Original Paper Received: June 29, 2010 Accepted: October 2, 2010 Published online: $ $ $
Dig Surg 321891 DOI: 10.1159/000321891
Surgical Management of Benign and Indeterminate Hepatic Lesions in the Era of Laparoscopic Liver Surgery Mohammed Abu Hilal Francesco Di Fabio Mabel Joey Teng Dean Anthony Godfrey John Neil Primrose Neil William Pearce Hepatobiliary-Pancreatic and Laparoscopic Surgical Unit, Southampton General Hospital, Southampton University Hospitals NHS Trust, Southampton, UK
Key Words Benign liver tumours ⴢ Laparoscopic surgery ⴢ Liver resection ⴢ Morbidity
Abstract Background/Aims: The expansion of the laparoscopic approach for the management of benign liver lesions has raised concerns regarding the risk of widening surgical indications and compromising safety. Large single-centre series focusing on laparoscopic management of benign liver lesions are sporadic. Methods: We reviewed a prospectively collected database of patients undergoing pure laparoscopic liver resection (LLR) for benign liver lesions. All cases were individually discussed at a multidisciplinary team meeting. Results: Forty-six patients underwent 50 LLRs for benign disease. Indications for surgery were: symptomatic lesions, preoperative diagnosis of adenoma or cystadenoma, and lesions with an indeterminate diagnosis. The preoperative diagnosis was uncertain in 11 cases. Of these, histological diagnosis was hepatocellular carcinoma in one (9%) and benign lesion in 10 patients (91%). Thirteen patients (28%) required major hepatectomy. Three patients (7%) developed postoperative complications. Mortality was nil. The median postoperative hospital stay following major and minor hepatectomy was 4 and 3 days, respectively. Conclusion: The laparoscopic approach
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represents a safe option for the management of benign and indeterminate liver lesions, even when major hepatectomy is required. LLR should be only performed in specialized centres to ensure safety and strict adherence to orthodox surgical indication. Copyright © 2011 S. Karger AG, Basel
Introduction
Laparoscopic liver resection (LLR) is becoming more popular, especially in specialized liver surgery centres [1]. In expert hands, the feasibility, safety and efficiency of the laparoscopic approach have been demonstrated when appropriate criteria are applied to patient selection [2–11]. In a recent review including approximately 2,800 patients, the mortality and morbidity rates were reported to be 0.3 and 10.5%, respectively [1]. Initially, the laparoscopic approach was adopted for wedge resection and left lateral sectionectomy, and only more recently it has been shown to be feasible and safe for major hepatectomies [12–16]. The majority of laparoscopic resections were originally performed for benign lesions [6, 7]. This appeared appropriate especially when considering initial concerns regarding tumour dissemination, incomplete tumour resections and involved marMr. M. Abu Hilal, MD, FRCS Hepatobiliary and Pancreatic Surgical Unit Southampton University Hospital Tremona Road, Southampton SO16 6YD (UK) Tel. +44 2380 796 796, Fax +44 2380 796 620, E-Mail abu_hlal @ yahoo.com
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gins [2, 17–20]. Several centres have now demonstrated the oncological efficiency of the laparoscopic approach [1, 21–24]. There is an increasing wealth of evidence to suggest that the minimally invasive technique offers significant advantages in both benign and malignant diseases (in terms of less pain and analgesic drug consumption, shorter hospital stay, less transfusion requirements, faster recovery, reduced postoperative adhesion and improved cosmetic results) compared to open surgery [5, 25–27]. Some of these benefits, especially shorter hospital stay and early return to work, appear more appealing in patients with benign disease, who are commonly fit and young. Traditional indications for surgery in benign liver lesions include preoperative diagnosis of adenoma or cystadenoma, symptomatic lesions and suspicious lesions with an indeterminate diagnosis [26]. Suspicious lesions represent a clinical management dilemma for the risk of missing a premalignant