Allergy Asthma Immunol Res.  2014 Jan;6(1):27-32. 10.4168/aair.2014.6.1.27.

Fractional Exhaled Nitric Oxide and Impulse Oscillometry in Children With Allergic Rhinitis

• Kim YH
• Park HB
• Kim MJ
• Kim HS
• Lee HS
• Han YK
• Kim KW
• Sohn MH
• Kim KE

• KMID: 2166925
• DOI: http://doi.org/10.4168/aair.2014.6.1.27

Abstract

PURPOSE
Airway inflammation, bronchial hyper-responsiveness (BHR), and bronchodilator response (BDR) are representative characteristics of asthma. Because allergic rhinitis (AR) is a risk factor for asthma development, we evaluated these 3 characteristics in AR using measurement of fractional exhaled nitric oxide (FeNO), a methacholine challenge test (MCT), and impulse oscillometry (IOS).
METHODS
This study included 112 children with asthma (asthma group), 196 children with AR (AR group), and 32 control subjects (control group). We compared pulmonary function parameters and FeNO levels among the 3 groups. The AR group was subdivided into 2 categories: the AR group with BHR and the AR group without, and again pulmonary function and FeNO levels were compared between the 2 subgroups.
RESULTS
FeNO levels were more increased in the AR and asthma groups than in the control group; within the AR group, FeNO was higher in the AR group with BHR than in the AR group without. The BDR was more increased in the AR group than in the control group when percent changes in reactance at 5 Hz (Delta X5) and reactance area (Delta AX) were compared. In the AR group, however, there was no difference in Delta X5 and Delta AX between the AR group with BHR and the AR group without.
CONCLUSIONS
Reversible airway obstruction on IOS and elevated FeNO levels were observed in children with AR. Because elevated FeNO levels can indicate airway inflammation and because chronic inflammation may lead to BHR, FeNO levels may be associated with BHR in AR. IOS can be a useful tool for detecting lower airway involvement of AR independent of BHR assessed in the MCT.

Keyword

Asthma; allergic rhinitis; bronchial hyper-responsiveness; bronchodilator effect; child; nitric oxide

MeSH Terms

Airway Obstruction
Asthma
Bronchodilator Agents
Child*
Humans
Inflammation
Methacholine Chloride
Nitric Oxide*
Oscillometry*
Rhinitis*
Risk Factors
Bronchodilator Agents
Methacholine Chloride
Nitric Oxide

Figure

• 

  Figure (A) Fractional exhaled nitric oxide (FeNO) in the control group, the allergic rhinitis (AR) group with bronchial hyper-responsiveness (BHR), the AR group without, and the asthma group. FeNO levels were higher in the asthma and AR groups than in the control group. The AR group with BHR tended to have higher FeNO than the AR group without (P=0.08). (B) BDR in reactance at 5 Hz (Δ X5) and reactance area (Δ AX) increased more in the asthma and AR groups than in the control group. Moreover, Δ X5 and Δ AX were not significantly different between the AR group with BHR and the AR group without.

Reference

1. Settipane RJ, Hagy GW, Settipane GA. Long-term risk factors for developing asthma and allergic rhinitis: a 23-year follow-up study of college students. Allergy Proc. 1994; 15:21–25.

2. Leynaert B, Neukirch C, Kony S, Guénégou A, Bousquet J, Aubier M, Neukirch F. Association between asthma and rhinitis according to atopic sensitization in a population-based study. J Allergy Clin Immunol. 2004; 113:86–93.

3. Ciprandi G, Caimmi D, Miraglia Del Giudice M, La Rosa M, Salpietro C, Marseglia GL. Recent developments in United airways disease. Allergy Asthma Immunol Res. 2012; 4:171–177.

4. Braman SS, Barrows AA, DeCotiis BA, Settipane GA, Corrao WM. Airway hyperresponsiveness in allergic rhinitis. A risk factor for asthma. Chest. 1987; 91:671–674.

5. Townley RG, Ryo UY, Kolotkin BM, Kang B. Bronchial sensitivity to methacholine in current and former asthmatic and allergic rhinitis patients and control subjects. J Allergy Clin Immunol. 1975; 56:429–442.

6. Ciprandi G, Cirillo I, Vizzaccaro A, Tosca M, Passalacqua G, Pallestrini E, Canonica GW. Seasonal and perennial allergic rhinitis: is this classification adherent to real life? Allergy. 2005; 60:882–887.

7. Jouaville LF, Annesi-Maesano I, Nguyen LT, Bocage AS, Bedu M, Caillaud D. Interrelationships among asthma, atopy, rhinitis and exhaled nitric oxide in a population-based sample of children. Clin Exp Allergy. 2003; 33:1506–1511.

8. Cardinale F, de Benedictis FM, Muggeo V, Giordano P, Loffredo MS, Iacoviello G, Armenio L. Exhaled nitric oxide, total serum IgE and allergic sensitization in childhood asthma and allergic rhinitis. Pediatr Allergy Immunol. 2005; 16:236–242.

9. National Asthma Education and Prevention Program. Expert Panel Report 3 (EPR-3): Guidelines for the Diagnosis and Management of Asthma-Summary Report 2007. J Allergy Clin Immunol. 2007; 120:S94–S138.

10. Dundas I, Chan EY, Bridge PD, McKenzie SA. Diagnostic accuracy of bronchodilator responsiveness in wheezy children. Thorax. 2005; 60:13–16.

