Laparoscopic staging of gastric cancer: an overview

Laparoscopic Staging of Gastric Cancer:An OverviewDomenico M D’Ugo, MD, FACS, Vito Pende, MD, Roberto Persiani, MD, Stefano Rausei, MD,Aurelio Picciocchi, MD, FACS

Jacobaeus,1 who first used the term laparoscopy in 1911,pointed out the enormous diagnostic implications ofthis technique, indicating that by using a laparoscope,diagnoses of cirrhosis, tuberculous peritonitis, and met-astatic tumors could be confirmed. With the advances invideo endoscopy and the addition of television monitor-ing, current techniques of laparoscopy using improvedimaging have led to the widest application in the diag-nosis of abdominal malignancy.2 One of the first impor-tant experiences involving the use of laparoscopy for thestaging of gastric neoplasms was reported by Gross andcolleagues3 in 1984 in a series of 46 cases. This reportwas followed by many others that we will discuss in thisarticle. At present, a number of published articles sug-gest that laparoscopy is indeed capable of solving themajority of the problems related to gastric cancer stag-ing, giving the unique opportunity of an accurate selec-tion of patient subgroups on the basis of their preciseclinical stage and specific prognosis, with the final goalof an individually “stage-adapted” treatment.4-9 Butthere is still some concern about possible implications ofdiagnostic laparoscopy for abdominal malignancies, be-cause many authors have reported the development ofport-site metastases and peritoneal seeding after laparo-scopic manipulation of a tumor.

In 1994 Nduka and coworkers10 focused their atten-tion on three factors that might be involved in the patho-genesis of port-site metastases. First, repeated passage ofsurgical instruments through the trocars could be re-sponsible for the vehiculation of exfoliated viable tumorcells. Also, prolonged manipulation of a primary tumorresulting from the lack of tactile sensation during a lapa-roscopic operation could result in an increase in theprobability of a tumor exfoliation process. Finally, a po-

tential direct effect of pneumoperitoneum (tumor cellaerosolization) should also be considered. Isolated re-ports have indicated a possible effect of smoke and de-bris produced by tissue electrocoagulation on the even-tual peritoneal diffusion of neoplastic cells.11 Morerecently, a number of articles have clarified the contro-versies in this field: animal studies clearly demonstratethat carbondioxide-induced pneumoperitoneum doesnot represent a statistically significant risk factor of port-site metastases;12 other articles have stated that even iftumor cell aerosolization might eventually occur, it isonly associated with high gas flow and a considerableconcentration of viable neoplastic cells.13,14 Recently,Pearlstone and coworkers15 reported that the incidenceof port-site metastases does not show any statisticallysignificant difference from that described in cases of lo-cal tumor recurrence on surgical incisional wounds afteropen surgery for gastrointestinal malignancies, suggest-ing that it is the biological behavior of cancer cells (andnot surgical manipulation or pneumoperitoneum) thatshould be blamed for the pathogenesis of tumor implan-tation on any surgical scar. Finally, Reymond and co-workers14 have pointed out that the majority of port-sitemetastases are observed in patients who underwent lapa-roscopic procedures associated with poor protectivemeasures (ie, retrieval bag or gas flow relay control); it isour opinion that the variability in the incidence of port-site metastases, ranging from 0% to 21% as reported indifferent series, is dependent on the personal experienceand technique of the individual surgical operator. Atpresent, it can be concluded that port-site metastasesand possible peritoneal seeding of cancer cells should notrepresent a factor limiting a wider application of diag-nostic laparoscopy for abdominal malignancies.

LAPAROSCOPIC TECHNIQUES FOR GASTRICCANCER STAGINGLaparoscopic staging of gastric cancer has had quite dif-ferent modalities of application throughout the world indiverse geographic sites with strikingly different social

No competing intervers declared.

Received August 12, 2002; Accepted November 25, 2002.From the Department of Surgical Sciences, Catholic University of Rome, “AGemelli” Medical School, Rome, Italy.Correspondence address: Domenico M D’Ugo, MD, FACS, Catholic Uni-versity of Rome, “A Gemelli” Medical School, Lgo F Vito 1, 00168 Rome,Italy.

