Surgery for malignant liver tumors by murplelake76


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Review Article                                                                                                           

Surgery for malignant liver tumors
Recent decades have witnessed an increase in liver resections. There is a need for an update on factors related to the management of       Parul J Shukla,
liver tumors in view of newer published data. A systematic search using Medline, Embase, and Cochrane Central Register of Controlled       Savio G Barreto1

Trials for the years 1983–2008 was performed. The IHPBA classification provides a suitable nomenclature of liver resections. While one     Department of
randomized trial has provided an objective time of 30 min as optimal for intermittent pedicle occlusion, another randomized study has      Gastrointestinal Surgical
demonstrated the feasibility of performing liver resections without pedicle clamping. A randomized trial has demonstrated the benefit      Oncology, Tata Memorial
                                                                                                                                           Hospital, Mumbai, India,
of clamp crushing over newer techniques of liver transection. Cohort studies support anatomical resections when feasible in terms          1
                                                                                                                                             Department of General
of outcomes. Nonrandomized studies also support nonanatomical and ablative therapies in patients with cirrhosis and small remnant          and Digestive Surgery,
livers. A randomized trial has shown comparable long-term outcomes of radiofrequency ablation (RFA) and surgery for tumors <5 cm.          Flinders Medical Center,
                                                                                                                                           Adelaide, Australia
No randomized trials comparing laparoscopy and open surgery exist. Surgery remains an important treatment modality for malignant
hepatic neoplasms. While anatomical resections provide improved survival, the choice of nonanatomical versus anatomical resections         For corresponence:
should be individualized taking into account factors such as cirrhosis and function of the liver remnant. A clear margin of resection is   Dr. Parul J Shukla,
                                                                                                                                           Department of
essential in all surgically resected cases. RFA is emerging as a useful, often complimentary tool, to surgery when dealing with complex
                                                                                                                                           Gastrointestinal Surgical
tumors or tumors in patients with a poor liver function. Laparoscopic ultrasonography is useful in staging and performance of RFA.         Oncology, Tata Memorial
                                                                                                                                           Hospital, Parel, Mumbai
                                                                                                                                           – 400 012, India. E-mail:
KEY WORDS: Hepatocellular carcinoma, metastasis, radiofrequency ablation                                                         

                                                                                                                                           DOI: 10.4103/0973-

INTRODUCTION                                                          update on the current principles of practice. The                    PMID: *****

                                                                      role of liver transplantation in the management
Over the last few decades, there has been a steady                    of liver tumors is rapidly advancing. A complete
increase in the number of liver resections being                      discussion of the role of liver transplant in the
performed across the world and definitely in India[1]                 management of hepatocellular carcinomas is
as well. Interestingly, this has been accompanied by                  beyond the scope of this review. This review thus
a reduction in morbidity and mortality[2-5] especially                focuses only on surgical and complementary
so when the surgeries are performed by trained                        ablative strategies for hepatocellular carcinomas.
surgeons. It would be unfair to attribute these
improvements to a single factor.                                      A systematic search of the scientific literature
                                                                      was carried out using the Medline, Embase, and
The various contributory factors include an                           the Cochrane Central Register of Controlled Trials
improved understanding of the anatomy (liver                          for the years 1983–2008 to obtain access to all
segments) [6-8] and physiology of the liver cell                      publications, especially randomized controlled
regeneration,[9] improved techniques of transecting                   trials, systematic reviews, and meta-analyses
the liver parenchyma,[10] technical innovations                       involving the various factors related to surgery and
aimed at reducing blood loss during surgery,[11-15]                   complementary ablative therapies for liver tumors.
better investigative modalities to aid the diagnosis[16]
and accurate planning of the surgery,[17-19] newer                    The search was carried out with the appropriate
insights into the perioperative changes taking                        specific search terms “hepatocellular carcinoma,”
place during liver surgery coupled with improved                      “surgery,” “metastasis,” “parenchymal transection,”
anesthetic management intraoperatively thereby                        and “radiofrequency ablation.”
aiding the surgeon during liver resection,[20,21] and
the impact of improved surgical technique coupled                     CLASSIFICATION OF LIVER RESECTIONS
with a wider exposure to liver surgery amongst
current surgical trainees.[22]                                        In 2000, the International Hepato-Pancreato-Biliary
                                                                      Association (IHPBA) proposed its classification of
With the ever-increasing data being published in                      liver anatomy and liver resections in an attempt
the literature on the management of liver tumors,                     to overcome the conflicting and inappropriate
it is essential to review these data to provide an                    terminology that had plagued liver surgery since

