ANNALS OF SURGERYVol. 223, No. 2, 134-140© 1996 Lippincott-Raven Publishers

The Value of Minimal Access Surgeryin the Staging of Patients withPotentially ResectablePeripancreatic MalignancyKevin C. Conlon, M.D., Ellen Dougherty, M.A., David S. Klimstra, M.D., Daniel G. Coit, M.D.,Alan D. M. Turnbull, M.D., and Murray F. Brennan, M.D.

From the Memorial Sloan-Kettering Cancer Center, New York, New York

ObjectiveThe purpose of this study was to determine if an endosurgical approach that mimics openexploration would improve the accuracy of simple diagnostic laparoscopy.

Summary Background DataMost patients with peripancreatic malignancy are found at exploration to be unable to undergoresection. Laparoscopy has been suggested as a sensitive method for detecting metastaticdisease in this group of patients. However, the ability to assess resectability with simplediagnostic laparoscopy remains relatively low (<40%).

MethodsBetween December 1992 and August 1994, 115 patients with radiologically resectableperipancreatic tumors underwent extended laparoscopy before undergoing a planned curativeresection. This technique required assessment of the peritoneal cavity, liver, lesser sac, portahepatis, duodenum, transverse mesocolon, and celiac and portal vessels.

ResultsSixty male and 55 female patients were included in the current study. The pancreatic head wasinvolved in 74 patients (64%), followed by the body in 21 (18%), tail in 8 (7%), ampulla in 8 (7%),duodenum in 3 (3%), and distal bile duct in 1 (1%). An abdominal computed tomography (CT)scan was performed for all patients before laparoscopy, ultrasonography for 74 patients (64%),endoscopic retrograde choleangiopancreatography for 59 patients (51 %), and mesentericangiography for 9 patients (8%). Pneumoperitoneum was established successfully in all but 2cases (98%). A complete examination of 108 patients was performed. Sixty-seven patients wereconsidered to have resectable disease, and 61 resections were performed. Laparoscopy failed toidentify hepatic metastases in 5 patients and portal venous encasement in 1 patient. Unresectabledisease was identified in 41 patients. Hepatic metastases were observed in 20 patients,mesenteric vascular encasement in 14, extrapancreatic/peritoneal involvement in 16, and celiacor portal lymphatic metastases in 8. There were no intraoperative or postoperative complicationsrelated to the laparoscopic procedure. The positive predictive index, negative predictive index,and accuracy of laparoscopy were 100%, 91%, and 94%, respectively.

ConclusionsThis study demonstrates that extended laparoscopy is accurate and safe and makes explorationunnecessary in many patients with potentially resectable peripancreatic malignancy. In this series,

134

Minimal Access Surgery in Staging of Peripancreatic Malignancy 135

76% of patients explored were resected, compared with the authors' experience between 1983and 1993 of 35%. The authors believe that laparoscopy is an important component in the stagingof this group of patients and should be performed before exploration.

In oncologic practice, minimal access surgery has beenproposed for the diagnosis, staging, palliation, and treat-ment of various malignancies without any substantivedata confirming its effectiveness.

Patients with peripancreatic malignancy may havemuch to gain from minimal access surgery. An estimated28,000 new cases ofpancreatic cancer occur each year inthe United States.' The incidence is stable, with mostcases occurring in the sixth, seventh, and eighth decadesoflife. More than 25,000 deaths per year are attributed tothe disease, making it the fourth leading cause ofcancer-related death, surpassed only by lung, colorectal, andbreast cancers. The prognosis is bleak, with an overall 5-year survival rate of between 2% and 3%. Surgical resec-tion offers the only prospect of cure. Symptomatology,which is dependent on site and cell type, is often vague,and most patients present with advanced disease, whichprecludes potentially curative therapy.>3

Despite recent advances in pancreatic imaging4e6 anddevelopment ofnonoperative techniques for reliefof bil-iary obstruction, most patients still undergo an explor-atory laparotomy for accurate staging and palliation.7For those who do not require a palliative procedure, ex-ploration does not confer any benefit and is associatedwith significant morbidity and mortality, affecting boththe quality and duration of survival.7-8Numerous reports have demonstrated that laparo-

scopic examination may identify peritoneal and hepaticdisease not seen with other diagnostic modalities.9'-3However, laparoscopic techniques as described have notbeen found to be an accurate predictor of resectabil-ity.213 In part, this is due to the inherent limitation oflaparoscopy as a two-dimensional imaging modality butalso because the existing laparoscopic methods ofstagingdo not replicate conventional open surgical staging.

