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Chapter 5
Figure5.9 • CT of patient with a primary hepatic lymphoma of the left liver. Note that the lesion appears as hypodense
lesion.
Key points
• Epidemiological studies indicate that both incidence and mortality of HCC are increasing worldwide,
but have stabilised in some Western countries.
• Development of HCC is linked to the presence of an underlying liver disease. Major risk factors for
HCC include viral infection, alcohol ingestion and metabolic syndrome.
• Surveillance of cirrhotic patients and at-risk populations is recommended to detect HCC at an early
stage provided treatment is feasible.
• US is recommended as a screening tool, while CT and MRI are useful to confirm the diagnosis. Liver
biopsy is recommended in selected cases.
• Patients with HCC should be managed in multidisciplinary settings including hepatologists, liver
surgeons, liver transplant teams, oncologists, pathologists and interventional radiologists.
• The level of evidence for most treatment options for HCC is limited to cohort investigations with few
randomised controlled trials, most of which deal with treatment of advanced disease.
• Five treatments are available on the basis of evidence-based data: transplantation, resection,
radiofrequency ablation, chemoembolisation and sorafenib.
• Liver transplantation is the treatment of choice in cirrhotic patients with limited tumour involvement,
as it removes both tumour and the preneoplastic liver.
• Liver resection is the treatment of choice in patients with normal liver parenchyma and is indicated in
cirrhotic patients with preserved liver function and no clinically significant portal hypertension.
• Percutaneous treatments are effective in patients with small tumours.
• Transarterial chemoembolisation and radioembolisation are effective in selected non-surgical patients
with preserved liver function.
• Sorafenib is effective in selected palliative patients who still have preserved liver function.
102
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Primary malignant tumours of the liver
Key references
1. FerlayJ, SoerjomataramI, Dikshit R, etal. Cancer
incidence and mortality worldwide: sources, methods
and major patterns in GLOBOCAN 2012. Int J
Cancer 2014;136(5):E359–86. PMID: 25220842.
3. PoordadF, Hezode C, Trinh R, et al. ABT-450/rombitasvir and dasabuvir with ribavirin for hepatitis
C with cirrhosis. N Engl J Med 2014;370(21):1973–
82. PMID: 24725237.
4. BelliLS, BerenguerM, CortesiPA, etal. Delisting of
liver transplant candidates with chronic hepatitis C
after viral eradication: a European study. J Hepatol
2016;65(3):524–31. PMID: 27212241.
9. Rinella ME. Nonalcoholic fatty liver disease: a
systematic review. JAMA 2015;313(22):2263–73.
PMID: 26057287.
13. Siegel AB, Zhu AX. Metabolic syndrome and
hepatocellular carcinoma: two growing epidemics
with a potential link. Cancer 2009;115(24):5651–
61. PMID: 19834957.
14. Cauchy F, Zalinski S, Dokmak S, et al. Surgical
treatment of hepatocellular carcinoma associated with
the metabolic syndrome. Br J Surg 2012;100(1):113–
21. PMID: 23147992.
15. ViganoL, ConciS, CesconM, etal. Liver resection
for hepatocellular carcinoma in patients with
metabolic syndrome: a multicenter matched analysis
with HCV-related HCC. J Hepatol 2015;63(1):93–
101. PMID: 25646890.
16. Wong RJ, Cheung R, Ahmed A. Nonalcoholic
steatohepatitis is the most rapidly growing indication
for liver transplantation in patients with hepatocellular
carcinoma in the U.S. Hepatology 2014;59(6):
2188–95. PMID: 24375711.
22. LaurentA, DokmakS, Nault JC, et al. European
experience of 573 liver resections for hepatocellular
adenoma: a cross-sectional study by the AFCHCA-2013 study group. HPB (Oxford) 2016;
18(9):748–55. PMID: 27593592.
42. Berzigotti A, Reig M, Abraldes JG, et al. Portal
hypertension and the outcome of surgery for
hepatocellular carcinoma in compensated cirrhosis:
a systematic review and meta-analysis. Hepatology
2014;61(2):526–36. PMID: 25212123.
60. LlovetJM, BruixJ. Systematic review of randomized
trials for unresectable hepatocellular carcinoma:
Chemoembolization improves survival. Hepatology
2003;37(2):429–42. PMID: 12540794.
