Sonographic Appearances of Renal Cell Carcinoma: a review of 78 patients

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1 中華放射醫誌 Chin J Radiol 2007; 32: Sonographic Appearances of Renal Cell Carcinoma: a review of 78 patients Ching-Yih Yang 1, Chui-Mei Tiu Yi-Hong Chou Hsin-Kai Wang Hong-Jen Chiou Jia-Hwia Wang See-Ying Chiou Ming-Huei Sheu Cheng-Yen Chang Kuang-Kuo Chen 3,4 Chun Yu Department of Radiology 1, Keelung Hospital, Department of Health, Executive Yuan Department of Radiology 2, Department of Surgery 3, Taipei Veterans General Hospital School of Medicine 4, National Yang-Ming University Renal cell carcinoma (RCC) is the most common malignant renal tumor in adults. The kidney can usually be adequately imaged with real-time ultrasound (US) scanners. To summarize the ultrasonographic manifestations of RCC, we reviewed 78 patients with pathologically proved RCC. Within a period of 5 years, sevent y-eight patients were found to have renal masses by ultrasonography (US) study of upper abdomen, and subsequently underwent surgical treatment and/or biopsy. Histopathological study confirmed the diagnosis of RCC in all patients. Thirty-five of them were asymptomatic and were found to have renal tumor incidentally at US examination. The US studies were reviewed to clarify the relationship between echopatterns and sizes of RCC. The echogenicity of the lesions was graded from I through V as compared to the echogenicity of renal medulla, renal cortex, liver/spleen and renal sinus. Most RCCs were presented as solid masses (n= 33; 42%) or complex masses (n= 42; 54%). Only 3 patients were presented with cystic masses (4%). Grade I echogenicity (not higher than renal medulla) was noted in only 5% of renal tumors; grade II (higher than medulla but not higher than renal cortex) in 35%; grade III (higher Reprint requests to: Dr. Yi-Hong Chou Department of Radiology, Taipei Veterans General Hospital. No. 201, Sec. 2, Shih Pai Road, Taipei 11217, Taiwan, R.O.C. than cortex but not higher than liver/spleen) in 50%; and grade IV (not higher than renal sinus) in 10%. Small RCCs ( 3cm) tended to be relatively homogeneous in echogenicity and ranged from grade II to III echogenicity. RCCs with a size between 3cm and 5 cm were relatively heterogeneous in echogenicity and had grade II to IV echogenicity. RCCs sized between 5cm and 7cm were frequently complex masses. RCCs with grade IV echogenicity were rare (10%), and cystic RCCs were noted in 4% of the patients. US is a cost-effective, easily available, portable, and non-radiating examination for kidneys. It can be used as a screening modality for renal cancer. In patients with inconclusive US imaging finding or clinically high suspicion of focal renal tumor, CT, MRI, or even angiography should be utilized as complementary diagnostic modalities. Renal cell carcinoma (RCC) or renal adenocarcinoma represents the third most common genitourinary neoplasm in adults. Although the ultrasonographic appearances of RCC were frequently reported before 1990 [1], there have been limited reports regarding the high-resolution sonographic findings of RCC in recent 10 years. More and more small-sized renal neoplasms were detected incidentally during routine upper abdomen ultrasonography (US). The relationship between tumor size and US presentation among patients with RCC still needs to be elucidated. The aim of this study was to analyze the link between echopatterns and tumor size of RCCs. Materials and Methods In 5-year period, a total of 78 patients found to have renal masses by US study and pathologically

2 178 Renal cell carcinoma Table 1. Grading of tumor echogenicity among 78 patients with renal cell carcinoma Grade Description of echogenicity No. (%) I renal medulla 4 5% II renal cortex and > medulla 27 35% III liver / spleen and > cortex 39 50% IV renal sinus and > liver/spleen 8 10% V > renal sinus 0 0% proved to be RCCs were included in this retrospective study. They included 68 men and 10 women ranging with age from 30 to 87 years (mean 67.3 years). Some of them (35/78, 45%) were incidentally discovered to have RCC during US study for health check-up (n= 30) or survey for abnormal liver function (n= 5). All 78 patients subsequently underwent surgical treatment (n= 66) and/or biopsy (n= 12) after receiving other imaging studies including computed tomography (CT) (n= 77) and angiography (n= 1). We reviewed the US studies to clarify the relationship between the echopatterns and tumor sizes of RCC. The echogenicity of the tumors was graded from I through V as compared to the echogenicity of the renal medulla, renal cortex, liver/spleen and renal sinus (Table 1). U