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AJR 2001; 177:653-658
© American Roentgen Ray Society


Pictorial Essay

Patterns of Recurrence in Renal Cell Carcinoma

Manifestations on Helical CT

John C. Scatarige1, Sheila Sheth, Frank M. Corl and Elliot K. Fishman

1 All authors: Russell H. Morgan Department of Radiology and Radiological Science, The Johns Hopkins Hospital, Baltimore, MD 21287.

Received December 22, 2000; accepted after revision January 30, 2001.

 
Address correspondence to E. K. Fishman, Department of Radiology, The Johns Hopkins Hospital, 601 N. Caroline St., JHOC Rm. 3254, Baltimore, MD 21287-0801.


Introduction
Top
Introduction
Clinical Features of Recurrent...
Helical CT Technique
Common Patterns of Recurrence...
Atypical Manifestations
Conclusion
References
 
Helical CT is invaluable in characterizing renal masses and in the preoperative staging of patients with suspected renal cell carcinoma. Equally important, however, is the role of CT in monitoring patients with renal cell carcinoma after nephrectomy. The accurate detection of recurrent disease provides key prognostic information and assists the oncologist in making treatment decisions involving either surgery or immunotherapy [1].

In this pictorial essay, we review some important clinical aspects of renal cell carcinoma, briefly discuss CT technique, and illustrate some common as well as atypical manifestations of renal cell carcinoma metastasis that may be encountered on postoperative CT surveillance.


Clinical Features of Recurrent Renal Cell Carcinoma
Top
Introduction
Clinical Features of Recurrent...
Helical CT Technique
Common Patterns of Recurrence...
Atypical Manifestations
Conclusion
References
 
Knowledge of the mechanisms, risk factors, and clinical timing of recurrent disease in surgically treated renal cell carcinoma can assist the radiologist in understanding the patterns of recurrence observed on imaging.

Frequency and Mechanisms of Recurrence
Local recurrence occurs in about 5% of patients. It is associated with incomplete resection of the primary tumor, positive surgical margins, and regional lymph node metastasis [2]. Distant metastases are present at the time of diagnosis in up to 30% of patients [1]. Among those with localized disease who are treated surgically, 20-30% will eventually develop distant metastasis [1, 3].

Dissemination occurs via lymphatic and hematogenous routes. Retrograde collateral flow via the lumbar veins into the vertebral plexuses of Batson appears to be particularly important in metastasis to the axial skeleton and the brain [4].

Risk Factors for Recurrence
The surgical stage of renal cell carcinoma at the time of diagnosis is the most important determinant in predicting local recurrence or distant metastasis. Large tumors that invade locally or propagate as venous tumor thrombus have higher rates of distant metastasis [1]. Regional lymph node metastases, a high Fuhrman grade on histopathology, and spindled (sarcomatoid) tumor architecture also adversely influence prognosis [1, 5, 6].

Timing of Recurrence and Metastasis
Distant metastases or local recurrence or both usually occur within the first 6 years after surgery [2, 5]. Patients with positive nodes at surgery relapse even sooner, generally within 3 years [2]. Late recurrence is a distinctive clinical aspect of renal cancer, observed in as many as 11% of patients surviving 10 years or more after surgery [3].


Helical CT Technique
Top
Introduction
Clinical Features of Recurrent...
Helical CT Technique
Common Patterns of Recurrence...
Atypical Manifestations
Conclusion
References
 
Like the primary tumor, local recurrences and metastases are highly vascular. Therefore, arterial phase scanning is essential for maximizing lesion conspicuity. To facilitate detection of vascular liver metastases, the abdomen and pelvis are scanned first, from the diaphragm to the symphysis pubis, during the arterial phase of enhancement. Next, the chest is imaged from the lung apices through the liver and remaining kidney. Because these patients, as well as those with familial renal carcinoma or von Hippel-Lindau disease, are at increased risk for additional renal primary carcinomas, the remaining kidney must be carefully scrutinized on each follow-up CT.

Retroperitoneal anatomy is significantly altered after nephrectomy (Fig. 1A,1B,1C). Small bowel and colon may migrate into the nephrectomy fossa. To help differentiate nonopacified bowel from local recurrence, we routinely administer 750 mL of oral contrast material 45-60 min before scanning.



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Fig. 1A. Normal and surgically altered retroperitoneum. Sm. bowel = small bowel, Duo. II = second portion of duodenum, Rt. K = right kidney, Lft. K = left kidney, Q. lumborum = quadratus lumborum. Drawing shows normal retroperitoneum.

