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One-stage ultrasonographically guided

hepatectomy for multiple bilobar
colorectal metastases: A feasible and
effective alternative to the 2-stage
Guido Torzilli, MD, PhD, Fabio Procopio, MD, Florin Botea, MD, Matteo Marconi, MD,
Daniele Del Fabbro, Matteo Donadon, MD, Angela Palmisano, MD, Antonino Spinelli, MD,
and Marco Montorsi, MD, Milan, Italy

Background. Two-stage hepatectomy with or without portal vein embolization allows treatment of
multiple bilobar metastases, thereby expanding operative indications for these patients. Two operations
are needed, however, and some patients are not able to complete the treatment strategy because of disease
progression. Using experience gained from our policy of ultrasonographically guided resection, we
explored the safety and effectiveness of 1-stage operative procedures in patients otherwise recommended for
the 2-stage approach.
Methods. A total of 29 patients with multiple ($4) bilobar colorectal liver metastases (CLM) were selected from 100 consecutive patients submitted to surgical resection. The total number of preoperative
CLM was 163 (median, 5; range, 2--20). The operative strategy was based on tumor-vessel relationships
at intraoperative ultrasonography (IOUS) and on findings at color Doppler IOUS.
Results. There was no in-hospital mortality. Tumor removal was feasible with 1-stage operative
procedures in all but 3 patients who underwent laparotomy. The overall morbidity rate was 23%
(6/26); none of the patients required reoperation. Major morbidity occurred in 1 patient (4%). Blood
transfusions were administered in 4 patients (15%). After a mean follow-up of 17 months (median, 14;
range, 6--54), 3 patients had died from systemic recurrence, 12 patients were alive without disease, and
11 were alive with disease. No local recurrences were observed at the resection margin.
Conclusion. IOUS-guided resection based on strict criteria allows a 1-stage operative treatment in selected
patients with multiple bilobar CLM. This strategy decreases the need for a two-stage hepatectomy, thereby
avoiding the disadvantages of a 2-stage approach. (Surgery 2009;146:60-71.)
From the Third Department of General Surgery, University of Milan, IRCCS Istituto Clinico Humanitas,
Rozzano, Milan, Italy

(CLM) remains the gold standard therapy, limited
only by its technical feasibility.1 The key to the procedure’s success is leaving enough remnant liver to ensure patient survival. In cases of multiple and bilobar
Supported in part by a research grant from the Cesare Banno`
Foundation for Cancer Research.
Accepted for publication February 13, 2009.
Reprint requests: Guido Torzilli, MD, PhD, Associate Professor
of Surgery, Chief, Liver Surgery Unit, Third Department of Surgery, University of Milan, IRCCS Istituto Clinico Humanitas, Via
Manzoni 56, 20089 Rozzano, Milan, Italy. E-mail: guido.torzilli@
0039-6060/$ - see front matter
Ó 2009 Mosby, Inc. All rights reserved.


CLM, the most commonly used operative approach
is a 2-stage hepatectomy.2 This multistep strategy
uses limited resections and major hepatectomies
with or without preresection portal vein embolization (PVE).2,3 This method also allows extending
operative indications to those patients previously
judged to be unresectable, because the metastatic
disease would demand the removal of too much
liver parenchyma for the resection to be curative.
This approach, however, has some drawbacks. Two
operations are needed, each of which is associated
with mortality and morbidity. In addition, some
patients do not complete this treatment approach
because of tumor progression during the interval
between the 2 surgical procedures or after PVE.
A possible alternative, however, does exist. We
have shown, both for primary and metastatic liver

the so-called hepatocaval confluence. and was analyzed after a minimum follow-up of 6 months. Number 1 A B DL C DL CLM DL CLM G A B P CLM G A B P HV D E DL CLM G A B P CLM DL HV Fig 1. computed tomography (CT). (2) 4 or more lesions.or second-order portal branches and/or HV at caval confluence). Liver failure was considered mild when the total serum bilirubin concentration ranged from 2 to 5 mg/dL for >3 days postoperatively. A.4-7 Using information gleaned from this experience. Technical feasibility . Postoperative death was analyzed at 30 days and 90 days after operation.5 cm distance between the CLM and the hepatic vein (HV). (B) <0. even when the tumors have complex presentations such as multiplicity and vascular invasion.5 cm) of at least 1 CLM with a major intrahepatic vascular structures (first. From 2004. Eligibility criteria. P.Torzilli et al 61 Surgery Volume 146. B. Inclusion criteria for the current study were as follows: (1) patients presenting with resectable CLM.5 cm distance between the CLM and the Glissonian pedicle (G). The dotted line shows the dissection line (DL). that a well-defined policy of ultrasonically guided hepatectomy allows us to carry out radical operations safely and without major removal of liver parenchyma in the vast majority of patients. was defined as the last 4 cm of the HV before its confluence into the inferior vena cava (IVC). we explored the feasibility.9 Local tumor recurrence was defined as recurrence at the cut-edge (true local recurrence). (C) contact <1/3 circumference between the CLM and G. Artery. (3) bilobar involvement of the liver. even with minimal bile duct dilation at any imaging modality. after a multidisciplinary meeting with our medical oncologists. Preoperative imaging work-up consisted of abdominal transcutaneous ultrasonography (US). (E) contact between the CLM and HV. Any adverse event that required additional operative treatment or any invasive corrective procedure was considered a major postoperative morbidity. Pre-operative work-up. Operative strategy based on intra-operative ultrasonography tumor type. appearance. neoplasms. METHODS Terminology. Patients were selected for 1-stage resection based on technical feasibility. and effectiveness of a 1-stage operative procedure in a prospective cohort of patients who otherwise would have undergone the 2-stage approach. and relation between colorectal liver metastases (CLM) and major hepatic vessels: (A) <0. A criterion for nonresectability was the presence of bilateral tumor involvement of the first-order portal branches for $1/3 vessel circumference. and chest spiral CT for every patient. bile duct. The hepatic vein (HV) at the caval confluence. or magnetic resonance imaging (MRI). regardless of size or number of metastases. (D) contact >1/3 circumference between the CLM and G. The terminology for liver anatomy and resections used in this study is based on the Brisbane classification. (4) contact or close adjacency (<0. 18-fluoro-2-deoxy-glucose positron emission tomography (18F FDG-PET) imaging was also included. and severe when it exceeded 10 mg/dL for >3 days postoperatively.8 Hepatic resections are considered major when at least 3 adjacent segments are removed. medium when it ranged from 5 to 10 mg/dL for >3 days postoperatively. portal branch. safety.