lt r a s o n og r a p h ic s t u d y w a s p e r fo r m e d using the following real-time scanners: DRF 400 (Diasonics, Milpita, CA, USA), UM8 (Advanced Technology Laboratories, Bothell, WA, USA), XP 10 (Acuson, MountainView, CA, USA), UM9 (Advanced Technology Laboratories, Bothell, WA, USA), VST (Diasonics, Milpita, CA, USA), GP 8500 (Hewlette-Packard, Andover, MA, USA), HDI 3000 (Advanced Technology Laboratories, Bothell, WA, USA), and Sequoia (Acuson, MountainView, CA, USA). Transducers from 3.0 to 5.0-MHz (most commonly 3.5 MHz) were used. Routine US scan of the kidneys included coronal, sagittal and transverse scans. The size, shape and outline of the kidneys were recorded. The sonographic appearances of the renal pathologies were documented with hard copies. Results Most RCCs were presented as solid masses (n= 33, 42%) or complex masses (n= 42, 54%). Only 3 patients were presented with cystic masses (4%). Grade I echogenicity (not higher than renal medulla) was noted in only 5% of renal tumors, grade II (higher than medulla but not higher than renal cortex) in 35%, grade III (higher than cortex but not 1a 1b Figure 1. A 66-year-old male: a. A round solid nodule, not larger than 3 cm, showing homogeneous echogenicity in US (arrow). b. Mild enhancement in the tumor (arrow) was noted on contrast-enhanced CT study.

3 Renal cell carcinoma 179 Table 2. Sonographic manifestations of 78 patients with renal cell carcinoma Tumor Echogenicity Homogeneity Shape Size (cm) Grade I ~ V Regular Round Ovoid Irregular 2.0 ~ 3.0 II ~ III 100 % ~ 4.0 II ~ III 60 % ~ 5.0 II ~ IV 60 % ~ 6.0 I ~ III 43 % ~ 7.0 I ~ IV 42 % > 7 I ~ IV 13 % Total 42% a 2b Figure 2. An 80-year-old male: a. A round mass, 3-4 cm in size, was detected (arrow) with presence of complex heterogeneous echogenicity at lower pole of right kidney. b. Color Doppler sonography revealed the presence of marginal color flow signals (arrows). higher than liver/spleen) in 50%, and grade IV (not higher than renal sinus) in 10%. None had an echogenicity greater than renal sinus (Grade V) (Table 1). Tumors less than 5 cm in size were commonly round and ovoid in shape (24/29, 83%)(Fig. 1, 2). However, when the tumor size was greater than 5 cm, the tumors were most commonly irregular in shape (40/49, 82%) (Fig. 3~5). Tumors less than 5 cm in size were most commonly homogeneous in echopattern, while tumors larger than 5 cm were frequently heterogeneous in echopattern (Fig. 6, 7). Most of the tumors in this study were of Grade III echogenicity (n= 39, 50%). In tumors larger than 5 cm, calcifications might be detected in US study (Fig. 6, 7). However, the correlation between the echogenicity grading and the tumor size was not statistically significant (P> 0.05) (Table 2). Discussion The typical clinical manifestations of RCC include hematuria, palpable renal mass, and flank pain. However, in our study, 45% (35/78) of the RCCs were incidental findings. It was consistent with the previous study, which revealed that 15-48% of patients with RCC presented with no clinical symptoms or signs [2]. Since the development of the gray-scale real time US and CT, evaluations of focal renal pathology have been shifted to these crosssectional tomographic techniques from the previously widely used intravenous urography. US is a well-accepted imaging modality in the evaluation of intra-abdominal organs. The advantages of US study include real-time imaging, noninvasiveness, no ionizing radiation, high portability, and relatively low

4 180 Renal cell carcinoma Figure 3. A 42-year-old female: US revealed a round mass, 4-5 cm in size, with complex heterogeneous echogenicity at upper pole of left kidney (arrow) with hypoechoic rim and a central hypoechoic area, representing central necrosis or hemorrhage. Figure 4. A 74-year-old male: A mass with irregular border, 5-7 cm in size, was evident with complex heterogeneous echogenicity with a mural nodule (arrow). 5a Figure 5. A 50-year-old male: a. A solid mass with irregular border, 5-7 cm in size, was noted with heterogeneous echogenicity in left kidney (large arrow) with renal vein thrombosis (small arrow). b. Contrast-enhanced CT further revealed contrast enhancement of tumor (large arrow) with left renal vein thrombosis (small arrow). 5b Figure 6. A 57-year-old male: A mass with irregular border, 7 cm in size, was depicted on US (large arrows). The lesion was associated with complex heterogeneous echogenicity and some calcifications (small arrows). Figure 7. A 42-year-old male: US revealed a renal mass with irregular border, 7 cm in size, associated with complex heterogeneous echogenicity and ring-like calcification (arrows).

