Diagnosis of Asthma with the Measurement of Exhaled Nitric Oxide: A Systematic Review_Chinese Journal of Respiratory and Critical Care Medicine

Authors：

LIANGBinmiao ¹ , WANG Maoyun ¹ ,  WANG Youjuan ² , YUAN Yuru ¹ , FENG Yulin. ¹

Department of Respiratory Medicine, West China Hospital, Sichuan University. Chengdu, Sichuan, 610041, China;

Corresponding author：

WANG Youjuan, Email: yjwang1963@163.com

Keywords：

Exhaled nitric oxide; Asthma; Diagnostic test; Systematic review

Video：

Export PDF Favorites Scan Get Citation

Abstract Full text Figures/Tables Video References Cited by

Objective To review literatures regarding the diagnosis of asthma with the measurement of exhaled nitric oxide( eNO) and assess the effectiveness and accuracy of eNO in the diagnosis of asthma.Methods MEDLINE, OVID, CBMdisc, CNKI( 1991 to 2008) for studies involving the diagnostic value of eNO were searched, and references of included studies were also hand searched. QUADAS ( Quality Assessment of Diagnostic Accuracy Studies) items were used for quality assessment in the systematic review. Meta-disc software was used to analyze heterogeneity. Sensitivity, specificity and summary diagnostic odds ratio( SDOR) were used for the pooled analysis. The summary receiver operating characteristic ( SROC)curves were drew and the summary areas under the SROC ( SAUC) were calculated. Finally, sensitivity analysis was performed. Results Eleven literatures with15 studies were included. These 15 studies had well controlled the bias of partial verification, differential verification, incorporation and withdrawals. The possibility of the disease progression bias was less and the reference standard review could have a greater bias. The spectrumcomposition of a study, the inclusion and exclusion criteria and the reporting quality were poorly reported. In statistical analysis, the totally pooled sensitivity, pooled specificity, SDOR, SAUC of the measurement of eNO in the diagnosis of asthma was 0. 68, 0. 79, 12. 73, 0. 8446, respectively. Sensitivity analysis demonstrated no disproportionate influences of individual study. Conclusions eNO has a certain value in the diagnosis of asthma. To make further analysis, more studies with high quality are needed.

Citation： LIANGBinmiao ,WANG Maoyun,WANG Youjuan,YUAN Yuru,FENG Yulin.. Diagnosis of Asthma with the Measurement of Exhaled Nitric Oxide: A Systematic Review. Chinese Journal of Respiratory and Critical Care Medicine, 2009, 09(2): 135-140. doi: Copy

