Resection of Intraabdominal Tumors With Cavoatrial Extension Using Deep Hypothermic Circulatory Arrest

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Christopher Lau, MD, Padraic O’Malley, MD, Mario Gaudino, MD, Douglas S. Scherr, MD, and Leonard N. Girardi, MD

Departments of Cardiothoracic Surgery and Urology, Weill Cornell Medical College, New York, New York

Background. Intraabdominal malignancies with cav- oatrial extension can be resected using cardiopulmonary bypass and deep hypothermic circulatory arrest (DHCA).

Methods. Twenty-five consecutive patients underwent resection of intraabdominal tumor with cavoatrial thrombectomy using DHCA at a single tertiary center. Recurrence-free survival, cancer-specific survival, and overall survival were estimated using Kaplan-Meier analysis.

Results. All patients had renal artery embolization preoperatively. Procedures were performed through a median sternotomy with bilateral subcostal incision. Tumors were resected under DHCA. Mean age was 57 ± 14 years, 60% were hypertensive, 20% were diabetic, 16% had coronary disease, 44% were smokers, 16% had neoplastic pulmonary embolism, and the mean creatinine was 1.4 ± 0.75 mg/dL. Mean cardiopulmonary bypass, cross-clamp, and DHCA times were 137.4 ± 25.5, 33.2 ± 14.7, and 26.3 ± 13.8 minutes, respectively. R0 resection

was achieved in 76% and R1 resection in 4%. Metastatic disease was present in 20%, and 8% had N1 disease. The pathologic diagnosis was renal cell carcinoma in 20 of 25 patients (80%) and adrenocortical carcinoma, Wilms tu- mor, adrenal melanoma, and spinal chordoma in 1 patient each. Operative mortality was 8%. Twelve percent needed hemodialysis, 8% had pneumonia, 4% stroke, and 8% required reexploration for bleeding. Mean follow-up time was 32.5 months. At last follow-up, 56% had died of disease and 28% were alive, 16% without evidence of disease. Actuarial 5-year survival for the entire cohort was 36%.

Conclusions. Intraabdominal malignancies with cav- oatrial extension can be safely resected. Excellent local tumor control can be anticipated. Long-term surveillance is necessary to detect recurrence.

(Ann Thorac Surg 2016;102:836-42) @ 2016 by The Society of Thoracic Surgeons

S everal types of malignancies have been associated with intravascular tumor thrombus extending into the inferior vena cava (IVC). Renal cell carcinomas (RCCs) comprise most of these cases. Wilms tumor, adrenocor- tical carcinoma, uterine leiomyoma, and liver malig- nancies have all been reported to extend through the IVC into the heart. When RCC can be completely resected, cardiac and IVC extension has not been shown to nega- tively affect long-term outcome [1-4]. Despite advances in adjuvant and neoadjuvant therapy for RCC and other aggressive intraabdominal malignancies with caval extension, chemotherapy and radiotherapy have done little to improve long-term survival. Complete surgical resection remains the mainstay of treatment [5].

The surgical technique used depends on the level of tumor extension. Level I and level II caval thrombus can be extracted without liver mobilization or the need for cardiopulmonary bypass (CPB). However, level III and level IV tumors create more challenging situations. Tumors extending to the level of the diaphragm can be

removed without the assistance of extracorporeal circu- lation, but tumors with significant extension into the right atrium may require arresting the circulation to provide complete visualization and maintain vascular control [2].

We examined our experience with resection of intra- abdominal malignancies with extension through the IVC into the heart using sound principles of surgical oncology and modern methods of CPB and end-organ protection. We summarize our short-term and long-term outcomes with these challenging malignancies.

