elapsed after PVE) sensitively predicts the risk of postoperative hepatic insufficiency. A kinetic growth

rate >2.0%/week is strongly associated with a low risk of postoperative morbidity and mortality

irrespective of the sFLR volume.125

Figure 60-13. Example of right and segment IV portal vein embolization (PVE). Adequate hypertrophy of future liver remnant is

observed from the standardized future liver remnant (sFLR) volume of 10% to 33% at 4 weeks after PVE.

Recently, a new short-interval, two-stage liver surgery technique was reported which consists of an

initial open right portal vein ligation with in situ splitting of the liver parenchyma followed by

reexploration for right trisectionectomy; this technique is called associating liver partition and portal

vein ligation for staged hepatectomy (ALPPS).137 The combination of portal vein ligation and in situ

splitting of the liver to prevent cross-portal circulation between the lobes of the liver is believed to lead

to profound hypertrophy of the FLR. However, preliminary data suggested a high incidence of major

morbidity and inpatient mortality associated with this new procedure. The true efficacy of ALPPS in

preventing postoperative hepatic insufficiency remains controversial and this procedure is still

investigational.

SURGICAL TECHNIQUE

Exposure

8 Incision and exposure are key components of the quality of the exploration of the liver and the safety

of hepatectomy. Various incisions – including the inverted-T (Mercedes) incision, bilateral subcostal

(chevron) incision, right/left subcostal (Kocher/Kehr) incisions, J-shaped (Makuuchi) incision with or

without thoracotomy, and inverted L-shaped (modified Makuuchi) incision (Fig. 60-14) – have been

used to achieve these objectives. Recently evolved laparoscopic approaches may reduce the

disadvantage of a large incision for hepatectomy. However, most hepatobiliary malignancies require

complex surgical manipulations, including handling of the vena cava or major vessels just beneath the

right atrium. Thus, hepatobiliary surgeons should be familiar with the traditional approaches for safe

handling of the liver.

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Figure 60-14. Inverted L-shaped incision and exposure. The inverted L-shaped (modified Makuuchi) incision. The incision begins

cephalad to the xiphoid, extends to 1 cm above the umbilicus, and then extends laterally to the right. This incision achieves a

superb en face view of critical structures, including the hepatocaval junction. (Adapted from Chang SB, Palavecino M, Wray CJ, et

al. Modified Makuuchi incision for foregut procedures. Arch Surg 2010;145:281–284.)

Principles of Parenchymal Transection

The routine use of intraoperative ultrasonography has contributed to major improvements in liver

resection techniques.138 Intraoperative ultrasonography allows confirmation of the location of the

tumors, the sites of intrahepatic anatomic structures, and the direction of transection. For anatomic

resection of Couinaud segments, a segmental staining method with ultrasound guidance has been used

to confirm the segmental border on the liver surface.

The key point in anatomic resection of the liver is exposure of the landmark vein on the cut surface of

the liver. The three-dimensional shape of the intersegmental plane is not always flat and it varies

considerably among individuals.36,139 However, the specific landmark vein for each intersegmental

plane of the liver is consistent. Because the actual shape of the intersegmental plane is difficult to

recognize during parenchymal transection without a special staining technique such as the ICG

fluorescent technique140 or contrast medium for ultrasound,141 the identification and exposure of the

landmark vein on the cut surface of the liver is the only convincing technique that allows precise

anatomic resection of the liver (Fig. 60-15).

