Volume 147, Issue 2 p. 351-356

Sinonasal Disorders

Exhaled Nitric Oxide Measurement in Patients Affected by Nasal Polyposis

Jacopo Galli MD,

Jacopo Galli MD

ENT Institute, Catholic University of the Sacred Heart Rome, Rome, Italy

These authors contributed equally to this study.

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Paolo Montuschi MD,

Paolo Montuschi MD

Pharmacology Institute, Catholic University of the Sacred Heart Rome, Rome, Italy

These authors contributed equally to this study.

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Giulio Cesare Passàli MD, PhD,

Corresponding Author

Giulio Cesare Passàli MD, PhD

[email protected]

ENT Institute, Catholic University of the Sacred Heart Rome, Rome, Italy

Giulio Cesare Passàli, MD, PhD, Otorhinolaryingology Department, Catholic University of the Sacred Heart Medical School, L.go Vito 1, 00168 Rome, Italy Email: [email protected]Search for more papers by this author

Marianna Laruffa MD,

Marianna Laruffa MD

ENT Institute, Catholic University of the Sacred Heart Rome, Rome, Italy

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Claudio Parrilla MD, PhD,

Claudio Parrilla MD, PhD

ENT Institute, Catholic University of the Sacred Heart Rome, Rome, Italy

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Gaetano Paludetti MD,

Gaetano Paludetti MD

ENT Institute, Catholic University of the Sacred Heart Rome, Rome, Italy

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Jacopo Galli MD,

Jacopo Galli MD

ENT Institute, Catholic University of the Sacred Heart Rome, Rome, Italy

These authors contributed equally to this study.

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Paolo Montuschi MD,

Paolo Montuschi MD

Pharmacology Institute, Catholic University of the Sacred Heart Rome, Rome, Italy

These authors contributed equally to this study.

Search for more papers by this author

Giulio Cesare Passàli MD, PhD,

Corresponding Author

Giulio Cesare Passàli MD, PhD

[email protected]

ENT Institute, Catholic University of the Sacred Heart Rome, Rome, Italy

Marianna Laruffa MD,

Marianna Laruffa MD

ENT Institute, Catholic University of the Sacred Heart Rome, Rome, Italy

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Claudio Parrilla MD, PhD,

Claudio Parrilla MD, PhD

ENT Institute, Catholic University of the Sacred Heart Rome, Rome, Italy

Search for more papers by this author

Gaetano Paludetti MD,

Gaetano Paludetti MD

ENT Institute, Catholic University of the Sacred Heart Rome, Rome, Italy

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First published: 02 April 2012

https://doi.org/10.1177/0194599812442322

Citations: 1

Sponsorships or competing interests that may be relevant to content are disclosed at the end of this article.

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Abstract

Objectives

Nitric oxide (NO) is produced in the respiratory tract with a major contribution coming from paranasal sinuses and the nose. The pathophysiological role of NO in the airways has been debated. The aims of this study were to measure fraction of exhaled NO (FENO), a validated marker of airway inflammation, in patients affected by nasal polyposis with and without asthma; to assess the importance of FENO measurement in detecting subclinical involvement of lower airways in patients with clinical rhinosinusal symptoms; and to clarify the impact of endoscopic surgical removal of polyps on airway inflammation.

Setting

The study was conducted at the O.R.L. Clinic and Clinical Pharmacology Unit, University Hospital Agostino Gemelli, Rome, Italy.

Study Design

Prospective study.

Subjects and Methods

Concentrations of FENO were measured with the NIOX system (Aerocrine, Stockholm, Sweden) by using a single-breath online method, according to the American Thoracic Society guidelines.

Results

Compared with those in healthy subjects (15 [11-19] ppb, n = 15; P <. 0001), FENO values were elevated in patients with nasal polyposis (41 [21-77] ppb, n = 43). There was no significant difference in FENO concentrations between asthmatic and nonasthmatic patients with nasal polyposis (P =. 73). Concentrations of FENO in patients with nasal polyposis were decreased after surgery (64.2 [30.0-132.7] ppb vs 56.0 [26.4-73.8] ppb, respectively; P =. 03).

