Skip to main content
Top
Published in: Sleep and Breathing 3/2019

Open Access 01-09-2019 | Sleep Breathing Physiology and Disorders • Original Article

Measurement of fractional exhaled nitric oxide and nasal nitric oxide in male patients with obstructive sleep apnea

Authors: Dongmei Zhang, Yi Xiao, Jinmei Luo, Xiaona Wang, Yixian Qiao, Rong Huang, Wei Wu

Published in: Sleep and Breathing | Issue 3/2019

Login to get access

Abstract

Objective

Airway inflammation plays an important role in obstructive sleep apnea (OSA); exhaled nitric oxide is regarded as a noninvasive marker of airway inflammation. The aim of this study was to evaluate fractional exhaled nitric oxide (FeNO) and nasal nitric oxide (nNO) in patients with OSA.

Methods

Seventy-five patients with OSA and 30 health controls were enrolled in this study. FeNO and nNO were measured before and after sleep. Nasal lavage was performed in 31 non-smoking individuals immediately after NO measurement in the morning. The sample of nasal lavage was taken for cell classification and analyzing interleukin 6 (IL-6) and interleukin 8 (IL-8).

Results

Both FeNO and nNO were significantly higher in OSA (before sleep FeNO 21.08 ± 8.79 ppb vs.16.90 ± 6.86 ppb, p = 0.022; after sleep FeNO 25.57 ± 15.58 ppb vs.18.07 ± 6.25 ppb, p = 0.003; before sleep nNO 487.03 ± 115.83 ppb vs. 413.37 ± 73.10 ppb, p = 0.001; after sleep nNO 550.07 ± 130.24 ppb vs. 460.43 ± 109.77 ppb, p < 0.001). Furthermore, in non-smoking OSA, nNO levels were positively correlated with apnea hypopnea index (AHI) and average decrease of pulse arterial oxygen saturation (SpO2); after sleep, nNO was also positively associated to recording time with SpO2 < 90% and negatively associated to minimum SpO2. Both before and after sleep nNO levels were positively correlated with the percentage of neutrophils in nasal lavage (r = 0.528, p = 0.014; r = 0.702, p < 0.001, respectively). Additionally, before sleep nNO was also positively associated with IL-6 (r = 0.586, p = 0.005) and IL-8 (r = 0.520, p = 0.016) concentration.

