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Liver metastases in close contact to hepatic veins ablated under vascular exclusion
S. Evrard a,b,*, V. Brouste c, P. McKelvie-Sebileau c, G. Desolneux a
a
Digestive Tumours Unit, Institut Bergonie, 229 cours de l’Argonne, 33076 Bordeaux Cedex, France
b
Universite Bordeaux Segalen, 166 cours de l’Argonne, 33076 Bordeaux, France
c
Clinical and Epidemiological Research Unit, Institut Bergonie, 229 cours de l’Argonne, 33076 Bordeaux Cedex, France
Accepted 24 August 2013
Available online - - -

Abstract

Background: Liver metastases (LM) in close contact to hepatic veins (HV) are a frequent cause of unresectability. Reconstruction of hepatic
veins is technically difficult and outcomes are poor. Intra-operative radiofrequency ablation (IRFA) with vascular exclusion (VE) may be a
useful approach.
Methods: Out of 358 patients operated for LM, 22 with LM close to a HV treated by IRFA under VE with at least one year of follow-up
were included in this retrospective study. Technical success was evaluated at four months by CT scan of the ablated lesion. Complications;
local, hepatic and extra-hepatic recurrence rates, and overall survival are reported.
Results: The median number of metastases was 4.5 [range: 1e12]. Seventeen patients had bilateral metastases. The median size of ablated
lesions was 2 cm [range: 1e5.5]. Seven complications occurred (1 Grade 1, 2 Grade 3b and 4 Grade IVa), with no mortality. No recurrence
of ablated lesions was detected at four months or during follow-up. Seventeen patients had new or extra-hepatic lesions. Median overall
survival for colorectal patients was 40 months 95%CI[17.5-not reached].
Conclusions: IRFA plus VE for LM in close contact to a HV is a novel approach, appearing to be a safe and effective technique which can
extend the applications of liver metastases surgery.
Ó 2013 Elsevier Ltd. All rights reserved.

Keywords: Ablation techniques; Radiofrequency ablation; Colorectal liver metastases; Complications; Mortality; Vascular exclusion; Hepatic vein

Introduction recurrence for ablated lesions were confirmed by a 46.1%

Intra-operative radiofrequency ablation (IRFA) is gain-
ing increasing acceptance in liver metastases surgery.1,2
The results of the ARF2003 study in which unresectable
colorectal liver metastases were treated with IRFA com-
bined or not with resection show an overall survival (OS)
rate of 43.3% (95%CI [21.2; 63.7]) at 5 years, highlighting
the relevance of this technique to extend surgical frontiers,
especially in complex, bilateral disease. As a local treat-
ment, IRFA has also demonstrated prospectively an accept-
able local rate of control with a 4%e6.5% rate of local
recurrence for ablated lesions.3,4 These low rates of
* Corresponding author. Digestive Tumours Unit, Surgical Oncology, In-
stitut Bergonie, 229 cours de l’Argonne, 33076 Bordeaux, France. Tel.:
þ33 5 56 33 32 66; fax: þ33 5 56 33 33 83.
E-mail address: s.evrard@bordeaux.unicancer.fr (S. Evrard).
(95%CI [32.3%; 58.9%]) liver progression-free survival at
one year including recurrence of treated and new hepatic le-
sions.3 There is some variability in the limits of resect-
ability across surgeons, including specialized surgeons5
but specific technical limits apply in all cases. Adjacency
to portal structures and hepatic veins (HV) has always pre-
sented a technical challenge for resection, and a balance is
required between two opposing risks: overtreating the
lesion and destroying the different vessels; or undertreating
the lesion leaving involved margins that lead to tumoral
relapse. Some small series of a radical approach involving
hepatic vein resection have been published using
demanding grafting techniques for reconstruction.6e10
Nevertheless, although thermal ablation is contra-
indicated to treat para-portal lesions due to the inability
of biliary ducts to support heating, it may be a useful tech-
nique to treat lesions close to the HV. The aim of this study
was to investigate feasibility and outcomes of this artful

