Skeletal Radiol (1992) 21:56-59
Skeletal Radiology
Case report 708 Peter L. Munk, M.D. 1 *, Stephen Gock, M.D. 2, Richard Gee, M.D. 2, Douglas G. Connell, M.D. 1, and Noel F. Quenville, M.D. 3 Departments of 1 Radiology and 3 Pathology, University of British Columbia and Vancouver General Hospital Vancouver, British Columbia, Canada; and 2 University of Auckland, Auckland, New Zealand
Figs. 1 and 2. See next page for corresponding legends 9 1992 International Skeletal Society
P.L. Munk et al. : Case report 708
57
Fig. 1. Contrast enhanced computed tomography (CT) scan, 5-mm thick, through the top of the right shoulder demonstrates an enhancing soft-tissue mass with lobulated contours (arrows) within skeletal muscle (probably trapezius) Fig. 2A-E. Magnetic resonance imaging (MRI) right shoulder. A A 5-ram Tl-weighted (TR 800 ms/TE 30 ms) axial image shows the lesion to be of slightly greater signal than adjacent muscle. B, C, D Coronal images 5-mm thick. Tl-weighted (TR 600 ms/TE 30 ms) proton density and T2-weighted (TR 2000ms/TE 30 and 80 ms) show increased signal within the lesion (arrows) relative to skeletal muscle as T2 weighting is augmented. Note the slightly reticular texture of the lesion. E A 5-mm thick sagittal gradient recall image (TR 600 ms/TE 20 ms, 0 = 25~ demonstrates a ring of high signal around the lesion (arrows) Fig. 3A, B. Subclavian angiogram demonstrating an intensely vascular lesion, A early phase and B late arterial phase
Clinical information A 57-year-old man with a history of a right radical nephrectomy for renal cell carcinoma J0 months previously presented with a 2-month history of a mass in his right shoulder. The mass was first noticed by the patient's wife and was slightly painful when lifting and performing " p u s h ups". Family history indicated that
* Present address: Department of Radiology, University Hospital, University of Western Ontario; London, Ontario, Canada Address reprint requests to . Peter L. Munk,
M.D., Department of Radiology, University Hospital, University of Western Ontario, 339 Windermere Road, PO Box 5339, London, Ontario, Canada N6A 5A5
three siblings had also undergone nephrectomy, but the diagnosis in each case was unclear. On examination, positive physical findings consisted of a solitary, firm, 4 x 3 cm mass of the right shoulder proximal and posterior to the acromioclavicular joint. The mass was nontender and appeared to be superficial. The remainder of the physical examination was grossly normal. Hematological studies were normal. Serum biochemical studies revealed an elevated creatinine of 127 gmol/1 and potassium of 54 retool/1. Contrast-enhanced CT demonstrated an enhancing mass with lobulated contours restricted to skeletal muscle, its epicenter in the right tra-
pezius (Fig. 1). M R showed the lesion to be of low signal on T1weighted sequences and high signal with T2-weighting (Fig. 2). The lesion had a slightly reticulated texture and revealed changes suggestive o f edema in the surrounding tissues. Angiography, performed to embolize the mass to facilitate surgery, demonstrated intense vascularity (Fig. 3). CT scans of the chest, abdomen, and pelvis were normal, as were abdominal ultrasound and whole-body bone scintigraphy results (apart from transient increased uptake in the lesion in the soft-tissue phase of the scan). The day following embolization a wide excision of the mass was performed.
