|Year : 2017 | Volume
| Issue : 2 | Page : 86-95
Can diffusion-weighted MRI predict the histological grade of urinary bladder carcinoma?
Nadine Barsoum, Mohamed Talaat, Samira Saraya
Department of Radiodiagnosis, Faculty of Medicine, Cairo University, Cairo, Egypt
|Date of Submission||17-Nov-2016|
|Date of Acceptance||23-Dec-2016|
|Date of Web Publication||22-Nov-2017|
126 Mamdouh Salem Street, Nasr City, Cairo, 11765
Source of Support: None, Conflict of Interest: None
The aim of this study was to prospectively evaluate the ability of diffusion-weighted (DW) MRI in determining the T-stage of bladder cancer and to measure the correlation between the apparent diffusion coefficient and the histologic grade.
Patients and methods
Totally, 50 patients with suspected bladder cancer underwent MRI. These patients presented with gross (macroscopic) hematuria or had urinary bladder mass detected on ultrasound and/or computed tomography examinations. Human ethics committee approval for this study was obtained from the institutional review board of the hospital where these cases were treated. Two of 50 patients were excluded from the study because of technical difficulties or failure of data acquisition. All 48 patients underwent transurethral cystoscopic biopsy after imaging. Their MRI were read by two different radiologists who were blinded to the results of each other to minimize the bias.
As regards the detection of urinary bladder carcinoma, DW-MRI showed an overall sensitivity of 100%, specificity of 75%, positive predictive value of 98%, negative predictive value of 100%, and accuracy of 98%. The sensitivity, specificity, and accuracy for differentiating superficial from invasive tumors using T2 images alone and combined use of T2 and diffusion-weighted images (DWIs) were 97, 64, and 88% and 100, 86, and 96%, respectively. The sensitivity, specificity, and accuracy for differentiating superficial from invasive tumors using postcontrast MRI alone and combined use of postcontrast MRI and DW images were 96, 71, and 91% and 100, 100, and 100%, respectively. In addition, we concluded that there is an inverse relationship between the mean apparent diffusion coefficient values and the histological grade of the tumor.
DW-MRI is a safe and confident method in the detection and local staging of urinary bladder carcinoma. In addition, DWIs may predict the histological grade of the tumor. Hence, DWI may be added to routine imaging protocols of urinary bladder tumors.
Keywords: diffusion-weighted imaging, magnetic resonance imaging, urinary bladder carcinoma
|How to cite this article:|
Barsoum N, Talaat M, Saraya S. Can diffusion-weighted MRI predict the histological grade of urinary bladder carcinoma?. Kasr Al Ainy Med J 2017;23:86-95
|How to cite this URL:|
Barsoum N, Talaat M, Saraya S. Can diffusion-weighted MRI predict the histological grade of urinary bladder carcinoma?. Kasr Al Ainy Med J [serial online] 2017 [cited 2018 Apr 24];23:86-95. Available from: http://www.kamj.eg.net/text.asp?2017/23/2/86/219000
| Introduction|| |
Urinary bladder cancer is the second most common malignancy of the genitourinary system. For the radiological evaluation of the urinary bladder and prostate gland, MRI is a valuable imaging modality due to high tissue contrast, multiplanar imaging capabilities, and the possibility of tissue characterization ,.
In recent times, diffusion-weighted imaging (DWI) has emerged as a diagnostic technique in the evaluation of various abdominal lesions. DWI reveals micromolecular diffusion, which is the Brownian motion of the spins in biologic tissues. This technique can delineate pathologic lesions with high tissue contrast against generally suppressed background signal. The apparent diffusion coefficient (ADC) value has been reported to be useful for quantitatively distinguishing malignancy from benign lesions. The cause of a decrease in the ADC values is considered to be due to commonly larger cell diameter and denser cellularity of malignancies compared with normal tissues, which restrict water diffusion .
The utilization of diffusion-weighted (DW) MRI was hindered by the presence of bulky physiologic motions such as respiration, peristalsis, and blood flow . These problems were solved, in 2009, when Takahara et al.  reported a procedure of body DW-MRI under free breathing, which enables longer scan times. This technique gives more, thin-slice images with multiple signal averaging, and provides high-quality multiplanar display .
