Laparoscopic Resection of Benign Hepatic Cysts: A New Standard T Clark Gamblin, MD, MS, Shane E Holloway, MD, Jason T Heckman, MD, David A Geller, MD We sought to evaluate the feasibility and outcomes of laparoscopic resection of symptomatic hepatic cysts. STUDY DESIGN: Fifty-one patients underwent laparoscopic resections for symptomatic hepatic cysts. Resection was accomplished laparoscopically with an Endo-GIA vascular stapler. Data were collected in a prospective database. RESULTS: Median patient age was 60 years, with a median lesion diameter of 13 cm. Indication for surgical treatment was pain in 92% of patients. Laparoscopic resection was successful in 100% of patients. A pure laparoscopic approach was used in 58% of patients, the remaining used a hand port. Median operating time was 178 minutes. Preoperative diagnosis was polycystic liver in 88% and simple cyst in 12% diagnosed by preoperative imaging. Histologic examination showed 90% to be simple cysts and 10% cystadenomas. There were nine minor perioperative complications. Median hospital stay was 2 days. Relief of symptoms was achieved in all patients operated on for pain, with a median followup of 13 months. Two patients required reoperation for recurrence of the same cyst. CT or MRI was used for yearly followup. CONCLUSIONS: Laparoscopic resection of symptomatic liver cysts is a feasible and effective method to relieve symptoms with minimal surgical trauma. This series represents the largest report of laparoscopic management for benign hepatic cysts and provides evidence for a routine laparoscopic approach to benign symptomatic cysts. Traditional surgical methods should be reserved for when a malignancy is expected, laparoscopy is contraindicated, or for recurrence after an initial laparoscopic approach. (J Am Coll Surg 2008;207:731–736. © 2008 by the American College of Surgeons) BACKGROUND:
reported in multiple small case series.5,10-16 We report the largest single-institution experience to date with laparoscopic resection of symptomatic nonparasitic liver cysts.
Nonparasitic hepatic cysts are present in approximately 4% to 7% of the general population.1 Up to 24% of these cysts can become symptomatic.2 Symptomatic cysts most commonly cause pain, jaundice, or nausea. Large asymptomatic cysts can rarely rupture, resulting in hemorrhage; generally, they are not resected but rather observed.3,4 Many treatments have been proposed for treatment of symptomatic hepatic cysts and include aspiration, aspiration followed by injection of sclerosing agents, enucleation, hepatic resection, and liver transplantation.5-8 The technique of unroofing the hepatic cyst was originally described by Lin and colleagues in 1968.9 Minimally invasive surgery developments in recent years have made a laparoscopic approach to these symptomatic cysts feasible, as has been
METHODS Between August 2001 and February 2008, 51 patients underwent laparoscopic resection for symptomatic hepatic cysts. Data were collected in a prospective database under Institutional Review Board approval. Cyst size was determined by preoperative CT or MRI and recurrence was evaluated by followup CT scan (Fig. 1). Surgical technique
Pure laparoscopic and hand-assisted techniques were used, based on location and size of the cyst. All patients were placed in supine positions, and a Foley catheter and nasogastric tube were placed immediately after induction. For those patients who underwent resection without use of a hand port, the initial port was placed in the supraumbilical midline using an open Hasson technique. Placement of the remaining two ports was then determined by the side of the dominant cyst. A 5-mm port was placed in the midclavicular line on the side opposite the dominant cyst for retrac-
Disclosure Information: The following disclosures have been reported by the authors: Dr Gamblin has received honoraria from Coviden, Aloka, and Bayer for speaking; and Dr Geller has received honoraria from Coviden, Aloka, and Bayer for speaking, and Applied Medical for consulting. Received April 28, 2008; Revised July 1, 2008; Accepted July 8, 2008. From the Department of Surgery, Liver Cancer Center, University of Pittsburgh, Pittsburgh, PA. Correspondence address: T Clark Gamblin, MD, Liver Cancer Center, University of Pittsburgh, 3459 Fifth Ave, 7 South, Pittsburgh, PA 15213.
© 2008 by the American College of Surgeons Published by Elsevier Inc.
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Figure 2. Port placement for laparoscopic cyst resection in central and right-sided cysts. For left-sided cysts, the 5-mm and 12-mm midclavicular port site positions are reversed.
Figure 1. Computed tomography imaging of solitary giant hepatic cyst. (A) A 19-cm hepatic cyst occupies the left lateral segment of the liver. (B) Three years after laparoscopic resection there is no recurrence.
tion and exposure. One 12-mm port, for use of the reticulating Endo-GIA (Autosuture) vascular stapling device, was placed in the midclavicular line at the level of the supraumbilical port on the ipsilateral side of the dominant cyst. For resections in which a hand port was used, the hand port was placed in the midline supraumbilical position, with the remaining 2 ports in the position of the pure laparoscopic approach (Fig. 2). Initially, hand ports were placed in almost all patients to aid in mobilization of the liver, especially the right lobe. As our experience with laparoscopic liver resection increased, we rarely used hand ports, except for lesions located centrally or very posterior in the right lobe, requiring extensive hepatic mobilization. Placement of the initial port in the supraumbilical position
allowed adequate visualization of both right- and left-sided cysts, including those in segments 6, 7, and 8. Even with large cysts that extend low in the abdomen, the previously mentioned port placement was used. If the ports were placed in a lower position, visualization and resection could be difficult. A 10-mm, 30-degree laparoscope was typically used to maximize visualization. The initial step involved fenestrating the cyst in the center using endoshears and aspiration of the entire cyst contents. The cyst wall was then resected at the parenchymal junction using the EndoGIA vascular stapler or Ligasure (Valleylab), or both, switching the stapler and camera between the 2 12-mm ports to obtain the best angle for resection of the cyst wall. The back wall of the cyst was carefully examined for evidence of a bile leak, and, if identified, this was sutured using absorbable monofilament suture. The internal cyst wall was left intact, with no additional treatment if there was no bile leak identified. The resected cyst wall was removed through placement into an Endobag (Autosuture) and was routinely sent for permanent, not frozen, histopathologic evaluation. A #10 Jackson-Pratt (JP) drain was placed within the cyst cavity, exiting through the 5-mm port site. The 12-mm port site was closed with a fascial closure device. JP drains were typically removed the day of discharge.
RESULTS Median patient age was 60 years (range 31 to 86 years). Eleven patients were men and 40 were women. Median
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cyst diameter was 13 cm (range 2 to 21 cm), with indications for surgical treatment being pain in 92% of patients and the remaining 8% having operations for jaundice, elevated liver function studies, or early satiety. Median diameter of the lesions was 13 cm (range 4 to 21 cm). Laparoscopic resection was successfully performed in all patients, with no conversions to open resection; all patients were approached laparoscopically during the time period of the study. Fifty-eight percent of patients were resected with a pure laparoscopic approach (3 trocars), and 42% of patients used a hand port because of size or location of the cyst. Median operating time was 178 minutes (range 54 to 380 minutes). Operative times trended downward as operative experience increased, with median operating time being 214 minutes for the first 25 patients in the series, compared with a median of 137 minutes for the subsequent 26 patients. Use of hand ports also declined with time. Of the first 25 patients, 60% had a hand port used, compared with only 20% of the last 26 patients. We completed our last 17 resections without use of a hand port. Twenty-two percent of patients had concomitant cholecystectomies either because the gallbladder abutted the cyst or because they had symptomatic cholelithiasis. In patients in whom concomitant cholecystectomies were performed, the cyst was fenestrated early if it prohibited a critical view of the cystic artery and duct. Conversely, if a critical view could be obtained without initial fenestration of the cyst, division of the cystic duct and artery and the gallbladder preceded removal of the cyst wall. Thirty-eight percent of cysts had bilious contents, but only one biliary tree communication was identified and sutured intraoperatively. On histologic examination of the cyst wall, 90% were simple cysts and 10% were cystademonomas with no cystadenocarcinomas identified. There were 9 intraoperative or postoperative complications, none of which required immediate reoperation or substantial morbidity, and 90-day mortality was 0. Median hospital stay was 2 days (range 1 to 11 days), with a mean stay of 2.9 days. Complete relief of symptoms after operation was achieved in all patients operated on for pain during postoperative followup of 13 months (range 1 to 49 months). Only 2 patients required reoperation for recurrence of the same cyst (4%); these were large central cysts that extended from the dome of the right lobe to the caudate lobe and also showed features of cystadenoma on final pathology. These were managed by performing right hepatectomies. There were no operative transfusions, and there were no postoperative bile leaks. A JP drain was placed in all patients and was removed before discharge in all patients. Postoperative pain was managed with oral opioids.