0748-7983/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.ejso.2013.08.028

Please cite this article in press as: Evrard S, et al., Liver metastases in close contact to hepatic veins ablated under vascular exclusion, Eur J Surg Oncol
(2013), http://dx.doi.org/10.1016/j.ejso.2013.08.028
2 S. Evrard et al. / EJSO xx (2013) 1e7
strategy, reporting technical success at four months, com-
plications rates, local, hepatic and extra-hepatic recurrence
rates and OS.
Patients and methods
Patients
From April 2000 to November 2010, 358 patients
received surgery for liver metastases in our tertiary care
centre. Their data were prospectively recorded and retro-
spectively analysed for this study. All patients receiving
IRFA with vascular exclusion (VE) for liver metastases of
any origin, with a minimum of one year of follow-up
data were considered for inclusion. Patient records were re-
viewed to confirm that all patients had liver metastases
touching the HV. The decision for surgery for each patient
was taken in a multidisciplinary team discussion including
medical oncologists, radiologists, and surgeons. All pa-
tients gave informed consent to receive surgery. Internal re-
view board approval was obtained for the study.
Indication
Ablation with total vascular occlusion was considered
for metastases in close contact with HV when no safety
margin could be achieved by resection or when a vascular
involvement required an en-bloc vascular resection fol-
lowed by a reconstruction (suture or grafting).
Surgical technique
All patients were operated on by the same surgeon (S.E)
by laparotomy. Operative assessment of the resectability of
LM always included a complete exploration of the perito-
neal cavity, liver mobilisation and liver ultrasonography
(Lynx 3101 then Profocus, B-K Medical, Copenhagen,
Denmark). IRFA was performed with an electrode needle
(Integra, Tuttlingen, Germany) infused with isotonic saline
and connected to a generator (Elektrotom 106 HFTT,
Berchtold, Tuttlingen, Germany). Introduction of the elec-
trode needle and coagulation were done under ultrasono-
graphic guidance. During the high frequency coagulation
(375 kHz), the electrode saline perfusion was automatically
regulated from 30 to 110 ml/h according to the variation in
tissue impedance. Power was adjustable from 5 to 60 W.
The number of coagulations and their duration depended
on the size of each metastasis.
The Pringle manoeuvre and a hepatic vein clamping
control were used to treat paravascular lesions. Vascular
flow is known to cool target tissue during heating and could
generate a zone of high recurrence risk just beside the
vessel. Pringle manoeuvre was performed by squeezing
the hepato-duodenal ligament with a tourniquet for the
duration of the heating process. When the needle has to
be repositioned in order to overlap the heating volumes,
clamping was intermittent. Vascular exclusion involved
clamping both the portal and arterial inflows as well as
the hepatic vein outflow, without interruption of the caval
Please cite this article in press as: Evrard S, et al., Liver metastases in close contact to hepatic veins ablated under vascular exclusion, Eur J Surg Oncol
(2013), http://dx.doi.org/10.1016/j.ejso.2013.08.028
flow. Most of the time, a total vascular exclusion including
the three HV was not necessary, and clamping one or two
of the HV depending on the size and location of the metas-
tasis was sufficient. Clamping the three HV was sometimes
necessary for wide lesions at the top of the liver, but due to
poor cardiovascular tolerance, this approach was always
evaluated firstly by short clamping test attempts. Optimal
selective HV clamping was achieved by small “bull-dog”
clamps when a non-selective HV triad clamping required
a straight vascular clamp.
Follow-up
Complications were recorded according to the Clavien-
Dindo classification.11 Clinical assessment, carcinoem-
