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Results of Inferior Vena Cava Resection for Renal Cell Carcinoma
'THE JOURNAL OF URDLOGY
Copy::(igb_t © 1981
The \;Villiarns & Viilkhs Co.
OF
RESECTION FOR RENAL CELL
GARY P. KEARNEY,* W. BEDFORD WATERS, LESTER A. KLEIN, JEROME P. RICHIE RUBEN F. GITTES
AND
From the Harvard Medical School Program in Urology and Department of Surgery, Division of Urology, Brigham and Women's Hospital and Beth Israel Hospital, Boston, Massachusetts
ABSTRACT
A total of 24 patients with renal cell carcinoma involving the inferior vena cava underwent tho:racoabdorninal radical nephrectomy with removal of tumor thrombus by an open or closed technique. The tumor extended in the inferior vena cava to the level of the renal or lower hepatic veins in 18 patients and it :reached the level of the diaphragm o:r right atrium in 6. Of the 24 patients 3 with preoperative findings minimally suggestive of disseminated disease were shown later to have metastases in the questionable areas, 3 with disease at the level of the diaphragm had incomplete resections, 4 had metastases to :regional lymph nodes and l had questionable preoperative findings and lymph node metastases. Only 13 of the 24 patients (54 per cent) did not have either disseminated or .residual tumor postoperatively. The mean survival duration of this subgroup (20 months) was comparable to that of the group as a whole (21 months). However, 4 patients from this subgroup are free of disease, with a mean followup of 30 months. There was l postoperative death. Morbidity, including renal int:raoperative hypotension and sepsis, was common. The results in this series suggest that the prognosis for patients with renal cell carcinoma and inferior vena caval involvement is guarded. Among the controversies with regard to renal cell carcinoma the prognostic significance of inferior vena caval involvement, which occurs in 4 to 10 per cent of the cases, 1' 2 remains unsettled. Several investigators have contended that extension into the inferior vena cava must portend a poor outcome, even in patients without distant metastases. 1' 3 ' 4 Other series have not substantiated this finding. 5 - 8 However, none of these studies provides detailed documentation of the level of inferior vena caval involvement in a substantial number of patients who have been treated by similar surgical techniques. We performed a retrospective review of 24 cases in which such detailed documentation was available. MATERIALS AND METHODS
From 1972 to 1979, 24 patients disease undervvent radical nPnh,rPr-trm'"!v tumor thrombus from the inferior vena ca.va. information v;as available for all but 1 The patients in age from 26 to 74 yea.rs, with a mean of 56 years. There were 14 men and 10 women, Inforruation on the individual IS in table l. 14 (58 per cent) had either gross or Of the 24 and 6 (25 per cent) presented with an (8 per cent) presented with a OlU'UVJCW.J.HU ffiaSS, pulmonary embolus that was to bland tumor thrombus, since preoperative chest was normal. All patients underwent excretory uro 5raphy with nephrotomogrnphy, selective renal arteriography, inferior venacavography and pulmonary tomography as part of the preoperative evaluation. In addition, most patients also had liver and bone scans, and patients with large tumors had celiac angiography. All patients were considered free of metastatic disease on the basis of these studies, although 4 had ambiguous findings, with
a questionable chest lesion shown in 3 and a questionable bone lesion demonstrated in l. The renal cell carcinoma originated in the right kidney in 21 patients (88 per cent) and in the left kidney in 3. In 9 of the 24 patients (38 per cent) the tumor in the inferior vena cava did not extend beyond the level of the renal veins (fig. 1). The tumor reached the level of the lower hepatic veins in 11 patients (46 per cent) and it extended either to the level of the diaphragm or into the right atrium in 4 (16 per cent). All patients underwent thoracoabdominal radical nephrectomy, The inferior vena cava was resected closed technique with margins free of tumor in 12 patients. In the remainder the tumor was removed from the inferior vena cava venacavotomy with extraction, with or without removal of a cuff of inferior vena cava (fig. 2). The pathology reports did not note c.v,,w,"cc,uc.,y whether the tumor invaded the inferior vena caval wall or extended into the inferior vena cava without When invasion of the inferior vena caval wall was found at operation it usually was limited to the area of the inferior vena cava at the renal vein. The resection was complete in 21 patients, while macroscopic residual disease remained postoperatively in 3 'Nith involvement above the lower veins. Histologic examination of regional lymph nodes removed at operation showed metastases in 5 patients. One of the patients (case 19) had a questionable chest lesion preoperatively and lymph node metastases (table This patient, thus, represents 2 of the 12 instances of negative prognostic factors. Only 13 of the 24 cases (54 per cent) did not exhibit poor prognostic factors, such as preoperative evidence of distant metastases, incomplete tumor resection or metastases to regional lymph nodes. RESULTS
One patient in the favorable subgroup was lost to followup 7 Accepted for publication August 29, 1980. months postoperatively and is presumed dead (case 21). One Read at annual meeting of American Urological Association, San other patient in that subgroup died without tumor 3 months Francisco, California, May 18-22, 1980. * Requests for reprints: 319 Longwood Ave., Boston, Massachu- postoperatively. The mean survival was 21 months (fig. 3). In the subgroup of setts 02115. 769
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770
KEARNEY AND ASSOCIATES TABLE
1. Data on 24 patients operated on for extension of renal cell carcinoma to the inferior vena cava
Questionable Preop. Findings• Chest
Complications
Resection Kidney
Pt.-Age-Sex
Tumor Level in Inferior Vena Cava
Rib
Technique
Proceduret
Completeness:j:
Rt. Lt. Rt. Rt. Rt. Rt. Rt.
Renal vein Hepatic vein Renal vein Renal vein Diaphragm Renal vein Rt. atrium
Open Closed Open Closed Open Open Open
Fig. 2,A Fig. 2,E Fig. 2,A Fig. 2,A Fig.2,A Fig. 2,A Fig. 2,A
C C C C I C C
8-73-M 9-49-F 10-69-M
Rt. Rt. Rt.