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                                                     Shukla, et al.: Surgery for malignant liver tumors

the description of the hepatic segments. Table 1 simplifies the                 30 min with 5 min of reperfusion. They found that extending
various hepatic resections in relation to the liver segments as                 the IPO time to 30 min not only helped achieve a greater
proposed by the Brisbane 2000 system.[8,22]                                     resection area per unit time, but was also associated with
                                                                                no significant difference in the bilirubin ratio compared
BASIC PRINCIPLES OF LIVER SURGERY                                               to 15-min occlusions. This ultimately led to an improved
                                                                                preservation of the remnant liver function. This is the only
Vascular inflow control                                                         randomized controlled trial till date. till such time as more
The Pringle maneuver has been shown to reduce blood                             evidence is available on the benefits and adverse effects
loss and preserve liver function in the early postoperative                     of hepatic pedicle clamping, hepatic surgeons would be
period. It has also been shown to reduce the need for blood                     better served by performing the technique they are familiar
transfusions.[23] This initial study by Man et al.[24] was followed             with bearing in mind the data available at the current time
by another study by Belghiti et al.[25] comparing intermittent                  which does seem to imply that safe hepatic resections can
versus continuous pedicular clamping. Interestingly, they                       be performed without the need to clamp the hepatic pedicle.
found that the intermittent clamping was better than                            However, should the need arise for pedicle clamping, the data
continuous clamping for a number of reasons, the most                           obtained from the study by Esaki et al.[30] would suggest that
important being increased ischemia time without increasing                      an IPO of 30 min would be adequate.
the ischemic insult to the liver. They felt that the greater
ischemia time afforded by intermittent clamping permitted                       Liver parenchyma transection
a safer and often more complete surgery to be performed
                                                                                Liver parenchymal transection has been performed by
even in patients with preexisting liver dysfunction. Nuzzo et
                                                                                numerous techniques over the last century. Early methods
al.[26] confirmed the safety of hepatic pedicle clamping. They
                                                                                used included the division of the liver by blunt instruments
routinely performed continuous pedicle clamping and reserved
                                                                                including the finger,[31] the blunt end of the haemostat[32] or
intermittent clamping for patients with an impaired liver
                                                                                the scalpel,[33] and the finger fracture technique popularized by
function and when more prolonged ischaemia were required.
                                                                                Lin et al.[34] Newer modalities for transecting the liver include
They avoided the performance of pedicle clamping in patients
with limited bleeding, jaundice, and patients undergoing                        an ultrasonic dissector (CUSA) using ultrasonic energy, the
simultaneous bowel anastomosis.                                                 hydrojet using a pressurized water jet, and a dissecting sealer
                                                                                (Tissue Link) using radiofrequency energy.
Van der Bilt et al.[27] in a murine model demonstrated that
ischemia/reperfusion was associated with an increased long-                     Weber et al. [35] demonstrated the safety and efficacy of
term risk of recurrence of colorectal hepatic metastasis in the                 heat coagulative necrosis using radiofrequency energy for
hepatic remnant. They followed this up by demonstrating that                    segmental and wedge resections of the liver. Their technique
perinecrotic hypoxia was possibly linked to this phenomenon.[28]                involved sequential insertion of radiofrequency needles around
                                                                                the tumor creating a necrotic rim of tissue around the tumor
In 2006, Capussotti et al.[29] citing adverse effects of hepatic                that could be transected in a bloodless manner.
pedicle clamping on liver regeneration performed a
randomized controlled trial comparing intermittent pedicle                      Table 2 shows the results of the various randomized studies
clamping versus no clamping and found that liver resections                     comparing some of the recently introduced techniques of
could be performed safely even in patients with diseased livers                 liver parenchymal transection with the older techniques.
without clamping the pedicle.                                                   Interestingly, in the randomized trial by Lesurtel et al.,[10] the
                                                                                clamp crushing technique was found to be the most efficient
Recently, Esaki et al.[30] reported their results following a                   compared to CUSA, hydrojet, and dissecting sealer in terms
randomized controlled trial comparing intermittent pedicle                      of resection time, blood loss, blood transfusion frequency, and
occlusion (IPO) for 15 min with 5 min of reperfusion versus                     cost efficiency.

