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Original Article |

Laparoscopic Localization and Resection of Insulinomas FREE

Dawn E. Jaroszewski, MD; Richard T. Schlinkert, MD; Geoffrey B. Thompson, MD; Denise K. Schlinkert, RN
[+] Author Affiliations

From the Division of General Surgery, Mayo Clinic, Scottsdale, Ariz (Drs Jaroszewski and Schlinkert and Ms Schlinkert); and the Division of Gastroenterologic and General Surgery, Mayo Clinic, Rochester, Minn (Dr Thompson).


Arch Surg. 2004;139(3):270-274. doi:10.1001/archsurg.139.3.270.
Text Size: A A A
Published online

Hypothesis  Laparoscopic localization and resection of insulinomas are feasible and safe and may decrease morbidity and the length of hospitalization.

Design  Case series identified through retrospective medical record review.

Setting  Mayo Clinic, Scottsdale, Ariz, and Rochester, Minn, a single-institution tertiary care medical center.

Patients  Nine patients (6 men and 3 women; mean age, 54 years) who underwent attempted laparoscopic insulinoma resection between September, 1997, and April, 2002.

Interventions  Laparoscopic localization and resection of insulinoma tumors of the pancreas.

Main Outcome Measures  Intraoperative complications, conversion to open laparotomy, and length of hospitalization.

Results  Preoperative localization was successful in 5 patients (56%). Four conversions to open exploration were required because of an inability to identify the tumor (n = 3) or to perform a safe laparoscopic resection owing to proximity to the portal vein (n = 1). Laparoscopic intraoperative ultrasonography facilitated identification of lesions (mean tumor size, 2.1 cm) in 4 (80%) of 5 patients; 3 patients underwent successful laparoscopic resection. Average hospital stay was shorter after laparoscopic resection (4.5 vs 7.0 days in uncomplicated cases). At follow-up (mean, 29 months; range, 3-57 months), 1 patient who underwent laparoscopic enucleation had recurrent hypoglycemia.

Conclusions  Laparoscopic localization and resection of insulinomas are feasible and safe. Laparoscopic ultrasound aids successful insulinoma localization and laparoscopic resection. Preoperative localization is not required, but previous knowledge of tumor location helps focus intraoperative ultrasound and limit pancreatic mobilization. Excluding patients with pancreatic leaks (observed in both groups), hospital stay and time to recovery may be shortened by using laparoscopic insulinoma resection.

Figures in this Article

Insulinoma is the most common functional neuroendocrine tumor of the pancreas,1,2 with an incidence of 4 per million person-years.3 Patients often initially have symptoms of neuroglycopenia (eg, confusion, somnolence, and visual disturbances) and hypoglycemia-induced catecholamine release (eg, tachycardia, sweating, and tremor). Diagnosis is confirmed biochemically during a supervised 72-hour fast. A diagnosis of insulinoma is made in symptomatic patients who demonstrate hypoglycemia, an inappropriate insulin level, and increased concentrations of C peptide.1,3 Plasma screening results for both classes of sulfonylureas must be negative during end-of-fast studies.

In most patients, the lesions are solitary, benign, and intrapancreatic (Figure 1, A). Excision of the insulinoma is the treatment of choice. Ninety percent of these tumors are benign and can be treated with simple enucleation (Figure 1B).1 At Mayo Clinic, 62% of nearly 200 insulinomas were enucleated.

Place holder to copy figure label and caption

A, Solitary, benign, intrapancreatic insulinoma. B, Simple enucleation of an insulinoma. C, Localization of an insulinoma with laparoscopic intraoperative ultrasonography.

Graphic Jump Location

The advantages of minimally invasive procedures are well known, and technical advances in laparoscopic surgery have led to its increasing use in the treatment of pathologic intra-abdominal conditions. Advanced laparoscopic techniques have been used to resect islet cell tumors in a few patients worldwide.410 Patients who undergo open exploration of the pancreas have considerable postoperative pain, resulting in extended hospitalization. Laparoscopic pancreatic procedures should shorten hospital stays and possibly decrease patient morbidity.

