The American Journal of Surgery (2009) 198, e42–e48

HowIDoIt Step-by-step isolated resection of segment 1 of the using the hanging maneuver

Rafael López-Andújar, Ph.D.*, Eva Montalvá, Ph.D., Marcos Bruna, M.D., Montiel Jiménez-Fuertes, M.D., Angel Moya, Ph.D., Eugenia Pareja, Ph.D., Jose Mir, Ph.D.

Hepatic Surgery and Liver Transplant Unit, La Fe University Hospital, Avda Campanar 21, 460009 Valencia, Spain

KEYWORDS: Abstract. The caudate lobe can be the origin of primary liver tumours or the sole site of liver Liver resection; metastases. This lobe is anatomically divided into 3 parts: Spiegel’s lobe (Couinaud’s segment 1), Surgical technique; paracaval portion (Couinaud’s segment 9), and the caudate process. In this series of 4 cases, we provide Caudate lobectomy; a step-by-step description of a surgical technique variation that can be applied to resections of lesions Isolated segment 1 localized in segment 1. We believe that other than size, lesion removal in this hepatic anatomic area, hepatectomy; which is difficult to perform, can be done more easily using this new approach because it requires Liver tumor; minimal mobilization without unnecessary parenchyma transection of other liver parts. Therefore, it Liver hanging reduces the risk of lesions in the inferior vena cava and the middle hepatic vein and respects adequate maneuver margins without the use of clamping maneuvers and in an acceptable surgical time. © 2009 Elsevier Inc. All rights reserved.

The caudate lobe is commonly involved in metastatic or divided into 3 parts: Spiegel’s lobe (Couinaud’s segment 1), primary liver neoplasms. Historically, it has been regarded the paracaval portion (Couinaud’s Segment 9), and the as an independent segment and was classified by Couinaud1 caudate process. as segment 1 of the liver, which comprised 8 segments. The resection of the caudate lobe can be performed as an Kumon2 first divided the caudate lobe into 3 parts: Spiegel’s extension of a lobectomy, other types of hepatectomies, or lobe, which was the equivalent to Couinaud’s segment 1 and even as an isolated resection. We present a surgical variant the conventional caudate lobe; the paracaval portion; and for isolated segment 1 resection that differs from previously the caudate process. Couinaud,3 like Healey and Schory,4 described techniques. We consider this to be an easier ap- later subdivided the caudate lobe into 2 subsegments named proach for a known difficult surgery because of its anatomic the left (segment 1 I) and right dorsal segments (segment situation. We describe our experience using this technique. 1r). Couinaud’s segment 1r is the equivalent to Kumon’s paracaval portion. Later, Couinaud5 called it segment 9, which encircled the side of the inferior vena cava (IVC). Therefore, the caudate lobe of the liver is anatomically Technique

Surgical * Corresponding author: Tel.: ϩ34-963-862-754; fax: ϩ34-961-973- 286. E-mail address: [email protected] For surgical anatomy purposes, the caudate lobe is con- Manuscript received November 15, 2008; revised manuscript February sidered to have 2 parts: Spiegel’s lobe (Couinaud’s segment 4, 2009 1) on the left and the paracaval portion (Couinaud’s seg-

0002-9610/$ - see front matter © 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.amjsurg.2009.02.012 R. Lopez-Andujar et al. Resection of segment 1 of the liver e43

