27

New Applications of Magnetic Resonance Imaging for Thoracic Oncology Yoshiharu Ohno, MD, PhD1,2 1 Division of Functional and Diagnostic Imaging Research, Department

of Radiology, Kobe University Graduate School of Medicine, Kobe, Hyogo, Japan 2 Advanced Biomedical Imaging Research Center, Kobe University Graduate School of Medicine, Kobe, Hyogo, Japan

Address for correspondence Yoshiharu Ohno, MD, PhD, Division of Functional and Diagnostic Imaging Research, Department of Radiology, Kobe University Graduate School of Medicine, 7-5-2 Kusunoki-cho, Chuo-ku, Kobe, Hyogo, 650-0017, Japan (e-mail: [email protected]; [email protected]; [email protected]).

Abstract

Keywords

► ► ► ► ► ►

lung mediastinum pleura MRI CT oncology

Since the clinical introduction of magnetic resonance imaging (MRI), the chest has been one of its most challenging applications, and since the 1980s many physicists and radiologists have been trying to evaluate images for various lung diseases as well as mediastinal and pleural diseases. However, thoracic MRI could not yield image quality sufficient for a convincing diagnosis within an acceptable examination time, so MRI did not find acceptance as a substitute for computed tomography (CT) and other modalities. Until the 2000, thoracic MRI was generally used only for select, minor clinical indications. Within the past decade, however, technical advances in sequencing, scanners and coils, adaptation of parallel imaging techniques, utilization of contrast media, and development of postprocessing tools have been developed. In addition, pulmonary functional MRI has been extensively researched, and MR is being assessed as a new research and diagnostic tool for pulmonary diseases. State-of-the art thoracic MRI now has the potential as a substitute for traditional imaging techniques and/or to play a complimentary role in patient management. In this review, we focus on these advances in MRI for thoracic oncologic imaging, especially for pulmonary nodule assessment, lung cancer staging, mediastinal tumor diagnosis and malignant mesothelioma evaluation, prediction of postoperative lung function, and prediction or evaluation of therapeutic effectiveness. We also discuss the potential and limitations of these advances for routine clinical practice in comparison with other modalities such as CT, positron emission tomography (PET), PET/CT, or nuclear medicine studies.

Since the clinical introduction of magnetic resonance imaging (MRI), the chest has been one of its most challenging applications, and since the 1980s many physicists and radiologists have been trying to evaluate images for various lung diseases as well as mediastinal and pleural diseases. However, thoracic MRI could not yield image quality sufficient for a convincing diagnosis within an acceptable examination time, so that MRI did not find acceptance as a substitute for computed tomography (CT) and other modalities. Until

Issue Theme Thoracic Imaging; Guest Editor, Martine Remy-Jardin, MD, PhD

2000, thoracic MRI was generally used only for select, minor clinical indications. During the first decade of this century, however, many basic and clinical researches, technical advances in sequencing, scanners and coils, adaptation of parallel imaging techniques, utilization of contrast media, and development of postprocessing tools were developed. In addition, pulmonary functional MRI has been extensively researched, and attempts have been made to reexamine MR as a new research

Copyright © 2014 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA. Tel: +1(212) 584-4662.

DOI http://dx.doi.org/ 10.1055/s-0033-1363449. ISSN 1069-3424.

This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.

Semin Respir Crit Care Med 2014;35:27–40.

New Applications of MRI for Thoracic Oncology

Ohno

and diagnostic tool for various pulmonary diseases. As a result, state-of-the art thoracic MRI now has the potential to be used as a substitute for traditional imaging techniques and/or to play a complimentary role in management of patients with chest diseases. In addition, MRI has been under continuous development in an effort to overcome the limitations of CT and nuclear medicine studies. Moreover, it currently provides not only morphological, but also pulmonary functional, physiological, and pathophysiological information at 1.5 Tesla (T) and will be gradually changed from 1.5 T to 3 T MR systems. In this review, we focus on these recent advances in MRI for thoracic oncologic imaging, especially for pulmonary nodule assessment, lung cancer staging, mediastinal tumor diagnosis and malignant mesothelioma evaluation, prediction of postoperative lung function and prediction or evaluation of therapeutic effectiveness. We will also discuss the potential and limitations of these advances for routine clinical practice in comparison with other modalities, such as, CT, positron emission tomography (PET), PET/CT, or nuclear medicine studies.

Pulmonary Nodule Assessment Although chest X-ray has been a key diagnostic tool for pulmonary disease, CT is still considered the current gold standard for the detection of lung nodules.1–5 However, repeated follow-up CT examinations may be undesirable, especially for young patients, because of radiation exposure. In addition, recent results of national lung cancer screening trials as well as previously reported results of CT-based lung cancer screenings have led to a growing need for better management of pulmonary nodules in routine clinical practice.4 In routine clinical practice, it is important to differentiate malignant from benign nodules and to make as specific and accurate a characterization as possible in the least invasive manner. Although CT is the most widely used examination for pulmonary nodule evaluation, it is still based on morphologic criteria.1–6 In addition, the major drawback of CT is iodinate radiation. To overcome these drawbacks, fluorodeoxyglucose (FDG)-PET and FDG-PET/CT were promoted in the 1990’s as more efficacious than CT.7–10 Furthermore, thoracic MRI using spin echo (SE) or turbo SE sequences shows many pulmonary nodules, including lung cancers, pulmonary metastases, and low-grade malignancies such as carcinoids and lymphomas, with low- or intermediate-signal intensity on T1-weighted imaging (T1WI) and with slightly high intensity on T2-weighted imaging (T2WI). According to previous reports,11–21 T2WI and/or precontrast or postcontrast-enhanced (CE) T1WI are capable of diagnosing bronchoceles, tuberculomas, mucin-containing tumors, hamartomas, and aspergillomas on the basis of their specific MR findings, although benign and malignant nodules could not be differentiated when these MRI modalities were used for other nodules due to significant overlap of relaxation time between benign and malignant nodules or masses.11–21 To overcome this limitation concerning relaxation time assessment, short tau inversion recovery (STIR) turbo SE Seminars in Respiratory and Critical Care Medicine

Vol. 35

No. 1/2014

imaging was introduced in 2008 as a more promising sequence than T2WI and pre- or post-CE T1WI for non-CE MRI for nodule assessment.22 One study of this imaging method demonstrated that the quantitative capability of this modality for differentiating malignant from benign solitary pulmonary nodules (SPNs) was significantly better than that of nonCE T1WI or T2WI, showing sensitivity, specificity, and accuracy of 83.3, 60.6, and 74.5%, respectively.23 Diffusion-weighted imaging (DWI) was also introduced in 2008 as another promising method.22,24,25 Theoretically, DWI, as does the apparent diffusion coefficient (ADC), assesses the diffusivity of water molecules within tissue in terms of cellularity, perfusion, tissue disorganization, extracellular space, and other variables.22 For a maximum b value ranging from 500 second mm2 to 1,000 second mm2, quantitative and/or qualitative sensitivities and specificities of the ADC for differentiation of malignant from benign SPNs were 70.0 to 88.9% for sensitivity and 61.1 to 97.0% for specificity.22,24,25 Moreover, specificity of DWI (97.0%) was significantly higher than that of FDG-PET/CT (79.0%).22 In addition, when the signal intensity ratio between lesion and spinal cord was used instead of the ADC, one study found that sensitivity, specificity, and accuracy of DWI were 83.3, 90.0, and 85.7%, respectively, and that the accuracy of this new parameter was significantly higher than that of the ADC (50.0%).22 These non-CE MR techniques thus make it possible to differentiate malignant from benign SPNs and can be considered at least as efficacious as FDG-PET or PET/CT (►Figs. 1 and 2). Therefore, dynamic CE-MRI warrants consideration as another MR technique which can lead to further improvement of diagnostic performance in routine clinical practice. As a result of advances in MR systems and pulse sequences, there are now several major methods for dynamic MRI of the lung. Many investigators have recommended that dynamic MRI be used for two-dimensional (2D) SE or turbo SE sequences or for various types of 2D or three-dimensional (3D) gradient echo (GRE) sequences and that enhancement patterns within nodules and/or parameters determined from signal intensity time course curves be assessed visually. These curves represent the first transit and/or recirculation and washout of contrast media under breath holding or repeated breath holding during less than 10-minute periods.26–38 This means that there are now various dynamic MR techniques for distinguishing malignant from benign nodules with reported sensitivities ranging from 94 to 100%, specificities from 70 to 96%, and accuracies of more than 94%.18–21,26,39–46 A recent meta-analysis reported that there were no significant differences in diagnostic performance among dynamic CE-CT, dynamic CE-MRI, FDG-PET and single photon emission tomography (SPECT).26 However, dynamic MRI with the 3D GRE sequence and ultrashort TE, which requires less than 30 second breath holding for acquisition of all data, has demonstrated its superior diagnostic performance in a direct and prospective comparison study of dynamic CE-CT and coregistered FDG-PET/CT40,42,46 (►Figs. 1 and 2). It was also found that completion of FDG-PET or PET/CT takes almost 2 hours after injection of FDG. Dynamic MRI may thus be able to play a complementary or substitutional role in the characterization

This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.

