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COUNTERPOINT: Should Oscillometry Be Used to Screen for Airway Disease? NoOscillometry Screening for Airway Disease? No FREE TO VIEW

Paul L. Enright, MD
Author and Funding Information

From the University of Arizona (retired).

CORRESPONDENCE TO: Paul L. Enright, MD, PO Box 675, Mount Lemmon, AZ 85619; e-mail: lungguy@gmail.com


CONFLICT OF INTEREST: P. L. E. has been reimbursed for travel expenses by professional societies during the past 3 years for giving talks at international meetings about pulmonary function testing. These societies were often given funding for these talks by ndd Medical Technologies, Inc, which does not make a forced oscillation technique instrument.

Reproduction of this article is prohibited without written permission from the American College of Chest Physicians. See online for more details.


Chest. 2015;148(5):1135-1137. doi:10.1378/chest.15-1038
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Pulmonary physiologists at the Mayo Clinic used a large loudspeaker to measure respiratory system resistance the year I was born (Fig 1).1 My first research project used a forced oscillator to measure bronchodilation during exercise in children with asthma.2 Joe Rodarte, MD, from whom I learned pulmonary physiology at the Mayo Clinic, said about the technique in 1990 that “one man’s noise is another man’s signal.” After five generations and 65 years of improvements in forced oscillation technique (FOT) instrumentation and software, I remain cautiously optimistic that this test will eventually find clinical value.

Figure Jump LinkFigure 1 –  Pulmonary physiologists at the Mayo Clinic using the forced oscillation technique in 1950. Note the 15-in subwoofer loudspeaker used to generate the low-frequency sounds (from Mayo Clinic archives).Grahic Jump Location

The holy grail of pulmonary physiologists during my lifetime has been a test that will reliably detect early chronic airway obstruction (CAO). The most common example of a disease that starts in the silent zone of small airways is COPD due to cigarette smoking. Clinically important airway obstruction develops in only one in 10 smokers, yet currently available tests cannot reliably detect this subset of susceptible smokers during the first 20 or so years of their disease progression. FOT enthusiasts believe that the silent zone is making noise (or at least reflecting it back toward the mouth).3

The use of spirometry to measure airway obstruction is clinically valuable because it (1) helps with the diagnosis of asthma and COPD, (2) is an index of disease severity (or lack of control for asthma), (3) is an independent predictor of morbidity and disease progression, (4) objectively measures response to bronchodilator therapy, and (5) predicts all-cause and COPD-related mortality. However, these benefits have not yet been proven for FOT indexes.

For children with respiratory symptoms who cannot reliably perform spirometry, FOT (or specific airway resistance measured in a body box) may be helpful for diagnosing asthma and response to therapy, but an experienced and motivated technologist can coach > 90% of school-aged children and people aged > 65 years (including patients with severe lung disease) to meet guidelines for acceptable and repeatable spirometry tests.4

Longitudinal studies of smokers have not been done to determine whether FOT indexes measured during baseline examinations add to models that predict progression of CAO, all of which have included spirometry.5 On the other hand, diffusing capacity of lung for carbon monoxide tests have this ability6,7 probably because a low diffusing capacity of lung for carbon monoxide is an index of the emphysema phenotype of COPD. In adult smokers, FOT indexes are modestly correlated with CAO as measured by spirometry and body plethysmography.8,9 Some FOT indexes are abnormal in smokers with normal spirometric findings,10 but more than one-half of smokers with airway obstruction by spirometry have normal FOT indexes.9 FOT indexes are weakly correlated with indexes of airway size measured by lung high-resolution CT scans.9 Despite the statistically significant correlations between FOT indexes and other measures of CAO, these cross-sectional studies do not prove that FOT is better than spirometry for detecting early CAO. Even if FOT indexes could detect early COPD, currently available inhaled drugs for COPD have been proven by large studies not to slow the loss of lung function in smokers with an FEV1 > 60% predicted.11

