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J Thorac Cardiovasc Surg 2008;135:816-822
© 2008 The American Association for Thoracic Surgery

General Thoracic Surgery

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

^a Department of Thoracic Surgery, Graduate School of Medical Sciences, Kumamoto University, Kumamoto, Japan
^b Department of Diagnostic Radiology, Graduate School of Medical Sciences, Kumamoto University, Kumamoto, Japan
^c Department of Radiology, Kumamoto Central Hospital, Kumamoto, Japan

Received for publication July 9, 2007; revisions received October 23, 2007; accepted for publication October 31, 2007.

^_* Address for reprints: Hiroaki Nomori, MD, PhD, Department of Thoracic Surgery, Graduate School of Medical Sciences, Kumamoto University, 1-1-1 Honjo, Kumamoto 860-8556, Japan. (Email: hnomori{at}qk9.so-net.ne.jp).

	Abstract

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Objective: One of the deficiencies of positron emission tomography for N staging in lung cancer is a false-positive result caused by concurrent lymphadenitis. Recently, diffusion-weighted magnetic resonance imaging has been reported to be able to image tumors of body organs. The aim of this study is to examine the usefulness of diffusion-weighted magnetic resonance imaging for N staging of non–small cell lung cancer compared with positron emission tomography–computed tomography.

Methods: Both positron emission tomography–computed tomography and diffusion-weighted magnetic resonance imaging were prospectively used in 88 patients before surgical intervention for non–small cell lung cancer to examine 734 lymph node stations. The diagnostic results of positron emission tomography–computed tomography and diffusion-weighted magnetic resonance imaging were compared. The diameters of the metastatic foci within lymph nodes were measured on hematoxylin and eosin–stained sections to compare the detectable size of metastatic foci between positron emission tomography–computed tomography and diffusion-weighted magnetic resonance imaging.

Results: The accuracy of N staging in the 88 patients was 0.89 with diffusion-weighted magnetic resonance imaging, which was significantly higher than the value of 0.78 obtained with positron emission tomography–computed tomography (P = .012), because of less overstaging in the former. Among the 734 lymph node stations examined pathologically, 36 had metastases, and the other 698 did not. Although there was no significant difference in the diagnosis of the 36 metastatic lymph node stations between the 2 methods, diffusion-weighted magnetic resonance imaging was more accurate for diagnosing the 698 nonmetastatic stations than positron emission tomography–computed tomography because of fewer false-positive results (P = .002). The detectable size of metastatic foci within lymph nodes was 4 mm in both positron emission tomography–computed tomography and diffusion-weighted magnetic resonance imaging.

Conclusions: Diffusion-weighted magnetic resonance imaging can be used in place of positron emission tomography–computed tomography for N staging of non–small cell lung cancer with fewer false-positive results compared with positron emission tomography–computed tomography.

	Introduction

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Several noninvasive diagnostic procedures are used for preoperative N staging in patients with non–small cell lung cancer (NSCLC), including computed tomography (CT), magnetic resonance imaging (MRI), and positron emission tomography (PET). However, CT is not sufficiently sensitive or specific for diagnosing lymph node metastases because a size of 1 cm or larger is the only criterion used to differentiate benign from malignant lymph nodes. In recent years fluorodeoxyglucose (FDG)–PET has been reported to be able to detect metastatic lymph nodes smaller than 1 cm.^1-4 Several meta-analytic studies have demonstrated PET to be superior to CT for N staging in lung cancer.^5-7 However, one of the deficiencies of PET for N staging is a false-positive result for concurrent lymphadenitis associated with NSCLC.^1,8

Recent advances in MRI gradient technology allow acquisition of diffusion-weighted magnetic resonance imaging (DWI), which provides excellent tissue contrast based on difference in the diffusion of water molecules among tissues and is different from ordinary T1- and T2-weighted images. Because the diffusion of water molecules is restricted by intracellular organelles and macromolecules, any architectural changes in the proportion of extracellular to intracellular water protons will alter the signal intensity of DWI and the apparent diffusion coefficient (ADC).^9-11 Malignant tumors have increased cellularity, larger nuclei with more abundant macromolecular proteins, larger nuclear cytoplasmic ratios, and less extracellular space compared with values in normal tissue. Therefore diffusion of water molecules in malignant tumors is usually restricted compared with that in normal tissue, resulting in a decreased ADC value.^12,13

Although the clinical utility of DWI was initially established in the central neural system, application of this technique to body organs has been considered difficult because DWI is highly sensitive to motion artifacts caused not only by breathing but also by the beats of the heart and aorta.¹⁴ However, the recent development of fast imaging techniques, such as echoplanar imaging and parallel imaging, has improved DWI for use in body organs.^15,16 In addition to these methods, 3-dimensional display of DWI with a reversed gray scale can also produce images similar to PET images.¹² The further recent development in fusion software, which overlays DWI onto ordinary magnetic resonance images, can identify the anatomic location of regions with intense signals on DWI. DWI has been recently reported to be able to show body tumors, including colorectal cancer, prostate cancer, and breast cancer.^13,17,18 Our recent study has also shown that DWI is useful for differentiating between malignant and benign pulmonary nodules as well as PET-CT (data not shown). However, there have been no reports for N staging of malignancies. In this study we evaluated N staging of NSCLC by using DWI compared with PET-CT.