Renal vein Renal vein Diaphragm
Closed Open Open
Fig. 2, B Fig. 2,A Fig.2,A
I
11-74-M
Lt.
Renal vein
Open
Fig. 2,D
C
12-26-M 13-53-M 14-60-M
Rt. Rt. Rt.
Renal vein Hepatic vein Hepatic vein
Open Open Closed
Fig. 2,A Fig.2,B Fig.2,B
C C C
15-52-M 16-57-F 17-71-F 18-58-M 19-63-M 20-66-F 21-70-M 22-52-M 23-60-M 24-61-F
Rt. Rt. Lt. Rt. Rt. Rt. Rt. Rt. Rt. Rt.
Renal vein Diaphragm Hepatic vein Hepatic vein Hepatic vein Hepatic vein Hepatic vein Hepatic vein Hepatic vein Hepatic vein
Closed Open Open Closed Closed Closed Closed Closed Closed Closed
Fig. 2, C Fig. 2, A Fig. 2, D Fig.2,B Fig. 2, B Fig. 2, C Fig. 2,B Fig. 2, C Fig. 2, C Fig. 2, B
C I C C C C C C C C
1-54-M 2-55-M 3-45-F 4-60-F 5-72-F 6-39-F 7-68-F
X
X X X
Node Involvement
Survival Renal Failure
Other
X
Sepsis
X
Arrhythmia, respiratory failure
X
C
X\I
C
Arrhythmia, wound infection Splenic laceration
X
X
Deep vein thrombosis rt. leg X
Arrhythmia X X X X X
Dead, 12 mos. Dead, 3 mos.§ Dead, 36 mos. Dead, 36 mos. Dead, 48 mos. Dead, 12 mos. Dead, 6mos. Alive, 30 mos. Alive, 6 mos. Dead, 8mos. Dead, 13 mos. Dead, 4mos. Dead, 10 mos. Alive, 18 mos. Dead, 40 mos. Dead, 48 mos. Dead, 24 mos. Dead, 24 mos. Dead, 5mos. Dead, 6mos. Dead, 7 mos. Alive, 69 mos. Dead, 24 mos. Dead, 6mos.
• Later shown to be metastatic disease. t Patients 1, 3, 5, 6, 7, 9, 10, 12 and 16 had the venacavotomy performed by the open technique. Patient 4 underwent the closed technique. :j: C, complete, I, incomplete. § Dead without evidence of disease. JI Did not require dialysis.
t~
_LEVEL CF INWL/..EMNl_ __
Atrium-Diaphragm
Lower Hepatic Veins
Renal Veins
A
B
C
NO. of Pts.
¼
4
16
---8
11
46
---c
9
38
Toto/
24
FIG. 1. Levels of tumor extension in inferior vena cava and number of patients in this series with tumor at various levels
13 cases without negative prognostic factors the average survival (20 months) was similar to that of the group as a whole. The range of survival times in the subgroup (3 to 69 months) was identical to that of the entire group. All 4 patients with preoperative studies that ambiguously suggested metastatic disease proved to have metastases in the questionable areas and all eventually died. The survival for these 4 patients ranged from 5 to 24 months, with a mean of 10
months. In contrast, patients without preoperative metastases had a mean survival of 23 months (range 3 to 69 months). The 5 patients with positive lymph nodes died and their survival averaged 19 months (range 5 to 24 months). Twenty patients (83 per cent) are known or presumed to have died. For these patients survival ranged from 3 to 48 months, with a mean of 19 months. Four patients, all of whom belonged to the subgroup with neither disseminated nor resid-
FIG. 2. Surgical techniques used in inferior vena caval resection for renal cell carcinoma. A, venacavotomy with tumor extraction with open or closed technique-used for tumor originating in right kidney and extending to level of :renal veins. B, ligation of left renal vein and inferior vena cava-done in cases with tumor on right side and extensive involvement at level of renal or lower hepatic veins. C, ligation of inferior vena cava distal to renal veins with maintenance of continuity of left renal vein and proximal inferior vena cava-used for tumor un,1s,uau1J,g in right kidney with extensive involvement of inferior vena cava at level of renal veins in non-collateralized D, venacavotomy with extraction tec:h1~iC[Ut,--p1,rfon;-rn,d in cases with tumor originating in left E, ligation inferior vena cava with maintenance of venous by renal vein-to-portal vein interposition m,.--u.,,1cu cases v,ith tumor on left side and extensive involvement of
postoperatively of Postmortem examination Other complications included thrombosis, m-,·nv,n,n ble 1). as a of lovver veins, did not occur in any DJSCUSSION
of rnnal cell carcinoma,
0
·40
60
80
PIG,_ 3. 9um1r,_~ative s~:rviv~J ,...of_ 24 patients vvho undervvent :rer.eoval of ren&.l cell ca.rc1norn2 tro:rr.: :nreno:r vena cava.
ual disease, a.re Nithout evidence of disease 6 to 69 months and their nH,an survival tiine is 30 months. The repn,sent 17 pe:r cent of the group as a whole per cent of the vvithout negafr1e prognostic factors. Of the 24 7 (29 per cent) had oliguria with renal failure in the immediate postoperative period and 6 of these required dialysis. A closed resection of the tumor in the inferior vena cava had been done in 4 of the 7 cases, while in 3 the remaining renal vein had been occluded temporarily or permanently as part of the surgical procedure. One of the patients with :renal failure died and this represented the only operative death (4 per cent) in the series. In this patient (case 2) there was a tumor on the left side, extending to the level of the hepatic veins, that required temporary interruption of the venous supply to the right kidney followed 0
2 of these have a <2 y.sars. In a treated between 1935 and 1965, 6 of 11 m1t1en,ts (55 per cent) who had inferior vena caval involvement without evidence of distant metastases were found to have survived at least 5 years after resection." ,-,.,,,,,.,,.,,, . . while this study has provided the basis for the optimism with which inferior vena caval involvement has been viewed it did not report the level of tumor extension in the inferior vena cava. The patients who had good survival might have had minimal extension from the renal vein found at operation and, therefore, might not be comparable to patients who have extensive involvement demonstrated inferior venacavography. The survival rate documented in other studies falls short of 55 per cent. In a 1977 study it was found that 4 of 12 patients (33 per cent) without metastatic disease who had been operated cu,,c,~,,.o,
~,o-
772
KEARNEY AND ASSOCIATES TABLE 2.