DWIs provided useful information for evaluating the T-stage of bladder cancer, particularly in differentiating T1 or lower tumors from T2 or higher tumors. The ADC may in part predict the histologic grade of bladder cancer .
DWIs are useful in evaluating the tumor invading the surrounding structures. Moreover, it can be applied to differentiate scars and reactive tissue after the biopsy .
Many studies concluded that DW-MRI is a highly reliable imaging approach for the identification of bladder tumors in patients with gross hematuria as in the study by Abou-El-Ghar et al. .
| Aim|| |
The aim of this study was to prospectively evaluate the ability of DW-MRI in determining the T-stage of bladder cancer and to measure the correlation between the ADC and histologic grade.
| Patients and methods|| |
Between September 2014 and March 2016, 50 consecutive patients with suspected bladder cancer underwent MRI. These patients presented with gross (macroscopic) hematuria or had urinary bladder mass detected on ultrasound and/or computed tomography examinations. Human ethics committee approval for this study was obtained from the institutional review board of the educational hospital where these cases were treated. Exclusion criteria included upper urinary tract tumors or stones, a history of urinary tract trauma, contraindications to MRI (e.g. pacemaker or metallic prostheses), and refusal to consent to the study. Two of 50 patients were excluded from the study because of technical difficulties or failure of data acquisition (owing to patient’s irritability and excessive patient’s motion).
All 48 patients underwent transurethral cystoscopic biopsy after imaging, and four patients were confirmed as negative for bladder carcinoma. The tumor was histologically confirmed in the remaining 44 patients with 51 urinary bladder neoplastic lesions.
Patients were instructed to start drinking water 1 h before the MRI examination to moderately distend the bladder. All patients were prohibited from urinating for at least 1 h before examination. In patients with a urethral catheter, 250–400 ml of sterile saline was used to distend the bladder. MRI was performed using a 1.5 T Imager (GyroscanIntera; Philips Medical Systems, Best, the Netherlands) equipped with a radiofrequency coil (Quadrature Body Coil; Philips Medical Systems).
Bladder fullness was checked on localizer images, and the examination was delayed if the bladder was not full.
Initially, turbo spin echo T2-weighted images were obtained (repetition time/echo time, 2250–3500/90–100; bandwidth, 20–83 kHz; matrix, 256×256; section thickness, 4–6 mm; intersection gap, 1–2 mm; field of view, 20 cm).
Thereafter, with the patient freely breathing, DWIs were obtained in the axial plane by using a body coil and a monodirectional gradient multisection fast spin echo echoplanar sequence (repetition time/echo time 3500–4500/60–70 ms; bandwidth, 142 kHz; matrix, 256×256; section thickness, 4–6 mm; intersection gap, 1–2 mm; field of view, 36 cm; signals acquired with b values of 0, 500 and 1000 s/mm2). Thirty to 55 sections were obtained in 60–120 s to cover the pelvis. In some cases, DWIs were obtained in the sagittal plane to be perpendicular to the base of tumors; T2-weighted images were also evaluated in the axial and sagittal planes, in accordance with the DWIs.
To gain better signal-to-noise ratio, a larger field of view was used for DWI than for T2-weighted imaging.
All MRI sets were interpreted independently from all histopathological information. There were three image sets: T2-weighted images alone, DWIs alone, and T2-weighted plus DWIs. Diagnostic accuracy of staging with MRI as compared with pathologic stage was assessed on a stage-by-stage basis.
The urinary bladder tumors were classified into the following four categories based on the tumor, node and metastasis classification from the American Joint Committee on Cancer: T1 or lower, T2 (T2a or T2b), T3 (T3a or T3b), and T4. The staging criteria used were similar to those described previously for T2-weighted images , contrast-enhanced images , and DWIs .
As the normal bladder wall can be seen as a low signal intensity (SI) line on T2-weighted images, the bladder wall was considered to be intact (stage T1 or lower) when the low SI line was present. The bladder wall was considered to be invaded by the tumor (stage T2 or higher) when the low SI line was disrupted focally in the region underlying the tumor.