28

Ohno

Fig. 1 A 73-year-old female patient with invasive adenocarcinoma. (A) Thin section computed tomography (CT) with lung window setting shows a solid nodule (arrow) with a diameter of 15 mm in the left upper lobe. (B) Black-blood T1-weighted turbo spin echo (SE), (C) T2-weighted turbo SE, (D) short tau inversion recovery (STIR) turbo SE (E) images and a diffusion-weighted image at b ¼ 1,000 second/mm2 show a nodule (arrow) with, respectively, low-, intermediate-, high- and very high signal intensity in the same lobe. (F) Dynamic magnetic resonance imaging with ultrafast gradient-echo technique (L to R, t ¼ 0.0 second, t ¼ 5.5 second, t ¼ 9.9 second, t ¼ 12.1 second, and t ¼ 22.0 second) shows a well-enhanced nodule (arrow) in the left upper lung field. The nodule was well enhanced in the systemic circulation phase (t ¼ 12.1 second and t ¼ 22.0 second) because of a high blood supply. (G) Fluorodeoxyglucose (FDG)–positron emission tomography/CT shows a solid nodule (arrow) with high FDG uptake in the left upper lobe.

of pulmonary SPNs assessed with dynamic CE-CT, FDG-PET, and/or PET/CT.

Lung Cancer Staging The international TNM classification proposed by the International Union against Cancer (UICC) has been widely used in the investigation and treatment of lung cancer as accurate staging is essential for determining the appropriate treatment option for lung cancer patients.47 Currently, CT, FDG-PET, and PET/CT are considered more effective for assessment of tumor extent because of their multiplanar capability, as well as for accurate diagnosis of metastatic lymph nodes because of PET or PET/CT ability to analyze the glucose metabolism of cancer cells in lung cancer patients.27–29,48,49 In contrast to CT, FDG-PET, and PET/CT, it was suggested in 1991 that MRI may also be useful for identifying mediastinal

and chest wall invasions because of its multiplanar capability and, compared with CT, superior contrast resolution of tumor and mediastinum, and/or tumor and chest wall.30 Recent advances in MR systems, the introduction of improved or newly developed pulse sequences and/or the more effective utilization of contrast media is likely to result in further improvement of TNM staging accuracy for lung cancer patients in routine clinical practice. As for T-factor assessment, the Radiologic Diagnostic Oncology Group (RDOG) published as a comparative study of CT and MRI for TNM staging of 170 nonsmall cell lung cancer (NSCLC) patients in 1991. This study used non-CE MRI, especially for MR-based T-factor assessments because the diagnostic performance of non-CE MRI (sensitivity, 56.0%; specificity, 80.0%) showed no significant difference from that of CT (sensitivity, 63.0%; specificity, 84.0%) for differentiating T3–T4 from T1–T2 tumors.30 Although this Seminars in Respiratory and Critical Care Medicine

Vol. 35

No. 1/2014

29

This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.

New Applications of MRI for Thoracic Oncology

New Applications of MRI for Thoracic Oncology

Ohno

Fig. 2 A 78-year-old male patient with organizing pneumonia. (A) Thin section computed tomography (CT) with lung window setting shows a solid nodule (arrow) with a diameter of 15 mm in the right upper lobe. (B) Black-blood T1-weighted turbo spin echo (SE), (C) T2-weighted turbo SE, (D) short tau inversion recovery (STIR) turbo SE images and (E) a diffusion-weighted image at b ¼ 1,000 second/mm 2 show a nodule (arrow) with, respectively, low-, intermediate-, low- and very low signal intensity in the same lobe. (F) Dynamic magnetic resonance imaging with ultrafast gradient-echo technique (L to R, t ¼ 0.0 second, t ¼ 5.5 second, t ¼ 8.8 second, t ¼ 13.2 second, and t ¼ 22.0 second) shows only a slightly enhanced nodule (arrow) in the right upper lung field. The nodule and surrounding area proved to be a perfusion defect or a decrease in perfusion in the lung parenchymal phase (t ¼ 5.5 second and t ¼ 8.8 second) and with only a slight enhancement in the systemic circulation phase (t ¼ 13.2 second and t ¼ 22.0 second) because of a low blood supply. (G) Fluorodeoxyglucose–positron emission tomography (FDG)/CT shows a solid nodule (arrow) with low FDG uptake in the left upper lobe.

study did not use cardiac or respiratory gating techniques for T1WI and T2WI, delineation of tumor invasion of pericardium (T3) or heart (T4) on MRI was superior to that obtained with CT scan when the cardiac-gated T1weighted sequence was used for enhanced avoidance of cardiac motion artifacts. 31 However, the accuracy of minimal mediastinal invasion assessment by both CT scanning and MRI is limited because it depends on visualization of the tumor within the mediastinal fat.32 A few new MR techniques have been added for MR-based T-factor assessment since 1997. Sakai et al used dynamic cine MRI rather than static MRI during breathing for evaluating Seminars in Respiratory and Critical Care Medicine

Vol. 35

No. 1/2014

chest wall invasion in lung cancer patients.33 This study assessed the movement of the tumor along the partial pleura during the respiratory cycle, which is displayed as a cine loop in a manner similar to that used for dynamic expiratory multisection CT.34 In another study, the tumor, which had invaded the chest wall and had become affixed to the chest wall, was seen to move freely along the partial pleura without invading it. In this study, the sensitivity, specificity, and accuracy of dynamic cine MRI for the detection of chest wall invasion were 100, 70, and 76%, respectively, whereas those of conventional CT and MRI were 80, 65, and 68%, respectively.33 Dynamic cine MRI in conjunction with static

This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.