Patients and Methods

Data from the Departments of Cardiothoracic Surgery and Urology databases at Weill-Cornell Medical College were examined to identify all patients who had intra- vascular extension of an intraabdominal tumor into the right atrium. Those undergoing resection with CPB and deep hypothermic circulatory arrest (DHCA) were chosen for analysis. Patients with tumors extending to the level of the diaphragm or below (n = 72 for RCC patients) un- derwent resection without DHCA and were excluded from this study. From 2000 to 2013, 25 consecutive patients were identified; of these, 20 patients required

Accepted for publication March 7, 2016.

Abbreviations and Acronyms
CI= confidence interval
CPB= cardiopulmonary bypass
CSS= cancer-specific survival
DHCA = deep hypothermic circulatory arrest
IVC= inferior vena cava
KM= Kaplan-Meier
OS= overall survival
RCC= renal cell carcinoma
RFS= recurrence free survival
SD= standard deviation

operative intervention for RCC, and the remaining 5 included 1 patient each with Wilms tumor, adrenal mel- anoma, adrenocortical carcinoma, leiomyosarcoma, and a lumbar chordoma. The Weill Cornell Medical College Institutional Review Board approved the study. The need for individual patient consent was waived.

Patients were considered operable if they were capable of self-care. Patients with poorer performance status were offered resection if the cause was the debilitating symp- toms of IVC obstruction and they had a reasonable chance of recovering to a better performance status. Pa- tients were deemed unresectable if life expectancy was less than 1 year or if they had severe systemic disease, such as advanced heart failure or pulmonary disease, which was not correctable before the operation. Informed consent involved the urologist and cardiac surgeon indi- vidually explaining benefits and risks of the operation, including major complications, death, recurrence of tu- mor requiring reoperation, and lack of improved long- term survival in those with metastatic disease.

Patients with known RCC received preoperative renal artery angioembolization within 24 hours of the opera- tion. Transesophageal echocardiography was performed to confirm tumor extension into the right atrium and the need for DHCA. Exploratory laparotomy was performed by Urology through a bilateral subcostal incision. The involved kidney was mobilized leaving the ipsilateral renal vein intact. In cases involving the adrenal gland, it was mobilized in continuity with the intravascular portion of the tumor. The anterior surface of the IVC was exposed by dividing the suspensory ligaments of the liver. Manipulation of the IVC was minimized. Meticu- lous hemostasis was obtained before opening the chest.

Once the primary tumor was deemed resectable, Cardiothoracic Surgery performed a sternotomy. Heparin was administered (400 IU/kg). A cannula was placed in the ascending aorta. Venous cannulation was with 2 single-stage cannulae. One cannula was placed in the superior vena cava, and the tip of the lower cannula was placed into the right atrium under transesophageal echocardiography guidance to avoid hitting the tumor.

The bypass circuit was set up for retrograde cerebral perfusion, as previously described [6]. CPB was initiated, and the patient was cooled to 18℃. Thiopental (1 g) was administered for cerebral protection 5 minutes before

DHCA. Once DHCA began, retrograde cerebral perfu- sion was administered through the superior vena cava cannula at 200 to 300 mL/min with a central venous pressure of 25 mm Hg. Intraoperative blood salvage was used in all cases.

Right atriotomy and infrahepatic cavotomy were per- formed concomitantly. The IVC was totally occluded in 6 patients. Tumor was separated from the atriocaval walls and mobilized into the abdominal cavity, where it was removed en bloc with the primary tumor. The tumor in 3 patients extended into the hepatic veins. All tumor frag- ments and residual thrombus were removed. Tumors were removed with an endarterectomy spatula as needed, except in 1 patient with direct caval invasion who required a bovine pericardial patch on the anterior IVC and 1 who required replacement with a Dacron tube graft (Maquet Corp, Oakland, NJ).

The atriotomy was closed and the IVC cannula was placed into the IVC. The infrahepatic IVC was closed over the cannula. CPB was resumed and the patient warmed to 35℃ before separation from CPB. Neoplastic pulmonary emboli were found in 4 patients, and a separate incision in the pulmonary artery was used to extract these emboli. Once hemostasis was obtained, the sternum was closed over a chest tube, and the abdomen was closed without drains. The patient returned to the cardiothoracic inten- sive care unit, which is under the supervision of cardiac anesthesiologists and surgeons at all times.