Frequently, preoperative localization of an insulinoma is not possible. In a few highly selected patients, intraoperative ultrasonography (IOUS) has been reported to be more sensitive than preoperative US and other intraoperative techniques for localizing insulinomas.1113 In most such cases, IOUS can be used to localize insulinomas more precisely and, thus, to facilitate safe resection (Figure 1C).1114

We describe our experience with laparoscopic localization and resection of insulinomas of the pancreas, and we review the reported success with this procedure at other institutions.

Nine patients underwent attempted laparoscopic resection of insulinomas between September 1997 and April 2002 at Mayo Clinic (6 patients were treated in Scottsdale and 3 were treated in Rochester, Minn). The diagnosis of insulinoma was made using a supervised 72-hour fast. All 9 procedures were initiated with the laparoscope, and laparoscopic IOUS (LIOUS) was conducted in 5 of the 9 patients. A review of the clinical records examined the variables of age; sex; preoperative localization studies; location, type, and site of the insulinoma; type of procedure; operative time; postoperative stay; morbidity; use of IOUS or LIOUS; and follow-up for recurrence. Additional follow-up was provided by telephone and written contact with patients.

Two surgical approaches were used. Three of the 9 patients underwent planned laparoscopic distal pancreatectomy. They were placed in the lateral decubitus position, and 3 trocars (10 mm) were used along the left subcostal region to facilitate the planned distal pancreatectomy. For distal pancreatectomy, the pancreas was dissected carefully away from the splenic vessels. The tail of the pancreas was freed and transected with a linear stapler. Six patients underwent planned pancreatic exploration and enucleation of the insulinoma if possible. They were placed in the dorsal lithotomy position, and 5 or 6 trocars were used. The lesser sac was opened by dividing the gastrocolic ligament with ultrasonic shears (Ethicon LCSC5; Ethicon Endosurgery, Cincinnati, Ohio). Attachments between the pancreas and the posterior aspect of the stomach were separated. When available, a 5-MHz laparoscopic ultrasonic probe (model 8566-S; B-K Medical Systems, Wilmington, Mass) was used to scan the pancreas. Enucleated tumors were removed in a bag through the 10-mm trocar site. One or 2 drains were left in the pancreatic vicinity.

Nine patients (6 men and 3 women) underwent attempted laparoscopic surgical treatment of insulinomas. Mean patient age was 54 years (range, 34-73 years). These tumors were located in the uncinate process (1 patient), the proximal body (2 patients), the junction of the tail and the body (2 patients), or the tail of the pancreas (4 patients). Mean tumor size was 2.1 cm (range, 1.5-3.0 cm).

Preoperative imaging was conducted in 8 patients (Table 1). Computed tomography (CT) in 7 of 9 patients showed evidence of a mass or "fullness" in the pancreas in 3 patients (43%). In 1 patient, an octreotide scan failed to show any areas of abnormal activity. Endoscopic US in 1 patient accurately identified the lesion. One patient had abdominal US findings that showed a mass; however, subsequent CT findings were negative.

Table Graphic Jump LocationTable 1. Localization and Surgical Procedures for Pancreatic Tumors in 9 Patients

Lesions were identified visually in 5 patients, and LIOUS was available to confirm visual findings for only 2 of these 5. Both patients underwent successful laparoscopic procedures (2 enucleations). Two other patients underwent planned laparoscopic distal pancreatectomy for tumor resection. The fifth patient had an apparent lesion at the superior border of the pancreas that could not be differentiated clearly from the splenic artery. Conversion to an open procedure showed that the lesion was an insulinoma resting on the portal vein.

Four patients did not have visible tumors. Laparoscopic IOUS was available for use with 3 of these patients and facilitated the identification of lesions in 2. One lesion was successfully enucleated from the tail of the pancreas. In the second patient, a lesion in the uncinate process adjacent to the superior mesenteric vein required conversion to celiotomy to facilitate safe dissection. The third patient had no lesion visualized, and findings with LIOUS were negative. At conversion to celiotomy, an insulinoma was palpated at the distal tail of the pancreas in the splenic hilum. Subsequent IOUS verified this lesion. For the fourth patient with no visible tumor, LIOUS was not available. Preoperative endoscopic US identified a lesion in the tail of the pancreas, and the patient underwent laparoscopic distal pancreatectomy. The specimen did not contain the lesion, and the operation was converted to celiotomy. The lesion was found proximal to the line of transection and was removed using further proximal resection.