Conclusion

The fraction of exhaled NO is elevated in the inflammatory process involving both the rhinosinusal district and lower airways, supporting the one-airway disease hypothesis.

References

1.Bredt DS, Snyder SH. Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. Proc Natl Acad Sci. 1990; 87: 682-685.
10.1073/pnas.87.2.682
CASPubMedWeb of Science®Google Scholar
2.Ragab SM, Lund VJ, Saleh HA, Scadding G. Nasal nitric oxide in objective evaluation of chronic rhinosinusitis therapy. Allergy. 2006; 61: 717-724.
10.1111/j.1398-9995.2006.01044.x
CASPubMedWeb of Science®Google Scholar
3.Watkins DN, Peroni DJ, Basclain KA, Garlepp MJ, Thompson PJ. Expression and activity of nitric oxide synthase in human airways epithelium. Am J Respir Cell Mol Biol. 1997; 16: 629-639.
10.1165/ajrcmb.16.6.9191464
CASPubMedWeb of Science®Google Scholar
4.Jeon SY, Kim E, Ma YW, Kim JP, Jung TG, Hwang EG. Nitric oxide mediates platelet activating factor-induced microvascular leakage in rat airways. Ann Otol Rhinol Laryngol. 2001; 110: 83-86.
10.1177/000348940111000115
CASPubMedWeb of Science®Google Scholar
5.Croen KD. Evidence for antiviral effect of nitric oxide. J Clin Invest. 1993; 91: 2446-2452.
10.1172/JCI116479
CASPubMedWeb of Science®Google Scholar
6.Sanders SP, Siekierski ES, Richards SM, Porter JD, Imani F, Proud D. Rhinovirus infection induces expression of type 2 nitric oxide synthase in human respiratory epithelial cells in vitro and in vivo. J Allergy Clin Immunol. 2001; 107: 245-243.
10.1067/mai.2001.112028
Web of Science®Google Scholar
7.Mancinelli RL, McKay CP. Effects of nitric oxide and nitrogen dioxide on bacterial growth. Appl Environ Microbiol. 1983; 46: 198-202.
10.1128/aem.46.1.198-202.1983
CASPubMedWeb of Science®Google Scholar
8.Al-Ali MK, Howarth PH. Nitric oxide and the respiratory system in health and disease. Respir Med. 1998; 92: 701-715.
10.1016/S0954-6111(98)90000-2
CASPubMedWeb of Science®Google Scholar
9.Runer T, Cervin A, Lindberg S. Nitric oxide is a regulator of mucociliary activity in the upper respiratory tract. Otolaryngol Head Neck Surg. 1998; 119: 278-287.
10.1016/S0194-5998(98)70063-4
CASPubMedWeb of Science®Google Scholar
10.Jain B, Rubinstain I, Robbins RA, Leise KL, Sisson JH. Modulation of airway epithelial cell ciliary beat frequency by nitric oxide. Biochem Biophys Res Commun. 1993; 191: 83-88.
10.1006/bbrc.1993.1187
CASPubMedWeb of Science®Google Scholar
11.Gaston B, Reilly J, Drazen JM, et al. Endogenous nitrogen oxides and broncodilator S-nitrosothiols in human airways. Proc Natl Acad Sci USA. 1993; 90: 10956-10961.
10.1073/pnas.90.23.10957
Web of Science®Google Scholar
12.Liu SF, Crawley DE, Barnes PJ, Evans TW. Endothelium-derived relaxing factor inhibits hypoxic pulmonary vasoconstriction in rats. Am Rev Respir Dis. 1991; 143: 32-37.
10.1164/ajrccm/143.1.32
CASPubMedWeb of Science®Google Scholar
13.Rubbo H, Radi R, Trujillo M, et al. Nitric oxide regulation of superoxide and oxynitrite-dependent lipid peroxidation: formation of novel nitrogen-containing oxidized lipid derivates. J Biol Chem. 1994; 269: 26066-26075.
10.1016/S0021-9258(18)47160-8
CASPubMedWeb of Science®Google Scholar
14.Lindberg JON, Farkas-Szallasi T, Weitzberg E, et al. High nitric oxide production in human paranasal sinuses. Nat Med. 1995; 1: 370-373.
