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Published in: BMC Pulmonary Medicine 1/2015

Open Access 01-12-2015 | Research article

Clinical impact of high-attenuation and cystic areas on computed tomography in fibrotic idiopathic interstitial pneumonias

Authors: Kiminobu Tanizawa, Tomohiro Handa, Sonoko Nagai, Toyohiro Hirai, Takeshi Kubo, Tsuyoshi Oguma, Isao Ito, Yutaka Ito, Kizuku Watanabe, Kensaku Aihara, Kohei Ikezoe, Toru Oga, Kazuo Chin, Takateru Izumi, Michiaki Mishima

Published in: BMC Pulmonary Medicine | Issue 1/2015

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Abstract

Background

Quantitative computed tomography (CT) analysis has been proposed as a means of objectively assessing fibrotic interstitial pneumonia (IP) including idiopathic pulmonary fibrosis (IPF). We investigated whether percentages of high-attenuation areas (HAA%) and cystic areas (CA%) quantified from CT images were useful as indices of fibrotic IP.

Methods

CT images of 74 patients with fibrotic idiopathic interstitial pneumonias (IPF, 36; non-specific interstitial pneumonia, 9; unclassifiable idiopathic interstitial pneumonia, 29) were analyzed via in-house computer software, which automatically calculated HAA%, CA%, mean lung density (MLD), standard deviation of lung density (SD-LD), kurtosis, and skewness from CT attenuation histograms. These indices were compared in each instance with physiologic measures, visual fibrosis score, clinical diagnosis, radiologic CT pattern, and prognosis.

Results

HAA% correlated significantly with physiologic measures and visual fibrosis score to a moderate extent (%forced vital capacity, rs = −0.59; % carbon monoxide diffusion capacity, rs = −0.43; fibrosis score, rs = 0.23). Densitometric parameters (MLD, SD-LD, kurtosis, and skewness) correlated significantly with physiologic measures and fibrosis score (|rs| = 0.28-0.59). CA% showed no association with pulmonary functions but differed significantly between IPF and other interstitial pneumonias (IPs) (1.50 ± 2.41 % vs. 0.41 ± 0.80 %; P < 0.01) and between the definite usual interstitial pneumonia (UIP) pattern and other patterns (1.48 ± 2.38 % vs. 0.55 ± 1.19 %; P < 0.01). On univariate analysis, HAA%, MLD, SD-LD, kurtosis, skewness, fibrosis score, and definite UIP pattern all correlated with survival, with kurtosis alone identified as a significant predictor of mortality on multivariate analysis (hazard ratio = 0.67; 95 % CI, 0.44-0.96; P = 0.03).