 


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Fig. 1B. Normal and surgically altered retroperitoneum. Sm. bowel = small bowel, Duo. II = second portion of duodenum, Rt. K = right kidney, Lft. K = left kidney, Q. lumborum = quadratus lumborum. Drawing shows that after right nephrectomy, right colon and right hepatic lobe occupy renal fossa. Second portion of duodenum and pancreatic head may assume more posterolateral position.

 


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Fig. 1C. Normal and surgically altered retroperitoneum. Sm. bowel = small bowel, Duo. II = second portion of duodenum, Rt. K = right kidney, Lft. K = left kidney, Q. lumborum = quadratus lumborum. Drawing shows that after left nephrectomy, pancreatic tail assumes a more posterior position, approaching quadratus lumborum. Spleen shifts posteromedially. Caudal to pancreas, proximal jejunum and descending colon fill left renal fossa.

 


Common Patterns of Recurrence Revealed on CT
Top
Introduction
Clinical Features of Recurrent...
Helical CT Technique
Common Patterns of Recurrence...
Atypical Manifestations
Conclusion
References
 
Local Recurrence in Renal Fossa
After nephrectomy, recurrent renal carcinoma appears as an enhancing mass in the surgical site. The recurrence often involves the quadratus lumborum and psoas muscles (Figs. 2A and 2B), and can displace or invade nearby structures. The cephalic extent may reach the adrenal bed (Fig. 2C) or may involve the ipsilateral adrenal gland if the latter was spared at the time of nephrectomy. Recurrent cancer after nephron-sparing surgery can be suggested when an enhancing nodule develops in the wedge-shaped partial nephrectomy defect.



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Fig. 2A. Locally recurrent renal cell carcinoma as seen in contrast-enhanced helical CT. CT scan of 46-year-old man with recurrent renal cell carcinoma who underwent left nephrectomy reveals enhancing mass (arrow) that invaded left psoas and quadratus lumborum muscles.

 


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Fig. 2B. Locally recurrent renal cell carcinoma as seen in contrast-enhanced helical CT. CT scan of 41-year-old woman with recurrent renal cell carcinoma in left renal fossa shows enhancing mass (arrow) anteriorly displacing pancreatic tail. Note adult polycystic kidney disease.

 


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Fig. 2C. Locally recurrent renal cell carcinoma as seen in contrast-enhanced helical CT. CT scan of 59-year-old man who underwent right radical nephrectomy for renal cell carcinoma several years earlier and who presented with back pain shows heterogenously enhancing recurrent tumor (arrows) in right adrenal bed.

 

Regional Lymphadenopathy
Lymph nodes close to the renal vascular pedicle are the most frequently involved [4] (Fig. 3) and represent an important predictor for multifocal distant metastasis [6].



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Fig. 3. 58-year-old man with left paraaortic lymphadenopathy occurring several years after left nephrectomy. Contrast-enhanced helical CT scan shows recurrent tumor (arrow) with peripheral contrast enhancement. Diagnosis was confirmed by imaging-guided percutaneous biopsy.

 

Distant Metastases
Renal carcinoma typically metastasizes to the following distant sites, listed in order of descending frequency: lung (Figs. 4 and 5) and mediastinum, bone (Fig. 6A,6B), liver (Figs. 7 and 8A,8B), contralateral kidney or adrenal gland or both (Fig. 9), and brain [6, 7]. Multifocal metastases are common. Pulmonary metastases occur in 50-60% of patients with distant disease [1]. These metastases may be hemorrhagic or involve the interstitial lymphatics (Figs. 4 and 5). Bone metastases are lytic, are expansile, and favor the axial skeleton, particularly from T12 to the pelvis [4] (Fig. 6A,6B).



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Fig. 4. 64-year-old man who underwent right nephrectomy for renal cell carcinoma and developed cough and hemoptysis. He was afebrile, and results of coagulation studies were normal. Contrast-enhanced helical CT scan shows bilateral lower lobe metastases and left lower lobe air-space opacity near largest mass. Air-space process rapidly and completely resolved, indicating spontaneous hemorrhage. Note left coronary artery calcification.

 


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Fig. 5. 60-year-old man with advanced right renal cell carcinoma. Contrast-enhanced helical CT scan shows thickened, nodular interlobular septae forming polygonal arcades (arrow) in right lower lobe close to right hemidiaphragm, indicating lymphangitic carcinomatosis. Subcarinal and retroperitoneal nodal metastases were evident on other images.

