Expiratory CT scan in patients with normal inspiratory CT scan: a finding of obliterative bronchiolitis and other causes of bronchiolar obstruction
© Gaeta et al.; licensee BioMed Central Ltd. 2013
Received: 24 March 2013
Accepted: 31 May 2013
Published: 9 July 2013
Expiratory CT scan is usually obtained as supplement to normal inspiratory CT scan to recognize air-trapping, which is expression of small airways obstruction. In some patients the air-trapping may be the only sign of an early-stage small airways disease in an otherwise normal lung.
The purpose of this article is to illustrate pathologic conditions, namely obliterative bronchiolitis, in which expiratory CT scan can be abnormal despite normal inspiratory CT examination, and to highlight indications for this technique in patients with clinical and functional suspect of bronchiolar obstruction.
Expiratory CT scan is sensitive for the detection of air-trapping, which is a definitive sign of airway obstruction in various airway disease, including emphysema, bronchiolitis obliterans, bronchial asthma, Swyer-James syndrome, cystic fibrosis, sarcoidosis, hypersensitivity pneumonitis [1, 2]. In many of such patients abnormal findings (i.e. areas of emphysema, bronchiectasis, ground-glass opacity, tree-in-bud) are usually depicted by inspiratory scan that permits a correct diagnosis. However, frequently, the air-trapping may be the only finding of a pulmonary disease in patients with a normal-appearing inspiratory CT scan . According to Fleischner Society glossary , “air-trapping is seen on end-expiration CT scans as parenchymal lung areas with less than normal increase in attenuation and lack of volume reduction”.
Although some authors recommend routine use of paired inspiratory and expiratory CT scans in patients suspected of having diffuse lung disease, this approach is questionable, especially considering the delivered radiation. This is of special concern in young patients or in subjects undergoing repeated exposures .
The purpose of this article, which is based on more than 100 consecutive patients who underwent expiratory CT scan after a normal inspiratory CT examination, is to illustrate diseases which may demonstrate abnormalities on expiratory CT scan despite normal inspiratory CT scan, as obliterative bronchiolitis and less usual causes of bronchiolar obstruction. Furthermore, we have highlighted the indications for expiratory CT scan in patients with clinical and functional suspect of bronchiolar obstruction.
CT scan techniques
Inspiratory and expiratory CT scans are typically obtained at the end of full inspiration and at the end of forced expiration. Expiratory CT scan can be performed with a volumetric or an incremental technique (a limited number of slices at different levels with a section thickness of 1-mm and a table increment of 10-mm). Moreover, it is possible to modulate the radiation dose burden using a low-dose acquisition by reducing the tube current. One study demonstrated that it is possible to reduce the tube current-time product up to 20 mAs without impairing the visualization of air-trapping .
Before expiratory scan, patients are usually instructed: “Take a deep breath, blow out hard, and do not breathe in again for 10 seconds.” It is useful that each patient practices this breathing instructions several times before scanning begin.
Both inspiratory and expiratory scans are performed with the patient in the supine position from the apex to the base of the lungs. No contrast medium administration is necessary.
Inspiratory and expiratory CT images are reconstructed by using a high-spatial-resolution (bone) algorithm at a display window width of 1,600 Hounsfield Units (HU) and a window center of −600 HU.
In recent years, several quantitative analyses for air trapping evaluation are used [6–10]. The most widely explored quantitative CT methods are density-based measures: a) expiratory to inspiratory ratio of mean lung density; b) expiratory to inspiratory relative volume change of voxels with attenuation values between −860 and −950 HU and c) percentage of voxels below −856 HU in expiratory CT scan [6, 7]. In a recent paper, the first of the above mentioned measures performed significantly better than the others in early detection of small airways disease on low-dose CT .
Moreover, it has been demonstrated that lung volume collapsibility, represented by the ratio of expiratory to inspiratory lung CT computed volume, correlates significantly with pulmonary function tests, tissue density-based measures and disease severity in chronic obstructive pulmonary disease [9, 10].
Normal findings on expiratory CT scan
Finally, normal lung tissue increases homogeneously in CT attenuation from inspiration to expiration (Figure 1) because the volume of air in the lung being scanned is reduced.
Air-trapping in healthy subjects
Pulmonary function tests
Interval asthma and chronic bronchitis
Obliterative bronchiolitis is defined histologically as concentric luminal narrowing of the membranous and respiratory bronchioles secondary to submucosal and peribronchiolar inflammation and fibrosis without any intraluminal granulation tissue or polyps. Obliterative bronchiolitis can be cryptogenic, postinfectious (mostly, secondary to prior viral or Mycoplasma infection), or secondary to noxious fume inhalation, graft-versus-host disease, lung transplantation, rheumatoid arthritis, inflammatory bowel disease, and penicillamine therapy [25, 26].
