Original Research
Cardiopulmonary Imaging
August 2010

Diffusion-Weighted MRI of Malignant Pleural Mesothelioma: Preliminary Assessment of Apparent Diffusion Coefficient in Histologic Subtypes


OBJECTIVE. The purpose of this study was to prospectively assess, in the evaluation of patients with suspected malignant pleural mesothelioma (MPM), apparent diffusion coefficient (ADC) values derived from diffusion-weighted images obtained with a free-breathing single-shot spin-echo echo-planar imaging sequence and to correlate the ADC values with the three histologic subtypes of MPM.
SUBJECTS AND METHODS. Sixty-two patients with a known pleural abnormality and clinical findings suggestive of MPM underwent diffusion-weighted 3-T MRI and ADC calculation. The pathologic diagnosis was confirmed by surgical procedure. ADC values were correlated with the histologic subtypes of MPM. Statistical analysis was performed with analysis of variance and the Student's t test.
RESULTS. Fifty-seven patients had MPM. Forty of the tumors were epithelioid, 11 were biphasic, and six were sarcomatoid. The other five patients had pleural thickening (two patients), metastatic adenocarcinoma (one patient), chronic inflammation (one patient), and malignant lymphoma (one patient). Because of image distortion, the diffusion-weighted images and ADC maps were not satisfactory for assessment in seven cases. The ADC values of MPM were 1.31 ± 0.15 × 10–3 mm2/s for the epithelioid, 1.01 ± 0.11 × 10–3 mm2/s for the biphasic, and 0.99 ± 0.07 × 10–3 mm2/s for the sarcomatoid subtypes of MPM. The ADC of the epithelioid subtype was statistically significantly higher than that of the sarcomatoid subtype (p < 0.05). The ADC in the two cases of benign plaque was 0.85 ± 0.17 × 10–3 mm2/s.
CONCLUSION. The ADC values of epithelioid mesothelioma are higher than those of sarcomatoid mesothelioma. There is no significant difference between the ACD values of biphasic and those of sarcomatoid MPM.


Malignant pleural mesothelioma (MPM) is an uncommon and highly lethal neoplasm originating from the mesothelial cells lining the visceral and parietal pleura. MPM is correlated with asbestos exposure [13]. The incidence is increasing worldwide, and 2,000–3,000 new cases are diagnosed annually in the United States [4, 5]. MPM is generally divided into three histologic subtypes: epithelioid, sarcomatoid, and biphasic. There is a significant difference in prognosis between epithelioid and nonepithelioid (biphasic and sarcomatoid) MPM [6], the epithelioid type having a better prognosis than the other two. Because of this difference, information on histologic subtype is important as a prognostic indicator.
MPM is extremely difficult to manage regardless of the stage, histologic subtype, and treatment options. The median survival period is 9–17 months from the time of diagnosis [7]. Cytoreductive extrapleural pneumonectomy combined with chemotherapy and radiation therapy is the therapy of choice for resectable disease. Unresectable disease can be managed with a combination chemotherapy regimen that includes platinum and antifolate agents [8]. Because of the scarcity of treatment options, it is vital to develop a noninvasive method that can be used both to map the in vivo pathophysiologic characteristics of MPM and to assess the biologic response to therapy.
Several imaging techniques, including CT, MRI, and FDG PET/CT, have been used for staging of MPM and for treatment planning [911]. Diffusion-weighted MRI (DWI) has the potential to reveal tissue characteristics based on the diffusivity of water molecules within the tissues. With this technique, signal loss can be quantitatively assessed with the apparent diffusion coefficient (ADC), which depends on restriction of water molecule diffusion by cell membranes and macromolecules, indirectly providing information about tissue cellularity [12, 13]. DWI has been widely used in the evaluation of CNS disorders, including acute cerebral infarction, intracranial tumors, and demyelinating disease [14], and ADC has been used to characterize glioma [15]. DWI is being used to evaluate multiple intrathoracic and intraabdominal organs [16, 17]. Matoba et al. [18] correlated the ADC with histologic subtypes of lung cancer and tumor cellularity.
To our knowledge, DWI has not been previously used to evaluate MPM, and we have found no published data correlating DWI-derived ADC values with MPM subtypes. The purpose of this study was to perform DWI in the evaluation of MPM by using a free-breathing single-shot spin-echo echo-planar imaging (EPI) sequence to assess ADC and to correlate the values with the three histologic subtypes of MPM.