This meta-analysis of randomised controlled
trials (RCTs) demonstrates that TACE should be
recommended as first-line non-curative option for
intermediate HCC (as defined by the BCLC staging
system) as it improved survival.
61. Yin L, Li H, LiAJ, etal. Partial hepatectomy vs.
transcatheter arterial chemoembolization for resectable multiple hepatocellular carcinoma beyond
Milan criteria: a RCT. J Hepatol 2014;61(1):
82–8. PMID: 24650695.
This is the first RCT to demonstrate an improved survival
benefit of resection in patients with multiple HCC.
62. LiuH, WangZG, FuSY, etal. Randomized clinical
trial of chemoembolization plus radiofrequency
ablation versus partial hepatectomy for
hepatocellular carcinoma within the Milan criteria.
Br J Surg 2016;103(4):348–56. PMID: 26780107.
This RCT demonstrates an improved survival benefit
of resection in patients with HCC within Milan criteria.
63. Lopez PM, Villanueva A, Llovet JM. Systematic
review: evidence-based management of
hepatocellular carcinoma –an updated analysis of
randomized controlled trials. Aliment Pharmacol
Ther 2006;23(11):1535–47. PMID: 16696801.
This meta-analysis of four RCTs shows the efficacy of
radiofrequency ablation (RFA) in terms of better local
control in patients with HCC >
percutanenous ethanol injection (PEI).
2 cm, as compared to
64. ChoYK, KimJK, KimMY, etal. Systematic review
of randomized trials for hepatocellular carcinoma
treated with percutaneous ablation therapies.
Hepatology 2009;49(2):453–9. PMID: 19065676.
This meta-analysis of four RCTs demonstrates that RFA
significantly improves survival for patients with HCC, as
compared to PEI.
74. LlovetJM, RicciS, MazzaferroV, etal. Sorafenib in
advanced hepatocellular carcinoma. N Engl J Med
2008;359(4):378–90. PMID: 18650514.
This RCT demonstrates an improved survival benefit
for sorafenib in patients with advanced HCC.
78. Vente MA, Wondergem M, van der Tweel I, etal.
Yttrium-90 microsphere radioembolization for the
treatment of liver malignancies: a structured metaanalysis. Eur Radiol 2009;19(4):951–9. PMID:
18989675.
88. Sapisochin G, Facciuto M, Rubbia-Brandt L, et al.
Liver transplantation for ‘very early’ intrahepatic
cholangiocarcinoma: international retrospective study
supporting a prospective assessment. Hepatology 2016;
64(4):1178–88. PMID: 27481548.
91. LaiQ, FeysE, KaramV, etal. Hepatic epithelioid
hemangio-endothelioma and adult liver transplantation: proposal for a prognostic score based
on the analysis of the Eltr-Elita Registry. Transplantation 2017;101:555–564. PMID: 27926594.
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103
6
6
Colorectal liver metastases
Amir A. Rahnemai-Azar
Mary E. Dillhoff
Carl Schmidt
Timothy M. Pawlik
Introduction
Despite recent advances in screening, diagnosis and
management, colorectal cancer (CRC) remains the
second leading cause of cancer death in Western
countries. In 2012, 1.4 million new CRC cases with
close to 694 000 deaths were estimated to have
occurred worldwide.1 Almost two-thirds of patients
with CRC develop distant metastases. The liver
is the most frequent site of metastases, with liver
disease being detected either at the time of CRC
diagnosis (synchronous; 20–25%) or subsequently
(metachronous; 40%). The extent of liver disease is a
key determinant of survival in patients with isolated
colorectal liver metastases (CRLM).
While the median survival of patients with
advanced CRLM has improved over the last several
decades with the introduction of more efficacious
chemotherapy, surgical resection remains the
cornerstone of potentially curative therapy.
2
2–4
Diagnosis
The diagnosis of CRLM is usually based on imaging
during evaluation of patients with CRC. Rarely,
depending on clinical presentation, percutaneous
fine-needle aspiration (FNA) biopsy may be used
to confirm the diagnosis. While the risk of tract
seeding following FNA biopsy for CRLM is low,
typically there is no need for biopsy.
5–7
Most often
well as laboratory tests (e.g. CEA [carcinoembryonic
antigen] level) and characteristic imaging of the lesion
are adequate to substantiate a diagnosis of CRLM.
Imaging is important to stage adequately the extent
of disease, which in turn will help tailor subsequent
therapy. Multiple different imaging modalities can
be utilised to assess patients with CRLM (Table6.1).
Transabdominal ultrasonography (US) is a
relatively inexpensive test that can provide general
information about the number, location and extent
of liver metastases. The addition of duplex can
increase US sensitivity to define the proximity of
lesions to adjacent vital structures such as the portal
vein and inferior vena cava.
US is not a sensitive diagnostic test for CRLM
and can fail to identify over 50% of metastatic
8,9
lesions.
One of the major limitations is reliance on the skill
and knowledge of the operator. In addition, other
factors such as the patient’s body habitus, presence
of steatosis and the inability to detect extrahepatic
disease hampers the diagnostic yield and utility of US.
In contrast to transabdominal US, intraoperative US
(IOUS) has a much higher sensitivity to detect CRLM
through high-resolution imaging of the liver.
with the increasing use of magnetic resonance imaging
(MRI) and positron emission tomography–computed
8
However,
104
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Colorectal liver metastases
Table6.1 • Advantages and limitations of various imaging modalities in evaluating liver metastases
Modality Advantages Pitfalls
US Low cost High operator dependence
Availability Body habitus dependence
Low sensitivity in
Small lesions
Extrahepatic spread
IOUS Localisation of deep-seated lesion Increases duration of surgery
Mapping vasculature
Real-time guidance for surgical plane
Guiding RFA
CT Availability Poor confidence in
Relatively low cost
High sensitivity and specificity Lesion detection in chemotherapy-induced liver steatosis
Extrahepatic spread evaluation Distinction of malignant from benign
Vascular mapping Not suitable for
Liver volume estimation
Planning targeted therapies Compromised renal function
Therapy monitoring
MRI Increased sensitivity and specificity for Not suitable for patients with
Detection of small lesions (<1 cm) Claustrophobia
Detection of lesions after chemotherapy-
induced fatty changes
Lesion characterisation Non-compliance
Treatment planning
Therapy response monitoring
PET Accurate extrahepatic site detection Limited accessibility
Superior sensitivity and specificity when combined
with CT/CE-CT
Therapy response monitoring
Detection of residual or recurrent disease After chemotherapy
Reproduced from Sahani DV, Bajwa MA, Andrabi Y, etal. Current status of imaging and emerging techniques to evaluate liver
metastases from colorectal carcinoma. Ann Surg 2014;259(5):861–72.
Liver steatosis
Detecting < 1cm lesions
CM allergies
Implants (pacemaker, stents, etc.)
Impaired renal function (CE-MRI)
High cost
Poor detection of lesions
< 1 cm
tomography (PET-CT), detection of new unsuspected
lesions by IOUS has decreased.
10,11
Nonetheless, IOUS
does help identify new lesions in a subset of patients
and also enables surgeons to perform hepatectomy
more safely by providing real-time guidance of the
resection plane. In a series of 60 patients with liver
metastases, Leen etal. demonstrated that the addition
of contrast improved diagnostic accuracy of IOUS up
to 96%.
12
Other studies have noted that the diagnostic
yield of contrast-enhanced US in the detection of liver
metastases is comparable to contrasted-enhanced
13–15
MRI.
At most centres, triple-phase contrast multi-
detector computed tomography (MDCT) is the
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modality of choice for CRC staging and scree ning
for liver metastases. CRLM typically appear as
hypoattenuating lesions and are best iden tified in the
portal venous phase of scanning (Fig.6.1).16 Arterial
phase images are typically used to distinguish
metastatic disease from benign vascular lesions
and also to identify the liver vascular anatomy
for pre-surgical planning or if placement of a
hepatic arterial infusion pump is being considered
Fig. 6.2).
(
17
Additionally, extrahepatic metastases
may be detected by obtaining chest, abdomen and
pelvic images. The major disadvantage of CT is its
lower sensitivity in recognising small liver lesions
1 cm), especially in patients with background
(<
liver parenchymal disease, such as steatosis.
18,19
105
Chapter 6
a b
Figure6.1 • (a) Axial contrast-enhanced portal phase CT of the liver shows the presence of two metastases (thin
arrows); (b)
Legou F. etal. Diagn Interv Imaging. 2014 May;95(5):505-12. Copyright © 2014 Elsevier Masson SAS. All rights
reserved.
Figure6.2 • CT angiogram. A maximum intensity
projection rendered coronal 3-dimensional image
demonstrating a replaced right hepatic artery from
superior mesenteric artery in a patient scheduled for right
lobe resection for liver metastases from CRC.
Sahani DV. etal. Current status of imaging and
emerging techniques to evaluate liver metastases
from colorectal carcinoma. Ann Surg. 2014
May;259(5):861-72.
MRI provides high-resolution assessment of
the liver and can be superior to CT in detecting
and characterising indeterminate small lesions
(Figs6.1,
compared to 71–73% for CT.
accurate in differentiating benign and malignant
subcentimetre liver lesions, with a specificity of
97.5%, compared to 77.3% for MDCT.
notably, MRI tends to be more accurate in
detecting and characterising CRLM if there is
underlying liver parenchymal disease.
diffusion MRI (b = 100 s/mm2): discovery of an additional metastasis in segment 2 (arrowhead).
advances in MRI techniques, including the
introduction of tissue-specific contrast agents
such as gadobenate dimeglumine and gadoxetate
(Gd-EOB-DTPA; Primovist in Europe and Eovist
in the USA), as well as diffusion-weighted imaging
(DWI), have further enhanced diagnostic yield of
CRLM (
Figs6.4, 6.5).
24–26
Positron emission tomography (PET) is another
commonly used imaging modality. PET utilises
an intravenously administered radioactive tracer,
fluorodeoxyglucose (FDG), to identify metabolically
active metastatic lesions. The use of PET can
supplement CT. For example, Strasberg etal. showed
that in 43 patients with CRLM, laparotomy was
avoided in six patients based on FDG-PET findings
that initially were not detected on CT.
randomised control study of 150 patients with
CRLM noted that the number of futile laparotomies
was reduced from 45% to 28% by the addition
of preoperative FDG-PET.
28
In a meta-analysis,
FDG-PET was reported to have superior results in
preoperative staging of CRC compared with CT
alone, especially for detecting extrahepatic disease
(sensitivity and specificity of 91.5% and 95.4%
versus 60.9% and 91.1%, respectively).
to the National Comprehensive Cancer Network
(NCCN) guidelines, FDG-PET should be considered
8
6.3),
with sensitivity rates of 91–97%,
20,21
MRI is also more
in patients with CEA elevation and suspected disease
recurrence. The use of PET in CRC staging is limited
due to insufficient anatomic detail, poor sensitivity
for lesions smaller than 1 cm, and false-positive
22
More
results in the setting of inflammation (Fig. 6.6).
However, integration of FDG-PET imaging and CT
addresses some of these limitations, particularly
8,23
Recent
with regard to anatomic detail and it is particularly
useful in detecting extrahepatic disease (
27
Another
29
According
Fig.6.7).
30
106
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a b
Colorectal liver metastases
c d
e f
Figure6.3 • (a) Portal venous phase contrast-enhanced liver CT: necrotic mass, with fibrous enhancement centred
on segments 2–4 (thick arrow); (b) a second hypodense lesion on CT scan is visible in segment 7 (thin arrow); (c) MRI
shows peripheral enhancement of both lesions (arrows); (d) both lesions are hypermetabolic on PET-CT (arrows); (e)
discovery of an additional lesion on portal venous phase contrast enhanced MRI (circle); (f) this third lesion was not seen
on CT or PET-CT (circle).
Legou F. etal. Diagn Interv Imaging. 2014 May;95(5):505-12. Copyright © 2014 Elsevier Masson SAS. All rights reserved.
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107
Chapter 6
a
a
c
c
Figure6.4 • A 44-year-old man, with stage III colon cancer resected 1year previously and treated with chemotherapy.
Follow-up restaging CE-CT examination (a, b) showed reduced liver attenuation in comparison to spleen due to steatosis
and a possible lesion in the right lobe (arrow). Liver MRI was performed with hepatobiliary contrast agent Eovist to
evaluate for surgical resection. Ten-minute delayed hepatobiliary phase, T1-weighted fat saturation MR images (c, d)
demonstrate enhancing liver parenchyma and numerous non-enhancing, small metastases scattered within the right and
left lobe of liver (arrows).
Sahani DV. etal. Current status of imaging and emerging techniques to evaluate liver metastases from colorectal
carcinoma. Ann Surg. 2014 May;259(5):861-72.
Surgical resection
Patient selection
Surgical resection with negative microscopic
b
b
d
d
as determinants of the best outcome following
surgical resection for CRLM.
31
However, with
recent advances in multidisciplinary management
of CRLM patients, the relevance of many of these
factors has been challenged.
32–36
margins (R0 resection) offers patients with
CRLM the best chance for long-term survival. The
optimal selection of patients for hepatic resection
is evolving and in recent years the paradigm of
surgical resectability has shifted from surgeonbased technical issues to a patient-disease-focused
multidisciplinary approach.
In 1989, Steele et al. introduced several factors
including the number of metastatic lesions (≤3),
maximum lesion dimension (<
5 cm), timing of
metastases (metachronous), adequate free margin
1 cm), and absence of extrahepatic metastases
(>
According to the Americas HepatoPancreato-Biliary Association (AHPBA) most recent
expert consensus statement and also the NCCN
guidelines, CRLM is considered resectable as long
as the tumour can be removed completely (R0
resection), the predicted future liver remnant (FLR)
function is adequate to prevent postoperative liver
failure, extrahepatic sites of the disease are
controllable, and the primary tumour can be resected
37,38
for cure.
108
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aa bb
Colorectal liver metastases
cc dd
Figure6.5 • A 51-year-old man with CRLM being treated with chemotherapy. Follow-up CE-CT (a) and CE-MRI
(b) failed to demonstrate left lobe metastasis that is more obvious on DW-MRI (c) as a focal bright area in the left lobe
(arrow) with associated restricted diffusion on apparent diffusion coefficient image (d) (arrow).
Sahani DV. etal. Current status of imaging and emerging techniques to evaluate liver metastases from colorectal
carcinoma. Ann Surg. 2014 May;259(5):861-72.
Issues in management of CRLM
A patient with a normal underlying liver requires
at least a 20% FLR to prevent postoperative
Current practice for margin status
Several studies have demonstrated that resection
margin width is not a determinant of long-term
survival.
39,40
Achieving R0 resection, regardless of
liver failure. The percentage increases to 30% for
patients who have steatosis or steatohepatitis, often
after receiving preoperative chemotherapy, and to
40% in patients with underlying cirrhosis.
42
its width, is enough to define the resectability of a
metastatic tumour.
Role of the FLR in resection of CRLM
The focus of current liver surgery practice is on
preserving adequate liver remnant function to
prevent post-resection liver failure, rather than the
Patients who do not meet FLR requirements
may benet from additional preoperative procedures
to induce hypertrophy of the FLR, such as portal vein
embolisation (PVE) or associating liver partition and
portal vein ligation for staged hepatectomy
(ALPPS).
43–46
volume of disease. Previously, the anticipated ability
to preserve a minimum of two contiguous segments
of hepatic parenchyma with adequate vascular inflow
and outflow, and adequate biliary drainage was
sufficient to consider a hepatic resection.
41
However,
recent advances in accurate prediction of FLR
volume and function have optimised the selection of
patients with CRLM for surgery (
Fig.6.8).
Extrahepatic metastatic disease and role
of surgery
The lungs, intra-abdominal lymph nodes (LNs)
and peritoneum are the most common sites of
CRC metastases after the liver. The presence of
extrahepatic metastases has been associated with
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109
Chapter 6
a
a
c
c
Figure6.6 • Small liver metastasis from CRC without increased FDG uptake in a 47-year-old woman. CE-MRI of the
liver shows two small metastatic deposits (arrow) in the right lobe (a, b). Representative coronal and axial images from a
whole-body FDG-PET examination (c, d) show no corresponding focal increased FDG uptake in the liver.
