Skip to main content
NCBI home page
Thorax logoLink to Thorax
. 2003 Jan;58(1):68–72. doi: 10.1136/thorax.58.1.68

Comparison of exhaled and nasal nitric oxide and exhaled carbon monoxide levels in bronchiectatic patients with and without primary ciliary dyskinesia

I Horvath 1, S Loukides 1, T Wodehouse 1, E Csiszer 1, P Cole 1, S Kharitonov 1, P Barnes 1
PMCID: PMC1746449  PMID: 12511725

Abstract

Methods: The levels of exhaled nitric oxide (eNO), carbon monoxide (eCO) and nasal NO (nNO) from bronchiectatic patients with PCD (n=14) were compared with those from patients with non-PCD bronchiectasis without (n=31) and with cystic fibrosis (CF) (n=20) and from normal subjects (n=37) to assess the clinical usefulness of these measurements in discriminating between PCD and other causes of bronchiectasis.

Results: Exhaled NO levels were lower in patients with PCD than in patients with non-PCD non-CF bronchiectasis or healthy subjects (median (range) 2.1 (1.3–3.5) ppb v 8.7 (4.5–26.0) ppb, p<0.001; 6.7 (2.6–11.9) ppb, p<0.001, respectively) but not lower than bronchiectatic patients with CF (3.0 (1.5–7.5) ppb, p>0.05). Nasal levels of nNO were significantly lower in PCD patients than in any other subjects (PCD: 54.5 (5.0–269) ppb, non-PCD bronchiectasis without CF: 680 (310–1000) ppb, non-PCD bronchiectasis with CF: 343 (30–997) ppb, control: 663 (322–1343) ppb). In contrast, eCO levels were higher in all patient groups than in control subjects (PCD: 4.5 (3.0–24.0) ppm, p<0.01, other bronchiectasis without CF: 5.0 (3.0–15.0) ppm, p<0.001; CF: 5.3 (2.0–23.0) ppm, p<0.001 v 3.0 (0.5–5.0) ppm). Low values in both eNO and nNO readings (<2.4 ppb and <187 ppb, respectively) identified PCD patients from other bronchiectatic patients with a specificity of 98% and a positive predictive value of 92%.

Conclusion: The simultaneous measurement of eNO and nNO is a useful screening tool for PCD.