On DWIs, bladder cancer has been reported to show high SI . Similar to a previous study published by Takeuchi et al. , we assumed that a line of intermediate SI outlining the bladder lumen and a low SI area between the tumor and muscle could reflect a muscle layer and a submucosal stalk, respectively. The staging criterion for DWI is as follows ([Figure 1]): a thin, flat, high SI area corresponding to the tumor or a high SI tumor with a low SI submucosal stalk or a thickened submucosa indicates stage T1 or lower; a high SI tumor without a submucosal stalk and with a smooth tumor margin indicates stage T2; extension into the perivesical fat with an irregular margin indicates stage T3; and extension into adjacent organs indicates stage T4.
|Figure 1: Schematic diagram showing diagnostic criteria for using diffusion-weighted imaging for staging bladder cancer. Cancer component, muscle layer, and submucosa show high, intermediate, and low signal intensity, respectively. Submucosal stalk or thickened submucosa indicates T1 or lower stage; smooth tumor margin without submucosal components, T2; irregular margin toward the perivesical fat tissue, T3; and extension into adjacent organs, T4 .|
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Apparent diffusion coefficient and histologic grade
ADC maps were generated in the tumors that were large enough (>5 mm) to contain the region of interest. The mean ADC values were analyzed by drawing one to three circles over the bladder tumor in the ADC map, each circle measures about 1 cm in diameter. The ADC values were measured to estimate the degree of diffusion ([Figure 2],[Figure 3],[Figure 4],[Figure 5]).
|Figure 2: (A–F) Large fungating urinary bladder soft tissue mass lesion is seen in T2 WI’s (A, B) showing restricted diffusion (C,D ADC WI’s and E, F DWI’s). The mass lesion is seen invading the dark T2 signal wall of the urinary bladder posteriorly (yellow arrows) and encasing the ureteric orifice (red arrow). The mean ADC value measures 0.89×10−3 mm2/s and pathologically proved as bladder Squamous cell carcinoma (grade III).|
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|Figure 3: (a–i) (A–C T2-weighted images, D–F diffusion-weighted imaging and G–I apparent diffusion coefficient maps). Multiple fungating urinary bladder mass lesions are seen with restricted diffusion. The lesions do not invade the dark T2 signal wall of the urinary bladder (yellow arrow). The mean apparent diffusion coefficient values of the bladder lesions measure 1.34×10−3 mm2/s, 1.31×10−3 mm2/s, 1.27×10−3 mm2/s, and 1.1×10−3 mm2/s. The lesions are pathologically proved as multicenteric bladder urothelial carcinoma (grade I).|
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|Figure 4: (a–f) A large fungating and other smaller nodular mass lesions were seen involving the trigon and left lateral wall of the urinary bladder. Both lesions showed exophytic components invading the perivesical fat planes with restricted diffusion (arrows in images C and D). The mean apparent diffusion coefficient values of the larger and smaller lesions were 1.06×10−3 mm2/s and 1.08×10−3 mm2/s, respectively. Both lesions were pathologically proved as urothelial carcinoma (grade II).|
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|Figure 5: (A–D) Large ill-defined fungating soft tissue mass lesion is seen involving the urinary bladder walls partially sparing its anterior wall (A–B) with diffusion restriction (C–D). The mass lesion shows large exophytic component projecting posteriorly (arrow head). Associated two discretely enlarged metastatic right internal iliac lymph nodes (arrows). The mean ADC values of the bladder mass lesion measured 0.89×10−3 mm2/s. The mass was pathologically proved as Urothelial carcinoma (grade III).|
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The specimens were stained with hematoxylin–eosin stain for conventional histopathologic evaluation. Histologic grading was evaluated with respect to increased cellularity, nuclear crowding, disturbance of cellular polarity, failure of differentiation from the base to the surface, polymorphism, irregularity in the size of cells, variations of shape, chromatin patterns of nuclei, displaced or abnormal mitotic figures, and giant cells. Tumors were classified into three grades: G1, the least degree of anaplasia; G2, an intermediate degree of anaplasia; and G3, severe anaplasia.
| Results|| |
Our study included 48 patients. All 48 patients underwent transurethral cystoscopic biopsy after imaging, and four patients were confirmed negative as regards bladder carcinoma. The tumor was histologically confirmed in the remaining 44 patients with 51 urinary bladder neoplastic lesions.