A major limitation of the FOT to measure changes in airway obstruction (in response to therapy or inhalation challenges) is that FOT indexes cannot be corrected for changes in the lung volume at which the airway resistance is measured. Successful bronchodilation of moderate to severe airway obstruction in both asthma and COPD reduces air trapping and hyperinflation, leading to a variable reduction of the functional residual capacity (FRC) at which airway resistance is measured. Lower FRC not only reduces the work of breathing (and, thus, often reduces the sensation of dyspnea) but also increases airway resistance compared with breathing at the previously higher lung volume. An index of FOT may be misleading by showing no change or a worsening of airway resistance.12 Airway resistance measured in a body plethysmograph avoids this problem by correcting the airway resistance for the measured FRC lung volume (specific airway resistance or specific airway conductance). Only one FOT index (respiratory system resistance slope) has been shown to be associated (but only weakly) with dyspnea in patients with a wide range of COPD severity.13

Reference equations for FOT indexes remain poorly established for adults. A study of healthy adults from five sites using various FOT instruments found excessive heterogeneity among the sites so that the results could not be pooled for a single set of reference equations. The investigators stated, “We conclude that rigorous calibration procedures should be developed to ensure data compatibility. Furthermore, new reference equations based on different setups are recommended to replace those established with a single device.”14 Reports of higher abnormality rates of FOT indexes compared with spirometry rates in groups of exposed or symptomatic subjects15 could be due to inappropriate reference equations for either or both tests, inappropriate abnormality thresholds, or multiple comparisons. Even if group differences are true, the clinical value of FOT tests for individuals remains unproven.

FOT measurements are easy for the patient but remain technically demanding. They are very sensitive to upper airway shunting (cheeks and floor of the mouth), glottic aperture, and leaks around the mouthpiece.16 Technologists must be trained and then gain experience to detect and minimize these sources of errors by carefully examining FOT graphs to eliminate artifacts from the FOT calculations17 (see the physician on the right in Fig 1). The intrasubject variability of FOT indexes (coefficient of variability, 5%-15%) remains substantially higher than for spirometry (coefficient of variability, about 3%),18 so techniques to reduce the variability of FOT indexes continue to evolve.19

In conclusion, I agree with investigators from Belgium who stated:

The impulse oscillation system provides estimates of central and peripheral pulmonary mechanics based on a model of the respiratory system. These estimates have not been critically investigated and no evidence in the literature has been found to support their validity. Until this validity is established, these estimates should be viewed with suspicion.16

Acknowledgments

Other contributions: This editorial is dedicated to the memory of my mentor and friend, Joseph Rodarte, MD.

Dubois AB, Brody AW, Lewis DH, Burgess BF Jr. Oscillation mechanics of lungs and chest in man. J Appl Physiol. 1956;8(6):587-594. [PubMed]
 
Enright PL, McNally JF, Souhrada JF. Effect of lidocaine on the ventilatory and airway responses of asthmatics. Am Rev Respir Dis. 1980;122(6):823-828. [PubMed]
 
Verbanck S, Schuermans D, Meysman M, Paiva M, Vincken W. Noninvasive assessment of airway alterations in smokers: the small airways revisited. Am J Respir Crit Care Med. 2004;170(4):414-419. [CrossRef] [PubMed]
 
Enright PL, Beck KC, Sherrill DL. Repeatability of spirometry in 18,000 adult patients. Am J Respir Crit Care Med. 2004;169(2):235-238. [CrossRef] [PubMed]
 
Drummond MB, Hansel NN, Connett JE, Scanlon PD, Tashkin DP, Wise RA. Spirometric predictors of lung function decline and mortality in early chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2012;185(12):1301-1306. [CrossRef] [PubMed]
 
Nishimura M, Makita H, Nagai K, et al; COPD Cohort Study Investigators. Annual change in pulmonary function and clinical phenotype in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2012;185(1):44-52. [CrossRef] [PubMed]
 
Farkhooy A, Janson C, Arnardóttir RH, Emtner M, Hedenström H, Malinovschi A. Impaired carbon monoxide diffusing capacity is the strongest lung function predictor of decline in 12 minute-walking distance in COPD; a 5-year follow-up study. COPD. 2015;12(3):240-248. [CrossRef] [PubMed]
 
Kolsum U, Borrill Z, Roy K, et al. Impulse oscillometry in COPD: identification of measurements related to airway obstruction, airway conductance and lung volumes. Respir Med. 2009;103(1):136-143. [CrossRef] [PubMed]
 
