Original Article
Application of cardiopulmonary bypass for resection of renal cell carcinoma and adrenocortical carcinoma extending into the right atrium
TATSUMASA OCHI, NOZOMU TANJI, KENJI SHIMAMOTO, TETSUHIRO IKEDA, AKIHIKO TOSHINO AND MASAYOSHI YOKOYAMA
Department of Urology, Ehime University School of Medicine, Tohon City, Ehime, Japan
Aim: The application of cardiopulmonary bypass to atrial involvement represents an important advance that has improved the safety and technical efficacy of a difficult surgical undertaking. Our experiences of the management of extended thrombi into the right atrium in patients with retroperitoneal malignancy using a cardiopulmonary bypass were discussed.
Methods: Data were reviewed for five patients (two men and three women; mean age, 60.4 years; range, 49-79 years) with retroperitoneal tumors displaying intracardiac tumor extension. Tumors originated in the right kidney in four patients, and in left adrenal gland in one patient. Cardiopulmonary bypass was used in all cases.
Results: Mean total blood loss was 6059 mL. Mean operative time was 14.7 h. No intra- or postoperative complications due to surgical technique were encountered, and no significant bleeding occurred during incision of the inferior vena cava or after removal of tumor thrombus. The follow-up period ranged from 3 to 20 months with a mean of 12.6 months. Of the five patients, three died of metastatic diseases, one died of liver dysfunction and one remains disease free as of 18 months postoperatively.
Conclusions: Our experience indicates that this procedure can be safely used for atrial involvement. Although superior long-term survival cannot be shown yet, favorable early results and a lack of perioperative complications were identified.
Key words cardiopulmonary bypass, intracardiac tumor extension, retroperitoneal tumor.
Introduction
Retroperitoneal malignancies, such as renal cell carcinoma (RCC) and adrenocortical carcinoma, can extend into the inferior vena cava (IVC). Tumors may extend as far as the right atrium in a small number of the cases.1 Spread of the tumor may lead to infarction of the lungs or other organs. Moreover, tricuspid atresia, caused by extension into the right ventricle through the right atrium, may be fatal.
As caval invasion in the case of adrenocortical carci- noma is quite rare, prognosis in such cases remains unclear. The review of 29 cases by Hedican and Marshall shows a 5-year survival rate of <10%.2 In patients displaying non- metastatic RCC with involvement of the IVC, 5-year sur- vival rates range between 18% and 68% after complete surgical resection.3,4 Whereas some studies have suggested that the risk of metastases and early death is increased in patients with more cephalad extension of IVC thrombi,5,6 Bissada et al.7 reported that 38% of patients with intracar-
Correspondence: Nozomu Tanji MD PhD, Department of Urology, Ehime University School of Medicine, Shitsukawa, Tohon-city, Ehime 791-0295, Japan.
Email: tanji@m.ehime-u.ac.jp
Received 2 January 2005; accepted 18 August 2005.
diac tumor extension and no metastases were alive with no evidence of disease after appropriate surgical resection. Poor results of non-operative treatments have prompted us to attempt radical operations, as complete removal of the tumor thrombus probably provides the only chance of cure.
Radical operations for tumor extension into the right atrium require careful planning.3 Traditionally, a thoraco- abdominal approach with median sternotomy to provide adequate exposure and vascular control, and cardiopulmo- nary bypass has been used. Application of cardiopulmo- nary bypass to atrial involvement represents an important advance that has improved the safety and technical efficacy of a difficult surgical undertaking.
We describe herein our experiences with the mana- gement of extended thrombi into the right atrium in five patients with retroperitoneal malignancies, using a transthoracoabdominal approach with cardiopulmonary bypass.
Methods
Data were reviewed for five patients (two men, three women; mean age, 60.4 years; range, 49-79 years) who presented with retroperitoneal tumors displaying intracar- diac tumor extension (Table 1). Tumors originated in the right kidney in four patients, and in the left adrenal gland
| Case | Age/ gender | PS | Tumor side | Tumor size | CRPt | Laboratory data Hbį AlP§ Cat | Metastasis | Pathological data Diagnosis Grade Venous invasion | ||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| 1 | 49/F | 1 | Left | 8 cm | 1.07 | 10 | 189 | 10 | Lung | AC | – | – |
| 2 | 79/M | 2 | Right | 7 cm | 11.9 | 8.2 | 578 | 8.2 | – | RCC | G2 | + |
| 3 | 56/F | 1 | Right | 7 cm | 0.08 | 11.9 | 133 | NE | – | RCC | G2 | + |
| 4 | 51/F | 2 | Right | 12 cm | 7.24 | 7.6 | 602 | 8.9 | – | RCC | G2 | + |
| 5 | 67/M | 0 | Right | 5 cm | 0.53 | 13.1 | 279 | 9.7 | – | RCC | G1 | + |
1mg/dL; ¿ g/dL; §IU/L. AC, adrenocortical carcinoma; AIP, alkaline phosphatase; CRP, C-reactive protein; Hb, hemoglobin; NE, not examined; RCC, renal cell carcinoma.
in one patient. Level of vena caval involvement was pre- operatively determined using imaging studies including ultrasonography of the IVC, echocardiography and mag- netic resonance imaging. Accurate assessment of the ceph- alad extent of thrombus inside the right atrium using these imaging studies confirmed almost complete occlusion of the IVC lumen, but provided no evidence of vessel-wall invasion by tumor thrombus. In all patients, detailed pre- operative studies were performed to evaluate cardiac, renal and respiratory status.
