Liver Transplantation Techniques for the Surgical ... - European Urology

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Aug 3, 2010 - ... University of Miami Miller School of Medicine, Miami, Florida, USA b Department ... fashion and the spleen–pancreas en bloc to the midline.
EUROPEAN UROLOGY 59 (2011) 401–406

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Surgery in Motion

Liver Transplantation Techniques for the Surgical Management of Renal Cell Carcinoma with Tumor Thrombus in the Inferior Vena Cava: Step-by-Step Description Gaetano Ciancio a,b, Javier Gonzalez c,*, Samir P. Shirodkar b, Javier C. Angulo c, Mark S. Soloway b a

Department of Surgery, Division of Transplantation, University of Miami Miller School of Medicine, Miami, Florida, USA

b

Department of Urology, University of Miami Miller School of Medicine, Miami, Florida, USA

c

Servicio de Urologı´a, Hospital Universitario de Getafe, Getafe (Madrid), Spain

Article info

Abstract

Article history: Accepted July 20, 2010 Published online ahead of print on August 3, 2010

Background: Renal cell carcinoma (RCC) with tumor thrombus in the inferior vena cava (IVC) poses a challenge to the surgeon given the operative difficulty, potential for massive hemorrhage, and possibility of tumor thromboemboli. Objective: To determine the applicability of a self-developed technique based on orthotopic liver transplantation procedures for safe resection of these tumors. Design, setting, and participants: From August 1997 to February 2008, 68 consecutive patients underwent resection of RCC with suprahepatic and/or retrohepatic (level 3 and 4) tumor thrombus in a single referral institution. Surgical procedure: A triradiate incision over the upper abdomen permits the placement of a Rochard retractor. Early vascular control of the renal artery is achieved by creating a posterior plane of dissection. Venous collateral decompression permits development of a bloodless anterior plane by mobilizing the liver in a ‘‘piggy-back’’ fashion and the spleen–pancreas en bloc to the midline. Thrombus extraction requires circumferential control at the renal veins, hepatic hilum, and IVC before cavotomy. The central tendon of the diaphragm may be opened for cranial control and gentle traction over the right atrium performed. Repositioning of the proximal clamp and Pringle release avoid veno-venous bypass and cardiopulmonary bypass (CPB) in most cases. Measurements: The extent of the tumor thrombus was retrohepatic in 56 patients and suprahepatic/intra-atrial in 12 patients. Results and limitations: Mean operative time was 5 h 32 min. Mean estimated blood loss (EBL) was 2112  3834 ml (range: 100–25 000), with a mean transfusion being 4.2  4.1 U (range: 0–30). Five patients (7.3%) required CPB. Three patients (4.4%) died in the immediate postoperative period. All had complete tumor resection. No patient developed intraoperative thromboembolism. Conclusions: This surgical approach provides excellent exposure and control of the IVC in cases with level 3 and 4 tumor thrombus, avoiding CPB except in rare circumstances. # 2010 European Association of Urology. Published by Elsevier B.V. All rights reserved.

Keywords: Renal cell carcinoma Surgical technique Caval thrombus Tumor thrombus Radical nephrectomy Please visit www.europeanurology.com and www.urosource.com to view the accompanying video.

* Corresponding author. Servicio de Urologı´a, Hospital Universitario de Getafe, Ctra. De Toledo Km 12,500, 28905 Getafe (Madrid), Spain. Tel. +34 916839360 ext. 6381; Fax: +34 916247309. E-mail address: [email protected] (J. Gonzalez).

0302-2838/$ – see back matter # 2010 European Association of Urology. Published by Elsevier B.V. All rights reserved.

doi:10.1016/j.eururo.2010.07.028

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1.

EUROPEAN UROLOGY 59 (2011) 401–406

Introduction

Renal cell carcinoma (RCC) unfortunately remains a common malignancy throughout the world. This cancer is unique in its proclivity for vascular invasion and not infrequently extends into the renal vein and inferior vena cava (IVC) [1]. When it occurs, extirpative surgery offers the only potential cure [2]. The approach varies among surgeons, yet the consensus is that such cases are complex, require an excellent understanding of the anatomy, and benefit from a team approach [3–9]. We describe in detail our techniques and experience managing 68 patients with RCC and suprahepatic/intra-atrial and/or retrohepatic IVC tumor thrombus using a transabdominal approach—without intraoperative bypass maneuvers in most cases. 2.