58
Diagnosis: Metastasis of renal cell carcinoma to skeletal muscle (right trapezius) The tumor involving the skeletal muscle, fascia and connective tissue measured 7 x 4 cm. It had a multinodular, focally necrotic, and hemorrhagic appearance on the cut surface, involved skeletal muscle and fascia, and demonstrated associated, multiple, dilated vascular channels containing thrombotic-appearing material. Histological sections showed extensive tumor thrombi within dilated veins and lymphatics, expanding the vascular lumens and infiltrating through the vessel walls into the surrounding fascia, connective tissue, and skeletal muscle (Fig. 4). The overall appearance was in keeping with extensive intravascular metastases. The morphological features were those of a relatively low-grade renal cell carcinoma, resembling the low-grade component of the renal cell carcinoma in the nephrectomy specimen previously removed. Of interest, the primary renal cell tumor was composed of equal parts of a low-grade clear cell type and high-
P.L. M u n k et al. : Case report 708
grade granular cell renal carcinoma, with the low-grade component presenting as the metastasis.
Discussion Renal cell carcinoma has been repeatedly demonstrated to have widespread, often insidious, metastatic potential. The reports of Middleton (149 of 503 cases) [11], Skinner and associates (77 of 309 cases) [16], and Tolia and Whitmore (174 of 586 cases) [18] suggest that one-quarter to one-third of patients with renal cell carcinoma have evidence of distant metastasis on presentation. The incidence of solitary metastasis in these studies was 3.6%, 1.6%, and 3.2%, respectively. In a more recent study of 1451 autopsy cases by Saitoh [15], 89% of cases demonstrated metastases at autopsy, with a rate of solitary metastasis of 8 %. Metastases to the lungs (76%) and lymph nodes (66%) occurred most frequently, followed by metastases to bone (42%), liver (41%), contralateral kidney (23%), ipsilateral adrenal (17%), and pancreas (14%). In fact, metastases
Histological study
Fig. 4. The photograph shows low-grade clear cell type renal cell carcinoma within two vascular spaces. The walls of the vessels are infiltrated with tumor, extending into the adjacent connective tissue and skeletal muscle (H & E, x 25). The inset (original magnification x 250) demonstrates the typical morphology of a clear cell renal cell carcinoma with small pycnotic nucleoli and abundant clear cytoplasm
from renal cell carcinoma have been reported in nearly every body system and organ [9, 10, 19]; metastases to skeletal muscle, however, are very uncommon. Skeletal muscle is one of the most unusual and rare sites of metastasis of renal cell carcinoma. Riches et al. [13] in 1951 reported four suspected metastases to muscle in 371 cases of metastatic renal cell carcinoma. Bennington and Kradjian [2] reported 3 cases out of 523 at the time of autopsy. In later accounts, such as Tolia and Whitmore's study of 586 cases [18] and Saitoh's study of 1451 cases [15], no cases of metastasis to skeletal muscle are documented. However, single case reports of renal cell carcinoma metastasizing to skeletal muscle continue to appear. Chandler et al. [3] in 1978 reported a case of a 52-year-old man with renal cell carcinoma presenting as a skeletal muscle mass of the right biceps; Karakousis et al. [5] in 1981 reported on a 63-year-old man with renal cell carcinoma metastatic to the right thigh; Alexio et al. [1] in 1984 reported a 74-year-old man with renal cell carcinoma presenting as a skeletal muscle mass of the left arm; and finally, Stener and associates [17] in 1984 reported two cases, a 46-year-old man and a 55-year-old man, of renal cell carcinoma metastasizing to the left thigh. Paget [12] compared the malignant embolic cells of renal cell carcinoma to seed scattered in soils of different degrees of fertility in an attempt to explain why some sites such as bone and liver are more susceptible to metastasis than others such as spleen and muscle. The issue of susceptibility is supported by later experiments demonstrating that tumor cell growth is dependent on the tissue in which the cells are placed [6]. However, a mechanical hypothesis postulated by Coman [4] explained the distribution of metastases by the mechanics of the circulation. Dissemination of embolic tumor cells could be lymphogenous, lymphohematogenous, or hematogenous. In lymphogenous spread, malignant cells from renal carcinoma metastasize to regional lymph nodes; in lymphohematogenous spread these cells gain access via the thoracic duct to the