Subjects and Methods

Sixty-two patients (51 men, 11 women; mean age, 64 years; range, 30–91 years) with known pleural abnormality and suspected MPM were enrolled in this study between June 2008 and January 2009. The institutional review board approved the study, and written informed consent was provided by all subjects.

Anatomic MRI

All MRI was performed with a 3-T whole-body system (Magnetom TIM Trio, Siemens Healthcare) with the manufacturer's body array coil for signal reception and body coil for transmission. All patients were imaged in the supine position. Initial anatomic imaging consisted of coronal and transverse T2-weighted single-shot acquisition (HASTE; TR/TE 1,200/101; section thickness 5.0 mm; interslice gap, 1.5 mm; number of signals averaged, 1; field of view, 400 mm2, matrix size, 320 × 224; integrated parallel acquisition technique [iPAT] factor, 2) and 3D T1-weighted volume-interpolated gradient-echo acquisitions (3.34/1.26; section thickness, 4.0 mm; interslice gap, 0 mm; number of signals averaged, 1; field of view, 400 mm2; matrix size, 320 × 256; iPAT factor, 2) to cover the entire thoracic cavity and diaphragm.
Fig. 1 71-year-old man with epithelioid malignant pleural mesothelioma. A, Transverse HASTE MR image shows tumor along left pleura and major fissure. B, Transverse contrast-enhanced volume-interpolated gradient-echo examination MR image shows slight enhancement of tumor. Arrow indicates invasion into anterior chest wall. C, Diffusion-weighted MR image (b = 750 s/mm2) clearly shows pleural tumor as having higher signal intensity than adjacent skeletal muscle. Arrow indicates invasion into anterior chest wall. D, Apparent diffusion coefficient (ADC) map shows low signal intensity in pleural tumor. ADC value was calculated as 1.187 × 10–3 mm2/s.
Fig. 2 68-year-old woman with biphasic malignant pleural mesothelioma. A, Transverse HASTE image shows pleural tumor along right pleura and major fissure. B, Transverse contrast-enhanced volume-interpolated gradient-echo examination image shows slight enhancement of tumor. C, Diffusion-weighted MR image (b = 750 s/mm2) clearly shows pleural tumor as having higher signal intensity than adjacent skeletal muscle. D, Apparent diffusion coefficient (ADC) map shows low signal intensity in pleural tumor. ADC value was calculated as 0.995 × 10–3 mm2/s.

Diffusion-Weighted Imaging

Axial DW images were acquired with fat suppression and a free-breathing single shot spin-echo EPI sequence (4,000/84; section thickness, 8.0-mm; interslice gap, 1.5 mm; number of signals averaged, 6; field of view, 400 mm; matrix size, 160 × 96; b value, 250, 500, and 750 s/mm2 for three orthogonal diffusion directions) with autocalibrating parallel imaging technique. The generalized autocalibrating partially parallel acquisition (GRAPPA) technique was chosen because accurate coil sensitivity maps are generated in the region of the lung that results in a more robust image reconstruction. The GRAPPA technique also has reduced sensitivity to aliasing artifacts when the imaged field of view is smaller than the object under investigation, an important consideration in thoracic imaging when the patient's arms are placed at the side of the body.
The free-breathing technique was chosen for the following reasons: to allow multiple thin-slice acquisition and signal averaging to improve the signal-to-noise and contrast-to noise ratios on the DW images [19, 20]; to allow the acquisition of multiple b values, which allows more accurate assessment of the ADC [2123]; and to make imaging more suitable for the patients, most of whom had difficulty performing a breath-hold. The receiver bandwidth (1,802 Hz/pixel), range of b values, and TE were selected to minimize susceptibility artifacts inherent in the EPI technique [24].
The DWI sequence consisted of a pair of diffusion gradient pulses applied before and after the 180° radiofrequency pulse. Thus was twice-refocused balanced echo diffusion spin-echo EPI used to reduce eddy currents that usually lead to undesired ghosting on an image [25]. In addition, a frequency-selective radiofrequency pulse was used before the pulse sequence to suppress strong signal from lipids, thus reducing chemical shift artifacts. Diffusion gradients were applied sequentially in three orthogonal axes to generate three sets of axial DW images per b value. The number and range of b values used were chosen to optimize ADC calculation by acquisition of four data points for calculating each ADC value while intravascular water perfusion effects were reduced [2123]. The total time for DWI acquisition was 6.5 minutes.