Reference Gleason and associates 14 Cole and associates3 Beck5 Pathak15 Esho and Owoseni16 Martinek17 Musiani18
Literature review of vena caval resection for renal cell carcinoma
Preop. Metastases
Node Involvement
Level of Vena Caval Tumor
Status
Yes Yes No No No Yes No ? ? Yes
Yes Yes No No No No Yes ? ? ?
Rt. atrium Hepatic vein Renal vein Renal vein Hepatic vein Hepatic vein Renal vein Renal vein Renal vein Rt. atrium
Alive with disease Dead Alive without disease Alive without disease Alive without disease Dead Alive with disease Alive without disease? Dead Alive W\th disease
on for renal cell carcinoma involving the inferior vena cava survived >2 years. 6 Although less favorable these results, nevertheless, seem encouraging. However, examination of the data shows that 3 of the 4 survivors had recurrent disease at last reported followup. Most other studies involve only a few cases, frequently with limited followup. Ten cases reported in 7 studies had a mean followup of 17 months (table 2). 3' 5 • 14- 18 Of these patients 4 were known to be free of metastases preoperatively, including 3 who were alive without disease 3 to 12 months postoperatively. Although our study suggests that the survival rate may be much lower than is suggested in the literature patients with inferior vena caval involvement but without distant metastases should not be denied an operation. Because there is no effective adjuvant therapy for renal cell carcinoma an operation should be offered to such patients in the hope of averting possible complications16• 19 and prolonging survival. While the average survival of such patients in this group was 23 months the survival ranged to 69 months. Patients with findings that suggest the presence of metastases should not be operated on before completion of careful metastatic diagnostic studies, including biopsy of suspicious lesions. All 4 patients with suspicious preoperative findings in our series were shown later to have metastatic disease in those areas. Their mean survival of 10 months was less than half that of the group as a whole and is comparable to that of patients reported elsewhere who had clear evidence of metastatic disease preoperatively, none of whom survived >12 months. 6 Inferior vena caval resection can be done safely and with little mortality. 1• 18• 20-24 The surgical techniques have been well established, although the procedure, which had been done as early as 1905,3 was not performed widely until the 1960s.6 • 16 The development of cardiopulmonary bypass techniques with circulatory arrest now even permits the safe resection of tumor extending into the right atrium. 14• 18• 21• 25 The surgical options depend on the kidney involved and on the level of tumor extension in the inferior vena cava (fig. 2). Although ultrasound26-28 and computerized tomography29 have shown promise in demonstrating vena caval involvement venacavography in frontal and lateral views must be done to obtain an accurate assessment of the extent of disease that will permit careful planning of the surgical approach. 5• 6 • 14• 24• 30- 32 Multiple collateral pathways, including the ascending lumbar, adrenal and spermatic or ureteral veins, are available to drain the left kidney but the right kidney lacks a collateral venous supply. 20 Renal cell carcinomas originating in the right kidney extend more frequently into the inferior vena cava than do tumors of the left kidney, possibly because the shorter right renal vein more easily allows vena caval extension. Thus, in many cases suprarenal inferior vena caval resection may involve ligation of the left renal vein, which can be accomplished with little difficulty. However, because of the lack of collaterals to the right kidney procedures done for tumors on the left side must include preservation of the venous drainage of the right kidney. In cases of tumor on the right side in which the inferior vena caval involvement does not extend beyond the level of the renal veins the tumor thrombus may be recovered by venacavotomy,
Followup (mos.) 12 10 10 12 3 6
30 12 12 7
using an open or closed technique (fig. 2, A). When there is extensive involvement at the renal vein level ligation of the inferior vena cava above the renal veins is possible for tumors on the right side (fig. 2, B). Because the obstruction of the inferior vena cava by the intracaval tumor promotes development of a collateral blood supply33 the ligation carries little morbidity (case 14). However, in the non-collateralized patient it is desirable to maintain the continuity of the left renal vein and proximal inferior vena cava to avoid transient renal failure (fig. 2, C). When the tumor extends above the level of the lower hepatic veins closed resection of the inferior vena cava is not possible, even with division of the coronary and triangular ligaments of the right lobe of the liver. 20 Venacavotomy using the Foley catheter technique21 or compression of the porta hepatis to reduce hepatic blood flow (the Pringle maneuver) can be used to treat tumors at the upper hepatic vein or diaphragmatic level. The importance of proximal inferior vena caval control to reduce blood loss in disease at this level cannot be overemphasized. Controlling tourniquets should be placed around 1) the inferior vena cava proximal to the resection, either above or below the diaphragm or intrapericardially, 2) the inferior vena cava distal to the resection and 3) the renal vein. In cases with intra-cardiac extension cardiopulmonary bypass is essential. With the 2-team technique the operation generally is done through a median sternotomy rather than by a thoracoabdominal approach. Circulatory arrest has been used with success after the patient has been placed on cardiac bypass. With a tumor on the left side the venous supply to the right kidney can be maintained by an open resection with extraction of the tumor (fig. 2, D) or by interposing an end-to-side renal vein-to-portal vein graft (fig. 2, E). Of the 4 patients in this series who have survived without disease 3 were operated on by an en bloc, closed technique without tumor spillage. Of these 3 patients 2 represent our longest survivors, with 30 and 69-month survival, respectively. However, the inference that the closed technique is superior to an open venacavotomy with extraction of tumor thrombus is not warranted since, over-all, there was little difference in the survival of patients operated on by the closed and open techniques (22 and 19 months mean survival, respectively). While the operative mortality in our series was low (4 per cent) morbidity was common, although the complications were manageable. Of the 7 patients who had renal failure 6 required dialysis. Of the 6 patients requiring dialysis 3 had closed resections and 3 had interruption of the venous egress of the remaining kidney. The other complications encountered, sepsis, wound infection, and respiratory and cardiac arrhythmias, responded well to medical treatment. REFERENCES
1. Marshall, V. F., Middleton, R. G., Holswade, G. R. and Goldsmith,
E. I.: Surgery for renal cell carcinoma in the vena cava. J. Urol., 103: 414, 1970. 2. Svane, S.: Tumor thrombus of the inferior vena cava resulting from renal carcinoma. A report on 12 autopsied cases. Scand. J. Urol. Nephrol., 3: 245, 1969.