Conclusion

CA% and HAA% are novel quantitative CT indices with differing properties in fibrotic IP evaluations. HAA% largely reflects physiologic impairments, whereas CA% corresponds with diagnosis and HRCT pattern. Of the CT indices examined, kurtosis constituted the strongest predictor of mortality.
Literature
1.
go back to reference Hartley PG, Galvin JR, Hunninghake GW, Merchant JA, Yagla SJ, Speakman SB, et al. High-resolution CT-derived measures of lung density are valid indexes of interstitial lung disease. J Appl Physiol. 1994;76:271–7.PubMed Hartley PG, Galvin JR, Hunninghake GW, Merchant JA, Yagla SJ, Speakman SB, et al. High-resolution CT-derived measures of lung density are valid indexes of interstitial lung disease. J Appl Physiol. 1994;76:271–7.PubMed
2.
go back to reference Best AC, Lynch AM, Bozic CM, Miller D, Grunwald GK, Lynch DA. Quantitative CT indexes in idiopathic pulmonary fibrosis: relationship with physiologic impairment. Radiology. 2003;228:407–14.CrossRefPubMed Best AC, Lynch AM, Bozic CM, Miller D, Grunwald GK, Lynch DA. Quantitative CT indexes in idiopathic pulmonary fibrosis: relationship with physiologic impairment. Radiology. 2003;228:407–14.CrossRefPubMed
3.
go back to reference Do KH, Lee JS, Colby TV, Kitaichi M, Kim DS. Nonspecific interstitial pneumonia versus usual interstitial pneumonia: differences in the density histogram of high-resolution CT. J Comput Assist Tomogr. 2005;29:544–8.CrossRefPubMed Do KH, Lee JS, Colby TV, Kitaichi M, Kim DS. Nonspecific interstitial pneumonia versus usual interstitial pneumonia: differences in the density histogram of high-resolution CT. J Comput Assist Tomogr. 2005;29:544–8.CrossRefPubMed
4.
go back to reference Camiciottoli G, Orlandi I, Bartolucci M, Meoni E, Nacci F, Diciotti S, et al. Lung CT densitometry in systemic sclerosis: correlation with lung function, exercise testing, and quality of life. Chest. 2007;131:672–81.CrossRefPubMed Camiciottoli G, Orlandi I, Bartolucci M, Meoni E, Nacci F, Diciotti S, et al. Lung CT densitometry in systemic sclerosis: correlation with lung function, exercise testing, and quality of life. Chest. 2007;131:672–81.CrossRefPubMed
5.
go back to reference Best AC, Meng J, Lynch AM, Bozic CM, Miller D, Grunwald GK, et al. Idiopathic pulmonary fibrosis: physiologic tests, quantitative CT indexes, and CT visual scores as predictors of mortality. Radiology. 2008;246:935–40.CrossRefPubMed Best AC, Meng J, Lynch AM, Bozic CM, Miller D, Grunwald GK, et al. Idiopathic pulmonary fibrosis: physiologic tests, quantitative CT indexes, and CT visual scores as predictors of mortality. Radiology. 2008;246:935–40.CrossRefPubMed
6.
go back to reference Handa T, Nagai S, Hirai T, Chin K, Kubo T, Oga T, et al. Computed tomography analysis of airway dimensions and lung density in patients with sarcoidosis. Respiration. 2009;77:273–81.CrossRefPubMed Handa T, Nagai S, Hirai T, Chin K, Kubo T, Oga T, et al. Computed tomography analysis of airway dimensions and lung density in patients with sarcoidosis. Respiration. 2009;77:273–81.CrossRefPubMed
7.
go back to reference Raghu G, Collard HR, Egan JJ, Martinez FJ, Behr J, Brown KK, et al. An official ATS/ERS/JRS/ALAT statement: idiopathic pulmonary fibrosis: evidence-based guidelines for diagnosis and management. Am J Respir Crit Care Med. 2011;183:788–824.CrossRefPubMed Raghu G, Collard HR, Egan JJ, Martinez FJ, Behr J, Brown KK, et al. An official ATS/ERS/JRS/ALAT statement: idiopathic pulmonary fibrosis: evidence-based guidelines for diagnosis and management. Am J Respir Crit Care Med. 2011;183:788–824.CrossRefPubMed
8.
go back to reference Lynch DA, Travis WD, Muller NL, Galvin JR, Hansell DM, Grenier PA, et al. Idiopathic interstitial pneumonias: CT features. Radiology. 2005;236:10–21.CrossRefPubMed Lynch DA, Travis WD, Muller NL, Galvin JR, Hansell DM, Grenier PA, et al. Idiopathic interstitial pneumonias: CT features. Radiology. 2005;236:10–21.CrossRefPubMed