Japan). In particular. Vessel resection was carried out (Fig 1. parenchyma fed by the portal branch that is to be resected must be considered. was established if residual liver volume (RLV) with optimal blood inflow and outflow and biliary drainage was expected to be sufficient.10. A and B). which was injected intravenously. blue in P6-7: blood flow opposite to the probe) once the right hepatic vein (RHV) is clamped by finger compression (no color inside the vessel). For those patients with tumor(s) close to the hepatocaval confluence or in the paracaval portion of segment 1. D and E). C). both equipped with the standard 2--6 MHz convex probe. Italy).8 mL of microbubbles filled with sulfur hexafluoride (SonoVue. based on the IOUS criteria for tumor--vessel relations reported previously. vessels were spared if IOUS showed the following: (1) the portal branch or HV was separated by a thin layer of liver parenchyma (detectable by IOUS even if < 5 mm) from a CLM (Fig 1. the contrast agent consisted of 4. Intraoperative ultrasonography (IOUS) was performed using an Aloka SDD 5500 and. and the 5--10 MHz microconvex probe. A J-shaped laparotomy was usually performed.5 mg/dL. Using CT or MRI. if it represented $50% of the whole liver volume in the presence of cirrhotic liver. C). surgeons calculated the liver volume by adding together the liver areas determined for each slice.5 and 2 mg/dL. or (2) the portal branch was in contact with a CLM without vessel wall discontinuation. with contact < 1/3 of the vessel diameter. Tokyo.11 At this point. more recently.62 Torzilli et al Surgery July 2009 Fig 2. The inferior right hepatic vein (IRHV) as it appears at intraoperative ultrasonography. Bracco Imaging. or if the total serum bilirubin level ranged between 1 and 1. In particular. tumorectomy alone was considered acceptable. a J-shaped thoracoabdominal incision was carried out. Fig 3. RLV was considered sufficient if it represented 40% of the whole liver volume in the case of normal (or even steatotic) liver. eFlow mode shows the hepatopetal flow (arrows) in the sectional (P5-8 and P6-7) portal branches (red in P5-8: blood flow toward the probe. the extension of the resection to the whole liver parenchyma drained theoretically by that vein was considered only in the absence of at least one of these conditions: . the vessel was considered invaded and therefore resected (Type Cb) (Fig 1.4. Operative technique. Inferior vena cava.4 In the case of resecting an HV. IVC. The main feature is that it runs behind the main right (RPV) and right sectional (P5-8 and P6-7) portal branches.5 the operative strategy was defined. In addition. E). and without proximal bile duct dilation (Fig 1. The staging was completed with contrast-enhanced intraoperative ultrasonography (CEIOUS). but between a CLM and an HV. hepatic resection was contraindicated if serum bilirubin level was $2 mg/dL. To determine the extent of resection. In the event of diseased liver parenchyma and a total serum bilirubin level ranging between 1. In all the other conditions (Type C). 5--10 MHz T-shaped. an Aloka Alpha 10 (Aloka. in a condition similar to type B (Fig 1.

Surgery Volume 146. both hemilivers were mobilized. Once thick vessels were exposed on the dissection plane. color flow in the portal branches to segment 8 ventral (P8v) and 8 dorsal (P8d) remains hepatopetal (red and blue. showing reversal of blood flow into the HV to be resected once it was clamped or compressed. after finger compression is applied to the caval confluence of the RHV. the surgeon used a fingertip to push on the opposite side. usually by dividing the right and left triangular and coronary ligaments. according to the aforementioned criteria. Number 1 Torzilli et al 63 Fig 4. d d d d IOUS showing accessory HVs (Fig 2). showing hepatopetal blood flow in the feeding portal branch once the HV to be resected was clamped. Once the operative strategy was defined. which appeared as an echogenic line due to the entrapment of air bubbles and clots between the cut surfaces (Fig 8). The flat tip of the device was positioned between the probe and the liver surface. Another method to draw the resection area on the liver surface with the aid of IOUS was to use the fingertips. Color Doppler IOUS. flow direction in the RHV indicated by the arrows is reversed (red).13 This technique involves encircling the vessel with a suture that is visible on IOUS as an echogenic spot with a posterior shadow. eFlow mode IOUS directly detecting collateral circulation and showing the HV to be resected connecting with the one adjacent to it (Fig 5). Vessels thicker than 2 mm were ligated with 2-0 or 3-0 sutures. Ultrasonographic guidance was used to direct the dissection plane. Color Doppler IOUS. with or without eFlow mode. With the thin tip of the electrocautery device positioned between the probe and the liver surface. On the right. This method enabled the surgeon to approach lesions located in the posterosuperior and paracaval segments. these HVs were compressed only by IOUS-guided finger compression when the plan was to divide the vessel away from its caval confluence. thus making the liver’s profile visible on IOUS. which resulted in a shadow visible on IOUS. and bipolar electrocautery for vessel coagulation. the so-called hooking technique was used to avoid erroneous vessel ligation. In contrast. As a result. and the tumor edge could be estimated precisely and the resection area marked on both liver surfaces (Fig 7). spatial relationships between the fingertip. Furthermore. Mobilization together with the J-shaped incision (and. the shadow of the electrocautery device. if not already occluded by the tumor5 (Fig 3). HVs were encircled and clamped when they were to be resected at their caval confluence. if not already occluded by the tumor (Fig 4). Arrows in the image on the left are showing flow directions toward the inferior vena cava (IVC) in the right hepatic vein (RHV) and middle hepatic vein (MHV). Ultrasonographic guidance enables the stitch to be hooked to the . the crush-clamping method. respectively). A) on the surface of the liver by using an electrocautery device under IOUS control. The parenchymal transection was performed using intermittent clamping by the Pringle maneuver12 using Pean forceps. while it remains hepatofugal (blue) as shown by the arrows in the MHV. with or without eFlow mode (Aloka. the J-shaped thoracoabdominal approach) allowed the liver to be retracted to the right or the left. Japan). Tokyo. The areas for resection were demarcated (Fig 6. in selected patients. using the eFlow mode.