ADC Calculation

ADC values were calculated with the following equation: ADC = –ln(Si / S0) / bi, where S0 and Si are the echo signal amplitudes with diffusion gradient strength set to 0 and Gi mT/m and bi is the attenuation factor (250–750 s/mm2). The slope of the straight line obtained by plotting –ln(Si / S0) versus bi yields the ADC. Mean diffusivity was calculated as an average of ADCx, ADCy, and ADCz. The validity of the ADC calculation technique was checked by measuring the ADC of water at 25°C and comparing the result with reference data [25].

Quantitative Analysis

The ADC values of MPM were measured by a single blinded observer with 10 years of experience in clinical chest MRI. The mean ADC of the tumor was measured on an ADC map (Figs. 1, 2, 3) in three circular regions of interest (ROIs) that were as large as possible. The average of these three ADC values was calculated. All ROIs were placed in the center of the tumor tissue to avoid artifacts from the tumor–air interface and artifacts from blood flow in the surrounding large vessels. Contrast-enhanced volume-interpolated breath-hold images (Figs. 1, 2, 3) also were used as a reference to avoid inclusion of necrotic areas in the ROI and to evaluate morphologic extension of the entire tumor.

Data and Statistical Analysis

The ADC values obtained were compared with histologic subtypes. The data were analyzed by analysis of variance and Student's t test to compare the ADC values of the epithelioid, biphasic, and sarcomatoid subtypes of MPM. A value of p < 0.05 was considered statistically significant.
Fig. 3 64-year-old man with sarcomatoid malignant pleural mesothelioma. A, Transverse HASTE image shows tumor in left anterior pleura invading left thoracic wall. Moderate amount of left pleural effusion is evident. B, Contrast-enhanced volume-interpolated gradient-echo examination image shows inhomogeneous enhancement of tumor. Arrows indicate enhanced, slightly thickened pleura. C, Diffusion-weighted MR image (b = 750 s/mm2) clearly shows pleural tumors and thickened left pleura as having higher signal intensity than adjacent skeletal muscle. D, Apparent diffusion coefficient (ADC) map shows significantly low signal intensity of pleural tumor. ADC value was calculated as 0.883 × 10–3 mm2/s.
Fig. 4 Plot shows distribution of apparent diffusion coefficient (ADC) values of malignant pleural mesothelioma among three histologic subtypes. Average ADC values were as follows: epithelioid, 1.31 ± 0.15 (SD) × 10–3 mm2/s; biphasic, 1.01 ± 0.11 × 10–3 mm2/s; sarcomatoid, 0.99 ± 0.07 × 10–3 mm2/s.