	Materials and Methods

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Eligibility
The study protocol for examining FDG-PET and DWI in patients with suspected NSCLC before undergoing surgical intervention was approved by the Ethics Committee of Kumamoto University Hospital in January 2006. Informed consent was obtained from all patients after discussing the risks and benefits of the study with their surgeons.

Patients
Between February 2006 and May 2007, 93 patients with lung cancer prospectively underwent PET-CT and DWI before pulmonary resection. Of these patients, 88 patients with NSCLC who underwent pulmonary resection and mediastinal lymph node dissection were enrolled in this study. The histologic types of lung cancer were adenocarcinoma in 67 patients, squamous cell carcinoma in 18 patients, and adenosquamous carcinoma in 3 patients ( Table 1). The pathologic N stages were N0 in 71 patients, N1 in 9 patients, and N2 in 8 patients. The lymph node stations were classified according to the lymph node map of Naruke, which is approved by the Japan Lung Cancer Society.¹⁹

The acquisition time for PET in 3-dimensional mode was 3 minutes per table position. CT data were resized from a 512 x 512 matrix to a 128 x 128 matrix to match the PET data to allow image fusion, and a CT transmission map was generated. PET image data were reconstructed iteratively by using the ordered subsets expectation maximization algorithm with segmented attenuation correction (4 iterations, 28 subsets) and the CT data. The 3.75-mm-thick transaxial CT images were reconstructed at 3.27-mm intervals (transaxial) for fusion with the transaxial PET images. The PET, CT, and fused images were available for review in axial, coronal, and sagittal planes by using software (Xeleris; GE Medical Systems) on a computer workstation.

DWI
All magnetic resonance images were obtained with a 1.5-T superconducting system (Gyroscan Intera Achieva Nova Dual; Philips Medical Systems). Conventional magnetic resonance images and DWI were acquired during the same procedure. The conventional magnetic resonance images consisted of a coronal T1-weighted sequence (repetition time [TR] in milliseconds/echocardiographic time [TE] in milliseconds/excitations: 234/4/1), a coronal and axial single-shot spin echocardiographic T2-weighted (800/90/1) sequence, and a coronal and axial short tau inversion recovery (STIR; TR/TE/inversion time, 4600/90/160) sequence. The T1-weighted, T2-weighted, and STIR sequences were acquired at a section thickness of 6 mm with a 1-mm intersection gap, a 128 x 128 – 256 matrix, and a 40- to 45-cm field of view.

DWI was performed for the thorax in the transverse plane by using a spin echocardiographic, echoplanar imaging sequence with the following parameters: TR/TE/flip angle, 5900/60/90; diffusion gradient encoding in 3 orthogonal directions; b value, 1000 s/mm²; field of view, 400 mm; matrix size, 112 x 100; section thickness, 6 mm; section gap, 1 mm; and number of signals acquired, 6. DWI data were evaluated semiquantitatively by using the ADC. The ADC was calculated as follows: , where S is the signal intensity of the region of interest obtained through 3 orthogonally oriented DWIs and b is the gradient b factor with a value of 1000 s/m².

N Staging by Means of PET-CT Scanning
Two radiologists (KK and SS, with 14 and 11 years, respectively, of radioisotope scintigraphy and PET interpretation experience) evaluated the PET-CT data before the operation. N staging by means of PET-CT was determined as follows. The region of interest was placed on the lymph nodes more than 1 cm in the long axis, for which the standard uptake value (SUV) was measured. The contrast ratio (CR) of SUV (SUV-CR) was calculated as the SUV of the lymph nodes divided by the SUV of the cerebellum in each lymph node, as reported previously.¹

N Staging by means of DWI
One radiologist (KK, with 14 years of MRI interpretation experience) evaluated the MRI data before the operation. N staging by means of DWI was determined as follows: the region of interest was placed on the lymph nodes more than 1 cm in the long axis, and the minimum ADC value (ADC-min) was measured.