outlining the traction point on IOUS. In addition. exposed vessel. To improve guidance along the proper trajectory of the dissection plane. the cut surface of the liver was refilled with saline to avoid the artifacts generated by the residual air bubbles . the vessel can then gently be pulled up. (A) The resection areas (arrows and asterisks) on various aspects of the liver surface defined with an electrocautery device under intraoperative ultrasonography guidance to completely remove the 49 CLM. the cuts (arrows and asterisks) on the various aspects of the liver surface obtained at the end of the resections that were carried out to remove the 49 CLM. The specimen was studied with the water bath technique.64 Torzilli et al Surgery July 2009 Fig 5. the specimen and the liver cut surface were examined with IOUS to be sure of complete nodule removal. From the left to the right. Once resection was accomplished. the surgeon’s fingertips were positioned at the posterior aspect of the resection area. which consists of realtime control to assure that the targeted nodule was entirely present within the specimen removed from the liver (Fig 9). which causes it to stretch slightly. arrows show intraoperative ultrasonography detection (with the eFlow) of a collateral vessel connecting the middle hepatic vein (MHV) and the right hepatic vein (RHV). (B) From left to right. Fig 6.

Surgery Volume 146. NJ) and/or fibrin glue (either Tissucol purchased from Baxter [Deerfield. 36--82). the electrocautery device positioned between the liver surface (arrows) and the surgeon’s fingertip positioned on the opposite side of the liver (F) allow the surgeon to draw an ideal plane for dissection (white arrows). A total of 44 patients were excluded because of massive liver involvement in 13. 2--13). 100 (69%) underwent liver resection. as described previously. To rule out bile leakage. we performed a careful examination of the resection area. Percutaneous ablation therapy was proposed when hepatic recurrence was visible at US. if necessary. with a median of 5 lesions per patient (range. We studied the morbidity. but did not routinely perform intraoperative cholangiography. The patients were followed in our institution by an expert hepatobiliary team every 3 months with a physical examination. At intraoperative ultrasonography. Fig 7. the same procedure of demarcation was repeated on the cut surface. we studied the rate of true local recurrence (at the resection margin) after a minimum follow-up of 6 months. stable disease in 7. and tumor . amount of blood loss. closed-suction drains were always left near the resection area. or lymph node metastases in 8. and CT or MRI (twice a year). Based on the above criteria. Chemotherapy was associated with disease progression in 10 patients. The total number of preoperative metastatic lesions was 163. and not close to any visceral cavities such as the stomach or colon. and alanine aminotransferase (ALT) on the 1st. 5th. and then re-imaged with IOUS. The median size of the largest CLM was 4 cm (range. Of the 29 patients.14 Multihole. B) were secured by suture control of vessels and. Finally. serum carcinoembryonic antigen levels. Among 144 consecutive patients referred to our unit between September 2001 and December 2007. by electrocautery. IL] or Quixil obtained from Ethicon). liver function tests. 2--20). and 2 underwent intraoperative ablation therapy at the time of the colon resection. we selected 29 patients (29%) including 16 males and 13 females with a mean age of 63 years (range. Re-resection of recurrences was always considered without or with resectable extrahepatic disease. aspartate aminotransferase (AST). and resection was accomplished (Fig 10). 2 patients underwent 1 limited resection at the same time as the colon resection. 19-French. Ethicon. mortality. Because the secondary outcome for this study was the reliability of the procedure from an oncologic standpoint.15 A chest tube was left in patients undergoing thoracoabdominal incision. 5th. < 2 cm. and 7th POD. Somerville. Outcome measures. and 7th POD) showed a decrement. If residual lesions were observed. multiple distant metastases in 23. 3rd. and clots. and rate of blood transfusions. the cut surfaces of the liver (Fig 6. Patients. The dissection plane (arrows) is visible at intraoperative ultrasonography and is passing just adjacent to the portal branch to segment 5 and 8 (P5-8) along a systematic extended right posterior sectionectomy (SERPS) procedure. Number 1 Torzilli et al 65 Fig 8. as well as the serum levels of total bilirubin. Drains were removed on the 7th postoperative day (POD) or when the bilirubin level in the drain discharge (sampled routinely on the 3rd. US (twice a year). 19 (66%) received chemotherapy before resection. fibrillar-oxidated regenerated cellulose (Fibrillar Tabotamp.

