# Lessons from Laparoscopic Liver Surgery:  A Nine-Year Case Series

Authors: Laura Spencer; Matthew S. Metcalfe; Andrew D. Strickland; Elisabeth J. Elsey; Gavin S. Robertson; David M. Lloyd
Journal: HPB Surgery
 (2008)

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## Abstract

Objective. This series describes a developing experience in laparoscopic liver surgery presenting results from 40 procedures including right hemihepatectomy, left lateral lobectomy, and microwave ablation therapy. Methods. Forty patients undergoing laparoscopic liver surgery between September 1997 and November 2006 were included. The data set includes: operative procedure and duration, intraoperative blood loss, conversion to open operation rates, length of hospital stay, complications, mortality, histology of lesions/resection margins, and disease recurrence. Results. Mean age of patient: 59 years, 17/40 male, 23/40 female, 23/40 of lesions were benign, and 17/40 malignant. Operations included: laparoscopic anatomical resections n=15, nonanatomical resections n=11, microwave ablations n=8 and deroofing of cysts n=7.  Median anaesthetic time: 120 minutes (range 40–240), mean blood loss 78 mL and 1/40  conversions to open. Median resection margins were 10 mm (range 1–14) and median length of stay 3 days (range 1–10). Operative and 30-day mortality were zero with no local disease recurrence. Conclusion. Laparoscopic liver surgery appears safe and effective and is associated with reduced hospital stay. Larger studies are required to confirm it is oncologically sound.


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## Body

## 1. Introduction

Experience in laparoscopic liver surgery is growing worldwide. This
single centre series describes 40 laparoscopic liver procedures carried out
between September 1997 and November 2006. Included are both anatomical and
nonanatomical laparoscopic resections for both malignant and benign tumours and
novel use of the microwave ablation probe on hepatocellular carcinoma and other
benign lesions. Operating times, resection margins, length of hospital stay,
amount of blood loss, and technical aspects of laparoscopic liver surgery are
discussed.