Data collected from 1997 to 2013 were stored using Access 2010 software (Microsoft Corp, Redmond, WA). Complications within 30 and 90 days were tracked and graded using the Clavien-Dindo system [7]. Primary end points were in-hospital death and follow-up death from any cause. Secondary end points were the incidence of major complications and the composite of major adverse events, defined as in-hospital death and major post- operative complications.

Data analysis was performed using IBM SPSS Statistics 20 software (IBM Corp, Armonk, NY). Results are expressed as mean, standard deviation, median, and range. Data were compared using x2 for categoric vari- ables and the Student t test for continuous variables. Overall survival (OS), cancer-specific survival (CSS), and recurrence-free survival estimates were generated using Kaplan-Meier analysis.

Results

Twenty-five patients underwent resection of an intra- abdominal tumor with right atrial tumor thrombus us- ing CPB/DHCA. Preoperative characteristics are in Table 1. Intraoperative variables are in Table 2. Metasta- ses were present in 3 RCC patients (15%) at time of the operation, and they underwent the operation for pallia- tion of IVC obstruction. Concomitant metastasectomy of other lesions was not performed. Of the 17 without me- tastases, 9 underwent lymphadenectomy. Two (22%) had node-positive disease. Detailed histologic features of the RCC group are in Table 3.

Table 1. Preoperative Characteristics
CharacteristicMean ± SD or No. (%) (N = 25)
Age, y57 ± 14
Male14 (56)
Histology
Renal cell carcinoma20 (80)
Adrenocortical carcinoma1 (4)
Metastatic melanoma/adrenal1 (4)
Leiomyosarcoma1 (4)
Spinal chordoma1 (4)
Wilms tumor1 (4)
Hypertension15 (60)
Diabetes5 (20)
Coronary artery disease4 (16)
Neoplastic pulmonary embolism4 (16)
Ejection fraction0.587 ± 0.067
Smoking11 (44)
Preoperative creatinine, mg/dL1.4 ± 0.75

SD = standard deviation.

Outcomes are in Table 4. There were 2 perioperative deaths (8%). One death occurred due to right ventricular failure and inability to separate from CPB. The other patient died on postoperative day 8 after refusing to be reintubated for respiratory failure. Hemorrhage that required reexploration occurred in 2 patients (8%). A tonic-clonic seizure occurred in 1 patient (4%) on post- operative day 1. Brain computed tomography showed there was no stroke, and the patient was discharged from the hospital on antiepileptic medications. Pneumonia occurred in 1 patient, and 1 required a temporary tra- cheostomy for respiratory failure. Renal failure requiring dialysis developed in 3 patients (12%) with normal creatinine preoperatively. One recovered adequate renal function in the hospital and was discharged without dialysis. In follow-up, the rate of major complications (grade 3a or higher) was 32% within 30 days and 36% within 90 days. A third patient died on postoperative day 61 of cardiac causes unrelated to her disease. Her last computed tomography showed no evidence of disease.

On univariate analysis (Table 5), the composite end point of major adverse events was associated with pre- operative hemodialysis, postoperative hemorrhage, longer CPB time (160 vs 130 minutes), circulatory arrest time (39 vs 22 minutes), and cross-clamp time (44 vs 30

Table 2. Intraoperative Characteristics
CharacteristicMean ± SD
Cardiopulmonary bypass time, min137.4 ± 25.5
Cardiac ischemic time, min33.2 ± 14.7
DHCA time, min26.3 ± 13.8
Packed red blood cell transfusion, U6.9 ± 6.3

DHCA = deep hypothermic circulatory arrest; deviation.