Full Text

The Full Text of this article is available as a PDF (129.7 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Arnal J. F., Flores P., Rami J., Murris-Espin M., Bremont F., Pasto I Aguilla M., Serrano E., Didier A. Nasal nitric oxide concentration in paranasal sinus inflammatory diseases. Eur Respir J. 1999 Feb;13(2):307–312. doi: 10.1034/j.1399-3003.1999.13b15.x. [DOI] [PubMed] [Google Scholar]
  2. Choi A. M., Alam J. Heme oxygenase-1: function, regulation, and implication of a novel stress-inducible protein in oxidant-induced lung injury. Am J Respir Cell Mol Biol. 1996 Jul;15(1):9–19. doi: 10.1165/ajrcmb.15.1.8679227. [DOI] [PubMed] [Google Scholar]
  3. Cunnington A. J., Hormbrey P. Breath analysis to detect recent exposure to carbon monoxide. Postgrad Med J. 2002 Apr;78(918):233–237. doi: 10.1136/pmj.78.918.233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Donnelly L. E., Barnes P. J. Expression of heme oxygenase in human airway epithelial cells. Am J Respir Cell Mol Biol. 2001 Mar;24(3):295–303. doi: 10.1165/ajrcmb.24.3.4001. [DOI] [PubMed] [Google Scholar]
  5. Ekroos H., Tuominen J., Sovijärvi A. R. Exhaled nitric oxide and its long-term variation in healthy non-smoking subjects. Clin Physiol. 2000 Nov;20(6):434–439. doi: 10.1046/j.1365-2281.2000.00277.x. [DOI] [PubMed] [Google Scholar]
  6. Eller J., Lapa e Silva J. R., Poulter L. W., Lode H., Cole P. J. Cells and cytokines in chronic bronchial infection. Ann N Y Acad Sci. 1994 May 28;725:331–345. doi: 10.1111/j.1749-6632.1994.tb39816.x. [DOI] [PubMed] [Google Scholar]
  7. Greenstone M., Rutman A., Dewar A., Mackay I., Cole P. J. Primary ciliary dyskinesia: cytological and clinical features. Q J Med. 1988 May;67(253):405–423. [PubMed] [Google Scholar]
  8. Ho L. P., Innes J. A., Greening A. P. Exhaled nitric oxide is not elevated in the inflammatory airways diseases of cystic fibrosis and bronchiectasis. Eur Respir J. 1998 Dec;12(6):1290–1294. doi: 10.1183/09031936.98.12061290. [DOI] [PubMed] [Google Scholar]
  9. Horvath I., Loukides S., Wodehouse T., Kharitonov S. A., Cole P. J., Barnes P. J. Increased levels of exhaled carbon monoxide in bronchiectasis: a new marker of oxidative stress. Thorax. 1998 Oct;53(10):867–870. doi: 10.1136/thx.53.10.867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Horváth I., Donnelly L. E., Kiss A., Kharitonov S. A., Lim S., Chung K. F., Barnes P. J. Combined use of exhaled hydrogen peroxide and nitric oxide in monitoring asthma. Am J Respir Crit Care Med. 1998 Oct;158(4):1042–1046. doi: 10.1164/ajrccm.158.4.9710091. [DOI] [PubMed] [Google Scholar]
  11. Horváth I., Donnelly L. E., Kiss A., Paredi P., Kharitonov S. A., Barnes P. J. Raised levels of exhaled carbon monoxide are associated with an increased expression of heme oxygenase-1 in airway macrophages in asthma: a new marker of oxidative stress. Thorax. 1998 Aug;53(8):668–672. doi: 10.1136/thx.53.8.668. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Karadag B., James A. J., Gültekin E., Wilson N. M., Bush A. Nasal and lower airway level of nitric oxide in children with primary ciliary dyskinesia. Eur Respir J. 1999 Jun;13(6):1402–1405. doi: 10.1183/09031936.99.13614069. [DOI] [PubMed] [Google Scholar]
  13. Keatings V. M., Jatakanon A., Worsdell Y. M., Barnes P. J. Effects of inhaled and oral glucocorticoids on inflammatory indices in asthma and COPD. Am J Respir Crit Care Med. 1997 Feb;155(2):542–548. doi: 10.1164/ajrccm.155.2.9032192. [DOI] [PubMed] [Google Scholar]
  14. Kharitonov S. A., Barnes P. J. Exhaled markers of pulmonary disease. Am J Respir Crit Care Med. 2001 Jun;163(7):1693–1722. doi: 10.1164/ajrccm.163.7.2009041. [DOI] [PubMed] [Google Scholar]
  15. Kharitonov S. A., Rajakulasingam K., O'Connor B., Durham S. R., Barnes P. J. Nasal nitric oxide is increased in patients with asthma and allergic rhinitis and may be modulated by nasal glucocorticoids. J Allergy Clin Immunol. 1997 Jan;99(1 Pt 1):58–64. doi: 10.1016/s0091-6749(97)70301-4. [DOI] [PubMed] [Google Scholar]
