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Ann Thorac Surg 2007;83:1731-1736
© 2007 The Society of Thoracic Surgeons
a Departments of Cardiothoracic and Vascular Surgery, All India Institute of Medical Sciences, New Delhi, India
b Department of Urology, All India Institute of Medical Sciences, New Delhi, India
c Department of Cardiac Anaesthesia, All India Institute of Medical Sciences, New Delhi, India
Accepted for publication December 27, 2006.
* Address correspondence to Dr Chowdhury, Department of Cardiothoracic and Vascular Surgery, All India Institute of Medical Sciences, Ansari Nagar, New Delhi-110029, India (Email: ujjwalchow{at}rediffmail.com).
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Abstract |
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Methods: A cohort of 6 patients aged 46, 50, 53, 56, 54, and 52 years underwent radical nephrectomy with tumor thrombectomy from the vena cava and right atrium under mild hypothermic cardiopulmonary bypass and intermittent cross-clamping of the supraceliac abdominal aorta. Intraatrial tumor thrombectomy was performed on a beating, perfused heart in 4 patients and a hypothermic, cardioplegia-perfused heart in 2 patients.
Results: There were no early or late deaths. The aortic cross-clamp time was 12 and 15 minutes for patients 5 and 6, respectively. The cumulative hepatic and renal ischemic time was 16 minutes (range, 14 to 22 minutes) at 32°C. The mean cardiopulmonary bypass time was 53.3 ± 8.9 minutes (range, 40 to 65 minutes). At a mean follow-up of 43 ± 24.6 months (range, 10 to 70 months), all patients are active and remain disease-free.
Conclusions: We conclude that radical nephrectomy and tumor thrombectomy in patients with level IV thrombi can be safely performed with cardiopulmonary bypass, mild hypothermia. and intermittent supraceliac abdominal aortic occlusion, avoiding potential hematologic, hepatic, renal, neurologic, and septic complications associated with circulatory arrest.
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Introduction |
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TopAbstractIntroductionPatients and MethodsResultsCommentAcknowledgmentsReferences |
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Techniques of resection in patients with level IV thrombus extension have evolved during the years and now encompass a number of techniques with and without using cardiopulmonary bypass (CPB), hypothermia, and exsanguinations [1–12]. Most of these methods do not solve completely the problems of suboptimal thrombectomy, massive intraoperative bleeding, profound hypotension, the risk of tumor embolization, ischemic injury to the vital organs, and perioperative mortality [1–12]. Herein, we report novel techniques of tumor thrombectomy using CPB, mild hypothermia, and intermittent cross-clamping of the supraceliac intraabdominal aorta on 6 patients with suprahepatic intraatrial extension of tumor thrombus in an attempt to avoid or minimize the above-mentioned complications.
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Patients and Methods |
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The laparotomy incision was extended cephalad with a median sternotomy. The apex of the tumor thrombus was palpated in the IVC and confirmed to extend within the RA in patients 1 through 4 and occupying almost half the cavity of the RA in patients 5 and 6. Mild hypothermic (32°C) CPB using angled venous cannulas into the superior vena cava, external iliac vein, and ascending aortic was performed in all patients (Fig 2). The first surgical step was to gain control above the cranial extreme of the thrombus by placing a tourniquet or a Satinsky clamp, and all manipulations to the tumor-bearing organs were kept to a minimum until proximal control was obtained to avoid tumor embolization. It was possible to isolate and control the cavoatrial junction above the tumor using umbilical tapes in patients 1 through 4 (Fig 3). However, in patients 5 and 6 with more extensive tumors extending cephalad into the cavity of the RA, the main pulmonary artery was dissected and looped to protect from a life-threatening pulmonary tumor embolism during assessment, palpation, and mobilization of the tumor-bearing organs (Fig 4).
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The liver was circumferentially mobilized to expose the retrohepatic vena cava by incising the falciform, triangular, and coronary ligaments. The diaphragm was split into the central tendon toward the IVC. Several short segmental veins between the dorsal surface of the liver and the vena cava were divided to expose the vena cava further. The hepatic artery and portal vein were exposed at the porta hepatis. The abdominal aorta was exposed at the supraceliac bare area by dividing the right crus of the diaphragm (Fig 2). The kidney was mobilized partially posteriorly, and the renal artery was ligated. This maneuver helps in minimizing significant shunting in many of the tumors. After division of the renal artery, dissection was carried superiorly to the right adrenal vein, which is usually higher and posterior.