Figure 1 (A) Transversal computed tomography scan image with a metastasis in segment 1 (red arrow). The black dotted line divides segments 1 and 9. (B) The anterior surface of the suprahepatic IVC is exposed, and the space between the RHV and the MHV is dissected 2 cm to 3 cm in the caudal direction using a right-angled clamp. (C) The infrahepatic IVC is dissected with direct vision between the anterior surface of the IVC and the posterior side of the liver (caudate segment) along 2 cm to 3 cm. (D) A long, curved Kelly clamp is inserted behind the caudal edge of the caudate lobe on the left side of the inferior RHV, if present. It is passed cranially along the anteromedian surface of the IVC toward the space between the previously dissected RHV and MHV. A tape is seized with the clamp and passed down between the anterior surface of the IVC and the posterior surface of the caudate lobe. ment 9) on the right, which includes the caudate process lobe come from the main left portal vein, they may also (Fig 1A). Both parts are anatomically divided by a deep come through from the right vein or the bifurcation.8 notch in 50% of individuals. In addition, the canal of Aran- The caudate lobe drains directly into the IVC and not tius, which is the in the embryonic typically through the left hepatic vein (LHV), right he- phase, can be used as an anatomic reference to define the patic vein (RHV), or middle hepatic vein (MHV). Ac- limit between segments 1 and 9.6,7 cording to the anatomical study of Kogure et al,9 the Although most arterial branches of the caudate lobe arise hepatic venous system not only comprises 1 or 2 proper from the left hepatic artery, some arise from the right he- hepatic veins draining the caudate lobe but also several patic artery. In addition, there might also be several small small accessory hepatic veins. The number and size of branches from the portal vein to the caudate lobe. There is these vary in each case, and they are distributed through- normally a large trunk about 1 mm in diameter and 5 mm in out the caudate lobe. The posterior edge of the caudate length. The identification and ligation of these arterial and lobe over the left side normally has a fibrous attachment venous branches are key steps in the resection of the caudate encircling the IVC to join segment 7. In up to 50% of lobe. Although most portal vein branches to the caudate patients, this fibrous band is replaced by hepatic paren- e44 The American Journal of Surgery, Vol 198, No 3, September 2009 chyma that can actually embrace the IVC completely. MHV and LHV, leaving the tape at the left side of the LHV This situation represents an additional obstacle to the (Fig 2B). Thereafter, the caudal end of the tape is relocated resection of the caudate. and passed to the left of the main portal vein (Fig 2C). Both Regarding the biliary drainage of the caudate lobe, be- ends of the tape are then pulled up to facilitate the direct tween 1 and 3 bile ducts usually drain each portion with a exposure of segment 1 (Fig 2D). We prefer to usea1cm maximum of 5 ducts for the whole caudate. Most of Spie- wide and 40 cm long cloth tape because those made of gel’s lobe ducts drain into the left hepatic duct, although plastic or silicone break easily when touched with the cav- some may drain into the right posterior sectoral duct and itron ultrasonic surgical aspirator (CUSA). less commonly into the right hepatic duct or the confluence At this point, the resection line of the right side of the of the hepatic ducts. Most ducts from the paracaval portion segment 1 is decided, leaving an adequate tumor-free mar- drain into the right posterior sectoral duct, although a sig- gin. We mark the line of the parenchyma section on the nificant percentage (27%) drain into the left hepatic duct.10 inferior edge of the caudate lobe, and 2 traction stitches are placed at both sides of the section line to delimit the line Surgical technique (Fig 3A). To perform the parenchyma resection, we pull from these 2 points to open the section line, at the same time The liver is exposed through a right subcostal abdominal pulling upward from the 2 ends of the tape to line up the incision. After an exploratory laparotomy, the liver is mo- parenchymal