bryonic antigen (CEA) dosage and imaging (CT scan or
MRI) were performed every four months for two years,
and every six months from then on. Thereafter, each new
event (recurrence including location, death) was recorded
in the database. The primary focus was to assess technical
success of IRFA was absence of contrast enhancement on
the CT scan at 4 months on the ablated lesion. If a suspicion
of recurrence was seen, a confirmatory MRI was observed.
New lesions occurring later in follow-up were recorded but
are not considered to reflect technical success of the
procedure.
Statistical considerations
Median follow-up was calculated by the reverse Kaplan
Meier method where deaths are censored. Survival was
calculated with Kaplan Meier plots where all deaths, irre-
spective of cause, are considered as events with participa-
tion time calculated between the date of the surgery and
the date of death. Patients alive at last news are censored
with participation time from the date of surgery to the
date of last news. OS was calculated only for patients
with primary colorectal cancer and is reported with 95%
confidence intervals (95%CI). Local recurrence was defined
as a modification of the IRFA necrosis area with no contrast
enhancement, and a confirmatory MRI as required. Compli-
cations are described using counts and percentages. All nor-
mally distributed quantitative data are described with
means and non-normally distributed with medians and
ranges.
Results
Patient characteristics
Twenty two patients were identified in our institutional
database as having at least one metastasis in contact with
a HV treated by IRFA with VE, with a minimum of one
year follow-up. There were 9 females and 13 males with
median ASA of 2 (range: 1e3). Median age was 67.5 years
[range: 38e80]. Eighteen (81.8%) patients had a primary
 S. Evrard et al. / EJSO xx (2013) 1e7
colorectal tumour and all except four received induction
chemotherapy.
Description of procedure (Table 1)
The median number of liver metastases was 4.5 [range:
1e12] (Table 1). Bilateral lesions were observed in 17
cases (77.3%). All patients received IRFA with VE, com-
bined or not with a parenchymal resection. The duration
of inflow vascular occlusion was always shorter or equal
to the heating time (median 13 min, range: 3e60) (Table
1). One patient received two IRFA with VE. One patient
received a 2-stage procedure. The median size of the abla-
ted lesions was 2.5 cm [range: 1e5.5].
Complications
No intra-operative complication was observed in rela-
tion with ablation. Seven (32%) patients experienced com-
plications, Grade 1 for one (chylous ascite), Grade 3b for
two requiring reoperation (biliary fistula þ septicaemia,
and bilioma), and Grade IVa for four (transitory liver failure
for two, and haemorrhage and peritonitis, both requiring re-
operation) (Table 2). Only the transitory liver failure was
considered to be a result of the IRFA procedure. No post-
operative mortality was observed.
Follow-up
No recurrence of ablated lesions was detected at the first
post-operative control at 4 months nor during follow-up
(Table 2). The median follow-up was 34.6 months, 95%
CI [31e51.2]. Eight patients had new hepatic lesions and
nine had extra-hepatic recurrences during the study dura-
tion. For the 18 patients with a colorectal cancer, median
OS was 40 months (95%CI[17.5- upper limit not reached).
OS at 2 years was 72.2%, 95%CI [45.6e87.4] (Fig. 1).
Discussion
This is the first series to our knowledge to comprehen-
sively describe indications, complications and outcomes af-
ter IRFA for liver metastases in close contact with the HV.
In addition, this series is also comparatively larger than
publications reporting complication rates after the surgical
alternative of reconstruction that have reported on small se-
ries involving 86,8 to 16 patients.7,9 Overall, results indicate