For all patients with renal tumors, the renal artery was embolized using a steel coil 1 day before the operation. The surgical approach involved a thoracoabdominal inci- sion in all cases. First, the heart was exposed by cardio- thoracic surgeons. Next, the retroperitoneal vessels were exposed and the renal arteries secured. Regional lym- phadenectomy was not performed in any cases. The kid- ney was isolated outside the envelop of Gerota’s fascia. Liver and IVC mobilization techniques were important to achieve successful thrombus removal. Intraoperative ultra- sonography of the hepatic veins was valuable in patients with suspected intrahepatic tumor extension. If the tumor extended into the hepatic vein, partial hepatectomy was considered. The ascending aorta, right atrium and superior vena cava were then cannulated after systemic hepariniza- tion. Subsequent cannulation of the right femoral vein was performed through a small inguinal incision to obtain additional venous drainage. Cardiopulmonary bypass was performed next, without circulatory arrest or cooling of the patient (Fig. 1). The bypass circuit (SIII; Stockert, Munich, Germany) was associated with vacuum-assisted venous drainage with a released valve, providing a nega- tive pressure of 20-40 mmHg in the venous line. Vascular control was achieved by clamping the infrarenal and intra- pericardial IVC and the contralateral renal vessels. The hepatic artery and portal vein were clamped as well to reduce bleeding from the hepatic veins. The renal artery was ligated in the proximal position of the coil after gentle retraction of the ipsilateral renal vein. Tumor thrombus was extracted by simultaneous atrial and caval approaches, and removed along with the kidney. The IVC was irrigated, inspected and cleared of residual neoplastic tissues before closure. If removal of more than half of the IVC wall was needed, a polytetrafluoroethylene patch- graft was anastomosed to the remaining IVC with a run- ning 4-0 polypropylene cardiovascular suture. Finally,
SVC
Liver
Biopump
Tumor
IVC
sequential removal of the vascular clump, arrest of car- diopulmonary bypass, decannulation, vascular suture, administration of protamine sulfate and hemostasis were accomplished.
Results
Of the five patients, four presented with symptoms such as general fatigue, macrohematuria, or dyspnea on effort, and two displayed signs including foot edema related to vena caval obstruction. All patients underwent complete extrac- tion of thrombus from the IVC. Consequently, the plane between the thrombus and the intima was easily identified and the thrombus could be gently freed from the IVC wall and extracted whole. Mean total cardiopulmonary bypass
| Case | Bypass time (h) | Bleeding (mL) | Transfusion (U) | Operation time (h) | Adjuvant therapy | Prognosis (months postoperatively) | |
|---|---|---|---|---|---|---|---|
| 1 | 70 | 12 200 | 30 | 14.5 | (-) | 12 | Deadt |
| 2 | 50 | 4 045 | 40 | 11.5 | INFa | 10 | Deadį |
| 3 | 130 | 4 500 | 36 | 16.5 | INFa + IL-2 | 20 | Dead§ |
| 4 | 60 | 8 000 | 40 | 22 | INFa | 3 | Dead™ |
| 5 | 50 | 1 550 | 20 | 9 | INFa | 21 | Alive |
*Brain metastasis; ¿ Lung metastasis; §Liver metastasis; [Liver failure.
time was 72 min (range, 50-130 min) and weaning from bypass was uneventful (Table 2). No significant bleeding was noted during incision of the IVC or after removal of the tumor thrombus. Mean total estimated blood loss was 6059 mL (range, 1550-12 200 mL). Mean volume of transfusion was 29.2 U (range, 20-40 U). Mean operative time was 14.7 h (range 9-22 h). No intra- or postoperative complications due to surgical technique were encountered. Postoperative respiratory function remained normal.
Pathological examination revealed clear cell carcinoma in the four renal tumors, and adrenocortical carcinoma in the adrenal tumor. Symptoms and signs that were appa- rent preoperatively all resolved. Mean follow up was 12.6 months (range, 3-20 months). Of the five patients, three died of metastatic diseases, one died of liver dysfunc- tion and one remains disease free as of 18 months after surgery.