## 2. Patients and Methods

Forty patients undergoing laparoscopic liver surgery by two surgeons
were identified from operating diaries between September 1997 and November
2006. Information was gathered on a standard proforma retrospectively from
operating notes, anaesthetic charts, histology reports, hospital notes,
hospital computer systems, general practitioner records, and direct observation
of procedures.No patient was excluded and patients were selected for laparoscopic
surgery as having a lesion which was technically possible to resect or treat
laparoscopically whilst leaving an adequate resection margin where applicable.
In the case of patients with hepatic tumours, a standard multidisciplinary team
approach in regards to preoperative staging, treatment, and selection was
adopted. Patients selected for microwave ablation included: patients with HCC
who would not withstand formal liver resection due to poor hepatic function,
one patient undergoing laparoscopic left lateral lobectomy for a suspicious
lesion (at operation suspected to be FNH), and a similar suspicious lesion in
segment 4a which was biopsied and then microwaved—this prevented a major
hemihepatectomy in a young patient for benign disease, that is, an inaccessible
haemangioma in segment 7, and a metastasis from a parathyroid carcinoma in
segment 4 preventing a major resection in a frail patient.Laparoscopic liver surgery was carried with most patients in a supine
low Lloyd-Davies position, some right sided lesions were accessed by
positioning the patient on their left side. One surgeon (DML) used an open
approach for obtaining a pneumoperitoneum for all candidates including those
who had had prior midline laparotomies. The second surgeon (GSR)
preferred to use a Veress needle inserted at Palmer's point (just
below the left costal margin in the midclavicular line), to insufflate the
abdomen and introduced a 5 mm laparoscope in the left upper quadrant to avoid
any adhesions whilst introducing the umbilical trocar in those with prior
midline laparotomies [1]. In
patients with no prior surgery, an open approach was used by GSR. A thirty-degree
laparoscope was used in all instances. Carbon dioxide pressures were maintained
between 8–12 mmHg. In general 5 ports including two 10/12 ports to interchange the cavitronic
ultrasound surgical aspirator (CUSA) (Valleylab Tyco Healthcare, Boulder, Colo, USA) and camera
were used. No hand assistance was used. Resections were carried out using the
harmonic scalpel (Ethicon Endosurgery, Cincinnati, Ohio, USA)
or argon beam coagulator (Valleylab Tyco Healthcare) to cut through the
capsule, and CUSA for parenchymal dissection in conjunction with an Allports
vascular staple gun (Ethicon Endosurgery), or a multiple clip applier for clipping
vessels. The harmonic scalpel uses ultrasonic energy vibrating at 55 500 Hz to allow precise cutting and focussed coaptive
coagulation allowing preservation of important structures such as bile ducts
and larger blood vessels. Coaptive coagulation requires a lower temperature
(50°C to 100°C) than electrocautery or lasers to denature proteins in the
tissues forming a haemostatic protein coagulum which seals smaller blood
vessels, when the effect is prolonged, secondary heat is produced and can seal
larger vessels useful for fast effective haemostasis in laparoscopic
hepatectomy. The argon beam coagulator is useful in laparoscopic hepatectomy as it may coagulate a
large area such as the cut surface of the liver after resection using lower
temperatures (50°C to 104°C) than standard electrocautery, thus minimising eschar and damage to
important structures such as bile ducts and large vessels.A single Pringle manoeuvre was applied for 30 minutes during the laparoscopic
right hemihepatectomy, no other resections required a Pringle manoeuvre and no
outflow control was necessary in any procedure.  Intraoperative ultrasound (BK Medical, Herlev, Denmark) was used to assess extent of
malignant tumours in all cases. At the end of the resection, fibrin glue
(Johnson and Johnson, Cincinnati, OH, USA) was used to seal the resection
site. All tumours were sealed in a retrieval pouch (Espiner Medical Limited retrieval products, Bristol, UK)
or an endocatch (Autosutures, Tyco Healthcare, Hampshire, UK)
before removal from the abdomen. For microwave ablation (Microsulis Medicial
Limited, Hampshire, UK) the 5 mm probe was inserted
through a laparoscopic port and the ceramic tip of the probe inserted directly
into the lesion, microwaves were then radiated from the tip. Ablation progress
was monitored by real-time laparoscopic intraoperative ultrasound. At the end of
the operation, a tube drain is placed in the liver bed to monitor any
postoperative bile leaks. When deroofing large liver and bile duct cysts a
portion of omentum is sutured into the defect to prevent bile leaks and a tube
drain is again left in situ for
postoperative monitoring.


