Semin Respir Crit Care Med 2003; 24(5): 473-488
DOI: 10.1055/s-2004-815599
Copyright © 2003 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA. Tel.: +1(212) 584-4662

Imaging of the Small Airways

Johny A. Verschakelen
  • Department of Radiology, University Hospitals, Leuven, Belgium
Further Information

Publication History

Publication Date:
15 January 2004 (online)

ABSTRACT

Small airways disease (SAD) is defined as a pathologic condition in which the small conducting airways are affected either primarily or as part of other pulmonary changes. Diagnosis is often difficult because the many histopathologic subtypes that have been described often lack obvious clinical or imaging correlates and because widespread involvement is needed before clinical symptoms and abnormalities on pulmonary function testing occur. High-resolution computed tomography (HRCT) can be helpful to detect, characterize, and quantify small airways involvement. These airways may become visible directly when inflammation of the bronchiolar wall and accompanying exudates develop. Obstruction of the small airways may be detected indirectly by HRCT when it causes regional underventilation resulting in reduced perfusion. This article discusses the direct and indirect HRCT signs of small airways involvement and, based on the fundamental differences between these signs, gives a short review of the HRCT features of the most important diseases that can affect the small airways.

REFERENCES

  • 1 Lange W. Ueber eine eigenthumliche Erkrankung der kleinen Bronchien und Bronchiolen (bronchitis et bronchiolitis obliterans).  Dtsch Arch Klin Med . 1901;  70 342-364
  • 2 Baar H S, Galindo J. Bronchiolitis fibrosa obliterans.  Thorax . 1966;  21 209-214
  • 3 Gosink B B, Friedman P J, Liebow A A. Bronchiolitis obliterans: roentgenologic-pathologic correlation.  Am J Roentgenol Radium Ther Nucl Med . 1973;  117 816-832
  • 4 Garg K, Lynch D A, Newell J D. et al . Proliferative and constrictive bronchiolitis: classification and radiologic features.  AJR Am J Roentgenol . 1994;  162 803-808
  • 5 Epler G R, Colby T V, McLoud T C. et al . Bronchiolitis obliterans-organizing pneumonia.  N Engl J Med . 1985;  312 152-158
  • 6 Sulavik S B. The concept of “organizing pneumonia.” Chest .  1989;  96 967-969
  • 7 Davison A G, Heard B E, McAllister W A, Turner-Warwick M E. Cryptogenic organizing pneumonitis.  Q J Med . 1983;  52(207) 382-394
  • 8 Geddes D M. BOOP and COP.  Thorax . 1991;  46 545-547
  • 9 ATS/ERS (American Thoracic Society/European Respiratory Society) International Multidisciplinary Consensus Classification of Idiopathic Interstitial Pneumonias.  Am J Respir Crit Care Med . 2002;  165 277-304
  • 10 Hansell D M, Rubens M B, Padley S PG. et al . Obliterative bronchiolitis: individual CT signs of small airways disease and functional correlation.  Radiology . 1997;  203 721-726
  • 11 Myers J L, Colby T V. Pathologic manifestations of bronchiolitis, constrictive bronchiolitis, cryptogenic organizing pneumonia, and diffuse panbronchiolitis.  Clin Chest Med . 1993;  14 611-622
  • 12 Worthy S A, Muller N L. Small airway diseases.  Radiol Clin North Am . 1998;  36 163-173
  • 13 Hwang J H, Kim T S, Lee K S. et al . Bronchiolitis in adults: pathology and imaging.  J Comput Assist Tomogr . 1997;  21 913-919
  • 14 Poletti V, Zompatori M, Cancellieri A. Clinical spectrum of adult chronic bronchiolitis.  Sarcoidosis Vasc Diffuse Lung Dis . 1999;  16 183-196
  • 15 Muller N L, Miller R R. Diseases of the bronchioles: CT and histopathologic findings.  Radiology . 1995;  196 3-12
  • 16 Webb W R, Gamsu G, Wall S D. et al . CT of a bronchial phantom: factors affecting appearance and size measurements.  Invest Radiol . 1984;  19 394-398
