Asia Pac Allergy.  2020 Jan;10(1):e7. 10.5415/apallergy.2020.10.e7.

Fractional exhaled nitric oxide and forced expiratory volume in 1 second/forced vital capacity have predictive value of asthma exacerbation in Korean school children

  • 1Department of Internal Medicine, Chungbuk National University Hospital, Chungbuk National University College of Medicine, Cheongju, Korea.
  • 2Department of Pediatrics, Chungbuk National University Hospital, Chungbuk National University College of Medicine, Cheongju, Korea.
  • 3Oksan and Gangnae Elementary School, Chungbuk, Cheongju, Korea.


The incidence of asthma exacerbation (AE) and the predictive value of spirometry and fractional exhaled nitric oxide (FeNO) in school children have not been evaluated.
We sought to evaluate the efficacy of spirometry measurement and FeNO monitoring for predicting AE in school children in the Cheongju area in Korea.
With parental agreement, we studied 170 students aged 7-12 years. Children were evaluated by an asthma specialist using baseline spirometry, skin prick test, seasonal FeNO measurement, and asthma control test. The study participants underwent a physical examination and their medical history was also evaluated by the specialist. They were assessed for asthma control status during regular doctor visits for 1 year.
In total, 160 children (94.1%) completed follow-up and FeNO monitoring. Of which, 26 children (16.3%) had AE. AE was associated with male children and children with allergic rhinitis (p < 0.05). While, children with AE tended to have higher FeNO than those without AE, no significant difference was found. The maximum value of FeNO ≥35 ppb was associated with AE (p < 0.05). Children with AE had a significantly decreased baseline forced expiratory volume in 1 second/forced vital capacity (FEV₁/FVC), %predicted, forced expiratory flow at 25%-75% of FVC (FEF(25%-75%)). FEV₁/FVC < 80% was associated with AE in children regardless of inhalant allergen sensitization (all p < 0.05).
Baseline spirometry had a predictive value of AE in school children. Sensitive spirometric parameters such as FEV₁/FVC and FEF(25%-75%) can be used as prognostic factors to predict future childhood AE. FeNO value ≥ 35 ppb during monitoring was associated with AE in school children.


Asthma; Exacerbation; Child; Exhaled nitric oxide; Spirometry

MeSH Terms

Follow-Up Studies
Forced Expiratory Volume*
Nitric Oxide*
Physical Examination
Rhinitis, Allergic
Vital Capacity*
Nitric Oxide

Cited by  1 articles

The 10th Anniversary of Asia Pacific Allergy
Yoon-Seok Chang
Asia Pac Allergy. 2020;10(1):.    doi: 10.5415/apallergy.2020.10.e10.