SD = standard

Table 3. Pathologic Features of Renal Cell Carcinoma Group
FeatureMean ± SD or No. (%) (N = 20)
Tumor size, cm9.0 ± 3.2
Primary tumor stage
pT3c17 (85)
pT43 (15)
Regional lymph node involvement
pNx/pN018 (90)
pN12 (10)
Distant metastases3 (15)
Perinephric fat invasion11 (55)
Histology
Clear cell16 (80)
Papillary4 (20)
Fuhrman grade
23 (15.8)
311 (57.9)
45 (26.3)

SD = standard deviation.

minutes). Among RCC patients, the analyzed oncologic variables were not associated with long-term survival (Table 6).

Follow-up was complete. Mean follow up time was 35.7 ± 38.8 months (median, 15.8; range, 7 to 143 months). At last follow-up, 14 patients (56%) had died of disease, 3 (12%) died of other causes, and 7 (28%) were alive, 4 (16%) without evidence of disease. Kaplan-Meier estimate of 5 year OS was 36% (Fig 1). Amongst RCC patients, 5-year probability of OS, CSS, and recurrence-free survival was 31%, 36%, and 34%, respectively (Figs 1 and 2).

Comment

Several intraabdominal tumors have a propensity to involve the IVC through intravascular extension or direct IVC invasion. RCC is particularly known for this behavior, with upwards of 15% of patients having some form of

Table 4. Postoperative Outcomes
OutcomeNo. (%) or Median (range) (N = 25)
Right ventricular failure1 (4)
Seizure1 (4)
Tracheostomy2 (8)
Stroke0 (0)
Postoperative hemodialysis3 (12)
Chest tube output in 24 hours, mL335 (180-4,900)
Mediastinal reexploration for bleeding2 (8)
Mortality2 (8)
Major complications
Within 30 days8 (32)
Within 90 days9 (36)
Table 5. Risk Factors for Major Complication or Death
VariableªSubgroups
Major Complication/Death (n = 6)No Major Complication (n = 19)p Value
Age, y56.67 ± 10.3556.95 ± 14.970.966
Hypertension2 (33.3)13 (68.4)0.126
Diabetes1 (16.7)4 (21.1)0.815
Coronary artery disease1 (16.7)3 (15.8)0.959
Neoplastic pulmonary embolism1 (16.7)3 (15.8)0.959
Preoperative hemodialysis5 (83.3)0 (0)<0.001b
Metastasis2 (33.3)4 (21.1)0.539
Reexploration for bleeding2 (33.3)0 (0)0.009b
CPB, min160.0 ± 25.03130.32 ± 22.520.012b
DHCA time, min38.83 ± 16.2022.37 ± 11.050.009b
Cross-clamp time, min44.00 ± 15.7229.79 ± 13.470.041b

a Continuous data are shown as mean ± standard deviation and categoric data as number (%).

b Statistically significant (p < 0.05).

CPB = cardiopulmonary bypass; DHCA = deep hypothermic circulatory arrest.

vascular involvement [2, 5]. The tumor thrombus in most of these cases is limited to the ipsilateral renal vein. The tumor in 10% of patients can extend into the IVC, and 1% extend into the right atrium [3, 4, 8]. The more advanced tumors can protrude through the tricuspid valve into the right ventricle. Tumors in 4 of our patients had entered the right ventricle, with documented pulmonary emboli from tumor fragmentation. This degree of invasion adds sig- nificant complexity to any attempt at surgical resection, but long-term survival can be achieved, particularly if RO resection can be achieved [9-11].

In addition, surgical intervention may be the only effective palliation for symptomatic IVC obstruction. Four of our patients, despite known metastases, chose a palli- ative operation for their unbearable symptoms rather than continue with failed medical therapy for IVC obstruction despite detailed discussions about the limited benefit in terms of survival. In addition, evidence exists that cytoreductive surgery, combined with immu- notherapy, may improve survival in patients with meta- static RCC with caval extension [12, 13].