Crim C, Celli B, Edwards LD, et al; ECLIPSE investigators. Respiratory system impedance with impulse oscillometry in healthy and COPD subjects: ECLIPSE baseline results. Respir Med. 2011;105(7):1069-1078. [CrossRef] [PubMed]
 
Faria AC, Costa AA, Lopes AJ, Jansen JM, Melo PL. Forced oscillation technique in the detection of smoking-induced respiratory alterations: diagnostic accuracy and comparison with spirometry. Clinics (Sao Paulo). 2010;65(12):1295-1304. [CrossRef] [PubMed]
 
Qaseem A, Wilt TJ, Weinberger SE, et al; American College of Physicians; American College of Chest Physicians; American Thoracic Society; European Respiratory Society. Diagnosis and management of stable chronic obstructive pulmonary disease: a clinical practice guideline update from the American College of Physicians, American College of Chest Physicians, American Thoracic Society, and European Respiratory Society. Ann Intern Med. 2011;155(3):179-191. [CrossRef] [PubMed]
 
Pisi R, Tzani P, Aiello M, et al. Small airway dysfunction by impulse oscillometry in asthmatic patients with normal forced expiratory volume in the 1st second values. Allergy Asthma Proc. 2013;34(1):e14-e20. [CrossRef] [PubMed]
 
Mahut B, Caumont-Prim A, Plantier L, et al. Relationships between respiratory and airway resistances and activity-related dyspnea in patients with chronic obstructive pulmonary disease. Int J Chron Obstruct Pulmon Dis. 2012;7:165-171. [PubMed]
 
Oostveen E, Boda K, van der Grinten CP, et al. Respiratory impedance in healthy subjects: baseline values and bronchodilator response. Eur Respir J. 2013;42(6):1513-1523. [CrossRef] [PubMed]
 
Berger KI, Reibman J, Oppenheimer BW, Vlahos I, Harrison D, Goldring RM. Lessons from the World Trade Center disaster: airway disease presenting as restrictive dysfunction. Chest. 2013;144(1):249-257. [CrossRef] [PubMed]
 
Hellinckx J, Cauberghs M, De Boeck K, Demedts M. Evaluation of impulse oscillation system: comparison with forced oscillation technique and body plethysmography. Eur Respir J. 2001;18(3):564-570. [CrossRef] [PubMed]
 
Bikov A, Pride NB, Goldman MD, et al. Glottal aperture and buccal airflow leaks critically affect forced oscillometry measurements. Chest. 2015;148(3):731-738. [CrossRef] [PubMed]
 
Oostveen E, MacLeod D, Lorino H, et al; ERS Task Force on Respiratory Impedance Measurements. The forced oscillation technique in clinical practice: methodology, recommendations and future developments. Eur Respir J. 2003;22(6):1026-1041. [CrossRef] [PubMed]
 
Robinson PD, Turner M, Brown NJ, et al. Procedures to improve the repeatability of forced oscillation measurements in school-aged children. Respir Physiol Neurobiol. 2011;177(2):199-206. [CrossRef] [PubMed]
 

Figures

Figure Jump LinkFigure 1 –  Pulmonary physiologists at the Mayo Clinic using the forced oscillation technique in 1950. Note the 15-in subwoofer loudspeaker used to generate the low-frequency sounds (from Mayo Clinic archives).Grahic Jump Location

Tables

References

Dubois AB, Brody AW, Lewis DH, Burgess BF Jr. Oscillation mechanics of lungs and chest in man. J Appl Physiol. 1956;8(6):587-594. [PubMed]
 
Enright PL, McNally JF, Souhrada JF. Effect of lidocaine on the ventilatory and airway responses of asthmatics. Am Rev Respir Dis. 1980;122(6):823-828. [PubMed]
 
Verbanck S, Schuermans D, Meysman M, Paiva M, Vincken W. Noninvasive assessment of airway alterations in smokers: the small airways revisited. Am J Respir Crit Care Med. 2004;170(4):414-419. [CrossRef] [PubMed]
 
Enright PL, Beck KC, Sherrill DL. Repeatability of spirometry in 18,000 adult patients. Am J Respir Crit Care Med. 2004;169(2):235-238. [CrossRef] [PubMed]
 