Methods

Fig. 1 – The thrombus reaches a level above the major hepatic veins. A vascular clamp is applied in the suprahepatic vena cava. The surgeon milks the thrombus upper limit downwards to a level below the major hepatic veins.

From August 1997 to February 2008, 104 patients with RCC and tumor thrombus were surgically treated. In 68 cases, RCC extended to the retrohepatic IVC or beyond. Sixty-four patients were managed by a transabdominal approach without bypass maneuvers. Diagnosis was

and caudate lobe are ligated and divided. The liver is dissected off the IVC

made radiographically by computed tomography (CT) scan or ultra-

until it lies in a piggy-back fashion, attached to the IVC only by the major

sound. Cardiac, renal, and respiratory status was evaluated preopera-

hepatic veins.

tively. The level of the thrombus was confirmed with magnetic

In this fashion, the infrahepatic, intrahepatic, and suprahepatic

resonance imaging (MRI) scans. Transesophageal echocardiography

portions of the IVC are completely exposed. In addition to mobilizing the

(TEE) was occasionally used to monitor tumor thrombi above the

liver off the cava, a plane created between the IVC and the posterior

infrahepatic vena cava. The cranial extent of the tumor was initially

abdominal wall is important, because it permits circumferential vascular

defined per Neves and Zincke [3]; however, for level 3 thrombi, we used

control of the cava [8,9,13]. Small tributaries can become engorged to

our modified definition [8].

look like lumbar vessels, and they should be identified and ligated. A useful technique, which we have applied for a thrombus located

2.1.

Operative technique

A triradiate incision is made commencing approximately two fingerbreadths below the right costal margin and extending laterally to the midaxillary line. This incision is extended below the left costal margin as far as necessary and vertically in the midline to the xiphoid process. A Rochard self-retaining retractor is placed, elevating the costal margins and splaying them laterally toward the axillae. We pursue early intraoperative ligation of the involved renal artery. The kidney is mobilized medially until the renal artery is identified and ligated [10]. Arterial ligation results in decompression of collateral

above the hepatic veins, is to milk the thrombus below the major hepatic veins (Fig. 1), and then apply a vascular clamp below these veins (Fig. 2). This technique is often feasible, because ligation of the renal artery reduces the blood supply to the tumor thrombus. The technique serves a dual function. First, it allows the liver to drain into the IVC, avoiding hypotension from decreased venous return. Second, by not clamping the major hepatic veins or porta hepatis, liver congestion and postoperative hepatic dysfunction are avoided. The surgeon must be careful when touching the thrombus so as to avoid dislodging it. For level 4 [16] and some level 3 thrombi [8], the central tendon of the diaphragm is dissected until the supradiaphragmatic, intrapericardial IVC is identified

circulation and decreases blood loss. Exposure of the left kidney begins by mobilization of the descending colon. The spleen is dissected off the diaphragm and mobilized en bloc with the pancreas toward the midline [11], exposing the entire upper retroperitoneal space from the diaphragm to the inferior border of the kidney. Liver mobilization begins with dissection of the ligamentum teres, which is divided. The falciform ligament is divided with cautery, and this incision is carried around both to the right superior coronary ligament and by passing to the left side, dividing the left triangular ligament. The visceral peritoneum on the right of the hepatic hilum and the infrahepatic vena cava are incised in conjunction with the right inferior coronary and hepato-renal ligaments. The liver is gradually rolled to the left using these techniques, as described for liver transplantation [8–15]. Opening the lesser omentum allows the porta hepatis to be controlled with a Rummel tourniquet; a Pringle maneuver can then be carried out (temporarily occluding the portal venous and arterial inflow to the liver) as required. Then, we proceed with the ‘‘piggy-back’’ liver transplantation technique [15]. Piggy-back liver transplantation is so called, because the recipient’s vena cava is left in situ and the liver mobilized off the vessel [15]. Small hepatic veins passing from the right

Fig. 2 – When the upper limit of the thrombus is placed properly, the vascular clamp is repositioned just below the major hepatic veins.

EUROPEAN UROLOGY 59 (2011) 401–406

Fig. 3 – The central tendon of the diaphragm is opened with cautery. Circumferential control over the suprahepatic portion of the vena cava is obtained and a pericardiotomy performed to gain access to the intrapericardic portion of the cava and the right atrium.