that this technical approach induces relatively low rates of
complications and good efficacy, enabling previously unre-
sectable patients to be treated by curative surgery.
Therapeutic choices in the management of LM, as for all
metastatic disease, must be made in multidisciplinary team
discussions. In particular, the question of neoadjuvant or
adjuvant chemotherapy must be systematically evaluated.
Patients with complex metastatic disease due to abundance
and/or bilateralism, should be selected based on the
Please cite this article in press as: Evrard S, et al., Liver metastases in close contact to hepatic veins ablated under vascular exclusion, Eur J Surg Oncol
(2013), http://dx.doi.org/10.1016/j.ejso.2013.08.028
3
following criteria: 1) disease progression must be
controlled by systemic treatment; 2) additional extra-
hepatic metastases must be limited (ie. <3 lung metasta-
ses); and 3) general health status should be good (ASA 3
patients should be particularly monitored). In this series,
all patients complied with these criteria and we observed
a 2-year OS of 72.2%. This is comparable to the rates
described in the literature after the surgical alternative of
hepatic vein reconstruction, with 3-year survival ranging
from 50%7e76%.9
Involvement of the liver vessels and the impossibility of
maintaining a sufficient volume of healthy parenchyma af-
ter surgery are major factors increasing the likelihood of
unresectability. However, lesions located in paravascular
situations can be treated by resection in some instances.
Resection of the metastasis leaving only clear margins is
not so much a technical concern, but an oncological one,
representing potential under-treatment. Indeed this resec-
tion is at high risk of leaving at least microscopic tumoral
residue on the vessel wall (R1 resection), increasing the
risk of recurrence as recently outlined: a 5-year OS rate
of 55% was observed for R0 resection versus only 26%
for R1 resection12; To resect the lesion plus the vessel en-
bloc is a good oncological solution, but this presents real
technical difficulties for reconstruction. Despite some pub-
lications from transplant liver surgeons,6e10 resection of
HV followed by different grafting reconstructions has not
gained widespread acceptance and cannot be advocated as
a routine procedure. In a series of 16 patients, Hemming
et al.7 classified hepatic vein reconstruction as a procedure
associated with a high level of technical challenge and risk,
justified due to the lack of curative alternatives. Data
regarding complications and outcomes vary across publica-
tions but mortality may be as high as 12%,7 morbidity as
high as 50%9 and survival outcomes have been reported
as “unsatisfactory”.6 A recent series reporting on extensive
hepatectomies for initially unresectable CLM receiving
conversion chemotherapy and portal vein obliteration, re-
ported 12 cases of vascular reconstructions, with half of
them being hepatic vein or caval resections. The mortality
was 33.3% (4/12) and authors concluded that a less aggres-
sive approach such as ablation should be proposed, espe-
cially for patients receiving more than 12 cycles of
conversion chemotherapy.13 The technique described in
our series, provides an alternative solution for these diffi-
cult cases, offering efficacy and simplicity using thermo-
ablation.
This approach has some experimental background.
Indeed some animal data have reported high resistance of
the HV to heat, especially in large vessels. Portal and hepat-
ic veins with diameters over 3.0 mm maintained high
patency after radiofrequency.14 Moreover, radiofrequency
ablation near the inferior vena cava appeared to be safe
and feasible in dogs.15 As vascular flow cools the surround-
ing tissues, and therefore precludes complete destruction of
the target,16 a vascular exclusion is required. Despite a
4 S. Evrard et al. / EJSO xx (2013) 1e7