INFERIOR VENA CAVA RESECTION FOR RENAL CELL CARCINOMA
3. Cole, A. T., Julian, W. A. and Fried, F. A.: Aggressive surgery for renal cell carcinoma with vena cava tumor thrombus. Urology, 6: 227, 1975. 4. Tsuchida, S., Sugawara, H., Harata, T., Yamaguchi, 0. and Arai, S.: Diagnosis, treatment and prognosis of renal cell carcinoma. Tohoku J. Exp. Med., 113: 319, 1974. 5. Beck, A. D.: Renal cell carcinoma involving the inferior vena cava: radiologic evaluation and surgical management. J. Urol., 118: 533, 1977.
6. Schefft, P., Novick, A. C., Straffon, R. A. and Stewart, B. H.: Surgery for renal cell carcinoma extending into the inferior vena cava. J. Urol., 120: 28, 1977. 7. McCullough, D. L. and Talner, L. B.: Inferior vena caval extension of renal carcinoma: a lost cause? Amer. J. Roentgen., 121: 819, 1974.
8. Skinner, D. G., Pfister, R. F. and Colvin, R.: Extension of renal cell carcinoma into the vena cava: the rationale for aggressive surgical management. J. Urol., 107: 711, 1972. 9. Murphy, G. P.: Current results from treatment of renal cell carcinoma. In: Proceedings of the Seventh National Cancer Conference. Philadelphia: J. B. Lippincott Co., p. 751, 1972. 10. Editorial: Renal-cell carcinoma. Lancet, 2: 887, 1976. 11. Bottinger, L. E.: Prognosis in renal cell carcinoma. Cancer, 26: 780, 1970. 12. Wagle, D. G.: Vagaries of renal cell carcinoma. J. Med., 3: 178, 1972. 13. deKernion, J.B., Ramming, K. P. and Smith, R. B.: The natural
14.
15.
16. 17. 18.
II
history of metastatic renal cell carcinoma: a computer analysis. J. Urol., 120: 148, 1978. Gleason, D. M., Reilly, R. J., Anderson, R. M., O'Hare, J. E., Kartchner, M. M. and Komar, N. N.: Removal ofhypernephroma and inferior vena cava: right atrial tumor thrombus. Arch. Surg., 105: 795, 1972. Pathak, I. C.: Survival after right nephrectomy, excision of infrahepatic vena cava and ligation of left renal vein: a case report. J. Urol., 106: 599, 1971. Esho, J. 0. and Owoseni, A.: Vena cava resection with renal cell carcinoma. Eur. Urol., 3: lll, 1977. Martinek, J. B.: Surgical treatment of renal tumors penetrating into the great veins. Int. Surg., 55: 417, 1971. Musiani, U .: Hypernephroma of the right kidney with inferior vena
773
caval and right atrial thrombosis: case study and successful removal. J. Urol., 118: 472, 1977. 19. Freed, S. Z.: Nephrectomy for renal cell carcinoma with metastases. Urology, 9: 613, 1977. 20. McCullough, D. L. and Gittes, R. F.: Vena cava resection for renal cell carcinoma. J. Urol., 112: 162, 1974. 21. Freed, S. Z. and Gliedman, M. L.: The removal of renal carcinoma thrombus extending into the right atrium. J. Urol., 113: 163, 1975. 22. Lome, L. G. and Bush, I. M.: Resection of the vena cava for renal cell carcinoma: an experimental study. J. Urol., 107: 717, 1972. 23. Duckett, J. W., Jr .. Lifland, J. H. and Peters, P. C.: Resection of
the inferior vena cava for adjacent malignant diseases. Surg., Gynec. & Obst., 136: 711, 1973. 24. Waters, W. B. and Richie, J. P.: Aggressive surgical approach to renal cell carcinoma: review of 130 cases. J. Urol., 122: 306, 1979. 25. Paul, J. G., Rhodes, D. B. and Skow, J. R.: Renal cell carcinoma presenting as right atrial tumor with successful removal using cardiopulmonary bypass. Ann. Surg., 181: 471, 1975. 26. Greene, D. and Steinbach, H. L.: Ultrasonic diagnosis of hypernephroma extending into the inferior vena cava. Radiology, 115: 679, 1975. 27. Wines, R. D., Frawley, J. and Palmer, J.: The use of ultrasound in
28.
29.
30. 31.
32.