Pathologic stage was determined in the 44 patients (age: 44–73 years; mean: 59 years). There were 41 men and three women. Four patients had multiple tumors (seven additional tumors), and hence a total of 51 tumors were analyzed. All patients underwent surgery within 35 days (mean: 7 days) after MRI. In patients who underwent transurethral resection (TUR), an additional deep muscle biopsy was performed at the base of the tumor. When no tumor cells were found, the pathologic stage was classified as T1 or less. Two patients who underwent TUR showed positive deep muscle biopsy, and hence they shifted into invasive bladder cancer and underwent radical cystectomy.
Noninvasive bladder cancer was proved in eight patients who underwent TUR, and invasive bladder cancer was proved in 36 patients. All patients with invasive bladder cancer underwent radical cystectomy.
The tumor was histologically confirmed in 44 patients with 51 urinary bladder neoplastic lesions. The DW-MRI was able to detect all 51 tumors noted at conventional cystoscopy, with no false-negative results. Four patients were confirmed as negative as regards bladder carcinoma using the transurethral cystoscopy and biopsy. One of these four patients was misdiagnosed with neoplastic lesion with DWIs. The sensitivity, specificity, accuracy, positive predictive value (PPV), and negative predictive value (NPV) are illustrated in Charts 1 and 2
The pathologic stage was between Tis and T1 in 27% (14 of 51) of tumors, T2 in 24% (12 of 51), T3 in 22% (11 of 51), and T4 in 27% (14 of 51). The tumors measured 1.2–10.0 cm in their maximum diameter (mean: 5.39 cm). Histologic diagnoses were urothelial carcinoma (n=29) and squamous cell carcinoma (n=22). The histologic grade was G1 in 10 (20%) of 51 tumors, G2 in 19 (37%), and G3 in 22 tumors (43%).
Staging using T2 weighed images versus diffusion-weighted images
The sensitivity, specificity, and overall accuracy of the consensus of MRI for differentiating Tis to T1 tumors from T2 to T4 tumors obtained using DWIs alone or DW plus T2-weighted images were significantly better than those using T2-weighted images alone. In addition, the sensitivity achieved using T2-weighted is high, reaching 97%. However, the sensitivity achieved with DWIs alone or DW plus T2-weighted images together is raised, reaching 100% ([Table 1]).
|Table 1: Diagnostic accuracy for differentiating stage Tis to T1 tumors from T2 to T4 tumors|
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The sensitivity, specificity, and accuracy of the MRI for differentiating T2 or lower tumors from T3 to T4 tumors obtained using DWIs were slightly higher than those using T2-weighted images. T2-weighted images together with DWIs showed a sensitivity, specificity, and accuracy of 100% for each ([Table 2]).
|Table 2: Diagnostic accuracy for differentiating stage Tis to T2 and tumors from T3 to T4 tumors|
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Correlation between apparent diffusion coefficient values and histological grade
The correlation between ADC values and histologic grade were as follows: the mean ADC of the 51 bladder tumors was 1.0197×10−3 mm2/s. The mean ADC values of G1, G2, and G3 tumors were 1.2064×10−3 mm2/s, 1.025×10−3 mm2/s, and 0.93×10−3 mm2/s, respectively. The differences in ADC were significant between G1 and G3 and between G1 and G2 but not significant between G2 and G3 ([Table 3]).
|Table 3: Correlation between apparent diffusion coefficient values and histologic grade|
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| Discussion|| |
Cancer of the urinary bladder is a common malignant tumor of the urinary tract in both men and women . Accurate preoperative staging is the most important factor in determining the appropriate management of urinary bladder cancer because the therapeutic method chosen and prognosis depend on the clinical findings and radiologic stage at presentation .