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DISCUSSION Pathogenesis of solitary benign hepatic cysts is most likely the result of a congenitally aberrant intrahepatic biliary duct that enlarges with time. Cystic neoplasms are acquired and the cause is unknown.14,17,18 Simple cysts are found in approximately 1% of large autopsy series and the incidence has been reported to be between 4.5% and 7% in reviews of imaging studies, including ultrasonography and CT.1,16 Few of these cysts ever enlarge and still fewer cause symptoms, with 80% to 95% remaining asymptomatic.2 Those patients with asymptomatic benign liver cysts require no treatment unless diagnosis is uncertain. Concerning features on imaging that would warrant possible intervention include septations and internal echogenic content.17 The mass effect of the enlarging cyst typically causes the presenting symptoms. In the majority of patients, results of liver function tests are within the normal range.19 Symptomatic cysts occur more commonly in women and present often in the fourth decade of life or later, as was evidenced in our series.17,18 Abdominal mass or pain are the most common presenting symptoms. Nausea, vomiting, early satiety, fatigue, and jaundice present less frequently.17 Diagnosis of hepatic cyst is easily made by ultrasonography, CT, and MRI. Because few present with symptoms, the majority of cysts are an incidental finding discovered by workup or surveillance for an unrelated reason.20 CT is superior to ultrasonography in determining the location and spatial relationship between the cyst and surrounding structures. Biliary cystadenoma can be differentiated from a simple cyst occasionally by internal echogenic content or septations on imaging studies.17 Biliary cystadenomas in our series were diagnosed preoperatively as simple hepatic cysts, it was only on final pathology that they were identified as cystadenomas. If, on preoperative imaging, these lesions had been diagnosed as cystadenomas, the planned therapy would have been surgical resection, as this is the recommended therapy secondary to their malignant potential. Patients are counseled preoperatively that their lesions appear to be benign but, if on final pathology a malignancy is identified, they might require additional operation. For those patients in our series who were found to have cystadenomas on final pathology, no additional intervention was taken and they are followed with an annual CT scan. If symptoms are present and attributed to the cyst, intervention is indicated. Ultrasonography-guided percutaneous aspiration alone is associated with a recurrence rate approaching 100%.21 Installation of a sclerosant (ie, alcohol) into the cystic cavity has been shown to be more effective but still with recurrence rates of 17%.18,22 Up to 24% of patients with symptomatic solitary cysts eventually re-
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quire surgical intervention. Since Lin and colleagues9 introduced the technique of unroofing the cyst and internal drainage into free peritoneal cavity, it has become the standard treatment of symptomatic polycystic and simple cysts of the liver. Current technology has now allowed a minimally invasive approach to unroof the cysts. Vogl and colleagues19 recommend that interventional radiologic methods be used only for patients with comorbidities considered high risk for surgical intervention. Cysts should be aspirated intraoperatively and fluid examined. Complete decompression of the cyst also serves as an aid in resection. The cyst wall is sent to pathology for evaluation by permanent sectioning to rule out a neoplastic process; frozen sections are not sent. Cyst excision is performed near the hepatic parenchyma; removing the entire cyst wall is not necessary.17 The cyst is allowed to drain freely into the peritoneal cavity. Previous reports have noted the most common reason for recurrence is inadequate collapse of the cavity, so wide fenestration or resection is necessary to prevent adhesion of the cyst wall and refilling of the cyst.23 Hemostasis is easily achieved using bovie cautery and Tissue-Link floating ball (Salient Surgical Technology). If a bile leak is noted at the cystic wall, the duct is sutured or clipped. The initial fenestration of the cyst should bisect the anterior surface, and then the two halves of the cyst’s front wall should be stapled circumferentially, preserving the back wall. At completion, all 10-mm trocar sites should be sutured closed to avoid incision hernias. We placed a #10 JP drain in all patients but found only 1 biliary communication and had no bile leaks. One could make a strong argument for more selective use of JP drains. Several authors have recognized cysts located in anterior segments and peripheral cysts as most easily accessible to a laparoscopic approach and caution difficulty in segment VI, VII, and IVa cysts.12,15 Although more challenging, we have approached these cysts laparoscopically as well and have used a hand port if necessary. In our experience, cysts that recur after laparoscopic resection were those centrally located, extending from the caudate to the dome. The 4% recurrence rate in our series is similar to that found in the largest earlier laparoscopic series by Hansman and colleagues.24 To avoid recurrence, one must resect as much of the wall as possible to prevent closure of the remnant wall and reaccumulation of cyst fluid. Also, patients with centrally located cysts should be counseled that the recurrence rate is higher when resected laparoscopically. In those patients with polycystic liver disease, we reserved operations for symptomatic patients only and resected the dominant cyst that abutted the liver surface. These patients clearly continue to have cystic lesions in their liver postoperatively
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but had excellent relief of their symptoms, and the resected cysts did not recur to date. Several other series have shown recurrence of these symptoms in many patients with polycystic liver disease,24,25 but we did not see this in our experience, although our median followup is shorter. Patients were followed with annual CT scans to evaluate for recurrence. The laparoscopic approach to these cysts carries several important advantages that have been noted previously, including reduced postoperative pain, early mobilization, no ileus, short hospital stay, rapid recovery, and cosmetic benefits.5 Although we do not have a series of open cyst resections at our institution to compare with laparoscopically resected patients, there is literature that shows shorter hospital stays, decreased blood loss, and equivalent outcomes for laparoscopic liver resections.26 We recently published a series of 100 consecutive open right hepatectomies, procedures performed by the same surgeons as this series, and mean hospital stay was 6 days.27 There is also an abundant body of literature showing decreased postoperative pain and narcotic use when equivalent operations can be completed laparoscopically rather than open.28,29 We do not advocate complete resection of the cyst, because it is not necessary and carries substantial risk to the patient.10 We do not treat the internal cyst wall with argon beam coagulation or any device other than assuring there is no evidence of a biliary leak. The internal cyst wall often overlies portal and hepatic venous structures. There is no clear evidence that for benign cysts treatment with argon beam coagulation, glue, or any other technique will decrease recurrence rates. As such, we believe the risks of treatment are greater than any benefit gained. There is also a risk of air embolism with use of argon beam in the laparoscopic setting, and, as such, we choose not to use this during laparoscopic procedures.30 It has been suggested that placement of omentum into the cyst cavity can reduce recurrence rates,14,31,32 but we did not place omentum into the cyst cavity and had similar, if not lower, recurrence rates than other series. In theory, placement of omentum in the cyst cavity could allow resequestration of fluid within the remaining cyst or make reoperative procedures more challenging. Hydatid cysts were not included in our series and, as is the case in most institutions in the US, are rarely encountered. Management of these cysts can be complicated, and surgical treatment in the opening setting can be challenging. In a series of six patients by Katkhouda and colleagues,15 four patients had complications with laparoscopic resection. Currently, based on their experience and lack of reported laparoscopic management, we would recommend open surgical intervention if an operation is necessary.
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Other laparoscopic procedures can be performed safely at the same time as laparoscopic cyst resection. Twenty-two percent of our patients underwent concomitant cholecystectomy. Other series have also reported simultaneous procedures, cholecystectomy being the most common.33,34 Inclusion of a second procedure did not add any morbidity or prolong the hospital course in our experience. For those patients in whom laparoscopic resection/ fenestration does not appear feasible because of location of the cyst or contraindications to laparoscopy, liver resection is a reasonable option.6 In conclusion, laparoscopic resection of symptomatic liver cysts is a simple and effective method to relieve symptoms with minimal surgical trauma. Adequate preoperative selection of patients and meticulous technique are mandatory. We recommend removing the majority of the cyst but do not pursue resection of the posterior wall adjacent to portal structures or hepatic veins. In our experience, which represents the largest reported series, this approach to hepatic cysts has resulted in minimal postoperative pain, short hospital stays allowing for early return to normal activity, resolution of symptoms, and a low recurrence rate. There continues to be an increasing body of literature supporting the equivalency of many laparoscopic and open procedures with regard to outcomes and advantages in avoiding a laparotomy, especially in benign disease. We propose minimally invasive cyst excision as the standard of care for management of these benign hepatic cysts. Author Contributions
Study conception and design: Gamblin, Holloway, Heckman, Geller Acquisition of data: Gamblin, Holloway Analysis and interpretation of data: Gamblin, Holloway, Heckman, Geller Drafting of manuscript: Gamblin, Holloway, Geller Critical revision: Gamblin, Holloway, Heckman, Geller
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