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170
However, if the patient has a compromised liver, then the liver volume does not
truly refl ect liver function [ 20 ]. CT volumetry is used for preoperative calculations
of the volume of resected livers, but does not demonstrate the effects of diseased
liver parenchyma on liver function. The evaluation of liver function before liver
surgery is dependent on the combination of the results of CT volumetry with those
of other liver function tests.
Transient Elastography
Recently, noninvasive measurements to assess the degree of liver fi brosis and cirrhosis
before operation, like transient elastography, acoustic radiation force impulse imaging
and magnetic resonance elastography, have been developed. The clinical studies are
ongoing to validate the strength and the power of these novel approaches [ 21 ].
Transient elastography (TE) measured by FibroScan is a rapid, non-invasive, and
reproducible method for measuring liver stiffness that is increasingly explored to
assess liver fi brosis. It measures the velocity of a low-frequency (50 Hz) elastic
shear wave propagating through the liver. This velocity is directly related to tissue
stiffness, called the elastic modulus. The stiffer the tissue, the faster the shear wave
propagates. TE measures liver stiffness in a volume that approximates a cylinder
that is 1-cm wide and 4-cm long, 25–65 mm below skin surface. The results are
expressed in kilopascals (kPa) and range from 2.5 to 75 kPa; a normal value is
around 5 kPa [ 22 ].
Several advantages of TE have been reported, such as low invasiveness, a short
procedure time (5 min), fast acquisition of results, and portability that enables testing at the bedside and in outpatient departments [ 50 ]. Although unreliable and unre-
peatable measurements caused by host obesity, anatomical diffi culties such as a
narrow intercostal space, and inadequate operator experience have also been
reported, the overall diagnostic accuracy for advanced liver fi brosis and early cirrhosis is up to 90 % in various liver diseases including chronic viral hepatitis and
nonalcoholic fatty disease [ 23 ].
To evaluate the effi cacy of preoperative assessment of liver fi brosis and cirrhosis
using TE in predicting post- hepatectomy outcomes , several clinical studies has been
carried out. In a prospective cohort [ 24 ], 90 patients undergoing hepatectomy for
HCC were prospectively evaluated with FibroScan. Postoperative liver failure
(PLF) occurred in 28.9 % of patients and receiver operating curves (ROC) analysis
identifi ed patients with liver stiffness value higher than or equal to 15.7 kPa as being
at higher risk of PLF, while patients with liver stiffness value lower than 14.8 kPa
had no PLF. Multivariate analysis showed that along with low preoperative serum
sodium levels (P = 0.012), histological cirrhosis (P = 0.024), elevated liver stiffness
(P = 0.005) was an independent predictors of PLF. In a larger prospective cohort
[ 25 ], 105 with a mean age of 59 years were included with both ICG retention rate at
15 min and TE were prospectively carried out. Using the calculated cutoff at 12.0
kPa, liver stiffness measurement was shown to have sensitivity of 85.7 % and speci-
Y. Mao and S. Du
171
fi city of 71.8 % in the prediction of major postoperative complications. On ROC,
only liver stiffness measurement but not ICG showed signifi cant correlation with
major postoperative complications.
The Indocyanine Green (ICG) Clearance Test
ICG is a highly protein-bound, water-soluble, tricarbocyanine dye that bounds in
plasma to albumin and β-lipoproteins and distributes uniformly in the blood within
a few minutes after injection. It is selectively taken up by hepatocytes with a plasma
extraction of 70–90 % and is excreted unchanged in the bile via a carrier-mediated
mechanism. Therefore, it refl ects several liver functions, including the blood fl owdependent clearance and transporter functions [ 26 ]. The standard procedure involves
a bolus injection of 0.5 mg/kg of ICG following an overnight fast, and blood samples are collected at 5-min intervals for 20 min. ICG concentrations are measured
using a spectrophotometer. The ICG clearance test can also be automatically calculated under a dye densito-graph (DDG) analyzer using an optical sensor placed on
the fi nger pulse [ 27 ]. The machine expands the application of ICG clearance test in
current clinical situation.
The results of ICG clearance test can be expressed in several ways, including the
plasma disappearance rate (ICG-PDR), the ICG elimination rate constant (ICG- k )
and the ICGR 15 which describes the percentage of circulatory retention of indocyanine green during the fi rst 15 min after bolus injection [ 28 ]. In order to prospec-
tively determine the effi cacy of ICG-PDR in the clinical course, 95 patients
undergoing liver resection were included in a cohort [ 29 ], with ICG-PDR, bilirubin
and prothrombin time selected and prospectively measured. After hepatectomy , 3
patients died due to liver failure and 21 patients developed signs of liver dysfunction. ROC analysis revealed that ICG-PDR did signifi cantly better indicate
postoperative liver dysfunctions. Of date, pulse spectrophotometry was developed
to noninvasively measure the ICG- k and a prospective clinical study was done [ 30 ].
Seventy fi ve patients who underwent anatomical liver resection for hepatocellular
carcinoma were enrolled and ICG- k was measured instantaneously using pulse
spectrophotometry before surgery , during infl ow occlusion and after hepatectomy.
Eight patients suffered liver failure with one died in hospital. In a logistic regression
model, the estimated remnant ICG- k was a signifi cant predictor of postoperative
liver failure and real-time monitoring of ICG- k was shown to be helpful for evaluat-
ing the remnant liver functional reserve before, during and after hepatectomy.
ICGR 15 , as the most commonly determined value, has been extensively investigated in various kinds of clinical setting and incorporated into a number of test
combinations or score systems. A decision tree for deciding the safe limit of hepatectomy was developed [ 31 ] basing on three variables: whether ascites is present,
the serum total bilirubin level, and the ICGR 15 . With strict application of this decision tree to 1,429 consecutive hepatectomy in 10 years, only one patient death was
encountered. So ICGR
15
> 15 % is a high risk factor for serious post-hepatectomy
14 What Is the Best Way to Assess Hepatic Reserve Prior to Liver Resection…
172
complications [ 32 ], although a cutoff of 14 % has been suggested by Lau et al. [ 33 ].
ICGR 15 , along with TE, was performed preoperatively in 44 patients with hepatocellular carcinoma [ 34 ]. ICGR 15 was found to correlate well with preoperative factors and postoperative outcome (peak AST level). A classifi cation system for liver
function using ICGR 15 and the ratio of uptake by the liver to that by the liver and
heart at 15 min (LHL15) in
99m
Tc-galactosyl human serum albumin scintigraphy for
hepatic resection , was created [ 35 ]. A total of 548 consecutive patients who under-
went hepatectomy were enrolled in a prospective study to validate the ranking system and the result confi rmed the usefulness of this system in predicting the safety of
hepatic resection .
99m
Tc-Galactosyl Serum Albumin Scintigraphy
Molecular nuclear imaging techniques have developed these years. Some new
agents, such as
99m
Tc- galactosyl serum albumin scintigraphy (GSA) and
99m
Tcmebrofenin hepatobiliary scintigraphy, can measure both total and future remnant
liver function and potentially identify patients at risk for postresectional liver
failure .
GSA is an analogue of asialoglycoprotein, which binds to asialoglycoprotein
receptors (ASGPR) on hepatocyte membranes, followed by receptor-mediated
endocytosis. ASGPR density is closely related to hepatocyte function [ 36 , 37 ]. The
level of expression of receptor is signifi cantly related to liver function and lower in
diseased livers such as chronic hepatitis, cirrhosis and HCC [ 3 ]. Radio labeled
ASGPR was developed originally by Vera et al. [ 38 ].
99m
Tc-GSA is very stable and
only distributes in the blood and liver after intravenous injection [ 36 ]. The liver is
the only uptake site for
99m
Tc-GSA, making
99m
Tc-GSA an ideal agent for predicting
hepatocyte mass and function by monitoring the functional status and distribution
of ASGPR [ 39 , 40 ].
After liver uptake,
99m
Tc-GSA remains trapped in the liver for at least 30 min, and
there is practically no biliary excretion. Thus, SPECT can assess both liver function
and functional volume at the same time [ 41 ]. The
99m
Tc-GSA liver uptake ratio
(LHL15) and blood clearance ratio (HH15) are quantitative indices frequently used in
planar dynamic
99m
Tc-GSA scintigraphy. LHL15 defi ned as 15 min after bullet injec-
tion of
99m
Tc-GSA and calculated by dividing the radioactivity in regions of interest
(ROIs) of the liver by the radioactivity in the liver and heart, it represents the number
of hepatocytes. HH15 is calculated by dividing the radioactivity in ROIs of the heart
15 min by the radioactivity 3 min after injection of
99m
Tc-GSA, it represents the rate
of blood clearance [ 42 ]. Harada and his colleagues recently developed a simple soft-
ware program to automatically calculate the pixel counts of the area between the
hepatic curve and heart curve from 3 to 15 min [ 43 ]. Both LHL15 and HH15 refl ect
the liver function and the severity of liver disease [ 44 ]. For LHL15 and HH 15 mea-
sures preoperative total liver function, not the function of the remnant liver, postoperative liver failure has been observed in patients with normal LHL15 values [
45 ].
Y. Mao and S. Du
173
LHL15 and HH15 are readily calculated from the radioactivity in the heart and
liver ROIs, it may not refl ect the actual liver function. So some complex and perfect
compartmental models of
99m
Tc-GSA kinetics are developed for the assessment of
liver function ([ 46 ] #174, [ 47 ] #30, [ 48 ] #149).
Many different parameters can be calculated from different kinetic models for
the quantitative evaluation of liver function. The liver blood fl ow and maximal
asialoglycoprotein receptor binding rate assessed by
99m
Tc-GSA are signifi cantly
correlated with other quantitative measures of liver function [ 48 ]. Total ASGPR
amount are proportional to the number of viable hepatocytes and the correlation of
total ASGPR amount with hepatocyte number was signifi cantly higher than the correlation of ICG-k with total hepatocyte number [ 53 ].
Kwon etc. reported previously that the maximal removal rate of GSA(GSARmax) values correlated well with the results from the transferrin, prealbumin, retinol binding protein, fi brinogen, prothrombin time, hepaplastin test, antithrombin
III, and ICG tests [ 49 ]. In another retrospective study [ 50 ], this team reviewed 178
patients for elective hepatectomy . Preoperative estimation of the GSA-Rmax in the
predicted remnant liver (GSA-RL) is used a parameter. In this study, seven patients
postoperative hyperbilirubinemia were recorded with GSA-RL <0.15 mg/min. Two
patients died of postoperative liver failure 1–2 months after surgery , the GSA-RL
values were 0.078 and 0.090, respectively. They considered a margin of safety
(0.05) and determined 0.15 as the cutoff value. Preoperative percutaneous transhepatic portal embolization should be performed for cases with a GSA-RL less than
0.15 to avoid postoperative hyperbilirubinemia or hepatic failure.
In another study, this team [ 51 ] followed 191 patients more than 1 year after
hepatectomy with 16 patients suffered from liver failure and 3 of them died. Total 35
clinicopathologic factors were performed to identify independent predictors of postoperative liver failure after resection of HCC by univariate and multivariate analyses. In univariate analyse, elder, a lower serum albumin level, lower cholinesterase
level, longer prothrombin time, lower platelet count, and lower GSA-Rmax, higher
values of ICGR15, total bilirubin, AST, type IV collagen 7S, hyaluronate (HA),
AFP, type IV collagen 7S/GSA-Rmax ratio, and HA/GSA-Rmax ratio, are the factors easy to the postoperative liver failure. Patients in the liver failure group had
signifi cantly more intraoperative blood loss and a longer postoperative hospital stay.
Multivariate logistic regression analysis showed that HA/GSA-Rmax ratio 500 mg
min/dl (OR 23.60; 95 % confi dence interval (CI) 1.91–62.09; P = 0.0138) was the
only independent predictor of postoperative liver failure. An increase of the HA/
GSA-Rmax ratio was associated with more severe liver dysfunction. The HA/GSARmax ratio was also positively correlated with various conventional liver function
tests, such as the ICGR 15 , AST, total bilirubin, platelet count, albumin, cholinesterase, prothrombin time, type IV collagen 7S, HA and GSA-Rmax, etc. They conclude that the HA/GSA-Rmax ratio can predict postoperative liver failure, and a
ratio 500 mg min/dl is a relative contraindication to liver resection with a sensitivity of 88 % and a specifi city of 92 %, and its negative predictive rate was 99 %.
Recently, Mao and Du [
52 , 53 ] set up a computerized image system based on a
two-compartment model, which could provide liver images, a freehand drawing
14 What Is the Best Way to Assess Hepatic Reserve Prior to Liver Resection…
174
tool for hepatectomy simulation, assess liver function and predict postoperative
remnant liver function, using uptake index (UI) as a parameter. That study [ 54 ]
recruited 71 pre-hepatectomy patients and 71 healthy volunteers. They found that
median UI = 2.81 was the normal reference, lower UI values were associated with
the more impaired liver functions. ROC analysis indicated that lower UI values
could be used to predict the presence of ascites with high accuracy (AUC = 0.88,
P < 0.0001). Preoperative UI values were also able to distinguish patients with and
without elevated bilirubin (AUC = 0.86, P < 0.0001). Preoperative UI was also negatively associated with ICGR 15 values, i.e., the lower UI value was, the larger ICGR 15
value would be(r = −0.92, P < 0.0001).
In this system, for each simulated liver resection plan, the corresponding anatomic and functional remnant liver volume, and the risk of postoperative liver failure were presented. There 33 patients had both preoperative and postoperative
measures of UI values for the remnant liver via the system. Regression analysis
using predicted UI as an explanatory variable showed a linear equation as: Post
Surgery UI = −0.09 + 1.04(Predicted UI). It supported the accuracy of the preoperative prediction. To further evaluate the reliability of predicted UI values for the
future remnant liver (FRL), predicted UIs were further compared with the parameters of the actual post operative liver functions tests. The results demonstrated that
predicted UI negatively correlated with PT and total bilirubin level (Pearson’s correlation coeffi cient r = −0.67 and −0.68 respectively, P < 0.0001). The AUC for predicted UI to distinguish patients with and without postoperative ascites was at 0.85,
P < 0.0001. While Child score of 9 or larger was defi ned as high risk of liver failure,
the ROC analysis results indicated that UI values had a high accuracy in predicting
the risk of liver failure (AUC = 0.95, P < 0.0001). The threshold for very high risk
was defi ned as P = 0.05 which corresponds to UI of 0.73 (FLVI = 26 %). In fact,
there are some weak points in this study. Without Child C patients enrolled in the
study might lead to conservative decision making rule. The small sample size also
might affect the accuracy of the threshold to defi ne the high risk region. Further
improving the accuracy and validating the system in phase III clinical trial is needed
before bring it to clinical practice.
Recommendations Based on the Data
The clinical methods to evaluate liver function including serological tests, various
evaluation scoring systems, ICG clearance, 3D- CT volumetric calculation are all
useful in clinical practice. They all have advantages and disadvantages, and cannot
be replaced, currently.
The preoperative liver function evaluation must be a comprehensive process. In
order to make a safe and thorough evaluation, multiple indices, as well as general
condition of the patient, type of planned surgery, and profi ciency of surgeons should
be considered and combined. The maturation and application of new GSA based
three-dimension imaging system may bring a new promising tool for the preoperative liver function evaluation.
Y. Mao and S. Du
175
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14 What Is the Best Way to Assess Hepatic Reserve Prior to Liver Resection…
179© Springer International Publishing Switzerland 2016
J.M. Millis, J.B. Matthews (eds.), Diffi cult Decisions in Hepatobiliary
and Pancreatic Surgery, Diffi cult Decisions in Surgery: An Evidence-Based
Approach, DOI 10.1007/978-3-319-27365-5_15
Chapter 15
Treatment Protocols for Small Hepatocellular
Carcinoma (3 cm): RFA or Resection?
Yudong Qiu and Yilei Mao
Abstract Treatment selection for small hepatocellular carcinoma remains contro-
versial. Although there are various studies showed different prognostic results in
patients with small HCC by resection compared with RFA or LT, some other important factors, not only the tumor size, which may correlate with prognosis are still
lack especially for gross classifi cation. The identifi cation of gross classifi cation is
crucial for the discrimination of small HCC and may play a great role for the fi nal
decision. Our results showed that not all the patients with small HCC are applicable
for RFA treatment, so as to say, resection may be more benefi cial for patients with
the nonboundary type of small HCC.
Keywords Small hepatocellular carcinoma • RFA • Hepatic resection • Gross
classifi cation
Introduction
Hepatocellular carcinoma ( HCC ) is a major health problem worldwide and a prevalent tumor type in mainland China [ 1 ]. Progresses in diagnostic imaging have
allowed detection of HCC at an early stage which can be curable by multiple treatment protocols. According to BCLC staging system, patients with very early or
early-stage HCC should be considered for resection , ablation or transplantation [ 2 ,
3 ]. Also, the use of Milan Criteria to select patients for liver transplant ation (LT)
leads to good results for a solitary HCC up to 5 cm or for multiple HCC up to 3 in
number and up to 3 cm for each tumor [ 4 , 5 ]. In 2014, a new staging system called
Y. Qiu
Department of Hepatobiliary and Pancreas Surgery , Drum Tower Hospital, Medical School of
Nanjing University , Nanjing , China
Y. Mao (
*)
Department of Liver Surgery , Peking Union Medical College Hospital, Peking Union Medical
College & Chinese Academy of Medical Sciences ,
1# Shuai-Fu-Yuan, Wang-Fu-Jing , Beijing 100730 , China
e-mail:
yileimao@126.com; pumch-liver@hotmail.com
180
HKLC system was erected which may be more applicable to Asian patients
(Fig. 15.1 ). For the HCC patients with stage I and IIa, resection, transplantation and
ablation are all recommended [ 6 ]. Hence, three various therapies including resec-
tion, transplantation and ablation have been adopted in patients with small HCC
although these three approaches have respective distinct indications which are not
mentioned in the current staging systems.
Strategy Discussion
Hepatitis B is endemic in China and this results in a heavy burden of hepatocellular
carcinoma ( HCC ) because hepatitis B virus is a major risk factor in the development
of the disease [ 7 , 8 ]. Most HCC patients with chronic infection with HCV have
remarkable cirrhosis with impaired liver function, whereas patients with HBVrelated HCC in general have better preserved liver function. Individuals would be
considered for liver transplant ation (LT) if they were with poor liver function reserve
and especially small HCC within Milan Criteria (solitary tumour 5 cm and up to
three nodules 3 cm) [ 9 ]. Nevertheless, this treatment which gives the potential to
both resect the entire potentially tumor-bearing liver and eliminate the cirrhosis can
be offered only to a minority of patients because of the shortage of donors and high
Fig. 15.1 The HKLC prognostic classifi cation scheme. EVM extrahepatic vascular invasion/
metastasis. Early tumor: 5 cm, 3 tumor nodules and no intrahepatic venous invasion; Intermediate
tumor: (1) 5 cm, either >3 tumor nodules or with intrahepatic venous invasion, or (2) >5 cm, 3
tumor nodules and no intrahepatic venous invasion; and Locally-advanced tumor: (1) 5 cm, >3
tumor nodules and with intrahepatic venous invasion, or (2) >5 cm, >3 tumor nodules or/and with
intrahepatic venous invasion, or (3) diffuse tumor
Y. Qiu and Y. Mao