section, thus facilitating better hemostasis and bilized from its peritoneal attachments. Then, the lesser preventing injury of the IVC and MHV. The hepatic paren- omentum is carefully divided by dissection so as not to chymal transection is performed by means of a CUSA, and injure an aberrant left hepatic artery, which is present in Pringle’s maneuver is only used if necessary. The paren- 18% of cases.11 An intraoperative ultrasonography must be chymal transection progresses and continues cephalad along performed, which allows the confirmation of the hepatic the tape, and all vasculobiliary branches found on the line of vascular anatomy in relation to the tumor and also rules out the hepatic section are resected between ligatures or clips other lesions and enables diagnosis of possible vascular until the section is completely finished (Fig 3B). infiltrations. Isolated resection of segment 1 involves 3 major steps: Step 3. Once the parenchymatous section has been com- (1) control of the inflow blood supply from the left portal pleted, the exposed short hepatic veins draining directly into vein and left hepatic artery; (2) parenchymal section; and the IVC are seen much easier (Fig 3C), even though the (3) dissection, ligature, and section of the retrohepatic veins. tumor is larger. Segment 1 can be moved to the left of the cava vein, thus facilitating the individual ligations and di- Step 1. Normally, a dissection of the caudate blood supply visions of the retrocaudate veins. Normally, there are 1 to 3 at the base of the umbilical fissure is easy because segment sizable veins and several fine veins at this location. When 1 vessels coming from the left side of the portal vein and the these have been divided, the hepatocave ligament surround- left hepatic artery are identified and sectioned. If they are ing the IVC is cut, and the resection is completed (Fig 3D). easily localized at this point, the biliary radicals of segment In addition, low central venous blood pressure controlled by 1 can be ligated and sectioned; otherwise, this step can be the anesthesia team is recommended because this helps to done during the parenchymatous section. reduce blood losses during the hepatectomy and in case of vein injury. Step 2. The anterior surface of the suprahepatic IVC is exposed, and the space between the RHV and the MHV is dissected 2 cm to 3 cm caudally using a right-angled clamp Results (Fig 1B). Then, the anterior surface of the infrahepatic IVC is dissected with direct visualization of 2 cm to 3 cm (Fig We have performed the isolated resection of segment 1 1C). This is followed by the insertion of a long, curved with the hanging maneuver in 4 cases (Table 1). All of these Kelly clamp behind the caudal edge of the caudate lobe on procedures were completed successfully. Patients (3 men the left side of the inferior RHV (if present), which is then and 1 woman, aged 56–73 years) were diagnosed with passed cranially along the anteromedian surface of the IVC metastases from colorectal cancer (3 cases) and breast can- toward the space between the previously dissected RHV and cer (1 case). No patient required blood transfusion during or MHV. About 2 cm to 3 cm are dissected without direct after the operation. The mean tumor diameter was 3 cm vision (Fig 1D). A tape is then seized with the clamp and (range 2–8 cm). The resection margin was negative in all passed down between the anterior surface of the IVC and patients (R0). There were no postoperative deaths and only the posterior surface of the caudate lobe (Fig 2A). After 1 minor complication, a wound infection. There was no retracting the lateral segment of the liver, the ligamentum postoperative liver failure in any patient. The mean postop- venosum is ligated and divided, and a tunnel is created on erative stay was 5 days (range 4–8 days). One relapse in a the posterior surface of the common trunk of the MHV and distant liver segment was observed after a 15-month follow- LHV. The cranial end of the tape is passed through the up, and 3 patients are disease free after a mean follow-up tunnel and pulled down behind the common trunk of the period of 16 months (range 8–20 months). R. Lopez-Andujar et al. Resection of segment 1 of the liver e45

