Early experience with laparoscopic resections of islet cell tumors

Early experience with laparoscopic resections of islet cell tumors Michel Gagner, MD, FRCSC, FACS, Alfons Pomp, MD, FRCSC, FACS, and Miguel F. Hen'era, MD, Cleveland, Ohio, Montreal, Quebec, Canada, and Mexico City, Mexico Background. Diagnostic laparoscopy and laparoscopic ultrasonography have been applied recently for diagnosis and localization of islet-cell tumors. A further step was taken by performing" resection of these tumors with laparoscopic techniques. Methods and Results. We studied a retrospective series of 12 patients operated on with taparoscopic techniques since January 1992. The seven female and five male patients had a mean age of 43 years. The mean tumor size was 3 cm. Thirty-six percent of the tumor site could not be identified before operation. Eight patients underwent planned laparoscopic distal pancreatectomy (five insulinomas, two gastrinomas, and one unknown origin), and four underwent planned laparoscopic enucleation (one insulinoma and three unknown origin). Of the eight distal procedures, three had conversions (one inability to localize the tumor and two metastatic gastrinomas). Average operating time was 4.5 hours, with an average hospital stay of 5 days. Of the four explorations for possible enucleation, one was performed and one was converted to a Whipple procedure for nesidioblastoma of the head of the pancreas. The other two had negative explorations. The successful enucleation of an insulinoma of the anterior body of the pancreas was perfo,vned in 3 hours, and the hospital stay was 4 days. No recurrence was seen in the enucleated or distal pancreatectomy group in follow-up (15 to 38 months). Conclusions. Laparoscopic enucleation or resection of benign islet tumors results in a shorter hospital recovery and is a good alternative to open surgery. (Surgery 1996;120:1051-4.) From the Department of General Surgery, The Cleveland Clinic Foundation, Cleveland, Ohio, the H6tel-Dieu de Montreal, Montreal, Quebec, and the Instituto Nacional de la Nutricion Salvador Zubiran, Mexico City, Mexico

THE INCREASINGUSE OF LAPAROSCOPufor staging permits a progressive ease of dissection around the pancreas. Exposure of the body through a window in the gastrocolic omentum and a laparoscopic Kocher maneuver is a logical step toward a successfffl laparoscopic resection. The increased use of diagnostic laparoscopic ultrasonography will also permit the localization of small pancreatic lesions and improve tactile sensation. Limited and anecdotal experiences with laparoscopic pancreatic resection have been reported. 1-s The aim of this study was to review retrospectively the collected series oflaparoscopic surgery for islet cell tumors of the pancreas and to determine the feasibility and morbidity of such surgery and better define its role in the overall surgical armamentarium.

PATIENTS AND METHODS We retrospectively reviewed the charts of 12 patients who u n d e r w e n t a laparoscopic p r o c e d u r e for an islet Presented at the Seventeenth Annual Meeting of the .MnericanAssociation of Endocrine Surgeons, Napa, Calif.,April 21-23, 1996. Reprint requests: Michel Gagner, MD, Tile Cleveland Clinic Foundation, 9500 Euclid Ave.,A80, Cleveland, OH 44195. Copyright 9 1996 by Mosby-YearBook, Inc. 0039-6060/96/$5.00 + 0 11/6/76610

cell rumor o f the pancreas between January 1992 and March 1996 at the H6tel-Dieu de Montr6al a n d the Instituto Nacional de la Nutricion Salvador Zubiran, Mexico City. Variables studied i n c l u d e d age, gender, localization studies, type, site, and location o f islet cell tumor, type of procedure, operative time, postoperative stay, morbidity, use o f laparoscopic ultrasonograpby, a n d follow-up p e r i o d for recurrence. Technique. Patients selected for potential laparoscopic resection u n d e r g o a laparoscopic staging procedure. This includes a three-trocar p r o c e d u r e (two 11 m m a n d one 5 ram) with a 30 ~ angled 10 m m laparoscope to visualize all aspects of the pancreatic gland. First, the body a n d tail are e x p o s e d anteriorly through a window in the gastrocolic ligament by lifting the greater curvature of the stomach with a laparoscopic Babcock forceps from an epigastric trocar. T h e window may b e p e r f o r m e d by using scissors with electrocautery o r ligafing transverse branches from the gasta-oepiploic arcade with medium-large titanium clips. T h e window has to be large e n o u g h (greater than 8 cm) to inspect b e y o n d the gastroduodenal artery to the hilum of the spleen anteriorly a n d inferiorly. A laparoscopic ultrasonographic p r o b e 10 m m in d i a m e t e r a n d with 7.5 SURGERY

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Surgery December 1996

T a b l e I. Preoperative localization Distal n

CT scan MRI Octreotide scan Angiography Portal venous sampling

+ Loc.

