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Lin Q, Wu Z, Huang M, Dang Z, Tian L, Guan Y, Liu G, Lu Y, Tian Y. Detection of early pulmonary emphysema by multi-contrast x-ray Talbot-Lau interferometer. Med Phys 2024; 51:4133-4142. [PMID: 38578373 DOI: 10.1002/mp.17053] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/16/2023] [Revised: 03/14/2024] [Accepted: 03/24/2024] [Indexed: 04/06/2024] Open
Abstract
BACKGROUND Pulmonary emphysema is a part of chronic obstructive pulmonary disease, which is an irreversible chronic respiratory disease. In order to avoid further damage to lung tissue, early diagnosis and treatment of pulmonary emphysema is essential. PURPOSE Early pulmonary emphysema diagnosis is difficult with conventional radiographic imaging. Recently, x-ray phase contrast imaging has proved to be an effective and promising imaging strategy for soft tissue, due to its high sensitivity and multi-contrast. The aim of this study is to diagnose pulmonary emphysema early utilizing an x-ray Talbot-Lau interferometer (TLI). METHODS We successfully established the mouse model of emphysema by porcine pancreatic elastase treatment, and then used the established x-ray TLI to perform imaging experiments on the mice with different treatment time. The traditional absorption CT and phase contrast CT were obtained simultaneously through TLI. The CT results and histopathology of mice lung in different treatment time were quantitatively analyzed. RESULTS By imaging mice lungs, it can be found that phase contrast has higher sensitivity than absorption contrast in early pulmonary emphysema. The results show that the phase contrast signal could distinguish the pulmonary emphysema earlier than the conventional attenuation signal, which can be consistent with histological images. Through the quantitative analysis of pathological section and phase contrast CT, it can be found that there is a strong linear correlation. CONCLUSIONS In this study, we quantitatively analyze mean linear intercept of histological sections and CT values of mice. The results show that the phase contrast signal has higher imaging sensitivity than the attenuation signal. X-ray TLI multi-contrast imaging is proved as a potential diagnostic method for early pulmonary emphysema in mice.
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Affiliation(s)
- Qisi Lin
- National Synchrotron Radiation Laboratory, University of Science and Technology of China, Hefei, China
| | - Zhao Wu
- National Synchrotron Radiation Laboratory, University of Science and Technology of China, Hefei, China
| | - Meng Huang
- National Synchrotron Radiation Laboratory, University of Science and Technology of China, Hefei, China
- Ultrasonic Department, The First Affiliated Hospital of Anhui Medical University, Hefei, China
| | - Zheng Dang
- National Synchrotron Radiation Laboratory, University of Science and Technology of China, Hefei, China
| | - Lijiao Tian
- National Synchrotron Radiation Laboratory, University of Science and Technology of China, Hefei, China
| | - Yong Guan
- National Synchrotron Radiation Laboratory, University of Science and Technology of China, Hefei, China
| | - Gang Liu
- National Synchrotron Radiation Laboratory, University of Science and Technology of China, Hefei, China
| | - Yalin Lu
- Hefei National Laboratory for Physical Sciences at the Microscale, University of Science and Technology of China, Hefei, China
| | - Yangchao Tian
- National Synchrotron Radiation Laboratory, University of Science and Technology of China, Hefei, China
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Elbehairy AF, Marshall H, Naish JH, Wild JM, Parraga G, Horsley A, Vestbo J. Advances in COPD imaging using CT and MRI: linkage with lung physiology and clinical outcomes. Eur Respir J 2024; 63:2301010. [PMID: 38548292 DOI: 10.1183/13993003.01010-2023] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/14/2023] [Accepted: 03/16/2024] [Indexed: 05/04/2024]
Abstract
Recent years have witnessed major advances in lung imaging in patients with COPD. These include significant refinements in images obtained by computed tomography (CT) scans together with the introduction of new techniques and software that aim for obtaining the best image whilst using the lowest possible radiation dose. Magnetic resonance imaging (MRI) has also emerged as a useful radiation-free tool in assessing structural and more importantly functional derangements in patients with well-established COPD and smokers without COPD, even before the existence of overt changes in resting physiological lung function tests. Together, CT and MRI now allow objective quantification and assessment of structural changes within the airways, lung parenchyma and pulmonary vessels. Furthermore, CT and MRI can now provide objective assessments of regional lung ventilation and perfusion, and multinuclear MRI provides further insight into gas exchange; this can help in structured decisions regarding treatment plans. These advances in chest imaging techniques have brought new insights into our understanding of disease pathophysiology and characterising different disease phenotypes. The present review discusses, in detail, the advances in lung imaging in patients with COPD and how structural and functional imaging are linked with common resting physiological tests and important clinical outcomes.