  • 17 Seneterre E, Paganin F, Bruel J M. et al . Measurement of the internal size of bronchi using high-resolution computed tomography (HRCT).  Eur Respir J . 1994;  7 596-600
  • 18 Kang E Y, Miller R R, Muller N L. Bronchiectasis: pathologic findings in resected specimens.  Radiology . 1995;  195 649-654
  • 19 Grenier P, Cordeau M P, Beigelman C. High-resolution computed tomography of the airways.  J Thorac Imaging . 1993;  8 213-229
  • 20 Miller W S. The Lung.  2nd ed. Springfield: CC Thomas 1947: 203-205
  • 21 Gruden J F, Webb W R, Warnock M. Centrilobular opacities in the lung on high-resolution CT: diagnostic considerations and pathologic correlation.  AJR Am J Roentgenol . 1994;  162 569-574
  • 22 Itoh H, Murata K, Konishi J. et al . Diffuse lung disease: pathologic basis for the high-resolution computed tomography findings.  J Thorac Imaging . 1993;  8 176-188
  • 23 Murata K, Itoh H, Todo G. et al . Centrilobular lesions of the lung: demonstration by high-resolution CT and pathologic correlation.  Radiology . 1986;  161 641-645
  • 24 Collins J. CT signs and patterns of lung disease.  Radiol Clin North Am . 2001;  39 1115-1135
  • 25 Lynch D A, Webb W R, Gamsu G. et al . Computed tomography in pulmonary sarcoidosis.  J Comput Assist Tomogr . 1989;  13 405-410
  • 26 Stein M G, Mayo J, Muller N. et al . Pulmonary lymphangitic spread of carcinoma: appearance on CT scans.  Radiology . 1987;  162 371-375
  • 27 Connolly S, Manson D, Eberhard A. et al . CT appearance of pulmonary vasculitis in children.  AJR Am J Roentgenol . 1996;  167 901-904
  • 28 Frazier A A, Rosado-de-Christenson M L, Galvin J R. et al . Pulmonary angiitis and granulomatosis: radiologic-pathologic correlation.  Radiographics . 1998;  18 687-710
  • 29 Kushihashi T, Munechika H, Ri K. et al . Bronchioalveolar adenoma of the lung: CT-pathologic correlation.  Radiology . 1994;  193 789-793
  • 30 Alasaly K, Muller N, Ostrow D N. et al . Cryptogenic organizing pneumonia: a report of 25 cases and a review of the literature.  Medicine (Baltimore) . 1995;  74 201-211
  • 31 Lee K S, Kullnig P, Hartman T E. et al . Cryptogenic organizing pneumonia: CT findings in 43 patients.  AJR Am J Roentgenol . 1994;  162 543-546
  • 32 Muller N L, Staples C A, Miller R R. Bronchiolitis obliterans organizing pneumonia: CT features in 14 patients.  AJR Am J Roentgenol . 1990;  154 983-987
  • 33 Hansell D M, Wells A U, Padley S P. et al . Hypersensitivity pneumonitis: correlation of individual CT patterns with functional abnormalities.  Radiology . 1996;  199 123-128
  • 34 Hartman T E, Tazelaar H D, Swensen S J. et al . Cigarette smoking: CT and pathologic findings of associated pulmonary diseases.  Radiographics . 1997;  17 377-390
  • 35 Howling S J, Hansell D M, Wells A U. et al . Follicular bronchiolitis: thin-section CT and histologic findings.  Radiology . 1999;  212 637-642
  • 36 Nishimura K, Kitaichi M, Izumi T. et al . Diffuse panbronchiolitis: correlation of high-resolution CT and pathologic findings.  Radiology . 1992;  184 779-785
  • 37 Remy-Jardin M, Remy J, Wallaert B. et al . Subacute and chronic bird breeder hypersensitivity pneumonitis: sequential evaluation with CT and correlation with lung function tests and bronchoalveolar lavage.  Radiology . 1993;  189 111-118
  • 38 Davies C WH, Tasker A D, Padley S PG. et al . Air trapping in sarcoidosis on computed tomography: correlation with lung function.  Clin Radiol . 2000;  55 217-221
  • 39 Gleeson F V, Traill Z C, Hansell D M. Expiratory CT evidence of small airways obstruction in sarcoidosis.  AJR Am J Roentgenol . 1996;  166 1052-1054
  • 40 Marti-Bonmati L, Ruiz Perales F, Catala F. et al . CT findings in Swyer-James syndrome.  Radiology . 1989;  172 477-480