P.L. Munk et al. : Case report 708 v a s c u l a r c i r c u l a t i o n to reach extrap e r i t o n e a l a b d o m i n a l sites. T h e hem a t o g e n o u s r o u t e for m e t a s t a s e s is the m o s t i m p o r t a n t a n d a c c o u n t s for the wide d i s t r i b u t i o n o f m e t a s t a t i c sites t h r o u g h o u t the b o d y . M e t a s tases to the eyes, skin, a n d muscles are m o r e difficult to e x p l a i n since the lung filters o u t m o s t e m b o l i c m a l i g n a n t cells [21]. M e t a s t a s e s to skeletal m u s c l e f r o m a n y p r i m a r y t u m o r are c o n s i d e r e d to be rare, b u t the true incidence is difficult to d e t e r m i n e since m e t a s tases to muscles m a y be a s y m p t o m a t ic. T h u s a search for such m e t a s tases is u s u a l l y n o t c a r r i e d o u t [7, 8]. A u t o p s y series q u o t e v a r i a b l e incidences o f m e t a s t a t i c disease to skeletal muscles b u t g e n e r a l l y r a n g i n g f r o m 1 % to 6 % [14, 20]. M a n y o f these m e t a s t a s e s a r e m i c r o s c o p i c in size a n d n o t r e a d i l y detectable. O u r case is i n t e r e s t i n g in t h a t the p a t i e n t not only presented with an asymptomatic muscle metastasis but what app e a r s to be a s o l i t a r y m e t a s t a s i s . N o f u r t h e r lesions have a p p e a r e d in the 6 m o n t h s since surgery. I n a d d i t i o n , the m e t a s t a s i s was well differentiated, in spite o f the fact t h a t the t u m o r was l a r g e l y a n a p l a s t i c . Since m e t a s tases to m u s c l e are i n f r e q u e n t , the initial w o r k i n g d i a g n o s e s t e n d e d to i g n o r e the final answer. In summary, a p a t i e n t is d e s c r i b e d w h o p r e s e n t e d w i t h a p a i n f u l softtissue m a s s in the r e g i o n o f the r i g h t s h o u l d e r 10 m o n t h s f o l l o w i n g nep h r e c t o m y f o r c a r c i n o m a . This m a s s
59 p r o v e d to be a m e t a s t a s i s to skeletal muscle. A full m e t a s t a t i c w o r k - u p d e m o n s t r a t e d no o t h e r d e t e c t a b l e lesions. M e t a s t a s e s to skeletal m u s c l e are rare, r e g a r d l e s s o f the site o f origin, a n d their true incidence is difficult to d e t e r m i n e since t h e y r a r e l y p r e s e n t clinically a n d are n o t r o u t i n e ly s e a r c h e d for, even on a u t o p s y .
References 1. Alexio G, Papadopoulou-Alexiou M, Karakousis CP (1984) Renal cell carcinoma presenting as a skeletal muscle mass. J Surg Oncol 27:23 2. Bennington JL, Kradjian RM (1967) Site of metastases at autopsy in 523 cases of renal carcinoma. In: Bennington JL, Kradjian RM (eds) Renal carcinoma. WB Saunders, Philadelphia, p 156 3. Chandler RW, Shulman I, Moore TM (1979) Renal cell carcinoma presenting as a skeletal muscle mass: a case report. Clin Orthop 145: 227 4. Coman DR (1953) Mechanisms responsible for origin and distribution of blood-borne tumor metastases: a review. Cancer Res 13 : 397 5. Karakousis CP, Rao U, Jennings E (1981) Renal cell carcinoma metastatic to skeletal muscle mass: a case report. J Surg Oncol 17:287 6. Kinsey DL (1960) An experimental study of preferential metastasis. Cancer 13:674 7. Lampenfeld ME, Reiley MA, Fein MA, Zaloudek CJ (1990) Metastasis to skeletal muscle from colorectal carcinoma: a case report. Clin Orthop 256:193 8. Laurence AE, Murray AJ (1970) Metastasis in skeletal muscle secondary to carcinoma of the colon - presentation of two cases. Br J Surg 57 : 529