9 additional lesions were found.5). Onestage. 4--49). a type B relation for 5 CLM in 4 patients. Gauze. 299-958). IOUS confirmed 29 CLM with macrovascular invasion (28 type C and 1 Cb subtype. A thoracoabdominal incision was carried out in 7 patients (27%). all of which were confirmed at pathology together with the 157 lesions detected preoperatively. Only 1 of 26 patients (4%) underwent a right hepatectomy associated with 2 limited leftsided resections. Once the specimen is removed. and type A + C combined relations for 6 CLM in 6 patients. 16 (61%) had tumors at the hepatocaval confluence. At exploratory laparotomy. which represents the only major hepatectomy. All procedures. Preconditioning was never used. transparent arrows indicate the resection margin that is defined on the cut surface with the electrocautery device under IOUS guidance. whereas proportions are presented as numbers and percentages. At follow-up. RESULTS Feasibility and intraoperative findings. In 14 of the 21 patients studied with CEIOUS.66 Torzilli et al Surgery July 2009 Fig 9. After IOUS. 65--348). G.000 mL). an overall clamping time of 348 minutes was required to resect 49 lesions (Fig 6. and 2 patients were referred to our Unit without any previous treatment. In 1 patient. IOUS. There were 67 tumor--vessel relations classified at IOUS (Table). Median clamping time was 116 minutes (range.7 was performed in . Therefore. An extended right posterior sectionectomy (a so-called systematic extended right posterior sectionectomy [SERPS procedure]). Continuous variables are presented as medians and ranges. the total number of resected lesions was 269. and CEIOUS. Each type of operative resection is outlined in the Table. A and B). 1 patient underwent percutaneous ablation for 2 CLM with incomplete tumor necrosis. 50-1. 3 patients had diffuse peritoneal carcinomatosis. Of the 26 patients. 103 new lesions were detected in 18 patients. All the preoperative treatments were carried out in other centers before referral. The median operation time was 555 minutes (range. The overall median blood loss was 500 mL (range. reduction in 2. Statistical analysis. including operations. the presence of the tiny CLM (arrows) is confirmed with intraoperative ultrasonography (A) and with the water bath technique (B).T. according to the IOUS criteria for tumor--vessel relations4. corresponding to a median of 6 lesions per patient (range. In 20 patients (77%). A tiny residual CLM (asterisk) is visualized with intraoperative ultrasonography (IOUS) exploring the cut surface (arrows) after tissue removal was accomplished. Operative procedures. Fig 10. IOUS disclosed a type A relation for 27 CLM in 17 patients. were performed by the same surgeon (G. complete resection of CLM was feasible in 26 of 29 patients. Only 4 patients (15%) received blood transfusions.).