Table 1: Classification of liver resections as per the IHPBA Brisbane 2000 system[8,22]
                                                                      Segment                             Appropriate terminology for the resection
First-order division anatomy and                              Right hemiliver (Sg 5–8)                                Right hepatectomy
resections                                                    Left hemiliver (Sg 2–4)                                  Left hepatectomy
Second-order division anatomy and                         Right anterior section (Sg 5, 8)                      Right anterior sectionectomy
resections                                                Right posterior section (Sg 6, 7)                     Right posterior sectionectomy
                                                             Left medial section (Sg 4)                           Left medial sectionectomy
                                                            Left lateral section (Sg 2, 3)                        Left lateral sectionectomy
Third-order division anatomy and                            Any one segment from 1–9                                   Segmentectomy
resections                                        Any two contiguous segments not deÞned above                        Bisegmentectomy
Resection of three sections                                        Sg 4–8 (± Sg 1)                                  Right trisectionectomy
                                                              Sg 2, 3, 4, 5, 8 (± Sg 1)                             Left trisectionectomy

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                                            Shukla, et al.: Surgery for malignant liver tumors

Table 2: Randomized trials comparing different techniques of liver parenchymal transection
Study                      Year       Groups                                                               Conclusion
Takayama et al..[36]       2001       Ultrasonic dissector (CUSA system, Valleylab Inc, Boulder,           Clamp crushing allows a higher
                                      Colorado) (n = 66) versus Pean clamp crushing (n = 66)               quality of surgery without an
                                                                                                           increase in blood loss
Rau et al.[37]             2001       CUSA (n = 30) versus jet cutter (n = 31)                             Jet-cutter is fast and safe for liver
Lesurtel et al.[10]        2005       Clamp crushing with Pringle’s maneuver versus CUSA (CUSA,            Clamp crushing was the most
                                      Tyco Healthcare,                                                     efÞcient
                                      MansÞeld, MA) versus hydrojet (Hydro-Jet, Erbe, Tubingen,
                                      Germany) versus dissecting sealer (TissueLink, Dover, NH)
                                      without Pringle’s maneuver (n = 25 in each group)
Saiura et al.[38]          2006       Ligasure (Valleylab, Boulder, CO) versus conventional clamping       Ligasure—safe and effective for
                                      methods (n = 30 in each group)                                       decreasing the liver resection time
Campagnacci et al.[39]     2007       EBVS ligasure V (Tyco Valleylab, Boulder, CO, USA) versus            EBVS—safe and effective with
                                      harmonic scalpel (Ultracision Ethicon Endo                           signiÞcant beneÞt on blood loss
                                      Surgery, Cincinnati, OH, USA) (n = 12 in each group)