Determining the Cutoff Values of SUV-CR and ADC-min
A receiver operating characteristic curve was constructed from the SUV-CR and ADC-min data by using SPSS software (SPSS 15.0 J for Windows, SPSS, Inc), and the cutoff values for a diagnosis of metastasis were determined. Lymph nodes with SUV-CR values of greater than the cutoff value were defined as positive by means of PET-CT. Lymph nodes with SUV-CR values of less than the cutoff value or those that could not be detected on PET-CT were defined as negative by means of PET-CT. By using DWI, lymph nodes with ADC-min values of less than the cutoff value were defined as positive by means of DWI. Lymph nodes with ADC-min values of greater than the cutoff value or those that could not be detected on DWI were defined as negative by means of DWI.

Measuring the Size of Metastatic Foci
The long-axis diameters of metastatic foci within lymph nodes were measured on hematoxylin and eosin–stained sections with a microscope to compare the detectable size of metastatic foci between PET-CT and DWI.

Statistical Analysis
True-positive (TP), true-negative (TN), false-positive (FP), and false-negative (FN) results of PET-CT and DWI images for the diagnosis of lymph node metastasis were compared with the results of the pathologic diagnosis. Sensitivity was calculated as , specificity as , and accuracy as . The sensitivity, specificity, and accuracy of PET-CT versus DWI for N staging and diagnosing each lymph node station were compared by using a McNemar test. The size of the metastatic foci was analyzed by using the 2-tailed Student t test. All values in the text and tables are given as means ± standard deviation.

	Results

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DWI identified metastatic lymph nodes, as well as primary tumors, like PET images ( Figure 1). Eighty lymph nodes in the 88 patients that were greater than 1 cm in their longest axis were studied to determine the cutoff values with the receiver operating characteristic curves. The receiver operating characteristic curves for the diagnosis of metastasis in these 80 lymph nodes showed an optimal cutoff value of SUV-CR on PET-CT to be 0.26 and ADC-min on DWI to be 1.6 x 10^–3 mm²/s ( Figures 2 and 3).

View larger version (111K): [in this window] [in a new window]   Figure 1. Diffusion-weighted magnetic resonance imaging with a reversed gray scale in adenocarcinoma of the right lower lobe with hilar lymph node metastases, which shows similar images of positron emission tomography.

View larger version (8K): [in this window] [in a new window]   Figure 2. Receiver operating characteristic curve and standard uptake value–contrast ratio value for diagnosing lymph node metastasis on positron emission tomography–computed tomography shows the optimal cutoff value to be 0.26. Area under the curve, 0.79; 95% confidence interval, 0.69 to 0.89.

View larger version (9K): [in this window] [in a new window]   Figure 3. Receiver operating characteristic curve and apparent diffusion coefficient value for diagnosing lymph node metastasis on diffusion-weighted magnetic resonance imaging shows the optimal cutoff value to be 1.6 x 10–3 mm2/s. Area under the curve, 0.82; 95% confidence interval, 0.71 to 0.94.

In the 698 nonmetastatic lymph node stations, results of both PET-CT and DWI were FP in 3 and TN in 678 (Table 5). Although results with 15 nonmetastatic lymph node stations were FP with PET-CT but TN with DWI, 2 were FP with DWI but TN with PET-CT. The specificities of PET-CT and DWI were 0.97 (95% confidence interval, 0.962–0.986) and 0.99 (95% confidence interval, 0.987–0.996), respectively. DWI showed a greater specificity than PET-CT (McNemar test, P = .002). The 18 lymph node stations that had FP results on PET-CT showed histologic findings of nonspecific lymphadenitis (n = 15) or tuberculosis (n = 3), with a mean size on CT of 12 ± 2 mm (range, 10–14 mm). The 5 lymph node stations that had FP results on DWI showed tuberculosis (n = 3) or nontuberculosis (n = 2) granulation, with a mean size on CT of 12 ± 2 mm (range, 10–14 mm). The results of DWI were not FP for the 15 stations with nonspecific lymphadenitis, which were FP with PET-CT.

In the overall 734 lymph node stations, both PET-CT and DWI gave correct diagnoses in 702 stations but incorrect diagnoses in 13 stations (Table 6). Although the diagnosis was correct by means of PET-CT but incorrect by means of DWI in 4 lymph node stations, it was correct by means of DWI but incorrect by means of PET-CT in 15 stations. DWI diagnosed lymph node stations significantly more accurately than PET-CT because of fewer FP results (McNemar test, P = .019).

The sizes of the metastatic foci in the lymph nodes that had FN results on PET-CT ranged from 0.5 to 3 mm, with a mean value of 1.2 ± 0.9 mm, whereas those with TP results ranged from 3 to 13 mm, with a mean value of 9 ± 4 mm ( Figure 4). There was a significant difference in the size of metastatic foci between the FN and TP lymph nodes (P < .001). PET was unable to detect any of the metastatic foci smaller than 4 mm, except for one foci with 3 mm, but detected all those larger than 4 mm.