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Affiliation(s)
- Amany F Elbehairy
- Department of Chest Diseases, Faculty of Medicine, Alexandria University, Alexandria, Egypt
- Division of Infection, Immunity and Respiratory Medicine, The University of Manchester and Manchester University NHS Foundation Trust, Manchester Academic Health Sciences Centre, Manchester, UK
| | - Helen Marshall
- POLARIS, Imaging, Department of Infection, Immunity and Cardiovascular Disease, University of Sheffield, Sheffield, UK
| | - Josephine H Naish
- MCMR, Manchester University NHS Foundation Trust, Manchester, UK
- Bioxydyn Limited, Manchester, UK
| | - Jim M Wild
- POLARIS, Imaging, Department of Infection, Immunity and Cardiovascular Disease, University of Sheffield, Sheffield, UK
- Insigneo Institute for in silico Medicine, Sheffield, UK
| | - Grace Parraga
- Robarts Research Institute, Western University, London, ON, Canada
- Department of Medical Biophysics, Western University, London, ON, Canada
- Division of Respirology, Western University, London, ON, Canada
| | - Alexander Horsley
- Division of Infection, Immunity and Respiratory Medicine, The University of Manchester and Manchester University NHS Foundation Trust, Manchester Academic Health Sciences Centre, Manchester, UK
| | - Jørgen Vestbo
- Division of Infection, Immunity and Respiratory Medicine, The University of Manchester and Manchester University NHS Foundation Trust, Manchester Academic Health Sciences Centre, Manchester, UK
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Abstract
Lung emphysema represents a major public health burden and still accounts for five percent of all deaths worldwide. Hence, it is essential to further understand this disease in order to develop effective diagnostic and therapeutic strategies. Lung emphysema is an irreversible enlargement of the airways distal to the terminal bronchi (i.e., the alveoli) due to the destruction of the alveolar walls. The two most important causes of emphysema are (I) smoking and (II) α1-antitrypsin-deficiency. In the former lung emphysema is predominant in the upper lung parts, the latter is characterized by a predominance in the basal areas of the lungs. Since quantification and evaluation of the distribution of lung emphysema is crucial in treatment planning, imaging plays a central role. Imaging modalities in lung emphysema are manifold: computed tomography (CT) imaging is nowadays the gold standard. However, emerging imaging techniques like dynamic or functional magnetic resonance imaging (MRI), scintigraphy and lately also the implementation of radiomics and artificial intelligence are more and more diffused in the evaluation, diagnosis and quantification of lung emphysema. The aim of this review is to shortly present the different subtypes of lung emphysema, to give an overview on prediction and risk assessment in emphysematous disease and to discuss not only the traditional, but also the new imaging techniques for diagnosis, quantification and evaluation of lung emphysema.