Table 1
Description of procedures.
ID Description of Liver metastases treated by IRFA with total vascular exclusion Others procedures Treatment
the disease Segment Size (mm) Localization Nb Duration Energy
of of heating delivered
shoots (min) (J)
1 3 mets. Bilateral 2 30 Median and Bi segmentectomy 5/6 8 35 100 000
Metachronous left HV
2 >10 mets. Bilateral 2 30 Left HV (Left lobe Left colectomy 6 25 41 000
Synchronous cleaning as a first stage)
Massive right lobe
involvement
plus left HV
-2-stage
procedure planed
-Radiological
right portal
vein embolization
-Lung mets
-Second stage
cancelled and
palliative
chemotherapy
3 7 mets. Bilateral 4 11 Median HV Right hepatectomy 3 10 26 700
4 1 met 4 55 Median and left HV Resection of a 10 60 160 400
Complete atrophy mesenteric metastasis
of left lobe
5 3 mets. bilateral 2 15 Left HV Bisegmentectomy 3 12 35 522
IV/V plus
peritonectomies
6 >10 mets. Bilateral 7 30 Right HV 1 IRFA plus 3 15 63 000
Massive left liver Left portal vein
involvement plus 2 alcoolisation/ligation.
right mets Two stage procedure
7 4 mets. Bilateral 2/4 27 Left and median HV Right hepatectomy 11 41 100 000
Involvement
of the 3 HV
8 7 mets. Bilateral 2/4 18 Left and median HV Bisegmentectomy 4 10 27 700
Involvement 4/5 plus 3
of the 3 HV others IRFA
9 3 mets. Bilateral 7 8 Right HV 2 3 4450
4a 20 Median HV Bisegmentectomy IVb/5 3 14 30 000
plus 1 other IRFA
10 >10 mets. 7 10 Right HV Bisegmentectomy II/III 8 8 40 000
11 3 mets. Bilateral 7 20 Right HV 2 wedge resections 3 10 28 300
12 5 Bilateral 4 10 Median and right HV Trisegmentectomy 3 5 11 000
6/7/8 plus 1
other RF
Ileostomy’s closure
13 3 mets. in the 7 20 Right HV 2 others RF 2 8 11 300
right liver
14 6 mets. Bilateral 7 15 Right HV Trisegmentectomy 2 7 10 000
2/3/4b plus 1
other IRFA plus
Left spleno-
pancreatectomy
15 >10 mets. 4 10 Median HV Right colectomy 5 10 16 300
bilateral Segmentectomy 3
Necessitating
a 2-stages
procedure
16 3 mets. Bilateral 7 40 Right HV Trisegmentectomy 10 42 78 100
3/4b/5
17 6 mets. Bilateral 7 40 Right HV Plus 5 others IRFA 6 44 63 800
18 12 mets Bilateral 7 12 Right HV Bisegmentectomy 2/3 2 5 7400
plus 7 IRFA