EXPANDING THE HORIZONS OF LIVER RESECTION                              a benefit in terms of overall survival of an anatomical over a
                                                                       nonanatomical resection for hepatocellular carcinomas. These
Traditionally, a curative resection has been defined in terms          studies, seen in Table 3, assume significance when we consider
of segmental anatomy (anatomical resections) and the margin            the possibility of offering a curative resection to patients
of resection. An adequate margin is defined as “a complete             without compromising their postoperative liver function. It
removal of tumor tissue plus a clear resection margin ≥ 1 cm           also provides support to centers capable of performing major
on pathological examination” in which negative findings by             liver resections but who do not have a liver transplant unit
angiography are followed by Lipiodol CT and ultrasound 1 or            to back them.
2 months after resection.[40] However, the expansion in the
indications for surgery for liver tumors to include large tumors       Numerous groups have continued to demonstrate significant
requiring major resections with often an inadequate quantity           survival advantages in the performance of anatomical
of remnant liver to sustain hepatic function, as well as the           resections over nonanatomical resections [49-51] even in
undertaking of resections on cirrhotic and diseased livers has         cirrhotic patients. The advantage of anatomical resections for
led to the questioning of such previously held beliefs as well as      hepatocellular carcinoma thus cannot be downplayed.
the introduction of newer modalities to reduce the size of the
tumor or improve the size of the remnant liver parenchyma.             The Barcelona Clinic Liver Cancer (BCLC) staging system[52]
                                                                       divides liver cancers into four groups, namely, early,
Anatomical versus nonanatomical resections                             intermediate, advanced, and terminal. However, according to
The basis for the performance of an anatomical resection               the outcomes considering each treatment option available and
for liver tumors has centered on the nature of spread of               outcomes, the BCLC has recommended that surgical resection
hepatocellular carcinomas. Hepatocellular carcinomas have              should be reserved for patients with tumors ≤ 3cm and with
been shown to invade the portal venous branches and                    a good liver function. For more than three tumors or tumors
then spread from there[41] as satellite nodules or as distant          >3 cm, they recommend other alternatives including liver
metastasis. It was thus recommended to divide the portal               transplantation or local ablative therapies.
pedicles prior to hepatic dissection in segmentetomies and
lobectomies to prevent tumor cell dissemination.[42] However,          Given the conflicting nature of reported data on survival
there have been numerous studies that have failed to show              following different types of resections, it is prudent to consider

Table 3: Studies highlighting the lack of benefit of anatomical resections over nonanatomical resections for liver resections
in terms of overall survival
Study                              Year       Number of patients      Conclusion
Takano et al.[43]                  2000             300               No difference in the 5- and 9- year cumulative survival rates
                                                                      depending on the type of resection
Ercolani et al.[44]                2003                224            No difference in recurrence or disease-free survival depending on the
                                                                      type of resection
Kondo et al.[45]                   2005                110            Type of hepatectomy did not affect survival
Suh[46]                            2005                119            No difference in cumulative recurrence nor disease-free survival
Kaibori et al.[47]                 2006                247            In hepatitis C patients, anatomical resections do not provide any
                                                                      survival beneÞt unless technically indicated
Tanaka et al.[48]                  2008                125            No difference in hepatic recurrence rates or overall survival; median
                                                                      survival time after recurrence was higher though in nonanatomical
                                                                      resections indicating the importance of preserving the liver function

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                                                     Shukla, et al.: Surgery for malignant liver tumors