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Affiliation(s)
- Katharina Martini
- Institute of Diagnostic and Interventional Radiology, University Hospital Zurich, Zurich, Switzerland
| | - Thomas Frauenfelder
- Institute of Diagnostic and Interventional Radiology, University Hospital Zurich, Zurich, Switzerland
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Crossley D, Turner A, Subramanian D. Phenotyping emphysema and airways disease: Clinical value of quantitative radiological techniques. World J Respirol 2017; 7:1-16. [DOI: 10.5320/wjr.v7.i1.1] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 08/31/2016] [Revised: 11/23/2016] [Accepted: 01/14/2017] [Indexed: 02/06/2023] Open
Abstract
The pathophysiology of chronic obstructive pulmonary disease (COPD) and Alpha one antitrypsin deficiency is increasingly recognised as complex such that lung function alone is insufficient for early detection, clinical categorisation and dictating management. Quantitative imaging techniques can detect disease earlier and more accurately, and provide an objective tool to help phenotype patients into predominant airways disease or emphysema. Computed tomography provides detailed information relating to structural and anatomical changes seen in COPD, and magnetic resonance imaging/nuclear imaging gives functional and regional information with regards to ventilation and perfusion. It is likely imaging will become part of routine clinical practice, and an understanding of the implications of the data is essential. This review discusses technical and clinical aspects of quantitative imaging in obstructive airways disease.
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Wielpütz MO, Kauczor HU. Imaging cystic fibrosis lung disease with MRI. IMAGING 2016. [DOI: 10.1183/2312508x.10002415] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/05/2022] Open
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Xia Y, Guan Y, Fan L, Liu SY, Yu H, Zhao LM, Li B. Dynamic contrast enhanced magnetic resonance perfusion imaging in high-risk smokers and smoking-related COPD: correlations with pulmonary function tests and quantitative computed tomography. COPD 2015; 11:510-20. [PMID: 25211632 DOI: 10.3109/15412555.2014.948990] [Citation(s) in RCA: 18] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/13/2022]
Abstract
The study aimed to prospectively evaluate correlations between dynamic contrast-enhanced (DCE) MR perfusion imaging, pulmonary function tests (PFT) and volume quantitative CT in smokers with or without chronic obstructive pulmonary disease (COPD) and to determine the value of DCE-MR perfusion imaging and CT volumetric imaging on the assessment of smokers. According to the ATS/ERS guidelines, 51 male smokers were categorized into five groups: At risk for COPD (n = 8), mild COPD (n = 9), moderate COPD (n = 12), severe COPD (n = 10), and very severe COPD (n = 12). Maximum slope of increase (MSI), positive enhancement integral (PEI), etc. were obtained from MR perfusion data. The signal intensity ratio (RSI) of the PDs and normal lung was calculated (RSI = SIPD/SInormal). Total lung volume (TLV), total emphysema volume (TEV) and emphysema index (EI) were obtained from volumetric CT data. For "at risk for COPD," the positive rate of PDs on MR perfusion images was higher than that of abnormal changes on non-enhanced CT images (p < 0.05). Moderate-to-strong positive correlations were found between all the PFT parameters and SIPD, or RSI (r range 0.445∼0.683, p ≤ 0.001). TEV and EI were negatively correlated better with FEV1/FVC than other PFT parameters (r range -0.48 --0.63, p < 0.001). There were significant differences in RSI and SIPD between "at risk for COPD" and "very severe COPD," and between "mild COPD" and "very severe COPD". Thus, MR perfusion imaging may be a good approach to identify early evidence of COPD and may have potential to assist in classification of COPD.