30

MRI can therefore be considered a useful method for chest wall invasion assessment. In the last decade, more advanced MR systems were introduced. These systems feature improved pulse sequences and use contrast media for employing noncardiac- or cardiac-gated CEMR angiography for assessment of cardiovascular or mediastinal invasion.35,36 Ohno et al reported on a series of 50 NSCLC patients with suspected mediastinal and hilar invasion of lung cancer visualized with CE-CT scans, cardiac-gated MRI, and noncardiac- and cardiac-gated CE-MR angiography.36 Sensitivity, specificity, and accuracy of CE MR angiography for detection of mediastinal and hilar invasion in this study ranged from 78 to 90%, 73 to 87%, and 75 to 88%, respectively, values that are higher than those for CE-CT and conventional T1WI.36 CE-MR angiography was thus thought to improve the diagnostic capability of MRI for T-factor assessment in routine clinical practice before the installation of multidetector row CT and the use of thin-section multiplanar reformatted (MPR) imaging for equal to or more accurate T-factor evaluation in routine clinical practice. Further investigations as well as comparative studies of thin-section MPR imaging and previously established or newly developed MRI techniques thus seem to be warranted to determine the actual significance of MRI for T-factor in routine clinical practice. As for N-factor assessment, it is thought that diagnostic criteria for MRI for differentiation of metastatic from nonmetastatic lymph nodes depend on lymph node size and are similar to CT criteria. RDOG reports therefore claimed that the direct multiplanar capability of MRI should thus be considered the only advantage for the detection of lymph nodes in areas that are suboptimally imaged in the axial plane, such as in the aortopulmonary window and subcarinal regions, although the diagnostic performance of MRI was not significantly better than that of CT.30,37 To improve the diagnostic performance of MR-based Nfactor assessment, studies published since 2002 have examined the clinical utility of cardiac- and/or respiratory-triggered conventional or black-blood STIR turbo SE imaging and have demonstrated its superiority over that of CE-CT, FDGPET or PET/CT, and other MR sequences.38,50–54 These studies reported that this novel sequence may make it possible for the signal intensity of lymph nodes to be quantitatively assessed by means of comparison with a 0.9% normal saline phantom or muscle, and also to visually differentiate metastatic from nonmetastatic lymph nodes with a diagnostic performance superior to that of other modalities.38,50–54 The STIR turbo SE is a simple sequence, which can be easily incorporated into clinical protocols to yield T1- and T2-relaxation times. On STIR turbo SE images, metastatic lymph nodes are shown as high-signal intensity and nonmetastatic lymph nodes as lowsignal intensity (►Figs. 3 and 4). Several other studies have reported that sensitivity of quantitatively and qualitatively assessed STIR turbo SE imaging ranged, on a per patient basis, from 83.7 to 100.0%, specificity from 75.0 to 93.1%, and accuracy from 86.0 to 92.2%, and these values are equal to or higher than those for CE-CT, FDG-PET, or PET/CT.38,50–54 Yet, another study showed that the quantitative and qualitative sensitivity, specificity, and accuracy of STIR turbo SE imaging were not significantly different from those of FDG-

Ohno

31

This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.

New Applications of MRI for Thoracic Oncology

Fig. 3 A 78-year-old male patient diagnosed with N2 disease from invasive adenocarcinoma. (A) Contrast-enhanced computed tomography (CT) shows primary lesion and lower paratracheal lymph nodes with short diameters of less than 10 mm, which led to a diagnosis of N0 disease. This case was shown as false-negative on contrast-enhanced CT. (B) The black-blood short tau inversion recovery (STIR) turbo spin echo (SE) image shows the same lymph nodes with high signal intensities as well as the primary lesion. The STIR turbo SE findings resulted in a diagnosis of N2 disease. This case was shown as truepositive on the STIR turbo SE image. In addition, multiple lung metastases were also displayed with high-signal intensities. (C) The diffusion-weighted image shows the lymph nodes with intermediate- or high-signal intensities compared with the signal intensity of the primary lesion. Diffusion-weighted magnetic resonance findings resulted in a diagnosis of N2 disease. This case was shown as true-positive on the diffusion-weighted image. (D) Fluorodeoxyglucose–positron emission tomography (FDG-PET)/CT shows these lymph nodes with low uptakes of FDG and yielded a diagnosis of N0 disease. This case was shown as false-negative on FDG-PET/CT.

Seminars in Respiratory and Critical Care Medicine

Vol. 35

No. 1/2014

New Applications of MRI for Thoracic Oncology

Ohno

Fig. 4 A 68-year-old female patient with N1 disease from invasive adenocarcinoma. (A) Contrast-enhanced computed tomography (CT) shows right hilar and subcarina lymph nodes with short diameters of less than 10 mm, which led to a diagnosis of N0 disease. This case was shown as false-negative on contrast-enhanced CT. (B) The black-blood short tau inversion recovery (STIR) turbo spin echo (SE) image displays the right hilar lymph node with high signal intensity, and the carina lymph node with low-signal intensity. STIR turbo SE findings resulted in a diagnosis of N1 disease. This case was shown as true-positive on the STIR turbo SE image. (C) The diffusion-weighted image shows the right hilar lymph node with low-signal intensity, and the carina lymph node with high-signal intensity. Diffusion-weighted magnetic resonance findings resulted in a diagnosis of N2 disease. This case was shown as false-positive on the diffusion-weighted image. (D) Fluorodeoxyglucose–positron emission tomography (FDG-PET)/CT shows these lymph nodes with low uptakes of FDG and yielded a diagnosis of N0 disease. This case was shown as false-negative on FDG-PET/CT. Seminars in Respiratory and Critical Care Medicine

Vol. 35

No. 1/2014

PET/CT. However, FDG-PET/CT in combination with qualitative STIR MRI analysis was found to be significantly more effective for detecting nodal involvement on a per patient basis (96.9% specificity, 90.3% accuracy) than was FDG PET/CT alone (65.6% specificity, 81.7% accuracy). STIR turbo SE imaging can therefore be expected to perform a complementary function to that of FDG-PET/CT for diagnostic N staging for NSCLC patients.53 Diffusion-weighted MRI (DWI) was introduced as another promising MR technique for this purpose in 2008.54–57 Sensitivity, specificity, and accuracy of quantitatively and qualitatively assessed DWI reportedly range between 77.4 and 80.0%, 84.4 and 97.0%, or 89.0 and 95.0%, respectively, on a per patient basis, results which appear to be equal to or better than those for FDG-PET or PET/CT (►Figs. 3 and 4).54–57 Ohno et al prospectively and directly compared these modalities to determine the clinical relevance of MR-based N factor assessment for this purpose as compared with that of FDG-PET/CT. Using feasible threshold values for the quantitative and qualitative assessment of each method, this study found that sensitivity and/or accuracy of STIR turbo SE imaging (quantitative sensitivity, 74.2%; qualitative sensitivity, 71.0%; and quantitative accuracy, 84.4%) proved to be significantly higher than those of DWI (74.2, 71.0, and 84.4%, respectively) and FDG-PET/CT (quantitative sensitivity, 74.2% and qualitative sensitivity, 69.9%).54 This means that quantitative and qualitative assessments of the N stage disease of NSCLC patients obtained with STIR turbo SE MRI are more sensitive and/or more accurate than those obtained with DWI and FDG PET/CT.54 According to these results and considering the limitations of DWI as well as FDG-PET/CT for detection of small metastatic foci or lymph nodes, STIR turbo SE imaging may be the better MR technique to use for this purpose before surgical treatment or lymph node sampling, during thoracotomy or mediastinoscopy for accurate pathologic TNM staging after surgical treatment, or before chemotherapy, radiation therapy, or both.54 However, further technical improvements in DWI are needed to overcome its current limitations and enable it to function in a complementary role or as a substitution for STIR turbo SE imaging in routine clinical practice. In terms of M factor assessment of lung cancer patients, metastasis detection has major implications for management and prognosis. According to previous reports,58,59 extrathoracic metastases are detected at presentation in approximately 40% of the patients with newly diagnosed lung cancer. Therefore, an accurate diagnosis of such metastases may help clinicians provide the most appropriate treatment and/or management for lung cancer patients. Depending on the metastatic site, chest radiography, CE-CT, non-CE, and CEMRI, and bone scintigraphy have all been recommended as surveillance modalities in preoperative guidelines.60–62 Moreover, although FDG-PET or PET/CT are not suitable for the detection of brain metastases, it has been suggested that whole-body FDG-PET or PET/CT is a more powerful tool for assessment of extrathoracic metastases in suspected nonNSCLC patients than conventional work ups comprising CT, MRI, and bone scintigraphy.27–29,48,49

This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.

32

Ohno

Fig. 5 A 73-year-old male patient with lung, mediastinal lymph node, liver, right adrenal gland, and multiple bone metastases from invasive adenocarcinoma. (A) Whole body short tau inversion recovery (STIR) turbo spin echo (SE), (B) diffusion-weighted, (C) contrast-enhanced T1-high resolution isotropic volume excitation images and (D) fluorodeoxyglucose–positron emission tomography (FDG-PET)/CT clearly demonstrate lung (white arrow heads), mediastinal lymph node (small white arrows), liver (yellow arrows), right adrenal gland (red arrow) and multiple bone (large white arrows) metastases. Nonenhanced and contrast-enhanced whole body magnetic resonance imaging with and without diffusionweighted imaging as well as FDG-PET/CT could depict all metastatic sites and these findings led to a diagnosis of stage IV.