that while anatomical resections can be performed even in                       an insufficient remnant liver, a limited hepatectomy with RFA
cirrhotic patients, the decision to perform an anatomical                       of the remaining lesions can now be performed. The benefit of
resection should take into consideration the size of the remnant                such combinations has been tested by numerous authors who
liver and the presence of cirrhosis. The choice of performance                  have reported the safety and effectivity of this combination in
of resections should thus be individualized.[53] Nonanatomical                  colorectal cancer metastasis to the liver, as well.[72-74]
resections and/or local ablative therapies should be considered
as options in patients with cirrhosis and in patients in whom                   Margin of resection
the remnant liver following an anatomical resection may not                     The concept of an ideal margin of resection for malignant liver
be compatible with an adequate postoperative liver function.                    tumors has been traditionally regarded as 1 cm.[40] Wakai et
The aim should thus be to achieve a curative resection without                  al.[75] confirmed that colorectal metastasis to the liver should
compromising the postoperative liver function.                                  be resected with a 1 cm margin (based on the distribution of
                                                                                intrahepatic micrometastasis) and Shi et al.[76] concluded that
EXTENDING THE BOUNDARIES OF LIVER RESECTION WITH                                a 2-cm margin is necessary while resecting hepatocellular
PORTAL VEIN EMBOLIZATION AND RADIOFREQUENCY                                     carcinomas. However, other studies evaluating the influence
ABLATION                                                                        of the surgical resection margin in patients with hepatocellular
                                                                                carcinomas, hepatoblastomas, and colorectal metastasis to the
Portal vein embolization                                                        liver seem to indicate that more than the size, it is the presence
Kinoshita et al.[54] and Makuuchi et al.[55] were amongst the                   of a negative margin that is a principal indicator of long-term
first to propose the benefit of portal vein embolization (PVE)                  survival.[77-85] This assumes significance when major resections
of the lobe of the liver bearing the tumor with an aim of                       are undertaken wherein the question of the function of the
inducing a compensatory hypertrophy in the contralateral                        remnant liver is of prime concern. In all other cases where
lobe. Since then, there have been numerous studies validating                   standard resections are being undertaken, it seems prudent
the safety and efficacy of this procedure.[56-60] The indication                at this time to obtain an adequate surgical resection margin
for the performance of PVE is based on the size of the future                   of around a centimeter.
liver remnant (FLR) in relation to the total volume of the liver.
The cut-off varies between institutes but usually includes an                   LAPAROSCOPIC LIVER RESECTION
FLR of 25–40% of the total liver volume. The benefit of the
performance of PVE in patients with a normal preoperative                       The last two decades have witnessed an increase in the number
liver function has been questioned based on the findings of                     of liver resections attempted laparoscopically following the
Farges et al.[61] They found no benefit of PVE in such patients                 first reported case in 1996.[86] The development of laparoscopic
but did confirm the benefit of PVE in patients with chronic                     ultrasonography[87,88] and radiofrequency ablation (lap RFA) [89]
liver disease.                                                                  has further helped in the assessment of lesions in terms of
                                                                                intraoperative staging and also to decide on the margins
Radiofrequency ablation                                                         of resection. Laparoscopy is a useful tool in the staging of
Radiofrequency ablation (RFA), which induces cell death by                      liver tumors. The feasibility of performance of laparoscopic
coagulation necrosis using radiofrequency energy, was first                     resections for small lesions located in the left lateral and right
described by Rossi et al.[62] Since then, numerous trials have                  anterior segments has been shown[90,91] and even confirmed
demonstrated the efficacy of RFA as a percutaneous ablative                     in a meta-analysis comprising only nonrandomized studies. [92]
therapy in patients who are not good surgical candidates.                       Recently, Cho et al.[93] have demonstrated the feasibility of using
        The success of these initial trials led to an exploration               laparoscopy for small resections even in posteriorly located
of the role of RFA as a curative agent in patients amenable to                  lesions. However, most of these studies have involved the
surgical resection as well.[68,69] In 2006, Chen et al.[70] performed           resection of benign tumors or colorectal metastases to the
a randomized controlled trial comparing RFA versus surgery                      liver and even more uncommonly, hepatocellular carcinomas.
for hepatocellular carcinomas < 5 cm and demonstrated                           Thus, it is important to exert caution when interpreting and
equivalent short- and long-term outcomes (including 5-year                      extrapolating the results of these data as representative of
survival rates). Livraghi et al.[71] reported a 97.2% complete                  all liver resections. Moreover, the safety and the long-term
response rate at a median follow-up of 31 months in 218                         outcomes need to be confirmed even for these lesions.
patients undergoing RFA for lesions ≤2 cm. However, it is                       This especially assumes significance when hepatocellular
important to recognize that patients treated by RFA, as with                    carcinomas arise in the setting of cirrhosis. Data from
patients undergoing surgical resections, need to undergo a                      randomized controlled trials are awaited.
strict surveillance postprocedure as intra- and extra-hepatic
recurrences have been reported following treatment.[71] Instead                 CONCLUSION
of considering RFA as an alternative to surgery, there are now
studies analyzing the outcomes following combining RFA with                     Surgery continues to remain an important modality of
surgery in unresectable (multifocal or bilobar) tumors. In such                 treatment of malignant hepatic neoplasms amenable to
patients, in whom a surgical resection would be precluded by                    resection. Advancements in imaging modalities coupled with

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                                                       Shukla, et al.: Surgery for malignant liver tumors

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                                                                                       and the risk of postoperative renal dysfunction. J Am Coll Surg
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