 


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Fig. 6A. Bone metastasis in renal cell carcinoma. Contrast-enhanced helical CT scan displayed at bone window settings in 55-year-old man who underwent prior nephrectomy for renal cell carcinoma, and who presented with diffuse bone pain, shows expansile lytic metastases (arrows) in sacrum and ilia.

 


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Fig. 6B. Bone metastasis in renal cell carcinoma. Contrast-enhanced helical CT scan in 59-year-old man who underwent left nephrectomy for renal cell carcinoma, and who presented with back pain and weakness, reveals enhancing lytic metastasis (arrow) of left T12 pedicle with spinal canal encroachment. Patient was treated with surgery.

 


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Fig. 7. 57-year-old man with widely metastatic renal cell carcinoma. Contrast-enhanced helical CT scan shows innumerable hypervascular liver metastases. Note right pleural effusion.

 


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Fig. 8A. 72-year-old man with solitary liver metastasis 3 years after left radical nephrectomy for renal cell carcinoma. Case emphasizes importance of arterial phase imaging in detecting renal cell carcinoma metastatic to liver. (Reprinted with permission from [9]) Contrast-enhanced helical CT scan during arterial phase reveals markedly hypervascular mass (arrow) in medial segment of left lobe that indents gallbladder.

 


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Fig. 8B. 72-year-old man with solitary liver metastasis 3 years after left radical nephrectomy for renal cell carcinoma. Case emphasizes importance of arterial phase imaging in detecting renal cell carcinoma metastatic to liver. (Reprinted with permission from [9]) Contrast-enhanced helical CT scan during portal venous phase obtained 63 sec after A shows mass (arrow) to be nearly isodense compared with normal liver. Metastasis was confirmed at surgery.

 


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Fig. 9. 69-year-old man who underwent right nephrectomy for renal cell carcinoma 3 years earlier. Contrast-enhanced helical CT scan shows multiple masses in left kidney and left adrenal gland (arrow). Because renal lesions appeared synchronously on serial CT scans with adrenal mass and pulmonary mass (not shown), they were thought to represent metastases.

 


Atypical Manifestations
Top
Introduction
Clinical Features of Recurrent...
Helical CT Technique
Common Patterns of Recurrence...
Atypical Manifestations
Conclusion
References
 
Metastases occurring in unusual sites or developing many years after nephrectomy are being recognized more frequently. An accurate diagnosis is important because some isolated recurrences can be cured with surgical excision.

Late Metastasis
Metastasis discovered 10 years or more after surgery is a well-recognized clinical peculiarity [3]. Lung, pancreas, bone, skeletal muscle, and bowel are the most frequent sites for metastases [3, 7] (Fig. 10). Surgical treatment is often warranted.



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Fig. 10. 85-year-old woman who complained of left scapular pain 10 years after nephrectomy for renal carcinoma. Contrast-enhanced helical CT scan shows enhancing mass (arrow) involving scapular spine. No other metastases were evident. Diagnosis was established at open biopsy.

 

Pancreatic Metastasis
Metastases to the pancreas may be solitary or multiple and may occur many years after nephrectomy [8]. In contrast to primary ductal pancreatic adenocarcinoma, pancreatic metastases from renal cell carcinoma are hypervascular (Fig. 11A,11B). Surgical resection can improve the likelihood of patient survival [8].



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Fig. 11A. Renal cell carcinoma metastatic to pancreas. Arterial phase contrast-enhanced CT scan in 63-year-old man who underwent left nephrectomy for renal carcinoma 7 years earlier shows enhancing mass (arrow) in tail of pancreas. Note surgical clips in left renal fossa. Solitary metastasis was confirmed on subsequent distal pancreatectomy. (Reprinted from [10])

 


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Fig. 11B. Renal cell carcinoma metastatic to pancreas. Contrast-enhanced helical CT scan of 54-year-old man with previously resected left renal carcinoma who presented with palpable mass in right upper quadrant reveals large hypervascular mass (curved arrows) in head of pancreas, which, at endoscopy, was noted to have invaded second portion of duodenum. Numerous smaller metastases were present in pancreatic body and tail. CT scan also shows collateral vein (straight arrow) resulting from splenic vein obstruction by mass.

 

Endobronchial Metastasis
These uncommon lesions can be detected incidentally or are discovered on imaging or bronchoscopy in patients presenting with hemoptysis or atelectasis (Fig. 12).