PRS5-6 (1 les. PRS8 (4 les. 1 CHV 19 22 2 AHV. Number 1 Table.). RH.).).).).). In-hospital mortality and 90-day mortality was nil.).).14 Pathology. PRS3 (1 les.). SX.).).). SS6-7 (1 les. PRS5-6 (7 les.) LL (2 les.).). PRS8 (2 les.). PRS2 (1 les. PRS7 (4 les.). 1 BP1.).). Patient lesions IOUS class CLM-vessel relation 4 4 6 4 5 5 6 6 9 10 11 6 11 10 1 CHV.). PRS5 (1 les. second-order portal branch. PRS5 (4 les.) PRS2 (1 les. PRS2 (1 les.). 2 CHV 20 21 22 5 6 49 3 AHV 1 AHV 3 AHV. partial resection.). PRS5 (1 les. 1 C+AHV.) ext S4sup LL (3 les. and showed signs of previously diagnosed chronic hepatitis in 1. PRS4inf (1 les. PRS4inf (1 les. PRS4-5 (5 les.) ext S4sup LL (2 les. 1 CP2 2 AHV 12 13 12 11 1 AP2.). cp.) PRS4sup (1 les. first-order portal branch.) SS2 (1 les. the drains .Torzilli et al 67 Surgery Volume 146. CLM.). Margins of 0 mm were obtained in all 5 patients with CLM having a B pattern at IOUS.). PRS2 (1 les. 1 CHV+AP2 AHV. A wedge resection of right-sided lung metastases was combined in 2 patients for 2 lung CLM.). based on our policy described previously. 1 CHV CP2+AHV. PRS5 (3 les.).). 1 AP1 AHV.).). Minimum resection margins ranged from 0 to 8 mm.).). PRS3 (2 les.).). P2.) ext S4sup LL (1 les. 2 CP3. IRHV. PRS3 (2 les. colorectal liver metastases.). PRS4inf-5 (8 les. PRS6 (1 les. PRS7 (1 les.). PRS6-7 (3 les.).). PRS6 (1 les. S4inf RH (1 les. PRS6 (3 les. PRS6 (1 les. PRS1cp (1 les. PRS8d (1 les.) PRS3 (1 les. The overall morbidity rate was 23% (6/26). PRS3-4inf (1 les. and was accomplished through the thoracoabdominal incision. 1 CP3 C P2+HV.).). PRS7-8 (11 les. PRS2-3 (3 les.). SS6 (1 les.). PRS4inf (2 les.).).).).).). HV. 1 CHV CHV. caudate lobe.). PRS2-3 (14 les.). SERPS (4 les. The liver parenchyma was steatotic in 12 patients. PRS5 (1 les. SS4sup (1 les.) PRS2-3 (1 les.) PRS2-3 (1 les.). 1Cb 24 25 26 Total 9 12 5 269 1 1 1 2 1 1 1 1 AHV. cirrhotic in 1. pp. PRS6 (2 les. Postoperative outcome. third-order portal branch.) PRS2-3 (1 les. UP. Type of liver resections No.). 1 CP3 AP1.). hepatic vein. PRS4-5-8 (6 les. PRS6-7 (2 les. PRS6-7 (3 les. PRS8v (1 les. PRS7 (3 les. 1 CHV 1 BP1. PRS7 (1 les. 1 CP2 1 2 3 4 5 6 7 8 BUP. PRS8 (3 les. PRS8 (2 les. PRS4sup (3 les.). PRS7 (2 les. right hepatic vein. P1. PRS8d (1 les. PRS4-5-8 (2 les. SS5 (1 les.). PRS5-8 (1 les.).). cl.). Minor morbidity consisted of transient fever in 2 patients and increased bilirubin level (#89 mg/dL) in the output of 1 drain in 3 patients.).).). and in 7 of the 21 patients with an A pattern at IOUS. left lobectomy (segments 2 and 3). Major morbidity occurred in 1 patient and consisted of pulmonary embolism. ext. PRS4inf-5 (3 les.) PRS2 (1 les. P3. PRS4inf-5 (1 les. PRS4inf-5 (3 les.).). PRS5 (1 les. SS7-8 with RHV in IRHV+ (3 les. 1 CP2.). 1 BP2 23 11 1AHV.).). PRS2-3 (2 les.).). PRS2-3 (5 les.).) PRS2-3 (1 les. PRS4sup (1 les. SERPS. PRS8d (1 les. right hepatectomy. 1 BUP. Intraoperative ultrasonography.) PRS1cl (1 les. PRS4inf-5 (1 les. PRS4 (1 les.). 3 CP3 AHV.). PR. PRS3-4-5 (6 les.). PRS2 (2 les.). 1 CP3 AP1.).) PRS4sup-8d (3 les. LL (1 les.) PRS2 (1 les. PRS8v (3 les.).) SS2 (1 les.). normal in 12. 5 patients. 1 C+AP2. PRS1pp (1 les. segment X. SERPS (9 les.). 1 CP3 1 AHV.).). umbilical portion. segmental resection segment X. All resected nodules proved to be metastases from adenocarcinoma.). PRS1pp (2 les. PRS8v (2 les. PRS4inf-5 (1 les. PRS8v (2 les. PRS8 (2 les. PRS6-7 (1 les. PRS7 (1 les.).). Drains were removed from all but 3 patients on the 7th POD.) PRS2 (1 les.). PRS1cl (1 les. PRS6-7 (5 les.). PRS4 (1 les. PRS6-7 (5 les.).) IOUS. SERPS (8 les. PRS4inf (1 les. 1 CHV 14 15 16 17 13 5 7 18 1 1 1 3 18 17 1 AHV. systematic extended right posterior sectionectomy. PRS7 (3 les. 1 CHV.). All these resections were combined with limited left-sided resections. PRS5 (1 les.). PRS3 (1 les. PRS4sup (1 les.). None of the patients required reoperation.). RHV. PRS8d (2 les. paracaval portion. SERPS (4 les.). 1 CHV+AP2 AHV.). PRS8 (2 les.) PRS3 (1 les. PRS5-6 (3 les. SSX.).). PRS1cp (1 les. PRS7 (1 les. PRS6 (1 les. SS7-8 with RHV in IRHV+ (1 les. PRS4inf-5 (1 les.). 1 CP2 C P2+HV+AP2.). LL.). inferior right hepatic vein.). caudate process. PRS6-7 (2 les.) PRS3 (1 les. PRS7 (2 les.) PRS2-4sup (1 les.). 1 CP2 2 CP3 1 AP1 1 CP2 67 Type of resection PRS2 (1 les. PRS5+SS8 (1 les.).).