Hypersensitivity pneumonitis is a diffuse granulomatous interstitial lung disease caused by inhalation of various antigenic organic particles. Hypersensitivity pneumonitis is often insidious to diagnose because the clinical manifestations are nonspecific and the radiological and histological patterns can mimic those of other interstitial and small airway diseases. Early diagnosis is mandatory since patients may develop UIP/NSIP lung fibrosis patterns .
Sarcoidosis is a multisystem disorder that is characterized by non-caseous epithelioid cell granulomas, which may affect almost any organ. Pulmonary sarcoidosis is a disease of the interstitium and occurs in approximately 90% of patients. Usually advanced pulmonary sarcoidosis causes a restrictive functional deficit due to fibrosis. On the other hand, the granulomas developing in centrilobular and peribronchiolar lymphatics frequently involve small airways; thus, evidence of air-trapping is considered a common feature of the disease .
Every pneumologist and radiologist should be aware that the air-trapping may be the only finding of a pulmonary disease in patients with a normal-appearing inspiratory CT scan. The knowledge of the possible underlying disorders is the key which permits to suspect the potential diagnoses. Final diagnosis can be reached by means of one or more of these approaches: transbronchial biopsy, open lung biopsy, bronchoscopy, bronchioloalveolar lavage, laboratory tests, response to therapy on follow-up.
patients with respiratory tests showing obstructive pattern, particularly patients showing a small airways obstruction pattern;
patients with chronic cough and/or wheezing;
patients with exertional dyspnea;
patients with demonstrated or suspected conditions associated with small airways diseases, namely sarcoidosis, hypersensitivity pneumonitis and diseases that may cause bronchiolitis obliterans.
Finally, it is worth of attention that MR imaging of the lung, whose main advantage is absence of radiation, is an emerging tool in diagnosis of pulmonary diseases; namely, in evaluating disease activity in chronic lung diseases , in evaluating mucus-containing lung lesions  and in diagnosing invasive mucinous adenocarcinoma (formerly known as mucinous bronchioloalveolar carcinoma) [33–35]. In patients with small airway obstruction, MR imaging with hyperpolarized Helium is an interesting diagnostic option which allows a functional and dynamic evaluation of pulmonary ventilation [36, 37]; however, today it is not widely disposable for clinical use since it is expensive and difficult to perform. In the future a combined use of CT and MR imaging could enhance our capacity to detect more specific patterns of obstructive pulmonary diseases.
Written informed consent was obtained from the patients for publication of this report and any accompanying images.
- Arakawa H, Niimi H, Kurihara Y, Nakajima Y, Webb WR: Expiratory high-resolution CT: diagnostic value in diffuse lung diseases. AJR Am J Roentgenol. 2000, 175: 1537-1543. 10.2214/ajr.175.6.1751537.View ArticlePubMedGoogle Scholar
- Matsuoka S, Kurihara Y, Yagihashi K, Nakajima Y: Quantitative assessment of peripheral airway obstruction on paired expiratory/inspiratory thin-section computed tomography in chronic obstructive pulmonary disease with emphysema. J Comput Assist Tomogr. 2007, 31: 384-389. 10.1097/01.rct.0000243457.00437.10.View ArticlePubMedGoogle Scholar
- Arakawa H, Webb WR: Air trapping on expiratory high-resolution CT scans in the absence of inspiratory scan abnormalities: correlation with pulmonary function tests and differential diagnosis. AJR Am J Roentgenol. 1998, 170: 1349-1353. 10.2214/ajr.170.5.9574614.View ArticlePubMedGoogle Scholar
- Hansell DM, Bankier AA, MacMahon H, McLoud TC, Müller NL, Remy J: Fleischner Society: glossary of terms for thoracic imaging. Radiology. 2008, 246: 697-722. 10.1148/radiol.2462070712.View ArticlePubMedGoogle Scholar