The abdominal aorta was cross-clamped at the supraceliac bare area (Fig 2). The clamp was intermittently applied approximately every 5 to 7 minutes to minimize ischemia of the hepatic and contralateral renal vascular bed and the lower torso. The inferior cavoatrial junction was cross-clamped above the tumor. Then the vena cava was incised with an ellipse of cava around the renal vein ostium. The tumor thrombus was dissected using endarterectomy instruments and was extracted in continuity with the nephrectomy specimen. The individual hepatic veins and the IVC were completely cleared of thrombus. As soon as the tumor thrombus was removed en bloc, the aorta was released to restore circulation. A cardiotomy sucker was placed within the opened IVC, and the venous return was managed successfully. The IVC was flushed vigorously with cold saline solution. The cavotomy and the cavoatriotomy were repaired in two layers using 5-0 polypropylene. One patient (patient 2) required excision of a portion of IVC wall, which was later repaired using a pericardial patch. The tumor thrombus was occupying nearly half of the RA cavity in patients 5 and 6. They required aortic cross-clamping, cardioplegic arrest, and clamping of the pulmonary artery to avoid tumor embolization. Tumor thrombectomy was performed through two separate incisions in the infrahepatic IVC and RA. After removing the tumor, the right heart chambers including the opened IVC were vigorously flushed with cold saline solution with the pulmonary arterial clamp in situ to wash away any residual tumor material.
During intermittent supraceliac clamping at 32°C, the systemic flow rates were maintained between 2.0 and 2.2 L · min–1 · m–2 with a mean perfusion pressure between 60 and 80 mm Hg. Cardiopulmonary bypass was decreased and terminated after rewarming the patients, and heparin was reversed. We did not use an IVC clip or filter on any patient.
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Results |
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Pathologic examination revealed a well-differentiated clear cell carcinoma confined within the Gerota’s fascia. All lymph nodes and resection margins were free of tumor. Based on the Robson modification of the system of Flocks and Kadesky, all patients were classified as having stage III cancer. Convalescence was uneventful. Postoperative immunotherapy with interferon 
2 was administered to all patients to improve survival. At a mean follow-up of 43 ± 24.6 months (range, 10 to 70 months; median, 50.0 months) all patients are active and remain disease-free.
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Comment |
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There are six basic principles involved in performing surgical removal of a suprahepatic intracardiac tumor thrombus. These principles are (1) isolate and control the IVC above and below the thrombus, (2) isolate and control the contralateral renal vein, (3) minimize hepatic and renal ischemia as much as possible, (4) incise the vena cava (suprahepatic and infrahepatic) or RA for combined manipulation and dissection, (5) remove the tumor thrombus en bloc including its intrahepatic extension along with a portion of the IVC wall around the renal vein ostium or the invaded vena caval wall, and (6) reconstruct the entire vena caval lumen with or without using a defatted pericardium in a relatively bloodless field.
The techniques described herein involve the use of CPB, mild hypothermia, and intermittent partial circulatory arrest of the lower torso by intermittent cross-clamping of the supraceliac abdominal aorta and addresses all the issues enunciated above.
Despite temporary occlusion of the suprahepatic vena cava, hepatic congestion could be reduced, retrohepatic dissection could be minimized, and back-bleeding from hepatic and lumbar veins could be avoided. There was no need for dissection and occlusion of the porta hepatis or ligation of multiple lumbar veins. Intermittent aortic occlusion allowed direct visual inspection of the entire vena caval lumen in a relatively bloodless field. An atriotomy could be performed easily, which permitted removal of not only the atrial thrombus but also friable or adherent pieces of the thrombus in the intrahepatic IVC. Thus, it allowed complete removal or reconstruction of the IVC (n = 1) with excellent exposure in a controlled operative setting. Our technique of obtaining proximal control above the cavoatrial junction or the main pulmonary artery in cases of massive intraatrial tumor thrombus avoided the problem of pulmonary tumor embolization. The procedure can be used for both right-sided and left-sided tumors and allows normal perfusion of the heart, lung, contralateral kidney, and brain with a consequent reduction in perfusion-related complications.
Although techniques of removal of infradiaphragmatic tumor are relatively straightforward, supradiaphragmatic extension presents more technical challenges and mandates an individualized management protocol. Analysis of the published literature documents various techniques of suprahepatic vena caval thrombectomy, including the use of a finger to push back the tumor thrombus under a tourniquet around the intrapericardial IVC [2], forceps [2, 13], Foley catheter [13], Fogarty catheter [14], and mobilization with or without resection of the caudate lobe of the liver [7, 15]. In 2001, we described a new technique of tumor thrombectomy on 2 patients with right-sided renal cell carcinoma with suprahepatic, supradiaphragmatic level IV tumor thrombus without using CPB through a right posterolateral thoracoabdominal incision [16]. Cerwinka and associates [17] have used a different approach of tumor extirpation through bilateral subcostal incision with superior midline T-extension. They performed right nephrectomy, an inferior vena cavectomy between the hepatic veins and the left renal vein, avoiding circulatory arrest altogether, and even CPB [17].
The use of venovenous bypass or vena caval–atrial bypass is limited to thrombi that can be milked inferior to the vena caval–atrial junction and extracted like level III thrombi [8–12]. One of the advantages of venovenous or vena caval–atrial bypass with an electromagnetic centrifugal pump and vacuum-assisted drainage is that full heparinization is not necessary and perioperative blood loss is possibly minimized [11, 12]. Janosko and associates [18] described a modified technique of venoatrial bypass that allows rapid conversion to total CPB if the thrombus cannot be mobilized under the tourniquet placed around the intrathoracic IVC. These non-CPB approaches are plagued by problems of profound intraoperative hypotension, suboptimal thrombectomy, risk of tumor embolization within the RA and pulmonary tree, disruption, the risk of unpredictable bleeding, and warm ischemic injury to the liver and kidneys [7–12, 15, 17–19]. Several reports of intraoperative massive pulmonary embolism requiring emergency pulmonary embolectomy have been published [19].