965© 2003 by the American College of Surgeons ISSN 1072-7515/03/$21.00Published by Elsevier Science Inc. doi:10.1016/S1072-7515(03)00126-1

and economic environments. On one hand, Possik andcolleagues4 in Brazil and Kriplani and Kapur5 in Indiahave applied a simple and basic laparoscopic staging tothe workup of gastric cancer patients, especially with theaim of limiting an unacceptably high rate of exploratorylaparotomies that, in most series, are associated withpostoperative morbidity in 12% to 23% of patients anda reported mortality ranging up to 21%.7,16,17 In theUSA, Western Europe, and Japan staging laparoscopyhas more recently been adopted, partly as a consequenceof the increasing indications in favor of multimodaltreatment plans; under such circumstances the maingoal of laparoscopic exploration is the application of amore accurate staging modality compared with conven-tional imaging, both for the selection of patients withtechnically unresectable gastric cancer (to be treated byinduction chemotherapy with radiologic or laparoscopicreevaluation at the end of treatment) and for patientswith locally advanced resectable disease that could rep-resent an indication for preoperative neoadjuvanttreatment.

Laparoscopic staging is generally performed undergeneral anesthesia, though some authors reported expe-riences under local anesthesia.18 In many instances, di-agnostic laparoscopy has been performed as a separateprocedure, but it can be performed immediately before aplanned open operation.16 The patient is placed supineon the operating table (in our practice, access to theabdominal cavity is provided by means of an open cut-down technique, usually performed periumbilically,while the Verres needle technique is seldom used becauseof concern related to vascular or visceral perforation). A10- to 12-mm “Hasson”-type catheter is inserted belowthe umbilicus into the peritoneal cavity and an angled30° scope is placed to obtain a wider view of the entiresupramesocolic area. Laparoscopic staging must be con-ducted following an “inverted TNM mode,” evaluatingat first the M factor (Figs. 1, 2), followed by the N and Tfactors (Figs. 3, 4). Before any maneuver of surgical stag-ing (in the absence of ascitic fluid that, if present, isinvariably aspirated and examined for immediate cytol-

ogy), 200 mL of normal saline are instilled into theperitoneal cavity. Specimens for cytology are aspiratedfrom the pelvis, subhepatic space, and the left upperquadrant. The parietal and visceral serosal surfaces of theperitoneum are inspected in a systematic fashion for ma-lignant implants. Discontinuous tumor deposits can beidentified and biopsied using endosurgical biopsy for-ceps. Placing the table in a Trendelenburg position facil-itates examination of the pelvis. In female patients, theovaries must be visualized in order to exclude Krukem-berg metastases. The visible surfaces of omentum, dia-phragm, and liver are then inspected; a palpating probeis inserted through a second 5-mm port, usually placedat the left of the midline, to obtain a minimal manipu-lation of the left liver lobe and the small intestine. Tiltingthe table facilitates the approach to the area of the stom-ach that is covered by the left liver lobe. Before deter-mining the extent of tumor infiltration on the gastricwall, the perigastric nodes are inspected along the greaterand lesser curvature, on the gastrohepatic ligament, andat the hepatic hilum.

As far as staging of the N factor is concerned, we differfrom other authors in that we do not routinely performa lymphonodal biopsy during preoperative laparoscopy;some reports have shown the low accuracy of N stagingby a “plain” laparoscopic exploration, when it is notimplemented by the use of laparoscopic ultrasonography(LUS)16,19 and—in our hands—the indication of a de-layed surgical exeresis after neoadjuvant chemotherapyhas, in most cases, been a consequence of T staging, withthe macroscopic evidence of an extraserosal infiltrationof the primary tumor. The most recent TNM classifica-tion of gastric carcinoma (5th ed, Union InternationaleContre le Cancer, 1997) with regard to lymphonodalinvolvement (N1, N2, and N3) is based on the numericcount of metastatic nodes, and the anatomic-topographic system—from the “Japanese” classificationsystem—was previously adopted.20 At present, this im-plies that only the removal and complete examination ofat least 15 nodes is capable of establishing if a node-positive patient is indeed to be considered N1 or N2;21

in rare circumstances, a single-node biopsy can be im-portant for the definition of the treatment strategy. Thishappens when preoperative imaging is strongly sugges-tive of a severe lymphonodal involvement but laparos-copy does not demonstrate any extraserosal primary tu-mor infiltration. In certain cases of T1–T2 tumors witha suspicion of advanced N staging at preoperative imag-