Sahani DV. etal. Current status of imaging and emerging techniques to evaluate liver metastases from colorectal
carcinoma. Ann Surg. 2014 May;259(5):861-72.
poor outcomes and traditionally considered a
contraindication for hepatic resection. However,
with recent advances in surgical techniques and
systemic medical treatment, hepatic resection
b
b
d
d
imaging modalities, diagnostic laparoscopy is
typically reserved for only high-risk patients (i.e.
very high CEA, indeterminate imaging for peritoneal
disease, etc.).
can be considered in patients with extrahepatic
disease amenable to surgical resection or long-term
oncologic control with adjuvant chemotherapy.
Patients with extrahepatic disease who are being
considered for resection should be managed in a
multidisciplinary setting and generally should be
treated with preoperative therapy to help define the
tumour biology.
Role of diagnostic laparoscopy before
CRLM resection
Diagnostic laparoscopy may prevent unnecessary
laparotomy in patients with occult intraperitoneal
metastases. In general, considering that many
patients will have undergone surgical exploration
of the peritoneum at the time of primary tumour
resection and because of the accuracy of current
Current surgical strategy in management
of patients with bilateral CRLM
The choice of surgical strategy for patients with
bilateral CRLM depends on the burden and
location of the tumour. One-stage simultaneous
multiple atypical hepatic resections, with
preservation of adequate FLR, is a safe and effective
technique in management of small and favourably
positioned bilateral CRLM. For patients with
extensive bilobar metastases, several strategies
including parenchymal-sparing hepatectomy (PSH),
combination of ablation with repeat PSH and two-
stage hepatectomy, can be applied.
PSH has been shown to be safe and effective
for the management of CRLM without compromising oncological outcomes. Furthermore, with
110
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Colorectal liver metastases
c
a
Figure6.7 • Whole-body PET-CT was performed on a 49-year-old woman with rectal cancer. Coronal FDG-PET
(a) and fused PET-CT (b) images from whole-body PET-CT show a focus of intense FDG uptake in the liver (arrows).
Corresponding axial image (c) acquired during CT shows the metastatic deposit in the right lobe of liver (arrow). Another
discrete extrahepatic peritoneal metastatic deposit is evident in the left side of upper abdomen on the FDG-PET and
fused PET-CT image (arrow) that on corresponding axial CT image (d) is located adjacent to the tail of pancreas (arrow).
(FDG indicates 18-fluoro-deoxyglucose.)
Sahani DV. etal. Current status of imaging and emerging techniques to evaluate liver metastases from colorectal
carcinoma. Ann Surg. 2014 May;259(5):861-72.
preservation of liver parenchyma, PSH increases
the potential of salvage repeat hepatectomy for
patients with recurrent intrahepatic disease. The
combination of multimodal therapies is another
approach to treat patients with multiple lesions
when complete resection of all metastases is not
feasible. In this approach, hepatectomy addresses
the main tumour mass while the residual tumour
b
d
debatable, most centres proceed with initial
resection of tumours within the FLR contralateral
to the planned PV occlusion, and then perform
the subsequent ipsilateral second‐stage resection.
The long-term survival of patients who complete
both stages is comparable to patients with more
limited disease treated by a conventional single‐
stage strategy.
is extirpated with local tumour-ablative therapy.
Combination resection-ablative therapy does
not compromise disease-specific survival when
Preoperative chemotherapy
compared with major resections and twostage hepatectomies. In certain circumstances,
combination resection-ablation can be associated
with decreased blood loss, shorter hospital stay and
less morbidity.
The role of preoperative chemotherapy in management
of CRLM can be discussed in three categories of
patients – those with resectable metachronous,
unresectable and synchronous disease.
Patients with inadequate FLR may be considered
for two-stage hepatectomy. In this approach,
removal of a portion of metastatic disease is
combined with occlusion of the contralateral portal
vein, either by surgical ligation or subsequent
percutaneous embolisation. A second curativeintent stage of the operation is performed after
hypertrophy of the contralateral liver when there
has been adequate increase of the FLR volume.
Although the choice between minor or major liver
resection at the first stage hepatectomy remains
Resectable metachronous CRLM
Current data regarding neoadjuvant chemotherapy
in patients with resectable metachronous CRLM
are conflicting. The potential advantages of
preoperative chemotherapy in this group are
in facilitating resection of large tumours and
assessment of tumour response to chemotherapy.
In contrast, progression of disease and the possible
increased risk of post-resection complications
and liver insufficiency are considered potential
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111