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Fig. 5 – The Pringle maneuver allows vascular control of the liver. By practicing an orifice in the lesser omentum, the liver hilum is identified and controlled with a vascular clamp.

(Fig. 3). This dissection is carried out circumferentially so that the intrapericardial IVC can be encircled at its confluence with the right atrium. The right atrium is gently pulled beneath the diaphragm (Fig. 4). A Pringle maneuver is then performed to temporarily occlude the vascular inflow to the liver (Fig. 5). It is recommended that the surgeon wait before applying the other vascular clamps, as doing so allows the liver to decompress (Fig. 6). The vascular clamps are placed in the following order: the infrarenal vena cava and the left or right vein are controlled, then a Satinsky clamp is placed across the right atrium under TEE monitoring (Fig. 7). For left-side tumors, the right adrenal vein is also clamped. For level 3d tumor thrombus, a vascular clamp is placed across the intrapericardial or suprahepatic IVC [8,16]. The IVC is incised from the diaphragm to the renal vein, and the tumor is removed (mobile tumor thrombus) or dissected sharply off the

Fig. 6 – This maneuver prevents blood entering freely in the liver and promotes liver decompression.

atrial wall (adherent tumor thrombus) and/or IVC. The three major hepatic veins can be directly visualized, their orifices inspected, and the tumor removed if it is invading them (Budd–Chiari syndrome; Fig. 8). Following removal of the tumor thrombus and closure of the upper cava, the vascular clamp is repositioned below the hepatic veins, the Pringle is released, and normal liver blood flow is reestablished (Fig. 9). The maneuver of clamping below the major hepatic vein allows a very short Pringle maneuver. The remaining IVC below the hepatic veins is sutured closed [16,17]. The diaphragm is closed with interrupted sutures, leaving some of the incision open and draining into the abdominal compartFig. 4 – The surgeon gently pulls the right atrium beneath the diaphragm into the abdominal cavity.

ment. The procedure is completed in the typical fashion for radical nephrectomy.

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Fig. 7 – A new clamp is placed above the major hepatic veins, and the inferior vena cava is incised from the diaphragm to the renal vein.

3.

Results

Sixty-eight patients underwent radical nephrectomy with resection of tumor thrombus from suprahepatic and/or retrohepatic IVC. Mean age was 61.8 yr (range: 25–84). The male-to-female ratio was 1.6:1, and the right-to-left ratio was 3.8:1. Fifty-six patients had a level 3 thrombus (retrohepatic IVC) [8], and 12 had a level 4 thrombus

Fig. 8 – The three major hepatic veins can be directly visualized, their orifices inspected, and the tumor removed if it is invading them.

Fig. 9 – Following removal of the tumor thrombus and closure of the upper cava, the vascular clamp is repositioned below the hepatic veins, the Pringle is released, normal liver blood flow is reestablished, and the rest of the cavotomy sutured is closed.

(supradiaphragmatic/intra-atrial). Mean discharge serum creatinine was 1.28 mg/dl (range: 0.6–2.8; normal: 0.9–1.4 mg/dl). Two patients were on hemodialysis preoperatively. None were started on dialysis de novo postoperatively. Clinical staging revealed 56 cases (82%) with level 3 thrombus (T3b, American Joint Committee on Cancer [AJCC] 2010) and 12 cases (18%) with level 4 thrombus (T3c, AJCC 2010). The level of thrombus on CT/MRI scans correlated well with the intraoperative findings. All patients had complete extraction of tumor from the IVC. Mean operative time was 5 h 32 min (range: 2 h 32 min to 13 h 35 min). Estimated blood loss (EBL) averaged 2112  3834 ml (range: 100–25 000). The number of transfusions ranged from 0 to 30 U, with a mean of 4.2  4.1 U. Three patients received cell saver blood only, 38 received allogeneic blood as well, and 27 did not require a transfusion. Two patients with level 3 thrombus presented with tumor thrombus embolized in the pulmonary arteries (before surgery) and required cardiopulmonary bypass (CPB) after the removal of the RCC and IVC tumor thrombus. Five patients with level 4 tumor thrombus required sternotomy—one for placement of an atrial catheter, three for institution of CPB, and one for exposure. Veno-venous bypass was not used. Sixty-five patients had an uneventful postoperative course, but three patients (4.4%) suffered major complications leading to death. One patient with a level 3 thrombus died on the first postoperative day from a cardiac arrhythmia. He did not undergo CPB or sternotomy intraoperatively. Another patient had severe Budd–Chiari syndrome and needed to go on CPB. She developed a coagulopathy and liver failure and died 2 wk postoperatively of multisystem organ failure. The third patient died of