  16. Kharitonov S. A., Wells A. U., O'Connor B. J., Cole P. J., Hansell D. M., Logan-Sinclair R. B., Barnes P. J. Elevated levels of exhaled nitric oxide in bronchiectasis. Am J Respir Crit Care Med. 1995 Jun;151(6):1889–1893. doi: 10.1164/ajrccm.151.6.7767536. [DOI] [PubMed] [Google Scholar]
  17. Konstantinides Stavros, Geibel Annette, Heusel Gerhard, Heinrich Fritz, Kasper Wolfgang, Management Strategies and Prognosis of Pulmonary Embolism-3 Trial Investigators Heparin plus alteplase compared with heparin alone in patients with submassive pulmonary embolism. N Engl J Med. 2002 Oct 10;347(15):1143–1150. doi: 10.1056/NEJMoa021274. [DOI] [PubMed] [Google Scholar]
  18. Leischow S. J., Merikle E. P., Cook G., Newman R., Muramoto M. An evaluation of NicCheck I: a dipstick method for analyzing nicotine and its metabolites. Addict Behav. 1999 Jan-Feb;24(1):145–148. [PubMed] [Google Scholar]
  19. Lindberg S., Cervin A., Runer T. Nitric oxide (NO) production in the upper airways is decreased in chronic sinusitis. Acta Otolaryngol. 1997 Jan;117(1):113–117. doi: 10.3109/00016489709118001. [DOI] [PubMed] [Google Scholar]
  20. Loukides S., Horvath I., Wodehouse T., Cole P. J., Barnes P. J. Elevated levels of expired breath hydrogen peroxide in bronchiectasis. Am J Respir Crit Care Med. 1998 Sep;158(3):991–994. doi: 10.1164/ajrccm.158.3.9710031. [DOI] [PubMed] [Google Scholar]
  21. Loukides S., Kharitonov S., Wodehouse T., Cole P. J., Barnes P. J. Effect of arginine on mucociliary function in primary ciliary dyskinesia. Lancet. 1998 Aug 1;352(9125):371–372. doi: 10.1016/S0140-6736(05)60471-0. [DOI] [PubMed] [Google Scholar]
  22. Lundberg J. O., Weitzberg E., Nordvall S. L., Kuylenstierna R., Lundberg J. M., Alving K. Primarily nasal origin of exhaled nitric oxide and absence in Kartagener's syndrome. Eur Respir J. 1994 Aug;7(8):1501–1504. doi: 10.1183/09031936.94.07081501. [DOI] [PubMed] [Google Scholar]
  23. Paredi P., Shah P. L., Montuschi P., Sullivan P., Hodson M. E., Kharitonov S. A., Barnes P. J. Increased carbon monoxide in exhaled air of patients with cystic fibrosis. Thorax. 1999 Oct;54(10):917–920. doi: 10.1136/thx.54.10.917. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Pedersen H., Mygind N. Absence of axonemal arms in nasal mucosa cilia in Kartagener's syndrome. Nature. 1976 Aug 5;262(5568):494–495. doi: 10.1038/262494a0. [DOI] [PubMed] [Google Scholar]
  25. Persson M. G., Zetterström O., Agrenius V., Ihre E., Gustafsson L. E. Single-breath nitric oxide measurements in asthmatic patients and smokers. Lancet. 1994 Jan 15;343(8890):146–147. doi: 10.1016/s0140-6736(94)90935-0. [DOI] [PubMed] [Google Scholar]
  26. Rayner C. F., Rutman A., Dewar A., Cole P. J., Wilson R. Ciliary disorientation in patients with chronic upper respiratory tract inflammation. Am J Respir Crit Care Med. 1995 Mar;151(3 Pt 1):800–804. doi: 10.1164/ajrccm.151.3.7881674. [DOI] [PubMed] [Google Scholar]
  27. Thomas S. R., Kharitonov S. A., Scott S. F., Hodson M. E., Barnes P. J. Nasal and exhaled nitric oxide is reduced in adult patients with cystic fibrosis and does not correlate with cystic fibrosis genotype. Chest. 2000 Apr;117(4):1085–1089. doi: 10.1378/chest.117.4.1085. [DOI] [PubMed] [Google Scholar]
  28. Zayasu K., Sekizawa K., Okinaga S., Yamaya M., Ohrui T., Sasaki H. Increased carbon monoxide in exhaled air of asthmatic patients. Am J Respir Crit Care Med. 1997 Oct;156(4 Pt 1):1140–1143. doi: 10.1164/ajrccm.156.4.96-08056. [DOI] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

[Corrected Figure 1]
thorax_58_1_68__index.html (1.7KB, html)
thorax_58_1_68__1.pdf (49.4KB, pdf)

Articles from Thorax are provided here courtesy of BMJ Publishing Group

RESOURCES