- Bankier AA, Schaefer-Prokop C, De Maertelaer V, Tack D, Jaksch P, Klepetko W, Gevenois PA: Air trapping: comparison of standard-dose and simulated low-dose thin-section CT techniques. Radiology. 2007, 242: 898-906. 10.1148/radiol.2423060196.View ArticlePubMedGoogle Scholar
- Matsuoka S, Kurihara Y, Yagihashi K, Hoshino M, Watanabe N, Nakajima Y: Quantitative assessment of air trapping in chronic obstructive pulmonary disease using inspiratory and expiratory volumetric MDCT. AJR Am J Roentgenol. 2008, 190: 762-769. 10.2214/AJR.07.2820.View ArticlePubMedGoogle Scholar
- Mets OM, Buckens CF, Zanen P, Isgum I, van Ginneken B, Prokop M, Gietema HA, Lammers JW, Vliegenthart R, Oudkerk M, van Klaveren RJ, de Koning HJ, Mali WP, de Jong PA: Identification of chronic obstructive pulmonary disease in lung cancer screening computed tomographic scans. JAMA. 2011, 306: 1775-1781. 10.1001/jama.2011.1531.View ArticlePubMedGoogle Scholar
- Mets OM, Zanen P, Lammers JJ, Isgum I, Gietema HA, van Ginneken B, Prokop M, de Jong PA: Early identification of small airways disease on lung cancer screening CT: comparison of current air trapping measures. Lung. 2012, 190: 629-633. 10.1007/s00408-012-9422-8.View ArticlePubMedGoogle Scholar
- Yamashiro T, Matsuoka S, Bartholmai BJ, San Josè Estepar R, Ross JC, Diaz A, Murayama S, Silverman EK, Hatabu H, Wanshko GR: Collapsibility of lung volume by paired inspiratory and expiratory CT scans: correlations with lung function and mean lung density. Acad Radiol. 2010, 17: 489-495. 10.1016/j.acra.2009.11.004.PubMed CentralView ArticlePubMedGoogle Scholar
- Kundu S, Gu S, Leader JK, Tedrow JR, Sciurba FC, Gur D, Kaminski M, Pu J: Assessment of lung collapsibility in chronic obstructive lung disease patients using CT. Eur Radiol. 2013, 23: 1564-1572. 10.1007/s00330-012-2746-1.PubMed CentralView ArticlePubMedGoogle Scholar
- Chung JH, Kanne JP, Gilman MD: CT of diffuse tracheal disease. AJR Am J Roentgenol. 2011, 196: W240-246. 10.2214/AJR.09.4146.View ArticlePubMedGoogle Scholar
- Tanaka N, Matsumoto T, Miura G, Emoto T, Matsunaga N, Ueda K, Lynch DA: Air trapping at CT: high prevalence in asymptomatic subjects with normal pulmonary function. Radiology. 2003, 227: 776-785. 10.1148/radiol.2273020352.View ArticlePubMedGoogle Scholar
- Weibel ER: Principles and methods for the morphometric study of the lung and other organs. Lab Invest. 1963, 12: 131-155.PubMedGoogle Scholar
- Mead J: The lung's "quiet zone". N Engl J Med. 1970, 282: 1318-1319. 10.1056/NEJM197006042822311.View ArticlePubMedGoogle Scholar
- Hogg JC, Macklem PT, Thurlbeck WM: Site and nature of airway obstruction in chronic obstructive lung disease. N Engl J Med. 1968, 278: 1355-1360. 10.1056/NEJM196806202782501.View ArticlePubMedGoogle Scholar
- Yanai M, Sekizawa K, Ohrui T, Sasaki H, Takishima T: Site of airway obstruction in pulmonary disease: direct measurement of intrabronchial pressure. J Appl Physiol. 1992, 72: 1016-1023.PubMedGoogle Scholar
- Devakonda A, Raoof S, Sung A, Travis WD, Naidich D: Bronchiolar disorders: a clinical-radiological diagnostic algorithm. Chest. 2010, 137: 938-951. 10.1378/chest.09-0800.View ArticlePubMedGoogle Scholar
- Mishima M: Physiological differences and similarities in asthma and COPD–based on respiratory function testing. Allergol Int. 2009, 58: 333-340. 10.2332/allergolint.09-RAI-0131.View ArticlePubMedGoogle Scholar
- Usmani OS, Barnes PJ: Assessing and treating small airways disease in asthma and chronic obstructive pulmonary disease. Ann Med. 2012, 44: 146-156. 10.3109/07853890.2011.585656.View ArticlePubMedGoogle Scholar
- Sorkness RL, Bleecker ER, Busse WW, Calhoun WJ, Castro M, Chung KF, Curran-Everett D, Erzurum SC, Gaston BM, Israel E, Jarjour NN, Moore WC, Peters SP, Teaque WG, Wenzel SE, National Heart, Lung, and Blood Institure Severe Asthma Research Program: Lung function in adults with stable but severe asthma: air trapping and incomplete reversal of obstruction with bronchodilation. J Appl Physiol. 2008, 104: 394-403.View ArticlePubMedGoogle Scholar