For hepatic parenchymal transection, multiple techniques and devices are available to hepatobiliary

surgeons, including clamps, staplers, jet cutters, ultrasonic aspirators (e.g., CUSA), saline-linked cautery

(e.g., TissueLink), bipolar electrocoagulation devices, radiofrequency transection devices, harmonic

scalpels, and microwave coagulators.142–145

Control of Bleeding

Inflow occlusion at the hepatic hilum (Pringle maneuver) is widely used to reduce blood loss during

hepatic parenchymal transection. Intermittent inflow occlusion (15 minutes of clamping and 5 minutes

of release) has been proven to be a safe procedure even for living-donor surgery for liver

transplantation.146,147 Under inflow occlusion, the amount of bleeding depends on the central venous

pressure and the height of the manipulating point from the level of the inferior vena cava. Therefore,

controlling central venous pressure by limiting the tidal volume and infusions in cooperation with

anesthesiologists is important. In addition, adequate lifting of the hepatic parenchyma with the

surgeon’s left hand decreases back-bleeding during hepatic parenchymal transection.

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Figure 60-15. Anatomic resection of Segments I + II + III + IV + VIII. This patient was found to have a huge HCC generated in

the left hemiliver on underlying steatohepatitis. Because the tumor also extended to Segments I and VIII, compressing the right

hepatic vein and hepatic hilum, left trisectionectomy was considered to be the most optimal approach. However, due to impaired

hepatic functional reserve (ICG-R15, 17%), the future liver remnant (i.e., right lateral sector) was considered too small (<30% vs.

standard liver volume). Therefore, Segment V was preserved with a staining technique. Top left: Puncture of Segment VIII portal

pedicle under ultrasound guidance and injection of indigocarmine (arrow). Top right: Segment VIII was clearly stained on the

surface of the liver (arrowheads). Bottom left: transection line for anatomic Segments I + II + III + IV + VIII resection was

marked by cautery. Bottom right: completion of anatomic resection fully preserving Segments V, VI, and VII. The right hepatic

vein is exposed on the cut surface of the liver (arrows).

Figure 60-16. Retrohepatic dissection and hanging maneuver during anterior approach. Left: The avascular plane between the

liver and the inferior vena cava is dissected and a tape is placed. Right: Traction of the tape during parenchymal transection

allows adequate control of bleeding from the deeper transection plane of the liver. (Adapted from Donadon M, Abdalla EK and

1565

Vauthey JN. J. Am Coll Surg 2007;204:329–333.)

When conventional mobilization of the liver is difficult prior to parenchymal transection due to tumor

invasion of the diaphragm on the right side of the liver, parenchymal transection needs to be preceded

by mobilization of the right lobe (anterior approach). To control bleeding at the deeper part of the liver

parenchyma in such cases, the hanging maneuver proposed by Belghiti et al.148 is widely used. This

maneuver involves dissecting the retrohepatic avascular space between the liver and the inferior vena

cava and placing a tape for lifting the liver. By retracting the tape during parenchymal transection,

squeezing pressure can be applied on the deep transection plane and may reduce bleeding (Fig. 60-16).

Bile Leak Test

Bile leak from the cut surface of the liver is a frequent major complication observed after liver resection

and requires postoperative drainage according to the degree of leakage (Table 60-3).149 Even though

various intraoperative tests have been tried, bile leaks are still reported in up to 8% of patients who

have undergone liver resection. Although it can be treated with adequate drainage, bile leak increases

the risk of sepsis and hepatic insufficiency. One group recently assessed the efficacy of transcystic

injection of air into the biliary system to test the patency of the biliary tract and to detect any air leak

from the major ducts of the parenchymal transection surface (Fig. 60-17) and found that postoperative

bile leak decreased from 10.8% to 1.0% (p = 0.008) with adequate use of a bile leak test after

completion of hepatectomy.150

Staged Surgery

When the liver tumor burden is limited, including small tumors and anatomically favorably positioned

bilateral metastases, a one-stage strategy involving one or more simultaneous partial hepatectomies in

lobar hepatic resection is safe and effective.151–156 In contrast, when extensive bilobar metastases are

present, different surgical strategies are required.

Figure 60-17. Air leak test for detection of bile leak. Left: With injection of air into the biliary tract, the point of bile leak can be

sensitively detected as an air leak point (arrows). Right: Patency of the bile duct can be confirmed as pneumobilia on ultrasound

image. (Adapted from Zimmitti G. Systematic use of an intraoperative air leak test at the time of major liver resection reduces the

rate of postoperative biliary complications. J Am Coll Surg 217;1028–1037, with permission.)

