|Year : 2014 | Volume
| Issue : 3 | Page : 552-557
Dynamic computed tomography and Doppler findings in different subtypes of renal cell carcinoma with their histopathological correlation
Binit Sureka1, Anupam Lal1, N Khandelwal1, Kusum Joshi2, SK Singh3, Mayank M Agarwal3, Aliza Mittal4
1 Department of Radiodiagnosis and Imaging, PGIMER, Chandigarh, India
2 Department of Histopathology, PGIMER, Chandigarh, India
3 Department of Urology, PGIMER, Chandigarh, India
4 Department of Pediatrics, PGIMER, Chandigarh, India
|Date of Web Publication||14-Oct-2014|
Department of Radiodiagnosis and Imaging, PGIMER, Chandigarh - 160 012
Source of Support: None, Conflict of Interest: None
Background: Renal cell carcinoma (RCC) is by far the most common soft-tissue mass and accounts for 85% of all malignant masses of the kidney. Histopathological subtype has clinical implications in the form of prognosis and response to various newer and adjuvant treatment strategies.
Aim: The aim of this study was to evaluate the morphology and enhancement patterns of different subtypes of RCC and correlate them with their histopathological subtypes.
Materials and Methods: The study group comprised of 20 consecutive patients of RCC. The patients were evaluated with multi-detector-row computed tomography (MDCT) and Doppler ultrasound prior to surgery and findings compared with histopathological subtypes of tumor.
Results: RCC was confirmed on histopathology. Out of 20 patients with RCC, 14 were finally diagnosed as clear cell, 4 chromophobe and 2 as papillary subtypes of RCC. None of clear-cell type showed homogenous enhancement. The mean attenuation in corticomedullary phase (CMP) and nephrographic phase (NP) for clear cell and chromophobe subtype was higher than papillary subtype, i.e. 116.1 ± 27 HU and 91.9 ± 21 HU for clear cell, 103 ± 22.4 HU and 96.2 ± 9.2 HU for chromophobe subtype and 78.5 ± 12.4 HU and 73.3 ± 12.2 HU for papillary subtype respectively. On Doppler US evaluation, non-clear-cell subtypes, which showed heterogenous enhancement on MDCT showed less color flow and peak systolic velocity (PSV). The difference in PSV and Doppler shift frequency values between clear-cell carcinoma and chromophobe subtypes were statistically significant (P = 0.003).
Keywords: Dynamic MDCT and Doppler US are reliable in differentiating clear cell from non-clear-cell subtypes of RCC
|How to cite this article:|
Sureka B, Lal A, Khandelwal N, Joshi K, Singh S K, Agarwal MM, Mittal A. Dynamic computed tomography and Doppler findings in different subtypes of renal cell carcinoma with their histopathological correlation. J Can Res Ther 2014;10:552-7
|How to cite this URL:|
Sureka B, Lal A, Khandelwal N, Joshi K, Singh S K, Agarwal MM, Mittal A. Dynamic computed tomography and Doppler findings in different subtypes of renal cell carcinoma with their histopathological correlation. J Can Res Ther [serial online] 2014 [cited 2020 Jun 4];10:552-7. Available from: http://www.cancerjournal.net/text.asp?2014/10/3/552/137924
| > Introduction|| |
Renal cell carcinoma (RCC) is by far the most common soft-tissue mass and accounts for 85% of all malignant masses of the kidney. , According to First International Workshop on RCC held by World Health Organization, RCC can be classified into conventional (i.e. clear cell) renal carcinoma, papillary renal carcinoma, chromophobe carcinoma, collecting duct renal carcinoma, medullary and unclassified renal carcinoma. The behavior of RCC depends upon its subtype, staging, Furhman grade and accordingly precise prediction of the subtype and stage may be helpful for planning appropriate surgical resection -radical nephrectomy, adrenal sparing nephrectomy or nephron sparing nephrectomy. Histopathological subtype has clinical implications in the form of prognosis and response to various newer and adjuvant treatment strategies. , Paralleling this clinical stage there is a growing trend for more limited surgical resection, such as adrenal-sparing radical nephrectomy, laparoscopic nephrectomy, or nephron-sparing partial nephrectomy. The past two decades have witnessed significant changes in the manifestation, diagnosis and management of RCC. Multi-detector-row computed tomography (MDCT), magnetic resonance imaging (MRI) and ultrasonography (USG) are increasingly performed in place of traditional diagnostic imaging tests, such as intravenous urography (IVU) and angiography. RCC has many varied appearances on MDCT, ranging from a small homogenous enhancing mass to a large cystic or solid heterogenous tumor extending to the adjacent organs.  The role of radiologist is to separate RCC from other renal masses with total confidence so that appropriate treatment plan could be envisaged. Any information regarding the possible subtype of RCC is invaluable as different subtypes have different prognostic implications and differing technique of surgical excision.  Prior attempts to differentiate among RCC subtypes involved angiography or contrast enhanced MDCT based observations that conventional clear cell carcinomas tend to be hypervascular, while papillary carcinomas tend to be hypovascular. Thus, depending on vascularity of the tumor it is expected that there will be different enhancing properties and Doppler flow parameters of different histological types of RCC. The present study was conducted to evaluate the potential of dynamic MDCT and Doppler findings in RCC and to correlate their findings with histopathology after surgery.