33.
the diagnosis of extension of malignant renal tumours into the inferior vena cava. Brit. J. Urol., 46: 120, 1974. Goldstein, H. M., Green, B. and Weaver, R. M., Jr.: Ultrasonic detection of renal tumor extension into the inferior vena cava. Amer. J. Roentgen., 130: 1083, 1978. Marks, W. M., Korobkin, M., Callen, P. W. and Kaiser, J. A.: CT diagnosis of tumor thrombosis of the renal vein and inferior vena cava. Amer. J. Roentgen., 131: 843, 1978. James, D. C.: Inferior caval venography in the assessment of renal carcinoma. Clin. Rad., 30: 525, 1979. Dorr, R. P., Cerny, J.C. and Hoskins, P.A.: Inferior venacavograms and renal venograms in the management of renal tumors. J. Urol., 110: 280, 1973. Palmer, J., Barry, B., Williams, R. and Briscoe, P.: Diagnosis of venous extension in renal cell carcinoma. The value of routine inferior venacavography. Aust. Rad., 19: 265, 1975. Leiter, E.: Inferior-vena-caval thrombosis in malignant renal lesions. J.A.M.A., 198: 145, 1966.
Copy::(igb_t © 1981
The \;Villiarns & Viilkhs Co.
OF
RESECTION FOR RENAL CELL
GARY P. KEARNEY,* W. BEDFORD WATERS, LESTER A. KLEIN, JEROME P. RICHIE RUBEN F. GITTES
AND
From the Harvard Medical School Program in Urology and Department of Surgery, Division of Urology, Brigham and Women's Hospital and Beth Israel Hospital, Boston, Massachusetts
ABSTRACT
A total of 24 patients with renal cell carcinoma involving the inferior vena cava underwent tho:racoabdorninal radical nephrectomy with removal of tumor thrombus by an open or closed technique. The tumor extended in the inferior vena cava to the level of the renal or lower hepatic veins in 18 patients and it :reached the level of the diaphragm o:r right atrium in 6. Of the 24 patients 3 with preoperative findings minimally suggestive of disseminated disease were shown later to have metastases in the questionable areas, 3 with disease at the level of the diaphragm had incomplete resections, 4 had metastases to :regional lymph nodes and l had questionable preoperative findings and lymph node metastases. Only 13 of the 24 patients (54 per cent) did not have either disseminated or .residual tumor postoperatively. The mean survival duration of this subgroup (20 months) was comparable to that of the group as a whole (21 months). However, 4 patients from this subgroup are free of disease, with a mean followup of 30 months. There was l postoperative death. Morbidity, including renal int:raoperative hypotension and sepsis, was common. The results in this series suggest that the prognosis for patients with renal cell carcinoma and inferior vena caval involvement is guarded. Among the controversies with regard to renal cell carcinoma the prognostic significance of inferior vena caval involvement, which occurs in 4 to 10 per cent of the cases, 1' 2 remains unsettled. Several investigators have contended that extension into the inferior vena cava must portend a poor outcome, even in patients without distant metastases. 1' 3 ' 4 Other series have not substantiated this finding. 5 - 8 However, none of these studies provides detailed documentation of the level of inferior vena caval involvement in a substantial number of patients who have been treated by similar surgical techniques. We performed a retrospective review of 24 cases in which such detailed documentation was available. MATERIALS AND METHODS
From 1972 to 1979, 24 patients disease undervvent radical nPnh,rPr-trm'"!v tumor thrombus from the inferior vena ca.va. information v;as available for all but 1 The patients in age from 26 to 74 yea.rs, with a mean of 56 years. There were 14 men and 10 women, Inforruation on the individual IS in table l. 14 (58 per cent) had either gross or Of the 24 and 6 (25 per cent) presented with an (8 per cent) presented with a OlU'UVJCW.J.HU ffiaSS, pulmonary embolus that was to bland tumor thrombus, since preoperative chest was normal. All patients underwent excretory uro 5raphy with nephrotomogrnphy, selective renal arteriography, inferior venacavography and pulmonary tomography as part of the preoperative evaluation. In addition, most patients also had liver and bone scans, and patients with large tumors had celiac angiography. All patients were considered free of metastatic disease on the basis of these studies, although 4 had ambiguous findings, with
a questionable chest lesion shown in 3 and a questionable bone lesion demonstrated in l. The renal cell carcinoma originated in the right kidney in 21 patients (88 per cent) and in the left kidney in 3. In 9 of the 24 patients (38 per cent) the tumor in the inferior vena cava did not extend beyond the level of the renal veins (fig. 1). The tumor reached the level of the lower hepatic veins in 11 patients (46 per cent) and it extended either to the level of the diaphragm or into the right atrium in 4 (16 per cent). All patients underwent thoracoabdominal radical nephrectomy, The inferior vena cava was resected closed technique with margins free of tumor in 12 patients. In the remainder the tumor was removed from the inferior vena cava venacavotomy with extraction, with or without removal of a cuff of inferior vena cava (fig. 2). The pathology reports did not note c.v,,w,"cc,uc.,y whether the tumor invaded the inferior vena caval wall or extended into the inferior vena cava without When invasion of the inferior vena caval wall was found at operation it usually was limited to the area of the inferior vena cava at the renal vein. The resection was complete in 21 patients, while macroscopic residual disease remained postoperatively in 3 'Nith involvement above the lower veins. Histologic examination of regional lymph nodes removed at operation showed metastases in 5 patients. One of the patients (case 19) had a questionable chest lesion preoperatively and lymph node metastases (table This patient, thus, represents 2 of the 12 instances of negative prognostic factors. Only 13 of the 24 cases (54 per cent) did not exhibit poor prognostic factors, such as preoperative evidence of distant metastases, incomplete tumor resection or metastases to regional lymph nodes. RESULTS
One patient in the favorable subgroup was lost to followup 7 Accepted for publication August 29, 1980. months postoperatively and is presumed dead (case 21). One Read at annual meeting of American Urological Association, San other patient in that subgroup died without tumor 3 months Francisco, California, May 18-22, 1980. * Requests for reprints: 319 Longwood Ave., Boston, Massachu- postoperatively. The mean survival was 21 months (fig. 3). In the subgroup of setts 02115. 769
-- -
-
770
KEARNEY AND ASSOCIATES TABLE
1. Data on 24 patients operated on for extension of renal cell carcinoma to the inferior vena cava
Questionable Preop. Findings• Chest
Complications
Resection Kidney
Pt.-Age-Sex
Tumor Level in Inferior Vena Cava
Rib
Technique
Proceduret
Completeness:j:
Rt. Lt. Rt. Rt. Rt. Rt. Rt.