Conclusion

This study sustains the presence of airway inflammation in OSA patients with the increase of FeNO and nNO. The data suggests nNO might have greater value than FeNO since it positively correlated with OSA severity, and nNO is a potential bio-marker of nasal inflammation in non-smoking OSA patients.
Appendix
Available only for authorised users
Literature
9.
go back to reference Olopade CO, Christon JA, Zakkar M, Hua C, Swedler WI, Scheff PA, Rubinstein I (1997) Exhaled pentane and nitric oxide levels in patients with obstructive sleep apnea. Chest 111(6):1500–1504CrossRefPubMed Olopade CO, Christon JA, Zakkar M, Hua C, Swedler WI, Scheff PA, Rubinstein I (1997) Exhaled pentane and nitric oxide levels in patients with obstructive sleep apnea. Chest 111(6):1500–1504CrossRefPubMed
12.
13.
go back to reference Gelardi M, Abbattista G, Quaranta VN, Quaranta N, Seccia V, Buttafava S, Frati F, Ciprandi G (2016) Standardization procedure for the nasal nitric oxide measurement method using Niox MINO® and the tidal-breathing technique with velum-closure. J Biol Regul Homeost Agents 30(3):853–858PubMed Gelardi M, Abbattista G, Quaranta VN, Quaranta N, Seccia V, Buttafava S, Frati F, Ciprandi G (2016) Standardization procedure for the nasal nitric oxide measurement method using Niox MINO® and the tidal-breathing technique with velum-closure. J Biol Regul Homeost Agents 30(3):853–858PubMed
14.
go back to reference Berry RB, Brooks R, Gamaldo CE, Harding SM, Lloyd RM, Marcus CL and Vaughn BV for the American Academy of Sleep Medicine (2016) The AASM manual for the scoring of sleep and associated events: rules, terminology and technical specifications, version 2.3. American Academy of Sleep Medicine, Darien. http://www.aasmnet.org Berry RB, Brooks R, Gamaldo CE, Harding SM, Lloyd RM, Marcus CL and Vaughn BV for the American Academy of Sleep Medicine (2016) The AASM manual for the scoring of sleep and associated events: rules, terminology and technical specifications, version 2.3. American Academy of Sleep Medicine, Darien. http://​www.​aasmnet.​org
16.
go back to reference Depalo A, Carpagnano GE, Spanevello A, Sabato R, Cagnazzo MG, Gramiccioni C, Foschino-Barbaro MP (2008) Exhaled NO and iNOS expression in sputum cells of healthy, obese and OSA subjects. J Intern Med 263(1):70–78CrossRefPubMed Depalo A, Carpagnano GE, Spanevello A, Sabato R, Cagnazzo MG, Gramiccioni C, Foschino-Barbaro MP (2008) Exhaled NO and iNOS expression in sputum cells of healthy, obese and OSA subjects. J Intern Med 263(1):70–78CrossRefPubMed
17.
go back to reference Lundberg JO, Farkas-Szallasi T, Weitzberg E, Rinder J, Lidholm J, Anggåard A, Hökfelt T, Lundberg JM, Alving K (1995) High nitric oxide production in human paranasal sinuses. Nat Med 1(4):370–373CrossRefPubMed Lundberg JO, Farkas-Szallasi T, Weitzberg E, Rinder J, Lidholm J, Anggåard A, Hökfelt T, Lundberg JM, Alving K (1995) High nitric oxide production in human paranasal sinuses. Nat Med 1(4):370–373CrossRefPubMed
22.
go back to reference Rubinstein I (1995) Nasal inflammation in patients with obstructive sleep apnea. Laryngoscope 105(2):175–177CrossRefPubMed Rubinstein I (1995) Nasal inflammation in patients with obstructive sleep apnea. Laryngoscope 105(2):175–177CrossRefPubMed
24.
go back to reference Inancli HM, Enoz M (2010) Obstructive sleep apnea syndrome and upper airway inflammation. Recent Patents Inflamm Allergy Drug Discov 4(1):54–57CrossRef Inancli HM, Enoz M (2010) Obstructive sleep apnea syndrome and upper airway inflammation. Recent Patents Inflamm Allergy Drug Discov 4(1):54–57CrossRef
25.
go back to reference Xie Q, Nathan C (1994) The high-output nitric oxide pathway: role and regulation. J Leukoc Biol 56(5):576–582CrossRefPubMed Xie Q, Nathan C (1994) The high-output nitric oxide pathway: role and regulation. J Leukoc Biol 56(5):576–582CrossRefPubMed
26.
go back to reference Shadan FF, Jalowayski AA, Fahrenholz J, Kline LE, Dawson A (2005) Nasal cytology: a marker of clinically silent inflammation in patients with obstructive sleep apnea and a predictor of noncompliance with nasal CPAP therapy. J Clin Sleep Med 1(3):266–270PubMed Shadan FF, Jalowayski AA, Fahrenholz J, Kline LE, Dawson A (2005) Nasal cytology: a marker of clinically silent inflammation in patients with obstructive sleep apnea and a predictor of noncompliance with nasal CPAP therapy. J Clin Sleep Med 1(3):266–270PubMed
28.
go back to reference Carpagnano GE, Kharitonov SA, Resta O, Foschino-Barbaro MP, Gramiccioni E, Barnes PJ (2002) Increased 8-isoprostane and interleukin-6 in breath condensate of obstructive sleep apnea patients. Chest 122(4):1162–1167CrossRefPubMed Carpagnano GE, Kharitonov SA, Resta O, Foschino-Barbaro MP, Gramiccioni E, Barnes PJ (2002) Increased 8-isoprostane and interleukin-6 in breath condensate of obstructive sleep apnea patients. Chest 122(4):1162–1167CrossRefPubMed
31.
go back to reference Moodie FM, Marwick JA, Anderson CS, Szulakowski P, Biswas SK, Bauter MR, Kilty I, Rahman I (2004) Oxidative stress and cigarette smoke alter chromatin remodeling but differentially regulate NF-kappaB activation and proinflammatory cytokine release in alveolar epithelial cells. FASEB J 18(15):1897–1899. https://doi.org/10.1096/fj.04-1506fje CrossRefPubMed Moodie FM, Marwick JA, Anderson CS, Szulakowski P, Biswas SK, Bauter MR, Kilty I, Rahman I (2004) Oxidative stress and cigarette smoke alter chromatin remodeling but differentially regulate NF-kappaB activation and proinflammatory cytokine release in alveolar epithelial cells. FASEB J 18(15):1897–1899. https://​doi.​org/​10.​1096/​fj.​04-1506fje CrossRefPubMed
34.
go back to reference Hoyt JC, Robbins RA, Habib M, Springall DR, Buttery LD, Polak JM, Barnes PJ (2003) Cigarette smoke decreases inducible nitric oxide synthase in lung epithelial cells. Exp Lung Res 29(1):17–28CrossRefPubMed Hoyt JC, Robbins RA, Habib M, Springall DR, Buttery LD, Polak JM, Barnes PJ (2003) Cigarette smoke decreases inducible nitric oxide synthase in lung epithelial cells. Exp Lung Res 29(1):17–28CrossRefPubMed
35.
36.
go back to reference Dias AR, Martinho C, Teixeira J et al (2010) Circadian pattern of exhaled nitric oxide in a group of obstructive sleep apnoea patients and healthy subjects. J Sleep Res 19(1 Pt 2):164 Dias AR, Martinho C, Teixeira J et al (2010) Circadian pattern of exhaled nitric oxide in a group of obstructive sleep apnoea patients and healthy subjects. J Sleep Res 19(1 Pt 2):164
38.
go back to reference Chatkin JM, Qian W, McClean PA, Zamel N, Haight J, Silkoff P (1999) Nitric oxide accumulation in the nonventilated nasal cavity. Arch Otolaryngol Head Neck Surg 125(6):682–685CrossRefPubMed Chatkin JM, Qian W, McClean PA, Zamel N, Haight J, Silkoff P (1999) Nitric oxide accumulation in the nonventilated nasal cavity. Arch Otolaryngol Head Neck Surg 125(6):682–685CrossRefPubMed
Metadata
Title
Measurement of fractional exhaled nitric oxide and nasal nitric oxide in male patients with obstructive sleep apnea
Authors
Dongmei Zhang
Yi Xiao
Jinmei Luo
Xiaona Wang
Yixian Qiao
Rong Huang
Wei Wu
Publication date
01-09-2019
Publisher
Springer International Publishing
Published in
Sleep and Breathing / Issue 3/2019
Print ISSN: 1520-9512
Electronic ISSN: 1522-1709
DOI
https://doi.org/10.1007/s11325-018-1760-1

Other articles of this Issue 3/2019

Sleep and Breathing 3/2019 Go to the issue

Sleep Breathing Physiology and Disorders • Original Article

Severity of obstructive sleep apnea and extension of coronary artery disease

Sleep Breathing Physiology and Disorders • Short Communication

A false alarm of narcolepsy: obstructive sleep apnea masquerading as narcolepsy and depression