9. Lipman JC, Loughlin KR, Richie JP, Tumeh SS (1988) Unusual solitary soft tissue metastases from renal cell carcinoma. Urol Radiol 10:110 10. Menter A, Boyd AS, McCaffree DM (1989) Recurrent renal cell carcinoma presenting as skin nodules: two case reports and review of the literature. Cutis 44:305 11. Middleton RG (1967) Surgery for metastatic renal cell carcinoma. J Urol 97: 973 12. Paget S (1889) The distribution of secondary growths in cancer of the breast. Lancet 1 : 571 13. Riches EW, Griffiths IH, Thrackray MA (1951) New growths of the kidney and ureter. Br J Urol 23 : 297 14. Rotterdam H, Slavutin L (1981) Secondary tumors of soft tissue: an autopsy study. In: Feroglio CM, Wolff M (eds) Progress in surgical pathology, vol 3. Masson, New York, p 147 15. Saitoh H (1981) Distant metastasis of renal adenocarcinoma. Cancer 48 : 1487 16. Skinner DG, Colvin RB, Vermillion CD, Pfister RC, Leadbetter WF (1971) Diagnosis and management of renal cell carcinoma. A clinical and pathological study of 309 cases. Cancer 28:1165 17. Stener B, Henriksson C, Johansson S, Gunterberg B, Pettersson S (1984) Surgical removal of bone and muscle metastases of renal cancer. Acta Orthop Scand 55:491 18. Tolia TM, Whitmore WF Jr (1975) Solitary metastasis from renal cell carcinoma. J Urol 114:836 19. Weigensberg IJ (1971) The many faces of metastatic renal carcinoma. Radiology 98:353 20. Willis RA (1952) The spread of tumours in the human body. Butterworths, London, p 284 21. Zeidman I, Buss JM (1952) Transpulmonary passage of tumor cell emboli. Cancer Res 12:731
Skeletal Radiology
Case report 708 Peter L. Munk, M.D. 1 *, Stephen Gock, M.D. 2, Richard Gee, M.D. 2, Douglas G. Connell, M.D. 1, and Noel F. Quenville, M.D. 3 Departments of 1 Radiology and 3 Pathology, University of British Columbia and Vancouver General Hospital Vancouver, British Columbia, Canada; and 2 University of Auckland, Auckland, New Zealand
Figs. 1 and 2. See next page for corresponding legends 9 1992 International Skeletal Society
P.L. Munk et al. : Case report 708
57
Fig. 1. Contrast enhanced computed tomography (CT) scan, 5-mm thick, through the top of the right shoulder demonstrates an enhancing soft-tissue mass with lobulated contours (arrows) within skeletal muscle (probably trapezius) Fig. 2A-E. Magnetic resonance imaging (MRI) right shoulder. A A 5-ram Tl-weighted (TR 800 ms/TE 30 ms) axial image shows the lesion to be of slightly greater signal than adjacent muscle. B, C, D Coronal images 5-mm thick. Tl-weighted (TR 600 ms/TE 30 ms) proton density and T2-weighted (TR 2000ms/TE 30 and 80 ms) show increased signal within the lesion (arrows) relative to skeletal muscle as T2 weighting is augmented. Note the slightly reticular texture of the lesion. E A 5-mm thick sagittal gradient recall image (TR 600 ms/TE 20 ms, 0 = 25~ demonstrates a ring of high signal around the lesion (arrows) Fig. 3A, B. Subclavian angiogram demonstrating an intensely vascular lesion, A early phase and B late arterial phase
Clinical information A 57-year-old man with a history of a right radical nephrectomy for renal cell carcinoma J0 months previously presented with a 2-month history of a mass in his right shoulder. The mass was first noticed by the patient's wife and was slightly painful when lifting and performing " p u s h ups". Family history indicated that
* Present address: Department of Radiology, University Hospital, University of Western Ontario; London, Ontario, Canada Address reprint requests to . Peter L. Munk,
M.D., Department of Radiology, University Hospital, University of Western Ontario, 339 Windermere Road, PO Box 5339, London, Ontario, Canada N6A 5A5