Renal vein Hepatic vein Renal vein Renal vein Diaphragm Renal vein Rt. atrium
Open Closed Open Closed Open Open Open
Fig. 2,A Fig. 2,E Fig. 2,A Fig. 2,A Fig.2,A Fig. 2,A Fig. 2,A
C C C C I C C
8-73-M 9-49-F 10-69-M
Rt. Rt. Rt.
Renal vein Renal vein Diaphragm
Closed Open Open
Fig. 2, B Fig. 2,A Fig.2,A
I
11-74-M
Lt.
Renal vein
Open
Fig. 2,D
C
12-26-M 13-53-M 14-60-M
Rt. Rt. Rt.
Renal vein Hepatic vein Hepatic vein
Open Open Closed
Fig. 2,A Fig.2,B Fig.2,B
C C C
15-52-M 16-57-F 17-71-F 18-58-M 19-63-M 20-66-F 21-70-M 22-52-M 23-60-M 24-61-F
Rt. Rt. Lt. Rt. Rt. Rt. Rt. Rt. Rt. Rt.
Renal vein Diaphragm Hepatic vein Hepatic vein Hepatic vein Hepatic vein Hepatic vein Hepatic vein Hepatic vein Hepatic vein
Closed Open Open Closed Closed Closed Closed Closed Closed Closed
Fig. 2, C Fig. 2, A Fig. 2, D Fig.2,B Fig. 2, B Fig. 2, C Fig. 2,B Fig. 2, C Fig. 2, C Fig. 2, B
C I C C C C C C C C
1-54-M 2-55-M 3-45-F 4-60-F 5-72-F 6-39-F 7-68-F
X
X X X
Node Involvement
Survival Renal Failure
Other
X
Sepsis
X
Arrhythmia, respiratory failure
X
C
X\I
C
Arrhythmia, wound infection Splenic laceration
X
X
Deep vein thrombosis rt. leg X
Arrhythmia X X X X X
Dead, 12 mos. Dead, 3 mos.§ Dead, 36 mos. Dead, 36 mos. Dead, 48 mos. Dead, 12 mos. Dead, 6mos. Alive, 30 mos. Alive, 6 mos. Dead, 8mos. Dead, 13 mos. Dead, 4mos. Dead, 10 mos. Alive, 18 mos. Dead, 40 mos. Dead, 48 mos. Dead, 24 mos. Dead, 24 mos. Dead, 5mos. Dead, 6mos. Dead, 7 mos. Alive, 69 mos. Dead, 24 mos. Dead, 6mos.
• Later shown to be metastatic disease. t Patients 1, 3, 5, 6, 7, 9, 10, 12 and 16 had the venacavotomy performed by the open technique. Patient 4 underwent the closed technique. :j: C, complete, I, incomplete. § Dead without evidence of disease. JI Did not require dialysis.
t~
_LEVEL CF INWL/..EMNl_ __
Atrium-Diaphragm
Lower Hepatic Veins
Renal Veins
A
B
C
NO. of Pts.
¼
4
16
---8
11
46
---c
9
38
Toto/
24
FIG. 1. Levels of tumor extension in inferior vena cava and number of patients in this series with tumor at various levels
13 cases without negative prognostic factors the average survival (20 months) was similar to that of the group as a whole. The range of survival times in the subgroup (3 to 69 months) was identical to that of the entire group. All 4 patients with preoperative studies that ambiguously suggested metastatic disease proved to have metastases in the questionable areas and all eventually died. The survival for these 4 patients ranged from 5 to 24 months, with a mean of 10
months. In contrast, patients without preoperative metastases had a mean survival of 23 months (range 3 to 69 months). The 5 patients with positive lymph nodes died and their survival averaged 19 months (range 5 to 24 months). Twenty patients (83 per cent) are known or presumed to have died. For these patients survival ranged from 3 to 48 months, with a mean of 19 months. Four patients, all of whom belonged to the subgroup with neither disseminated nor resid-
FIG. 2. Surgical techniques used in inferior vena caval resection for renal cell carcinoma. A, venacavotomy with tumor extraction with open or closed technique-used for tumor originating in right kidney and extending to level of :renal veins. B, ligation of left renal vein and inferior vena cava-done in cases with tumor on right side and extensive involvement at level of renal or lower hepatic veins. C, ligation of inferior vena cava distal to renal veins with maintenance of continuity of left renal vein and proximal inferior vena cava-used for tumor un,1s,uau1J,g in right kidney with extensive involvement of inferior vena cava at level of renal veins in non-collateralized D, venacavotomy with extraction tec:h1~iC[Ut,--p1,rfon;-rn,d in cases with tumor originating in left E, ligation inferior vena cava with maintenance of venous by renal vein-to-portal vein interposition m,.--u.,,1cu cases v,ith tumor on left side and extensive involvement of
postoperatively of Postmortem examination Other complications included thrombosis, m-,·nv,n,n ble 1). as a of lovver veins, did not occur in any DJSCUSSION
of rnnal cell carcinoma,
0
·40
60
80
PIG,_ 3. 9um1r,_~ative s~:rviv~J ,...of_ 24 patients vvho undervvent :rer.eoval of ren&.l cell ca.rc1norn2 tro:rr.: :nreno:r vena cava.