1. Centers for Disease Control and Prevention. Most recent asthma data. 2017 [Internet]. Atlanta (GA): Centers for Disease Control and Prevention;[cited 2017 Jan 20]. Available from:. 2017.
2. Cain A, Reznik M. Asthma management in New York City schools: a classroom teacher perspective. J Asthma. 2016; 53:744–50.
3. Asher MI, Keil U, Anderson HR, Beasley R, Crane J, Martinez F, Mitchell EA, Pearce N, Sibbald B, Stewart AW, et al. International Study of Asthma and Allergies in Childhood (ISAAC): rationale and methods. Eur Respir J. 1995; 8:483–91.
4. Bruzzese JM, Evans D, Kattan M. School-based asthma programs. J Allergy Clin Immunol. 2009; 124:195–200.
5. Abramson JM, Wollan P, Kurland M, Yawn BP. Feasibility of school-based spirometry screening for asthma. J Sch Health. 2003; 73:150–3.
6. Jackson DJ, Gangnon RE, Evans MD, Roberg KA, Anderson EL, Pappas TE, Printz MC, Lee WM, Shult PA, Reisdorf E, Carlson-Dakes KT, Salazar LP, DaSilva DF, Tisler CJ, Gern JE, Lemanske RF Jr. Wheezing rhinovirus illnesses in early life predict asthma development in high-risk children. Am J Respir Crit Care Med. 2008; 178:667–72.
7. 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(5 Suppl):S94–138.
8. Masoli M, Fabian D, Holt S, Beasley R. Global Initiative for Asthma (GINA) Program. The global burden of asthma: executive summary of the GINA Dissemination Committee report. Allergy. 2004; 59:469–78.
9. White J, Paton JY, Niven R, Pinnock H. Guidelines for the diagnosis and management of asthma: a look at the key differences between BTS/SIGN and NICE. Thorax. 2018; 73:293–7.
10. Dweik RA, Boggs PB, Erzurum SC, Irvin CG, Leigh MW, Lundberg JO, Olin AC, Plummer AL, Taylor DR. American Thoracic Society Committee on Interpretation of Exhaled Nitric Oxide Levels (FENO) for Clinical Applications. An official ATS clinical practice guideline: interpretation of exhaled nitric oxide levels (FENO) for clinical applications. Am J Respir Crit Care Med. 2011; 184:602–15.
11. 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; 171:912–30.
12. 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; 26:319–38.
13. Wanger J, Clausen JL, Coates A, Pedersen OF, Brusasco V, Burgos F, Casaburi R, Crapo R, Enright P, van der Grinten CP, Gustafsson P, Hankinson J, Jensen R, Johnson D, Macintyre N, McKay R, Miller MR, Navajas D, Pellegrino R, Viegi G. Standardisation of the measurement of lung volumes. Eur Respir J. 2005; 26:511–22.
14. Hankinson JL, Odencrantz JR, Fedan KB. Spirometric reference values from a sample of the general U.S. population. Am J Respir Crit Care Med. 1999; 159:179–87.
15. 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.
16. Di Cara G, Carelli A, Latini A, Panfili E, Bizzarri I, Ciprandi G, Buttafava S, Frati F, Verrotti A. Severity of allergic rhinitis and asthma development in children. World Allergy Organ J. 2015; 8:13.
17. Kim YH, Park HB, Kim MJ, Kim HS, Lee HS, Han YK, Kim KW, Sohn MH, Kim KE. Fractional exhaled nitric oxide and impulse oscillometry in children with allergic rhinitis. Allergy Asthma Immunol Res. 2014; 6:27–32.
18. Zeiger RS, Schatz M, Zhang F, Crawford WW, Kaplan MS, Roth RM, Chen W. Elevated exhaled nitric oxide is a clinical indicator of future uncontrolled asthma in asthmatic patients on inhaled corticosteroids. J Allergy Clin Immunol. 2011; 128:412–4.
19. Pijnenburg MW, Hofhuis W, Hop WC, De Jongste JC. Exhaled nitric oxide predicts asthma relapse in children with clinical asthma remission. Thorax. 2005; 60:215–8.
20. Yang S, Park J, Lee YK, Kim H, Hahn YS. Association of longitudinal fractional exhaled nitric oxide measurements with asthma control in atopic children. Respir Med. 2015; 109:572–9.
21. Bjermer L, Alving K, Diamant Z, Magnussen H, Pavord I, Piacentini G, Price D, Roche N, Sastre J, Thomas M, Usmani O. Current evidence and future research needs for FeNO measurement in respiratory diseases. Respir Med. 2014; 108:830–41.
22. Linn WS, Rappaport EB, Berhane KT, Bastain TM, Avol EL, Gilliland FD. Exhaled nitric oxide in a population-based study of southern California schoolchildren. Respir Res. 2009; 10:28.
23. Lebecque P, Kiakulanda P, Coates AL. Spirometry in the asthmatic child: is FEF25-75 a more sensitive test than FEV1/FVC? Pediatr Pulmonol. 1993; 16:19–22.
24. Quanjer PH, Stanojevic S, Stocks J, Hall GL, Prasad KV, Cole TJ, Rosenthal M, Perez-Padilla R, Hankinson JL, Falaschetti E, Golshan M, Brunekreef B, Al-Rawas O, Kühr J, Trabelsi Y, Ip MS. Global Lungs Initiative. Changes in the FEV₁/FVC ratio during childhood and adolescence: an intercontinental study. Eur Respir J. 2010; 36:1391–9.
25. Szefler SJ, Mitchell H, Sorkness CA, Gergen PJ, O'Connor GT, Morgan WJ, Kattan M, Pongracic JA, Teach SJ, Bloomberg GR, Eggleston PA, Gruchalla RS, Kercsmar CM, Liu AH, Wildfire JJ, Curry MD, Busse WW. Management of asthma based on exhaled nitric oxide in addition to guideline-based treatment for inner-city adolescents and young adults: a randomised controlled trial. Lancet. 2008; 372:1065–72.
26. Grzelewski T, Witkowski K, Makandjou-Ola E, Grzelewska A, Majak P, Jerzyńska J, Janas A, Stelmach R, Stelmach W, Stelmach I. Diagnostic value of lung function parameters and FeNO for asthma in schoolchildren in large, real-life population. Pediatr Pulmonol. 2014; 49:632–40.
27. Yoon JY, Woo SI, Kim H, Sun YH, Hahn YS. Fractional exhaled nitric oxide and forced expiratory flow between 25% and 75% of vital capacity in children with controlled asthma. Korean J Pediatr. 2012; 55:330–6.
28. Forno E, Fuhlbrigge A, Soto-Quirós ME, Avila L, Raby BA, Brehm J, Sylvia JM, Weiss ST, Celedón JC. Risk factors and predictive clinical scores for asthma exacerbations in childhood. Chest. 2010; 138:1156–65.
29. Lara M, Rosenbaum S, Rachelefsky G, Nicholas W, Morton SC, Emont S, Branch M, Genovese B, Vaiana ME, Smith V, Wheeler L, Platts-Mills T, Clark N, Lurie N, Weiss KB. Improving childhood asthma outcomes in the United States: a blueprint for policy action. Pediatrics. 2002; 109:919–30.
30. Hanson JR, Lee BR, Williams DD, Murphy H, Kennedy K, DeLurgio SA Sr, Portnoy J, Reddy M. Developing a risk stratification model for predicting future health care use in asthmatic children. Ann Allergy Asthma Immunol. 2016; 116:26–30.
Full Text Links
  • APA
export Copy
  • Twitter
  • Facebook
Similar articles
Copyright © 2023 by Korean Association of Medical Journal Editors. All rights reserved.     E-mail: