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 Table of Contents  
Year : 2009  |  Volume : 5  |  Issue : 3  |  Page : 154-160

Surgery for malignant liver tumors

1 Department of Gastrointestinal Surgical Oncology, Tata Memorial Hospital, Mumbai, India
2 Department of General and Digestive Surgery, Flinders Medical Center, Adelaide, Australia

Date of Web Publication16-Oct-2009

Correspondence Address:
Parul J Shukla
Department of Gastrointestinal Surgical Oncology, Tata Memorial Hospital, Parel, Mumbai - 400 012
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0973-1482.57119

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 > Abstract 

Recent decades have witnessed an increase in liver resections. There is a need for an update on factors related to the management of liver tumors in view of newer published data. A systematic search using Medline, Embase, and Cochrane Central Register of Controlled Trials for the years 1983-2008 was performed. The IHPBA classification provides a suitable nomenclature of liver resections. While one randomized trial has provided an objective time of 30 min as optimal for intermittent pedicle occlusion, another randomized study has demonstrated the feasibility of performing liver resections without pedicle clamping. A randomized trial has demonstrated the benefit of clamp crushing over newer techniques of liver transection. Cohort studies support anatomical resections when feasible in terms of outcomes. Nonrandomized studies also support nonanatomical and ablative therapies in patients with cirrhosis and small remnant livers. A randomized trial has shown comparable long-term outcomes of radiofrequency ablation (RFA) and surgery for tumors <5 cm. 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 should be individualized taking into account factors such as cirrhosis and function of the liver remnant. A clear margin of resection is essential in all surgically resected cases. RFA is emerging as a useful, often complimentary tool, to surgery when dealing with complex tumors or tumors in patients with a poor liver function. Laparoscopic ultrasonography is useful in staging and performance of RFA.

Keywords: Hepatocellular carcinoma, metastasis, radiofrequency ablation

How to cite this article:
Shukla PJ, Barreto SG. Surgery for malignant liver tumors. J Can Res Ther 2009;5:154-60

How to cite this URL:
Shukla PJ, Barreto SG. Surgery for malignant liver tumors. J Can Res Ther [serial online] 2009 [cited 2022 Dec 1];5:154-60. Available from: https://www.cancerjournal.net/text.asp?2009/5/3/154/57119

 > Introduction Top

Over the last few decades, there has been a steady increase in the number of liver resections being performed across the world and definitely in India [1] as well. Interestingly, this has been accompanied by a reduction in morbidity and mortality [2],[3],[4],[5] especially so when the surgeries are performed by trained surgeons. It would be unfair to attribute these improvements to a single factor.

The various contributory factors include an improved understanding of the anatomy (liver segments) [6],[7],[8] and physiology of the liver cell regeneration, [9] improved techniques of transecting the liver parenchyma, [10] technical innovations aimed at reducing blood loss during surgery, [11],[12],[13],[14],[15] better investigative modalities to aid the diagnosis [16] and accurate planning of the surgery, [17],[18],[19] newer insights into the perioperative changes taking place during liver surgery coupled with improved anesthetic management intraoperatively thereby aiding the surgeon during liver resection, [20],[21] and the impact of improved surgical technique coupled with a wider exposure to liver surgery amongst current surgical trainees. [22]

With the ever-increasing data being published in the literature on the management of liver tumors, it is essential to review these data to provide an update on the current principles of practice. The role of liver transplantation in the management of liver tumors is rapidly advancing. A complete discussion of the role of liver transplant in the management of hepatocellular carcinomas is beyond the scope of this review. This review thus focuses only on surgical and complementary ablative strategies for hepatocellular carcinomas.

A systematic search of the scientific literature was carried out using the Medline, Embase, and the Cochrane Central Register of Controlled Trials for the years 1983-2008 to obtain access to all publications, especially randomized controlled trials, systematic reviews, and meta-analyses involving the various factors related to surgery and complementary ablative therapies for liver tumors.

The search was carried out with the appropriate specific search terms "hepatocellular carcinoma," "surgery," "metastasis," "parenchymal transection," and "radiofrequency ablation."

 > Classification of Liver Resections Top

In 2000, the International Hepato-Pancreato-Biliary Association (IHPBA) proposed its classification of liver anatomy and liver resections in an attempt to overcome the conflicting and inappropriate terminology that had plagued liver surgery since the description of the hepatic segments. [Table 1] simplifies the various hepatic resections in relation to the liver segments as proposed by the Brisbane 2000 system. [8],[22]

 > Basic Principles of Liver Surgery Top

Vascular inflow control

The Pringle maneuver has been shown to reduce blood loss and preserve liver function in the early postoperative period. It has also been shown to reduce the need for blood transfusions. [23] This initial study by Man et al. [24] was followed by another study by Belghiti et al. [25] comparing intermittent versus continuous pedicular clamping. Interestingly, they found that the intermittent clamping was better than continuous clamping for a number of reasons, the most important being increased ischemia time without increasing the ischemic insult to the liver. They felt that the greater ischemia time afforded by intermittent clamping permitted a safer and often more complete surgery to be performed even in patients with preexisting liver dysfunction. Nuzzo et al. [26] confirmed the safety of hepatic pedicle clamping. They routinely performed continuous pedicle clamping and reserved intermittent clamping for patients with an impaired liver function and when more prolonged ischaemia were required. They avoided the performance of pedicle clamping in patients with limited bleeding, jaundice, and patients undergoing simultaneous bowel anastomosis.

Van der Bilt et al.[27] in a murine model demonstrated that ischemia/reperfusion was associated with an increased long-term risk of recurrence of colorectal hepatic metastasis in the hepatic remnant. They followed this up by demonstrating that perinecrotic hypoxia was possibly linked to this phenomenon. [28]

In 2006, Capussotti et al. [29] citing adverse effects of hepatic pedicle clamping on liver regeneration performed a randomized controlled trial comparing intermittent pedicle clamping versus no clamping and found that liver resections could be performed safely even in patients with diseased livers without clamping the pedicle.

Recently, Esaki et al. [30] reported their results following a randomized controlled trial comparing intermittent pedicle occlusion (IPO) for 15 min with 5 min of reperfusion versus 30 min with 5 min of reperfusion. They found that extending the IPO time to 30 min not only helped achieve a greater resection area per unit time, but was also associated with no significant difference in the bilirubin ratio compared to 15-min occlusions. This ultimately led to an improved preservation of the remnant liver function. This is the only randomized controlled trial till date. till such time as more evidence is available on the benefits and adverse effects of hepatic pedicle clamping, hepatic surgeons would be better served by performing the technique they are familiar with bearing in mind the data available at the current time which does seem to imply that safe hepatic resections can be performed without the need to clamp the hepatic pedicle. However, should the need arise for pedicle clamping, the data obtained from the study by Esaki et al. [30] would suggest that an IPO of 30 min would be adequate.

Liver parenchyma transection

Liver parenchymal transection has been performed by numerous techniques over the last century. Early methods used included the division of the liver by blunt instruments including the finger, [31] the blunt end of the haemostat [32] or the scalpel, [33] and the finger fracture technique popularized by Lin et al. [34] Newer modalities for transecting the liver include an ultrasonic dissector (CUSA) using ultrasonic energy, the hydrojet using a pressurized water jet, and a dissecting sealer (Tissue Link) using radiofrequency energy.

Weber et al. [35] demonstrated the safety and efficacy of heat coagulative necrosis using radiofrequency energy for segmental and wedge resections of the liver. Their technique involved sequential insertion of radiofrequency needles around the tumor creating a necrotic rim of tissue around the tumor that could be transected in a bloodless manner.

[Table 2] shows the results of the various randomized studies comparing some of the recently introduced techniques of liver parenchymal transection with the older techniques. Interestingly, in the randomized trial by Lesurtel et al., [10] the clamp crushing technique was found to be the most efficient compared to CUSA, hydrojet, and dissecting sealer in terms of resection time, blood loss, blood transfusion frequency, and cost efficiency.

 > Expanding the Horizons of Liver Resection Top

Traditionally, a curative resection has been defined in terms of segmental anatomy (anatomical resections) and the margin of resection. An adequate margin is defined as "a complete removal of tumor tissue plus a clear resection margin ≥ 1 cm on pathological examination" in which negative findings by angiography are followed by Lipiodol CT and ultrasound 1 or 2 months after resection. [40] However, the expansion in the indications for surgery for liver tumors to include large tumors requiring major resections with often an inadequate quantity of remnant liver to sustain hepatic function, as well as the undertaking of resections on cirrhotic and diseased livers has led to the questioning of such previously held beliefs as well as the introduction of newer modalities to reduce the size of the tumor or improve the size of the remnant liver parenchyma.

Anatomical versus nonanatomical resections

The basis for the performance of an anatomical resection for liver tumors has centered on the nature of spread of hepatocellular carcinomas. Hepatocellular carcinomas have been shown to invade the portal venous branches and then spread from there [41] as satellite nodules or as distant metastasis. It was thus recommended to divide the portal pedicles prior to hepatic dissection in segmentetomies and lobectomies to prevent tumor cell dissemination. [42] However, there have been numerous studies that have failed to show a benefit in terms of overall survival of an anatomical over a nonanatomical resection for hepatocellular carcinomas. These studies, seen in [Table 3], assume significance when we consider the possibility of offering a curative resection to patients without compromising their postoperative liver function. It also provides support to centers capable of performing major liver resections but who do not have a liver transplant unit to back them.

Numerous groups have continued to demonstrate significant survival advantages in the performance of anatomical resections over nonanatomical resections [49],[50],[51] even in cirrhotic patients. The advantage of anatomical resections for hepatocellular carcinoma thus cannot be downplayed.

The Barcelona Clinic Liver Cancer (BCLC) staging system [52] divides liver cancers into four groups, namely, early, intermediate, advanced, and terminal. However, according to the outcomes considering each treatment option available and outcomes, the BCLC has recommended that surgical resection should be reserved for patients with tumors ≤ 3cm and with a good liver function. For more than three tumors or tumors >3 cm, they recommend other alternatives including liver transplantation or local ablative therapies.

Given the conflicting nature of reported data on survival following different types of resections, it is prudent to consider that while anatomical resections can be performed even in cirrhotic patients, the decision to perform an anatomical resection should take into consideration the size of the remnant liver and the presence of cirrhosis. The choice of performance of resections should thus be individualized. [53] Nonanatomical resections and/or local ablative therapies should be considered as options in patients with cirrhosis and in patients in whom the remnant liver following an anatomical resection may not be compatible with an adequate postoperative liver function. The aim should thus be to achieve a curative resection without compromising the postoperative liver function.

 > Extending the Boundaries of Liver Resection with Portal Vein Embolization and Radiofrequency Ablation Top

Portal vein embolization

Kinoshita et al. [54] and Makuuchi et al.[55] were amongst the first to propose the benefit of portal vein embolization (PVE) of the lobe of the liver bearing the tumor with an aim of inducing a compensatory hypertrophy in the contralateral lobe. Since then, there have been numerous studies validating the safety and efficacy of this procedure. [56],[57],[58],[59],[60] The indication for the performance of PVE is based on the size of the future liver remnant (FLR) in relation to the total volume of the liver. The cut-off varies between institutes but usually includes an FLR of 25-40% of the total liver volume. The benefit of the performance of PVE in patients with a normal preoperative liver function has been questioned based on the findings of Farges et al.[61] They found no benefit of PVE in such patients but did confirm the benefit of PVE in patients with chronic liver disease.