10.1038/nm0495-370
PubMedWeb of Science®Google Scholar
15.Bernareggi M, Cremona G. Measurement of exhaled nitric oxide in humans and animals. Pulm Pharmacol Ther. 1999; 12: 331-352.
10.1006/pupt.1999.0216
CASPubMedWeb of Science®Google Scholar
16.Antonelli A, Bisetti A, Ferrara A, Grassi V. Le sindromi rinosinusobronchiali. In: A Antonelli, A Bisetti, A Ferrara, et al. eds. Fisiologia e fisiopatologia del tratto respiratorio integrato. Brescia, Italy: Edizioni Scientifiche Valeas; 1995.
Google Scholar
17.Cruz AA, Popov T, Pawankar R, et al; ARIA Initiative Scientific Committee. Common characteristics of upper and lower airways in rhinitis and asthma: ARIA update, in collaboration with GA(2)LEN. Allergy. 2007; 62(suppl 84): 1-41.
10.1111/j.1398-9995.2007.01551.x
PubMedWeb of Science®Google Scholar
18.Fokkens W, Lund V, Mullol J; European Position Paper on Rhinosinusitis and Nasal Polyps group. European position paper on rhinosinusitis and nasal polyps 2007 [review]. Rhinol Suppl. 2007; 20: 1-136.
PubMedWeb of Science®Google Scholar
19.Lamblin C, Saelens T, Bergoin C, Wallaert B. The common mucosal immune system in respiratory disease. Rev Mal Respir. 2000; 17: 941-946.
CASPubMedWeb of Science®Google Scholar
20.Hens G, Vanaudenaerde BM, Bullens DM, et al. Sinonasal pathology in nonallergic asthma and COPD: ‘united airway disease’ beyond the scope of allergy. Allergy. 2008; 63: 261-267.
10.1111/j.1398-9995.2007.01545.x
CASPubMedWeb of Science®Google Scholar
21.Lund VJ, Mackay IS. Staging in rhinosinusitus. Rhinology. 1993; 31: 183-184.
CASPubMedWeb of Science®Google Scholar
22. National Asthma Education and Prevention Program: Expert Panel Report III. Guidelines for the Diagnosis and Management of Asthma. Bethesda, MD: National Heart, Lung, and Blood Institute;. 2007: 1-61. NIH publication no. 08-5847. www.nhlbi.nih.gov
Google Scholar
23. American Thoracic Society Recommendations for standardized procedures for the on-line and off-line measurement of exhaled lower respiratory nitric oxide and nasal nitric oxide in adults and children—1999. Official statement of the American Thoracic Society. Am J Respir Crit Care Med. 1999; 160: 2104-2117.
PubMedWeb of Science®Google Scholar
24.Sanders SP, Siekierski ES, Richards SM, Porter JD, Imani F, Proud D. Rhinovirus infection induces expression of type 2 nitric oxide synthase in human respiratory epithelial cells in vitro and in vivo. J Allergy Clin Immunol. 2001; 107: 245-243.
10.1067/mai.2001.112028
Web of Science®Google Scholar
25.Nathan C, Xie QW. Regulation of biosynthesis of nitric oxide. J Biol Chem. 1994; 269: 13725-13728.
10.1016/S0021-9258(17)36703-0
CASPubMedWeb of Science®Google Scholar
26.Jeon SY, Kim E, Ma YW, Kim JP, Jung TG, Hwang EG. Nitric oxide mediates platelet activating factor-induced micorvascular leakage in rat airways. Ann Otol Rhinol Laryngol. 2001; 110: 83-86.
10.1177/000348940111000115
CASPubMedWeb of Science®Google Scholar
27.Tasman AJ, Bogatzki B, Heppt W, Hause-Kronberger C, Fisher A. Nitric oxide synthase in the innervation of the human nasal mucosa: correlation with neuropeptides and tyrosine hydroxylase. Laryngoscope. 1998; 108: 128-133.
10.1097/00005537-199801000-00025
CASPubMedWeb of Science®Google Scholar