Enucleation n

4

+ Loc.

8

4

4

0

--

--

2

7 7 4

2 3 2

2 3 --

0 1 --

+ Loc., Positive preoperative localization; MR/, magnetic resonance imaging.

MHz o f frequency (Aloka, Tokyo, Japan) may be used t h r o u g h any p o r t a n d a p p l i e d anteriorly directly on the pancreatic neck, body, and tail. T h e image can be transmitted directly to the main laparoscopic m o n i t o r a n d split with a video mixer so the o p e r a t o r can get b o t h views (laparoscopic and ultrasonographic). T h e h e a d of the pancreas can also be scanned with the p r o b e by making contact directly over the h e a d o f the gland a r o u n d the d u o d e n a l loop. In addition, a laparoscopic Kocher maneuver Can be p e r f o r m e d with an additional trocar inserted in the right p a r a m e d i a n area at least 15 cm from the umbilicus to get a lateral view o f the seco n d a n d third portions of the d u o d e n u m . T h e retrop e r i t o n e u m is e n t e r e d with 5 m m scissors between the right kidney and the lateral portion of the second d u o d e n u m . Once dissection is b e y o n d the vena cava, d u o d e n u m is elevated with a laparoscopic Babcock forceps. T h e laparoscopic p r o b e can again be positioned b e h i n d the uncinate process to evaluate both this blind area a n d the posterior pancreas. Once the decision to resect or enucleate has b e e n reached, the patient is rotated laterally 45 ~ so his or h e r left side is up and patients in a reverse T r e n d e l e n b u r g position. If the gastrocolic window is n o t wide enough, the mobilization is carried out until the lower short gastric vessels are divided. This will greatly e n h a n c e the anterior view o f the tail o f the pancreas. Four trocars are necessary to perform the dissection and transection (three 11 m m and one 19 m m ) . T h e inferior b o r d e r of the pancreas is dissected from the retroperitoneal fat with a 5 m m h o o k with cautery until the gland is mobile a n d the splenic vein is r e a c h e d posteriorly a n d superiorly. T h e tail is then grasped with a 5 m m atraumatic forceps. Traction is applied anteriorly a n d inferiorly to expose u n d e r tension the transverse branches of the splenic artery and vein. A splenic preserving caudal pancreatectomy will thus result. T h e branches are ligated with m e d i u m titanium clips until the desired length has b e e n reached. Mobilization of the tail and body up to the portal vein can be achieved in this manner. T h e pancreas is then transversely transected with an endoscopic linear stapler (30 m m in length and 12 m m in diameter, U.S. Surgical, Norwalk, CT, or 60 m m in

length, 18 m m in diameter, Ethicon,Johnson &Johnson, Cincinnati, OH). This provides an adequate closure of the pancreatic duct and a partial ligature o f the pancreatic arterial arcades. These arcades may n e e d to be ligated with clips or cauterized. The specimen is then extracted by using a rigid plastic bag, 8 x 12 cm (Cook Urological, Spencer, IN), through a minimally enlarged umbilical incision. All fascial incisions are closed, and a Jackson-Pratt drain is left near the transection plane. For enucleation the exposure is similar to a distal pancreatectomy. O n c e the islet cell t u m o r has b e e n localized, the dissection is usually d o n e with a 5 m m h o o k with cautery between the n o r m a l p a r e n c h y m a a n d the t u m o r itself. The feeding pancreatic vessels to the t u m o r are ligated with medium-large titanium clips. Extraction is p e r f o r m e d by inserting the insulinoma into a sterile plastic bag t h r o u g h one o f the ports (10 m m ) , which is e n l a r g e d to the d i a m e t e r of the lesion. A Jackson-Pratt drain is left over the enucleation in the lesser sac. RESULTS