1.	Braman SS. The Global Burden of Asthma. Chest, 2006, 130: 4S-12S.
2.	Global Strategy for Asthma Management and Prevention: Global Initiative For Asthma( GINA) 2006. Available from: URL: http: / /www. ginasthma. org.
3.	nd edition.
4.	Crapo RO, Casaburi R, Coates AL, et al. Guidelines for methacholine and exercise challenge testing-1999. Am J Respir Crit Care Med, 2000, 161: 309-329.
5.	Dupont LJ, Rochette F, Demedts MG, et al. Exhaled nitric oxide correlates with airway hyperresponsiveness in steroid-naive patients with mild asthma. AmJ Respir Crit Care Med, 1998, 157: 894-898.
6.	Markus B, Heiner B, Matthias E, et al. The Bayes Library of Diagnostic Studies and Reviews.
7.	Salome CM, Roberts AM, Brown NJ, et al. Exhaled nitric oxide measurements in a population sample of young adults. Am J Respir Crit Care Med, 1999, 159: 911-916.
8.	Chiron R, Vachier I, Godard P, et al. The measurement of exhaled nitric oxide, a new tool in the management of asthma. Presse Med, 2004, 33: 1451-1458.
9.	Kharitonov SA, Gonio F, Kelly C, et al. Reproducibility of exhaled nitric oxide measurements in healthy and asthmatic adults and children. Eur Respir J, 2003, 21: 433-438.
10.	Choi J, Hoffman LA, Rodway GW, et al. Markers of lung disease in exhaled breath: nitric oxide. Biol Res Nurs, 2006 , 7: 241-255 .
11.	Whiting P, Ruties AW, Reitsma JB, et al. The development of QUADAS: a tool for the quality assessment of studies of diagnostic accuracy included in systematic reviews. BMC Med Res Methodol,2003, 3: 25.
12.	Zamora J, Abraira V,Muriel A, et al. Meta-DiSc: a software for metaanalysis of test accuracy data. BMC Med Res Methodol, 2006 , 6: 31 .
13.	Arora R, Thornblade CE, Dauby PA, et al. Exhaled nitric oxide levels in military recruits with new onset asthma. Allergy Asthma Proc, 2006, 27: 493-498.
14.	Berkman N, Avital A, Breuer R, et al. Exhaled nitric oxide in the diagnosis of asthma: comparison with bronchial provocation tests.Thorax, 2005, 60: 383-388.
15.	Chatkin JM, Ansarin K, Silkoff PE, et al. Exhaled nitric oxide as a noninvasive assessment of chronic cough. Am J Respir Crit Care Med, 1999, 159: 1810-1813.
16.	Miedinger D, Chhajed PN, Tamm M, et al. Diagnostic Tests for Asthma in Firefighters. Chest, 2007, 131: 1760-1767.
17.	Deykin A, Massaro AF, Drazen JM, et al. Exhaled Nitric Oxide as a Diagnostic Test for Asthma Online versus Offline Techniques and Effect of Flow Rate. Am J Respir Crit Care Med, 2002, 165: 1597-1601.
18.	Dupont LJ, Demedts MG, Verleden GM. Prospective Evaluation of the Validity of Exhaled Nitric Oxide for the Diagnosis of Asthma.Chest, 2003, 123: 751-756.
19.	Franklin PJ, Turner SW, Le Souef PN, et al. Exhaled nitric oxide and asthma: complex interactions between atopy, airway responsiveness, and symptoms in a community population of children. Thorax, 2003, 58: 1048-1052.
20.	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: 1981-1987.
21.	Malmberg LP, Pelkonen AS, Haahtela T, et al. Exhaled nitric oxide rather than lung function distinguishes preschool children with probable asthma. Thorax, 2003, 58: 494-499.
22.	Smith AD, Cowan JO, Filsell S, et al. Diagnosing asthma:Comparisons between Exhaled Nitric Oxide Measurements and Conventional Tests. Am J Respir Crit Care Med, 2004, 169: 473-478.
23.	Thomas PS, Gibson PG, Wang H, et al. The relationship of exhaled nitric oxide to airway inflammation and responsiveness in children. J Asthma, 2005, 42: 291-295.
24.	Irwig L, Macaskill P, Glasziou P, et al. Meta-analytic methods for diagnostic test accuracy. J Clin Epidemiol, 1995, 48: 119-130.
25.	Riedler J, Reade T, Dalton M, et al. Hypertonic saline challenge in an epidemiologic survey of asthma in children. Am J Respir Crit Care Med, 1994, 150: 1632-1639.
26.	Riedler J, Reade T, Robertson CF. Repeatability of response to hypertonic saline aerosol in children with mild to severe asthma.Pediatr Pulmonol, 1994, 18: 330-336.
27.	Makker HK, Holgate ST. Relation of the hypertonic saline responsiveness of the airways to exercise induced asthma symptom severity and to histamine or methacholine reactivity. Thorax, 1993 ,48: 142-147.
28.	Haby MM, Anderson SD, Peat JK, et al. An exercise challenge protocol for epidemiological studies of asthma in children:comparison with histamine challenge. Eur Respir J, 1994, 7 : 43-49.
29.	Kivity S, Greif J, Reisner B, et al. Bronchial inhalation challenge with ultrasonically nebulized saline; comparison to exercise-induced asthma. Ann Allergy, 1986 , 57: 355 -358.
30.	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.
31.	Pijnenburg MW, Jobsis Q, de J　ngste JC. “Inflammometry” with nitric oxide in exhaled air: a new test for lung diseases [ in Dutch] .Ned Tijdschr Geneeskd, 2001, 145: 946-950.
32.	.