Recent improvements in minimal access surgery in-strumentation and techniques have persuaded us thatlaparoscopy can achieve more than detect peritoneal andsuperficial hepatic metastases, and a full surgical stagingprocedure for peripancreatic tumors is possible. This

study was designed to test this hypothesis and to deter-mine the role of minimal access surgery in the diagnosticalgorithm for these tumors.

PATIENTS AND METHODSPatients presenting for operation at Memorial Sloan-

Kettering Cancer Center between December 1992 andAugust 1994 who after radiologic examination were con-sidered to have potentially resectable peripancreatic tu-mors were eligible for this study. Clinicopathologic andoperative data were recorded and stored in a prospectivedata base maintained by the department of surgery.

Radiologic AssessmentAll patients underwent a preoperative, contrast-en-

hanced, dynamic CT scan ofthe abdomen that was ana-lyzed for the following:

1. Tumor size and location2. Presence or absence ofhepatic or peritoneal metas-

tases or ascites3. Presence of extrapancreatic tumor extension4. Presence or absence ofadenopathy, particularly ce-

liac, peripancreatic, or periportal5. Vascular encasement.

Hepatic or peritoneal metastases, definitive vascularencasement, or obstruction constituted absolute radio-logic criteria for unresectability. Adenopathy, minimalascites, or the appearance of vascular encroachmentwere considered relative criteria for unresectability. Be-cause of our referral pattern, most of the studies wereperformed outside of our institution. However, if on re-view the study did not provide the required information,it was repeated at Memorial Sloan-Kettering. Other ra-diologic investigations (i.e., angiography, ERCP, and/orultrasonography), if performed, were also reviewed todetermine whether the patient had potentially resectabledisease.

Presented at the 80th Annual Clinical Congress of the American Col-lege of Surgeons, October 13th, 1994, Chicago, Illinois.

Supported in part by the Milton Ludmar Memorial Fund, the LillianWells Foundation, and the Bernice and Milton Stern Foundation.

Address reprint requests to Kevin C. Conlon, M.D., Director, Endo-surgical Program, Gastric and Mixed Tumor Service, MemorialSloan-Kettering Cancer Center, 1275 York Avenue, New York,NY 10021.

Accepted for publication March 2, 1995.

Surgical TechniqueLaparoscopy was performed with use of general anes-

thesia. The patient was placed supine on the operatingtable. A warming blanket was used to maintain normalbody temperature. An open surgical technique for car-bon dioxide insufflation was used in all cases. A 1-cmsubumbilical incision was made to expose the abdominal

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136 Conlon and Others

rating port

port

Figure 1. Position of the operating ports.

wall fascia. The peritoneum was opened under direct vi-sion, and a 10/11 mm Hasson type trocar was inserted(Endopath, Ethicon Endo-Surgery, Cincinnati, OH).This was attached to a high-flow carbon dioxide in-sufflator (Karl Storz Endoscopy-America, Inc., CulverCity, CA). Carbon dioxide (CO2) insufflation was com-menced through this trocar to an intra-abdominal pres-sure of 14 mm Hg. A 30-degree angled telescope wasused. Three further metallic trocars (Surgiport, U.S. Sur-gical Corp. Norwalk, CT) were inserted under direct vi-sion. Two 10-mm trocars were inserted into the right andleft upper quadrants, respectively, and a 5-mm trocarwas placed between the umbilical and left upper quad-rant trocars (Fig. 1).

Intraperitoneal adhesions, if present, were divided.The primary tumor was assessed, and local extent, size,and fixation were noted. Extension to contiguous organs,such as the colon, duodenum, liver, spleen, and stomach,were identified. The patient was then placed in a 20-de-gree reverse Trendelenburg position with 10 degrees ofleft lateral tilt. Examination began with visualization ofthe anterior and posterior surfaces of the left lateral seg-ment ofthe liver and ofthe anterior and inferior surfacesof its right lobe (Fig. 2). Palpation of the liver wasachieved with use of a 10-mm instrument. The hilus ofthe liver was visualized, and by correctly positioning the30-degree telescope, the foramen ofWinslow was exam-ined4 and periportal lymph nodes were biopsied if re-quired. The patient was then placed in a 10-degree Tren-delenburg position without lateral tilt, and the momen-

tum was identified and retracted toward the left upperquadrant. This allowed for identification ofthe ligamentof Treitz.s The mesocolon was inspected, with particularattention paid to the mesocolic vein, which normally isquite visible. On completion of the mesocolic examina-tion, the gastrohepatic omentum was then incised,exposing the caudate lobe of the liver, vena cava, andceliac axis.6 In most cases, the lesser sac was inspectedby means of this approach. Celiac, portal, or perigastriclymph nodes were sampled, if necessary. The hepatic ar-tery was identified and its course to the porta visualized.During the examination, any suspicious lesions were bi-opsied with the use of specially designed endosurgical bi-opsy forceps (Jarit Instruments, Hawthorne, NY) andsent for frozen section.