Since 2007, whole-body MRI has become clinically feasible after installation of fast imaging and moving table equipment, and is now seen as a single, cost-effective imaging test using 1.5 T and 3 T systems for patients with not only lung cancer, but also other malignancies.52,63–72 Furthermore, wholebody DWI has been recommended as a promising new tool for whole-body MR examination of oncologic patients.70–72 A comparison of the efficacy of whole-body MRI for M factor assessment with that of FDG-PET or PET/CT showed that the diagnostic capability of whole-body MRI with or without DWI (sensitivity, 52.0–80.0%; specificity, 74.3–94.0%; accuracy, 80.0–87.7%) was equal to or significantly higher than that of FDG-PET or PET/CT (sensitivity, 48.0–80.0%; specificity, 74.3–96%; accuracy, 73.3–88.2%).52,70–72 However, the following drawbacks of the use of whole-body DWI for wholebody MR examination in this setting should be carefully considered. When only whole-body DWI was used, specificity (87.7%), and accuracy (84.3%) of DWI on a per patient basis were significantly lower than those of FDG-PET/CT (specificity, 94.5%; accuracy, 90.4%).70 In addition, the diagnostic accuracy of whole-body MRI combined with DWI (87.8%) was not significantly different from that of FDG-PET/CT (►Fig. 5), while that of whole-body MRI without DWI (85.8%) was significantly lower than that of FDG-PET/CT.70 This indicates that the accuracy of whole-body MRI combined with DW imaging for M stage assessment of patients with NSCLC is as good as that of FDG-PET/CT (►Fig. 5). Moreover, the use of whole-body DWI as part of whole-body MR examination would be advisable to improve the diagnostic accuracy of M factor assessment of NSCLC patients.70

Mediastinal Tumor Assessment For detection and diagnosis of mediastinal tumors, CT is the most widely used modality. However, MRI provides important findings diagnosis of disease and facilitates more accu-

rate assessment of location, extension patterns of the diseases and their anatomical relationship with adjacent structures. For obtaining thoracic MR images, including those of mediastinal tumors, a major problem is the presence of motion artifacts, while the use of electrocardiogram (ECG) and respiratory triggering or breath-holding techniques is essential. Currently, ECG-triggered, non-CE-T1WI and CE-T1WI, and ECG-triggered T2WI, obtained by means of turbo SE imaging with and without half-Fourier acquisition, provide sufficient image quality for the assessment of tumor extension within mediastinum, lung, chest wall and thorax, tumor infiltration into the pericardium and large vessels and MR findings used for differentiation of various types of mediastinal tumors such as thymic epithelial tumor, mediastinal malignant lymphoma, germ cell tumor, teratoma, cystic tumor including bronchogenic cyst, thymic and pericardial cysts, neurogenic tumor, etc. as previously reported.73 Recent technical advances in MRI for mediastinal tumors thus seem to have addressed the problematic factors which could not be solved by non-CE-T1WI and T2WI, nor by CE-T1WI obtained by ECGand respiratory-triggered SE and/or turbo SE imaging or ECGtriggered turbo SE imaging with breath holding. Chemical shift MRI was first put forward in 2003 as useful for differentiation of thymic hyperplasia from other thymic tumors. This MR technique can depict intravoxel fat and water within the tissue and has been frequently used for adrenal glands and liver. In overall chemical shift, MRI has been able to depict physiological fatty replacement of the normal thymus in nearly 50% of the subjects aged 11 to 15 years, and in nearly 100% of those over 15 years.74 True thymic hyperplasia is defined as an increase in the size of thymus with normal gross and histological appearance and commonly occurs as a rebound phenomenon secondary to atrophy caused by chemotherapy.75 On CT and MRI, thymic hyperplasia appears as an enlargement of the thymus, and its attenuation seen on CT and signal intensity on MRI are similar to those of normal Seminars in Respiratory and Critical Care Medicine

Vol. 35

No. 1/2014

33

This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.

New Applications of MRI for Thoracic Oncology

New Applications of MRI for Thoracic Oncology

Ohno

thymus.73 In patients more than 15 years old with an enlarged thymus, chemical shift MRI can diagnose thymic hyperplasia by detecting fatty infiltration within the thymus and it has been suggested that this is useful for differentiation of thymic hyperplasia from other neoplastic processes.76,77 Inaoka et al further demonstrated that chemical shift MRI could differentiate thymic hyperplasia (n ¼ 23) from thymic neoplasms (n ¼ 18) in all the patients. All patients with hyperplastic

thymus showed an apparent decrease in the signal intensity of the thymus on opposed-phase images, in contrast to the signal intensity on in-phase images, whereas none of the patients with thymic tumors showed a reduction in signal intensity on opposed-phase images (►Figs. 6 and 7).77 We therefore recommend the addition of chemical shift MRI as part of thoracic MRI for the detection and diagnosis of mediastinal tumors in routine clinical practice.

Fig. 6 A 45-year-old female patient with thymic hyperplasia. Contrastenhanced computed tomography (A) shows a soft tissue density mass (arrow) in the anterior mediastinum. (B) In-phase and (C) opposedphase T1-weighted gradient echo images display an anterior mediastinal mass (arrows), which shows an apparent decrease in the signal intensity of the mass. This finding suggests that this mass is a thymic hyperplasia rather than another type of thymic neoplasm.

Fig. 7 A 59-year-old male with invasive thymoma (thymoma WHO type B). (A) Contrast-enhanced computed tomography shows an anterior mediastinal mass (arrow) with an irregular border. (B) In-phase and (C) opposed-phase T1-weighted gradient echo images display an anterior mediastinal mass (arrows) without evidence of a decrease in signal intensity. This finding suggests that this mass is a thymoma rather than a thymic hyperplasia.

This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.

34

Seminars in Respiratory and Critical Care Medicine

Vol. 35

No. 1/2014

Malignant Mesothelioma Evaluation Pleural malignancy is usually first suspected on the basis of clinical history and chest radiography findings, with further assessment by CT or MRI, and by PET-CT if necessary. Currently, CT is usually the preferred initial investigative stage for pleural disease. As with thoracic MRI in general, the main causes of artifacts in pleural MRI are also respiratory and cardiac motion, so that the choice of pulse sequences for pleural MRI is similar to that for other thoracic MRI applications. Multiplanar ECG-triggered T1WI, T2WI, and CE-T1WI with respiratory-triggering or breath-holding techniques are basic sequences for this purpose.78 In addition, STIR turbo SE imaging may be used to look for bone involvement in malignant pleural disease as well as for easier evaluation of pleural tumor extension.78 Although MRI is not usually the first-line investigative stage for imaging of suspected pleural malignancy, it may be useful for difficult cases or for patients with a contraindication to iodinated contrast media. Falaschi et al79 compared the diagnostic accuracy of MR and CT for patients with pleural disease (18 malignant and 16 benign), and found that CT and MR were equally effective in terms of assessment of morphological features. They also found that high signal intensity on proton-density weighted imaging (PDWI) and T2WI was helpful for distinguishing malignant from benign disease (sensitivity 100%, specificity 87%) and that the ratios of lesion to muscle signal intensity on T1WI, T2WI, PDWI, and CE-T1WI showed significant differences between malignant and benign disease. Although malignant pleural tumors have various causes, malignant pleural mesothelioma (MPM) is one of the more aggressive malignant neoplasms, and its major histologic subtypes are epithelial, sarcomatoid, and biphasic, while osteosarcomatous degeneration in MPM is considered a rare subtype. The majority of MPM cases are associated with asbestos exposure so that, although MPM was once uncommon, its incidence is increasing worldwide as a result of widespread exposure to asbestos.80,81 MRI has proven to be superior to CT for the differentiation of malignant from benign pleural disease.78–83 High-signal intensity in relation to adjacent musculature on T2WI and/ or significant contrast enhancement on T1WI is suggestive of malignant disease, and as MRI allows for the use of morphologic features in combination with signal intensity information, it is highly sensitive and specific for the detection of pleural malignancy. 78–83 In addition, fat-suppressed CE-T1WI sequences constitute the most sensitive technique for detecting enhancement of interlobar fissures and tumor invasion of adjacent structures.84 Patz et al made a comparative evaluation of MRI and CT for predicting resectability. The sensitivity of both modalities was high for evaluating the resectability of MPM in the diaphragm and chest wall (94 and 93% sensitivity for CT, and 100% and 100% for MRI),85 as they provided similar information in most cases. In difficult cases, however, important complementary anatomical information could be obtained only from MRI. Heelan et al also found MRI superior to CT for

