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Ann Thorac Surg 2010;89:505-510. doi:10.1016/j.athoracsur.2009.11.025
© 2010 The Society of Thoracic Surgeons
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Original Articles: Adult Cardiac

Renal Carcinoma With Supradiaphragmatic Tumor Thrombus: Avoiding Sternotomy and Cardiopulmonary Bypass

Gaetano Ciancio, MDa,*, Samir P. Shirodkar, MDb, Mark S. Soloway, MDb, Alan S. Livingstone, MDc, Michael Barron, MDd, Tomas A. Salerno, MDe

a Department of Surgery, Division of Transplantation, University of Miami Miller School of Medicine, Miami, Florida
b Department of Urology, University of Miami Miller School of Medicine, Miami, Florida
c Department of Surgery, Division of Surgical Oncology, University of Miami Miller School of Medicine, Miami, Florida
d Department of Anesthesia, University of Miami Miller School of Medicine, Miami, Florida
e Department of Surgery, Division of Cardiothoracic Surgery, University of Miami Miller School of Medicine, Miami, Florida

Accepted for publication November 9, 2009.

* Address correspondence to Dr Ciancio, University of Miami Miller School of Medicine, Department of Surgery, Division of Transplantation, PO Box 012440, Miami, FL 33101 (Email: gciancio{at}miami.edu).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
Background: Renal cell carcinoma with tumor thrombus extension into the inferior vena cava (IVC) is rare. Surgical resection provides the only reasonable chance for cure, but the approach poses a challenge to the surgical team. We describe our technique to safely resect these tumors through a transabdominal incision that exposes the intrapericardial IVC and right atrium (RA) transdiaphragmatically, without the use of sternotomy, cardiopulmonary bypass (CBP), or deep hypothermic circulatory arrest (DHCA). Clinical outcomes of these patients and techniques are reported.

Methods: Between May 1997 and January 2009, 102 patients (mean age, 63 years) underwent resection of renal tumor extending into the IVC by techniques developed to avoid sternotomy and CBP. The tumor thrombus in 12 patients (13%) extended into the supradiaphragmatic IVC and RA.

Results: Complete resection was successful through the transabdominal approach without CBP in all patients. Mean operative time was 8 hours 15 minutes. Estimated blood loss was 2960 mL, and a mean of 9 U of blood was transfused. Two patients died postoperatively, 1 on day 4 of arrhythmia and 1 on day 22 of multisystem organ failure. All discharged patients were alive at the last follow-up. Three patients had tumor recurrence and have been referred for adjuvant therapy.

Conclusions: In select cases, renal cell carcinoma extending into the IVC to the intrapericardial level and RA can be resected without sternotomy, CBP, or DHCA.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 References
 
Tumor thrombus in the inferior vena cava (IVC) occurs in 4% to 10% of patients with renal cell carcinoma (RCC) and poses a challenge for the surgical team [1]. Because there is no systemic therapy available to significantly reduce tumor burden, surgical intervention is the only treatment [2, 3]. However, the surgical approach is associated with significant morbidity and mortality. To minimize operative complications, adequate exposure and a virtually bloodless surgical field in the upper abdomen and retroperitoneum are essential.

The IVC must be opened when it is involved with tumor. Surgeons, therefore, must know preoperatively the precise extent of the tumor and thrombus, allowing them to plan their approach accordingly [4]. When the thrombus extends above the diaphragm, the use of cardiopulmonary bypass (CPB) and accompanying deep hypothermic circulatory arrest (DHCA) have usually been advocated [5–7]. However, complications inherent to CPB and DHCA, such as coagulopathy and central nervous system complications [1, 2, 6], have led us to search for an alternative surgical approach to these tumors [4, 8, 9]. Few cases have been reported describing the surgical approach of avoiding sternotomy, CPB, and DHCA when dealing with RCC tumor thrombus extending into the intrapericardial IVC or right atrium [10–12].

Our surgical approach has been applied to complex situations, including removing adherent [13] and nonadherent [14] level IV (intraatrial) tumor thrombus from RCC without a thoracoabdominal approach, median sternotomy, CPB, or DHCA. The purpose of this study is to describe the surgical technique used in 12 patients (including 4 patients with Budd-Chiari syndrome) with large RCC with tumor thrombus extending into the supradiaphragmatic IVC and RA, who underwent extensive resection without sternotomy, CPB, and DHCA. Clinical outcomes and follow-up of these patients are detailed.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
The Center for Institutional Review Board (IRB) approved the study, and waved patient consent for this retrospective chart review.