9.
go back to reference American Thoracic Society; European Respiratory Society. American Thoracic Society/European Respiratory Society International Multidisciplinary Consensus Classification of the Idiopathic Interstitial Pneumonias. This joint statement of the American Thoracic Society (ATS), and the European Respiratory Society (ERS) was adopted by the ATS board of directors, June 2001 and by the ERS Executive Committee, June 2001. Am J Respir Crit Care Med. 2002;165:277–304.CrossRef American Thoracic Society; European Respiratory Society. American Thoracic Society/European Respiratory Society International Multidisciplinary Consensus Classification of the Idiopathic Interstitial Pneumonias. This joint statement of the American Thoracic Society (ATS), and the European Respiratory Society (ERS) was adopted by the ATS board of directors, June 2001 and by the ERS Executive Committee, June 2001. Am J Respir Crit Care Med. 2002;165:277–304.CrossRef
10.
go back to reference Travis WD, Costabel U, Hansell DM, King Jr TE, Lynch DA, Nicholson AG, et al. An official American Thoracic Society/European Respiratory Society statement: Update of the international multidisciplinary classification of the idiopathic interstitial pneumonias. Am J Respir Crit Care Med. 2013;188:733–48.CrossRefPubMed Travis WD, Costabel U, Hansell DM, King Jr TE, Lynch DA, Nicholson AG, et al. An official American Thoracic Society/European Respiratory Society statement: Update of the international multidisciplinary classification of the idiopathic interstitial pneumonias. Am J Respir Crit Care Med. 2013;188:733–48.CrossRefPubMed
11.
go back to reference Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, et al. Standardisation of spirometry. Eur Respir J. 2005;26:319–38.CrossRefPubMed Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, et al. Standardisation of spirometry. Eur Respir J. 2005;26:319–38.CrossRefPubMed
12.
go back to reference The Committee of Pulmonary Physiology JRS. Guidelines for Pulmonary Function Tests: Spirometry, Flow-Volume Curve, Diffusion Capacity of the Lung. Tokyo: The Japanese Respiratory Society; 2004. The Committee of Pulmonary Physiology JRS. Guidelines for Pulmonary Function Tests: Spirometry, Flow-Volume Curve, Diffusion Capacity of the Lung. Tokyo: The Japanese Respiratory Society; 2004.
13.
go back to reference Ohara T, Hirai T, Sato S, Terada K, Kinose D, Haruna A, et al. Longitudinal study of airway dimensions in chronic obstructive pulmonary disease using computed tomography. Respirology. 2008;13:372–8.CrossRefPubMed Ohara T, Hirai T, Sato S, Terada K, Kinose D, Haruna A, et al. Longitudinal study of airway dimensions in chronic obstructive pulmonary disease using computed tomography. Respirology. 2008;13:372–8.CrossRefPubMed
14.
go back to reference Hansell DM, Bankier AA, MacMahon H, McLoud TC, Muller NL, Remy J. Fleischner Society: glossary of terms for thoracic imaging. Radiology. 2008;246:697–722.CrossRefPubMed Hansell DM, Bankier AA, MacMahon H, McLoud TC, Muller NL, Remy J. Fleischner Society: glossary of terms for thoracic imaging. Radiology. 2008;246:697–722.CrossRefPubMed
15.
go back to reference Kazerooni EA, Martinez FJ, Flint A, Jamadar DA, Gross BH, Spizarny DL, et al. Thin-section CT obtained at 10-mm increments versus limited three-level thin-section CT for idiopathic pulmonary fibrosis: correlation with pathologic scoring. AJR Am J Roentgenol. 1997;169:977–83.CrossRefPubMed Kazerooni EA, Martinez FJ, Flint A, Jamadar DA, Gross BH, Spizarny DL, et al. Thin-section CT obtained at 10-mm increments versus limited three-level thin-section CT for idiopathic pulmonary fibrosis: correlation with pathologic scoring. AJR Am J Roentgenol. 1997;169:977–83.CrossRefPubMed
16.