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sepsis 2 wk after surgery. One patient presented preoperatively with Budd–Chiari syndrome and multiple comorbidities and sustained ventricular fibrillation in the operating room. He was successfully resuscitated, but a sternotomy was performed for placement of an atrial catheter for fluid and blood return. It was felt that his performance status and health made him a very high risk for mortality while under CPB, and the decision was made not to institute this or deep hypothermic circulatory arrest (DHCA) along with the cardiothoracic surgery service. In addition, the patient had significant hepatic congestion related to the Budd–Chiari syndrome and obstruction of all three hepatic veins. As a result, the vena cava was opened, and the liver was allowed to decompress through the cavotomy without the Pringle maneuver. During this part of the procedure, blood loss was significant. The patient ultimately lost 25 l of blood and received extensive autologous and heterologous blood transfusion. His postoperative course was uneventful after extubation. 4.

Discussion

Optimal management of RCC with extension into the retrohepatic IVC or beyond poses a challenge to the treating surgeon. It entails full excision of the tumor mass, including tumor thrombus above or below the diaphragm, while maintaining oncologic principles and patient safety. Generally, management of the IVC is the most stressful and difficult aspect of this operation, yet it is absolutely critical for favorable outcomes [18]. Much of the risk of vena cava manipulation stems from the potential for significant hemorrhage and concern for inadvertent embolization of the thrombus during caval handling. Such complications have significant morbidity for the patients, entailing transfusion, further operation, and potential mortality. To minimize such risks, a number of approaches to surgical extirpation of advanced renal tumors have been undertaken over the past three decades. The evolution of these techniques is often related to application of surgical principles from differing subspecialties [19,20]. One of the earliest methods of nephrectomy and thrombectomy relied heavily on CPB, usually with DHCA. Borrowed from cardiothoracic surgery, these adjuncts allowed an extensive oncologic operation to be performed safely with complete tumor resection and less blood loss than prior methods [21,22]. As in cardiac surgery, the institution of CPB—with or without DHCA—engenders a number of sequelae that may paradoxically increase the difficulty of the operation. It is well known that CPB can produce platelet dysfunction and coagulopathy [6,22,23], often resulting in bleeding from the extensive operative retroperitoneal surfaces [5]. CPB in patients with a bulky, fixed, intra-atrial thrombus may be required, but patients with a minimal, nonadherent atrial thrombus or level 3 tumor extension usually do not require CPB and may benefit from the use of liver transplantation techniques. The drawbacks of our report stem from the limited number of patients and the extended period of treatment but reflect a firm institutional experience.

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We continue to advocate applying techniques gleaned from liver transplantation surgery and adding them to the armamentarium of the urologic oncologist in dealing with renal malignancies with tumor thrombus in the IVC. The orthotopic liver transplantation (piggy-back) technique is advantageous over right-to-left hepatic mobilization, as it allows circumferential control over the IVC, thus facilitating clamp placement above the thrombus and diminishing bleeding from hepatic circulation. A better approach for cavotomy and thrombus milking is gained in cases with retrohepatic and suprahepatic involvement. Our refinement of the surgical approach to these tumors, consisting of an entirely intra-abdominal approach without CPB or veno-venous bypass, is the byproduct of this novel approach [12]. A common presentation to some centers maybe the patient who has been diagnosed with a large, advanced renal tumor and undergoes angioembolization prior to evaluation by the urologic oncologist. Advocates of preoperative renal artery embolization claim that it makes the operation easier, because (1) it reduces blood loss by collapsing the many collaterals on the surface of the kidney and the hilum; (2) it allows ligation of the renal vein without first ligating the artery; and (3) if 24–48 h are allowed to elapse after infarction, considerable edema develops around the tumor, facilitating dissection from contiguous structures. We have never requested preoperative embolization for any of our patients, but an important principle of our surgical approach includes mobilization of the kidney with early ligation of the renal artery. It may appear that en bloc kidney mobilization raises the risk of thrombus dislodgement; nevertheless, the experience we present reveals that this maneuver is safe for the patient, with no thrombus migration observed in these 68 cases. With the posterior approach, fewer varices are encountered as opposed to dissection anterior to the kidney. Once the kidney is mobilized medially, the renal artery is identified, ligated, and divided. The collateral circulation is reduced, making the rest of the dissection easier, and has the same effect as preoperative embolization without the morbidity [10]. In personal experience in local lesions without vascular invasion, we have found that angioembolization can often increase the difficulty of the surgery from a combination of local reaction and necrosis. As a result, meticulous use of these techniques precludes the need for embolization prior to definitive surgical management. 5.