  • 41 Padley S P, Adler B D, Hansell D M. et al . Bronchiolitis obliterans: high resolution CT findings and correlation with pulmonary function tests.  Clin Radiol . 1993;  47 236-240
  • 42 Stern E J, Frank M S. Small-airways disease of the lungs: findings at expiratory CT.  AJR Am J Roentgenol . 1994;  163 37-41
  • 43 Austin J H, Muller N L, Friedman P J. et al . Glossary of terms for CT of the lungs: recommendations of the Nomenclature Committee of the Fleischner Society.  Radiology . 1996;  200 327-331
  • 44 Worthy S A, Muller N L, Hartman T E. et al . Mosaic attenuation pattern on thin-section CT scans of the lung: differentiation among infiltrative lung, airway, and vascular diseases as a cause.  Radiology . 1997;  205 465-470
  • 45 Primack S L, Muller N L, Mayo J R. et al . Pulmonary parenchymal abnormalities of vascular origin: high-resolution CT findings.  Radiographics . 1994;  14 739-746
  • 46 Mandel J, Mark E J, Hales C A. Pulmonary veno-occlusive disease.  Am J Respir Crit Care Med . 2000;  162 1964-1973
  • 47 Sherrick A D, Swensen S J, Hartman T E. Mosaic pattern of lung attenuation on CT scans: frequency among patients with pulmonary artery hypertension of different causes.  AJR Am J Roentgenol . 1997;  169 79-82
  • 48 Dennie C J, Veinot J P, McCormack D G. et al . Intimal sarcoma of the pulmonary arteries seen as a mosaic pattern of lung attenuation on high-resolution CT.  AJR Am J Roentgenol . 2002;  178 1208-1210
  • 49 Guckel C, Wells A U, Taylor D A. et al . Mechanism of mosaic attenuation of the lungs on computed tomography in induced bronchospasm.  J Appl Physiol . 1999;  86 701-708
  • 50 Arakawa H, Webb W R. 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
  • 51 Desai S R, Hansell D M. Small airways disease: expiratory computed tomography comes of age.  Clin Radiol . 1997;  52 332-337
  • 52 Lucidarme O, Coche E, Cluzel P. et al . Expiratory CT scans for chronic airway disease: correlation with pulmonary function test results.  AJR Am J Roentgenol . 1998;  170 301-307
  • 53 Verschakelen J A, Scheinbaum K, Bogaert J. et al . Expiratory CT in cigarette smokers: correlation between areas of decreased lung attenuation, pulmonary function tests and smoking history.  Eur Radiol . 1998;  8 1391-1399
  • 54 Arakawa H, Webb W R, McCowin M. et al . Inhomogeneous lung attenuation at thin-section CT: diagnostic value of expiratory scans.  Radiology . 1998;  206 89-94
  • 55 Stern E J, Swensen S J, Hartman T E. et al . CT mosaic pattern of lung attenuation: distinguishing different causes.  AJR Am J Roentgenol . 1995;  165 813-816
  • 56 Coche E E, Muller N L, Kim K I. et al . Acute pulmonary embolism: ancillary findings at spiral CT.  Radiology . 1998;  207 753-758
  • 57 Arakawa H, Kurihara Y, Sasaka K. et al . Air trapping on CT of patients with pulmonary embolism.  AJR Am J Roentgenol . 2002;  178 1201-1207
  • 58 Webb W R, Stern E J, Kanth N. et al . Dynamic pulmonary CT: findings in healthy adult men.  Radiology . 1993;  186 117-124
  • 59 Lee K W, Chung S Y, Yang I. et al . Correlation of aging and smoking with air trapping at thin-section CT of the lung in asymptomatic subjects.  Radiology . 2000;  214 831-836
  • 60 Grenier P A, Beigelman-Aubry C, Fetita C. et al . New frontiers in CT imaging of airway disease.  Eur Radiol . 2002;  12 1022-1044
  • 61 Loubeyre P, Revel D, Delignette A. et al . Bronchiectasis detected with thin-section CT as a predictor of chronic lung allograft rejection.  Radiology . 1995;  194 213-216
  • 62 Remy-Jardin M, Remy J, Cortet B. et al . Lung changes in rheumatoid arthritis: CT findings.  Radiology . 1994;  193 375-382
  • 63 Logan P M, Primack S L, Miller R R. et al . Invasive aspergillosis of the airways: radiographic, CT, and pathologic findings.  Radiology . 1994;  193 383-388
