Lane AP (2013) Interferon gamma causes olfactory dysfunction without concomitant neuroepithelial damage. In: International forum of allergy and rhinology. Wiley Online Library, Hoboken, pp 861–865Google Scholar
  43. 43.
    Jankowski R, Bodino C (2003) Olfaction in patients with nasal polyposis: effects of systemic steroids and radical ethmoidectomy with middle turbinate resection (nasalisation). Rhinology 41:220–230PubMedGoogle Scholar
  44. 44.
    DeConde AS, Mace JC, Alt JA, Schlosser RJ, Smith TL, Soler ZM (2014) Comparative effectiveness of medical and surgical therapy on olfaction in chronic rhinosinusitis: a prospective, multi-institutional study. In: International forum of allergy and rhinology. Wiley Online Library, Hoboken, pp 725–733Google Scholar
  45. 45.
    Vaidyanathan S, Barnes M, Williamson P, Hopkinson P, Donnan PT, Lipworth B (2011) Treatment of chronic rhinosinusitis with nasal polyposis with oral steroids followed by topical steroids: a randomized trial. Ann Intern Med 154:293–302CrossRefPubMedGoogle Scholar
  46. 46.
    Gevaert P, Calus L, Van Zele T, Blomme K, De Ruyck N, Bauters W, Hellings P, Brusselle G, De Bacquer D, Van Cauwenberge P (2013) Omalizumab is effective in allergic and nonallergic patients with nasal polyps and asthma. J Allergy Clin Immunol 131:110.e111–116.e111.CrossRefGoogle Scholar
  47. 47.
    Bachert C, Mannent L, Naclerio RM, Mullol J, Ferguson BJ, Gevaert P, Hellings P, Jiao L, Wang L, Evans RR (2016) Effect of subcutaneous dupilumab on nasal polyp burden in patients with chronic sinusitis and nasal polyposis: a randomized clinical trial. JAMA 315:469–479CrossRefPubMedGoogle Scholar
  48. 48.
    Bachert C, Sousa AR, Lund VJ, Scadding GK, Gevaert P, Nasser S, Durham SR, Cornet ME, Kariyawasam HH, Gilbert J (2017) Reduced need for surgery in severe nasal polyposis with mepolizumab: randomized trial. J Allergy Clin Immunol 140:1024.e1014–1031.e1014.CrossRefGoogle Scholar
  49. 49.
    AlBader A, Levine CG, Casiano RR (2017) Does endoscopic sinus surgery improve olfaction in nasal polyposis? Laryngoscope 127:2203–2204CrossRefPubMedGoogle Scholar
  50. 50.
    Rombaux P, Huart C, Levie P, Cingi C, Hummel T (2016) Olfaction in chronic rhinosinusitis. Curr Allergy Asthma Rep 16:41CrossRefPubMedGoogle Scholar
  51. 51.
    Alobid I, Benítez P, Cardelús S, de Borja Callejas F, Lehrer-Coriat E, Pujols L, Picado C, Mullol J (2014) Oral plus nasal corticosteroids improve smell, nasal congestion, and inflammation in sino-nasal polyposis. Laryngoscope 124:50–56CrossRefPubMedGoogle Scholar
  52. 52.
    Gudis DA, Soler ZM (2016) Chronic rhinosinusitis-related smell loss: medical and surgical treatment efficacy. Curr Otorhinolaryngol Rep 4:142–147CrossRefPubMedCentralPubMedGoogle Scholar
  53. 53.
    Crisafulli U, Xavier AM, Santos FB, Cambiaghi TD, Chang SY, Porcionatto M, Castilho BA, Malnic B, Glezer I (2018) Topical dexamethasone administration impairs protein synthesis and neuronal regeneration in the olfactory epithelium. Front Mol Neurosci 11:50CrossRefPubMedCentralPubMedGoogle Scholar
  54. 54.
    Sivam A, Jeswani S, Reder L, Wang J, DeTineo M, Taxy J, Baroody FM, Naclerio RM, Pinto JM (2010) Olfactory cleft inflammation is present in seasonal allergic rhinitis and is reduced with intranasal steroids. Am J Rhinol Allergy 24:286–290CrossRefPubMedGoogle Scholar
  55. 55.
    Alobid I, Benitez P, Valero A, Munoz R, Langdon C, Mullol J (2012) Oral and intranasal steroid treatments improve nasal patency and paradoxically increase nasal nitric oxide in patients with severe nasal polyposis. Rhinology 50:171–177PubMedGoogle Scholar
  56. 56.
    Alobid I, Benitez P, Cardelus S, de Borja Callejas F, Lehrer-Coriat E, Pujols L, Picado C, Mullol J (2014) Oral plus nasal corticosteroids improve smell, nasal congestion, and inflammation in sino-nasal polyposis. Laryngoscope 124:50–56CrossRefPubMedGoogle Scholar
  57. 57.