Superficial tumors are treated with TUR with or without adjuvant intravesical chemotherapy or photodynamic therapy , whereas invasive tumors are treated with radical cystectomy, radiation therapy, chemotherapy, or a combination . Therefore, preoperative imaging studies would play an important diagnostic role if they could be used to precisely differentiate between the two categories of bladder cancer.
Contrast agents used in conventional MRI can have adverse effects, including nephrogenic systemic fibrosis . Cystoscopy and transurethral endoscopic ultrasonography are considered as invasive techniques. Therefore, further improvement of a diagnostic modality may be desirable.
Hence, the purpose of our study was to assess the detection of urinary bladder carcinoma using DW-MRI and to determine whether this noninvasive technique has supplementary value for preoperative T staging. In addition, we conducted this study to measure the correlation between ADC and histologic grade of the urinary bladder cancer.
Role of diffusion-weighted MRI in the detection of urinary bladder carcinoma
The feasibility of using DW-MRI for the detection of a urinary bladder carcinoma has been reported by Matsuki et al. . The sensitivity and PPV of DWI in that study were both 100% for the detection of carcinomas . However, that study had several limitations as it was a retrospective study of a small number of patients (15 patients). In addition, all patients’ MR examinations occurred after biopsy, which may have affected the results. Furthermore, all patients included in the study were known to have bladder tumors, thus there was case selection bias in the report.
In a study carried out by Abou-El-Ghar et al. , on 130 patients with hematuria, the cystoscopy was considered as a standard reference. The sensitivity, specificity, PPV, NPV, and accuracy of DW-MRI were found to be 98.5, 93.3, 100, 92.3, and 97%, respectively . The authors found excellent agreement between the DW-MRI and the conventional cystoscopy. Reviewers could identify almost all bladder lesions and missed only two lesions that were less than 4 mm in diameter.
Another study was published by Ceylan et al. , who conducted their study on 59 patients referred to the clinic with complains of hematuria and evaluated using upper urinary system pathology and then DW-MRI and cystoscopy. The sensitivity, specificity, and accuracy values of DW-MRI were 90, 93, and 91%, respectively .
In accordance with the results of the previous studies, all bladder cancers we have evaluated were clearly detectable with DWI showing 100, 75, 98.1, 100, and 98.1% sensitivity, specificity, PPV, NPV, and accuracy, respectively.
In addition, DW-MRI can provide information on lesion size, number, and location to surgeons who perform conventional cystoscopy. The common limitation of our as well as other previous studies was the lack of follow-up after interventional or operative therapy.
It also appears as an alternative to cystoscopy because it possesses a noninvasive nature, provides a proximate relationship of diagnostic value for cystoscopy, requires a short time to take an image (151 s), it has no any necessities for a contrast, and enables uncomplicated patient compatibility.
In our knowledge, many of the previously mentioned published studies had a common limitation that the value of DW versus T2-weighted MRI for staging of bladder tumors was not assessed.
Role of diffusion-weighted MRI in staging of urinary bladder carcinoma
Results of a study reported by Takeuchi et al.  on 52 bladder tumors were compared with our results (Charts 3 and 4); the results of Takeuchi et al.  matched our study results, which concluded that the sensitivities, specificities, and accuracy obtained using T2-weighted plus DWIs were significantly better than that obtained using T2-weighted images alone. We believe that this was due to the enhanced visibility of the structures of the tumor, muscle layer, and thickened submucosa, all of which showed different SI on DWIs
The characteristic finding, reported by Takeuchi et al.  on the DWIs of the high SI bladder cancer over the low SI submucosal stalk was an arch-shaped appearance similar to an inchworm. We agree with the authors with regard to this characteristic finding to be indicative of stage T1 or lower tumor, and hence dynamic contrast-enhanced images could be skipped.
Tekes et al.  reported that 81% of bladder tumors showed a SI similar to that of muscle on T2-weighted images and that overstaging was the most common error when evaluating T-stage. We also believe that the insufficient SI contrast between tumor and submucosa might cause relatively low accuracy.