| > Materials and methods|| |
The study was given ethical clearance by the Ethical Committee of the Institute. A total of 21 consecutive patients who presented to the institute between June 2008 and July 2010 with presumed diagnosis of RCC either clinically or by other investigations like ultrasound and IVU underwent dynamic helical MDCT scan. Doppler evaluations were performed within 1 week of expected day of surgery. RCC was subsequently confirmed on histopathological examination of surgical specimen. On MDCT scan, the enhancement patterns, attenuation of the tumor in unenhanced, CMP and NP; and on Doppler various parameters were evaluated.
Dynamic CT protocol
All MDCT examinations were performed on a Siemens Sensation 16 (Siemens medical system, Erlangen, Germany). The parameters were 120 kVp; 210 mA; section collimation 5 mm; table feed 7 mm/s; and reconstruction interval 5 mm. All patients received 1.5-2 L of diluted ionic oral contrast medium (Urografin 76%, Zydus, German Remedies) 30-40 min before MDCT and 120 ml of intravenous iodinated contrast medium (Iopamiro 300 mg/dl, Bracco, Italy); the intravenous contrast material was injected into an antecubital vein using a pressure injector at a rate of 3.0 ml/s. MDCT examination included unenhanced, corticomedullary and nephrographic phase (NP) scanning. Scanning for the corticomedullary phase (CMP) was acquired 30 s after IV contrast injection and scanning for the NP was acquired 120 s after contrast injection. In addition, immediately after the scanning for the NP, scanning covering the lower abdomen and pelvis was performed. The enhancement pattern of the tumor was classified as homogeneous, heterogeneous, or predominantly peripheral. Homogeneous enhancement was indicated when most areas in the tumor showed a uniform degree of enhancement. Predominantly peripheral enhancement was considered when most portions of the tumor did not enhance and only the peripheral rim or septa showed enhancement. The remaining cases were considered to have heterogeneous enhancement. To evaluate the degree of enhancement of a tumor, the attenuation of three separate regions of interest with a ROI of 1 cm 2 were measured within the mass lesion and the mean of these three values were calculated. The location for measuring the attenuation value was chosen within the solid enhancing area. A round or elliptic region-of-interest cursor was placed over an enhanced area, which was at least 1 cm 2 in the area and consistent in location during all phases of MDCT. The enhanced area was covered as much as possible in the region of interest and the area of calcification, necrosis and hemorrhage were excluded from the region of interest. The degrees of enhancement were measured by calculating the difference in the mean attenuation values between the corticomedullary and unenhanced phase scans and between the nephrographic and unenhanced phase scans. To eliminate the influence of tumor size on enhancement pattern, tumors were divided into the following groups according to the maximum diameter: less than 3 cm, 3-7 cm and greater than 7 cm. Perinephric change was indicated when evidence of strands of soft-tissue attenuation or parasitized vessels in the perinephric area and thickening of Gerota's fascia were present. Venous involvement was indicated when the lumen of the renal vein or the inferior vena cava (IVC) was replaced by the tumor. Lymphadenopathy was considered to be present when a lymph node was enlarged more than 1 cm in short axis diameter.