Table 6. Oncologic Variables for Long-Term Survival in Renal Cell Carcinoma Patients
VariableSubgroups
Death (n = 14)No Death (n = 6)p Value
Metastasis3 (21.4)1 (16.7)0.807
Fat invasion0.950
Perinephric5 (35.7)2 (33.3)
Hilar3 (21.4)1 (16.7)
Histology0.796
Clear cell11 (78.6)5 (83.3)
Papillary2 (14.3)1 (16.7)
Adrenal involvement3 (21.4)0 (0)0.219
Positive lymph node1 (7.1)1 (16.7)0.515

With complete resection, long-term survival can be expected. In the Mayo Clinic experience with RCC, 5-year CSS was 49.1% for patients with no tumor thrombus, 31.7% for level I, 26.3% for level II, 29.4% for level III, and 37% for level IV tumor thrombus [2]. Significant prog- nostic determinants of survival were histologic subtype, histologic grade, perinephric fat invasion, nodal status, and metastatic status [2]. Another large multiinstitutional study reported a 5-year cumulative survival of 22% for patients with RCC and level IV tumors [14]. The results of our study compare favorably, with OS of 31% and CSS of 36%.

Fig 1. Kaplan-Meier (KM) analysis shows overall survival (OS) for all patients (green line) and renal cell carcinoma (RCC) patients (blue line). Median OS was 22.0 months (95% confidence interval, 0 to 50 months) in the entire cohort and 22.0 months (95% confidence in- terval, 0 to 78.8 months) for RCC patients.

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Fig 2. Kaplan-Meier (KM) anal- ysis shows cancer-specific survival (CSS) and recurrence-free survival (RFS) for renal cell carcinoma (RCC) patients. (A) Median CSS amongst the RCC cohort was 41.0 months (95% confidence interval, 0 to 92 months). (B) RFS for RCC patients was a median of 16.0 months (95% confidence interval, 0.096 to 31.9 months).

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Less is known about the effect that tumor extension into the IVC or right atrium has on long-term survival with the other tumor types found in our series. Adre- nocortical carcinoma carries a poor prognosis, with a 5-year survival of 16% to 47%, depending on stage. The major prognostic determinant is completeness of the initial resection [15]. The long-term prognosis of pri- mary adrenal melanoma is even worse, with a median survival of less than 19 months after complete resec- tion [16]. Our patients chose to maximize their chance of long-term survival with surgical intervention, despite the overall poor prognosis. Wilms tumor, however, has a better prognosis, with 5-year survival exceeding 90% [17]. Despite the poor expected survival with certain non-RCC tumor types, the technique us- ing DHCA can be applied with reliable results to attempt to maximize long-term survival by achieving a complete resection.

Several surgical approaches to atriocaval tumors are available. Consensus regarding the optimal technique is lacking. Standard vascular control may be suitable for tumors extending up to the level of the diaphragm, but tumors extending into the heart may be best served with circulatory assistance using venovenous bypass, CPB alone, or CPB/DHCA.

Critics of CPB argue that it is associated with the release of inflammatory mediators that cause a systemic inflammatory response, leading to coagulopathy, platelet dysfunction, and increased postoperative bleeding [18]. The extensive retroperitoneal dissection required and the significant amount of collateral vessels associated with caval obstruction may increase the risk of postoperative bleeding. Care must be taken to cauterize or ligate any bleeding vessels before CPB is initiated.

Preoperative renal artery embolization was performed in our RCC patients. Although the oncologic benefits are debated, the procedure is clearly associated with less blood loss and decreased need for blood transfusion in locally advanced RCC [19]. Other potential benefits include a questionable role for “autovaccination,” but our use of preoperative embolization is purely for the benefit of decreased blood loss [19].