Table 60-3 Definition and Grades of Bile Leak After Liver Resection by

International Study Group of Liver Surgery (ISGLS)

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Two-stage liver resection is a reasonable approach for patients with advanced bilateral CLM who

responded to chemotherapy and in whom limited resection could clear the less affected side of the liver

before a planned extended contralateral liver resection. Patients undergo first-stage limited resection of

metastases in the left lobe that is followed by right PVE with or without Segment IV embolization to

allow hypertrophy of the FLR. Then, extended right hepatectomy is completed after the sFLR meets the

volume criteria. A previous study reported that 72.3% of the patients with planned two-stage liver

resection completed the second-stage resection and the 5-year survival of these patients was 51% but

15% in the cases treated with chemotherapy alone.157

The ALPPS procedure is a similar approach in which right portal vein ligation and parenchymal

transection at the time of first resection is performed instead of PVE. This procedure seems to offer

rapid growth of the FLR compared with conventional PVE. However, because the safety of this new

approach and the detailed techniques are still under investigation, clinical application should be limited

to highly selected patients at high-volume hepatobiliary centers.

Laparoscopic Liver Resection

9 The laparoscopic approach for liver resection has evolved since the early 1990s

158–161 and its

feasibility has since been established, especially for patients undergoing partial hepatectomy or left

lateral segmentectomy.162–165 Although this approach has benefits, including less postoperative pain,

earlier recovery, and shorter length of hospital stay compared to the conventional open approach,166–169

it requires experience with an open approach and advanced techniques in laparoscopic surgery. Because

the liver is a large, heavy organ, mobilization and parenchymal transection require advanced skill in a

limited surgical field. Recently, several centers have reported on the feasibility of the laparoscopic

approach for major hepatectomy or graft procurement of living donors for liver transplantation;

however, these complex laparoscopic procedures should not be approached by surgeons without

significant laparoscopic liver surgery experience. In addition, for patients with hepatic malignancies,

oncologic curability should be secured if the laparoscopic liver resection is adopted. Therefore, the

indication for laparoscopic approach should be determined according to the technical feasibility, the

surgeon’s surgical skill, and the oncologic curability of the tumors.

Liver Transplantation

Liver transplantation is a reasonable approach with a theoretically higher chance of eradication of

tumors, especially for patients with severe hepatic dysfunction. However, because of the negative

impact of posttransplant immunosuppression on tumor recurrence or progression, liver transplantation

was originally thought to be a contraindication for hepatic malignancy. More recent experience with

liver transplantation for hepatoblastoma in children170 or early-stage HCC77 has led to cautious

application of liver transplantation for hepatic malignancies. As we mentioned previously, several highvolume transplant centers have used their original expanded criteria for liver transplantation for

HCC,86–97,171 although these criteria have not yet been standardized and HCC meeting the Milan criteria

remains a standard indication for liver transplantation.

Liver transplantation has also been used in selected patients with other hepatobiliary malignancies,

such as NET,172–174 epithelioid hemangioendothelioma,175 colorectal cancer,176 and hilar

cholangiocarcinoma.177,178 However, the clinical evidence remains limited and true efficacy over other

nonsurgical treatments has not yet been proven.

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SUMMARY

Despite recent advances in the nonsurgical treatment of hepatic neoplasms, surgical resection still plays

a pivotal role. In the era of effective chemotherapy and interventional radiology, primary unresectable

tumor can become resectable during the treatment course, especially for CLM. However, oncologic

curability and surgical safety are, by nature, conflicting factors. Comprehensive assessment of the

oncologic characteristics, the hepatic lesions, and the status of the underlying liver is essential for

proper risk management and for selecting candidates with the greatest survival benefit from surgical

resection.

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