Doppler ultrasound protocol
Doppler US examination was performed on Philips HD 11, Bothell, U.S.A. Patients were examined in the supine and lateral decubitus positions using transverse, intercostals and parasagittal scanning using a curvilinear probe of 2-5 MHz and if required linear probe of 3-12 MHz. The wall filter was set to as low as possible. Vascular areas in the focal renal lesions were identified on color Doppler and the Doppler shift frequency DSF of the lesions were calculated. Power Doppler imaging of focal renal lesions were done to identify and localize slow moving blood flow, i.e. the signals which was not localized by color Doppler. The peak systolic velocity (PSV), end diastolic velocity (EDV) and the resistive index (RI = PSV - EDV/PSV) of the lesions were recorded. Venous invasion was indicated when there was an absence of a venous flow pattern in intrarenal veins, distension of the renal vein or IVC by echogenic material and partial or complete absence of flow detected by color Doppler sonographic examinations.
Descriptive statistics in terms of frequency counts and percentages were used for discrete variables such as socio-demographic variables, tumor calcification, renal vein and lymph node involvement. Mean and standard deviations were calculated for all the continuous variables, i.e. certain sociodemographic variables, tumor size, degree of enhancement and attenuation values in different phases. Statistical analysis was performed using Kruskal-Wallis test and Mann-Whitney test.
| > Results|| |
A total of 20 with RCC confirmed on histopathological examination of surgical specimen removed after radiological investigations were included in the study. In one subject, a lesion involving the interpolar region of the right kidney turned out to be medullary fibroma on histopathology, hence was excluded from the study. Three subtypes of RCC found included clear cell RCC, papillary RCC and chromophobe RCC. The mean age of patients with clear cell RCC was 54.2 ± 8.1, chromophobe RCC was 40 ± 14.4 and papillary RCC was 59.5 ± 6.3. The mean size of the tumor, sex distribution and presence of calcification in three subtypes of RCC is shown in [Table 1]. The clear cell [Figure 1] and chromophobe RCC [Figure 2] showed greater mean enhancement in CMP when compared with papillary RCC [Figure 3]. Heterogenous enhancement was seen in 64.3% cases of clear cell, 50% subjects of chromophobe and papillary RCC. Predominantly peripheral enhancement was noted in 35.7% subjects of clear cell RCC. Homogenous enhancement was seen in 50% cases of papillary and chromophobe RCC. None of clear cell RCC showed homogenous enhancement and none of the chromophobe and papillary tumor had predominantly peripheral enhancement. The mean attenuation value of different subtypes of RCC is shown in [Table 2]. We observed perinephric spread in 9 clear cell, 4 chromophobe and 1 papillary RCC in CT scan. However, 4 cases with clear cell RCC, 3 with chromophobe RCC and 1 with papillary RCC were confirmed not to have perinephric spread on histopathological examination. Tumor thrombus was seen in 5 (35.7%) subjects of clear cell RCC and none in chromophobe and papillary RCC. In four cases, this was correlated with Doppler. Only 2 cases were confirmed on histopathology. In another 2 cases with tumor thrombus on histopathology, the tumor thrombus was not picked up by CT and Doppler USG. Lymph node enlargement was seen in 5 (35.7%) clear cell RCC and none in chromophobe and papillary RCC on CT. Doppler Indices of different subtypes of RCC are shown in [Table 3]. It was observed that PSV in clear cell RCC was significantly higher when compared with that in chromophobe RCC (P = 0.003). The Doppler shift frequency was 1 ± 0.5 in clear cell RCC, 0.3 ± 0.08 in chromophobe and 0.9 ± 0.1 in papillary RCC [Figure 4]. DSF was significantly higher in clear cell when compared to chromophobe RCC (P = 0.003).