Discussion
The surgical approach to retroperitoneal tumor extending into the right atrium is challenging. Non-metastatic tumors are potentially curable provided complete removal of can- cerous tissue can be achieved. The presence of intracaval tumor extension does not affect any independent prognos- tic value in cases of RCC,8 whereas previous investigations have suggested that cephalad extent of tumor thrombus exerts a substantial impact on clinical prognosis.5 In addi- tion, dissection of tumor thrombus extending into the right atrium reportedly results in significant therapy-related mortality.5 However, the lower frequency of peri- and post- operative complications and improved long-term survival following extracorporeal circulation have been reported.8,9 Some reports advocate the use of cardiopulmonary bypass to facilitate removal of tumor thrombus, particularly tumor thrombus extending into the right atrium.10,11 Important goals are to minimize bleeding and prevent pulmonary embolism of the thrombus, which can have disastrous and often fatal consequences. Cardiopulmonary bypass can be safely used, allowing atrial and IVC thrombectomy to be performed in a bloodless and clearly visible operative field within a safe time interval. Resection can easily include parts of the vessel wall if infiltration is present. Some authors have advocated profound hypothermia and circu- latory arrest in patients.10,11 However, we achieved satisfac- tory visualization and excision using cardiopulmonary
bypass without hypothermia or circulatory arrest, avoiding potential renal, hepatic, neurological or septic complica- tions associated with circulatory arrest.
Use of liver and IVC mobilization techniques helps to achieve additional exposure and enables the surgeon to have excellent control of the IVC, thus minimizing blood loss, and allowing the IVC to be opened both below and above the liver so that tumor thrombus is removed as effec- tively as possible in a bloodless field.
However some concerns exist with regard to possible dissemination of carcinoma cells by means of extracorpo- real circulation. This problem of possible dissemination remains controversial. In addition, disadvantages include a comparatively more invasive procedure due to the need for sternotomy, in addition to the need for cardiopulmonary bypass equipment and the assistance of thoracic surgeons.
In conclusion, our experience indicates that this proce- dure is relatively safe. Although superior long-term sur- vival cannot be shown yet, favorable early results including improvement of symptoms such as general fatigue or loss of appetite after surgery and a lack of perioperative com- plications were identified. Further experience is necessary to evaluate whether this method can actually improve prog- noses in such cases. Anyway, the surgical challenges inher- ent in resecting intracardiac extension of retroperitoneal malignancies require close cooperation between the urolo- gist and gastrointestinal or cardiovascular surgeons.
References
1 Bissada NK, Finkbeiner AE, Williams GD, Weiss JB. Suc- cessful extraction of intracardiac tumor thrombus of renal carcinoma. J. Urol. 1977; 118: 474-5.
2 Hedican SP, Marshall FF. Adrenocortical carcinoma with intracaval extension. J. Urol. 1997; 158: 2056-61.
3 Hatcher PA, Anderson EE, Paulson DF, Carson CC, Rob- ertson JE. Surgical management and prognosis of renal cell carcinoma invading the vena cava. J. Urol. 1991; 145: 20-4.
4 Glazer AA, Novick AC. Long-term follow-up after surgical treatment for renal cell carcinoma extending into the right atrium. J. Urol. 1996; 155: 448-50.
5 Skinner DG, Pritchett TR, Lieskovsky G, Boyd SD, Stiles DR. Vena caval involvement by renal cell carcinoma. Sur- gical resection provides meaningful long-term survival. Ann. Surg. 1989; 210: 387-92.
6 Sosa RE, Muecke EC, Vaughan ED Jr, McCarron JP Jr. Renal cell carcinoma extending into the inferior vena cava: the prognostic significance of the level of IVC involvement. J. Urol. 1984; 132: 1097-100.
7 Bissada NK, Yakout HH, Babanouri A et al. Long-term experience with management of renal cell carcinoma involving the inferior vena cava. Urology 2003; 61: 89-92.
8 Kuczyk MA, Munch T, Machtens S, Grunewald V, Jonas U. The impact of extracorporal circulation on therapy- related mortality and long-term survival of patients with renal cell cancer and intracaval neoplastic extension. World J. Urol. 2002; 20: 227-31.
9 Welz A, Schmeller N, Schmitz C, Reichart B, Hofstetter A. Resection of hypernephromas with vena caval or right atrial tumour extension using extracorporeal circulation and
deep hypothermic circulatory arrest: a multidisciplinary approach. Eur. J. Cardiothorac. Surg. 1997; 12: 127-32.
10 Marshall FF, Reitz BA, Diamond DA. A new technique for the management of renal cell carcinoma involving the right atrium: hypothermia and cardiac arrest. J. Urol. 1984; 131: 103-9.
11 Novick AC, Kaye MC, Pontes JE, Mitchell CK, Cosgrove DM. Experience with cardiopulmonary bypass and deep hypothermic circulatory arrest in the management of retro- peritoneal tumors with large vena caval thrombi. Ann. Surg. 1990; 212: 472-7.