11. Capasso M, Varricchio A, Ciprandi G. Impact of allergic rhinitis on asthma in children: effects on bronchodilation test. Allergy. 2010; 65:264–268.

12. Suh DI, Lee JK, Lee JH, Koh YY. Bronchodilator response and its relationship to bronchial hyperresponsiveness in children with allergic rhinitis/asthma. Pediatr Allergy Respir Dis. 2010; 20:59–67.

13. Song TW, Kim KW, Kim ES, Park JW, Sohn MH, Kim KE. Utility of impulse oscillometry in young children with asthma. Pediatr Allergy Immunol. 2008; 19:763–768.

14. Kim YH, Kim KW, Baek J, Park HB, Kim H, Song KJ, Lee JM, Sohn MH, Kim KE. Usefulness of impulse oscillometry and fractional exhaled nitric oxide in children with Eosinophilic bronchitis. Pediatr Pulmonol. 2013; 48:221–228.

15. Aronsson D, Tufvesson E, Ankerst J, Bjermer L. Allergic rhinitis with hyper-responsiveness differ from asthma in degree of peripheral obstruction during metacholine challenge test. Clin Physiol Funct Imaging. 2008; 28:81–85.

16. Chai H, Farr RS, Froehlich LA, Mathison DA, McLean JA, Rosenthal RR, Sheffer AL, Spector SL, Townley RG. Standardization of bronchial inhalation challenge procedures. J Allergy Clin Immunol. 1975; 56:323–327.

17. Brown WG, Halonen MJ, Kaltenborn WT, Barbee RA. The relationship of respiratory allergy, skin test reactivity, and serum IgE in a community population sample. J Allergy Clin Immunol. 1979; 63:328–335.

18. Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, Crapo R, Enright P, van der Grinten CP, Gustafsson P, Jensen R, Johnson DC, MacIntyre N, McKay R, Navajas D, Pedersen OF, Pellegrino R, Viegi G, Wanger J. ATS/ERS Task Force. Standardisation of spirometry. Eur Respir J. 2005; 26:319–338.

19. American Thoracic Society. European Respiratory Society. ATS/ERS recommendations for standardized procedures for the online and offline measurement of exhaled lower respiratory nitric oxide and nasal nitric oxide, 2005. Am J Respir Crit Care Med. 2005; 171:912–930.

20. Goldman MD. Clinical application of forced oscillation. Pulm Pharmacol Ther. 2001; 14:341–350.

21. Komarow HD, Myles IA, Uzzaman A, Metcalfe DD. Impulse oscillometry in the evaluation of diseases of the airways in children. Ann Allergy Asthma Immunol. 2011; 106:191–199.

22. Fruchter O, Hardak E, Yigla M. The response to bronchodilators in adults is not predictive of bronchial-hyperreactivity. J Asthma. 2009; 46:455–459.

23. Suh DI, Lee JK, Kim CK, Koh YY. Bronchial hyperresponsiveness to methacholine/AMP and the bronchodilator response in asthmatic children. Eur Respir J. 2011; 37:800–805.

24. Petanjek BB, Grle SP, Pelicaric D, Vrankovic D. Bronchodilator response in patients with persistent allergic asthma could not predict airway hyperresponsiveness. Allergy Asthma Clin Immunol. 2007; 3:123–127.

25. Shi Y, Aledia AS, Tatavoosian AV, Vijayalakshmi S, Galant SP, George SC. Relating small airways to asthma control by using impulse oscillometry in children. J Allergy Clin Immunol. 2012; 129:671–678.

26. Ciprandi G, Signori A, Cirillo I. Relationship between bronchial hyperreactivity and bronchodilation in patients with allergic rhinitis. Ann Allergy Asthma Immunol. 2011; 106:460–466.

27. Ciprandi G, Tosca MA, Capasso M. Exhaled nitric oxide in children with allergic rhinitis and/or asthma: a relationship with bronchial hyperreactivity. J Asthma. 2010; 47:1142–1147.

28. Motomura C, Odajima H, Tezuka J, Murakami Y, Moriyasu Y, Kando N, Taba N, Hayashi D, Okada K, Nishima S. Effect of age on relationship between exhaled nitric oxide and airway hyperresponsiveness in asthmatic children. Chest. 2009; 136:519–525.

29. Patelis A, Gunnbjörnsdottir M, Malinovschi A, Matsson P, Onell A, Högman M, Alving K, Janson C. Population-based study of multiplexed IgE sensitization in relation to asthma, exhaled nitric oxide, and bronchial responsiveness. J Allergy Clin Immunol. 2012; 130:397–402.e2.

30. Steerenberg PA, Janssen NA, de Meer G, Fischer PH, Nierkens S, van Loveren H, Opperhuizen A, Brunekreef B, van Amsterdam JG. Relationship between exhaled NO, respiratory symptoms, lung function, bronchial hyperresponsiveness, and blood eosinophilia in school children. Thorax. 2003; 58:242–245.

31. Hervás D, Milán JM, Garde J. Differences in exhaled nitric oxide in atopic children. Allergol Immunopathol (Madr). 2008; 36:331–335.

32. Koh YY, Kim CK. The development of asthma in patients with allergic rhinitis. Curr Opin Allergy Clin Immunol. 2003; 3:159–164.