go back to reference Lynch DA, Godwin JD, Safrin S, Starko KM, Hormel P, Brown KK, et al. High-resolution computed tomography in idiopathic pulmonary fibrosis: diagnosis and prognosis. Am J Respir Crit Care Med. 2005;172:488–93.CrossRefPubMed Lynch DA, Godwin JD, Safrin S, Starko KM, Hormel P, Brown KK, et al. High-resolution computed tomography in idiopathic pulmonary fibrosis: diagnosis and prognosis. Am J Respir Crit Care Med. 2005;172:488–93.CrossRefPubMed
17.
go back to reference Iwasawa T, Asakura A, Sakai F, Kanauchi T, Gotoh T, Ogura T, et al. Assessment of prognosis of patients with idiopathic pulmonary fibrosis by computer-aided analysis of CT images. J Thorac Imaging. 2009;24:216–22.CrossRefPubMed Iwasawa T, Asakura A, Sakai F, Kanauchi T, Gotoh T, Ogura T, et al. Assessment of prognosis of patients with idiopathic pulmonary fibrosis by computer-aided analysis of CT images. J Thorac Imaging. 2009;24:216–22.CrossRefPubMed
18.
go back to reference Sumikawa H, Johkoh T, Yamamoto S, Yanagawa M, Inoue A, Honda O, et al. Computed tomography values calculation and volume histogram analysis for various computed tomographic patterns of diffuse lung diseases. J Comput Assist Tomogr. 2009;33:731–8.CrossRefPubMed Sumikawa H, Johkoh T, Yamamoto S, Yanagawa M, Inoue A, Honda O, et al. Computed tomography values calculation and volume histogram analysis for various computed tomographic patterns of diffuse lung diseases. J Comput Assist Tomogr. 2009;33:731–8.CrossRefPubMed
19.
go back to reference Sumikawa H, Johkoh T, Colby TV, Ichikado K, Suga M, Taniguchi H, et al. Computed tomography findings in pathological usual interstitial pneumonia: relationship to survival. Am J Respir Crit Care Med. 2008;177:433–9.CrossRefPubMed Sumikawa H, Johkoh T, Colby TV, Ichikado K, Suga M, Taniguchi H, et al. Computed tomography findings in pathological usual interstitial pneumonia: relationship to survival. Am J Respir Crit Care Med. 2008;177:433–9.CrossRefPubMed
20.
go back to reference Sumikawa H, Johkoh T, Yamamoto S, Oota M, Ueguchi T, Ogata Y, et al. Volume histogram analysis for lung thin-section computed tomography: differentiation between usual interstitial pneumonia and nonspecific interstitial pneumonia. J Comput Assist Tomogr. 2007;31:936–42.CrossRefPubMed Sumikawa H, Johkoh T, Yamamoto S, Oota M, Ueguchi T, Ogata Y, et al. Volume histogram analysis for lung thin-section computed tomography: differentiation between usual interstitial pneumonia and nonspecific interstitial pneumonia. J Comput Assist Tomogr. 2007;31:936–42.CrossRefPubMed
21.
go back to reference Tanabe N, Muro S, Hirai T, Oguma T, Terada K, Marumo S, et al. Impact of exacerbations on emphysema progression in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2011;183:1653–9.CrossRefPubMed Tanabe N, Muro S, Hirai T, Oguma T, Terada K, Marumo S, et al. Impact of exacerbations on emphysema progression in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2011;183:1653–9.CrossRefPubMed
22.
go back to reference Haruna A, Muro S, Nakano Y, Ohara T, Hoshino Y, Ogawa E, et al. CT scan findings of emphysema predict mortality in COPD. Chest. 2010;138:635–40.CrossRefPubMed Haruna A, Muro S, Nakano Y, Ohara T, Hoshino Y, Ogawa E, et al. CT scan findings of emphysema predict mortality in COPD. Chest. 2010;138:635–40.CrossRefPubMed
23.
go back to reference Ohara T, Hirai T, Muro S, Haruna A, Terada K, Kinose D, et al. Relationship between pulmonary emphysema and osteoporosis assessed by CT in patients with COPD. Chest. 2008;134:1244–9.CrossRefPubMed Ohara T, Hirai T, Muro S, Haruna A, Terada K, Kinose D, et al. Relationship between pulmonary emphysema and osteoporosis assessed by CT in patients with COPD. Chest. 2008;134:1244–9.CrossRefPubMed
24.
go back to reference Matsumoto H, Niimi A, Takemura M, Ueda T, Minakuchi M, Tabuena R, et al. Relationship of airway wall thickening to an imbalance between matrix metalloproteinase-9 and its inhibitor in asthma. Thorax. 2005;60:277–81.CrossRefPubMedPubMedCentral Matsumoto H, Niimi A, Takemura M, Ueda T, Minakuchi M, Tabuena R, et al. Relationship of airway wall thickening to an imbalance between matrix metalloproteinase-9 and its inhibitor in asthma. Thorax. 2005;60:277–81.CrossRefPubMedPubMedCentral