|Figure 1: (a) Unenhanced phase at the level of renal hilum shows mass lesion in the right kidney with mean attenuation 40 HU. (b) Corticomedullary phase shows intense heterogenous enhancement with computed tomography (CT) attenuation 125 HU. (c) Nephrographic phase shows washout of contrast with CT attenuation 105 HU. (d) Photomicrograph showing tumor cells having abundant clear cytoplasm arranged in alveolar pattern (H and E, ×120) consistent with clear cell renal cell carcinoma|
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|Figure 2: (a) Unenhanced phase at the level of renal hilum shows exophytic lobulated mass in left kidney with peripheral and central calcification and mean computed tomography (CT) attenuation 39 HU. (b) Corticomedullary phase shows homogenous enhancement with mean CT attenuation 113 HU. (c) Nephrographic phase showing homogenous spoke-wheel type enhancement wit CT attenuation 102 HU. (d) Photomicrograph showing tumor cells with perinuclear halos and positivity by Hale's colloidal iron stain (Hale's colloidal iron stain, ×540) consistent with chromophobe cell renal cell carcinoma|
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|Figure 3: (a) Unenhanced phase at the level of renal hilum of right kidney shows an exophytic mass with mean attenuation value of 49 HU. (b) Corticomedullary phase shows homogenous enhancement with mean computed tomography attenuation 69 HU. (c) Nephrographic phase again shows no significant washout with mean attenuation of 64 HU. (d) Photomicrograph showing variably sized papillae with central vascular core lined by cuboidal to columnar tumor cells (H and E, ×120) consistent with papillary cell renal cell carcinoma|
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|Figure 4: Doppler ultrasound in (a) clear cell carcinoma showing heterogenous mass in right kidney with peak systolic velocity (PSV) 13 cm/s (b) Chromophobe cell carcinoma showing relatively hypoechoic mass with vascularity seen on power Doppler (c) Papillary cell carcinoma showing homogenous isoechoic mass with PSV 16.9 cm/s|
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|Table 1: Mean tumor size, sex distribution and presence of calcification in three subtypes of RCC|
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|Table 2: Mean attenuation value of 3 subtypes of RCC in unenhanced, corticomedullary and nephrographic phases|
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| > Discussion|| |
RCC is the most common adult renal cancer with up to 30-40% of being accidently discovered at imaging.  The challenges of renal tumor imaging include not only reliable differentiation between benign and malignant lesions but also accurate delineation of the extent of the disease to ensure optimal treatment planning. Triphasic MDCT is the ideal method for comprehensive evaluation of renal masses. Ultrasound and CT complement each other in the characterization of renal lesions. In the subgroup of patients whose renal lesions are ''indeterminate'' on ultrasound, a dedicated renal protocol MDCT may help characterize the lesion further.  Conversely, ultrasound may prove useful for renal lesions that are considered indeterminate on MDCT.  The vascular distribution at Doppler potentially can add information in differentiation of solid renal masses.
Clear cell carcinoma is the most common subtype; accounting for approximately 70% of RCCs. Overall 5 years survival rate of patients with clear cell carcinomas range from 55% to 60% respectively.  Papillary renal carcinomas, the second most common subtype, comprises from 15% to 20% of RCCs with a high 5 years survival rate ranging from 80 to 90%.  Chromophobe renal carcinomas accounts for 6-11% of the cases. Patients with this subtype have the best prognosis: The 5 years survival rate is approximately 90%.  Collecting duct carcinoma is a rare subtype comprising about 1% of the cases; however patients with collecting duct carcinoma have the worst prognosis, with a 5 years survival rate of less than 5%.  With the advent of newer treatment options and adjuvant therapies like immunotherapy with interleukin-2, interferon-α and autolymphocytes, antiangiogenic therapy, cytotoxic chemotherapy, radiofrequency and cryoablation techniques, predicting the subtype of RCC is beneficial for both the surgeon as well as patient. Clear cell and chromophobe RCC may show response to immunotherapy which is not useful in papillary RCC. Antiangiogenic therapy may be useful in clear cell RCC. Collecting duct and sarcomatoid RCC may be susceptible to cytotoxic chemotherapy.
Subtypes can be predicted by using multiphasic MDCT and Doppler USG as shown by previous studies. ,,,, We did not find any significant difference between three subtypes of RCC with regard to mean tumor size similar to the earlier study conducted by Kim et al. The mean attenuation in CMP was 116.1 ± 27 in clear cell, 103 ± 22.4 in chromophobe and 78.5 ± 12.4 in papillary RCC. This result is consistent with the angiographic findings that most clear cell RCC show hypervascularity in the arterial and capillary phase and most papillary RCC show hypovascularity. , Strong enhancement of clear cell RCC is due to its rich vascular network and alveolar architecture.  In our study, in NP the mean attenuation value for clear cell was 91.9 ± 21 and for papillary RCC was 73.3 ± 12.2. Papillary RCC are relatively more hypovascular and homogenous than clear cell RCC. Our observations are consistent with the results of previous studies. The type of tumor might be of interest to the surgeon because if he resects a hypervascular renal clear cell carcinoma, he must expect more bleeding than with hypovascular renal papillary carcinoma. The same information might be of interest for minimally invasive ablative approaches like radiofrequency or cryotherapy for two reasons: It might be safer to perform an embolization in clear cell type of renal clear cell carcinoma - a palliative procedure-before the planned curative intervention to avoid bleeding.