or malignant lesion, or subjecting the patient to an unnecessary procedure [28–31]. In this respect, fears of a non-judicious approach in widening the surgical indications for doubtful lesions due to the availability of the minimally invasive approach have been raised [26]. These concerns are justified as benign, asymptomatic lesions are now increasingly identified due to wider availability and use of imaging [26]. Large single-centre series focusing on laparoscopic management of benign liver lesions are still sporadic. Only one similar single-centre series on LLR for benign disease has been published [32]. In this paper we present a single-centre experience of minor and major pure LLR for benign liver lesions with a critical analysis of the indications for surgery and postoperative outcome. Methods We reviewed a prospectively collected database of all patients undergoing pure LLR [26] for presumed benign disease at Southampton University Hospitals NHS Trust between June 2004 and December 2009. The data were analysed in regards to patient demographics, indication for surgery, type of resection, intra-operative blood loss (calculated by measuring the volume of blood in the suction bottles, after subtracting wash fluid at the end of surgery with the addition of weighed swabs), duration of surgery, conversion rate, complication rate, length of high dependency unit (HDU) stay, and postoperative length of stay. Routine blood tests, ultrasound of the abdomen, computed tomography of the abdomen with tri-phasic liver contrast enhancement and liver specific double contrast MRI scanning were performed in all patients. Prior to surgery, each case was individually evaluated at an open multidisciplinary team meeting with sur-
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Table 1. Indication for surgery and histology
Main indication for surgery (n = 46 patients) Presence of symptoms (pain, palpable mass/ discomfort, GORD, infection/sepsis) 23 (50) Preoperative diagnosis of adenoma or cystadenoma 13 (28) Uncertain preoperative diagnosis 10 (22) Histology (n = 50 specimens) Adenoma Cystadenoma FNH Simple cyst Complex cyst Hydatid cyst Haemangioma Miscellaneous1
13 (26) 4 (8) 10 (20) 11 (22) 6 (12) 1 (2) 1 (2) 4 (8)
Figures in parentheses are percentages. GORD = Gastro-oesophageal reflux disease; FNH = focal nodular hyperplasia. 1 One patient with benign oriental cholangiopathy, 2 patients with benign intrahepatic biliary stricture causing recurrent infections, and 1 post-traumatic liver resection.
geons, pathologists, oncologists, gastroenterologists and radiologists in our centre. Patients were assessed for indication, feasibility and the type of resection required, prior to a decision regarding the surgical approach. Surgical indications included preoperative diagnosis of adenoma or cystadenoma, presence of symptoms, and uncertain diagnosis on imaging or biopsy (in particular when it was not possible to exclude cancer). Only lesions remote from the inferior vena cava, the middle hepatic vein and liver hilus were considered potentially suitable for a laparoscopic resection. Patients undergoing hepatic cyst de-roofing were not considered. Two laparoscopic hepatobiliary-pancreatic surgeons (M.A.H. and N.W.P.) were involved in this series and standard nomenclature was used to describe the resection performed [33]. Pure laparoscopic procedure was attempted in all patients. No hand-assisted or ‘hybrid’ techniques [26] were used. Our group have previously described the technique for left lateral sectionectomy, major hemi-hepatectomy and segmentectomies [8, 11, 24]. Median values and range were considered for continuous variables when their values’ distribution was skewed.
Results
Between August 2003 and December 2009, 178 patients underwent LLR in our unit. Of them, 46 patients (33 female and 13 male) underwent 50 LLRs for benign diseases. The median age of the patients was 48 years Abu Hilal/Di Fabio/Teng/Godfrey/ Primrose/Pearce
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Table 2. Patients with uncertain preoperative diagnosis
Patient
Age
Year of surgery
Previous cancer
Indication for surgery
Pathology
J.A. C.B. E.H. B.L. B.A. J.W. S.E. A.K. S.S. J.M. P.S.