- Sutherland ER, Martin RJ, Bowler RP, Zhang Y, Rex MD, Kraft M: Physiologic correlates of distal lung inflammation in asthma. J Allergy Clin Immunol. 2004, 113: 1046-1050. 10.1016/j.jaci.2004.03.016.View ArticlePubMedGoogle Scholar
- Stanescu D: Small airways obstruction syndrome. Chest. 1999, 116: 231-233. 10.1378/chest.116.1.231.View ArticlePubMedGoogle Scholar
- Cohen J, Postma DS, Vink-Klooster K, van der Bij W, Verschuuren E, Ten Hacken NH, Koeter GH, Douma WR: FVC to slow inspiratory vital capacity ratio: a potential marker for small airways obstruction. Chest. 2007, 132: 1198-1203. 10.1378/chest.06-2763.View ArticlePubMedGoogle Scholar
- Silva CIS, Colby TV, Müller NL: Asthma and associated conditions: high-resolution CT and pathologic findings. AJR Am J Roentgenol. 2004, 183: 817-824. 10.2214/ajr.183.3.1830817.View ArticlePubMedGoogle Scholar
- Pipavath SJ, Lynch DA, Cool C, Brown KK, Newell JD: Radiologic and pathologic features of bronchiolitis. AJR Am J Roentgenol. 2005, 185: 2354-2363.Google Scholar
- D'Andrea N, Vigliarolo R, Sanguinetti CM: Respiratory involvement in inflammatory bowel diseases. Multidiscipl Resp Med. 2010, 5: 173-182. 10.1186/2049-6958-5-3-173.View ArticleGoogle Scholar
- Mueller-Mang C, Grosse C, Stiebellehner L, Bankier AA: What every radiologist should know about idiopathic interstitial pneumonias. Radiographics. 2007, 27: 595-615. 10.1148/rg.273065130.View ArticlePubMedGoogle Scholar
- Silva CIS, Churg A, Müller NL: Hypersensitivity pneumonitis: spectrum of high-resolution CT and pathologic findings. AJR Am J Roentgenol. 2007, 188: 334-344. 10.2214/AJR.05.1826.View ArticlePubMedGoogle Scholar
- Hawtin KE, Roddie ME, Mauri FA, Copley SG: Pulmonary sarcoidosis: the “Great Pretender’. Clin Radiol. 2010, 65: 642-650. 10.1016/j.crad.2010.03.004.View ArticlePubMedGoogle Scholar
- Zhang J, Hasegawa I, Hatabu H, Feller-Kopman D, Boiselle PM: Frequency and severity of air trapping at dynamic expiratory CT in patients with tracheobronchomalacia. AJR Am J Roentgenol. 2004, 182: 81-85. 10.2214/ajr.182.1.1820081.View ArticlePubMedGoogle Scholar
- Gaeta M, Blandino A, Scribano E, Minutoli F, Barone M, Andò F, Pandolfo I: Chronic infiltrative lung disease: value of gadolinium-enhanced MRI in the evaluation of disease-activity. Chest. 2000, 117: 1173-1178. 10.1378/chest.117.4.1173.View ArticlePubMedGoogle Scholar
- Gaeta M, Vinci S, Minutoli F, Mazziotti S, Ascenti G, Salamone I, Lamberto S, Blandino A: CT and MRI findings of mucin-containing tumors and pseudotumors of the thorax: pictorial review. Eur Radiol. 2002, 12: 181-189. 10.1007/s003300100934.View ArticlePubMedGoogle Scholar
- Gaeta M, Blandino A, Scribano E, Vinci S, Minutoli F, Pergolizzi S, Pandolfo I: Magnetic resonance imaging of bronchioloalveolar carcinoma. J Thorac Imaging. 2000, 15: 41-47. 10.1097/00005382-200001000-00009.View ArticlePubMedGoogle Scholar
- Gaeta M, Minutoli F, Ascenti G, Vinci S, Mazziotti S, Pandolfo I, Blandino A: MR white lung sign: incidence and significance in pulmonary consolidations. J Comput Assist Tomogr. 2001, 25: 890-896. 10.1097/00004728-200111000-00011.View ArticlePubMedGoogle Scholar
- Gaeta M, Ascenti G, Mazziotti S, Contiguglia R, Barone M, Mileto A: MRI differentiation of pneumonia-like mucinous adenocarcinoma and infectious pneumonia. Eur J Radiol. 2012, 81: 3587-3591. 10.1016/j.ejrad.2011.12.022.View ArticlePubMedGoogle Scholar
- Fain S, Schiebler ML, McCormack DG, Parraga G: Imaging of lung function using hyperpolarized Helium-3 magnetic resonance imaging: review of current and emerging translational methods and applications. J Magn Reson Imaging. 2010, 32: 1398-1408. 10.1002/jmri.22375.PubMed CentralView ArticlePubMedGoogle Scholar
- Holmes JH, O’Halloran RL, Brodsky EK, Bley TA, Francois CJ, Velikina JV, Sorkness RL, Busse WW, Fain SB: Three dimensional imaging of ventilation dynamics in asthmatics using multi-echo projection acquisition with constrained reconstruction. Magn Reson Med. 2009, 62: 1543-1556. 10.1002/mrm.22150.PubMed CentralView ArticlePubMedGoogle Scholar
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