25.
go back to reference Nakano Y, Muro S, Sakai H, Hirai T, Chin K, Tsukino M, et al. Computed tomographic measurements of airway dimensions and emphysema in smokers. Correlation with lung function. Am J Respir Crit Care Med. 2000;162:1102–8.CrossRefPubMed Nakano Y, Muro S, Sakai H, Hirai T, Chin K, Tsukino M, et al. Computed tomographic measurements of airway dimensions and emphysema in smokers. Correlation with lung function. Am J Respir Crit Care Med. 2000;162:1102–8.CrossRefPubMed
26.
go back to reference Mishima M, Hirai T, Itoh H, Nakano Y, Sakai H, Muro S, et al. Complexity of terminal airspace geometry assessed by lung computed tomography in normal subjects and patients with chronic obstructive pulmonary disease. Proc Natl Acad Sci U S A. 1999;96:8829–34.CrossRefPubMedPubMedCentral Mishima M, Hirai T, Itoh H, Nakano Y, Sakai H, Muro S, et al. Complexity of terminal airspace geometry assessed by lung computed tomography in normal subjects and patients with chronic obstructive pulmonary disease. Proc Natl Acad Sci U S A. 1999;96:8829–34.CrossRefPubMedPubMedCentral
27.
go back to reference Maldonado F, Moua T, Rajagopalan S, Karwoski RA, Raghunath S, Decker PA, et al. Automated quantification of radiological patterns predicts survival in idiopathic pulmonary fibrosis. Eur Respir J. 2014;43:204–12.CrossRefPubMed Maldonado F, Moua T, Rajagopalan S, Karwoski RA, Raghunath S, Decker PA, et al. Automated quantification of radiological patterns predicts survival in idiopathic pulmonary fibrosis. Eur Respir J. 2014;43:204–12.CrossRefPubMed
28.
go back to reference Watadani T, Sakai F, Johkoh T, Noma S, Akira M, Fujimoto K, et al. Interobserver variability in the CT assessment of honeycombing in the lungs. Radiology. 2013;266:936–44.CrossRefPubMed Watadani T, Sakai F, Johkoh T, Noma S, Akira M, Fujimoto K, et al. Interobserver variability in the CT assessment of honeycombing in the lungs. Radiology. 2013;266:936–44.CrossRefPubMed
29.
go back to reference Sumikawa H, Johkoh T, Nagareda T, Sekiguchi J, Matsuo K, Fujita Y, et al. Pulmonary adenocarcinomas with ground-glass attenuation on thin-section CT: quantification by three-dimensional image analyzing method. Eur J Radiol. 2008;65:104–11.CrossRefPubMed Sumikawa H, Johkoh T, Nagareda T, Sekiguchi J, Matsuo K, Fujita Y, et al. Pulmonary adenocarcinomas with ground-glass attenuation on thin-section CT: quantification by three-dimensional image analyzing method. Eur J Radiol. 2008;65:104–11.CrossRefPubMed
30.
go back to reference Martinez FJ, de Andrade JA, Anstrom KJ, King Jr TE, Raghu G, Idiopathic Pulmonary Fibrosis Clinical Research N. Randomized trial of acetylcysteine in idiopathic pulmonary fibrosis. N Engl J Med. 2014;370:2093–101.CrossRefPubMedPubMedCentral Martinez FJ, de Andrade JA, Anstrom KJ, King Jr TE, Raghu G, Idiopathic Pulmonary Fibrosis Clinical Research N. Randomized trial of acetylcysteine in idiopathic pulmonary fibrosis. N Engl J Med. 2014;370:2093–101.CrossRefPubMedPubMedCentral
31.
go back to reference Nishiyama O, Taniguchi H, Kondoh Y, Kimura T, Kato K, Kataoka K, et al. A simple assessment of dyspnoea as a prognostic indicator in idiopathic pulmonary fibrosis. Eur Respir J. 2010;36:1067–72.CrossRefPubMed Nishiyama O, Taniguchi H, Kondoh Y, Kimura T, Kato K, Kataoka K, et al. A simple assessment of dyspnoea as a prognostic indicator in idiopathic pulmonary fibrosis. Eur Respir J. 2010;36:1067–72.CrossRefPubMed
32.
go back to reference Lama VN, Flaherty KR, Toews GB, Colby TV, Travis WD, Long Q, et al. Prognostic value of desaturation during a 6-minute walk test in idiopathic interstitial pneumonia. Am J Respir Crit Care Med. 2003;168:1084–90.CrossRefPubMed Lama VN, Flaherty KR, Toews GB, Colby TV, Travis WD, Long Q, et al. Prognostic value of desaturation during a 6-minute walk test in idiopathic interstitial pneumonia. Am J Respir Crit Care Med. 2003;168:1084–90.CrossRefPubMed