Figure 2 (A) The tape is placed on the anterior surface of the retrohepatic IVC. (B) A tunnel is created on the posterior surface of the common trunk of the MHV and the LHV. Through the tunnel, the cranial end of the tape is passed toward the left side of the LHV. (C) The caudal end of the tape is relocated and passed to the left of the portal trunk. (D) Pulling up both ends of the tape plays an important role in raising the liver. The blue vessel loop is placed around the left portal vein. The red vessel loop is placed around the left hepatic artery. The cranial end of the tape arises from the left of the LHV and the caudal end does so from the left side of the portal trunk.

Comments approach in right hepatectomies. This assistance has been further spread to other types of resections,20 and its use has The caudate lobe is commonly involved in metastatic or been described in caudate resections.21 Two tunnelings are primary liver neoplasms. Several techniques to resect tu- required in this maneuver: one is retrohepatic and in front of mors in this lobe, including lobectomy, segmentectomy, the IVC, and the other is caudal to the common trunk of the caudate lobectomy, isolated caudate lobectomy, and partial MHV and LHV. These tunnelings should not be attempted hepatectomy, have been described in the literature.6–8,12–17 when tumors either invade the retrohepatic IVC or are This highlights the lack of a standard technique and absence of uniform criteria to perform this type of surgery, which is behind the common trunk of the MHV and LHV because likely because of the difficulty in performing this resection they may cause profuse hemorrhaging or tumor spillage. given the depth and complicated location of the caudate However, this technique offers several advantages. A lobe adjacent to major vessels. Isolated caudate lobectomy straight transection plane from the anterior surface of the is a challenging technical procedure for which safe and liver to the IVC can be obtained, and the lifting of the tape reliable techniques have not yet been developed. pulls the liver up, providing a better exposure, protection of Lai et al18 proposed the previous approach for right the IVC, and easy control of any bleeding in the transection hepatic tumors, which are difficult to mobilize with a view surface or the deeper parenchyma of the liver. to facilitate their handling. Belghiti et al19 proposed the liver Based on previous findings, we have performed the same hanging maneuver using a tape placed in the anterior sur- surgical technique in 4 clinical cases (Table 1) and have also face of the IVC as a complement to facilitate the previous introduced several modifications that facilitate the resection e46 The American Journal of Surgery, Vol 198, No 3, September 2009

Figure 3 (A) The line of the parenchyma section leaving a wide tumor-free margin is marked (white dotted line), and 2 traction stitches at both sides of the section line are placed (black arrow). The blue vessel loop is placed around the left portal vein. The red vessel loop is placed around the left hepatic artery. (B) While performing the parenchyma section, it is easy to control, ligate, and section the segment 1 biliary ducts (white arrow). The blue vessel loop is placed around the left portal vein, and the red vessel loop is placed around the left hepatic artery. (C) The parenchymatous section has been completed, and, by pulling the segment 1 (S1) to the left, the exposed short hepatic veins draining directly into the IVC can be controlled and sectioned easily. The blue vessel loop is placed around the left portal vein, and the red vessel loop is placed around the left hepatic artery. (D) Surgical bed after resection. The blue vessel loop is placed around the left portal vein, and the red vessel loop is placed around the left hepatic artery. with the previously described technique.21 We performed hilar plate. Although seemingly tedious, the afferents from the parenchymatous section before approaching the retro- the portal veins to the caudate lobe can be visualized and hepatic direct veins. The mobilization of the caudate lobe in controlled with meticulous dissections. Back bleeding from large tumors is a very challenging technique to perform, given the small hepatic veins is rarely an issue because it is the problems involved in exposing the surgical area. This controlled before portal dissection. Moreover, we did not technique can generate hemorrhages or lead to mandatory clamp the LHV or MHV during resection, and we had no vascular controls of major vessels with subsequent hemody- hemorrhaging. The initial control of the arterial and portal namic disorder. Moreover, it involves intense manipulations of veins minimizes the risk of bleeding during the parenchy- the tumor, potentially causing tumor dissemination. matous transection. Furthermore, the section can be com- In addition, we disagree that a hepatic inflow occlusion pleted with a meticulous dissection of the parenchyma by (Pringle’s maneuver) is mandatory as others have pro- CUSA without Pringle’s maneuver, which may lead to posed.12 In fact, we did not use this technique in any of our disorders because of the ischemic injuries in the remaining patients. Inflow occlusion of the caudate lobe can be liver, specifically in those with previous chemotherapy achieved by portal dissection, even without lowering the and/or cirrhosis. R. Lopez-Andujar et al. Resection of segment 1 of the liver e47

Table 1 Clinical and pathological features

Extra operative Blood Surgical Tumor Resection Hospital Patient Sex/age Diagnosis procedure transfusion (mL) time (min) size (cm) margin (R) stay (d) 1 M/73 CCR metastasis Incisional 0 250 5 ϫ 3R08 Ϫrelapse hernia repair 2 M/62 CCR metastasis 0 180 2 ϫ 3R04 3 F/56 Breast Cancer 0 200 3 ϫ 3R04 metastasis 4 M/70 CCR metastasis Limited 0 220 2 ϫ 2R05 resection S6 CCR ϭ colorectal cancer; M ϭ male; F ϭ female; R ϭ resection.

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