All 62 patients underwent surgical procedures, and the histologic specimens of the lesions were analyzed for diagnosis. The procedures included extrapleural pneumonectomy (n = 16), pleurectomy (n = 7), pleural biopsy (n = 38), and cytologic examination of pleural effusion obtained with thoracentesis (n = 1).
Five of 62 suspected cases of MPM initially diagnosed clinically and with CT were histologically not MPM. The diagnoses in these cases included two benign pleural plaques, one case of nonspecific chronic inflammation, one metastatic pleural tumor, and one malignant lymphoma. The ADC could not be calculated in seven of the 57 MPM cases because the tumor volume was too small for visualization of the lesions or for reliable measurement of ADC (n = 5; three epithelioid, one biphasic, and one sarcomatoid MPM); the ADC map had severe image degradation (one epithelioid MPM); and the tumor had severe necrosis (one epithelioid MPM). The 50 MPMs with measured ADC values included 35 epithelioid, 10 biphasic, and five sarcomatoid MPMs (Appendix 1).
The average ADC in each histologic subtype of MPM was 1.31 ± 0.15 (SD) × 10–3 mm2/s for epithelioid, 1.01 ± 0.11 × 10–3 mm2/s for biphasic, and 0.99 ± 0.07 × 10–3 mm2/s for sarcomatoid tumors. The distribution of ADC values by histologic subtype is shown in Figure 4. The ADC of the epithelioid subtype was statistically significantly higher than the ADC values of the biphasic and sarcomatoid subtypes (p = 2.48 × 10–4, p = 8.14 × 10–5, respectively). There was minimum overlap in the ADC distribution of epithelioid and sarcomatoid subtypes, but 32 of 35 cases (91%) of epithelioid tumors had higher ADC values than did sarcomatoid tumors (cutoff ADC threshold, 1.1 × 10–3 mm2/s). The sensitivity, specificity, and accuracy for differentiating epithelioid and sarcomatoid MPM on the basis of ADC value at a threshold of 1.1 × 10–3 mm2/s were 60%, 94%, and 84%. The ADC values of biphasic MPM had a wide range of overlap with the ADC values of other subtypes, ranging from 0.9 × 10–3 mm2/s to the highest value's being closer to the mean epithelioid ADC of 1.31 ± 0.15 × 10–3 mm2/s, even though there was a statistically significant difference across the three types (F2,55 = 7.61, p = 0.001, analysis of variance). There was no statistically significant difference between the ADC values of biphasic and sarcomatoid MPM (p = 0.095).
In the two cases of benign plaque, the ADC values were similar to the ADC of adjacent muscle and lower than that of all the histologic MPM subtypes. The average ADC in the two cases of benign plaque was 0.85 ± 0.17 × 10–3 mm2/s.


Differences in water molecule diffusivity within different tissue types can be detected with DWI [22]. High-grade gliomas such as glioblastoma tend to have lower ADC values than do low-grade gliomas such as astrocytoma. High-grade gliomas have higher cellularity and expanded extracellular space with greater tortuosity and a more sophisticated histologic structure than do low-grade gliomas [23, 24]. Such factors restrict water molecule motion and consequently lower the ADC of high-grade gliomas. Similar results have been reported for other tumors, including lung cancer [25].
Sarcomatoid MPM is composed of spindle-shaped cells with relatively high cellularity, and epithelioid MPM is composed of tubular, cuboidal cells. Sarcomatoid MPM often forms a storiform pattern, which can complicate the histologic structure and further restrict water diffusion. In addition, sarcomatoid MPM, with its higher microvascular density, micronecrosis, and cell edema, tends to undergo more aggressive tumor growth than the epithelioid subtype and has a large nucleus-to-cell ratio. These factors can contribute to the much lower ADC of sarcomatoid than of epithelioid MPM.
The ADC values of biphasic MPM had a wide range of overlap with the ADC values of other subtypes. Biphasic MPM consists of a mixture of both epithelioid and sarcomatoid cells with assorted volumes of high cellularity and low cellularity. It therefore is reasonable for this subtype to have moderately high average ADC values overlapping with the values for both epithelioid and sarcomatoid MPM. Furthermore, the ADC values were based on an average of three ROIs within a tumor and therefore depended on the location of the ROIs. The value thus may have varied depending on whether an ROI was located within more epithelioid or more sarcomatoid tissue.
The histologic subtype of MPM is usually determined at pleural cytologic examination, needle biopsy, pleurectomy, or examination of a specimen obtained by video-assisted thoracoscopy. The sensitivity of pleural cytologic evaluation is only 20–33% [26]. Although the diagnostic accuracy of video-assisted thoracoscopy is high (greater than 95%), the procedure is invasive and may lead to seeding of tumors along the surgical incision or chest tube track in as many as 20% of patients [9]. Compared with these methods, DWI is noninvasive and can be complementary to MRI with other sequences routinely used to assess resectability and establish a treatment plan. DWI may have great potential in the noninvasive diagnosis of subtypes of MPM.
In the two cases of benign plaque, in which the ADC values were similar to those of adjacent muscle and were lower than those of all of the MPM subtypes, it may be that the cellular structure in the benign plaque was similar to the structure of normal tissue determined with the ADC values. However, because our cohort of patients had only two cases of benign plaque, statistical analysis was not applicable. It would be beneficial to rule out benign pleural disease by adding ADC information before invasive biopsy is considered. It is necessary to continue to investigate larger patient populations with benign plaques; there may be great potential for differentiating benign plaques from MPM on the basis of ADC.
One of the challenges in applying DWI to the thoracic region is image distortion due to respiratory motion, heart motion, and susceptibility artifacts from air–tumor interfaces. We used the GRAPPA technique [21], in which autocalibration is used to limit susceptibility in the lung, resulting in robust image reconstruction. The DW images and ADC maps obtained were satisfactory for assessment of signal intensity and for ADC measurement. Comparative studies [26, 27] with free-breathing techniques and a larger number of signals acquired, breath-holding technique, and respiratory and cardiac triggering have shown that free-breathing technique is robust not only for obtaining DW images with improved signal-to-noise and contrast-to-noise ratios but also for accurately evaluating ADC, for which more than two b values are acquired [28]. Kwee et al. [29] reported that free-breathing technique has better reproducibility in calculating ADC than does respiratory triggering technique and is as good as breath-holding techniques in imaging of the liver. Studies of DWI of the lung have been performed with cardiac gating, respiratory triggering, and breath-holding techniques [27]. Because many patients in this cohort had marked restrictive physiologic conditions due to the circumferential encasing pattern of the disease and were not capable of performing a breath-hold, we adopted free-breathing spin-echo EPI DWI. It is true, however, that free-breathing technique is subject to error in ADC calculation due to image misregistration. The error can vary with the magnitude of respiratory motion and the size of the lesion. In other words, ADC can become less accurate in patients with severe dyspnea and those with small lesions. Motion-induced error may account in part for the variability of ADC measurement in our results.
Our study had several limitations. First, the location of ROIs on the ADC maps could not be matched with the biopsy locations. Therefore, we averaged three ROIs from carefully selected nonnecrotic regions of the tumor. Especially in the biphasic subtype of MPM, the ADC can vary depending on the location of the ROIs because the tumor cell distribution is known to be inhomogeneous and the ADC value may have not reflected the histologic features. Second, the number of patients with the biphasic subtype was relatively small. Continued investigation of this subtype is necessary.
On the basis of the results of this preliminary study, we conclude that the ADC of the epithelioid subtype of MPM is higher than that of the sarcomatoid subtype, a difference that may serve as a surrogate imaging biomarker.
APPENDIX 1: Histologic Findings and Apparent Diffusion Coefficients
Patient No.SexAge (y)Histologic DiagnosisApparent Diffusion Coefficient (× 10-3 mm2/s)
5M67Pleural plaque0.85
7M73Plaque, no tumor0.87
13M60EpithelioidNot measurable
15M59Chronic inflammation1.07
17M66EpithelialNot measurable
21M43EpithelioidNot measurable
23M61MixedNot measurable
48M46SarcomatoidNot measurable
57M65EpithelioidNot measurable