Between May 1997 and January 2009, 102 patients with a preoperative diagnosis of RCC and tumor thrombus in the IVC underwent surgical resection and removal of the thrombus. Clinical variables are presented in Table 1. The cranial extent of the tumor was partly defined as suggested by Neves and Zincke [2]; however, we used our own previously reported definition for level III thrombus [4]. Level I thrombus (renal vein only) was present in 25, level II thrombus (infra-hepatic IVC) in 13, level III thrombus in 52, according to the definition we use in our institution [4], and level IV (intraatrial thrombus) in 12.


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  		Table 1 Staging of Tumor Thrombus Level in Renal Cell Carcinoma
 
The 12 patients (5 men, 7 women) with supradiaphragmatic thrombi were a median age of 63 years (range, 42 to 80 years). They underwent surgical resection of a large RCC with vena caval thrombus through an abdominal incision using a transdiaphragmatic approach. Median sternotomy, CBP, venovenous bypass, or DHCA were not used. The intrapericardial IVC entering the RA was approached through the abdominal cavity. The renal tumor was at the right side in 9 and on the left in 3. Five patients were staged as level IIId (supradiaphragmatic) [4] and 7 were level IV (intraatrial thrombus).

The preoperative diagnosis and work-up included measurements of serum electrolytes, creatinine, urea nitrogen, and alkaline phosphatase; liver function tests, chest roentgenogram, ultrasound imaging, chest and abdominal computed tomography (CT), and selective use of magnetic resonance imaging (MRI). Additional studies were done to evaluate cardiac and respiratory status. Medical clearance was ascertained in all patients. Preoperative CT, MRI, and echocardiography were used to determine thrombus level. Preoperative embolization was not performed. Intraoperative transesophageal echocardiography (TEE) was used to assess mobility of the thrombus and to guide the surgeon when a partial clamp was applied in the RA to confirm patency of the coronary sinus.

Surgical Technique
A modified chevron incision is used, commencing approximately two fingerbreadths below the right costal margin and extending out laterally to the midaxillary line. The right kidney is mobilized laterally and posteriorly, and the perirenal collateral circulation is ligated. The renal artery is identified, ligated, and divided. The collateral circulation collapses, making the rest of the dissection easier [15].

The ligamentum teres is ligated and divided, and the falciform ligament is divided with cautery. The incision is continued around each portion of the divided falciform ligament to the right superior coronary ligament. The left triangular ligament is also divided. The central diaphragm tendon is dissected until the supradiaphragmatic intrapericardial IVC is identified (Fig 1). The dissection is circumferential so that the intrapericardial IVC can be encircled below or above the confluence into the RA. The RA is gently pulled beneath the diaphragm and into the abdomen. If more exposure of the RA is required, the central tendon of the diaphragm is incised in the midline, the pericardium is exposed, and pericardiotomy is performed.


Figure 1
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  		Fig 1. Intraoperative photo shows diaphragm of dissected suprahepatic inferior vena cava (IVC). The intrapericardial IVC is exposed through the abdominal cavity. Curved arrow shows mobilization of the diaphragm.

 
Intraoperative TEE is critical to delineate the cranial extent and mobility of the thrombus and also during the dissection of the supradiaphragmatic IVC and RA. Also, it guides the surgeon during application of the partial clamp in the RA to make sure that the clamp excludes the tumor and is not impinging on the coronary sinus.

The visceral peritoneum on the right side of the hepatic hilum—just below the inferior edge of the liver—and the infrahepatic IVC are incised with the right inferior coronary and hepatorenal ligaments. Because of the collaterals, we advise ligation and division of all tissue in a plane starting from the right and advancing toward the hilum.

The liver is gradually rotated to the left, exposing the right superior coronary ligament. After the incision of this ligament, the liver can be further rotated to the midline, exposing the retrohepatic IVC, gaining access to small hepatic veins passing from the right and caudate lobe to the IVC, which are ligated and divided. The liver is dissected off the IVC, and the only remaining structural attachments are the hepatic veins and the porta hepatis (piggyback liver mobilization; Fig 2A). An opening in the lesser omentum allows control of the porta hepatis with a Rummel tourniquet or a vascular clamp to allow Pringle's maneuver (occlusion of blood inflow to the liver).