Systemic chemotherapy was also given to the patient with extrahepatic relapses only. Among the latter. After a median follow-up of 14 months (mean.18 it still results in additional morbidity for the treatment strategy as a whole.29 Performing more conservative hepatic resections allows for repeat hepatectomies should a new CLM be detected. in the side where more CLM were removed in 3.4-6 we herein explored the possibility of providing at least the same therapeutic results of the 2-stage approach with a 1-stage approach.3 Furthermore. 1 patient (10%) died.18 whereas others have a worse outcome because of a greater rate of new lesions in the remnant liver compared with patients who did not undergo PVE.1 Indeed. several studies have demonstrated that a limited tumor-free margin is not a contraindication for resection by showing that the risk of recurrence at the resection margin does not appear to be greater. for the other 3 patients. range. contrary to the 2 major reports on 2-stage hepatectomies. 16th. but we did not observe any local recurrence at the resection margin. our aim was to establish a surgical procedure that maximizes parenchymal-sparing and allows curative resection in 1 stage. 17. 5 (50%) are alive with disease. and 23rd POD. with no need for a two-stage approach.8. 12 (46%) are alive without disease. The median follow-up for this subgroup was 8 months. The median hospital stay was 9 days (range. Long-term outcome.25 In contrast.68 Torzilli et al were left in place until the bilirubin level in the drain output decreased to <10 mg/dL. whereas none of the patients who underwent liver resection under the guidance of IOUS had residual tumor. The drain was then removed. often resulted in resection margins of 0 mm.4. However. Indeed. It is noteworthy that. re-resection was possible in 2 of the 5 patients with hepatic relapses only in our series.24 we have shown how. AST.2 and 19 (median. and 11 (42%) are alive with disease. although we never achieved a minimal resection margin of 1 cm. respectively. there was no recurrence at the resection margin during a mean follow-up similar to that of the 2 major reports on 2-stage hepatectomies: 17 (median. percutaneous ablation was carried out in 3.5. it is possible to spare liver parenchyma in most circumstances. percutaneous ablation was carried out in 2. Indeed.19-23 Using the experience gained from our established policy. Rather than making major resections safer. following and expanding on previous experiences. 19--24% of patients do not complete the treatment strategy. Of those 10 patients operated for CLM who had progression during chemotherapy. and in 1 patient with hepatic recurrences and resectable extrahepatic . with the aid of IOUS. Liver recurrences occurred bilaterally in 7 patients. liver resection was combined with total abdominal hysterectomy and salpingo-oophorectomy in 1. DISCUSSION Two-stage hepatectomy combining limited resection and major hepatectomies with or without PVE is a multistep strategy for the treatment of otherwise unresectable multiple bilobar CLM. Moreover. procedures that preserve major vascular structures allow more surgical options than a major hepatectomy. As a consequence. Of the 26 patients.28. 5 patients have had both liver and extrahepatic recurrences: 5 hepatic recurrences only and 1 extrahepatic recurrence only. 14) of our series versus 22 (median.3 respectively. and 4 (40%) are alive disease-free. Serum levels of bilirubin. and the patients were discharged on the 13th. despite complex presentations. 8--33).27 Based on precise criteria. In addition. not reported).2. which we believe are suboptimal even when compared with 0-mm margin resection. other authors in the 1990s showed that 16% to 18% of patients with hepatocellular carcinoma who underwent liver resection without IOUS guidance had positive margins.3. in cases of recurrence.2. and in the opposite side in the remaining 3 patients. 12).16 although more recent series describe greater levels of safety.17 PVE itself is associated with morbidity.3 we never adopted intraoperative ablation therapies. Of the 8 patients who had hepatic relapses combined with extrahepatic disease. major hepatectomies are still associated with appreciable rates of mortality and major morbidity including liver failure. and systemic chemotherapy was administered in the remaining 4. 6--54). Re-resection was carried out in 2 of the 5 patients who had only liver recurrences. although reported at only 2%. mainly because of disease progression or insufficient Surgery July 2009 remnant liver hypertrophy.7 IOUS guidance helps maximize the possibility of getting closer to the tumor. 3 patients died from both liver and extrahepatic recurrence (12%). however. it was feasible to limit the use of a formal right hepatectomy to just 1 of the 26 patients (4%) in our series. This policy. and the third patient refused any other treatment.4-7 For this reason. 15% of patients do not benefit from PVE.2. and ALT returned to normal usually by POD 5.26.

36. and courses are available to train surgeons in the use of ultrasound in surgical practice. representing 42% of all the lesions removed. A possible criticism of our approach is that the procedure is based on intraoperative findings and.39 especially for those patients undergoing operation after chemotherapy. we have started a School for Surgical Ultrasonography in Europe. The intraoperative detection of 112 new lesions by IOUS and CEIOUS.35 Although these intermittent clamping times are quite long.4-7 By using the criteria we have outlined.2. Furthermore. Multiple CLM lesions are associated generally with a greater rate of missed lesions at preoperative imaging. Our approach. The 1-stage procedure may also be safer than the 2-stage approach with or without PVE. the inflow occlusion. does not ignore the preoperative findings. Such long operations have often been associated with those series featuring the best results in terms of safety. the preoperative workup was crucial in allowing us to expect the feasibility of a 1-stage approach by means of aggressive parenchymal sparing. The American College of Surgeons has recognized recently the need for specifically trained surgeons in the United States and. AST. which minimized blood transfusion rates (15% in this series).32-34 We were able to obtain good results with up to 348 minutes of clamping time similar to that of 322 minutes reported by Sakamoto et al. in the spared hemiliver with the greatest number of CLM to be removed.3 We included patients with a minimum of 4 bilobar CLM. has beneficial effects on both shortand long-term outcomes.6. furthermore. although we acknowledge that we have not included a comparable control group undergoing a 2-stage approach. Our series includes those patients with unfavorable Torzilli et al 69 conditions compared with those considered for the 2-stage procedure. parenchymal-sparing approach may even lead to a greater overall resection rate than a 2-stage approach. a complete resection using a 1-stage. there was no mortality or increased incidence of major morbidity.2 Furthermore.1. there did not appear to be a greater rate of liver recurrence. seems inadequate for accurate intrahepatic staging. were able to receive local treatment with radical intent. patients with CLM having relations with major intrahepatic vascular structures. All these considerations should help in the concerns about major selection bias and.7 Intermittent hepatic inflow clamping has been shown in several series to be safe and effective compared to no clamping and to continuous clamping with or without preconditioning. the multimodal approach has a fundamental role that should be discussed with every patient with multiple CLM when obtaining informed consent for the first operative treatment.38. With our approach.19-23 The operative technique we proposed herein is not simple because it involves multiple combined procedures that account for the long durations of the operative procedure and the long clamping times.30 even in cirrhotic patients.37 This prospective cohort of patients was compared with historic data reported by other centers. and recurrences were bilateral.2. many lesions that would appear to require a major hepatic resection by conventional criteria can actually be resected without a major hepatic resection as shown in the herein presented series. including the cost of state-of-the-art ultrasound machines and the need for hepatic surgeons to be well trained in their use. all 5 patients with hepatic relapses only.31 A long and careful procedure may be required to achieve optimal hemostasis and the prevention of biliary leak. except the 1 patient who refused both reoperation and percutaneous ablation therapy. and ALT returned to normal usually by POD 5. In fact. and patients with disease progression after chemotherapy. the 3 patients submitted to exploratory laparotomy for diffuse carcinomatosis also would not have been considered suitable for the 2-stage operation. serum levels of bilirubin. show that this approach is not just an alternative to the 2-stage policy.Surgery Volume 146. . We noted that 54% of patients developed disease during the follow-up (50% involving the liver) in our study compared to 64% (48% involving the liver) reported by Jaeck et al3 and 69% (61% involving the liver) reported by Adam et al. a wide range of prices for suitable ultrasound machine exists. The resectability rate of our series from outpatient clinic to exploration is rather high (>60%). Number 1 disease. Sparing a substantial amount of the liver parenchyma by our aggressive parenchymal-sparing technique does not seem to expose patients to a greater risk of recurrence. cannot be applied systematically. These considerations highlight the central and crucial role played by IOUS and CEIOUS in treating these patients.3. for this reason. Patients should agree to their willingness for re-treatment to not invalidate this approach. However.4. similarly. but may allow the opportunity to operate on patients otherwise considered unresectable by the conventional approaches. Furthermore. There are limitations of IOUS and CEIOUS. Furthermore. however. however.40 who represented 66% of our series. is worthy of discussion.5. In this sense.39 PET.