The addition of DHCA may add to the risk due to coagulopathy associated with prolonged CPB and hypo- thermia. However, no significant postoperative intra- abdominal bleeding occurred, and only 2 patients required reexploration for mediastinal hemorrhage. Contemporary blood salvage techniques have proven beneficial for patients having more traditional open heart operations [20]. The need for packed red blood cell transfusion in this series was acceptable, and the need for additional blood products was surprisingly low. Despite most patients having hepatic venous congestion, liver dysfunction did not have a significant effect on coagulopathy.

CPB can cause hepatic and renal dysfunction. The incidence of renal failure after routine open heart oper- ations is estimated to be 2% [21]. In this higher-risk cohort with compromised baseline renal function, postoperative renal dysfunction may be a more significant consider- ation given the need for nephrectomy. In our series, renal failure developed postoperatively in 3 patients (12%) with normal creatinine preoperatively. Two were RCC patients who underwent nephrectomy, and 1 was a patient with leiomyosarcoma, who did not have a nephrectomy. The renal function in this last patient recovered, and the pa- tient was discharged home without dialysis.

All patients with RCC required radical nephrectomy, putting them at higher risk for chronic kidney disease. Preoperative chronic renal insufficiency, open vs laparo- scopic operation, and the need for radical rather than partial nephrectomy are predictors of postoperative chronic kidney disease in the RCC population [22].

Contrary to the proposed risks of CPB and DHCA, several authors have published data supporting its use [5, 10, 23, 24]. The operative mortality in the series of Shuch and colleagues [23] of level IV RCC was 22.2%. Interestingly, mortality for patients resected with DHCA was significantly lower than those resected using CPB alone (8.3% vs 37.5%, p = 0.006). There was no difference in estimated blood loss or rate of transfusions.

Hypothermia may have a protective effect on the abdominal organs, decreasing warm ischemic time, especially of the liver and the remaining kidney [24]. The

single-institution series of Dominik and colleagues [25] of 21 level IV tumors resected with DHCA had a perioper- ative mortality of 9.5%, similar to other contemporary series. A more recent study by Abel and colleagues [26] examined outcomes of resection of level III and level IV RCC in several large tertiary centers. The study included 162 patients, and 60 were resected with CPB, of which 26 had DHCA. DHCA was not associated with any differ- ence in major complications or deaths at 90 days. The rate of major complications was 34%, and 8.6% had acute renal failure requiring dialysis. Perioperative mortality for patients with level IV thrombus was 11.8% [26].

Our preferred method is to resect atriocaval tumors using CPB/DHCA. Having a dedicated multidisciplinary team and the routine use of CPB/DHCA have allowed us to achieve favorable perioperative and long-term out- comes. Our study demonstrates this with a perioperative mortality rate of 8% and a moderate rate of complications at 90 days of 36% but, a long-term benefit from resection, with 5-year OS of 36% (RCC 31%), despite having several patients with known metastatic disease.

Some groups have used CPB with mild hypothermia to 32℃ rather than DHCA for atriocaval tumors. However, this requires intermittent use of the Pringle maneuver or supraceliac aortic clamping to decrease blood flow into the operative field [27]. Neither of these techniques re- sults in a dry operative field, making visualization diffi- cult. These maneuvers may contribute to warm ischemia to the liver and may risk dissecting the aorta or causing embolization of aortic plaque. Another group described using normothermic CPB with a beating heart in 3 pa- tients, which also required the Pringle maneuver and infrarenal IVC control [28]. Although DHCA was avoided in this small series, their mean packed red blood cell transfusion was 6 units, which was not significantly different from ours (6.5 units).

In an effort to avoid the use of CPB, one group de- scribes dissecting into the pericardial space through the abdomen and obtaining circumferential control of the IVC. The tumor is the “milked” down into the intra- hepatic IVC blindly and the IVC is clamped, a seemingly risky maneuver given the risk for tumor embolization and injury to the IVC or hepatic veins. The extensive dissec- tion required and limited surgical exposure in the difficult retrohepatic space led to significant blood loss of 6 to 7 liters in several cases, prolonged operative times of more than 8 hours, and mean transfusion of 9 units packed red blood cells [9].