three siblings had also undergone nephrectomy, but the diagnosis in each case was unclear. On examination, positive physical findings consisted of a solitary, firm, 4 x 3 cm mass of the right shoulder proximal and posterior to the acromioclavicular joint. The mass was nontender and appeared to be superficial. The remainder of the physical examination was grossly normal. Hematological studies were normal. Serum biochemical studies revealed an elevated creatinine of 127 gmol/1 and potassium of 54 retool/1. Contrast-enhanced CT demonstrated an enhancing mass with lobulated contours restricted to skeletal muscle, its epicenter in the right tra-
pezius (Fig. 1). M R showed the lesion to be of low signal on T1weighted sequences and high signal with T2-weighting (Fig. 2). The lesion had a slightly reticulated texture and revealed changes suggestive o f edema in the surrounding tissues. Angiography, performed to embolize the mass to facilitate surgery, demonstrated intense vascularity (Fig. 3). CT scans of the chest, abdomen, and pelvis were normal, as were abdominal ultrasound and whole-body bone scintigraphy results (apart from transient increased uptake in the lesion in the soft-tissue phase of the scan). The day following embolization a wide excision of the mass was performed.
58
Diagnosis: Metastasis of renal cell carcinoma to skeletal muscle (right trapezius) The tumor involving the skeletal muscle, fascia and connective tissue measured 7 x 4 cm. It had a multinodular, focally necrotic, and hemorrhagic appearance on the cut surface, involved skeletal muscle and fascia, and demonstrated associated, multiple, dilated vascular channels containing thrombotic-appearing material. Histological sections showed extensive tumor thrombi within dilated veins and lymphatics, expanding the vascular lumens and infiltrating through the vessel walls into the surrounding fascia, connective tissue, and skeletal muscle (Fig. 4). The overall appearance was in keeping with extensive intravascular metastases. The morphological features were those of a relatively low-grade renal cell carcinoma, resembling the low-grade component of the renal cell carcinoma in the nephrectomy specimen previously removed. Of interest, the primary renal cell tumor was composed of equal parts of a low-grade clear cell type and high-
P.L. M u n k et al. : Case report 708
grade granular cell renal carcinoma, with the low-grade component presenting as the metastasis.
Discussion Renal cell carcinoma has been repeatedly demonstrated to have widespread, often insidious, metastatic potential. The reports of Middleton (149 of 503 cases) [11], Skinner and associates (77 of 309 cases) [16], and Tolia and Whitmore (174 of 586 cases) [18] suggest that one-quarter to one-third of patients with renal cell carcinoma have evidence of distant metastasis on presentation. The incidence of solitary metastasis in these studies was 3.6%, 1.6%, and 3.2%, respectively. In a more recent study of 1451 autopsy cases by Saitoh [15], 89% of cases demonstrated metastases at autopsy, with a rate of solitary metastasis of 8 %. Metastases to the lungs (76%) and lymph nodes (66%) occurred most frequently, followed by metastases to bone (42%), liver (41%), contralateral kidney (23%), ipsilateral adrenal (17%), and pancreas (14%). In fact, metastases
Histological study
Fig. 4. The photograph shows low-grade clear cell type renal cell carcinoma within two vascular spaces. The walls of the vessels are infiltrated with tumor, extending into the adjacent connective tissue and skeletal muscle (H & E, x 25). The inset (original magnification x 250) demonstrates the typical morphology of a clear cell renal cell carcinoma with small pycnotic nucleoli and abundant clear cytoplasm