Unresectability was determined ifone ofthe followingconditions was present: (1) metastases (hepatic, serosal,or peritoneal) (2) extrapancreatic extension of tumor(i.e., mesocolic involvement), (3) celiac or portal nodeinvolvement, (4) invasion or encasement of the celiacaxis or hepatic artery, or (5) encasement by tumor oftheportal or superior mesenteric vein and/or superior mes-enteric artery. Patients who were found to have portal ormesenteric vein encroachment by tumor were consid-ered to be potential candidates for resection and thus un-derwent an exploratory laparotomy.

Figure 2. Sequence of the staging procedure.

Ann. Surg. * February 1996

Minimal Access Surgery in Staging of Peripancreatic Malignancy 137

Table 1. POSTOPERATIVE HISTOLOGICDIAGNOSIS

Histologic Diagnosis No. of Patients

Malignant tumorsAdenocarcinoma 103Metastatic carcinoma 3Cystadenocarcinoma 1Islet cell tumors 4Lymphoma 1

Benign diseasePancreatitis 2Cystadenoma 1

RESULTS

Between December 1992 and August 1994, 115 pa-

tients with potentially resectable peripancreatic tumorshad laparoscopy attempted before undergoing curativeresection. There were 60 male and 55 female patientswith a mean age of 65 years (range, 21-84 years). Ninetypercent of the patients were white, 5% black, and 5%Asian.Most patients (n = 111 [97%]) were symptomatic.

Pain was the most common symptom on presentation (n= 81 [70%]), followed byjaundice (n = 64 [56%]), weightloss of more than 10 lb (n = 50 [43%]), nausea (n = 20[ 17%]), and vomiting (n = 13 [ 1%]). Four patients un-

derwent exploration elsewhere within a month of refer-ral, and one patient had received chemotherapy and ex-

ternal-beam radiotherapy. Prior biliary drainage hadbeen performed in 39 patients (endoscopic stenting, n= 30; percutaneous transhepatic drainage, n = 5; andsurgical drainage, n = 4).An antecedent history of abdominal surgery was ob-

tained for 42 patients (37%). Thirteen patients had a his-tory of malignant disease (prostate, n = 3; breast, n = 2;skin, n = 2; and bladder, colon, fallopian tube, kidney,or uterus sarcoma, n = 1 each).The head of the pancreas was the predominant tumor

site (n = 74 [64%,]), followed by the body ofthe pancreas(n = 21 [18%]), pancreatic tail (n = 8 [7%]), ampulla (n= 8 [7%]), duodenum (n = 3 [3%]), and distal bile duct(n = 1 [ 1%]). Malignant disease was present in 109 cases,with ductal adenocarcinoma being the most common di-agnosis (n = 103 [90%]) (Table 1.)

Prior radiologic studies included abdominal CT for115 patients (100%), ultrasonography for 74 (64%),ERCP for 59 (51%), and mesenteric angiography for 9(8%). Radiologic criteria were used to establish eligibilityof patients for resection.Pneumoperitoneum was successfully established in

113 cases (98%). Five patients underwent a limited ex-

ploration only. A complete examination was performedsuccessfully for 108 patients (94%).

Unresectable disease was found in 41 patients. He-patic metastases were found in 20 patients, vascular en-

casement in 14, extrapancreatic/peritoneal involvementin 16, and celiac or portal lymphatic metastases in 8 (Ta-ble 2). Histologic confirmation ofunresectability was ob-tained in 39 cases. Early in our experience, two patientswere considered to have portal vascular encasement, buthistologic proof was not obtained; subsequent explor-atory laparotomy confirmed the laparoscopic findings.

Sixty-seven patients were considered to have resect-able disease on completion ofthe laparoscopic examina-tion. A resection was performed for 61 of these patients(91%). Six patients (9%) did not undergo resection be-cause of disease that was not discovered at laparoscopy.At laparotomy, small, deep hepatic metastases were ob-served in five patients and portal venous encasement inone patient with pancreatitis. The positive predictive in-dex, negative predictive index, and accuracy ofthe lapa-roscopic examination were 100%, 91%, and 94%, respec-

tively.In the group of patients who did not undergo resec-

tion, a laparoscopic procedure alone was performed in28 cases (68%). Three patients underwent a laparoscopicbiliary or gastric bypass. Twelve patients had an open

exploration for a biliary or gastric drainage, and 7 hadan exploratory laparotomy alone. For all patients whounderwent exploration, the laparoscopic findings were

confirmed and none underwent resection.No perioperative morbidity was associated with the

laparoscopic procedure. Postoperative hospital stay forall patients is listed in Table 3. There was a significantdecrease in length of stay after open exploration com-

pared with laparoscopy alone (p = 0.009). Two patientsin the laparoscopic group received cytotoxic chemother-apy before discharge.