Figure 2
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  		Fig 2. Drawing shows abdominal removal of renal cell carcinoma with level IV thrombus (intraatrial tumor thrombus). (A) The abdominal inferior vena cava (IVC) is exposed by mobilizing the liver off the retrohepatic IVC. (B) The central tendon of the diaphragm and the IVC are dissected off the posterior abdominal wall (dotted lines). The right atrium, distal IVC, porta hepatis, and left renal vein are clamped. (C) The surgeon's fingers are wrapped around the IVC to perform the milking down process. A vascular clamp is placed below the hepatic veins, and the porta hepatis clamp is released. Hepatic venous drainage is permitted during closure or reconstruction and the IVC.

 
A plane is created between the IVC and posterior abdominal wall. Small tributaries can become engorged to look like lumbar vessels, and they are identified and ligated. The advantage of creating this plane is to facilitate circumferential control of the IVC. Vascular isolation of the IVC is then achieved superior and inferior to the thrombus and the left or right renal veins.

The tumor thrombus is then "milked" downward out of the RA, and the intrapericardial IVC (TEE identified any free floating thrombus) so that it is below the level of the major hepatic veins. This allows the hepatic veins to drain into the IVC so venous return is not compromised. This technique allows hepatic venous drainage during inspection and closure or reconstruction of the IVC. If the IVC were tethered to the wall, any attempts to milk down the thrombus would exert traction on the wall and could result in a tear. Milking down of thrombus is facilitated by IVC mobilization, because the surgeon's fingers can wrap around the IVC circumferentially, thereby avoiding embolization.

In some circumstances, the tumor thrombus is bulky, not freely mobile, or adherent to the IVC or RA, or both. Pringle's maneuver is performed to temporarily occlude blood inflow to the liver. Vascular clamps are placed in the following order: the infrarenal IVC and the left or right veins are controlled, and a Satinsky clamp is placed across the RA, under TEE monitoring, or across the intrapericardial or suprahepatic IVC in level IIId tumor thrombi (Fig 2B). For left-side tumor, the right adrenal vein is also clamped.

The IVC is incised from the diaphragm to the renal vein, and the tumor is removed (for a large mobile tumor thrombus) or dissected sharply off the IVC wall (for adherent tumor thrombus). The 3 major hepatic veins are visualized, their orifices are inspected, and invading tumor is removed (Budd-Chiari syndrome). After tumor thrombus is removed and the upper cava is closed, the vascular clamp is repositioned below the hepatic veins. Pringle's maneuver is discontinued, and blood flow to the liver is reestablished (Fig 2C). Clamping below the major hepatic vein allows for a short Pringle maneuver. The remaining IVC below the hepatic veins is sutured closed.

When tumor cannot be safely pulled down from below, as has occurred in 4 patients not included in this series with level IV thrombus, a sternotomy is performed. The heart is cannulated through the ascending aorta and superior vena cava, which is snared once normothermic CPB is established. The RA is open and blood from the coronary sinus is aspirated with a pump suction catheter. The tumor is completely removed and the RA is inspected. The RA is then closed and CPB is discontinued.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
Twelve patients underwent radical nephrectomy with complete extraction of tumor thrombus from the supradiaphragmatic IVC without median sternotomy, CPB, or DHCA. Extensive mobilization provided a bloodless area in a deep retrohepatic field to allow removal of the primary tumor and the thrombus.

The operative time was 8 hours 6 minutes (range, 4 hours 15 min, to 11 hours 4 min). Estimated blood loss was 2960 mL (range, 500 to 7000 mL), and a mean of 9 U of blood (range, 0 to 16 U) was transfused intraoperatively. Cell-saving techniques, used routinely in our institution, were only needed in 8 of the 12 patients.

Three patients had blood loss of 6000, 6000, and 7000 mL, respectively. The tumor thrombus was bulky in these patients and extended to the RA, involving the hepatic veins and causing a Budd-Chiari syndrome. This added to the problem of aberrant systemic venous drainage, resulting from complete IVC obstruction. The congested liver was amenable to complete mobilization, and the suprahepatic, intrapericardial IVC, and RA were exposed by the abdominal approach. Blood loss in these patients was a combination of multiple varices associated with Budd-Chiari syndrome and the aberrant systemic venous drainage resulting from the IVC obstruction. Another patient had level IIId (supradiaphragmatic) tumor thrombus also causing a Budd-Chiari syndrome, but her blood loss was only 500 mL.

Splenic tear in 1 patient was repaired with Vicryl mesh (Ethicon, Somerville, NJ) with no further sequela. No other intraoperative complications occurred. There were no intraoperative deaths. No pulmonary emboli of any cause were seen on clinical or ultrasonographic evaluation by TEE.