  • 64 McGuinness G, Scholes J V, Garay S M. et al . Cytomegalovirus pneumonitis: spectrum of parenchymal CT findings with pathologic correlation in 21 AIDS patients.  Radiology . 1994;  192 451-459
  • 65 Primack S L, Logan P M, Hartman T E, Lee K S, Muller N L. Pulmonary tuberculosis and Mycobacterium avium-intracellulare: a comparison of CT findings.  Radiology . 1995;  194 413-417
  • 66 Aquino S L, Gamsu G, Webb W R. et al . Tree-in-bud pattern: frequency and significance on thin section CT.  J Comput Assist Tomogr . 1996;  20 594-599
  • 67 Fitzgerald J E, King Jr E T, Lynch D A. et al . Diffuse panbronchiolitis in the United States.  Am J Respir Crit Care Med . 1996;  154 497-503
  • 68 Murphy J M, Schnyder P, Verschakelen J. et al . Linear opacities on HRCT in bronchiolitis obliterans organising pneumonia.  Eur Radiol . 1999;  9 1813-1817
  • 69 Logan P M, Miller R R, Muller N L. Cryptogenic organizing pneumonia in the immunocompromised patient: radiologic findings and follow-up in 12 patients.  Can Assoc Radiol J . 1995;  46 272-279
  • 70 Lohr R H, Boland B J, Douglas W W. et al . Organizing pneumonia: features and prognosis of cryptogenic, secondary, and focal variants.  Arch Intern Med . 1997;  157 1323-1329
  • 71 Moon J, duBois R M, Colby T V. et al . Clinical significance of respiratory bronchiolitis on open lung biopsy and its relationship to smoking related interstitial lung disease.  Thorax . 1999;  54 1009-1014
  • 72 Heyneman L E, Ward S, Lynch D A. et al . Respiratory bronchiolitis, respiratory bronchiolitis-associated interstitial lung disease, and desquamative interstitial pneumonia: different entities or part of the spectrum of the same disease process?.  AJR Am J Roentgenol . 1999;  173 1617-1622
  • 73 Perez T, Remy-Jardin M, Cortet B. Airways involvement in rheumatoid arthritis: clinical, functional, and HRCT findings.  Am J Respir Crit Care Med . 1998;  157 1658-1665
  • 74 Worthy S A, Flint J D, Muller N L. Pulmonary complications after bone marrow transplantation: high-resolution CT and pathologic findings.  Radiographics . 1997;  17 1359-1371
  • 75 Worthy S A, Park C S, Kim J S. et al . Bronchiolitis obliterans after lung transplantation: high-resolution CT findings in 15 patients.  AJR Am J Roentgenol . 1997;  169 673-677
  • 76 Stern E J, Muller N L, Swensen S J. et al . CT mosaic pattern of lung attenuation: etiologies and terminology.  J Thorac Imaging . 1995;  10 294-297
  • 77 Bankier A A, Van Muylem A, Knoop C. et al . Bronchiolitis obliterans syndrome in heart-lung transplant recipients: diagnosis with expiratory CT.  Radiology . 2001;  218 533-539
  • 78 Lee E S, Gotway M B, Reddy G P. et al . Early bronchiolitis obliterans following lung transplantation: accuracy of expiratory thin-section CT for diagnosis.  Radiology . 2000;  216 472-477
  • 79 Leung A N, Fisher K, Valentine V. et al . Bronchiolitis obliterans after lung transplantation: detection using expiratory HRCT.  Chest . 1998;  113 365-370
  • 80 Siegel M J, Bhalla S, Gutierrez F R. et al . Post-lung transplantation bronchiolitis obliterans syndrome: usefulness of expiratory thin-section CT for diagnosis.  Radiology . 2001;  220 455-462
  • 81 Hansell D M, Wells A U, Rubens M B. et al . Bronchiectasis: functional significance of areas of decreased attenuation at expiratory CT.  Radiology . 1994;  193 369-374
  • 82 Im J G, Kim S H, Chung M J. et al . Lobular low attenuation of the lung parenchyma on CT: evaluation of forty-eight patients.  J Comput Assist Tomogr . 1996;  20 756-762
  • 83 Roberts H R, Wells A U, Milne D G. et al . Airflow obstruction in bronchiectasis: correlation between computed tomography features and pulmonary function tests.  Thorax . 2000;  55 198-204