Ohno

identifying invasion of the diaphragm (55% accuracy for CT vs. 82% for MRI) and endothoracic fascia or solitary resectable foci of chest wall invasion (46% accuracy for CT vs. 69% for MRI) in 95 patients with MPM.84 Currently, the prognoses for epithelioid and nonepithelioid (biphasic and sarcomatoid) MPM are significantly different.86 In 2010, Gill et al reported that the ADC values of MPM were 1.31  0.15  103 mm2/s for the epithelioid, 1.01  0.1103 mm2/s for the biphasic, and 0.99  0.07  103 mm2/s for the sarcomatoid subtypes of MPM, and that the ADC of the epithelioid subtype was statistically significantly higher than that of the sarcomatoid subtype.87 These findings indicate that DWI can be considered to have potential for MPM evaluation, especially for subtype assessment (►Fig. 8).87

Prediction of Postoperative Lung Function for Nonsmall Cell Lung Cancer Primary lung cancer, especially among the elderly and heavy smokers, is frequently associated with some degree of chronic obstructive pulmonary disease.88–92 In such lung cancer patients with compromised lung function, surgical resection of lung cancer is associated with high rates of morbidity and mortality. It is therefore of the utmost importance to evaluate lung function accurately to determine resectability and predict postoperative lung function.88–92 The standard lung function tests currently performed include spirometry, plethysmography, and carbon monoxide diffusing capacity as well as CT and/or nuclear medicine examinations. In addition, thoracic MRI, especially pulmonary functional MRI for this purpose has also been assessed since 2004. There are two approaches for using MRI for the prediction of postoperative lung function: 3D CE-perfusion MRI93–96 and oxygen (O2)-enhanced MRI.97 When compared with quantitatively and/ or qualitatively assessed thin-section CT, perfusion scan, perfusion SPECT, and/or perfusion SPECT combined with CT (SPECT/CT), the predictive capability of quantitatively assessed 3D CE-perfusion MRI is better than that of qualitatively assessed thinsection CT, perfusion scan, perfusion SPECT and almost similar to that of quantitatively assessed thin-section CT and perfusion SPECT/CT.94–96 In addition, the limits of agreement between actual and predicted postoperative lung function when using 3D CE-perfusion MRI is reportedly less than 10% and therefore small enough for clinical purposes.94–96 This technique can thus utilize the same data set as employed for dynamic CE-MRI with an ultrashort echo time (TE), which can also be used as dynamic MRI for pulmonary nodule assessment, is not time consuming in routine clinical practice, and thus may replace perfusion scan, SPECT and SPECT/CT in routine clinical practice. In contrast to the numerous data for 3D CE-perfusion MRI, only one report has presented the findings of a comparative study of the predictive capability for postoperative lung function of O2-enhanced MRI, quantitative and qualitative thin-section CT, and perfusion scan.97 This study found that postoperative lung function predicted by O2-enhanced MRI (r ¼ 0.90, p < 0.0001) as well as by quantitatively assessed Seminars in Respiratory and Critical Care Medicine

Vol. 35

No. 1/2014

35

This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.

New Applications of MRI for Thoracic Oncology

New Applications of MRI for Thoracic Oncology

Ohno

Fig. 8 A 63-year-old male with epithelial type malignant mesothelioma. (A) Contrast-enhanced computed tomography shows irregularly thickened pleura in the left hemithorax, and this finding suggests the presence of a malignant mesothelioma. (B) Black blood T1-weighted turbo spin echo (SE), (C)T2-weighted turbo SE, (D) contrast-enhanced T1-weighted SE, (E) short tau inversion recovery (STIR) turbo SE , and (F) diffusionweighted image at b ¼ 1,000 second/mm 2 show a malignant mesothelioma as an irregularly thickened pleura in the left hemithorax with, respectively, low-, intermediate-, slightly enhanced high-, high- and very high signal intensity. In addition, the STIR turbo SE image also displays prevascular and subcarina lymph node metastases with high-signal intensity. (G) Fluorodeoxyglucose (FDG)–positron emission tomography/CT displays the malignant mesothelioma as an irregularly thickened pleura with high FDG uptake in the left hemithorax.

thin-section CT (r ¼ 0.90, p < 0.0001) showed significant positive correlation with actual postoperative lung function, and the correlation coefficients for both techniques were better than those for qualitatively assessed thin-section CT (r ¼ 0.87, p < 0.0001) and perfusion scan (r ¼ 0.88, p < 0.0001). In addition, the limits of agreement for the difference between actual and predicted postoperative lung function when O2-enhanced MRI was used was reportedly less than 10%, almost equal to that for the use of quantitatively assessed thin-section CT, smaller than that for qualitatively assessed thin-section CT and perfusion scan, and small enough for clinical purposes.97 This MR technique is therefore currently regarded as a promising predictive modality to be included in the guidelines for presurgical examination of NSCLC patients.92 Although further investigations using large prospective cohorts are warranted to determine the real significance of both MR techniques for this purpose, pulmonary functional MRI may be regarded as a promising tool for prediction of postoperative lung function that can function as a substitute for CT and nuclear medicine examinations for candidates for lung resection. Seminars in Respiratory and Critical Care Medicine

Vol. 35

No. 1/2014

Prediction and Evaluation of Therapeutic Effects for Nonsmall Cell Lung Cancer The standard evaluation of treatment response in the oncologic field is based on the response evaluation criteria in solid tumors, which evaluate size changes of tumors on CT.98 However, several studies have reported that perfusion CT and FDG-PET are promising tools for monitoring and evaluating early response or predicting prognosis after chemotherapy for oncology patients. As for other malignancies, it has been suggested that dynamic CE-MRI including perfusion MR technique and DWI are effective for treatment response prediction or evaluation for thoracic oncology patients.41,99–104 It has further been suggested that dynamic CE-MRI is effective for assessment of tumor angiogenesis,41 so that it has been speculated that the quantitative and/or semiquantitative parameters provided by this technique can be useful for prediction of prognosis for adenocarcinomas41 and of recurrence after conservative therapy for NSCLC patients,99 as well as for treatment response assessment after antiangiogenic therapy for NSCLC100 and MPM patients.101,102

This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.

36

New Applications of MRI for Thoracic Oncology

4 Aberle DR, Adams AM, Berg CD, et al; National Lung Screening Trial

5

6

7

8

9

10

11

Conclusion In this article, we have reviewed state-of-the-art MR techniques for thoracic oncology. Currently, it has become possible to routinely use advanced MR systems and fast imaging and/or parallel imaging techniques to realize unprecedented contrast with recently developed MR sequences, superior contrast resolution with and without contrast media and quantitative and qualitative analyses of MRI for thoracic oncology. It seems, however, that further development of protocols, more clinical trials and the more widespread use of advanced analysis tools are needed to determine the real significance of thoracic MRI. In addition, previously and currently published results indicate that MRI can perform a complementary role or function as a substitute for CT, FDG-PET or PET/CT, and nuclear medicine examinations, and we expect future study results will validate this use of MRI.

12 13

14

15

16

17

18 19

Acknowledgement This article was partly supported by research grants from The Sagawa Foundation for Promotion of Cancer Research, Grants-in-Aid for Scientific Research from the Japanese Ministry of Education, Culture, Sports, Science and Technology (JSTS.KAKEN; No. 20591442), Philips Healthcare and Toshiba Medical Systems.