R. R. Gill and S. Umeoka contributed equally to this study.
Address correspondence to R. R. Gill. ([email protected]).
This is a Web exclusive article.


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Information & Authors


Published In

American Journal of Roentgenology
Pages: W125 - W130
PubMed: 20651171


Submitted: August 24, 2009
Accepted: December 19, 2009


  1. apparent diffusion coefficient
  2. diffusion-weighted imaging
  3. malignant pleural mesothelioma
  4. MRI



Ritu R. Gill
Department of Radiology, Brigham and Women's Hospital, 75 Francis St., Boston, MA 02115.
Shigeaki Umeoka
Department of Radiology, Brigham and Women's Hospital, 75 Francis St., Boston, MA 02115.
Hatsuho Mamata
Department of Radiology, Brigham and Women's Hospital, 75 Francis St., Boston, MA 02115.
Tamara R. Tilleman
Department of Surgery, Brigham and Women's Hospital, Boston, MA.
Peter Stanwell
Department of Radiology, Brigham and Women's Hospital, 75 Francis St., Boston, MA 02115.
Reiko Woodhams
Department of Radiology, Brigham and Women's Hospital, 75 Francis St., Boston, MA 02115.
Robert F. Padera
Department of Pathology, Brigham and Women's Hospital, Boston, MA.
David J. Sugarbaker
Department of Surgery, Brigham and Women's Hospital, Boston, MA.
Hiroto Hatabu
Department of Radiology, Brigham and Women's Hospital, 75 Francis St., Boston, MA 02115.

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