## 3. Results and Discussion

Forty-three procedures including 41 laparoscopic liver procedures on 40
patients were performed between September 1997 and November 2006. The mean age
of patient at operation was 59 years, 17/40 of patients were male and 23/40
were female. The median American Society of Anaesthesiologist's (ASA) score was
2.Malignant lesions resected were colorectal metastases. Benign lesions
treated included haemangiomas, liver cell adenoma, focal nodular hyperplasia,
and deroofing of liver cysts and a bile duct cyst. Microwave ablation was
utilised for hepatocellular carcinoma, haemangioma, metastatic parathyroid
carcinoma, and focal nodular hyperplasia. Three operations incorporated
multiple procedures these included a 74-year-old frail male patient who had a
right inguinal hernia repair immediately before proceeding to a planned segment
5 resection of a colorectal metastasis. This negated the requirement for a second
anaesthetic. A 73-year-old male who had a wedge excision of a haemangioma in
segment 5 and microwave ablation of a second highly vascular haemangioma in
segment 6,  minimising the amount of tissue resected for benign disease.  A
34-year-old female undergoing laparoscopic left lateral lobectomy for a
suspicious lesion thought to be FNH, with a similar suspicious lesion found in
segment 4a, intraoperative frozen section confirmed this lesion also to be FNH
and a successful microwave ablation was performed  preventing a formal hemihepatectomy in a
young patient with benign disease.The operations included right
hemihepatectomyn=1, (a second right hemihepatectomy was aborted due to
widespread peritoneal disease following an exploratory laparoscopy n=1), left
lateral lobectomy n=4, bisegmentectomy n=2, segmetectomy n=8, wedge resection
n=11, microwave ablation n=8, and deroofing of liver and bile duct cysts n=7,
right inguinal hernia repair n=1. Table 1 describes the demographic,
intraoperative and postoperative details of all the patients.Table 1
Demographic, intraoperative, and postoperative details of patients undergoing laparoscopic liver surgery.
PatientAgeSexProcedureHistologyOperation timeBlood lossResection marginLength ofComplications(M/F)(minutes)(mL)(mm)stay (days)163MRHHCRM240150014Nil260MWES3HMG2400CE2Nil351FWES5LCA1200CE3Nil468FS5/6RCRM2400CE5Nil574FS4RCRM1800223Nil669MS6RCRM105053Nil774MS5R+RIHCRM1800CE7Nil843FS2RFNH1200CE3Nil975MS3RCRM2400103Nil1082MLLBCRM180500CE4Nil1177MMAS4/8HCC1500CE6Nil1245FWES6HMG1800456Nil1364MLLBCRM2400104Nil1473MS6RCRM24060046Nil1573MWES6, MAS5HMG900CE4Nil1670MMAS4aHCC900N/A7Nil1769MS5RCRM210500CE10Nil1857FWES5HMG1200CE2Convert to open due to CUSA failure1936FLLBFNH1200CE3Nil2034FLLB,MAS4FNH1200CE3Nil2155MMAS7HMG900N/A2Nil2258FWES3 SOCLC900CE2Nil2338MEL: (Planned RHH aborted)CRM Peritoneal deposits900N/A2Nil2451MWES2/3HMG1200CE3Nil2547FWE2/3Angiomyo-leiyoma600CE2Nil2652FWES3Mucinous cystaden-oma600CE1Nil2762FLDBDC, SOCBiliary cystaden-oma400N/A2Nil2841FLDLCLC400N/A2Nil2973FLDLCLC600N/A1Nil3057FLDBDC, SOCBDC600N/A2Nil3156FLDLC, SOCLC600N/A1Nil3284MS5RCRM6010CE1Nil3342FLDPCLLCPCL300N/A3Nil3479MLDPCLLCPCL600N/A3Nil3571FMAS4HCC400N/A2Nil3632FWES5/6FNH1200303Nil3743FMAS4Parathyro-ID carcinoma metastasis600N/A1Nil3851FWES6HMG1200203Nil3972FS4/S6RCRM200043Nil4034FMAFNH1300N/A2NilMedian operating time for the entire group of patients as judged by
length of time under general anaesthetic in theatre was 120 minutes (range 40–240 minutes).
Mean blood loss was 78 mL and only one patient required transfusion. Conversion
to open operation was carried out in 1 out of 40 patients; this was a segment 5
resection for a colorectal metastasis and was due to CUSA failure. There was no
perioperative mortality and no 30-day mortality. Median total length of stay in
hospital was 3 days. No bile leaks were experienced and there were no other complications.Median operating time excluding patients having only cyst deroofing or
microwave ablation, and excluding the patient who was converted to open hepatectomy
and the patient having a failed right hemihepatectomy due to the presence of
peritoneal metastasis, was unchanged at 120 minutes (range 60–240 minutes),
mean blood loss was 104  mL, and median length of stay remained 3 days for this
group. This data is described in Table2.Table 2All patients (including resections, ablations, and cyst deroofings)N=40Patients undergoing only laparoscopic hepatectomyN=25Median operation time (minutes)120120Mean blood loss (mL)78104Median length of stay (days)33Median resection margins given by the pathologist were 10 mm (range 1–45 mm), where
actual resection margins were not given malignant lesions were described as
completely excised (CE). Of the 17
malignant tumours, one patient has died of coronary artery disease and one
patient who had a segment 5 resection of colorectal liver metastasis has
developed lung metastases. No patient has had locally recurrent disease.


## 4. Discussion

The benefits and indications for laparoscopic liver surgery have yet to
be fully established. The first reported laparoscopic liver resection was
undertaken in 1991 for a benign lesion [2]. Since then data from a recent
review suggests that most laparoscopic resections
have been nonanatomical or simple wedge resections or cyst fenestration and deroofing
for liver cysts [3]. Left lateral lobectomy (Couinaud segments 2 and 3) has
been carried out and also more rarely formal left or right hemihepatectomy [4].  Approximately 70% of resections have been
carried out for benign lesions and 30% malignant lesions [5]. The largest
series reports 100 resections [6].Laparoscopic liver surgery is a developing field and our experience and
learning curve together with a discussion pertaining to indications, safety,
and efficacy of laparoscopic hepatic resection and technical aspects of the
surgery is presented.The first laparoscopic liver resection at our institution was a left
lateral lobectomy in 1997 for focal nodular hyperplasia. Since then the number
of hepatic resections carried out laparoscopically has increased year on year
see Figure1.Figure 1
Graph showing the number of laparoscopic liver procedures per year 1997-2006.Lesions selected for laparoscopic resection at our institution are in
the easily accessible segments: 2, 3, 4a, 5, and 6 well away from the major
hepatic veins. These lesions are often visible on the liver surface and well
characterised by saggital and coronal magnetic resonance images. Initially only
benign lesions were resected due to concerns regarding oncological adequacy of
laparoscopic resection margins and the risk of tumour seeding in the port sites.
The publication of the conventional versus laparoscopic-assisted surgery in
patients with colorectal cancer (CLASICC) trial verified that there were no
significant differences between open surgery and laparoscopic-assisted
colorectal tumour excision with respect to tumour and nodal status, therefore,
laparoscopic surgery in relation to excision of malignant hepatic tumours
seemed justified [7].Microwave ablation has been under investigation by the authors for the
treatment of liver tumours in both animal models and human patients [8–10].
The indications for the use of microwave ablation are, as yet, not clearly
defined though patients with HCC who could not withstand a formal hepatectomy
due to loss of hepatic tissue, symptomatic benign tumours (excluding liver cell
adenoma), unusual single liver tumours, and patients with tumour recurrence in
a liver that has previously undergone a resection are all potential candidates
and have been described in this series.Controversy exists as to the adequacy of tumour excision and resection
margin. One large seriesreports
median resection margins of 5 and 10 mm for colorectal metastasis and HCC, respectively
[4]. Usage of the intraoperative ultrasound probe has been shown by Gigot et al. [11] to improve adequacy of
resection margin. The intraoperative ultrasound probe is therefore used
routinely in our establishment when resecting malignant tumours.There are currently no randomised controlled trials comparing open and
laparoscopic hepatectomy but several small nonrandomised comparative trials
have suggested that
there is no difference in adequacy of resection margin between open and
laparoscopic hepatectomy [12–15]. The median resection margin for
malignant tumours in this study is 10 mm and there has been no local recurrence.
Recent studies have now suggested that the width of a negative resection margin
does not affect survival, recurrence risk, or site of recurrence for colorectal
metastasis [16]. It is of note that anatomical resections for colorectal
metastases have also not been shown to be superior to wedge resections as long
as the tumour is clear at the resection margins [17].Abdominal wall metastasis at port sites has been reported after
laparoscopic surgery for malignant tumours [18]. Recent data has shown that there is no
difference in wound-site tumour recurrence between open and laparoscopic
colorectal surgery for  if conventional
oncological techniques such as no touch technique and sealing resected
specimens in retrieval pouches before removal are employed, rates should be
less than 1% [19]. No wound site recurrence has been experienced in this series
to date.Some surgeons have raised concerns for the possibility of gas embolism