The mean size of the renal mass was 6 cm (range, 3.2 to 13 cm). Histopathologic examination revealed RCC of clear type in 10 patients, papillary type in 1, and granular type in 1. Tumors were grade IV in 3 patients, grade III in 7, grade II in 1, and grade I in 1 (Table 2). Lymph node metastasis was found in 1 patient, who also had a small, unexpected, 2-cm liver metastasis. Another patient had a single, unexpected, small liver metastasis of approximately 3 cm. These were completely removed in both during the nephrectomy. An additional patient had an unexpected mesenteric mass that final pathology documented as metastatic RCC. The level of the thrombus on CT or MRI correlated with intraoperative findings.


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  		Table 2 Pathologic Features
 
Postoperatively, average intensive care unit length of stay was 7 days (range, 1 to 17 days). Median length of stay in those discharged was 12 days (range, 7 to 22 days). The oldest patient, who was 80 years old and had a level IIID tumor, died on postoperative day 4 of cardiac arrest due to arrhythmia. Patient 7 had a difficult postoperative course and could not be weaned from the ventilator. She had acute respiratory distress syndrome, and care was withdrawn on day 22 after repeated episodes of multisystem organ failure and sepsis. No autopsy was performed. One patient required reoperation for abdominal wall hematoma caused by subcutaneous injection of low-molecular-weight heparin. No intraabdominal or retroperitoneal pathology was noted at laparotomy in this patient. None of the patients discharged from the hospital needed dialysis postoperatively.

Two of the discharged patients were lost to follow up. Of the remaining patients, 3 have had tumor recurrence postoperatively. Pulmonary metastases were noted at 1 year on surveillance radiography in patient 9, and new and enlarging pulmonary nodules were found at 3 years in patient 10. Given his age and excellent functional status, he was prescribed tyrosine-kinase inhibitor therapy in the adjuvant setting. A 6-month postoperative CT scan documented recurrence in the left renal fossa in patient 12. She was referred to the oncology service, and plans were made to begin an adjuvant trial shortly. No other patients had evidence of recurrence or residual disease on postoperative imaging.


   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
Survival at 5 years after extirpative surgical intervention has been reported to be 32% to 69% in patients with a tumor thrombus invading the IVC [2, 3, 16–18]. When preoperative evaluation reveals metastasis, palliative operations often have a place in treating IVC syndrome or symptoms associated with the primary tumor, including polycythemia and paraneoplastic syndromes [17, 19], but the prognosis in this setting remains poor [17, 18]. Excision of the entire tumor is mandatory for a reasonable attempt at a long survival, as demonstrated by Nesbitt and colleagues [20] and Hatcher and colleagues [21], where no patients with incomplete local resection survived to 5 years.

The operative approach depends on the cranial extent of the IVC thrombus. Although level I and II thrombi can be adequately managed by proximal and distal control of the IVC and the contralateral renal vein, extension of the thrombus up to or beyond the hepatic veins is more challenging. Optimal operative management is debatable in this situation, especially in the 10% to 25% of patients in whom the thrombus extends above the hepatic veins [22]. Prevention of major bleeding, embolism from tumor thrombus, and hepatic and renal dysfunction during dissection requires the development of techniques to manage these problems. One commonality to these new techniques is the clear and bloodless exposure of the entire IVC [4, 7] after proximal and distal control above and below the level of the tumor thrombus has been achieved.

Budd-Chiari syndrome is a rare disorder resulting from occlusion of the major hepatic veins or the suprahepatic IVC. Different conditions predispose to the development of Budd-Chiari syndrome, but hepatocellular, adrenal, and renal cell carcinoma are the most common malignant causes [23–25]. A hepatic vein obstruction that causes Budd-Chiari syndrome is an adverse feature.

Portosystemic varices add to the problem of enlarged caval collaterals. Meticulous attention to homeostasis is essential. Liver congestion makes mobilization more difficult, and poor liver function and increased third-space losses due to portal hypertension further complicate postoperative management and can be associated with life-threatening sequela, such as hepatic failure [23]. In 4 of our patients with hepatic vein occlusion and secondary Budd-Chiari syndrome, collateral circulation and varices of sufficient magnitude partially compensated for the greatly reduced outflow from the hepatic veins. These extensive collaterals, caused by both the IVC and hepatic vein occlusion, make the operation especially challenging. Our technique allows complete removal of all gross tumor extending into the hepatic veins and can be used in conjunction with CBP when necessary.