Seven women a n d five m e n were o p e r a t e d on for p r e s u m e d islet cell tumors of the pancreas on the basis o f clinical findings a n d / o r preoperative radiologic or nuclear localization. Patients h a d a m e a n age o f 43 years (range 29 to 74 years). T h e metal size o f r e s e c t e d lesions was 3 cm (range, 2 to 6 cm). Preoperative localization consisted of multiple series of radiologic examinations including combinations of c o m p u t e d t o m o g r a p h i c (CT) scan of the a b d o m e n with contrast, magnetic reso n a n c e imaging, a b d o m i n a l angiography, portal venous sampling, and octreotide nuclear scan (Table I). In spite o f all preoperative localization, 36% of the tumors were n o t identified before laparoscopy. T h e best results (50%) have been with CT scan, angiography, or portal venous sampling. Endoscopic ultrasonography has n o t b e e n available at o u r institutions. During the laparoscopic staging procedure, laparoscopic ultrasonography was available for 8 (67%) o f 12 patients. Interestingly, two insulinomas were n o t visualized (2 a n d 2.5 cm); they were located in the retroportal neck a n d in the body. But laparoscopic ultrasonography also excluded two lesions that were artifact on CT scan in one woman with hypoglycemia without hyperinsulinism and in a n o t h e r with p r e s u m e d vasoactive plasmatic substances. Laparoscopic distal pancreatectomies were p l a n n e d in eight patients for islet cell tumors and were confirmed in seven patients (Table II). In one patient there was, in fact, a 5 cm serous cystadenocarcinoma. T h r e e conversions were seen in this group. Enucleation was p l a n n e d for four patients a n d was perf o r m e d in one instance (Table III), with one conversion. T h e p r o c e d u r e p e r f o r m e d during conversion was pancreatotomy with enucleation of an insulinoma that was retroportal in the neck b u t n o t visible anteriorly. This

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Gagner, Pomp, Herrera

T a b l e IV. Operative time

T a b l e II. Laparoscopic p l a n n e d distal pancreatectomies

Preoperative diagnosis Insulinoma Insulinoma Insulinoma Insulinoma

Gastrinoma Insulinoma Unknown

Postoperative diagnosis Insulinoma Insulinoma (body-tail) Insulinoma (neck) Malignant mixed insulinomagastrinoma Malignant gastrinoma Insulinoma Cystadenocarcinoma

No. of hours (range) Conversion

+ (Retroportal) +

+

Postoperative diagnosis

Insulinoma (tail) Unknown Vasoactive secreting tumor Hypoglycemia

Insulinoma (body) Nesidioblastoma Normal pancreas Normal pancreas

Distal pancreatectomy Converted Nonconverted Enucleation Converted Nonconverted Diagnostic

6.3 (4-8) 4.5 (4-5) 4.5 3.0 1.3 (1-1.5)

T a b l e V. Postoperative stay

No. of days (range) --

T a b l e III. P l a n n e d laparoscopic enucleation

Preoperative diagnosis

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Conversion

Distal pancreatectomy Converted Nonconverted Enucleation Converted Nonconverted Diagnostic

21 (16-33) 5.0 (4-7) 14.0 4.0 1.5 (1-2)

--

+ (Whipple)

--

lesion was missed by laparoscopic ultrasonography b u t detected by o p e n ultrasonography. Mso the preoperative localization with portal venous sampling revealed an area in the body of the pancreas. Two m a l i g n a n t gastrinomas were converted after diagnostic laparoscopy in view of the extensive intraabd o m i n a l disease. O n e patient r e q u i r e d a distal pancreatectomy (body a n d tail) with splenectomy, left adrenalectomy, partial gastrectomy (greater curvature), transverse colectomy, a n d hepatic segmentectomy II-III. T h e second patient also u n d e r w e n t a distal pancreatectomy (tail), splenectomy, partial gastrectomy, and hepatic metastasectomy. O n e patient u n d e r w e n t enucleation for a nonsecreting islet cell t u m o r o f the h e a d of the pancreas because at laparoscopy the t u m o r was too d e e p in the pancreatic parenchyma. Therefore she underwent an o p e n pylorus-preserving W h i p p l e for nesidioblastoma (3 cm) with a positive antibody to somatostatin a n d glucagon. Operative time was shorter for n o n c o n v e r t e d distal pancreatectomy and enucleation (Table IV). Only two complications were seen in the laparoscopic group, significant intraoperative b l e e d i n g from an inferior tear o f the splenic vein requiring multiple titanium clips. T h e patient who u n d e r w e n t resection for a cystadenocarcin o m a was o l d e r (74 years of age) a n d h a d to be readmitted for a small infected collection near the pan-