DISCUSSION

Surgical extirpation remains the only curative therapyfor the most patients with a peripancreatic malignancy.

Table 2. REASONS FORUNRESECTABILITY

Sole SiteDisease Site No. of Patients of Disease

Liver metastases 20 12Extrapancreatic disease 16 3Nodal disease 8 1Vascular invasion 16 10

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138 Conlon and Others

Table 3. LENGTH OF HOSPITAL STAY

No. of Mean Median RangeProcedure Patients (days) (days) (days)

Explored only 13 7.4 7 2-21Resected 62 14.9 14 6-48Biliary bypass 8 10.6 9.5 7-16Gastric/biliary bypass 7 14.3 12 7-27Laparoscopy 25 3.6 2 1-13

* Laparoscopy vs. explored only (p = 0.009).

However, improved noninvasive diagnostic modalities,development ofbetter nonoperative techniques for palli-ation,7'8"14"15 awareness of the significant morbidity andmortality rates associated with unnecessary operation,8and the desire for cost-containment have rendered obso-lete the traditional surgical approach ofopen explorationfor the diagnosis and staging ofthese tumors.Dynamic, contrast-enhanced CT is the initial nonin-

vasive diagnostic and staging modality ofchoice for thesepatients.'6 Freeny et al. prospectively assessed the accu-

racy ofthis modality in 213 patients with pancreatic car-

cinoma.'7 A correct diagnosis was made in 97% of cases.Most of the patients (88%) were thought to have unre-

sectable disease by virtue of vascular invasion (82%), lo-cal extension (72%), distant metastases (50%), or contig-uous organ involvement (43%). Computed tomographycorrectly predicted unresectability in 100% of cases butcorrectly predicted resectability in only 67% of cases,missing tumor invasion into the root of the colonic andsmall bowel mesentery, metastatic portal adenopathy,and posterior pancreatic extension of tumor. Similar re-

sults were reported by Fuhrman and colleagues, who an-

alyzed the results of 42 patients with pancreatic adeno-carcinoma who had resectable disease according to CTcriteria and who underwent exploration.'8 A pancreaticresection was performed for 37 (88%); the remaining 5patients had locally advanced or metastatic disease andwere eligible for resection. Gulliver et al. demonstrated a

80% positive predictive value for determining resectabil-ity.'9 Using CT criteria alone, Dooley et al. reported aresectability rate of 60% for periampullary tumors.20This finding is similar to the predictive value of 57%found in the current study.Dooley and colleagues also assessed the role ofangiog-

raphy in staging.20 Angiograms from 90 patients consid-ered resectable by CT criteria were examined: 62 hadnormal study results, and ofthese patients, 48 ultimatelyunderwent resection. Fourteen patients with normal ar-

teriogram results were found to have unresectable dis-ease at laparotomy (hepatic metastases, n = 7; peritonealdisease, n = 3; vascular involvement, n = 3). Angio-

graphic criteria of unresectability was found for 28 pa-tients, but at laparotomy 21% were noted to be resectableand underwent pancreaticoduodenectomy. Despite thishigh false-positive rate, the authors concluded that angi-ography has a role in staging. Warshaw et al. also notedthat selective angiography was a significant independentstaging factor.'2 In contrast, some authors believe thatangiography adds little staging information to dynamicCT scanning.'7'9 We do not perform angiography rou-tinely, and only nine patients in the current study un-derwent this test, most before referral to our institution.All ofthe results were considered normal. However, onlyfour ofthese nine patients underwent resection. At lapa-roscopy, three patients were found to have vascular en-casement; three, extrapancreatic disease; three, nodaldisease; and one, solitary hepatic metastasis.The concept that laparoscopy can prevent unneces-