The mean operative time was 215 minutes (range, 160-285 minutes) for the laparoscopic approach and 203 minutes (range, 179-225 minutes) for procedures converted to celiotomy. The average hospital stay was 9.4 days (range, 2-29 days) for patients whose lesions were resected laparoscopically (Table 2) and 11.8 days (range, 5-26 days) for patients whose surgical procedures were converted to celiotomy (Table 3). Excluding 1 patient in each group with a pancreatic leak, the average hospital stay was 4.5 days after laparoscopic surgery and 7.0 days after celiotomy.

Table Graphic Jump LocationTable 2. Laparoscopically Resected Insulinomas
Table Graphic Jump LocationTable 3. Outcomes of 4 Conversions to Celiotomy

Three patients had early postoperative complications, 2 of which were due to postoperative pancreatic leaks. One leak occurred after laparoscopic enucleation of a lesion, and the other occurred after open distal pancreatectomy. Both leaks resolved with conservative therapy. The third patient was hospitalized for 9 days because he experienced persistent fever of unknown cause and an elevated white blood cell count after open enucleation of a lesion.

Patient follow-up was 3 to 57 months (mean, 29 months). Eight patients remained asymptomatic. One patient who had laparoscopic enucleation was hyperglycemic in the immediate postoperative period and had recurrent hypoglycemia at 6-week follow-up. Biochemical testing results suggested recurrent disease, but CT findings did not reveal an insulinoma. No additional surgical treatment was undertaken. This patient's symptoms were minimal, and his blood glucose concentrations remained stable with use of diazoxide (50 mg twice daily).

Benign insulinomas of the pancreas are ideally suited for laparoscopic resection. They generally are singular, small, and well encapsulated.7 With advancing technology and increasing surgical experience, laparoscopic resection of the pancreas undoubtedly will contribute increasingly to the care of patients with benign insulinomas. Laparoscopic resection is technically demanding and, thus, is challenging even for experienced surgeons with advanced laparoscopic skills.

The lack of tactile sensation during laparoscopic surgical procedures for insulinoma is a concern. Detection of an insulinoma during a laparoscopic procedure depends solely on visualization or the use of LIOUS. In all but 1 of our patients, LIOUS helped localize and resect the tumors.

Similar results have been reported from other series. Berends et al5 found that LIOUS failed to localize insulinomas in 1 of 10 patients, and Gagner et al4 were unable to visualize 2 of the 5 insulinomas with LIOUS in their series. In our patients, the size of the tumor did not always correlate with successful intraoperative localization. The largest lesion (3.0 cm) was not identified with LIOUS but was identified by manual palpation after conversion.

Preoperative knowledge of tumor location helps focus US localization and limits mobilization and exposure of the pancreas.11,13,15 Yet, the use of preoperative imaging techniques for insulinomas is controversial. Many techniques to localize insulinomas have been described, and there is a wide range of reported accuracy with each one. Detection rates of transabdominal US and CT are lower than 50% to 60%.11,1517 Spiral CT has improved this sensitivity considerably.17 Magnetic resonance imaging has identified 45% to 91% of insulinomas in several series.11,1719 Endoscopic US seems to be even more sensitive, with preoperative detection rates of 86% to 93%.16,2022 Invasive techniques such as percutaneous transhepatic venous sampling for insulin are successful in 70% to 95% of cases, and arterial stimulation and venous sampling for insulin identify insulinomas in 75% to 80% of patients.11,13 Laparoscopic IOUS complements preoperative localization techniques and generally yields excellent results.1114