28.Lindberg S, Cervin A, Runer T. Nitric oxide (NO) production in the upper airways is decreased in chronic sinusitis. Acta Otolaryngol (Stockh). 1997; 117: 113-117.
10.3109/00016489709118001
CASPubMedWeb of Science®Google Scholar
29.Arnal JF, Flores P, Ramis J, et al. Nasal nitric concentration in paranasal sinus inflammatory disease. Eur Resp J. 1999; 13: 307-312.
10.1034/j.1399-3003.1999.13b15.x
CASPubMedWeb of Science®Google Scholar
30.Watkins DN, Lewis RH, Basclain KA. Expression and localization of the inducible isoform of nitric oxide synthase in nasal epithelium. Clin Exp Allergy. 1998; 28: 211-219.
10.1046/j.1365-2222.1998.00215.x
CASPubMedWeb of Science®Google Scholar
31.Kharitonov SA, Karalasingam R, O’Connor B, et al. Nasal nitric oxide is increased in patients with asthma and allergic rhinitis and may be modulated by nasal glucocorticoids. J Allergy Clin Immunol. 1997; 99: 55-64.
Web of Science®Google Scholar
32.Passàli D, Damiani V, Passali FM, Passàli GC, Bellussi L. Pattern of expression of inducile nitric oxide synthase (iNOS) in rhinosinusal mucosa. Folia Otorhinolaryngologica. 2003; 8: 7-12.
Google Scholar
33.Zitt M. Clinical applications of exhaled nitric oxide for the diagnosis and management of asthma: a consensus report. Clin Ther. 2005; 27: 1238-1250.
10.1016/j.clinthera.2005.07.005
CASPubMedWeb of Science®Google Scholar
34.Vijverberg SJH, Koenderman L, Koster ES, van der Ent CK, Raaijmakers JAM, Maitland-van der Zee AH. Biomarkers of therapy responsiveness in asthma: pitfalls and promises. Clin Exp Allergy. 2011; 41: 615-629.
10.1111/j.1365-2222.2011.03694.x
CASPubMedWeb of Science®Google Scholar
35.Williamson PA, Vaidyanathan S, Clearie K, Barnes M, Lipworth BJ. Airway dysfunction in nasal polyposis: a spectrum of asthmatic disease? Clin Exp Allergy. 2011; 10: 1-7.
Google Scholar
36.Yamamoto M, Tochino Y, Chibana K, et al. Nitric oxide and related enzymes in asthma: relation to severity, enzyme function and inflammation. Clin Exp Allergy. 2011 Sep 25 [Epub ahead of print]. doi: 10.1111/j.1365-2222.2011.03860.x10.1111/j.1365-2222.2011.03860.x.
10.1111/j.1365?2222.2011.03860.x
PubMedWeb of Science®Google Scholar
37.Montuschi P, Santonico M, Mondino C, et al. Diagnostic performance of an electronic nose, fractional exhaled nitric oxide, and lung function testing in asthma. Chest. 2010; 137: 790-796.
10.1378/chest.09-1836
CASPubMedWeb of Science®Google Scholar
38.Montuschi P, Mondino C, Koch P, Ciabattoni G, Barnes PJ, Baviera G. Effects of montelukast treatment and withdrawal on exhaled nitric oxide and lung function in children with asthma. Chest. 2007; 132: 1876-1881.
10.1378/chest.07-1587
CASPubMedWeb of Science®Google Scholar

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Volume147, Issue2

August 2012

Pages 351-356

Exhaled Nitric Oxide Measurement in Patients Affected by Nasal Polyposis

Abstract

Objectives

Setting

Study Design

Subjects and Methods

Results

Conclusion

References

Citing Literature

References

Information

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Exhaled Nitric Oxide Measurement in Patients Affected by Nasal Polyposis

Abstract

Objectives

Setting

Study Design

Subjects and Methods

Results

Conclusion

References

Citing Literature

References

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