ual disease, a.re Nithout evidence of disease 6 to 69 months and their nH,an survival tiine is 30 months. The repn,sent 17 pe:r cent of the group as a whole per cent of the vvithout negafr1e prognostic factors. Of the 24 7 (29 per cent) had oliguria with renal failure in the immediate postoperative period and 6 of these required dialysis. A closed resection of the tumor in the inferior vena cava had been done in 4 of the 7 cases, while in 3 the remaining renal vein had been occluded temporarily or permanently as part of the surgical procedure. One of the patients with :renal failure died and this represented the only operative death (4 per cent) in the series. In this patient (case 2) there was a tumor on the left side, extending to the level of the hepatic veins, that required temporary interruption of the venous supply to the right kidney followed 0
2 of these have a <2 y.sars. In a treated between 1935 and 1965, 6 of 11 m1t1en,ts (55 per cent) who had inferior vena caval involvement without evidence of distant metastases were found to have survived at least 5 years after resection." ,-,.,,,,,.,,.,,, . . while this study has provided the basis for the optimism with which inferior vena caval involvement has been viewed it did not report the level of tumor extension in the inferior vena cava. The patients who had good survival might have had minimal extension from the renal vein found at operation and, therefore, might not be comparable to patients who have extensive involvement demonstrated inferior venacavography. The survival rate documented in other studies falls short of 55 per cent. In a 1977 study it was found that 4 of 12 patients (33 per cent) without metastatic disease who had been operated cu,,c,~,,.o,
~,o-
772
KEARNEY AND ASSOCIATES TABLE 2.
Reference Gleason and associates 14 Cole and associates3 Beck5 Pathak15 Esho and Owoseni16 Martinek17 Musiani18
Literature review of vena caval resection for renal cell carcinoma
Preop. Metastases
Node Involvement
Level of Vena Caval Tumor
Status
Yes Yes No No No Yes No ? ? Yes
Yes Yes No No No No Yes ? ? ?
Rt. atrium Hepatic vein Renal vein Renal vein Hepatic vein Hepatic vein Renal vein Renal vein Renal vein Rt. atrium
Alive with disease Dead Alive without disease Alive without disease Alive without disease Dead Alive with disease Alive without disease? Dead Alive W\th disease
on for renal cell carcinoma involving the inferior vena cava survived >2 years. 6 Although less favorable these results, nevertheless, seem encouraging. However, examination of the data shows that 3 of the 4 survivors had recurrent disease at last reported followup. Most other studies involve only a few cases, frequently with limited followup. Ten cases reported in 7 studies had a mean followup of 17 months (table 2). 3' 5 • 14- 18 Of these patients 4 were known to be free of metastases preoperatively, including 3 who were alive without disease 3 to 12 months postoperatively. Although our study suggests that the survival rate may be much lower than is suggested in the literature patients with inferior vena caval involvement but without distant metastases should not be denied an operation. Because there is no effective adjuvant therapy for renal cell carcinoma an operation should be offered to such patients in the hope of averting possible complications16• 19 and prolonging survival. While the average survival of such patients in this group was 23 months the survival ranged to 69 months. Patients with findings that suggest the presence of metastases should not be operated on before completion of careful metastatic diagnostic studies, including biopsy of suspicious lesions. All 4 patients with suspicious preoperative findings in our series were shown later to have metastatic disease in those areas. Their mean survival of 10 months was less than half that of the group as a whole and is comparable to that of patients reported elsewhere who had clear evidence of metastatic disease preoperatively, none of whom survived >12 months. 6 Inferior vena caval resection can be done safely and with little mortality. 1• 18• 20-24 The surgical techniques have been well established, although the procedure, which had been done as early as 1905,3 was not performed widely until the 1960s.6 • 16 The development of cardiopulmonary bypass techniques with circulatory arrest now even permits the safe resection of tumor extending into the right atrium. 14• 18• 21• 25 The surgical options depend on the kidney involved and on the level of tumor extension in the inferior vena cava (fig. 2). Although ultrasound26-28 and computerized tomography29 have shown promise in demonstrating vena caval involvement venacavography in frontal and lateral views must be done to obtain an accurate assessment of the extent of disease that will permit careful planning of the surgical approach. 5• 6 • 14• 24• 30- 32 Multiple collateral pathways, including the ascending lumbar, adrenal and spermatic or ureteral veins, are available to drain the left kidney but the right kidney lacks a collateral venous supply. 20 Renal cell carcinomas originating in the right kidney extend more frequently into the inferior vena cava than do tumors of the left kidney, possibly because the shorter right renal vein more easily allows vena caval extension. Thus, in many cases suprarenal inferior vena caval resection may involve ligation of the left renal vein, which can be accomplished with little difficulty. However, because of the lack of collaterals to the right kidney procedures done for tumors on the left side must include preservation of the venous drainage of the right kidney. In cases of tumor on the right side in which the inferior vena caval involvement does not extend beyond the level of the renal veins the tumor thrombus may be recovered by venacavotomy,
Followup (mos.) 12 10 10 12 3 6
30 12 12 7
using an open or closed technique (fig. 2, A). When there is extensive involvement at the renal vein level ligation of the inferior vena cava above the renal veins is possible for tumors on the right side (fig. 2, B). Because the obstruction of the inferior vena cava by the intracaval tumor promotes development of a collateral blood supply33 the ligation carries little morbidity (case 14). However, in the non-collateralized patient it is desirable to maintain the continuity of the left renal vein and proximal inferior vena cava to avoid transient renal failure (fig. 2, C). When the tumor extends above the level of the lower hepatic veins closed resection of the inferior vena cava is not possible, even with division of the coronary and triangular ligaments of the right lobe of the liver. 20 Venacavotomy using the Foley catheter technique21 or compression of the porta hepatis to reduce hepatic blood flow (the Pringle maneuver) can be used to treat tumors at the upper hepatic vein or diaphragmatic level. The importance of proximal inferior vena caval control to reduce blood loss in disease at this level cannot be overemphasized. Controlling tourniquets should be placed around 1) the inferior vena cava proximal to the resection, either above or below the diaphragm or intrapericardially, 2) the inferior vena cava distal to the resection and 3) the renal vein. In cases with intra-cardiac extension cardiopulmonary bypass is essential. With the 2-team technique the operation generally is done through a median sternotomy rather than by a thoracoabdominal approach. Circulatory arrest has been used with success after the patient has been placed on cardiac bypass. With a tumor on the left side the venous supply to the right kidney can be maintained by an open resection with extraction of the tumor (fig. 2, D) or by interposing an end-to-side renal vein-to-portal vein graft (fig. 2, E). Of the 4 patients in this series who have survived without disease 3 were operated on by an en bloc, closed technique without tumor spillage. Of these 3 patients 2 represent our longest survivors, with 30 and 69-month survival, respectively. However, the inference that the closed technique is superior to an open venacavotomy with extraction of tumor thrombus is not warranted since, over-all, there was little difference in the survival of patients operated on by the closed and open techniques (22 and 19 months mean survival, respectively). While the operative mortality in our series was low (4 per cent) morbidity was common, although the complications were manageable. Of the 7 patients who had renal failure 6 required dialysis. Of the 6 patients requiring dialysis 3 had closed resections and 3 had interruption of the venous egress of the remaining kidney. The other complications encountered, sepsis, wound infection, and respiratory and cardiac arrhythmias, responded well to medical treatment. REFERENCES
1. Marshall, V. F., Middleton, R. G., Holswade, G. R. and Goldsmith,
E. I.: Surgery for renal cell carcinoma in the vena cava. J. Urol., 103: 414, 1970. 2. Svane, S.: Tumor thrombus of the inferior vena cava resulting from renal carcinoma. A report on 12 autopsied cases. Scand. J. Urol. Nephrol., 3: 245, 1969.