The patient benefits of minimally invasive surgical procedures are well known. Patients successfully treated in our series realized the advantages that laparoscopic surgery offers over upper abdominal incisions, and they visibly experienced less postoperative pain. By excluding patients with pancreatic leaks, the hospital stay for patients who had undergone laparoscopic resection was shorter than that for patients whose laparoscopic procedure was converted to open exploration (4.3 days vs 7.0 days). However, if patients with pancreatic leaks are included (9.4 days vs 11.8 days), the average stay for patients with laparoscopic procedures improved only slightly. Pancreatic leaks are a well-known complication of pancreatic operations. We noted a pancreatic leak in 1 patient in the laparoscopic group and in 1 in the open group. The patient whose procedure was converted had undergone a distal pancreatectomy, whereas the laparoscopic patient had undergone enucleation of a 1.7-cm tumor in the tail of the pancreas. Both pancreatic leaks were noted about 1 week postoperatively, and they resolved without further surgical intervention.

The published studies on laparoscopic resection of insulinomas include case reports and small series that indicate a similar incidence of complications and conversions. Berends et al5 successfully resected 6 of 10 insulinomas laparoscopically. Five of these were enucleations. They found 2 pancreatic fistulas in the laparoscopic group (total hospitalization, 3-21 days). Gagner et al4 published a series on patients with mixed histologic findings who had pancreatic tumors for which laparoscopic resection was attempted. Five of these were insulinomas, 3 of which were removed successfully by laparoscopy. This series did not report the type of procedures or the complications associated with them. The overall hospital stay for these laparoscopic patients was 4 to 7 days, so patients who had laparoscopic treatment for insulinomas may have been released with minimal complications within 7 days of the procedure. Other case reports410 noted minimal complications and hospital stays of 3 to 10 days (Table 4).

Table Graphic Jump LocationTable 4. Summary of Published Cases of Laparoscopic Insulinoma Resection

Laparoscopic ultrasound probes frequently do not provide the resolution of standard intraoperative probes. Improvements in technology should resolve this problem eventually.

In conclusion, as indicated by the results of this small preliminary series, laparoscopic localization and resection of insulinomas seem to be feasible and safe. With appropriate equipment and expertise, treatment of these tumors in most areas of the pancreas is possible by laparoscopic resection. Conversion to open exploration should be considered for tumors that cannot be identified accurately or for those located close to vascular structures that prevent safe resection. Failure of the laparoscopic procedure did not impede open localization or treatment and did not affect patients negatively. Overall, patients did not experience increased complications as a result of laparoscopic attempts, and, when pancreatic leaks are excluded, they had a shorter hospitalization and a faster return to usual activity. Our sample size is small, however, and 1 patient showed evidence of recurrent disease. Further study is required.

Corresponding author: Richard T. Schlinkert, MD, Division of General Surgery, Mayo Clinic, 13400 E Shea Blvd, Scottsdale, AZ 85259.

Accepted for publication August 5, 2003.