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Fig. 12. 75-year-old man with history of renal cell carcinoma metastatic to lungs. Contrast-enhanced helical CT scan displayed at lung window setting reveals unsuspected endobronchial nodule (arrows) in bronchus intermedius. Other lower lobe metastases are present.

 

Skeletal Muscle Metastasis
Most skeletal muscle metastases detected on helical CT are asymptomatic and occur in patients with advanced disease. These metastases tend to enhance uniformly. The erector spinae muscle is a favored site for skeletal muscle metastases (Fig. 13).



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Fig. 13. 59-year-old man who had known lung and brain metastases from renal cell carcinoma 2 years after right radical nephrectomy. Contrast-enhanced helical CT scan shows uniformly enhancing metastasis (arrow) in right erector spinae muscle. Mass was palpable but not tender.

 

Peritoneal and Bowel Metastases
Locally recurrent renal carcinoma may directly invade the ascending or descending colon. More advanced patterns of recurrence include peritoneal carcinomatosis and mesenteric lymphadenopathy (Fig. 14). Metastases to the small bowel may produce gastrointestinal hemorrhage or intussusception (Fig. 15A,15B).



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Fig. 14. 45-year-old woman who underwent right radical nephrectomy for renal cell carcinoma 4 months earlier and complained of persistent nausea. Contrast-enhanced helical CT scan shows extensive enhancing mesenteric and paraaortic metastases (arrows). Note surgical clips in right renal fossa.

 


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Fig. 15A. Renal cell carcinoma metastatic to small bowel. Unenhanced helical CT scan of 67-year-old man who had upper gastrointestinal bleeding, emesis, and renal insufficiency 6 years after right nephrectomy shows intraluminal mass (arrow) in second portion of duodenum. Endoscopic biopsy confirmed metastasis from renal cell carcinoma. Treatment was pancreaticoduodenectomy.

 


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Fig. 15B. Renal cell carcinoma metastatic to small bowel. Contrast-enhanced helical CT scan of 44-year-old man who had prior resection of large right renal tumor and who had symptoms of intestinal obstruction reveals two small bowel metastases (arrows), the larger representing lead point of ileocolic intussusception. Both lesions, as well as omental and mesenteric metastases, were confirmed at surgery.

 


Conclusion
Top
Introduction
Clinical Features of Recurrent...
Helical CT Technique
Common Patterns of Recurrence...
Atypical Manifestations
Conclusion
References
 
The clinical course of renal cell carcinoma after nephrectomy is variable and unpredictable. Contrast-enhanced helical CT is the ideal modality for conducting postoperative surveillance in patients at risk for recurrent or metastatic disease. Optimum care is rendered to these patients when radiologists understand the unique clinical features of this neoplasm and are familiar with the common and the atypical manifestations of recurrent disease.


References
Top
Introduction
Clinical Features of Recurrent...
Helical CT Technique
Common Patterns of Recurrence...
Atypical Manifestations
Conclusion
References
 

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  2. Rabinovitch RA, Zelefsky MJ, Gaynor JJ, Fuks Z. Patterns of failure following surgical resection of renal cell carcinoma: implications for adjuvant local and systemic therapy. J Clin Oncol 1994;12:206 -212[Abstract]
  3. Newmark JR, Newmark GM, Epstein JI, Marshall FF. Solitary late recurrence of renal cell carcinoma. Urology 1994;43:725 -728[Medline]
  4. Arkless R. Renal carcinoma: how it metastasizes. Radiology 1965;84:496 -501
  5. Saidi JA, Newhouse JH, Sawczuk IS. Radiologic follow-up of patients with T1-3a, b, c or T4N+M0 renal cell carcinoma after radical nephrectomy. Urology 1998;52:1000 -1003[Medline]
  6. Johnsen JA, Hellsten S. Lymphatogenous spread of renal cell carcinoma: an autopsy study. J Urol 1997;157:450 -453[Medline]
  7. Saitoh H, Nakayama M, Nakamura K, Satoh T. Distant metastasis of renal adenocarcinoma in nephrectomized cases. J Urol 1982;127:1092 -1095[Medline]
  8. Ghavamian R, Klein KA, Stephens DH, et al. Renal cell carcinoma metastatic to the pancreas: clinical and radiological features. Mayo Clin Proc 2000;75:581 -585[Medline]
  9. Shirkhoda A, ed. Variants and pitfalls in body imaging. Philadelphia: Lippincott Williams & Wilkins, 2000: 201
  10. Scatarige JC, Horton KM, Sheth S, Fishman EK. Pancreatic parenchymal metastasis. AJR 2001;176:695 -699[Free Full Text]

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