creatic b e d that was percutaneously drained. T h e converted group had an overall p r o l o n g e d hospital stay (Table V) because o f multiple complications (delay in gastric emptying, p n e u m o n i a , a n d pancreatic leak). In the m e a n follow-up p e r i o d o f 27 m o n t h s (range, 15 to 28 months), no recurrences were seen in any o f the resected or laparoscopically e n u c l e a t e d insulinomas. However, three subsequent reoperations for debulking and metastasectomy h a d to be p e r f o r m e d in tile converted g r o u p because of multiple metastases in the right lobe of the liver from malignant gastrinomas in two patients. DISCUSSION

In a study by Yeo et al.,4 preoperative CT correctly localized the t u m o r in 59% o f patients, which is n o t different from our series. However, angiography seemed to have a better yield in their study (75 %). This situation puts the surgeon in a difficult situation because the localization has to be done in m o r e than one third of all cases during the surgical intervention. 5 O t h e r than examining the dissectable pancreatic surfaces, the laparoscopi~c surgeon has a decreased tactile sensation that is somewhat d i m i n i s h e d by the compression o f the pancreatic tissue with a 10 m m palpation probe. Laparoscopic ultrasonography did n o t identify all lesions during the staging procedure, a n d it is expected to r e p r o d u c e the results from o p e n surgery, where the best strategy is to c o m b i n e palpation and ultrasonography. 6 However, laparoscopic ultrasonography can be useful in questionable cases, where artifacts arise from radiologic imaging. It can also help avoid an unnecessary laparotomy. T h e technique may be espe-

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cially u s e f u l in n o n f u n c t i o n i n g islet cell t u m o r s . As w i t h o u r p a t i e n t s , we h a v e n o t h e s i t a t e d to c o n v e r t to a W h i p p l e b e c a u s e t h e s e t u m o r s m a y p r o g r e s s to n o n f u n c t i o n i n g islet cell c a r c i n o m a s if t h e y c a n n o t b e e n u c l e a t e d o r r e s e c t e d by l a p a r o s c o p y . 7' 8 I n n o n c o n v e r t e d p a t i e n t s very little m o r b i d i t y was enc o u n t e r e d w i t h r e d u c e d p o s t o p e r a t i v e stay, p r e s u m a b l y b e c a u s e o f r e d u c e d t r a u m a to t h e a b d o m i n a l wall a n d less e x p o s u r e to a m b i e n t air. N o p a n c r e a t i c leaks w e r e e n c o u n t e r e d i n spite o f o u r u s e o f a n e n d o s c o p i c stapler. Also p a t i e n t s d i d n o t h a v e r e c u r r e n c e s a f t e r a r e a s o n a b l e follow-up, c o r r o b o r a t i n g t h e f i n d i n g t h a t t r u e successful e n u c l e a t i o n a n d r e s e c t i o n a r e a c h i e v e d w i t h t h e l a p a r o s c o p i c m e t h o d . I n a r e c e n t series o f o p e n r e s e c t i o n f o r i n s u l i n o m a s i n 34 p a t i e n t s , 31 w e r e sympt o m f r e e at a m e a n follow-up o f 16 m o n t h s . 9 T h e r e f o r e , it is c o n c l u d e d f r o m this small series t h a t l a p a r o s c o p i c e n u c l e a t i o n a n d r e s e c t i o n o f islet cell t u m o r s are feasible. I n d i c a t i o n s for this p r o c e d u r e s h o u l d b e initially r e s e r v e d for b e n i g n lesions o f t h e tail o r b o d y o f t h e p a n c r e a s , especially a n t e r i o r l y . It d o e s r e q u i r e t h e e x p e r t i s e o f a d v a n c e d l a p a r o s c o p i c digestive s u r g e o n s with available i n t r a o p e r a t i v e l a p a r o s c o p i c u l t r a s o n o g r a phy. T h o s e s u r g e o n s s h o u l d also b e c o m p e t e n t i n t h e o p e n o p e r a t i o n a n d w i t h o p e n i n t r a o p e r a t i v e ultrasonography of the pancreas.