sary exploration in patients with pancreatic cancer is notnew. In 191 1, Bernheim (Johns Hopkins University) re-ported the first laparoscopy in the United States, whichwas performed on a patient ofHalstead's with pancreaticcancer.2' He stated that the novel technique "may revealgeneral metastases or a secondary nodule in the liver,thus rendering further procedures unnecessary and sav-ing the patient a rather prolonged convalescence." Morerecently, Ishida examined 71 patients and detected he-patic metastases in 30% and peritoneal disease in 41%.9Warshaw et al. examined 40 patients considered to havelocalized disease who underwent diagnostic laparos-copy. " Laparoscopic findings of hepatic (n = 6), perito-neal (n = 7), or omental (n = 1) metastases resulted in achange of therapy for 14 patients. Of the remaining 26patients, 3 at subsequent laparotomy were noted to havemetastatic disease in the liver, which had been over-looked at laparoscopy. The resectability rate for the re-mainder of the patients was not given. A subsequentstudy from the same unit reported that laparoscopy andbiopsy detected 96% of patients with small hepatic orperitoneal implants.'2 However, in 19 cases in which nometastases were seen, only 8 patients underwent subse-quent resection. Cuschieri noted similar results from aretrospective review of 51 patients who underwent lapa-roscopy and subsequent laparotomy.'3 Nine patientswere considered resectable after laparoscopic assess-ment, but only 4 underwent resection. Invasion of theportal vein in four cases and unsuspected hepatic metas-tasis in one case were the reasons for unresectability. Al-though these studies emphasized the positive predictivevalue of simple laparoscopy, they also highlight theweakness ofa "negative" examination.Our methodology differed from the previous reports

in that a multiport technique was used, thereby allowingfor retraction and dissection. Despite a history ofabdom-inal operation for 37% of the patients, a full staging pro-

Ann. Surg. . February 1996

Vol. 223 . No. 2 Minimal Access Surgery in Staging of Peripancreatic Malignancy 139

Table 4. RESULTS OF LAPAROSCOPICSTAGING

LaparoscopicAssessment Resected Unresectable

Resectable 61 6Unresectable 0 41

cedure was possible in 94% of cases. Reasons for unre-sectability were identified for 41 patients: most had dis-ease that would not have been identified by simplelaparoscopy alone. As can shown in Table 2, most pa-tients had multiple reasons for unresectability similar tothose found in previous studies. Histologic proof of un-resectability was obtained in 39 patients at the time oflaparoscopy, whereas the remaining 2 patients werethought to have portal encasement but were examinedearly in our experience, at which time dissection was lim-ited and biopsies were not attempted. Currently, whenthere is a suggestion of portal venous obstruction (i.e.,enlarged mesenteric, omental, or perigastric veins), weare more aggressive in exposing the suprapancreatic por-tal vein through the lesser sac or superior mesenteric veinby dividing the gastrocolic omentum to allow for biopsy.A correct assessment of resectability was made for 61

of 67 patients (91 %) (Table 4). Open exploration and re-section was performed with use ofthe same type of anes-thesia on completion ofthe laparoscopy. Six patients hadtheir disease understaged at laparoscopy, five of whomhad liver metastases. In one case, the lesion was on thesurface of segment V and was obscured by adhesions tothe colon and gallbladder, which were not divided. Theremaining patients had small intraparenchymal metas-tases. Although using two instruments to palpate theliver has allowed us to identify some intraparenchymallesions, the lack oftactile sensation hinders the detectionofsuch lesions. Recent reports have suggested that intra-operative laparoscopic ultrasonography can overcomethis deficiency.4'22 Murugiah et al. recently reported theirexperience with laparoscopic ultrasonography in 10 pa-tients with pancreatic cancer with use ofa rigid 7.5-MHzlinear array probe.23 For two patients, unsuspected he-patic metastases were detected by ultrasonography afterstandard laparoscopy was performed.The use of laparoscopy has significantly reduced the

percentage of patients undergoing open explorationwithout resection at our institution. Between October1983 and December 1992, 1135 patients with peripan-creatic tumor underwent laparotomy at our institution,35% of whom underwent resection (Brennan MF, un-published data, 1996). In the current series, 80 patientsunderwent open exploration, with an overall resectabil-

ity rate of 76% (p < 0.00001). Continued developmentof laparoscopic staging and palliative biliary or gastricbypass offers hope that this figure can be increased. Itbears mentioning, however, that the increased resectabil-ity rate reflects improved selection of patients for openoperation rather than an increase in the number of re-sectable patients per se.Our data demonstrate that patients who underwent

laparoscopy alone had minimal surgical morbidity, re-duced hospital stay, and a shorter postoperative recoverycompared with those received a comparable open proce-dure. The decrease in hospital stay alone confers consid-erable cost savings. We believe that the combination ofcontrast-enhanced dynamic CT scanning and laparos-copy is a cost-effective, accurate, and safe means of stag-ing peripancreatic malignancy, which can prevent need-less operations in some patients while offering poten-tially curative surgery for patients who would benefit.

Acknowledgment

The authors thank Mr. Roger Moccia for his assistance with datamanagement.

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