21 23 59 48 75 34 64 35 62 52 37
2003 2004 2005 2006 2006 2006 2006 2007 2007 2008 2008
no no colorectal no no no breast no no colorectal no
uncertain diagnosis (adenoma?) pain, uncertain diagnosis liver metastasis? pain, uncertain diagnosis HCC? HCC? liver metastasis? uncertain diagnosis pain, weight loss, uncertain diagnosis liver metastasis? pain, dyspepsia, uncertain diagnosis
HCC1 FNH FNH FNH adenoma adenoma hemangioma FNH FNH FNH cyst
HCC = Hepatocellular carcinoma; FNH = focal nodular hyperplasia. 1 Patient not included in the analysis of laparoscopic resections for benign liver disease.
(range 16–75 years) with a quarter of the study population aged less than 35 years (table 1). The main surgical indication was the presence of symptoms (50%), followed by preoperative diagnosis of adenoma or cystadenoma (28%), and uncertain diagnosis on imaging or biopsy (22%). Regarding adenomas (median size 85 mm, range 25– 180 mm) indications for surgery were: symptoms (n = 10), impossibility to rule out malignancy (n = 2), and preoperative diagnosis of large adenoma (15 cm) (n = 1). Symptoms were related to adenoma rupture in 8 patients and mass effect in one case (shoulder tip pain). The indications for surgery for hepatic cysts were: symptoms in 11 cases, presence of complex cyst in 6 cases, and hydatid cyst in one case. Most of these cysts were not amendable for fenestration as they were peripheral and within liver parenchyma, hence resection was considered an easier and less risky option. Among the symptomatic patients, we included a 16-year-old patient who had a blunt abdominal trauma after a bike fall, causing liver lesion of segment 2 and 3 and subsequent biliary peritonitis. He underwent a successful left lateral hepatic sectionectomy. Definitive histology of the liver specimens resected is described in table 1. The preoperative diagnosis was uncertain in 11 cases, and more than a third of these patients had 35 years or less. A 21-year-old female had an incidental ultrasound finding of a segment 2–3 lesion suspected to be an adenoma. She underwent laparoscopic left lateral sectionectomy with a histological diagnosis of hepatocellular carci-
noma (HCC). This case was not included in the present analysis of LLR for benign liver disease. The remaining 10 patients had histological diagnosis of benign lesions [adenoma n = 2, focal nodular hyperplasia (FNH) n = 6, cyst n = 1, hemangioma n = 1]. The patient with the cyst and 3 of 6 patients with FNH had associated symptoms as well. Three other patients were followed up after previous surgery for colon or breast cancer and a liver metastasis could not been excluded. The characteristics of patients with uncertain preoperative diagnosis are summarized in table 2. The types of resections performed were: wedge resection (n = 10), single sectionectomy (n = 6), bisegmentectomy (n = 3; two 5–6 and one 6–7 bi-segmentectomies), left lateral sectionectomy (n = 18), right hemi-hepatectomy (n = 7) and left hemi-hepatectomy (n = 6). Conversion to an open procedure (right hemi-hepatectomy) was necessary in one patient (2%) due to bleeding. This patient had a large complex cyst of the right lobe causing recurrent infections. The median operative time for pure laparoscopic procedures was 165 minutes (range 55–375 min). Preparation was made for a laparoscopic Pringle manoeuvre by positioning a Nylon tape around the portal triad, passing it through a 10-cm-long 14-Fr rubber tube and left loose within the abdominal cavity. The tape was positioned in all cases but was only required in 18 (39%). Median blood loss was 200 ml (range 10–1,800 ml). Only 1 patient (2%) required blood transfusion intra-operatively. The median size of the excised lesions was 48 mm (range 5–180 mm). In patients undergoing major hepa-
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tectomy the median size of the resected lesion was 88 versus 43 mm in patients who had a minor hepatectomy. Four patients did not have a defined mass lesion: two patients had benign intra-hepatic biliary stricture causing recurrent cholangitis, one had oriental cholangiopathy presenting with sepsis and the final one case had a posttraumatic liver resection. There were three post-operative complications in our series (7%): a bile leak treated with CT-guided drainage (after a right hemi-hepatectomy); a massive postoperative (adynamic) ileus which warranted an exploratory laparoscopy on postoperative day 3 as a mechanical obstruction could not be excluded by CT scan (after a right hemihepatectomy); one pleural effusion (after a left lateral sectionectomy). Mortality was nil. The median hospital stay was 3 days (range 1–10 days) and the median HDU stay was 1 day (range 0–5 days).