    Banglawala SM, Oyer SL, Lohia S, Psaltis AJ, Soler ZM, Schlosser RJ (2014) Olfactory outcomes in chronic rhinosinusitis with nasal polyposis after medical treatments: a systematic review and meta-analysis. Int Forum Allergy Rhinol 4:986–994CrossRefPubMedGoogle Scholar
  58. 58.
    Schwob JE, Youngentob SL, Mezza RC (1995) Reconstitution of the rat olfactory epithelium after methyl bromide-induced lesion. J Comp Neurol 359:15–37CrossRefPubMedGoogle Scholar
  59. 59.
    Kanaya K, Kondo K, Suzukawa K, Sakamoto T, Kikuta S, Okada K, Yamasoba T (2014) Innate immune responses and neuroepithelial degeneration and regeneration in the mouse olfactory mucosa induced by intranasal administration of Poly (I: C). Cell Tissue Res 357:279–299CrossRefPubMedCentralPubMedGoogle Scholar
  60. 60.
    Yagi S, Tsukatani T, Yata T, Tsukioka F, Miwa T, Furukawa M (2007) Lipopolysaccharide-induced apoptosis of olfactory receptor neurons in rats. Acta Oto-laryngol 127:748–753CrossRefGoogle Scholar
  61. 61.
    Corps KN, Islam Z, Pestka JJ, Harkema JR (2010) Neurotoxic, inflammatory, and mucosecretory responses in the nasal airways of mice repeatedly exposed to the macrocyclic trichothecene mycotoxin roridin A: dose-response and persistence of injury. Toxicol Pathol 38:429–451CrossRefPubMedGoogle Scholar
  62. 62.
    Imamura F, Hasegawa-Ishii S (2016) Environmental toxicants-induced immune responses in the olfactory mucosa. Front Immunol 7:475CrossRefPubMedCentralPubMedGoogle Scholar
  63. 63.
    Gudziol V, Buschhüter D, Abolmaali N, Gerber J, Rombaux P, Hummel T (2009) Increasing olfactory bulb volume due to treatment of chronic rhinosinusitis—a longitudinal study. Brain 132:3096–3101CrossRefPubMedGoogle Scholar
  64. 64.
    Rombaux P, Potier H, Bertrand B, Duprez T, Hummel T (2008) Olfactory bulb volume in patients with sinonasal disease. Am J Rhinol 22:598–601CrossRefPubMedGoogle Scholar
  65. 65.
    Herzallah IR, Askar SM, Amer HS, Ahmed AF, El-Anwar MW, Eesa MH (2013) Olfactory bulb volume changes in patients with sinonasal polyposis: a magnetic resonance imaging study. Otolaryngol Head Neck Surg 148:689–693CrossRefPubMedGoogle Scholar
  66. 66.
    Alarabawy RA, Eltomey MA, Shehata EM (2016) Volumetric study of the olfactory bulb in patients with chronic rhinonasal sinusitis using MRI. Egypt J Radiol Nucl Med 47:487–491CrossRefGoogle Scholar
  67. 67.
    Han P, Whitcroft KL, Fischer J, Gerber J, Cuevas M, Andrews P, Hummel T (2017) Olfactory brain gray matter volume reduction in patients with chronic rhinosinusitis. In: International forum of allergy and rhinology. Wiley Online Library, Hoboken, pp 551–556Google Scholar
  68. 68.
    Curtis MA, Kam M, Nannmark U, Anderson MF, Axell MZ, Wikkelso C, Holtås S, van Roon-Mom WM, Björk-Eriksson T, Nordborg C (2007) Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 315:1243–1249CrossRefPubMedGoogle Scholar
  69. 69.
    Lledo P-M, Saghatelyan A, Lemasson M (2004) Inhibitory interneurons in the olfactory bulb: from development to function. Neuroscientist 10:292–303CrossRefPubMedGoogle Scholar
  70. 70.
    Rombaux P, Duprez T, Hummel T (2009) Olfactory bulb volume in the clinical assessment of olfactory dysfunction. Rhinology 47:3PubMedGoogle Scholar
  71. 71.
    Konkimalla A, Tata PR (2017) Plasticity in olfactory epithelium: is it a sniffer or shape shifter? Cell Stem Cell 21:707–708CrossRefPubMedGoogle Scholar
  72. 72.
    Choi R, Goldstein BJ (2018) Olfactory epithelium: cells, clinical disorders, and insights from an adult stem cell niche. Laryngoscope Investig Otolaryngol 3:35–42CrossRefPubMedCentralPubMedGoogle Scholar
  73. 73.
    Chen M, Reed RR, Lane AP (2017) Acute inflammation regulates neuroregeneration through the NF-κB pathway in olfactory epithelium. Proc Natl Acad Sci 114:8089–8094CrossRefPubMedGoogle Scholar
  74. 74.