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Affiliation(s)
- Yi Xia
- 1Department of Radiology, Changzheng Hospital of the Second Military Medical University , Shanghai , China
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Assessment of the relationship between morphological emphysema phenotype and corresponding pulmonary perfusion pattern on a segmental level. Eur Radiol 2014; 25:72-80. [PMID: 25163898 DOI: 10.1007/s00330-014-3385-5] [Citation(s) in RCA: 6] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/14/2014] [Revised: 07/09/2014] [Accepted: 08/05/2014] [Indexed: 01/23/2023]
Abstract
PURPOSE Distinct morphological emphysema phenotypes were assessed by CT to show characteristic perfusion defect patterns. MATERIAL/METHODS Forty-one patients with severe emphysema (GOLD III/IV) underwent three-dimensional high resolution computed tomography (3D-HRCT) and contrast-enhanced magnetic resonance (MR) perfusion. 3D-HRCT data was visually analyzed for emphysema phenotyping and quantification by consensus of three experts in chest-radiology. The predominant phenotype per segment was categorized as normal, centrilobular, panlobular or paraseptal. Segmental lung perfusion was visually analyzed using six patterns of pulmonary perfusion (1-normal; 2-mild homogeneous reduction in perfusion; 3-heterogeneous perfusion without focal defects; 4-heterogeneous perfusion with focal defects; 5-heterogeneous absence of perfusion; 6-homogeneous absence of perfusion), with the extent of the defect given as a percentage. RESULTS 730 segments were evaluated. CT categorized 566 (78%) as centrilobular, 159 (22%) as panlobular and 5 (<1%) as paraseptal with no normals. Scores with regards to MR perfusion patterns were: 1-0; 2-0; 3-28 (4%); 4-425 (58%); 5-169 (23%); 6-108 (15%). The predominant perfusion pattern matched as follows: 70 % centrilobular emphysema - heterogeneous perfusion with focal defects (score 4); 42% panlobular--homogeneous absence of perfusion (score 5); and 43% panlobular--heterogeneous absence of perfusion (score 6). CONCLUSION MR pulmonary perfusion patterns correlate with the CT phenotype at a segmental level in patients with severe emphysema. KEY POINTS • MR perfusion patterns correlate with the CT phenotype in emphysema. • Reduction of MR perfusion is associated with loss of lung parenchyma on CT • Centrilobular emphysema shows heterogeneous perfusion reduction while panlobular emphysema shows loss of perfusion.
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Abstract
Lung involvement in cystic fibrosis (CF) disease continues to be a major life-limiting factor of this autosomal recessive genetic disorder. Efforts made toward early diagnosis and advances in therapy have led to sustained survival of affected patients, and many are now of adult age. Because imaging provides detailed information on regional distribution of CF lung disease, repetitive imaging is required for severity assessment and therapy monitoring not only in clinical routine but also for interventional trials. Computed tomography has long succeeded chest radiograph because it provides the highest morphologic detail of airway and parenchymal changes. This is inseparably accompanied by an increase in radiation exposure to CF individuals, who are critically susceptible to, and may accumulate, relevant doses during their lifetime. Magnetic resonance imaging (MRI) as an ionizing radiation-free cross-sectional imaging modality is capable of depicting anatomic hallmarks of CF lung disease at lower spatial resolution but with enhanced tissue characterization. Comprehensive functional lung imaging (imaging of respiratory mechanics, ventilation, and lung perfusion) provides valuable additional information that cannot or can hardly be obtained by any other single diagnostic procedure. The present review article strives to present the current state of lung MRI in CF, as well as its future perspectives. Functional MRI of the CF lung is at the threshold of being considered a routine application, which, supporting early diagnosis, may help to further improve the survival of CF patients.
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9
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Hopkins SR, Wielpütz MO, Kauczor HU. Imaging lung perfusion. J Appl Physiol (1985) 2012; 113:328-39. [PMID: 22604884 PMCID: PMC3404706 DOI: 10.1152/japplphysiol.00320.2012] [Citation(s) in RCA: 64] [Impact Index Per Article: 4.9] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/13/2012] [Accepted: 05/14/2012] [Indexed: 11/22/2022] Open
Abstract
From the first measurements of the distribution of pulmonary blood flow using radioactive tracers by West and colleagues (J Clin Invest 40: 1-12, 1961) allowing gravitational differences in pulmonary blood flow to be described, the imaging of pulmonary blood flow has made considerable progress. The researcher employing modern imaging techniques now has the choice of several techniques, including magnetic resonance imaging (MRI), computerized tomography (CT), positron emission tomography (PET), and single photon emission computed tomography (SPECT). These techniques differ in several important ways: the resolution of the measurement, the type of contrast or tag used to image flow, and the amount of ionizing radiation associated with each measurement. In addition, the techniques vary in what is actually measured, whether it is capillary perfusion such as with PET and SPECT, or larger vessel information in addition to capillary perfusion such as with MRI and CT. Combined, these issues affect quantification and interpretation of data as well as the type of experiments possible using different techniques. The goal of this review is to give an overview of the techniques most commonly in use for physiological experiments along with the issues unique to each technique.
