Diagnostic value of exhaled nitric oxide in adult asthma: a systemic review and meta-analysis_Chinese Journal of Respiratory and Critical Care Medicine

Authors：

LI Yi'na ,  LIU Chuntao

Department of Respiratory and Critical Care Medicine, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P. R. China;

Corresponding author：

LIU Chuntao, Email: taosen666@vip.163.com

Keywords：

Fractional exhaled nitric oxide; Asthma; Diagnosis; Meta-analysis

DOI：

10.7507/1671-6205.202105010

Video：

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Objective To explore the diagnostic value of fractional exhaled nitric oxide (FeNO) in adult asthma.Methods PubMed, Embase, Cochrane Library, Wanfang, CNKI and VIP databases were searched for relevant literatures from the time of database establishment to February 2021. Data analysis were made by Revman and Stata.Results A total of 44 articles with 47 records and 9654 subjects were included. The diagnosis sensitivity, specificity, positive and negative predictive value of FeNO were 0.71 (95%CI 0.65 - 0.76), 0.80 (95%CI 0.75 - 0.84), 3.47 (95%CI 2.86 - 4.21), and 0.37 (95%CI 0.31 - 0.43), respectively. The diagnostic odds ratio was 9.49 (95%CI 7.13 - 12.61), and the area under the receiver operating characteristic curve was 0.82 (95%CI 0.79 - 0.85).Conclusions FeNO has certain diagnostic value in diagnosis of asthma. Types of asthma, region and cut-off value all have impact on the diagnostic efficiency of FeNO.

Citation： LI Yi'na, LIU Chuntao. Diagnostic value of exhaled nitric oxide in adult asthma: a systemic review and meta-analysis. Chinese Journal of Respiratory and Critical Care Medicine, 2021, 20(6): 416-423. doi: 10.7507/1671-6205.202105010 Copy