    Yee KK, Pribitkin EA, Cowart BJ, Rosen D, Feng P, Rawson NE (2009) Analysis of the olfactory mucosa in chronic rhinosinusitis. Ann N Y Acad Sci 1170:590–595CrossRefPubMedCentralPubMedGoogle Scholar
  75. 75.
    Jafek BW, Murrow B, Michaels R, Restrepo D, Linschoten M (2002) Biopsies of human olfactory epithelium. Chem Senses 27:623–628CrossRefPubMedGoogle Scholar
  76. 76.
    Victores AJ, Chen M, Smith A, Lane AP (2018) Olfactory loss in chronic rhinosinusitis is associated with neuronal activation of c-Jun N-terminal kinase. In: International forum of allergy and rhinology. Wiley Online Library, Hoboken, pp 415–420Google Scholar
  77. 77.
    Oka H, Tsuzuki K, Takebayashi H, Kojima Y, Daimon T, Sakagami M (2013) Olfactory changes after endoscopic sinus surgery in patients with chronic rhinosinusitis. Auris Nasus Larynx 40:452–457CrossRefPubMedGoogle Scholar
  78. 78.
    Nguyen DT, Bey A, Arous F, Nguyen-Thi PL, Felix-Ravelo M, Jankowski R (2015) Can surgeons predict the olfactory outcomes after endoscopic surgery for nasal polyposis? Laryngoscope 125:1535–1540CrossRefPubMedGoogle Scholar
  79. 79.
    Kuperan AB, Lieberman SM, Jourdy DN, Al-Bar MH, Goldstein BJ, Casiano RR (2015) The effect of endoscopic olfactory cleft polyp removal on olfaction. Am J Rhinol Allergy 29:309–313CrossRefPubMedGoogle Scholar
  80. 80.
    Kim DW, Kim J-Y, Jeon S-Y (2011) The status of the olfactory cleft may predict postoperative olfactory function in chronic rhinosinusitis with nasal polyposis. Am J Rhinol Allergy 25:e90–e94CrossRefPubMedGoogle Scholar
  81. 81.
    Lee JT, Kennedy DW, Palmer JN, Feldman M, Chiu AG (2006) The incidence of concurrent osteitis in patients with chronic rhinosinusitis: a clinicopathological study. Am J Rhinol 20:278–282CrossRefPubMedGoogle Scholar
  82. 82.
    Giacchi RJ, Lebowitz RA, Yee HT, Light JP, Jacobs JB (2001) Histopathologic evaluation of the ethmoid bone in chronic sinusitis. Am J Rhinol 15:193–197CrossRefPubMedGoogle Scholar
  83. 83.
    Snidvongs K, McLachlan R, Sacks R, Earls P, Harvey RJ (2013) Correlation of the Kennedy Osteitis Score to clinico-histologic features of chronic rhinosinusitis. In: International forum of allergy and rhinology. Wiley Online Library, Hoboken, pp 369–375Google Scholar
  84. 84.
    Bhandarkar ND, Mace JC, Smith TL (2011) The impact of osteitis on disease severity measures and quality of life outcomes in chronic rhinosinusitis. In: International forum of allergy and rhinology. Wiley Online Library, Hoboken, pp 372–378Google Scholar
  85. 85.
    Zhao YC, Wormald P-J (2017) Biofilm and osteitis in refractory chronic rhinosinusitis. Otolaryngol Clin N Am 50:49–60CrossRefGoogle Scholar
  86. 86.
    Georgalas C, Videler W, Freling N, Fokkens W (2010) Global Osteitis Scoring Scale and chronic rhinosinusitis: a marker of revision surgery. Clin Otolaryngol 35:455–461CrossRefPubMedGoogle Scholar
  87. 87.
    Videler W, Georgalas C, Menger D, Freling N, Fokkens W (2011) Osteitic bone in recalcitrant chronic rhinosinusitis. Rhinology 49:139–147PubMedGoogle Scholar
  88. 88.
    Sethi N (2015) The significance of osteitis in rhinosinusitis. Eur Arch Otorhinolaryngol 272:821–826CrossRefPubMedGoogle Scholar
  89. 89.
    Bhandarkar ND, Sautter NB, Kennedy DW, Smith TL (2013) Osteitis in chronic rhinosinusitis: a review of the literature. In: International forum of allergy and rhinology. Wiley Online Library, Hoboken, pp 355–363Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Otolaryngology, Beijing Anzhen HospitalCapital Medical UniversityBeijingChina
  2. 2.Department of OtolaryngologyMassachusetts Eye and Ear InfirmaryBostonUSA
  3. 3.Department of OtolaryngologyHarvard Medical SchoolBostonUSA

Personalised recommendations