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Affiliation(s)
- Susan R Hopkins
- Departments of Medicine and Radiology, Pulmonary Imaging Laboratory, University of California-San Diego, 9500 Gilman Drive, La Jolla, CA 92093, USA.
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10
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Abstract
Pulmonary magnetic resonance (MR) imaging has been put forward as a new research and diagnostic tool mainly to overcome the limitations of computed tomography and nuclear medicine studies. However, pulmonary MR imaging has been difficult to use because of inherently low proton density, a multitude of air-tissue interfaces, which create significant magnetic field distortions and are commonly referred to as susceptibility artifacts; diminishing signal in the lung; and respiratory and/or cardiac motion artifacts. To overcome these drawbacks of pulmonary MR imaging, technical advances made during the last decade in sequencing, scanner and coil, adaptation of parallel imaging techniques, and utilization of contrast media have been reported as being useful for functional and morphologic assessment of various pulmonary diseases including airway diseases. This review article covers (1) pulmonary MR techniques for morphologic and functional assessment of airway diseases, and (2) pulmonary MR imaging for cystic fibrosis, asthma, and chronic obstructive pulmonary disease. Pulmonary MR imaging provides not only morphology-related but also pulmonary function-related information. It has the potential to replace nuclear medicine studies for the identification of regional pulmonary function and may perform a complementary role in airway disease assessment instead of nuclear medicine study. We believe that the findings of further basic studies as well as clinical applications of this new technique will validate the real significance of pulmonary MR imaging for the future of airway disease assessment and its usefulness for diagnostic radiology and pulmonary medicine.
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11
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Henzler T, Schmid-Bindert G, Schoenberg SO, Fink C. Diffusion and perfusion MRI of the lung and mediastinum. Eur J Radiol 2011; 76:329-36. [PMID: 20627435 DOI: 10.1016/j.ejrad.2010.05.005] [Citation(s) in RCA: 62] [Impact Index Per Article: 4.4] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/05/2010] [Accepted: 05/05/2010] [Indexed: 11/29/2022]
Abstract
With ongoing technical improvements such as multichannel MRI, systems with powerful gradients as well as the development of innovative pulse sequence techniques implementing parallel imaging, MRI has now entered the stage of a radiation-free alternative to computed tomography (CT) for chest imaging in clinical practice. Whereas in the past MRI of the lung was focused on morphological aspects, current MRI techniques also enable functional imaging of the lung allowing for a comprehensive assessment of lung disease in a single MRI exam. Perfusion imaging can be used for the visualization of regional pulmonary perfusion in patients with different lung diseases such as lung cancer, chronic obstructive lung disease, pulmonary embolism or for the prediction of postoperative lung function in lung cancer patients. Over the past years diffusion-weighted MR imaging (DW-MRI) of the thorax has become feasible with a significant reduction of the acquisition time, thus minimizing artifacts from respiratory and cardiac motion. In chest imaging, DW-MRI has been mainly suggested for the characterization of lung cancer, lymph nodes and pulmonary metastases. In this review article recent MR perfusion and diffusion techniques of the lung and mediastinum as well as their clinical applications are reviewed.
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Affiliation(s)
- Thomas Henzler
- Institute of Clinical Radiology and Nuclear Medicine, University Medical Center Mannheim, Medical Faculty Mannheim - Heidelberg University, Germany.
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Ley-Zaporozhan J, van Beek EJ. Imaging phenotypes of chronic obstructive pulmonary disease. J Magn Reson Imaging 2010; 32:1340-52. [DOI: 10.1002/jmri.22376] [Citation(s) in RCA: 19] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/17/2022] Open
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Ley-Zaporozhan J, Puderbach M, Kauczor HU. MR for the evaluation of obstructive pulmonary disease. Magn Reson Imaging Clin N Am 2008; 16:291-308, ix. [PMID: 18474333 DOI: 10.1016/j.mric.2008.02.014] [Citation(s) in RCA: 22] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/25/2022]
Abstract
Obstructive lung diseases include emphysema, chronic bronchitis, chronic obstructive pulmonary disease, asthma, and cystic fibrosis. These diseases are a heterogeneous group of pulmonary disorders that share in common obstruction of air flow and deranged gas exchange. Traditionally these diseases are evaluated with clinical testing, such as pulmonary function tests, but such tests provide only global measures of respiratory function. MR techniques designed for obstructive lung disease have the capability of directly imaging the anatomic and pathophysiologic derangements and may prove useful for monitoring response to therapy.