  • 84 McDonagh J, Greaves M, Wright A R. et al . High-resolution computed tomography of the lungs in patients with rheumatoid arthritis and interstitial lung disease.  Br J Rheumatol . 1994;  33 118-122
  • 85 Perez T, Farre J M, Gosset P. et al . Subclinical alveolar inflammation in rheumatoid arthritis: superoxide anion, neutrophil chemotactic activity and fibronectin generation by alveolar macrophages.  Eur Respir J . 1989;  2 7-13
  • 86 Wolfe F, Schurle D RE, Lin J J. et al . Upper and lower airway disease in penicillamine treated patients with rheumatoid arthritis.  J Rheumatol . 1983;  10 406-410
  • 87 Hansell D M, Moskovic E. High-resolution computed tomography in extrinsic allergic alveolitis.  Clin Radiol . 1991;  43 8-12
  • 88 Silver S F, Muller N L, Miller R R. et al . Hypersensitivity pneumonitis: evaluation with CT.  Radiology . 1989;  173 441-445
  • 89 Small J H, Flower C D, Traill Z C. et al . Air-trapping in extrinsic allergic alveolitis.  Clin Radiol . 1996;  51 684-688
  • 90 Soleman A, Colby T V. Histologic diagnosis of extrinsic allergic alveolitis.  Am J Surg Pathol . 1988;  12 514-518
  • 91 Adler B D, Padley S P, Muller N L. et al . Chronic hypersensitivity pneumonitis: high-resolution CT and radiographic features in 16 patients.  Radiology . 1992;  185 91-95
  • 92 Lynch D A, Newell J D, Logan P M. et al . Can CT distinguish hypersensitivity pneumonitis from idiopathic pulmonary fibrosis?.  AJR Am J Roentgenol . 1995;  165 807-811
  • 93 Hansell D M, Milne D G, Wilsher M L. et al . Pulmonary sarcoidosis: morphologic associations of airflow obstruction at thin-section CT.  Radiology . 1998;  209 697-704
  • 94 Carrington C B. Structure and function in sarcoidosis.  Ann N Y Acad Sci . 1976;  278 265-283
  • 95 Magkanas E, Voloudaki A, Bouros D. et al . Correlation of expiratory high-resolution CT findings with inspiratory patterns and pulmonary function tests.  Acta Radiol . 2001;  42 494-501
  • 96 Carr D H, Hibon S, Rubens M. et al . Peripheral airways obstruction on high-resolution computed tomography in chronic severe asthma.  Respir Med . 1998;  92 448-453
  • 97 Gevenois P A, Scillia P, de Maertelaer V. et al . The effects of age, sex, lung size, and hyperinflation on CT lung densitometry.  AJR Am J Roentgenol . 1996;  167 1169-1173
  • 98 Grenier P, Mourey-Gerosa I, Benali K. et al . Abnormalities of the airways and lung parenchyma in asthmatics: CT observations in 50 patients and inter- and intra-observer variability.  Eur Radiol . 1996;  6 199-206
  • 99 Lynch D A, Newell J D, Tschomper B A. et al . Uncomplicated asthma in adults: comparison of CT appearance of the lungs in asthmatic and healthy subjects.  Radiology . 1993;  188 829-833
  • 100 Paganin F, Seneterre E, Chanez P. et al . Computed tomography of the lungs in asthma: influence of disease severity and etiology.  Am J Respir Crit Care Med . 1996;  153 110-114
  • 101 Park C S, Muller N L, Worthy S A. et al . Airway obstruction in asthmatic and healthy individuals: inspiratory and expiratory thin-section CT findings.  Radiology . 1997;  203 361-367
  • 102 Awadh N, Muller N L, Park C S. et al . Airway wall thickness in patients with near fatal asthma and control groups: assessment with high-resolution computed tomography.  Thorax . 1998;  53 248-253
  • 103 Niimi A, Matsumoto H, Amitani R. et al . Airway wall thickness in asthma assessed by computed tomography.  Am J Respir Crit Care Med . 2000;  162 1518-1523
  • 104 Laurent F, Latrabe V, Raherison C. et al . Functional significance of air trapping detected in moderate asthma.  Eur Radiol . 2000;  10 1404-1410
  • 105 Newman K B, Lynch D A, Newman L S. et al . Quantitative computed tomography detects air trapping due to asthma.  Chest . 1994;  106 105-109
    >