5 Renal cell carcinoma 181 cost. Although patients referred for abdominal US study usually have certain clinical symptoms, more and more patients received upper abdominal US study as a routine health check up in recent years in Taiwan [3]. The high prevalence of RCC as an incidental finding of US examinations thus prove the excellent utility of US in screening for RCC. The characteristic sonographic findings of a RCC are a solid, well-defined mass with various echogenicity patterns. The echo texture can be heterogeneous, especially when necrosis or bleeding occurs. In about 20% of the cases, the masses are highly reflective and thus difficult to be differentiated from angiomyolipoma [4]. In children, the RCCs can appear as hypoechoic (35%), isoechoic (44%), or hyperechoic (21%) intrarenal masses [5-7]. The average diameter of the tumor at the time of diagnosis is 4 cm. The sensitivity of US in detecting a solid renal mass with diameter between 1 to 2 cm is approximately 65%, which increases to 85% in those between 2 to 3 cm [4]. Calcifications occur in about 10-25% of tumors, appearing as echogenic foci and usually located within the intrarenal mass. When tumor spreads into retroperitoneum and lymph nodes or invades the renal vein, sonography can be helpful to identify the extrarenal pathologies [8, 9]. Although US can detect RCC and venous invasion, it is not as sensitive as CT or MRI in assessing extracapsular extension of tumor, lymph node involvement, and contralateral tumors. Familiarity with the US pattern of relatively small RCCs is important for physicians operating the US study. US is a useful tool for the detection of incidental RCC. Improvement in the overall survival rate of incidental RCC patients implies that early detection results in better prognosis [2]. In RCCs there may be small anechoic areas with various distal acoustic enhancement, which correspond to intra-tumoral cysts or cystic necrosis at histologic evaluations. On the contrary, the anechoic areas indicative of cysts are rarely found in angiomyolipomas. Therefore, demonstration of an anechoic rim and/or intra-tumoral cysts in a hyperechoic mass at US suggests the diagnosis of RCC [10, 11]. The US features of cystic renal masses can be categorized according to the classification scheme proposed by Bosniak [12]. Cystic renal masses are frequently undetermined by US and CT study, whereas hemorrhagic contents are more commonly demonstrated on magnetic resonance imaging (MRI) [13, 14]. The typical pattern of internal hemorrhage on MRI is usually high signal on both T1- and T2-weighted sequences. CT scan and/or direct surgical intervention are required to assess any cystic lesions that deviate from a typical simple cyst on US. Moreover, indeterminate multilocular lesions on CT scan should be surgically explored [15]. Computerized tomography scan is currently the standard modality for staging of urologic cancer in most institutions. It is used for demonstrating nodal involvement and invasion of the primary lesion into surrounding fat, muscle, and other tissue or organs. It is also useful for disclosing hepatic metastases from renal and urinary tract carcinomas [16]. Ultrasonography is particularly valuable in assessing masses