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2.	Huang K, Yang T, Xu J, et al. Prevalence, risk factors, and management of asthma in China: a national cross-sectional study. Lancet, 2019, 394(10196): 407-418.
3.	Brigham EP, West NE. Diagnosis of asthma: diagnostic testing. Int Forum Allergy Rhinol, 2015, 5 Suppl 1: S27-S30.
4.	Reddel HK, Taylor DR, Bateman ED, et al. An official American thoracic society/European respiratory society statement: asthma control and exacerbations: standardizing endpoints for clinical asthma trials and clinical practice. Am J Respir Crit Care Med, 2009, 180(1): 59-99.
5.	Crapo RO, Casaburi R, Coates AL, et al. Guidelines for methacholine and exercise challenge testing-1999. This official statement of the American Thoracic Society was adopted by the ATS board of directors, July 1999. Am J Respir Crit Care Med, 2000, 161(1): 309-329.
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7.	National institute for health and care excellence: clinical guidelines[M]. Asthma: Diagnosis, monitoring and chronic asthma management. London; National Institute for Health and Care Excellence (UK) Copyright © NICE 2020.2020.
8.	Karrasch S, Linde K, Rücker G, et al. Accuracy of FENO for diagnosing asthma: a systematic review. Thorax, 2017, 72(2): 109-116.
9.	Lluncor M, Barranco P, Amaya ED, et al. Relationship between upper airway diseases, exhaled nitric oxide, and bronchial hyperresponsiveness to methacholine. J Asthma, 2019, 56(1): 53-60.
10.	Liu J, Xu R, Zhan C, et al. Clinical utility of ultrahigh fractional exhaled nitric oxide in predicting bronchial hyperresponsiveness in patients with suspected asthma. Postgrad Med J, 2019, 95(1128): 541-546.
11.	Chen FJ, Huang XY, Lin GP, et al. Validity of fractional exhaled nitric oxide and small airway function indices in diagnosis of cough-variant asthma. J Asthma, 2018, 55(7): 750-755.
12.	Porpodis K, Domvri K, Kontakiotis T, et al. Comparison of diagnostic validity of mannitol and methacholine challenges and relationship to clinical status and airway inflammation in steroid-naïve asthmatic patients. J Asthma, 2017, 54(5): 520-529.
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14.	Wang Y, Li L, Han R, et al. Diagnostic value and influencing factors of fractional exhaled nitric oxide in suspected asthma patients. Int J Clin Exp Pathol, 2015, 8(5): 5570-5576.
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1. Masoli M, Fabian D, Holt S, et al. The global burden of asthma: executive summary of the GINA dissemination committee report. Allergy, 2004, 59(5): 469-478.
2. Huang K, Yang T, Xu J, et al. Prevalence, risk factors, and management of asthma in China: a national cross-sectional study. Lancet, 2019, 394(10196): 407-418.
3. Brigham EP, West NE. Diagnosis of asthma: diagnostic testing. Int Forum Allergy Rhinol, 2015, 5 Suppl 1: S27-S30.
4. Reddel HK, Taylor DR, Bateman ED, et al. An official American thoracic society/European respiratory society statement: asthma control and exacerbations: standardizing endpoints for clinical asthma trials and clinical practice. Am J Respir Crit Care Med, 2009, 180(1): 59-99.
5. Crapo RO, Casaburi R, Coates AL, et al. Guidelines for methacholine and exercise challenge testing-1999. This official statement of the American Thoracic Society was adopted by the ATS board of directors, July 1999. Am J Respir Crit Care Med, 2000, 161(1): 309-329.
6. Holz O, Buhl R, Hausen T, et al. Measuring airway inflammation in clinical practise - application and interpretation. Pneumologie, 2007, 61(3): 194-201.
7. National institute for health and care excellence: clinical guidelines[M]. Asthma: Diagnosis, monitoring and chronic asthma management. London; National Institute for Health and Care Excellence (UK) Copyright © NICE 2020.2020.
8. Karrasch S, Linde K, Rücker G, et al. Accuracy of FENO for diagnosing asthma: a systematic review. Thorax, 2017, 72(2): 109-116.
9. Lluncor M, Barranco P, Amaya ED, et al. Relationship between upper airway diseases, exhaled nitric oxide, and bronchial hyperresponsiveness to methacholine. J Asthma, 2019, 56(1): 53-60.
10. Liu J, Xu R, Zhan C, et al. Clinical utility of ultrahigh fractional exhaled nitric oxide in predicting bronchial hyperresponsiveness in patients with suspected asthma. Postgrad Med J, 2019, 95(1128): 541-546.
11. Chen FJ, Huang XY, Lin GP, et al. Validity of fractional exhaled nitric oxide and small airway function indices in diagnosis of cough-variant asthma. J Asthma, 2018, 55(7): 750-755.
12. Porpodis K, Domvri K, Kontakiotis T, et al. Comparison of diagnostic validity of mannitol and methacholine challenges and relationship to clinical status and airway inflammation in steroid-naïve asthmatic patients. J Asthma, 2017, 54(5): 520-529.