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Affiliation(s)
- Julia Ley-Zaporozhan
- Department of Pediatric Radiology, University Hospital Heidelberg, Im Neuenheimer Feld 153, 69120 Heidelberg, Germany.
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14
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Abstract
Lung diseases of children often need diagnostic imaging beyond X-ray. Although CT is considered the gold standard of lung imaging, MRI is sufficient to answer most of the questions raised. After all, the exposure to radiation caused by one CT examination corresponds to approximately the effective dose of 200 chest radiographs. What is MRI's potential in the lung today? In diseases with alveolar pathology, cardiac- and respiratory-triggered MRI examinations are roughly equivalent to CT examinations. Distinct interstitial processes are easily diagnosable using MRI. Early interstitial processes may be missed by MRI, but conventional plain films fail to recognize them just as often. For identification of lung metastases, CT is still used as the initial diagnostic measure. Subsequent therapy monitoring may then be carried out with the help of MRI. Small bullae and pulmonary emphysema at present pose a problem to MRI. On the other hand, MRI is reliable for follow-up examinations in inflammatory diseases or for imaging of complications, and the increased use of lung MRI as an alternative to chest CT may contribute immensely to reducing radiation exposure in children.
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Ley-Zaporozhan J, Ley S, Kauczor HU. Morphological and functional imaging in COPD with CT and MRI: present and future. Eur Radiol 2007; 18:510-21. [PMID: 17899100 DOI: 10.1007/s00330-007-0772-1] [Citation(s) in RCA: 68] [Impact Index Per Article: 3.8] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/08/2007] [Revised: 08/26/2007] [Accepted: 08/31/2007] [Indexed: 11/26/2022]
Abstract
Chronic obstructive pulmonary disease (COPD) is one of the leading causes of morbidity and mortality worldwide. COPD is defined by irreversible airflow obstruction. It is a heterogeneous disease affecting the airways (i.e. chronic bronchitis, airway collapse), the parenchyma (i.e. hyperinflation, air trapping and emphysematous destruction) as well as the vasculature (i.e. hypoxic vasoconstriction, rarefication and pulmonary arterial hypertension) with different severity during the course of the disease. These different aspects of COPD can be best addressed by imaging using a combination of morphological and functional techniques. Three-dimensional high-resolution computed tomography (3D-HRCT) is the technique of choice for morphological imaging of the lung parenchyma and airways. This morphological information is to be accomplished by functional information about perfusion, regional lung mechanics, and ventilation mainly provided by MRI. The comprehensive diagnostic possibilities of CT complemented by MRI will allow for a more sensitive detection, phenotype-driven characterization and dedicated therapy monitoring of COPD as presented in this review.
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Affiliation(s)
- Julia Ley-Zaporozhan
- Department of Radiology (E010), German Cancer Research Center, Im Neuenheimer Feld 280, 69120 Heidelberg, Germany.
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Affiliation(s)
- Julia Ley-Zaporozhan
- Department of Radiology, E 010, German Cancer Research Center, Heidelberg, Germany.
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Rabe KF, Beghé B, Luppi F, Fabbri LM. Update in chronic obstructive pulmonary disease 2006. Am J Respir Crit Care Med 2007; 175:1222-32. [PMID: 17545457 DOI: 10.1164/rccm.200704-586up] [Citation(s) in RCA: 67] [Impact Index Per Article: 3.7] [Reference Citation Analysis] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/05/2023] Open
Affiliation(s)
- Klaus F Rabe
- Department of Pulmonology, Leiden University Medical Center, Leiden, The Netherlands
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