Abbreviations and Acronyms

CT � computed tomographyEDL� extended diagnostic laparoscopyLUS � laparoscopic ultrasonographyUS � ultrasonography

966 D’Ugo et al Laparoscopic Staging of Gastric Cancer J Am Coll Surg

ing, a single-node biopsy is performed, in the light of apossible indication for an induction treatment.

Most of the tumors localized on the anterior wall ofthe stomach can be inspected without manipulation.The position for the placement of the third trocar isdictated by the patient’s anatomy as it becomes evidentduring the laparoscopic examination (this port is the oneemployed for LUS or a possible lesser sac endoscopy[LSE] or both). When the tumor originates from theposterior wall or a posterior fixity is suspected, the pos-terior tumor mass can be lifted to test its mobility overthe pancreatic body capsule in order to perform a lessersac endoscopy. One of the probes can be inserted deeply

behind the stomach through an avascular area of thegastrocolic ligament for better staging accuracy and alonger operative time. In most of the series, the averageoperative time of this technique is 20 minutes.16,19

Lesser sac endoscopy was first experimented with andofficially patented in 1984 in the USSR. According tothe original description, the laparoscope is introducedinto the lesser sac through a window created in the gas-trocolic ligament attracted under laparoscopic control tothe surface of the abdominal wall through a 1.5- to 2-cmminilaparotomy incision (Fig. 5). While the lesser sac isinsufflated with the gas through the instrumental chan-nel of the laparoscope or trocar sheath, all organs andligaments forming the borders of the lesser sac are rou-tinely inspected. Instrumental palpation, aspiration,

Figure 1. Peritoneal carcinomatosis. Figure 2. Carcinomatosis of round ligament.

Figure 3. Extraserosal tumor infiltration (T3). Figure 4. Extraserosal tumor infiltration (T3).

967Vol. 196, No. 6, June 2003 D’Ugo et al Laparoscopic Staging of Gastric Cancer

puncture, and forceps biopsy are performed through theinstrumental channel of the laparoscope. The describedmethod permitted a better inspection of the head, body,and tail of the pancreas with respect to the classicalapproach.22

Extended diagnostic laparoscopyExtended diagnostic laparoscopy (EDL) was first ap-plied in 1995 by some authors participating in the Ger-man Gastric Cancer Study Group.23 It includes a con-ventional laparoscopic staging with peritoneal and lessersac exploration complemented by the use of LUS for abetter appreciation of pancreas, liver, and gastric wallthicknesses.

Since standard laparoscopy is a two-dimensional mo-dality, the lack of tactile sensation prevents the detectionof small intraparenchymal liver lesions and the palpatoryassessment of the T stage of the primary tumor. Intra-operative ultrasonography has the potential to overcomethis deficiency.24 Initially developed for the assessment ofhepatic disease, LUS has recently been used in benignbiliary tract disease and in the staging of hepatic andpancreatic malignancies.25-27

Generally, a flexible-tip, multifrequency (5 to 7.5MHz/6 to 10 MHz), curved-array ultrasonographicprobe with color-flow Doppler capability, which fitsthrough a 12-mm port, is used for LUS.28,29 LUS is usedto evaluate tumor size and extent, celiac and portalnodes, vascular invasion, and the involvement of contig-uous structures, and to perform a complete assessmentof the liver. Biopsies of suspected metastatic lesions are

taken under direct laparoscopic or ultrasonographicguidance using biopsy forceps or needle aspiration.30

Feussner and coworkers19 studied EDL in 111 gastriccancer patients: Overall, detailed laparoscopy plus LUSaltered the preoperative diagnosis in 46% of the patients(51 of 111) leading to changes in management in 45(40.5%). LUS proved to be useful in confirming or ex-cluding invasion and in revealing unsuspected liver me-tastases, and was responsible for a change in the diagno-sis in 15.7% of the patients. The authors conclude thatLUS should always form an integral part of diagnosticlaparoscopy.