Please cite this article in press as: Evrard S, et al., Liver metastases in close contact to hepatic veins ablated under vascular exclusion, Eur J Surg Oncol
(2013), http://dx.doi.org/10.1016/j.ejso.2013.08.028
 S. Evrard et al. / EJSO xx (2013) 1e7 5

Table 1 (continued )
ID Description of Liver metastases treated by IRFA with total vascular exclusion Others procedures Treatment
the disease
Segment Size (mm) Localization Nb Duration Energy
of of heating delivered
shoots (min) (J)
19 1 met 8 20 Median and right HV 6 32 85 000
20 4 mets. Bilateral 4 20 Median HV Bisegmentectomy 5/6 3 15 42 000
plus 1 metastasectomy
21 1 met in segt 7/8. 7/8 17 Right HV 2 13 15 000
Atrophy of
the left liver.
Impossibility to
perform a right
hepatectomy
22 Recurrence 8/4 40 Median and right HV Plus 5 others IRFA 10 42 150 700
of 6 mets.

Pringle manoeuvre, some blood circulates in the HV by this remains to be confirmed in practice. Irreversible elec-
flow-back from the vena cava. For an HV-adjacent lesion, troporation is a new technique using a non-thermal treat-
it is not necessary to clamp the vena cava and just the ment effect by high-voltage electrical pulses. In the
HV in contact with the target can be clamped. Indeed, future, electroporation should be able to treat lesions close
clamping the vena cava often has haemodynamic side ef- to vascular and also biliary structures. Nevertheless,
fects which can be a real concern, whereas selective clamp- research and development are still needed as now only par-
ing of HV is much better tolerated. tial devascularization of the tumour has been obtained20 in
Patients in this series were treated with a first generation such difficult situations. In this series, we did not observe
RF generator requiring several repositionings of the needle any IRFA-specific complications like thrombosis or rupture
in order to obtain overlapping of the heat volumes. Current of the vessel and the vessel was maintained, as shown in
generators are now more powerful. The treatment time has Fig. 2(a and b). Maintaining HV flow is a prerequisite of
also decreased and most of the time, a one-shot procedure this technique when it is used to treat the last HV (when
is sufficient. Moreover, microwave ablation is now pro- the other two are resected) during a concomitant contralat-
posed to offer molecular agitation, as opposed to the RF eral hemi-hepatectomy. On the other hand, we observed
ionic agitation, with a more precise definition of the geo- two transitory liver failures. Indeed, IRFA of HV-adjacent
metric thermal field.17,18 Theoretically, vessel clamping LM is often done in a context of severe bilateral disease
should not always be necessary with this technology19 but and the risk of going beyond the limits of the residual func-
tional liver is always present.
Table 2
Post-operative outcomes for patients with liver metastases in close contact
to supra hepatic veins ablated under vascular exclusion.
N (%)
Recurrences of the ablated lesion at 4 months 0 (0)
Recurrence of ablated lesion during follow-up 0 (0)
Other recurrences
New liver lesions 8 (36)
Extra-hepatic lesions 9 (41)
Complications (Dindo & Clavien)11
No 15 (68%)
Yes 7 (32)
Grade Ia 1 (5)
Grade II e e
Grade IIIbb 2 (9)
Grade IVac 4 (18)
a
Grade I: Chylous ascite.
b
Grade IIIb: Biliary fistula (reoperation) septicaemia, Bilioma
(Reoperation).
c
Grade Iva: Liver failure, Liver failure þ Septicaemia, Peritonitis due to Figure 1. Overall survival estimates for patients with liver metastases of
rectal anastomotic leakage (reoperation), Haemorrhage (anticoagulation colorectal origin in close contact to hepatic veins ablated under vascular
for aortic valve) plus Septic gram (reoperation). exclusion.

Please cite this article in press as: Evrard S, et al., Liver metastases in close contact to hepatic veins ablated under vascular exclusion, Eur J Surg Oncol
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6 S. Evrard et al. / EJSO xx (2013) 1e7

Figure 2. Male patient, ID 22, 79 years with primary colon tumour a) 4 cm colic liver metastasis located at the top of segment VIII. Close contact with the
right and the median hepatic vein. Overlapping of 10 needle applications delivering 150 773 J. Vascular exclusion lasting 13 min b) Follow-up at 2 months.
Notice that the right hepatic vein is clearly functional.

As with any retrospective analyses, there are some lim- lesions appears to be an effective and recommended
itations to consider such as the small size of the series, technique.
although as previously mentioned it is larger than other
retrospective analyses published. The survival rates calcu-
lated with 18 patients would certainly need validating in
Role of the funding source
a larger series, but serve principally as an indication that
this procedure is not only technically feasible, but also pro-
The Ligue Nationale Contre le Cancer, Gironde, France
duces acceptable outcomes compared to reports in the liter-
donated the RF generator but had no role in study design,
ature. However, as adjacency with an HV (with at the same
data analysis or manuscript preparation.
time, other lesions being resectable or ablatable) is not a
common occurrence (22 out of 358 patients treated for liver
metastases in our institution, representing 6.1%), and large
series are difficult to obtain. Research support
Intra-operative ablation of liver metastasis in close con-
tact to hepatic veins is a relatively unknown technique in Supported by the Ligue Nationale Contre le Cancer, Gi-
liver surgery. The most widespread notion is that this spe- ronde, France.
cific paravascular localization is a source of recurrence or
complications. This is true for the portal pedicle, but not
for the hepatic and caval veins. Comparing our data to Conflicts of interest
the literature from resection followed by reconstruction,
intra-operative ablation under vascular exclusion for these The authors have no conflicts of interest to declare.

Please cite this article in press as: Evrard S, et al., Liver metastases in close contact to hepatic veins ablated under vascular exclusion, Eur J Surg Oncol
(2013), http://dx.doi.org/10.1016/j.ejso.2013.08.028
 S. Evrard et al. / EJSO xx (2013) 1e7
Acknowledgements
The authors thank the Ligue Nationale contre le Cancer,
Gironde, France for their generous gift of the RF generator.
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