33.
go back to reference Ley B, Collard HR, King Jr TE. Clinical course and prediction of survival in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2011;183:431–40.CrossRefPubMed Ley B, Collard HR, King Jr TE. Clinical course and prediction of survival in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2011;183:431–40.CrossRefPubMed
34.
go back to reference du Bois RM, Weycker D, Albera C, Bradford WZ, Costabel U, Kartashov A, et al. Ascertainment of individual risk of mortality for patients with idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2011;184:459–66.CrossRefPubMed du Bois RM, Weycker D, Albera C, Bradford WZ, Costabel U, Kartashov A, et al. Ascertainment of individual risk of mortality for patients with idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2011;184:459–66.CrossRefPubMed
35.
go back to reference Hamada K, Nagai S, Tanaka S, Handa T, Shigematsu M, Nagao T, et al. Significance of pulmonary arterial pressure and diffusion capacity of the lung as prognosticator in patients with idiopathic pulmonary fibrosis. Chest. 2007;131:650–6.CrossRefPubMed Hamada K, Nagai S, Tanaka S, Handa T, Shigematsu M, Nagao T, et al. Significance of pulmonary arterial pressure and diffusion capacity of the lung as prognosticator in patients with idiopathic pulmonary fibrosis. Chest. 2007;131:650–6.CrossRefPubMed
36.
go back to reference Collard HR, King Jr TE, Bartelson BB, Vourlekis JS, Schwarz MI, Brown KK. Changes in clinical and physiologic variables predict survival in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2003;168:538–42.CrossRefPubMed Collard HR, King Jr TE, Bartelson BB, Vourlekis JS, Schwarz MI, Brown KK. Changes in clinical and physiologic variables predict survival in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2003;168:538–42.CrossRefPubMed
37.
go back to reference Lee JS, Ryu JH, Elicker BM, Lydell CP, Jones KD, Wolters PJ, et al. Gastroesophageal reflux therapy is associated with longer survival in patients with idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2011;184:1390–4.CrossRefPubMedPubMedCentral Lee JS, Ryu JH, Elicker BM, Lydell CP, Jones KD, Wolters PJ, et al. Gastroesophageal reflux therapy is associated with longer survival in patients with idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2011;184:1390–4.CrossRefPubMedPubMedCentral
38.
go back to reference Jegal Y, Kim DS, Shim TS, Lim CM, Do Lee S, Koh Y, et al. Physiology is a stronger predictor of survival than pathology in fibrotic interstitial pneumonia. Am J Respir Crit Care Med. 2005;171:639–44.CrossRefPubMed Jegal Y, Kim DS, Shim TS, Lim CM, Do Lee S, Koh Y, et al. Physiology is a stronger predictor of survival than pathology in fibrotic interstitial pneumonia. Am J Respir Crit Care Med. 2005;171:639–44.CrossRefPubMed
39.
go back to reference Taniguchi H, Kondoh Y, Ebina M, Azuma A, Ogura T, Taguchi Y, et al. The clinical significance of 5% change in vital capacity in patients with idiopathic pulmonary fibrosis: extended analysis of the pirfenidone trial. Respir Res. 2011;12:93.CrossRefPubMedPubMedCentral Taniguchi H, Kondoh Y, Ebina M, Azuma A, Ogura T, Taguchi Y, et al. The clinical significance of 5% change in vital capacity in patients with idiopathic pulmonary fibrosis: extended analysis of the pirfenidone trial. Respir Res. 2011;12:93.CrossRefPubMedPubMedCentral
Metadata
Title
Clinical impact of high-attenuation and cystic areas on computed tomography in fibrotic idiopathic interstitial pneumonias
Authors
Kiminobu Tanizawa
Tomohiro Handa
Sonoko Nagai
Toyohiro Hirai
Takeshi Kubo
Tsuyoshi Oguma
Isao Ito
Yutaka Ito
Kizuku Watanabe
Kensaku Aihara
Kohei Ikezoe
Toru Oga
Kazuo Chin
Takateru Izumi
Michiaki Mishima
Publication date
01-12-2015
Publisher
BioMed Central
Published in
BMC Pulmonary Medicine / Issue 1/2015
Electronic ISSN: 1471-2466
DOI
https://doi.org/10.1186/s12890-015-0069-0

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