1. Braman SS. The Global Burden of Asthma. Chest, 2006, 130: 4S-12S.
2. Global Strategy for Asthma Management and Prevention: Global Initiative For Asthma( GINA) 2006. Available from: URL: http: / /www. ginasthma. org.
3. nd edition.
4. Crapo RO, Casaburi R, Coates AL, et al. Guidelines for methacholine and exercise challenge testing-1999. Am J Respir Crit Care Med, 2000, 161: 309-329.
5. Dupont LJ, Rochette F, Demedts MG, et al. Exhaled nitric oxide correlates with airway hyperresponsiveness in steroid-naive patients with mild asthma. AmJ Respir Crit Care Med, 1998, 157: 894-898.
6. Markus B, Heiner B, Matthias E, et al. The Bayes Library of Diagnostic Studies and Reviews.
7. Salome CM, Roberts AM, Brown NJ, et al. Exhaled nitric oxide measurements in a population sample of young adults. Am J Respir Crit Care Med, 1999, 159: 911-916.
8. Chiron R, Vachier I, Godard P, et al. The measurement of exhaled nitric oxide, a new tool in the management of asthma. Presse Med, 2004, 33: 1451-1458.
9. Kharitonov SA, Gonio F, Kelly C, et al. Reproducibility of exhaled nitric oxide measurements in healthy and asthmatic adults and children. Eur Respir J, 2003, 21: 433-438.
10. Choi J, Hoffman LA, Rodway GW, et al. Markers of lung disease in exhaled breath: nitric oxide. Biol Res Nurs, 2006 , 7: 241-255 .
11. Whiting P, Ruties AW, Reitsma JB, et al. The development of QUADAS: a tool for the quality assessment of studies of diagnostic accuracy included in systematic reviews. BMC Med Res Methodol,2003, 3: 25.
12. Zamora J, Abraira V,Muriel A, et al. Meta-DiSc: a software for metaanalysis of test accuracy data. BMC Med Res Methodol, 2006 , 6: 31 .
13. Arora R, Thornblade CE, Dauby PA, et al. Exhaled nitric oxide levels in military recruits with new onset asthma. Allergy Asthma Proc, 2006, 27: 493-498.
14. Berkman N, Avital A, Breuer R, et al. Exhaled nitric oxide in the diagnosis of asthma: comparison with bronchial provocation tests.Thorax, 2005, 60: 383-388.
15. Chatkin JM, Ansarin K, Silkoff PE, et al. Exhaled nitric oxide as a noninvasive assessment of chronic cough. Am J Respir Crit Care Med, 1999, 159: 1810-1813.
16. Miedinger D, Chhajed PN, Tamm M, et al. Diagnostic Tests for Asthma in Firefighters. Chest, 2007, 131: 1760-1767.
17. Deykin A, Massaro AF, Drazen JM, et al. Exhaled Nitric Oxide as a Diagnostic Test for Asthma Online versus Offline Techniques and Effect of Flow Rate. Am J Respir Crit Care Med, 2002, 165: 1597-1601.
18. Dupont LJ, Demedts MG, Verleden GM. Prospective Evaluation of the Validity of Exhaled Nitric Oxide for the Diagnosis of Asthma.Chest, 2003, 123: 751-756.
19. Franklin PJ, Turner SW, Le Souef PN, et al. Exhaled nitric oxide and asthma: complex interactions between atopy, airway responsiveness, and symptoms in a community population of children. Thorax, 2003, 58: 1048-1052.
20. 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: 1981-1987.
21. Malmberg LP, Pelkonen AS, Haahtela T, et al. Exhaled nitric oxide rather than lung function distinguishes preschool children with probable asthma. Thorax, 2003, 58: 494-499.
22. Smith AD, Cowan JO, Filsell S, et al. Diagnosing asthma:Comparisons between Exhaled Nitric Oxide Measurements and Conventional Tests. Am J Respir Crit Care Med, 2004, 169: 473-478.
23. Thomas PS, Gibson PG, Wang H, et al. The relationship of exhaled nitric oxide to airway inflammation and responsiveness in children. J Asthma, 2005, 42: 291-295.
24. Irwig L, Macaskill P, Glasziou P, et al. Meta-analytic methods for diagnostic test accuracy. J Clin Epidemiol, 1995, 48: 119-130.
25. Riedler J, Reade T, Dalton M, et al. Hypertonic saline challenge in an epidemiologic survey of asthma in children. Am J Respir Crit Care Med, 1994, 150: 1632-1639.
26. Riedler J, Reade T, Robertson CF. Repeatability of response to hypertonic saline aerosol in children with mild to severe asthma.Pediatr Pulmonol, 1994, 18: 330-336.
27. Makker HK, Holgate ST. Relation of the hypertonic saline responsiveness of the airways to exercise induced asthma symptom severity and to histamine or methacholine reactivity. Thorax, 1993 ,48: 142-147.
28. Haby MM, Anderson SD, Peat JK, et al. An exercise challenge protocol for epidemiological studies of asthma in children:comparison with histamine challenge. Eur Respir J, 1994, 7 : 43-49.
29. Kivity S, Greif J, Reisner B, et al. Bronchial inhalation challenge with ultrasonically nebulized saline; comparison to exercise-induced asthma. Ann Allergy, 1986 , 57: 355 -358.
30. 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.
31. Pijnenburg MW, Jobsis Q, de J　ngste JC. “Inflammometry” with nitric oxide in exhaled air: a new test for lung diseases [ in Dutch] .Ned Tijdschr Geneeskd, 2001, 145: 946-950.
32. .

Chinese Journal of Respiratory and Critical Care Medicine

Diagnosis of Asthma with the Measurement of Exhaled Nitric Oxide: A Systematic Review

Abstract Full text Figures/Tables Video References Cited by

Previous Article

Next Article

Format

Content