that are indeterminate on CT when enhancement is equivocal or when intravenous contrast medium cannot be administered [17]. Duplex Doppler US may be as accurate as CT scanning in the staging of RCC [18]. Furthermore, in patients with renal vein or caval thrombi, color and duplex Doppler US is highly accurate (87%) in establishing the diagnosis and in determining the extent of the thrombosis [19]. Fine needle aspiration of focal renal pathology can also provide an accurate diagnosis in most renal tumors; however, aspiration cytology of the kidney has limitations and pitfalls. Low grade RCC has to be differentiated from oncocytoma, angiomyolipoma, renal infarct and related conditions. Nevertheless, renal fine needle aspiration has a high negative predictive value, which is useful in reassuring patient with radiologically and cytologically benign lesions. Negative fine needle aspiration does not exclude malignancy in the presence of a suspicious image finding [20]. The majority of RCCs are tumors of clear cell or granular cell type. They are characterized by prominent neovascularity and have the tendency to invade renal veins, inferior vena cava, and the right atrium with a frequency of 20%, 10%, and 2%, respectively. The presence and location of venous tumor thrombus are of great importance in surgical decision-making [21]. Ultrasonographic evaluation of renal veins and inferior vena cava in the presence of focal renal mass should be done as a routine procedure [10, 19]. Although US study is an effective screening tool for the detection of renal tumors, especially cystic lesions and grade V masses, it is noteworthy that CT remains the most widely available and most effective modality for tumor staging. Other more advanced and/or invasive diagnostic modalities, such as MRI, angiography, and biopsy may also be required to rule out renal pseudotumors (e.g. column

6 182 Renal cell carcinoma of Bertin hypertrophy, fetal lobation). In conclusion, small RCCs ( 3cm) tended to be relatively homogeneous in US imaging with the echogenicity ranging from grade II to III. Renal cell carcinomas with a size between 3cm and 5cm were relatively heterogeneous with grade II to IV echogenicity, whereas RCCs sized between 5cm and 7 cm were frequently complex masses. Grade IV RCCs were rare (10%), and cystic RCCs were noted in 4% of the patients. Ultrasonography is a cost-effective, easily available, portable and non-radiating tool that can be used as an effective screening modality. In patients with inconclusive US imaging findings or clinically high suspicion of focal renal tumor, CT, MRI, or even angiography should be utilized as complementary diagnostic modalities. References 1. Porena M, Vespasiani G, Rosi P, et al. Incidentally detected renal cell carcinoma: role of ultrasonography. J Clin Ultrasound 1992; 20: Ou YC, Yang CR, Kuo JH, Kao YL. Cheng CL. Incidental renal cell carcinoma: pathologic features and survival rate. Chin J Med 1998; 61: Chen YF, Li YW, Sheih CP, Hsu CY. Renal cell carcinoma: unusual pediatric renal tumors. J Formos Med Assoc 1999; 98: Rossi MC. The kidneys and adrenal glands. In Goldberg BB, Petersons H (eds): Ultrasonography. Oslo: the Nicer Institute ISIS Medical Media 1996; Nieder