Drummond MB, Hansel NN, Connett JE, Scanlon PD, Tashkin DP, Wise RA. Spirometric predictors of lung function decline and mortality in early chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2012;185(12):1301-1306. [CrossRef] [PubMed]
 
Nishimura M, Makita H, Nagai K, et al; COPD Cohort Study Investigators. Annual change in pulmonary function and clinical phenotype in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2012;185(1):44-52. [CrossRef] [PubMed]
 
Farkhooy A, Janson C, Arnardóttir RH, Emtner M, Hedenström H, Malinovschi A. Impaired carbon monoxide diffusing capacity is the strongest lung function predictor of decline in 12 minute-walking distance in COPD; a 5-year follow-up study. COPD. 2015;12(3):240-248. [CrossRef] [PubMed]
 
Kolsum U, Borrill Z, Roy K, et al. Impulse oscillometry in COPD: identification of measurements related to airway obstruction, airway conductance and lung volumes. Respir Med. 2009;103(1):136-143. [CrossRef] [PubMed]
 
Crim C, Celli B, Edwards LD, et al; ECLIPSE investigators. Respiratory system impedance with impulse oscillometry in healthy and COPD subjects: ECLIPSE baseline results. Respir Med. 2011;105(7):1069-1078. [CrossRef] [PubMed]
 
Faria AC, Costa AA, Lopes AJ, Jansen JM, Melo PL. Forced oscillation technique in the detection of smoking-induced respiratory alterations: diagnostic accuracy and comparison with spirometry. Clinics (Sao Paulo). 2010;65(12):1295-1304. [CrossRef] [PubMed]
 
Qaseem A, Wilt TJ, Weinberger SE, et al; American College of Physicians; American College of Chest Physicians; American Thoracic Society; European Respiratory Society. Diagnosis and management of stable chronic obstructive pulmonary disease: a clinical practice guideline update from the American College of Physicians, American College of Chest Physicians, American Thoracic Society, and European Respiratory Society. Ann Intern Med. 2011;155(3):179-191. [CrossRef] [PubMed]
 
Pisi R, Tzani P, Aiello M, et al. Small airway dysfunction by impulse oscillometry in asthmatic patients with normal forced expiratory volume in the 1st second values. Allergy Asthma Proc. 2013;34(1):e14-e20. [CrossRef] [PubMed]
 
Mahut B, Caumont-Prim A, Plantier L, et al. Relationships between respiratory and airway resistances and activity-related dyspnea in patients with chronic obstructive pulmonary disease. Int J Chron Obstruct Pulmon Dis. 2012;7:165-171. [PubMed]
 
Oostveen E, Boda K, van der Grinten CP, et al. Respiratory impedance in healthy subjects: baseline values and bronchodilator response. Eur Respir J. 2013;42(6):1513-1523. [CrossRef] [PubMed]
 
Berger KI, Reibman J, Oppenheimer BW, Vlahos I, Harrison D, Goldring RM. Lessons from the World Trade Center disaster: airway disease presenting as restrictive dysfunction. Chest. 2013;144(1):249-257. [CrossRef] [PubMed]
 
Hellinckx J, Cauberghs M, De Boeck K, Demedts M. Evaluation of impulse oscillation system: comparison with forced oscillation technique and body plethysmography. Eur Respir J. 2001;18(3):564-570. [CrossRef] [PubMed]
 
Bikov A, Pride NB, Goldman MD, et al. Glottal aperture and buccal airflow leaks critically affect forced oscillometry measurements. Chest. 2015;148(3):731-738. [CrossRef] [PubMed]
 
Oostveen E, MacLeod D, Lorino H, et al; ERS Task Force on Respiratory Impedance Measurements. The forced oscillation technique in clinical practice: methodology, recommendations and future developments. Eur Respir J. 2003;22(6):1026-1041. [CrossRef] [PubMed]
 
Robinson PD, Turner M, Brown NJ, et al. Procedures to improve the repeatability of forced oscillation measurements in school-aged children. Respir Physiol Neurobiol. 2011;177(2):199-206. [CrossRef] [PubMed]
 
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