The application of CPB and hypothermia, initially introduced by Marshall and colleagues [14] in 1970s, to patients with suprahepatic vena caval thrombi from renal cell carcinoma has improved the safety and efficacy of a difficult surgical undertaking. The use of adjuncts like hypothermia, cardiac arrest, and temporary exsanguinations with CPB facilitates controlled dissection, provides a bloodless field, and reduces the risk of tumor embolization [5–7]. However, up to 40% risk of complications including renal failure, hepatic failure, and postoperative sepsis and up to 33% perioperative mortality after hypothermic circulatory arrest have been reported by various investigators [5–7, 20]. Risk of complications has been shown to be associated with endothelial dysfunction in the cerebral microvasculature, renal arteries, and pulmonary veins [20]. A state of relative coagulopathy is known to exist in these patients as a result of hepatic venous obstruction, congestive hepatomegaly, and depressed hepatic function [20]. Addition of systemic heparinization, prolonged CPB time, and adverse effects of hypothermic circulatory arrest compounds the magnitude of the procedure. Literature documents 1.7 to 9.1 L of blood loss using circulatory arrest to remove tumors with supradiaphragmatic extension [5–7]. It is noteworthy that no patients in this study experienced renal failure, hepatic failure, sepsis, cerebrovascular accidents, myocardial infarction, or pulmonary embolus.
For the surgical exposure, a midline, a thoracoabdominal, or a bilateral subcostal with superior midline T-extension approach have been advocated [1–12, 15–17]. A thoracoabdominal approach provides better access to the IVC but makes atrial and aortic cannulation difficult. However, the midline sternotomy and laparotomy provide satisfactory exposure of the kidney and excellent exposure of the heart [1–12, 15–17].
Accurate preoperative information regarding the presence and extent of an IVC tumor thrombus is essential to determine the appropriate operative approach. Although computed tomographic scanning and ultrasound detect gross renal vein and IVC tumor thrombus, they are unreliable in delineating the cephalad extent of a thrombus. Although inferior venacavography accurately detects the presence of IVC thrombi, a single antegrade study may be insufficient in patients with complete caval occlusion. A second retrograde injection of the IVC is needed in such cases to delineate the distal extent of the thrombus [21, 22].
Recent publications indicate that magnetic resonance imaging is an accurate noninvasive method for delineating the cephalad and caudal extent of IVC thrombi and now is the preferred caval imaging modality in our center. The major advantages of magnetic resonance imaging are that thrombosis versus patency in the vena cava can be determined without using intravenous contrast agent, and images of the tumor thrombus can be acquired in sagittal, coronal, and axial planes [21]. Inferior venacavography is reserved for patients in whom magnetic resonance imaging findings are equivocal or when magnetic resonance imaging is contraindicated, eg, in patients with claustrophobia, cardiac pacemakers, certain intracerebral vascular clips, cochlear implants, or intraocular foreign bodies [21]. Intraoperative transesophageal echocardiography is very useful in delineating the cephalad extent of the tumor and detecting any adherence of the caval thrombus. Cerwinka and associates have described an entirely transabdominal approach, milking the tumor thrombus into the subdiaphragmatic IVC under transesophageal echocardiography control. Additionally, it is useful during the key portion of the operation and allows placement of a clamp in the RA to exclude the tumor [22].
We conclude that cardiopulmonary bypass, mild hypothermia, and intermittent occlusion of the supraceliac abdominal aorta represents an alternative modality in the evolutionary management of renal cell carcinoma with suprahepatic level IV neoplastic extension. Avoidance of deep hypothermic circulatory arrest reduces CPB time, and allows normal perfusion of the heart, lung, and brain with a consequent reduction in perfusion-related complications. Cardioplegic arrest allows removal of massive intraatrial thrombi, clamping of the pulmonary artery avoids the problem of pulmonary tumor embolization, and a combination of right atriotomy and infrahepatic vena cavotomy allows complete removal of extensive intracardiac and vena caval tumor thrombi.
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Acknowledgments |
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References |
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This article has been cited by other articles:
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  G. J. Wang, J. P. Carpenter, R. M. Fairman, B. M. Jackson, B. Malkowicz, K. N. Van Arsdalen, and E. Y. Woo Single-Center Experience of Caval Thrombectomy in Patients With Renal Cell Carcinoma With Tumor Thrombus Extension Into the Inferior Vena Cava Vascular and Endovascular Surgery, August 1, 2008; 42(4): 335 - 340. [Abstract] [PDF]
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 G. Ciancio and T. A. Salerno Removal of Renal Cell Carcinoma and Thrombectomy With Intraatrial Tumor Without Cardiopulmonary Bypass Ann. Thorac. Surg., March 1, 2008; 85(3): 1145 - 1145. [Full Text] [PDF]
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U. K. Chowdhury and A. Seth Reply Ann. Thorac. Surg., March 1, 2008; 85(3): 1145 - 1146. [Full Text] [PDF]
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