due to transection of low pressure veins under pneumoperitoneum. This has led
some centres to adopt a gasless laparoscopy technique, whereby intra-abdominal
space is created by abdominal suspension techniques [20]. Others have used a
lower pressure carbon dioxide pneumoperitoneum, maintained between 10–12 mmHg
[4, 12].Usage of the argon beam coagulator in both laparoscopic cholecystectomy
and laparoscopic liver surgery has been associated with a clinical diagnosis of
venous gas embolism in several case reports [21–23]. A recent review
suggests that the incidence of clinical gas embolism in 700 laparoscopic liver procedures carried
out worldwide is reportedly 0.3% [5]. It is, however, of interest that
following laparoscopic cholescystectomy intravascular gas bubbles have been
routinely observed using transoesophageal echocardiography; this does not seem
to correlate with the clinical picture of gas embolism [24].An experimental study assessing the usage of argon-enhanced coagulation
of cut sections of liver in a porcine model, whereby gas emboli were detected
using a Doppler flow cuff around the caudal vena cava, demonstrated that the
number of gas emboli produced increased with increasing gas flow rates but was
not affected by coagulation power. This study recommended that surgeons and
anaesthetists should be aware that there is a potential to develop a clinically important gas
embolism and that adequate precautions should be taken to prevent this such as
selecting a low flow setting on the argon beam coagulator and adequate venting
of the abdomen through chimneys in laparoscopic ports to maintain safe
pressures of between 8–12 mmHg [25].
These measures have been adopted at our institution where argon gas flow is set
to 4 L/min (low flow) on the laparoscopic setting which incorporates an alarm if
intra-abdominal pressures exceed preselected limits—12 mmHg for
laparoscopic hepatectomy which alerts the surgeon who can open the port chimney to vent the abdomen. No
clinical signs of gas embolism have been observed in association with the argon
beam coagulator. Hepatectomy can be associated with severe haemorrhage and a
major concern to some is the threat of uncontrollable haemorrhage with minimal
access to the abdomen. This series presents an extremely low operative blood
loss rate with a mean blood loss of 78 mL. It is worthwhile noting that where
laparoscopic liver resections are converted to open procedures it is often due
to bleeding.In general, some studies comparing laparoscopic versus open procedures
have demonstrated that the laparoscopic approach may well be associated with
less blood loss than open equivalents [14, 26]. This observation may be due
to the tamponading effect of a pneumoperitoneum and the anaesthetists at our
institution raise the central venous pressure to between 7–10 mmHg whilst
the surgeons decrease the carbon dioxide insufflation pressure at the end of
all laparoscopic liver procedures in order to assess safely for haemostasis.
Additional anaesthetic considerations pertaining to laparoscopic liver surgery
include initially running a lower central venous pressure of 1-2 mmHg to
decrease bleeding and placement of a central line for central venous pressure
monitoring, but an epidural is not required as postoperative analgesia
requirements are usually confined to oral preparations.The final consideration for safe laparoscopic surgery pertains to
technical ability and experience of the surgeon. It is recommended by the
specialist advisory committee to the National Institute of Clinical Excellence
that laparoscopic liver resections should only be carried out in specialist
centres and by those with advanced skills in hepatic resection and laparoscopy
[27]. It is also apparent that the lesions most suitable for laparoscopic
resection are those situated in the left lateral and right anterior segments
away from the main hepatic veins this in turn reduces the risk of serious
haemorrhage.In conclusion this series confirms evidence already published in support
of laparoscopic liver resections. Patients experience a shorter hospital stay,
minimal blood loss, shorter operation time, and short-term data indicates
equivalent oncological results when compared with conventional open
hepatectomy. Randomised controlled trials assessing the oncological efficacy of
laparoscopic and open hepatectomy for selected lesions are indicated at this
stage.



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