Radiofrequency ablation

Radiofrequency ablation (RFA), which induces cell death by coagulation necrosis using radiofrequency energy, was first described by Rossi et al. [62] Since then, numerous trials have demonstrated the efficacy of RFA as a percutaneous ablative therapy in patients who are not good surgical candidates. [63],[64],[65],[66],[67] The success of these initial trials led to an exploration of the role of RFA as a curative agent in patients amenable to surgical resection as well. [68],[69] In 2006, Chen et al. [70] performed a randomized controlled trial comparing RFA versus surgery for hepatocellular carcinomas < 5 cm and demonstrated equivalent short- and long-term outcomes (including 5-year survival rates). Livraghi et al. [71] reported a 97.2% complete response rate at a median follow-up of 31 months in 218 patients undergoing RFA for lesions ≤2 cm. However, it is important to recognize that patients treated by RFA, as with patients undergoing surgical resections, need to undergo a strict surveillance postprocedure as intra- and extra-hepatic recurrences have been reported following treatment. [71] Instead of considering RFA as an alternative to surgery, there are now studies analyzing the outcomes following combining RFA with surgery in unresectable (multifocal or bilobar) tumors. In such patients, in whom a surgical resection would be precluded by an insufficient remnant liver, a limited hepatectomy with RFA of the remaining lesions can now be performed. The benefit of such combinations has been tested by numerous authors who have reported the safety and effectivity of this combination in colorectal cancer metastasis to the liver, as well. [72],[73],[74]

Margin of resection

The concept of an ideal margin of resection for malignant liver tumors has been traditionally regarded as 1 cm. [40] Wakai et al. [75] confirmed that colorectal metastasis to the liver should be resected with a 1 cm margin (based on the distribution of intrahepatic micrometastasis) and Shi et al. [76] concluded that a 2-cm margin is necessary while resecting hepatocellular carcinomas. However, other studies evaluating the influence of the surgical resection margin in patients with hepatocellular carcinomas, hepatoblastomas, and colorectal metastasis to the liver seem to indicate that more than the size, it is the presence of a negative margin that is a principal indicator of long-term survival. [77],[78],[79],[80],[81],[82],[83],[84],[85] This assumes significance when major resections are undertaken wherein the question of the function of the remnant liver is of prime concern. In all other cases where standard resections are being undertaken, it seems prudent at this time to obtain an adequate surgical resection margin of around a centimeter.

 > Laparoscopic Liver Resection Top

The last two decades have witnessed an increase in the number of liver resections attempted laparoscopically following the first reported case in 1996. [86] The development of laparoscopic ultrasonography [87],[88] and radiofrequency ablation (lap RFA)[89] has further helped in the assessment of lesions in terms of intraoperative staging and also to decide on the margins of resection. Laparoscopy is a useful tool in the staging of liver tumors. The feasibility of performance of laparoscopic resections for small lesions located in the left lateral and right anterior segments has been shown [90],[91] and even confirmed in a meta-analysis comprising only nonrandomized studies. [92] Recently, Cho et al. [93] have demonstrated the feasibility of using laparoscopy for small resections even in posteriorly located lesions. However, most of these studies have involved the resection of benign tumors or colorectal metastases to the liver and even more uncommonly, hepatocellular carcinomas. Thus, it is important to exert caution when interpreting and extrapolating the results of these data as representative of all liver resections. Moreover, the safety and the long-term outcomes need to be confirmed even for these lesions. This especially assumes significance when hepatocellular carcinomas arise in the setting of cirrhosis. Data from randomized controlled trials are awaited.

 > Conclusion Top

Surgery continues to remain an important modality of treatment of malignant hepatic neoplasms amenable to resection. Advancements in imaging modalities coupled with the development of complimentary modalities like thermal ablative therapies and interventional radiology (e.g., PVE) will provide hepatic surgeons more options when dealing with such tumors. While laparoscopy does provide useful adjuvant options including staging (using ultrasonography) and performance of RFA, its benefit in resection of malignant neoplasms of the liver has yet to be completely understood.

 > References Top

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  [Table 1], [Table 2], [Table 3]

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