Conclusions

RCC with vascular invasion into the IVC remains a significant challenge to the urologic oncologist. It is clear that complete excision of the tumor, including caval thrombus with negative margins, allows the best chance for patient survival. A number of techniques, including CPB with or without DHCA, have been attempted and discarded to facilitate the surgery with minimal morbidity to the patient. We currently do not use CPB except in very rare circumstances. Our techniques, adapted from liver transplant methods, including liver mobilization, caval isolation,

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and atrial access via a transdiaphragmatic approach, allow the total resection of such tumors with minimal adverse effects to the patient and maximum oncologic efficacy.

[7] Nesbit JC, Soltero ER, Dinney CP, et al. Surgical management of renal cell carcinoma with inferior vena cava tumor thrombus. Ann Thorac Surg 1997;63:1592–600. [8] Ciancio G, Vaidya A, Savoie M, Soloway M. Management of renal cell

Author contributions: Javier Gonzalez had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

carcinoma with level III thrombus in the inferior vena cava. J Urol 2002;168:1374–7. [9] Ciancio G, Livingstone AS, Soloway M. Surgical management of renal cell carcinoma with thrombus in the inferior vena cava:

Study concept and design: Ciancio, Gonza´lez. Acquisition of data: Ciancio, Shirodkar, Gonza´lez. Analysis and interpretation of data: Ciancio, Shirodkar. Drafting of the manuscript: Ciancio, Gonza´lez, Shirodkar.

the University of Miami experience in using liver transplant techniques. Eur Urol 2007;51:988–95. [10] Ciancio G, Vaidya A, Soloway M. Early ligation of the renal artery using the posterior approach: a basic surgical concept reinforced

Critical revision of the manuscript for important intellectual content:

during resection of large hypervascular renal cell carcinoma

Ciancio, Soloway, Angulo.

with or without inferior vena cava thrombus. BJU Int 2003;92:

Statistical analysis: Ciancio, Gonza´lez, Shirodkar. Obtaining funding: None.

488–489. [11] Ciancio G, Vaidya A, Shirodkar S, Manoharan M, Hakky T, Soloway

Administrative, technical, or material support: None. Supervision: Ciancio, Gonza´lez.

M. En bloc mobilization of pancreas and spleen to facilitate resec-

Other (specify): Figures by Gonza´lez.

quadrant of the abdomen: techniques derived from multivisceral

Financial disclosures: I certify that all conflicts of interest, including specific financial interests and relationships and affiliations relevant to the subject matter or materials discussed in the manuscript (eg, employment/affiliation, grants or funding, consultancies, honoraria, stock ownership or options, expert testimony, royalties, or patents filed, received, or pending), are the following: None. Funding/Support and role of the sponsor: None.

tion of large tumors primarily renal and adrenal in the left upper transplantation. Eur Urol 2009;55:1106–11. [12] Ciancio G, Soloway M. Renal cell carcinoma invading the hepatic veins. Cancer 2001;92:1836–42. [13] Ciancio G, Soloway M. Resection of the abdominal inferior vena cava for complicated renal cell carcinoma with tumor thrombus. BJU Int 2005;96:815–8. [14] Ciancio G, Hawke C, Soloway M. The use of liver transplant techniques to aid in the surgical management of urological tumors. J Urol 2000;164:665–72. [15] Tzakis A, Todo S, Starzl TE. Orthotopic liver transplantation with

Appendix A. Supplementary data

preservation of the inferior vena cava. Ann Surg 1989;210:649–52. [16] Ciancio G, Soloway M. Renal cell carcinoma with tumor thrombus extending above the diaphragm: avoiding cardiopulmonary bypass.

The Surgery in Motion video accompanying this article can be found in the online version at doi:10.1016/j.eururo. 2010.07.028 and via www.europeanurology.com.

Urology 2005;66:266–70. [17] Cerwinka WH, Ciancio G, Salerno TA, Soloway M. Renal cell cancer with invasive atrial tumor thrombus excised off-pump. Urology 2005;66, 1319.e9–11.

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