REFERENCES 1. Gagner M, Pomp A. Laparoscopic pylorus-preserving pancreatoduodenectomy. Surg Endosc 1994;8:408-10. 2. Gagner M. Laparoscopic duodenopancreatectomy. In~ Steichen F, Welter R, editors. Minimally invasive surgery and technology. St. Louis: Quality Medical Publishing, 1994:192-9. 3. Gagner M. La Pancr~atectomie Distale Par Laparoscopie Pour Insulinomes: Reunion des Endocrinologues de l'Universite de Montreal, Hopital Sacre-Coeur. Montreal: April 5, 1993. 4. Yeo CJ, Wang BH, Anthone GJ, Comeron JL. Surgical experience with pancreatic islet-cell tumors. Arch Surg 1993;128: 1143-8. 5. Broughan TA, LeslieJD, SotoJM, Hermann RE. Pancreatic isletcell tumors. Surgery 1986;99:671-8. 6. Norton JA, Cromack DT, Shawken TH, et al. Intraoperative ultrasonographic localization of islet-cell tumors: a prospective comparison to palpation. Ann Surg 1988;207:160-8. 7. Evans DB, Skibber JM, Lee JE, et al. Non-functioning islet-cell carcinoma of the pancreas. Surgery 1993;114:1175-81. 8. Udelsman R, Yeo CJ, Hruban RH, et al. Pancreato-duodenectomy for selected pancreatic endocrine tnmors. Sm'g Gynecol Obstet 1993;177:269-78. 9. Geoghegan JG, Jackson JE, Lewis MP, et al. Localization and surgical management of insulinoma. BrJ Surg 1994;81:1025-8.

DISCUSSION Dr. Lawrence A. Danto (Davis, CA). Maybe I missed it, but could you c o m m e n t on your use of drains after operation? Dr. Gagner. I did not state that in the technique, but I always position a drain that is positioned laparoscopically in the lesser sac when we make a gastrocolic window just over the nucleation or next to the transected plane.

Surgery December 1996 Dr. Charles Proye (Lille, France). I could see that you had two false negatives of intraoperative laparoscopic echography a n d that you did not use endoscopic uRrasonography before operation. D o n ' t you think that it might be of some help before and also even during operation for more accurate localization of the tumors? Dr. Gagner. I agree with you, it would have been nice to have the endoscopic sonography. This has b e e n a cost-effective issue for us, and it is not available. Dr. Michael B r u n t (St. Louis, MO). I have a question about your postoperative recuperation in these patients. With many advanced laparoscopic procedures, even those involving the gastrointestinal tract, like fundoplication, patients are going h o m e within 1 or 2 days after the procedure. I noticed your average length of stay was just over 4 days and tile range was 4 to 7 days. Could you c o m m e n t on that? Might you be able to get these people out m u c h earlier? Or were there concerns about the pancreatic stapling that led you to keep these patients longer? Dr. Gagner. At the beginning I had some concern about having pancreatic leaks, so I was leaving these patients in the hospital a n d studying their pancreatic fluid coming out from the drain waiting for some complication to occur. We h a d one patient who stayed 7 days; this patient was the eldest of the group at 74 years of age. We have to make sure when they leave the hospital, especially in the Canadian system, that they are n o t going to have any problems, because that is the way the care is being done. I agree with you that now looking back at the experience that some of these patients could leave earlier, even with tile drain in place if it is having quite a lot of drainage. Dr. Barbara K. Kinder (New Haven, CT). Using this technique we have done one distal pancreatectomy for a small glucagonoma in the tail. It was really effective and the patient did extremely well. In terms of the patients with whom you have localization problems, have you used the intraarterial stimulation hepatic venous sampling at all? We have found that to be really nseful. Dr. Gagner. No, I have had no experience with this technique. Dr. Richard A. Prinz (Chicago, IL). In approximately two thirds of your patients you had a positive preoperative localization of the tumor. How successful were you in removing the lesion in that group of patients.compared with those in whom you were unable to localize the tumor? Dr. Gagner. In two thirds of them we knew that there was some form of localization; in one third we did not know where they were localized. In that group this created a tremendous amount of stress in trying to identify them with laparoscopic ultrasonography. We did not identify more lesions a n d h a d to do blind resections, which successfully localized them. In the ones that we knew where they were before operation, there was some false localization, as I mentioned. I d o n ' t think that laparoscopic nltrasonography right now is the magic bullet. It is the combination of things that will help US,