from renal cell carcinoma have been reported in nearly every body system and organ [9, 10, 19]; metastases to skeletal muscle, however, are very uncommon. Skeletal muscle is one of the most unusual and rare sites of metastasis of renal cell carcinoma. Riches et al. [13] in 1951 reported four suspected metastases to muscle in 371 cases of metastatic renal cell carcinoma. Bennington and Kradjian [2] reported 3 cases out of 523 at the time of autopsy. In later accounts, such as Tolia and Whitmore's study of 586 cases [18] and Saitoh's study of 1451 cases [15], no cases of metastasis to skeletal muscle are documented. However, single case reports of renal cell carcinoma metastasizing to skeletal muscle continue to appear. Chandler et al. [3] in 1978 reported a case of a 52-year-old man with renal cell carcinoma presenting as a skeletal muscle mass of the right biceps; Karakousis et al. [5] in 1981 reported on a 63-year-old man with renal cell carcinoma metastatic to the right thigh; Alexio et al. [1] in 1984 reported a 74-year-old man with renal cell carcinoma presenting as a skeletal muscle mass of the left arm; and finally, Stener and associates [17] in 1984 reported two cases, a 46-year-old man and a 55-year-old man, of renal cell carcinoma metastasizing to the left thigh. Paget [12] compared the malignant embolic cells of renal cell carcinoma to seed scattered in soils of different degrees of fertility in an attempt to explain why some sites such as bone and liver are more susceptible to metastasis than others such as spleen and muscle. The issue of susceptibility is supported by later experiments demonstrating that tumor cell growth is dependent on the tissue in which the cells are placed [6]. However, a mechanical hypothesis postulated by Coman [4] explained the distribution of metastases by the mechanics of the circulation. Dissemination of embolic tumor cells could be lymphogenous, lymphohematogenous, or hematogenous. In lymphogenous spread, malignant cells from renal carcinoma metastasize to regional lymph nodes; in lymphohematogenous spread these cells gain access via the thoracic duct to the
P.L. Munk et al. : Case report 708 v a s c u l a r c i r c u l a t i o n to reach extrap e r i t o n e a l a b d o m i n a l sites. T h e hem a t o g e n o u s r o u t e for m e t a s t a s e s is the m o s t i m p o r t a n t a n d a c c o u n t s for the wide d i s t r i b u t i o n o f m e t a s t a t i c sites t h r o u g h o u t the b o d y . M e t a s tases to the eyes, skin, a n d muscles are m o r e difficult to e x p l a i n since the lung filters o u t m o s t e m b o l i c m a l i g n a n t cells [21]. M e t a s t a s e s to skeletal m u s c l e f r o m a n y p r i m a r y t u m o r are c o n s i d e r e d to be rare, b u t the true incidence is difficult to d e t e r m i n e since m e t a s tases to muscles m a y be a s y m p t o m a t ic. T h u s a search for such m e t a s tases is u s u a l l y n o t c a r r i e d o u t [7, 8]. A u t o p s y series q u o t e v a r i a b l e incidences o f m e t a s t a t i c disease to skeletal muscles b u t g e n e r a l l y r a n g i n g f r o m 1 % to 6 % [14, 20]. M a n y o f these m e t a s t a s e s a r e m i c r o s c o p i c in size a n d n o t r e a d i l y detectable. O u r case is i n t e r e s t i n g in t h a t the p a t i e n t not only presented with an asymptomatic muscle metastasis but what app e a r s to be a s o l i t a r y m e t a s t a s i s . N o f u r t h e r lesions have a p p e a r e d in the 6 m o n t h s since surgery. I n a d d i t i o n , the m e t a s t a s i s was well differentiated, in spite o f the fact t h a t the t u m o r was l a r g e l y a n a p l a s t i c . Since m e t a s tases to m u s c l e are i n f r e q u e n t , the initial w o r k i n g d i a g n o s e s t e n d e d to i g n o r e the final answer. In summary, a p a t i e n t is d e s c r i b e d w h o p r e s e n t e d w i t h a p a i n f u l softtissue m a s s in the r e g i o n o f the r i g h t s h o u l d e r 10 m o n t h s f o l l o w i n g nep h r e c t o m y f o r c a r c i n o m a . This m a s s
59 p r o v e d to be a m e t a s t a s i s to skeletal muscle. A full m e t a s t a t i c w o r k - u p d e m o n s t r a t e d no o t h e r d e t e c t a b l e lesions. M e t a s t a s e s to skeletal m u s c l e are rare, r e g a r d l e s s o f the site o f origin, a n d their true incidence is difficult to d e t e r m i n e since t h e y r a r e l y p r e s e n t clinically a n d are n o t r o u t i n e ly s e a r c h e d for, even on a u t o p s y .