13. Nickels AS, Lim KG. Evaluation of exhaled nitric oxide's ability to predict methacholine challenge in adults with nonobstructive spirometry. Ann Allergy Asthma Immunol, 2016, 117(4): 365-369.
14. Wang Y, Li L, Han R, et al. Diagnostic value and influencing factors of fractional exhaled nitric oxide in suspected asthma patients. Int J Clin Exp Pathol, 2015, 8(5): 5570-5576.
15. He L, Wei M, Luo J, et al. Re-evaluation of the diagnostic value of fractional exhaled nitric oxide & its impact in patients with asthma. Indian J Med Res, 2018, 148(4): 441-448.
16. Beretta C, Rifflart C, Evrard G, et al. Assessment of eosinophilic airway inflammation as a contribution to the diagnosis of occupational asthma. Allergy, 2018, 73(1): 206-213.
17. 方思, 陈树煜, 何熹, 等. 呼出气一氧化氮与脉冲振荡技术对亚急性咳嗽患者筛查咳嗽变异性哮喘的价值. 中华医学杂志, 2017, 97(30): 2338-2343.
18. Arora R, Thornblade CE, Dauby PA, et al. Exhaled nitric oxide levels in military recruits with new onset asthma. Allergy Asthma Proc, 2006, 27(6): 493-498.
19. ElHalawani SM, Ly NT, Mahon RT, et al. Exhaled nitric oxide as a predictor of exercise-induced bronchoconstriction. Chest, 2003, 124(2): 639-643.
20. Florentin A, Acouetey DS, Remen T, et al. Exhaled nitric oxide and screening for occupational asthma in two at-risk sectors: bakery and hairdressing. Int J Tuberc Lung Dis, 2014, 18(6): 744-750.
21. Fortuna AM, Feixas T, González M, et al. Diagnostic utility of inflammatory biomarkers in asthma: exhaled nitric oxide and induced sputum eosinophil count. Respir Med, 2007, 101(11): 2416-2421.
22. Fukuhara A, Saito J, Sato S, et al. Validation study of asthma screening criteria based on subjective symptoms and fractional exhaled nitric oxide. Ann Allergy Asthma Immunol, 2011, 107(6): 480-486.
23. Heffler E, Guida G, Marsico P, et al. Exhaled nitric oxide as a diagnostic test for asthma in rhinitic patients with asthmatic symptoms. Respir Med, 2006, 100(11): 1981-1987.
24. Katsoulis K, Ganavias L, Michailopoulos P, et al. Exhaled nitric oxide as screening tool in subjects with suspected asthma without reversibility. Int Arch Allergy Immunol, 2013, 162(1): 58-64.
25. Kostikas K, Papaioannou AI, Tanou K, et al. Portable exhaled nitric oxide as a screening tool for asthma in young adults during pollen season. Chest, 2008, 133(4): 906-913.
26. Kowal K, Bodzenta-Lukaszyk A, Zukowski S. Exhaled nitric oxide in evaluation of young adults with chronic cough. J Asthma, 2009, 46(7): 692-698.
27. Malinovschi A, Backer V, Harving H, et al. The value of exhaled nitric oxide to identify asthma in smoking patients with asthma-like symptoms. Respir Med, 2012, 106(6): 794-801.
28. Pedrosa M, Cancelliere N, Barranco P, et al. Usefulness of exhaled nitric oxide for diagnosing asthma. J Asthma, 2010, 47(7): 817-821.
29. Sato S, Saito J, Sato Y, et al. Clinical usefulness of fractional exhaled nitric oxide for diagnosing prolonged cough. Respir Med, 2008, 102(10): 1452-1459.
30. Schleich FN, Asandei R, Manise M, et al. Is FE_NO50 useful diagnostic tool in suspected asthma?. Int J Clin Pract, 2012, 66(2): 158-165.
31. Schneider A, Schwarzbach J, Faderl B, et al. FENO measurement and sputum analysis for diagnosing asthma in clinical practice. Respir Med, 2013, 107(2): 209-216.
32. Smith AD, Cowan JO, Brassett KP, et al. Exhaled nitric oxide: a predictor of steroid response. Am J Respir Crit Care Med, 2005, 172(4): 453-459.
33. Tilemann L, Gindner L, Meyer F, et al. Differences in local and systemic inflammatory markers in patients with obstructive airways disease. Prim Care Respir J, 2011, 20(4): 407-414.
34. Voutilainen M, Malmberg LP, Vasankari T, et al. Exhaled nitric oxide indicates poorly athlete's asthma. Clin Respir J, 2013, 7(4): 347-353.
35. 张永明, 林江涛, 苏楠, 等. 呼出气一氧化氮检测在慢性咳嗽病因诊断中的价值. 中华医学杂志, 2011, 91(18): 1254-1258.
36. 敖敏, 郭述良, 税莉莉, 等. 呼出气一氧化氮在咳嗽变异性哮喘诊断中的价值. 重庆医科大学学报, 2019, 44(3): 322-326.
37. 陈凤佳, 严英硕, 周燕斌. 呼出气一氧化氮监测对支气管哮喘的诊断及治疗评估价值研究. 中国全科医学, 2014, 17(29): 3430-3434.
38. 陈洁, 李秀. 呼出气一氧化氮诊断支气管哮喘的临床价值. 临床肺科杂志, 2015, 20(9): 1706-1708.
39. 邓海燕, 彭丽慈, 王海潮. 呼出气一氧化氮检测在咳嗽变异性哮喘中的诊断意义. 中外医疗, 2017, 36(2): 1-4+9.
40. 杜丽艳, 庞桂芬, 于国云, 等. 呼出气一氧化氮与肺功能联合检测对于慢性咳嗽病因的诊断价值. 临床肺科杂志, 2018, 23(6): 1081-1084.
41. 黄金华, 许浦生, 黎教武, 等. 支气管激发试验、FENO 及诱导痰 ECP 在哮喘中的相关性及 FENO、诱导痰 ECP 诊断价值. 临床肺科杂志, 2016, 21(7): 1177-1181.
42. 江银玲, 杨万春, 沈欣. 呼出气一氧化氮与支气管哮喘患者外周血嗜酸性粒细胞相关性及联合检测价值. 分子诊断与治疗杂志, 2020, 12(8): 1115-1118+1132.
43. 姜箜鸣, 陈国忠. 呼出气一氧化氮检测在慢性咳嗽病因诊断中的临床意义. 武汉大学学报(医学版), 2018, 39(5): 793-796.
44. 刘莉, 张红梅, 王伟霞, 等. 呼出气一氧化氮在老年咳嗽变异性哮喘鉴别诊断中的应用. 检验医学与临床, 2018, 15(15): 2325-2328.
45. 刘敏, 许西琳, 刘冬, 等. 呼出气一氧化氮和外周血嗜酸性粒细胞百分率对支气管哮喘诊断和病情评估价值. 中华实用诊断与治疗杂志, 2017, 31(8): 769-771.
46. 买智涛, 姜明明, 万善志. FENO 联合血清 ECP、IgE 检测对支气管哮喘的临床诊断价值. 分子诊断与治疗杂志, 2020, 12(5): 625-628+633.
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