Discussion
Since Gagner’s team performed the first LLR in 1992 [12], laparoscopic liver surgery has been widely discussed with debate focusing on feasibility, safety, oncological efficiency and surgical indications. The first two issues were addressed early in the first part of this decade [2, 15–17] and oncological efficiency has been recently demonstrated [1, 21–25]. However, surgical indications continue to raise concerns especially for the treatment of benign liver lesions. Many authors stress that indication for liver resection should not be changed or widened due to the availability of the minimally invasive approach [7, 26, 34]. These concerns have been raised due to the observation that LLRs were mostly performed for benign disease, as reported in major case series [6, 7, 32]. However, initial resistance in the use of laparoscopy for the treatment of liver malignancies may have been the consequence of caution when data regarding oncological efficiency were still lacking. In addition, a sensible patient selection could have played a role, as livers with benign disease are expected to be less technically demanding. Our data confirm that most of our patients underwent LLR for HCC and colorectal liver metastases, while only 29% had the procedure for a benign disease. However, our experience started at the end of the first half of this decade, when LLR had already gained acceptance in the treatment of malignant lesions, and in the era of noticeable development in diagnostic radiology leading to a better preoperative characterization of liver lesion. Our indications were in line with the 4
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worldwide-agreed criteria: preoperative diagnosis of adenoma or cystadenoma, presence of symptoms, and uncertain diagnosis on imaging or biopsy (in particular when is not possible to exclude cancer) [1]. While the first two indications can be straightforward, lesions with uncertain diagnosis may represent a clinical dilemma. In our series, approximately a fifth of patients had uncertain preoperative diagnosis. Of these, 27% had malignant or pre-malignant lesions (table 2). A 21-year-old patient with a suspected adenoma had a definitive histological diagnosis of HCC. Three other patients were followed up after previous surgery for colon or breast cancer and a liver metastasis could not been excluded, while the remaining ones had uncertain diagnosis of adenoma or cystadenoma. Four of 11 patients with indeterminate diagnosis were symptomatic, and the presence of symptoms per se an indication for excision of a benign liver lesion [26]. In a previous single-centre large case series published by Cherqui et al. [32], uncertain preoperative diagnosis was reported in 58% of cases. Particularly for FNH, uncertain diagnosis was reported in 15 of 22 lesions. The risk of missing a malignancy on one hand and the risk of carrying out an unnecessary procedure on the other often involve a difficult clinical decision. Optimal individual treatment must always be discussed in a multidisciplinary meeting including a liver surgeon, hepatologist, oncologist, and radiologist with specific competence. Clearly, advancement of technology leading to continuous improvement of preoperative imaging is expected. Benign liver lesions tend to be more frequent in younger individuals [30, 32] and our data shows that a quarter of our study population were aged less than 35 years. An extensive laparotomy for liver resection in a young patient may be a devastating event, potentially causing deleterious psychological consequences and social life impairment. Although there are no specific studies analyzing quality of life after LLR, cosmetic results and early return to social life should not be perceived as surrogate parameters, but as relevant end-points to pursue [35], as long as safety is not minimally compromised. We report a 28% rate of major liver resections confirming that even when major hepatectomies are needed these can be performed with a pure laparoscopic approach. The extensive use of the pure laparoscopic approach may explain the short hospital stay we observed, which is one of the main benefits of the minimally-invasive surgery. Longer hospital stays after major LLR for benign disease reported by other authors may be explained by the routine adoption of hand-assisted approach [32]. Abu Hilal/Di Fabio/Teng/Godfrey/ Primrose/Pearce
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Conclusion
The laparoscopic approach represents a safe and feasible option for the management of benign and indeterminate liver lesions in expert hands. It can be performed
with excellent results even when major hepatectomies are required. However, surgical indications for benign liver lesions are well established and should not change for the mere availability of a minimally invasive approach.
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