References

20

21

22

1 Henschke CI, McCauley DI, Yankelevitz DF, et al. Early Lung Cancer

Action Project: overall design and findings from baseline screening. Lancet 1999;354(9173):99–105 2 Swensen SJ, Jett JR, Hartman TE, et al. CT screening for lung cancer: five-year prospective experience. Radiology 2005;235(1): 259–265 3 Tuddenham WJ. Glossary of terms for thoracic radiology: recommendations of the Nomenclature Committee of the Fleischner Society. AJR Am J Roentgenol 1984;143(3):509–517

37

23

24

Research Team. Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med 2011;365(5):395–409 Church TR; National Lung Screening Trial Executive Committee. Chest radiography as the comparison for spiral CT in the National Lung Screening Trial. Acad Radiol 2003;10(6):713–715 Hansell DM, Bankier AA, MacMahon H, McLoud TC, Müller NL, Remy J. Fleischner Society: glossary of terms for thoracic imaging. Radiology 2008;246(3):697–722 Patz EF Jr, Lowe VJ, Hoffman JM, et al. Focal pulmonary abnormalities: evaluation with F-18 fluorodeoxyglucose PET scanning. Radiology 1993;188(2):487–490 Dewan NA, Gupta NC, Redepenning LS, Phalen JJ, Frick MP. Diagnostic efficacy of PET-FDG imaging in solitary pulmonary nodules. Potential role in evaluation and management. Chest 1993;104(4):997–1002 Croft DR, Trapp J, Kernstine K, et al. FDG-PET imaging and the diagnosis of non-small cell lung cancer in a region of high histoplasmosis prevalence. Lung Cancer 2002;36(3):297–301 Chun EJ, Lee HJ, Kang WJ, et al. Differentiation between malignancy and inflammation in pulmonary ground-glass nodules: The feasibility of integrated (18)F-FDG PET/CT. Lung Cancer 2009;65(2):180–186 Sakai F, Sone S, Maruyama A, et al. Thin-rim enhancement in GdDTPA-enhanced magnetic resonance images of tuberculoma: a new finding of potential differential diagnostic importance. J Thorac Imaging 1992;7(3):64–69 Sakai F, Sone S, Kiyono K, et al. MR of pulmonary hamartoma: pathologic correlation. J Thorac Imaging 1994;9(1):51–55 Fujimoto K, Meno S, Nishimura H, Hayabuchi N, Hayashi A. Aspergilloma within cavitary lung cancer: MR imaging findings. AJR Am J Roentgenol 1994;163(3):565–567 Blum U, Windfuhr M, Buitrago-Tellez C, Sigmund G, Herbst EW, Langer M. Invasive pulmonary aspergillosis. MRI, CT, and plain radiographic findings and their contribution for early diagnosis. Chest 1994;106(4):1156–1161 Chung MH, Lee HG, Kwon SS, Park SH. MR imaging of solitary pulmonary lesion: emphasis on tuberculomas and comparison with tumors. J Magn Reson Imaging 2000;11(6):629–637 Gaeta M, Minutoli F, Ascenti G, et al. MR white lung sign: incidence and significance in pulmonary consolidations. J Comput Assist Tomogr 2001;25(6):890–896 Gaeta M, Vinci S, Minutoli F, et al. CT and MRI findings of mucincontaining tumors and pseudotumors of the thorax: pictorial review. Eur Radiol 2002;12(1):181–189 Ohno Y, Sugimura K, Hatabu H. MR imaging of lung cancer. Eur J Radiol 2002;44(3):172–181 Sieren JC, Ohno Y, Koyama H, Sugimura K, McLennan G. Recent technological and application developments in computed tomography and magnetic resonance imaging for improved pulmonary nodule detection and lung cancer staging. J Magn Reson Imaging 2010;32(6):1353–1369 Kono M, Adachi S, Kusumoto M, Sakai E. Clinical utility of GdDTPA-enhanced magnetic resonance imaging in lung cancer. J Thorac Imaging 1993;8(1):18–26 Kusumoto M, Kono M, Adachi S, et al. Gadopentetate-dimeglumine-enhanced magnetic resonance imaging for lung nodules. Differentiation of lung cancer and tuberculoma. Invest Radiol 1994;29(Suppl 2):S255–S256 Uto T, Takehara Y, Nakamura Y, et al. Higher sensitivity and specificity for diffusion-weighted imaging of malignant lung lesions without apparent diffusion coefficient quantification. Radiology 2009;252(1):247–254 Koyama H, Ohno Y, Kono A, et al. Quantitative and qualitative assessment of non-contrast-enhanced pulmonary MR imaging for management of pulmonary nodules in 161 subjects. Eur Radiol 2008;18(10):2120–2131 Mori T, Nomori H, Ikeda K, et al. Diffusion-weighted magnetic resonance imaging for diagnosing malignant pulmonary nodules/ Seminars in Respiratory and Critical Care Medicine

Vol. 35

No. 1/2014

This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.

In addition to its utility for contrast enhancement evaluation, a few investigators have reported that the ADC is effective for early tumor response evaluation and tumor response prediction. Yabuuchi et al reported finding significant correlation between early change in the ADC and final tumor size reduction rate (r2 ¼ 0.41).103 In addition, they reported that the median progression-free survival for the group with a good increase in the ADC was 12.1 months, and 6.67 months for the group with a stable or reduced ADC, whereas the median overall survival for the two groups was 22.4 and 12.3 months, respectively.103 In addition, Ohno et al reported that the ADC on DWI may have better potential than maximum standard uptake value (SUVmax) on FDG PET/CT for distinguishing NSCLC patients with partial response from those with no change and with disease progression, and those with better prognosis from those with poor prognosis group.104 This means that DWI may also have potential for predicting which oncologic patients will be candidates for conservative therapy.

Ohno

New Applications of MRI for Thoracic Oncology

25

26

27 28 29

30

31 32

33

34

35

36

37

38

39

40

41

42

43

Ohno

masses: comparison with positron emission tomography. J Thorac Oncol 2008;3(4):358–364 Satoh S, Kitazume Y, Ohdama S, Kimula Y, Taura S, Endo Y. Can malignant and benign pulmonary nodules be differentiated with diffusion-weighted MRI? AJR Am J Roentgenol 2008;191(2): 464–470 Cronin P, Dwamena BA, Kelly AM, Carlos RC. Solitary pulmonary nodules: meta-analytic comparison of cross-sectional imaging modalities for diagnosis of malignancy. Radiology 2008;246(3): 772–782 Acker MR, Burrell SC. Utility of 18F-FDG PET in evaluating cancers of lung. J Nucl Med Technol 2005;33(2):69–74, quiz 75–77 Bruzzi JF, Munden RF. PET/CT imaging of lung cancer. J Thorac Imaging 2006;21(2):123–136 Kligerman S, Digumarthy S. Staging of non-small cell lung cancer using integrated PET/CT. AJR Am J Roentgenol 2009;193(5): 1203–1211 Webb WR, Gatsonis C, Zerhouni EA, et al. CT and MR imaging in staging non-small cell bronchogenic carcinoma: report of the Radiologic Diagnostic Oncology Group. Radiology 1991;178(3): 705–713 White CS. MR evaluation of the pericardium and cardiac malignancies. Magn Reson Imaging Clin N Am 1996;4(2):237–251 Wong J, Haramati LB, Rozenshtein A, Yanez M, Austin JH. Nonsmall-cell lung cancer: practice patterns of extrathoracic imaging. Acad Radiol 1999;6(4):211–215 Sakai S, Murayama S, Murakami J, Hashiguchi N, Masuda K. Bronchogenic carcinoma invasion of the chest wall: evaluation with dynamic cine MRI during breathing. J Comput Assist Tomogr 1997;21(4):595–600 Murata K, Takahashi M, Mori M, et al. Chest wall and mediastinal invasion by lung cancer: evaluation with multisection expiratory dynamic CT. Radiology 1994;191(1):251–255 Takahashi K, Furuse M, Hanaoka H, et al. Pulmonary vein and left atrial invasion by lung cancer: assessment by breath-hold gadolinium-enhanced three-dimensional MR angiography. J Comput Assist Tomogr 2000;24(4):557–561 Ohno Y, Adachi S, Motoyama A, et al. Multiphase ECG-triggered 3D contrast-enhanced MR angiography: utility for evaluation of hilar and mediastinal invasion of bronchogenic carcinoma. J Magn Reson Imaging 2001;13(2):215–224 Boiselle PM, Patz EF Jr, Vining DJ, Weissleder R, Shepard JA, McLoud TC. Imaging of mediastinal lymph nodes: CT, MR, and FDG PET. Radiographics 1998;18(5):1061–1069 Takenaka D, Ohno Y, Hatabu H, et al. Differentiation of metastatic versus non-metastatic mediastinal lymph nodes in patients with non-small cell lung cancer using respiratory-triggered short inversion time inversion recovery (STIR) turbo spin-echo MR imaging. Eur J Radiol 2002;44(3):216–224 Gückel C, Schnabel K, Deimling M, Steinbrich W. Solitary pulmonary nodules: MR evaluation of enhancement patterns with contrast-enhanced dynamic snapshot gradient-echo imaging. Radiology 1996;200(3):681–686 Ohno Y, Hatabu H, Takenaka D, Adachi S, Kono M, Sugimura K. Solitary pulmonary nodules: potential role of dynamic MR imaging in management initial experience. Radiology 2002; 224(2):503–511 Fujimoto K, Abe T, Müller NL, et al. Small peripheral pulmonary carcinomas evaluated with dynamic MR imaging: correlation with tumor vascularity and prognosis. Radiology 2003;227(3): 786–793 Ohno Y, Hatabu H, Takenaka D, et al. Dynamic MR imaging: value of differentiating subtypes of peripheral small adenocarcinoma of the lung. Eur J Radiol 2004;52(2):144–150 Schaefer JF, Vollmar J, Schick F, et al. Solitary pulmonary nodules: dynamic contrast-enhanced MR imaging—perfusion differences in malignant and benign lesions. Radiology 2004;232(2): 544–553