Marconi M.241:715-22. Broglio KR. Caridi JG. Del Fabbro D. Bachellier P.197:164-70. Right portal vein ligation: a new planned two step all-surgical approach for complete resection of primary gastrointestinal tumors with multiple bilateral metastases. Palmisano A. et al. Ruszniewski P. Montorsi M. Healey AJ. Marconi M. Sugai S. Kosuge T. Rosso E. Ouellet JF. et al.240:1037-49.9:1148-53. Two-stage hepatectomy: a planned strategy to treat irresectable liver tumors. J Am Coll Surg 2005. Notes on the arrest of hepatic hemorrhage due to trauma. Minagawa M. The Brisbane 2000 terminology of hepatic anatomy and resections. Ijichi M. Torzilli G. Am J Surg 1999. Tam PC. Kawasaki S.11:815-8. 14. 3. Makuuchi M. Preoperative portal vein embolization for extended hepatectomy. Ann Surg 2008. Miki Y. Pringle JH. 28. et al. Torzilli G. Long-term results of resection for large hepatocellular carcinoma: a multivariate analysis of clinicopathological features. Is extended hepatectomy for hepatobiliary malignancy justified? Ann Surg 2004. Ann Surg 2004. Bachellier P. Torzilli G. Torzilli G. Roncalli M. Surg Gynecol Obstet 1987. Del Fabbro D. J Am Coll Surg 2003. 16. 6.239:722-39. Olivari N. Arch Surg 2000. Hepatology 1990. Gambetti A. Fan ST. Donadon M. 5. 15. et al. Pawlik TM. 9. et al. Yamazaki S. Fujita S. Takayama T. Del Fabbro D. Donadon M. Ann Surg Oncol 2007. Preoperative portal vein embolization for major liver resection: a metaanalysis. Hemming AW. Ng MM. Oussoultzoglou E. 8. Kubota K Makuuchi M. Denys A. Ultrasonographically-guided surgical approach to liver tumours involving the hepatic veins close to the caval confluence. Ann Surg 2000. Torzilli G. Hochwald SN. Palmisano A. Hepatectomy for stage B and stage C hepatocellular carcinoma in the Barcelona Clinic Liver Cancer classification: results of a prospective analysis. Donadon M. Montorsi M. Sugawara Y. Four new hepatectomy procedures for resection of the right hepatic vein and preservation of the inferior right hepatic vein. Marconi M.48:541-9. 17. Arch Surg 2008. Roche A. The authors thank Ms Rosalind Roberts for her editorial assistance during manuscript preparation. 24. Di Stefano DR. Sano K. Bismuth H. Hasegawa H. Kokudo N. The terminology committee of the IHPBA. Donadon N. et al. Surgery July 2009 13. et al. et al. Nemr RA. 19. J Gastrointest Surg 2005.240:1037-49. Leoni P. 26. Azoulay D. Radiology 2005. Toyoda H. et al. HPB 2002. et al. 22.131:294-9. Andres A. Ellis LM. 12. et al. Makuuchi M. Systematic extended right posterior sectionectomy: a safe and effective alternative to right hepatectomy. Donadon M. Belghiti J. Ann Surg 2004.2:333-9. Harihara Y. et al. Makuuchi M. 20. Preoperative percutaneous portal vein embolization: evaluation of adverse events in 188 patients.231:480-6.237:686-93. Del Fabbro D. Laurent A. Sano K. et al. Genetic and histological assessment of surgical margins in resected liver metastases from colorectal carcinoma: minimum surgical margins for successful resection. Imamura H. A two-stage hepatectomy procedure combined with portal vein embolization to achieve curative resection for initially unresectable multiple and bilobar colorectal liver metastases. Ng IO. Kato Y. Elias D. Lai EC. Botea F.139:766-74. Ann Surg 2008. Takayasu K. . Castaing D. Effect of surgical margin status on survival and site of recurrence after hepatic resection for colorectal metastases. A new technical aspect of ultrasound-guided liver surgery. Kubota K. Farges O. 23. Lok AS. Howard RJ.70 Torzilli et al In conclusion. de Baere T. Torzilli G. Torzilli G. Ann Surg 2003. Reed AI. REFERENCES 1. Pawlik TM. Sequential preoperative arterial and portal venous embolizations in patients with hepatocellular carcinoma. Laurent A. 18.232:777-85. Makuuchi M. Del Fabbro D. may rise above many of the limitations and consequences of a 2-stage approach. 21. Del Fabbro D. ‘‘Radical but conservative’’ is the main goal for ultrasonography-guided liver resection: prospective validation of this approach. Extension of the frontiers of surgical indications in the treatment of liver metastases from colorectal cancer: long-term results of our experience. Torzilli G.239: 818-25. Ann Surg 2005. Lasser P. Ann Surg 2000. Spinelli A. Adam R. 2. Weber JC.247:49-57. Hasegawa K. Palmisano A. Arch Surg 2002. Kianmanesh R. Sakamoto Y. 11. Ellis V. et al. Takayama T. Hepatogastroenterology 2005. 4. 7. De Baere T.234:625-30. Sauvanet A.93:1238-46. Bilirubin level fluctuation in drain discharge after hepatectomies justifies long-term drain maintenance. Cailliez V. Spinelli A. Azoulay D. Abdalla EK. Yanagisawa A.143:1082-90. Palmisano A. Surgery 2002. Gambetti A. Preoperative selective portal vein embolization before hepatectomy for liver metastases: long-term results and impact on survival. Jaeck D. Ann Surg 1908. Smail A.52: 1206-10. Torzilli G. Greget M. Aoki T. Recurrence and outcomes following hepatic resection. et al. Vauthey JN. Ann Surg 2000. This strategy limits the need for 2-stage hepatectomy and. Palmisano A. Gendarini A. Ann Surg 2004.14: 1347-55. Bianchi P. Oussoultzoglou E. 25. Castaing D. Contrast-enhanced intraoperative ultrasonography during surgery for hepatocellular carcinoma in liver cirrhosis: is it useful or useless? A prospective cohort study of our experience. Weber JC. Makuuchi M. Jaeck D.137:833-40.178:341-3. 27. in so doing. et al. Arch Surg 2004. 1-stage hepatectomy/ metastasectomy in patients with multiple bilobar CLM. A two-stage hepatectomy procedure combined with portal vein embolization to achieve curative resection for initially unresectable multiple and bilobar colorectal liver metastases. Greget M. Arens JF. Del Fabbro D. Palmisano A. 201:517-28. Matsukura A. Rosso E. Wei SH. Abdalla EK. Abdalla EK. Scoggins CR. Takayama T. Adam R. Vauthey JN. Zorzi D. Eng C. Donadon M.164:68-72. and combined resection/ablation for colorectal liver metastases.231:487-99. Hui AM. Abdalla EK. Abulkhir A.135: 1395-400. Br J Surg 2006. Contrast-enhanced intraoperative ultrasonography during hepatectomies for colorectal cancer liver metastases. Limongelli P. Pollock R. 10.247:603-11. we have shown that IOUS-guided resection based on strict criteria allows a radical but parenchymal-sparing. radiofrequency ablation. Randomized trial of the usefulness of a bile leakage test during hepatic resection. Resection of nonresectable liver metastases from colorectal cancer after percutaneous portal vein embolization.