Heterogenous enhancement was seen in nine and predominantly peripheral enhancement in five clear cell RCC. This type of enhancement on MDCT correlated well with pathological finding of intratumoral necrosis which is common in clear cell RCC.  Homogenous enhancement was seen in two cases of chromophobe and one case of papillary RCC. None of the clear cell variety showed homogenous enhancement. This concludes that homogenous enhancement is common in non-clear cell type RCC.
With respect to tumor spreading pattern, one each of chromophobe and papillary RCC had perinephric spread but none had renal vein involvement or lymphadenopathy and were detected in early stage. Although, four cases were detected in Stage 3a and two were detected in Stage 3b in clear cell RCC. Prognosis is generally reflected in staging severity, with lower-stage disease being associated with longer survival rates. This also explains the fact that clear cell RCC has a poor prognosis probably due to its late stage at detection. Lymph node involvement was seen in five cases on MDCT. On histopathology only two cases showed lymph node enlargement due to involvement by tumor. In the remaining three cases reactive lymph node enlargement was seen on histopathology. Enlarged (>1 cm) nodes are not necessarily metastatic but may be reactive, i.e. false positive (58% in one series by Studer et al.  - which may be more common in necrotic tumors or tumors that involve the renal vein. Identification of thrombus in the venous system, especially the IVC, is particularly important because it affects surgical management, typically necessitating an anterior abdominal approach. Furthermore, if thrombus extends into the heart, a combined thoracic and intracardiac approach with cardiac bypass may be required. Current MDCT techniques have reported sensitivities and specificities for detecting renal vein thrombus of 85% and 98%, respectively.  Color Doppler sonography has reported sensitivities and specificities for detecting thrombus in the renal veins of 75% and 96% respectively, with 100% accuracy for detection of thrombus in the IVC.  Tumor thrombus was seen in 5 (35.7%) subjects of clear cell RCC and none in chromophobe and papillary RCC, but only 2 cases were confirmed on histopathology. False-positive results in two patients was observed in patients with an enlarged renal vein without tumor thrombosis, the chief cause of which was increased flow with higher vascularized tumors and arterio-venous shunts. One case had a large right renal mass, the distinction between intraluminal tumor thrombus and extrinsic caval compression caused by this large primary tumor was difficult. Four (28.58%) subjects of clear cell RCC showed tumor thrombus on Doppler USG. In one case, it showed dilated renal vein and in the other case it was large right renal mass obscuring the visualization of renal vein, which was thought to be thrombosed while actually the mass was compressing the vein. Additional 2 cases which showed tumor thrombus on histopathology were found to be normal on MDCT and Doppler USG. Both these cases showed to have intrarenal tumor emboli on histopathology and were obese making Doppler evaluation difficult in these two cases.
The study revealed highly significant difference in regard to PSV and Doppler Shift Frequency between clear cell and chromophobe RCC. This may be due to hypervascularity seen in clear cell RCC. High PSV in clear cell RCC is due to increased flow and arterio-venous shunts being more in clear cell type. Non-clear cell type RCC shows decreased intratumoral vascularity measured in terms of microvessel density. ,
Contrast-enhanced ultrasound (CEU) is also a useful and emerging modality in diagnosing various subtypes of RCCs. The advantages of CEU agents are they remain intravascular without diffusing into the interstitial space, better visualization of intralesional microvasculature, higher temporal resolution of ultrasound than of CT/MRI and free from risks of nephrotoxicity or nephrogenic systemic fibrosis in patients with renal dysfunction. According to Gerst et al.  lesion washout, grade of contrast enhancement and quantitative measure of peak intensity may be useful for differentiating clear cell carcinoma and non-clear cell renal tumors. Non-clear cell subtypes usually show less avid enhancement when compared to clear cell types. Heterogenous lesion, marked enhancement when compared to adjacent renal parenchyma and delayed washout of microbubble contrast ultrasound agent favors a diagnosis of clear cell carcinoma. Time-enhancement curve shows higher peak of enhancement with the relative lack of washout after renal peak in corticomedullary phase (CMP). Papillary and chromophobe subtypes show less or minimal enhancement compared to clear cell type.
| > Conclusions|| |
Thus, multiphasic MDCT is the preferred modality for detection, characterization and staging of RCC. Detection of color flow on color Doppler USG in a renal mass is almost diagnostic of malignant renal mass and the spectral waveform may be helpful in differentiating clear cell type of RCC from others.
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[Figure 1], [Figure 2], [Figure 3], [Figure 4]
[Table 1], [Table 2], [Table 3]