INFERIOR VENA CAVA RESECTION FOR RENAL CELL CARCINOMA
3. Cole, A. T., Julian, W. A. and Fried, F. A.: Aggressive surgery for renal cell carcinoma with vena cava tumor thrombus. Urology, 6: 227, 1975. 4. Tsuchida, S., Sugawara, H., Harata, T., Yamaguchi, 0. and Arai, S.: Diagnosis, treatment and prognosis of renal cell carcinoma. Tohoku J. Exp. Med., 113: 319, 1974. 5. Beck, A. D.: Renal cell carcinoma involving the inferior vena cava: radiologic evaluation and surgical management. J. Urol., 118: 533, 1977.
6. Schefft, P., Novick, A. C., Straffon, R. A. and Stewart, B. H.: Surgery for renal cell carcinoma extending into the inferior vena cava. J. Urol., 120: 28, 1977. 7. McCullough, D. L. and Talner, L. B.: Inferior vena caval extension of renal carcinoma: a lost cause? Amer. J. Roentgen., 121: 819, 1974.
8. Skinner, D. G., Pfister, R. F. and Colvin, R.: Extension of renal cell carcinoma into the vena cava: the rationale for aggressive surgical management. J. Urol., 107: 711, 1972. 9. Murphy, G. P.: Current results from treatment of renal cell carcinoma. In: Proceedings of the Seventh National Cancer Conference. Philadelphia: J. B. Lippincott Co., p. 751, 1972. 10. Editorial: Renal-cell carcinoma. Lancet, 2: 887, 1976. 11. Bottinger, L. E.: Prognosis in renal cell carcinoma. Cancer, 26: 780, 1970. 12. Wagle, D. G.: Vagaries of renal cell carcinoma. J. Med., 3: 178, 1972. 13. deKernion, J.B., Ramming, K. P. and Smith, R. B.: The natural
14.
15.
16. 17. 18.
II
history of metastatic renal cell carcinoma: a computer analysis. J. Urol., 120: 148, 1978. Gleason, D. M., Reilly, R. J., Anderson, R. M., O'Hare, J. E., Kartchner, M. M. and Komar, N. N.: Removal ofhypernephroma and inferior vena cava: right atrial tumor thrombus. Arch. Surg., 105: 795, 1972. Pathak, I. C.: Survival after right nephrectomy, excision of infrahepatic vena cava and ligation of left renal vein: a case report. J. Urol., 106: 599, 1971. Esho, J. 0. and Owoseni, A.: Vena cava resection with renal cell carcinoma. Eur. Urol., 3: lll, 1977. Martinek, J. B.: Surgical treatment of renal tumors penetrating into the great veins. Int. Surg., 55: 417, 1971. Musiani, U .: Hypernephroma of the right kidney with inferior vena
773
caval and right atrial thrombosis: case study and successful removal. J. Urol., 118: 472, 1977. 19. Freed, S. Z.: Nephrectomy for renal cell carcinoma with metastases. Urology, 9: 613, 1977. 20. McCullough, D. L. and Gittes, R. F.: Vena cava resection for renal cell carcinoma. J. Urol., 112: 162, 1974. 21. Freed, S. Z. and Gliedman, M. L.: The removal of renal carcinoma thrombus extending into the right atrium. J. Urol., 113: 163, 1975. 22. Lome, L. G. and Bush, I. M.: Resection of the vena cava for renal cell carcinoma: an experimental study. J. Urol., 107: 717, 1972. 23. Duckett, J. W., Jr .. Lifland, J. H. and Peters, P. C.: Resection of
the inferior vena cava for adjacent malignant diseases. Surg., Gynec. & Obst., 136: 711, 1973. 24. Waters, W. B. and Richie, J. P.: Aggressive surgical approach to renal cell carcinoma: review of 130 cases. J. Urol., 122: 306, 1979. 25. Paul, J. G., Rhodes, D. B. and Skow, J. R.: Renal cell carcinoma presenting as right atrial tumor with successful removal using cardiopulmonary bypass. Ann. Surg., 181: 471, 1975. 26. Greene, D. and Steinbach, H. L.: Ultrasonic diagnosis of hypernephroma extending into the inferior vena cava. Radiology, 115: 679, 1975. 27. Wines, R. D., Frawley, J. and Palmer, J.: The use of ultrasound in
28.
29.
30. 31.
32.
33.
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