AM, Taneja SS. The role of partial nephrectomy for renal cell carcinoma in contemporary practice. Urol Clin North Am 2003; 30: Chan HSL, Danemen A, Gribbin M, Martin DJ. Renal cell carcinoma in the first decades of life. Pediatr Radiol 1983; 13: Kabala JE, Shield J, Duncan A. Renal cell carcinoma in childhood. Pediatr Radiol 1992; 22: Webb JAW, Murray A, Bary PR, Hendry WF. The accuracy and limitations of ultrasound in the assessment of venous extension in renal carcinoma. Br J Urol 1987; 60: Ramos IM, Taylor KJW, Kier R et al. Tumor vascular signals in renal masses: detection with Doppler US. Radiology 1988; 168: Yamashita Y, Ueno S, Makita O, et al. Hyperechoic renal tumors: anechoic rim and intratumoral cysts in US differentiation of renal cell carcinoma from angiomyolipoma. Radiology 1993; 188: Siegel CL, Middleton WD, Teefey SA, McClennan BL. Angiomyolipoma and renal cell carcinoma: US differentiation. Radiology 1996; 198: Bosniak MA. The current radiological approach to renal cysts. Radiology 1986; 158: Murray JG, Eustace S, Breatnach E, Stack JP.MR diagnosis of haemorrhagic cystic renal cell carcinoma. J Comput Assist Tomogr 1994; 18: Hilpert PL, Friedman AC, Radecki PD, et al. MRI of hemorrhagic renal cysts in polycystic kidney disease. AJR Am J Roentgenol 1986; 146: Ooi GC, Sagar G, Lynch D, Arkell DG. Ryan PG. Cystic renal cell carcinoma: radiological features and clinico-pathological correlation. Clin Radiol 1996; 51: Friedland GW. Staging of genitourinary cancers: the role of diagnostic imaging. Cancer 1987; 60: Foster WL Jr., Roberts L Jr., Halvorsen RA Jr., Dunnick NR. Sonography of small renal masses with indeterminate density characteristics on computed tomography. Urol Radiol 1988; 10: Bos SD. Mensink HJ. Can duplex Doppler ultrasound replace computerized tomography in staging patients with renal cell carcinoma? Scand J Urol Nephrol 1998; 32: Habboub HK, Abu-Yousef MM, Williams RD, See WA. Schweiger GD. Accuracy of color Doppler sonography in assessing venous thrombus extension in renal cell carcinoma. AJR Am J Roentgenol 1997; 168: Zardawi IM. Renal fine needle aspiration cytology. Acta Cytol 1999; 43: Nguyen BD. Westra WH. Zerhouni EA. Renal cell carcinoma and tumor thrombus neovascularity: MR demonstration with pathologic correlation. Abdom Imaging 1996; 21:

7 Renal cell carcinoma 183 腎細胞癌在超音波的表現 :78 名案例之回顧 楊境亦 1, 刁翠美 周宜宏 王信凱 邱宏仁 王家槐 丘思穎 許明輝 張政彥 陳光國 3,4 于俊 1 行政院衛生署基隆醫院放射線科 2 台北榮民總醫院放射線部外科部 4 國立陽明大學醫學院 3 腎細胞癌是成人最常見的腎臟惡性腫塊 絕大多數的腎臟, 皆可利用即時性高解像力超音波作檢查 為歸納腎細胞癌超音波表現的徵象, 我們回顧 78 例曾接受超音波檢查, 並經病理證實為腎細胞癌的患者 在 5 年中, 總共收集了 78 例經上腹部超音波檢查發現腎臟腫塊, 隨後並接受手術或切片檢查的病患 組織病理學檢驗證實這些病患皆有腎細胞癌 其中 35 名病患屬於無臨床症狀, 但於例行超音波檢查中意外發現有腎臟腫瘤者 我們回顧相關超音波檢查結果, 分析超音波型態與腫瘤大小的關係 病灶的回音強度在與腎臟髓質 腎臟皮質 肝臟或脾臟 和腎竇比較後, 依序分為一至五級 大多數腎細胞癌呈現實質性腫塊 (33 例,42%) 或複合性腫塊 (42 例,54%); 僅有 3 例呈現囊性腫塊 (4%) 第一級回音強度 ( 不高於腎臟髓質 ) 在所有腫瘤中佔 5%; 第二級回音強度 ( 高於腎臟髓質, 但不高於腎臟皮質 ) 佔 35%; 第三級回音強度 ( 高於腎臟皮質, 但不高於肝臟或脾臟 ) 佔 50%; 第四級回音強度 ( 高於肝臟或脾臟, 但不高於腎竇 ) 佔 10% 較小 ( 小於或等於 3 公分 ) 的腎細胞癌相對而言多呈現同質性 (homogeneous), 且回音強度範圍多在第二至第三級之間 3-5 公分的腎細胞癌呈現相對的異質性 (heterogeneous), 且回音強度多在第二至第四級之間 至於 5-7 公分的腎細胞癌, 則經常表現為複合性腫塊 第四級回音強度的腎細胞癌少見 ( 佔 10%), 囊性腎細胞癌則僅只佔 4% 超音波檢查係具經濟效益 容易取得 可攜帶 且沒有游離輻射, 並可作為篩檢腎臟癌症的檢查方式 對於超音波檢查後沒有定論的患者, 或是臨床上高度懷疑局部腎臟腫瘤者, 電腦斷層掃描, 磁振造影檢查, 或是甚至血管攝影檢查, 則可用來作為補足的診斷檢查