View larger version (7K): [in this window] [in a new window]   Figure 4. The distribution of sizes of metastatic foci in false-negative and true-positive lymph nodes with positron emission tomography–computed tomography (PET-CT). The difference between them was a P value of less than .001.

View larger version (7K): [in this window] [in a new window]   Figure 5. The distribution of sizes of metastatic foci in false-negative and true-positive lymph nodes with diffusion-weighted imaging (DWI). The difference between them was a P value of less than .001.

	Discussion

Top Abstract Introduction Materials and Methods Results Discussion References

The difference in the ADC value between metastatic and nonmetastatic lymph nodes is considered to be caused by the difference in cellularity and structural features between them. Malignant lymph nodes have increased cellularity, larger nuclei with more abundant macromolecular proteins, nuclear cytoplasmic ratios, and less extracellular space than benign nodes, which reduce diffusion of water molecules on DWI, resulting in decreased ADC values.^12,13 The significant decrease in FP results on DWI might be due to the following reasons: although the nonspecific lymphadenitis increases FDG uptake, this would not change the basic architecture of lymph nodes, resulting in a similar ADC value between lymphadenitis and normal lymph nodes. However, granulation tissue in tuberculosis or nontuberculosis lymph nodes showed FP results on DWI because an architectural change with granulation tissue decreases the diffusion of water molecules on DWI.

Although SUV has frequently been used for evaluation of FDG-PET, it has been reported that several factors can affect the SUV, such as body size,²⁰ blood glucose level,²¹ and time after injection.²² We previously compared the results of SUV-max, SUV-CR with contralateral lung, and SUV-CR with cerebellum for pulmonary nodules and reported that SUV-CR with contralateral lung or cerebellum showed significantly higher sensitivity than SUV-max,²³ a result supported by Obrzut and associates.²⁴

Although the present study showed the cutoff value of ADC-min for diagnosing metastatic lymph nodes to be 1.6 x 10^–3 mm²/s, our recent study for diagnosing malignant pulmonary nodules by means of DWI showed the cutoff value of ADC-min to be 1.1 x 10^–3 mm²/s. The reason why the cutoff value of ADC for diagnosing metastatic lymph nodes was higher than that for diagnosing malignant pulmonary nodules could be due to the fact that the ADC value of lymph nodes might increase with motion artifact by the beats of the heart and great vessels in the hilum and mediastinum, whereas the ADC value of peripheral pulmonary nodules should be little affected by these motion artifacts. The cutoff value of SUV-CR on PET-CT for differentiating metastatic lymph nodes was 0.26 in this study, which was similar to our previous report and others.^1,24

FN results were similar between PET-CT and DWI. Both diagnostic tools had very limited ability to detect lymph nodes with metastatic foci smaller than 4 mm. Considering the spatial resolution of the PET scanner, artifacts resulting from respiratory movements, and image reconstruction, it is difficult to evaluate such small metastatic foci. Even on DWI, STIR sequences were acquired at a section thickness of 6 mm, causing lymph nodes with small metastatic foci to be missed. We previously reported that 32% of metastatic lymph nodes of NSCLC had metastatic foci smaller than 4 mm.¹ Because neither PET-CT nor DWI was able to detect metastatic foci smaller than 4 mm, which were not unusual sizes of metastatic lymph nodes in NSCLC, lymph node dissection cannot be reduced for patients with N0 stage NSCLC diagnosed by means of either PET-CT or DWI.

Our study had the following limitations: (1) because the patients in the present study were referred to surgical intervention, 71 (81%) of 88 patients had N0 disease, which might cause a group-specific bias and a superiority of DWI to PET, and (2) DWI in the present study just examined the thorax and not the whole body, whereas PET-CT showed the whole body. Recently, whole-body DWI has become available. Lichy and colleagues²⁵ compared the tumor detection between whole-body DWI and PET-CT for 19 patients with various kinds of tumors, showing a feasibility of the former for clinical practice. We believe that whole-body DWI will be used routinely for TNM staging of patients with lung cancer in the near future.

MRI has the following advantages over PET: (1) patients do not have to fast before examination; (2) there is no radiation exposure; (3) less time is required for examination (30 minutes for DWI vs 90 minutes for PET-CT); and (4) there is less cost ($100 for DWI vs $700 for PET-CT in Japan). Although PET-CT is still superior to DWI on whole-body imaging, this study showed that that DWI can be used in place of PET-CT for N staging of NSCLC and is associated with significantly fewer FP results compared with PET-CT. In the future, a multicenter study with a larger dataset will be necessary.

	References

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Hiroaki Nomori Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Nomori, H. Articles by Yamashita, Y. Search for Related Content PubMed Articles by Nomori, H. Articles by Yamashita, Y. Related Collections Lung - cancer