Raeburn  CDMcIntyre Jr  RC Laparoscopic approach to adrenal and endocrine pancreatic tumors. Surg Clin North Am. 2000;801427- 1441
PubMed
Lo  CYLam  KYKung  AWLam  KSTung  PHFan  ST Pancreatic insulinomas: a 15-year experience. Arch Surg. 1997;132926- 930
PubMed
Service  FJMcMahon  MMO'Brien  PCBallard  DJ Functioning insulinoma: incidence, recurrence, and long-term survival of patients: a 60-year study. Mayo Clin Proc. 1991;66711- 719
PubMed
Gagner  MPomp  AHerrera  MF Early experience with laparoscopic resections of islet cell tumors. Surgery. 1996;1201051- 1054
PubMed
Berends  FJCuesta  MAKazemier  G  et al.  Laparoscopic detection and resection of insulinomas. Surgery. 2000;128386- 391
PubMed
Sussman  LAChristie  RWhittle  DE Laparoscopic excision of distal pancreas including insulinoma. Aust N Z J Surg. 1996;66414- 416
PubMed
Spitz  JDLilly  MCTetik  CArregui  ME Ultrasound-guided laparoscopic resection of pancreatic islet cell tumors. Surg Laparosc Endosc Percutan Tech. 2000;10168- 173
PubMed
Tihanyi  TFMorvay  KNehez  LWinternitz  TRusz  ZFlautner  LE Laparoscopic distal resection of the pancreas with the preservation of the spleen. Acta Chir Hung. 1997;36359- 361
PubMed
Fernandez-Cruz  LHerrera  MSaenz  APantoja  JPAstudillo  ESierra  M Laparoscopic pancreatic surgery in patients with neuroendocrine tumours: indications and limits. Best Pract Res Clin Endocrinol Metab. 2001;15161- 175
PubMed
Cogliandolo  APidoto  RRCausse  XKerdraon  RSaint Marc  O Minimally invasive management of insulinomas: a case report. Surg Endosc. 2001;151042
PubMed
Boukhman  MPKaram  JMShaver  JSiperstein  AEDeLorimier  AAClark  OH Localization of insulinomas. Arch Surg. 1999;134818- 822
PubMed
Grant  CSvan Heerden  JCharboneau  JWJames  EMReading  CC Insulinoma: the value of intraoperative ultrasonography. Arch Surg. 1988;123843- 848
PubMed
Kuzin  NMEgorov  AVKondrashin  SALotov  ANKuznetzov  NSMajorova  JB Preoperative and intraoperative topographic diagnosis of insulinomas. World J Surg. 1998;22593- 597
PubMed
Heniford  BTIannitti  DAHale  JGagner  M The role of intraoperative ultrasonography during laparoscopic adrenalectomy. Surgery. 1997;1221068- 1073
PubMed
Hashimoto  LAWalsh  RM Preoperative localization of insulinomas is not necessary. J Am Coll Surg. 1999;189368- 373
PubMed
Ardengh  JCRosenbaum  PGanc  AJ  et al.  Role of EUS in the preoperative localization of insulinomas compared with spiral CT. Gastrointest Endosc. 2000;51552- 555
PubMed
Chung  MJChoi  BIHan  JKChung  JWHan  MCBae  SH Functioning islet cell tumor of the pancreas: localization with dynamic spiral CT. Acta Radiol. 1997;38135- 138
PubMed
Semelka  RCCumming  MJShoenut  JP  et al.  Islet cell tumors: comparison of dynamic contrast-enhanced CT and MR imaging with dynamic gadolinium enhancement and fat suppression. Radiology. 1993;186799- 802
PubMed
Pavone  PMitchell  DGLeonetti  F  et al.  Pancreatic β-cell tumors: MRI. J Comput Assist Tomogr. 1993;17403- 407
PubMed
Bansal  RKochman  MLBude  R  et al.  Localization of neuroendocrine tumors utilizing linear-array endoscopic ultrasonography. Gastrointest Endosc. 1995;4276- 79
PubMed
Knobel  BRosman  PCzerniak  A Endoscopic ultrasonography for the preoperative localization of insulinoma: a new, useful modality: case report and review of the literature. Isr J Med Sci. 1995;31365- 367
PubMed
Rosch  TLightdale  CJBotet  JF  et al.  Localization of pancreatic endocrine tumors by endoscopic ultrasonography. N Engl J Med. 1992;3261721- 1726
PubMed

Figures

Place holder to copy figure label and caption

A, Solitary, benign, intrapancreatic insulinoma. B, Simple enucleation of an insulinoma. C, Localization of an insulinoma with laparoscopic intraoperative ultrasonography.

Graphic Jump Location

Tables

Table Graphic Jump LocationTable 1. Localization and Surgical Procedures for Pancreatic Tumors in 9 Patients
Table Graphic Jump LocationTable 2. Laparoscopically Resected Insulinomas
Table Graphic Jump LocationTable 3. Outcomes of 4 Conversions to Celiotomy
Table Graphic Jump LocationTable 4. Summary of Published Cases of Laparoscopic Insulinoma Resection