References 1. Alexio G, Papadopoulou-Alexiou M, Karakousis CP (1984) Renal cell carcinoma presenting as a skeletal muscle mass. J Surg Oncol 27:23 2. Bennington JL, Kradjian RM (1967) Site of metastases at autopsy in 523 cases of renal carcinoma. In: Bennington JL, Kradjian RM (eds) Renal carcinoma. WB Saunders, Philadelphia, p 156 3. Chandler RW, Shulman I, Moore TM (1979) Renal cell carcinoma presenting as a skeletal muscle mass: a case report. Clin Orthop 145: 227 4. Coman DR (1953) Mechanisms responsible for origin and distribution of blood-borne tumor metastases: a review. Cancer Res 13 : 397 5. Karakousis CP, Rao U, Jennings E (1981) Renal cell carcinoma metastatic to skeletal muscle mass: a case report. J Surg Oncol 17:287 6. Kinsey DL (1960) An experimental study of preferential metastasis. Cancer 13:674 7. Lampenfeld ME, Reiley MA, Fein MA, Zaloudek CJ (1990) Metastasis to skeletal muscle from colorectal carcinoma: a case report. Clin Orthop 256:193 8. Laurence AE, Murray AJ (1970) Metastasis in skeletal muscle secondary to carcinoma of the colon - presentation of two cases. Br J Surg 57 : 529
9. Lipman JC, Loughlin KR, Richie JP, Tumeh SS (1988) Unusual solitary soft tissue metastases from renal cell carcinoma. Urol Radiol 10:110 10. Menter A, Boyd AS, McCaffree DM (1989) Recurrent renal cell carcinoma presenting as skin nodules: two case reports and review of the literature. Cutis 44:305 11. Middleton RG (1967) Surgery for metastatic renal cell carcinoma. J Urol 97: 973 12. Paget S (1889) The distribution of secondary growths in cancer of the breast. Lancet 1 : 571 13. Riches EW, Griffiths IH, Thrackray MA (1951) New growths of the kidney and ureter. Br J Urol 23 : 297 14. Rotterdam H, Slavutin L (1981) Secondary tumors of soft tissue: an autopsy study. In: Feroglio CM, Wolff M (eds) Progress in surgical pathology, vol 3. Masson, New York, p 147 15. Saitoh H (1981) Distant metastasis of renal adenocarcinoma. Cancer 48 : 1487 16. Skinner DG, Colvin RB, Vermillion CD, Pfister RC, Leadbetter WF (1971) Diagnosis and management of renal cell carcinoma. A clinical and pathological study of 309 cases. Cancer 28:1165 17. Stener B, Henriksson C, Johansson S, Gunterberg B, Pettersson S (1984) Surgical removal of bone and muscle metastases of renal cancer. Acta Orthop Scand 55:491 18. Tolia TM, Whitmore WF Jr (1975) Solitary metastasis from renal cell carcinoma. J Urol 114:836 19. Weigensberg IJ (1971) The many faces of metastatic renal carcinoma. Radiology 98:353 20. Willis RA (1952) The spread of tumours in the human body. Butterworths, London, p 284 21. Zeidman I, Buss JM (1952) Transpulmonary passage of tumor cell emboli. Cancer Res 12:731