Can diffusion-weighted MRI predict the histological grading of urinary bladder carcinoma?
The usefulness of DW MRI for depicting malignant tumors  and an ADC for characterizing tumor grades have been suggested recently.
ADCs representing the degree of water molecular diffusion and the degree of restriction to water diffusion in biological tissues are inversely correlated to the tissue cellularity and the integrity of the cell membranes . Several authors had already reported decreased ADC among various malignant lesions due to dense cellularity and large cellular size .
In the literature, there are many reports evaluating the feasibility of DWI in the diagnosis of urinary bladder cancers, such as that by Yoshida et al. , Matsuki et al. , and El-Assmy et al. , in which the ADC values of the tumor tissue were found to be significantly low when compared with ADC values of the vicinity tissues (normal bladder wall, prostate, and seminal vesicles).
Matsuki et al.  stated that there was no overlap between the ADC values of tumors and those of normal bladder wall; however, they did not define a cutoff value. In contrast to their study, other studies published, such as those by El-Assmy et al.  and Kiliçkesmez et al. , reported that, despite the significant difference in the ADC values of tumors and bladder wall, there was a small amount of overlap, and they could not determine a cutoff point for the detection of malignancy. Moreover, El-Assmy et al.  found that there was no overlap between the ADC values of the tumors and the urine.
As regards ADC values concluded by Ceylan et al. , mean ADC values of patients who were diagnosed with a bladder tumor (1.05±0.22×10−3 mm2/s) were significantly lower than the mean ADC values obtained from the normal bladder wall (1.830±0.18×10−3 mm2/s).
In our study, the mean ADC of G1 tumors was significantly higher than that of G2 and G3 tumors. Meanwhile, there was an inverse relationship between the mean ADC values and the histological grade of the tumor. Our results were nearly matching with those of Takeuchi et al. ; however, the authors found that all G3 tumors had an ADC less than 1.0×10−3 mm2/s, whereas in our study all G3 tumors had an ADC less than 1.25×10−3 mm2/s. Nevertheless, the mean ADC value in our study for G3 tumors was less than 0.95×10−3 mm2/s. On the basis of our study and prior studies, the ADC could predict the histologic grade of bladder cancer.
The limitations of the present study were the inclusion of a larger number of advanced stage tumors and large-sized lesions (mean: 5.39 cm), and this could explain the high sensitivity, specificity, and accuracy of DW-MRI for differentiating Tis to T2 tumors from T3 to T4 tumors. Second, DWI is known to be sensitive for lymph node and bone metastases: we did not evaluate its diagnostic performance for N or M staging in this study. However, further study is needed to assess whether the use of DWI improves such diagnoses.
We agree with Choi et al.  and Abou-El-Ghar et al.  as regards two main disadvantages of DW-MRI where failure to visualize the lumen of the urethra, as it is routinely seen at conventional cystoscopy, and patients with metal prostheses or implants could not be adequately examined. In addition, this technique is limited by poor spatial resolution and there is potential risk for image distortion caused by postbiopsy hemorrhage or previous interventional therapy.
However, DW-MRI has many advantages such as short acquisition time, noninvasive technique, and does not contain ionized radiation. Moreover, in our study, DWI was performed without breath holding, thus allowing examination of severely ill, old, or obese patients who were unable to hold their breath for a long time.
In addition, in recent times, DW-MRI is accepted as an important marker of tumor cellularity; it may be used as an alternative in future diagnosis and follow-up of bladder tumors.
DW-MRI is emerging as a powerful clinical tool for directing the care of patients with cancer. DW-MRI may be added to routine abdominal imaging protocols that add confidence to lesion detection, characterization against suppressed background signal, especially in urinary bladder cancers and determining therapy response.
| Conclusion|| |
According to our results we assume that DW-MRI is a safe and confident method in the detection and local staging of urinary bladder carcinoma. In addition, DWIs may predict the histological grade of the tumor. Hence, DWI may be added to routine imaging protocols of urinary bladder tumors.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
[Table 1], [Table 2], [Table 3]