Seminars in Respiratory and Critical Care Medicine

Vol. 35

No. 1/2014

44 Schaefer JF, Schneider V, Vollmar J, et al. Solitary pulmonary

45

46

47 48

49 50

51

52

53

54

55

56

57

58

59

60

61

nodules: association between signal characteristics in dynamic contrast enhanced MRI and tumor angiogenesis. Lung Cancer 2006;53(1):39–49 Kono R, Fujimoto K, Terasaki H, et al. Dynamic MRI of solitary pulmonary nodules: comparison of enhancement patterns of malignant and benign small peripheral lung lesions. AJR Am J Roentgenol 2007;188(1):26–36 Ohno Y, Koyama H, Takenaka D, et al. Dynamic MRI, dynamic multidetector-row computed tomography (MDCT), and coregistered 2-[fluorine-18]-fluoro-2-deoxy-D-glucose-positron emission tomography (FDG-PET)/CT: comparative study of capability for management of pulmonary nodules. J Magn Reson Imaging 2008;27(6):1284–1295 Sobin L, Gospodarowicz M, Wittekind C. TNM Classification of Malignant Tumors. 7th ed. New York, NY: Wiley-Liss; 2009 Marom EM, Erasmus JJ, Patz EF. Lung cancer and positron emission tomography with fluorodeoxyglucose. Lung Cancer 2000;28(3):187–202 Vansteenkiste JF. Imaging in lung cancer: positron emission tomography scan. Eur Respir J Suppl 2002;35:49s–60s Ohno Y, Hatabu H, Takenaka D, et al. Metastases in mediastinal and hilar lymph nodes in patients with non-small cell lung cancer: quantitative and qualitative assessment with STIR turbo spin-echo MR imaging. Radiology 2004;231(3):872–879 Ohno Y, Koyama H, Nogami M, et al. STIR turbo SE MR imaging vs. coregistered FDG-PET/CT: quantitative and qualitative assessment of N-stage in non-small-cell lung cancer patients. J Magn Reson Imaging 2007;26(4):1071–1080 Yi CA, Shin KM, Lee KS, et al. Non-small cell lung cancer staging: efficacy comparison of integrated PET/CT versus 3.0-T wholebody MR imaging. Radiology 2008;248(2):632–642 Morikawa M, Demura Y, Ishizaki T, et al. The effectiveness of 18FFDG PET/CT combined with STIR MRI for diagnosing nodal involvement in the thorax. J Nucl Med 2009;50(1):81–87 Ohno Y, Koyama H, Yoshikawa T, et al. N stage disease in patients with non-small cell lung cancer: efficacy of quantitative and qualitative assessment with STIR turbo spin-echo imaging, diffusion-weighted MR imaging, and fluorodeoxyglucose PET/CT. Radiology 2011;261(2):605–615 Nomori H, Mori T, Ikeda K, et al. Diffusion-weighted magnetic resonance imaging can be used in place of positron emission tomography for N staging of non-small cell lung cancer with fewer false-positive results. J Thorac Cardiovasc Surg 2008; 135(4):816–822 Hasegawa I, Boiselle PM, Kuwabara K, Sawafuji M, Sugiura H. Mediastinal lymph nodes in patients with non-small cell lung cancer: preliminary experience with diffusion-weighted MR imaging. J Thorac Imaging 2008;23(3):157–161 Pauls S, Schmidt SA, Juchems MS, et al. Diffusion-weighted MR imaging in comparison to integrated [18F]-FDG PET/CT for Nstaging in patients with lung cancer. Eur J Radiol 2012;81(1): 178–182 Quint LE, Tummala S, Brisson LJ, et al. Distribution of distant metastases from newly diagnosed non-small cell lung cancer. Ann Thorac Surg 1996;62(1):246–250 Pantel K, Izbicki J, Passlick B, et al. Frequency and prognostic significance of isolated tumour cells in bone marrow of patients with non-small-cell lung cancer without overt metastases. Lancet 1996;347(9002):649–653 Silvestri GA, Gould MK, Margolis ML, et al; American College of Chest Physicians. Noninvasive staging of non-small cell lung cancer: ACCP evidenced-based clinical practice guidelines (2nd edition). Chest 2007;132(3 Suppl):S178–S201 Simon GR, Turrisi A; American College of Chest Physicians. Management of small cell lung cancer: ACCP evidence-based clinical practice guidelines (2nd edition). Chest 2007;132(3 Suppl):S324–S339

This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.