References

Raeburn  CDMcIntyre Jr  RC Laparoscopic approach to adrenal and endocrine pancreatic tumors. Surg Clin North Am. 2000;801427- 1441
PubMed
Lo  CYLam  KYKung  AWLam  KSTung  PHFan  ST Pancreatic insulinomas: a 15-year experience. Arch Surg. 1997;132926- 930
PubMed
Service  FJMcMahon  MMO'Brien  PCBallard  DJ Functioning insulinoma: incidence, recurrence, and long-term survival of patients: a 60-year study. Mayo Clin Proc. 1991;66711- 719
PubMed
Gagner  MPomp  AHerrera  MF Early experience with laparoscopic resections of islet cell tumors. Surgery. 1996;1201051- 1054
PubMed
Berends  FJCuesta  MAKazemier  G  et al.  Laparoscopic detection and resection of insulinomas. Surgery. 2000;128386- 391
PubMed
Sussman  LAChristie  RWhittle  DE Laparoscopic excision of distal pancreas including insulinoma. Aust N Z J Surg. 1996;66414- 416
PubMed
Spitz  JDLilly  MCTetik  CArregui  ME Ultrasound-guided laparoscopic resection of pancreatic islet cell tumors. Surg Laparosc Endosc Percutan Tech. 2000;10168- 173
PubMed
Tihanyi  TFMorvay  KNehez  LWinternitz  TRusz  ZFlautner  LE Laparoscopic distal resection of the pancreas with the preservation of the spleen. Acta Chir Hung. 1997;36359- 361
PubMed
Fernandez-Cruz  LHerrera  MSaenz  APantoja  JPAstudillo  ESierra  M Laparoscopic pancreatic surgery in patients with neuroendocrine tumours: indications and limits. Best Pract Res Clin Endocrinol Metab. 2001;15161- 175
PubMed
Cogliandolo  APidoto  RRCausse  XKerdraon  RSaint Marc  O Minimally invasive management of insulinomas: a case report. Surg Endosc. 2001;151042
PubMed
Boukhman  MPKaram  JMShaver  JSiperstein  AEDeLorimier  AAClark  OH Localization of insulinomas. Arch Surg. 1999;134818- 822
PubMed
Grant  CSvan Heerden  JCharboneau  JWJames  EMReading  CC Insulinoma: the value of intraoperative ultrasonography. Arch Surg. 1988;123843- 848
PubMed
Kuzin  NMEgorov  AVKondrashin  SALotov  ANKuznetzov  NSMajorova  JB Preoperative and intraoperative topographic diagnosis of insulinomas. World J Surg. 1998;22593- 597
PubMed
Heniford  BTIannitti  DAHale  JGagner  M The role of intraoperative ultrasonography during laparoscopic adrenalectomy. Surgery. 1997;1221068- 1073
PubMed
Hashimoto  LAWalsh  RM Preoperative localization of insulinomas is not necessary. J Am Coll Surg. 1999;189368- 373
PubMed
Ardengh  JCRosenbaum  PGanc  AJ  et al.  Role of EUS in the preoperative localization of insulinomas compared with spiral CT. Gastrointest Endosc. 2000;51552- 555
PubMed
Chung  MJChoi  BIHan  JKChung  JWHan  MCBae  SH Functioning islet cell tumor of the pancreas: localization with dynamic spiral CT. Acta Radiol. 1997;38135- 138
PubMed
Semelka  RCCumming  MJShoenut  JP  et al.  Islet cell tumors: comparison of dynamic contrast-enhanced CT and MR imaging with dynamic gadolinium enhancement and fat suppression. Radiology. 1993;186799- 802
PubMed
Pavone  PMitchell  DGLeonetti  F  et al.  Pancreatic β-cell tumors: MRI. J Comput Assist Tomogr. 1993;17403- 407
PubMed
Bansal  RKochman  MLBude  R  et al.  Localization of neuroendocrine tumors utilizing linear-array endoscopic ultrasonography. Gastrointest Endosc. 1995;4276- 79
PubMed
Knobel  BRosman  PCzerniak  A Endoscopic ultrasonography for the preoperative localization of insulinoma: a new, useful modality: case report and review of the literature. Isr J Med Sci. 1995;31365- 367
PubMed
Rosch  TLightdale  CJBotet  JF  et al.  Localization of pancreatic endocrine tumors by endoscopic ultrasonography. N Engl J Med. 1992;3261721- 1726
PubMed

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