CBP, with or without DHCA, has been used in patients with RCC with tumor thrombus [6, 7]. CPB with hypothermia may be associated with platelet dysfunction, however, and when combined with systemic use of heparin, coagulopathy and bleeding from the retroperitoneum are risks [5–7]. CBP is necessary if there is a large intraatrial thrombus; however, patients with a small atrial adherent thrombus or IIId tumor extension [4] usually do not require CBP.

Stewart and colleagues [7] as well as Langenburg and colleagues [26] demonstrated increased blood loss and transfusion requirements in patients with level III or IV thrombus who underwent CBP with or without DHCA. They concluded that the risk of bleeding, sepsis, and multiorgan failure sometimes associated with CBP and DHCA did not justify their routine use in this setting.

Further data have shown that CPB often results in renal dysfunction, which may be subclinical or manifests as postoperative acute renal failure [27, 28]. In patients with increased risk of renal failure secondary to nephrectomy [29], maximal conservation of renal function is of paramount importance. This is the main reason why we favor our approach in this patient population, despite advances in CPB in recent years. We believe that increased operative time and slightly increased blood loss are acceptable to reduce the risk of future dialysis with its attendant complications in these patients. Fortunately, none of our patients have needed dialysis after discharge from the hospital.

Venovenous bypass [30] is an alternative, but not without risk, because complications such as lymphocele, infection, vessel injury to the vascular access, and air embolism have been reported [31]. The development of collateral drainage of the IVC, through communication with ascending lumbar veins and the azygous/hemiazygous system in the setting of the longstanding obstruction of the cava, can help to avoid hemodynamic alteration during the procedure [32]. Procedures used to reduce bleeding or hypotension, such as clamping the aorta, the superior mesenteric artery, and contralateral renal artery, are not necessary using our surgical technique.

Perioperative TEE is an important adjunct during the surgical procedure, allowing for real-time visualization of the cranial extent of the tumor thrombus. It should be used uniformly in these cases. TEE has multiple uses, including monitoring of movement of the thrombus, accurately placing vascular clamps to exclude the thrombus, preventing occlusion of the coronary sinus, observing for tumor or air emboli, and evaluating cardiac function and motion [33] No pulmonary emboli were seen intraoperatively, and there were no clinical indicators of pulmonary emboli postoperatively, which would have triggered a deeper evaluation.

We add our experience with resection of IVC tumor thrombi without CBP to that of others, because the outcome is at least comparable to CPB techniques, with lower morbidity and mortality. Coagulopathy was not seen in our patients, nor were neurologic sequela. Pulmonary complications, chest tube drainage, and sternal dehiscence were avoided using this surgical approach.

A further technical point that significantly aids in the operation is the use of complete piggyback liver mobilization [4, 8]. This technique facilitates thrombectomy because the cavotomy may be extended cranially to remove any adherent tumor thrombus. This exposure also minimizes the IVC occlusion time. After milking the thrombus below the hepatic veins is completed, the upper clamp may be repositioned to restore hepatic venous drainage. Sometimes a curved vascular clamp may be placed longitudinally at the cavotomy site to facilitate repair after tumor removal while the remaining renal vein is unclamped, thereby minimizing renal ischemia. The excellent exposure provided with the piggyback mobilization facilitates complete tumor extraction and eliminates residual tumor thrombus. Resection of the IVC wall was not necessary in our series. Concomitant fusiform dilatation of the IVC offers redundancy, thereby allowing closure of the vessel to its normal caliber. Although prosthetic grafts can be successfully placed in this setting, we avoid them to prevent anticoagulant therapy.

Resection of these complex tumors requires expertise of a team consisting of a transplant surgeon, urologic oncologist, a cardiothoracic surgeon, and an anesthesiologist familiar with intraoperative TEE. CPB should be readily available in the operating room, with the perfusionist on stand-by. Planning of the procedure is of great importance, familiarizing the team with the anatomy of the disease and the approach to be used.

In conclusion, surgical resection of supradiaphragmatic and intraatrial RCC tumor thrombus in the IVC is a challenge. The procedure has historically been performed using CPB techniques with low flows, DHCA, or distal clamping of the aorta for a short period. Morbidity and mortality of these adjuncts are well known, however, and have a significant effect on patient survival and recovery. The alternative technique we present uses abdominal and transdiaphragmatic approach to these lesions, without sternotomy, CPB, or DHCA. In our series, there were no complications related to the procedure and no operative deaths or pulmonary emboli. It has become our preferred approach to treat these complex renal tumors.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

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A. Culliford
Invited Commentary
Ann. Thorac. Surg., February 1, 2010; 89(2): 511 - 511.
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