38

62 Samson DJ, Seidenfeld J, Simon GR, et al; American College of

63

64

65

66

67

68

69

70

71

72

73

74

75 76

77

78

79

80 81

Chest Physicians. Evidence for management of small cell lung cancer: ACCP evidence-based clinical practice guidelines (2nd edition). Chest 2007;132(3 Suppl):S314–S323 Walker R, Kessar P, Blanchard R, et al. Turbo STIR magnetic resonance imaging as a whole-body screening tool for metastases in patients with breast carcinoma: preliminary clinical experience. J Magn Reson Imaging 2000;11(4):343–350 Antoch G, Vogt FM, Freudenberg LS, et al. Whole-body dualmodality PET/CT and whole-body MRI for tumor staging in oncology. JAMA 2003;290(24):3199–3206 Lauenstein TC, Goehde SC, Herborn CU, et al. Whole-body MR imaging: evaluation of patients for metastases. Radiology 2004; 233(1):139–148 Goehde SC, Hunold P, Vogt FM, et al. Full-body cardiovascular and tumor MRI for early detection of disease: feasibility and initial experience in 298 subjects. AJR Am J Roentgenol 2005;184(2): 598–611 Schmidt GP, Haug AR, Schoenberg SO, Reiser MF. Whole-body MRI and PET-CT in the management of cancer patients. Eur Radiol 2006;16(6):1216–1225 Charles-Edwards EM, deSouza NM. Diffusion-weighted magnetic resonance imaging and its application to cancer. Cancer Imaging 2006;6:135–143 Ohno Y, Koyama H, Nogami M, et al. Whole-body MR imaging vs. FDG-PET: comparison of accuracy of M-stage diagnosis for lung cancer patients. J Magn Reson Imaging 2007;26(3): 498–509 Ohno Y, Koyama H, Onishi Y, et al. Non-small cell lung cancer: whole-body MR examination for M-stage assessment—utility for whole-body diffusion-weighted imaging compared with integrated FDG PET/CT. Radiology 2008;248(2):643–654 Takenaka D, Ohno Y, Matsumoto K, et al. Detection of bone metastases in non-small cell lung cancer patients: comparison of whole-body diffusion-weighted imaging (DWI), whole-body MR imaging without and with DWI, whole-body FDG-PET/CT, and bone scintigraphy. J Magn Reson Imaging 2009;30(2): 298–308 Sommer G, Wiese M, Winter L, et al. Preoperative staging of nonsmall-cell lung cancer: comparison of whole-body diffusionweighted magnetic resonance imaging and 18F-fluorodeoxyglucose-positron emission tomography/computed tomography. Eur Radiol 2012;22(12):2859–2867 Takahashi K, Al-Janabi NJ. Computed tomography and magnetic resonance imaging of mediastinal tumors. J Magn Reson Imaging 2010;32(6):1325–1339 Inaoka T, Takahashi K, Iwata K, et al. Evaluation of normal fatty replacement of the thymus with chemical-shift MR imaging for identification of the normal thymus. J Magn Reson Imaging 2005; 22(3):341–346 Linegar AG, Odell JA, Fennell WM, et al. Massive thymic hyperplasia. Ann Thorac Surg 1993;55(5):1197–1201 Takahashi K, Inaoka T, Murakami N, et al. Characterization of the normal and hyperplastic thymus on chemical-shift MR imaging. AJR Am J Roentgenol 2003;180(5):1265–1269 Inaoka T, Takahashi K, Mineta M, et al. Thymic hyperplasia and thymus gland tumors: differentiation with chemical shift MR imaging. Radiology 2007;243(3):869–876 Yamamuro M, Gerbaudo VH, Gill RR, Jacobson FL, Sugarbaker DJ, Hatabu H. Morphologic and functional imaging of malignant pleural mesothelioma. Eur J Radiol 2007;64(3):356–366 Falaschi F, Battolla L, Mascalchi M, et al. Usefulness of MR signal intensity in distinguishing benign from malignant pleural disease. AJR Am J Roentgenol 1996;166(4):963–968 Robinson BW, Lake RA. Advances in malignant mesothelioma. N Engl J Med 2005;353(15):1591–1603 Curran D, Sahmoud T, Therasse P, van Meerbeeck J, Postmus PE, Giaccone G. Prognostic factors in patients with pleural mesothe-

82 83 84

85

86

87

88

89

90

91

92

93

94

95

96

97

98

99

100

Ohno

lioma: the European Organization for Research and Treatment of Cancer experience. J Clin Oncol 1998;16(1):145–152 Helm EJ, Matin TN, Gleeson FV. Imaging of the pleura. J Magn Reson Imaging 2010;32(6):1275–1286 Hierholzer J, Luo L, Bittner RC, et al. MRI and CT in the differential diagnosis of pleural disease. Chest 2000;118(3):604–609 Heelan RT, Rusch VW, Begg CB, Panicek DM, Caravelli JF, Eisen C. Staging of malignant pleural mesothelioma: comparison of CT and MR imaging. AJR Am J Roentgenol 1999;172(4):1039–1047 Patz EF Jr, Shaffer K, Piwnica-Worms DR, et al. Malignant pleural mesothelioma: value of CT and MR imaging in predicting resectability. AJR Am J Roentgenol 1992;159(5):961–966 Sugarbaker DJ, Flores RM, Jaklitsch MT, et al. Resection margins, extrapleural nodal status, and cell type determine postoperative long-term survival in trimodality therapy of malignant pleural mesothelioma: results in 183 patients. J Thorac Cardiovasc Surg 1999;117(1):54–63, discussion 63–65 Gill RR, Umeoka S, Mamata H, et al. Diffusion-weighted MRI of malignant pleural mesothelioma: preliminary assessment of apparent diffusion coefficient in histologic subtypes. AJR Am J Roentgenol 2010;195(2):W125-30 Pierce RJ, Copland JM, Sharpe K, Barter CE. Preoperative risk evaluation for lung cancer resection: predicted postoperative product as a predictor of surgical mortality. Am J Respir Crit Care Med 1994;150(4):947–955 Bolliger CT, Jordan P, Solèr M, et al. Exercise capacity as a predictor of postoperative complications in lung resection candidates. Am J Respir Crit Care Med 1995;151(5):1472–1480 Wyser C, Stulz P, Solèr M, et al. Prospective evaluation of an algorithm for the functional assessment of lung resection candidates. Am J Respir Crit Care Med 1999;159(5 Pt 1):1450–1456 Mazzone PJ, Arroliga AC. Lung cancer: Preoperative pulmonary evaluation of the lung resection candidate. Am J Med 2005; 118(6):578–583 Colice GL, Shafazand S, Griffin JP, Keenan R, Bolliger CT; American College of Chest Physicians. Physiologic evaluation of the patient with lung cancer being considered for resectional surgery: ACCP evidenced-based clinical practice guidelines (2nd edition). Chest 2007;132(3 Suppl):161S–177S Iwasawa T, Saito K, Ogawa N, Ishiwa N, Kurihara H. Prediction of postoperative pulmonary function using perfusion magnetic resonance imaging of the lung. J Magn Reson Imaging 2002; 15(6):685–692 Ohno Y, Hatabu H, Higashino T, et al. Dynamic perfusion MRI versus perfusion scintigraphy: prediction of postoperative lung function in patients with lung cancer. AJR Am J Roentgenol 2004; 182(1):73–78 Ohno Y, Koyama H, Nogami M, et al. Postoperative lung function in lung cancer patients: comparative analysis of predictive capability of MRI, CT, and SPECT. AJR Am J Roentgenol 2007;189(2): 400–408 Ohno Y, Koyama H, Nogami M, et al. State-of-the-art radiological techniques improve the assessment of postoperative lung function in patients with non-small cell lung cancer. Eur J Radiol 2011; 77(1):97–104 Ohno Y, Hatabu H, Higashino T, et al. Oxygen-enhanced MR imaging: correlation with postsurgical lung function in patients with lung cancer. Radiology 2005;236(2):704–711 Eisenhauer EA, Therasse P, Bogaerts J, et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer 2009;45(2):228–247 Ohno Y, Nogami M, Higashino T, et al. Prognostic value of dynamic MR imaging for non-small-cell lung cancer patients after chemoradiotherapy. J Magn Reson Imaging 2005;21(6):775–783 de Langen AJ, van den Boogaart V, Lubberink M, et al. Monitoring response to antiangiogenic therapy in non-small cell lung cancer using imaging markers derived from PET and dynamic contrastenhanced MRI. J Nucl Med 2011;52(1):48–55 Seminars in Respiratory and Critical Care Medicine

Vol. 35

No. 1/2014

39

This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.

New Applications of MRI for Thoracic Oncology

New Applications of MRI for Thoracic Oncology

Ohno

101 Giesel FL, Bischoff H, von Tengg-Kobligk H, et al. Dynamic

103 Yabuuchi H, Hatakenaka M, Takayama K, et al. Non-small cell lung

contrast-enhanced MRI of malignant pleural mesothelioma: a feasibility study of noninvasive assessment, therapeutic followup, and possible predictor of improved outcome. Chest 2006; 129(6):1570–1576 102 Giesel FL, Choyke PL, Mehndiratta A, et al. Pharmacokinetic analysis of malignant pleural mesothelioma-initial results of tumor microcirculation and its correlation to microvessel density (CD-34). Acad Radiol 2008;15(5):563–570

cancer: detection of early response to chemotherapy by using contrast-enhanced dynamic and diffusion-weighted MR imaging. Radiology 2011;261(2):598–604 104 Ohno Y, Koyama H, Yoshikawa T, et al. Diffusion-weighted MRI versus 18F-FDG PET/CT: performance as predictors of tumor treatment response and patient survival in patients with nonsmall cell lung cancer receiving chemoradiotherapy. AJR Am J Roentgenol 2012;198(1):75–82

This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.

40

Seminars in Respiratory and Critical Care Medicine

Vol. 35

No. 1/2014

Copyright of Seminars in Respiratory & Critical Care Medicine is the property of Thieme Medical Publishing Inc. and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.