Use of venovenous bypass has been limited to tumors with minimal atrial component. Granberg and colleagues [8] found that venovenous bypass was associated with shorter bypass, operative, and anesthesia times, although 1 patient in the venovenous bypass group died intra- operatively from tumor embolus. Bulky level IV tumors were resected with CPB and DHCA [8, 23].

This study is one of the largest contemporary single- institution studies on this subject. The limitations of the present study include the small sample size due to the rarity of the disease and the retrospective nature of the investigation. In addition, this is a single-institution,

single-surgical team study and may not be generalizable to other surgeons or institutions that may have less experience with these techniques.

In conclusion, intraabdominal malignancies with cav- oatrial extension can be safely resected using CPB/ DHCA. Risks of increased hemorrhage and need for transfusion due to coagulopathy associated with CPB/ DHCA have been mostly mitigated by contemporary surgical, interventional, and blood salvage techniques. Excellent local tumor control can be anticipated, but long- term surveillance is necessary to detect recurrent disease. The combined experience of a dedicated multidisci- plinary team may result in lower morbidity and death.

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The International Renal Cell Carcinoma-Venous Thrombus Consortium [1] showed that the anatomic tu- mor level is predictive of survival and that a radical surgical procedure remains the main avenue for possible cure. However, the technique and approach used for surgical removal (with cardiopulmonary bypass [CPB] with or without deep hypothermic circulatory arrest [DHCA], or off pump with exposure of the inferior vena cava [IVC] used for liver transplantation) had no onco- logic effect on 5-year survival for level III or IV tumors. Some surgeons, like Lau and colleagues [2] in this cur- rent article in The Annals, advocate DHCA; others, like Ciancio and colleagues [3], have developed techniques to remove these tumors, including those going above the diaphragm, without CPB. The reason for the latter approach is that DHCA is not benign and is associated with potentially serious neurologic sequelae, renal fail- ure and coagulopathy. Even for tumor thrombus extending into the right atrium and pulmonary artery, ascending aorta and superior vena cava cannulation (with snaring) allows easy access to the infra-, intra-, and suprahepatic veins, and removal of tumor thrombus from the heart and pulmonary artery. Given that the IVC is usually already occluded by tumor thrombus, venous drainage is not an issue. All this in an effort to prevent DHCA. In the end, and in consideration of the literature, there seems to be no difference in surgical oncologic outcome regardless of the surgical approach or tech- nique used. Therefore, the team (urologist, cardiac sur- geon, and cardiac anesthesiologist) should use the technique and approach that they feel most comfortable with when removing such tumors. It is hoped that this

article will provide guidance for surgeons who deal with such complex tumors.

Tomas A. Salerno, MD

Division of Cardiothoracic Surgery University of Miami Miller School of Medicine Jackson Memorial Hospital 1611 NW 12th Ave East Tower 3072 (R-114) Miami, FL 33136 email: tsalerno@med.miami.edu

Gaetano Ciancio, MD

Department of Surgery (Division of Transplantation) and Urology University of Miami Miller School of Medicine Jackson Memorial Hospital Miami, FL

References

1. Martínez-Salamanca JI, Linares E, González J, et al. Lessons learned from the International Renal Cell Carcinoma-Venous Thrombus Consortium (IRCC-VTC). Curr Urol Rep 2014;15: 404-13.

2. Lau C, O’Malley P, Gaudino M, Scherr DS, Girardi LN. Resection of intraabdominal tumors with cavoatrial extension using deep hypothermic circulatory arrest. Ann Thorac Surg 2016;102:836-42.

3. Ciancio G, Shirodkar SP, Soloway MS, Livingstone AS, Barron M, Salerno TA. Renal carcinoma with supra- diaphragmatic tumor thrombus: avoiding sternotomy and cardiopulmonary bypass. Ann Thorac Surg 2010;89:505-10.