Arch Surg 2004.134:984-92. Metser U. Torzilli G.80:493-4. Donadon M. No-mortality liver resection for hepatocellular carcinoma in cirrhotic and noncirrhotic patients: is there a way? A prospective analysis of our approach. Jagot P. et al. et al. Wong J. Kokudo N. Gambetti A. Liu CL.244:921-30.6:16-23. Torzilli et al 71 36. Sugawara Y. Prospective evaluation of Pringle maneuver in hepatectomy for liver tumors by a randomized study. Feingold D.139:1061-5. 32. Geva R. Pringle’s maneuver lasting 322 min. et al. . Lubezky N. Botea F. Fan ST. Ng IO. 39. Jacobson JS. Wang X. Maema A. Abrams JA. et al. Procopio F. Ultrasonography during liver resection for hepatocellular carcinoma. controlled trial comparing intermittent portal triad clamping versus ischemic preconditioning with continuous clamping for major liver resection. The role and limitations of 18-fluoro-2-deoxy-D-glucose positron emission tomography (FDG-PET) scan and computerized tomography (CT) in restaging patients with hepatic colorectal metastases following neoadjuvant chemotherapy: comparison with operative and pathological findings. Eur J Cancer 2008. Sakamoto Y. Arch Surg 1999. 40. Predictors of survival after hepatic resection among patients with colorectal liver metastasis. McCormack L. Makuuchi M. Lo CM.its impact on operative outcome. Leung KL. Yamamoto J. Leoni P. et al.46:457-8. Takayama T. Malafosse R. Petrowsky H. Imamura H.Surgery Volume 146. Arch Surg 2003. Inoue K. Noun R.115:303-9. Man K. 30. et al. Kita Y. Hepatogastroenterology 1999.138:1198-206. Number 1 29. et al. Belghiti J. Grann VR. Takayama T. Perioperative blood transfusion promotes recurrence of hepatocellular carcinoma after hepatectomy. Torzilli G. Techniques for hepatectomies without blood transfusion focusing on interpretation of postoperative anemia. Br J Surg 1993.97:1606-12. Sano K. Montorsi M. Use of contrast-enhanced intraoperative ultrasonography during liver surgery for colorectal cancer liver metastases -.226:704-13. A prospective. 34. J Gastrointest Surg 2007. et al. 37. Continuous versus intermittent portal triad clamping for liver resection: a controlled study. 35. 31. randomized. Lau WY. One thousand fifty-six hepatectomies without mortality in 8 years. et al. Ann Surg 1999. Del Fabbro D. Kosuge T. Analysis of a prospective cohort study. Ann Surg 1997. 38. Seyama Y. et al. Makuuchi M. 33. Trujillo M. Surgery 1994. Br J Cancer 2007. Hershman DL. Torzilli G. Minagawa M.229:369-75.11: 472-8. Ann Surg 2006. Lee TW.