DIAGNOSTIC ACCURACY OF LAPAROSCOPY INGASTRIC CANCERThe clinical role of ultrasonography (US) and computedtomography (CT) for the diagnosis of gastric cancer hasbeen questioned because of the low accuracy of thesemeans in clinical staging: The high false-negative rate forCT has been confirmed by prospective studies and someauthors have pointed out that negative US or CT scansdo not entirely exclude the possibility of liver or perito-neal malignancy.4,5

Gross and colleagues3 reported their experience with46 gastric cancer patients: metastatic disease was ob-served by laparoscopy in 27 out of 46 cases (57%) thathad been previously staged as MO (Table 1).

Possik and associates4 evaluated laparoscopic stagingin 360 patients with gastric cancer. They demonstratedan accuracy of 89% for the detection of peritoneal dis-semination and 96% for hepatic metastases.

Figure 5. Lesser sac endoscopy technique.


More recently, Kriplani and Kaipur5 performed pre-operative staging laparoscopy as a separate procedure ona series of 40 patients who were considered resectableafter a US and CT workup. Laparoscopy showed thepresence of unsuspected metastatic disease in 13% andunresectable T4 cancer in 27.5% of the patients with anoverall diagnostic accuracy of 92%.

Lowy and associates6 performed staging laparoscopyon 71 patients with potentially resectable gastric canceras determined by current-generation CT scanning: In 16(23%) of these patients, laparoscopy identified distantmetastatic disease undetected by conventional stagingand a surgical exploration was avoided in 12 of thesepatients.

Stell and coworkers7 performed a prospective com-parison of laparoscopy, US, and CT in gastric cancerstaging. With regard to the detection of hepatic metas-tases they reported an accuracy of 99% for laparoscopyversus 76% and 79%, respectively, for US and CT; sen-sitivity by laparoscopy was 96% compared with 37%and 52%, respectively, by US and CT. Concerning peri-toneal carcinomatosis, the accuracy was 94% for lapa-roscopy, 84% for US, and 81% for CT (sensitivity 69%by laparoscopy versus 23% and 8% by US and CT).

Burke and colleagues8 studied laparoscopy in a con-secutive series of 110 gastric cancer patients. Metastaticdisease was demonstrated in 37% of patients who wereconsidered to have localized gastric cancer by preopera-tive CT or endoscopic ultrasonography. Laparoscopy ac-curately staged 94% of patients with respect to meta-static disease. A sensitivity of 84% and a specificity of100% have been noted in this study. Compared withpatients who had an exploratory laparotomy only during

the same time period, postoperative hospital stay wassignificantly reduced (1.4 days versus 6.5 days).

In 1997 we prospectively compared the diagnosticaccuracy of preoperative laparoscopy with ultrasonogra-phy and computed tomography, respectively, in a mul-ticentric series of 70 patients and, more recently, in 100gastric cancer patients. In the latter series, laparoscopydetected 21 unsuspected metastases in 100 patients clin-ically considered as M0. Concerning locally advancedtumors, laparoscopy showed a sensitivity of 69.7% forT3 and 89.6% for T4 tumors, significantly higher thanUS/CT staging (respectively, 23.2% and 48.3%;p � 0.02). Laparoscopy showed an accuracy of 100%for M staging with an overall TNM staging accuracy of72% compared with 38% for US/CT.9,16

In summary, it can be stated that laparoscopy is arelatively simple, well-tolerated, and safe procedure.Though some controversies on the role of staging lapa-roscopy still exist,31 the majority of published reportsand our data9,16,32 support the belief that laparoscopy is avaluable technique in the staging of gastric cancer andconfirm its important role in the detection of under-staged metastatic disease compared with preoperativestaging.

CLINICAL IMPLICATIONS OF STAGINGLAPAROSCOPY AND DIAGNOSTIC-THERAPEUTIC PROTOCOLSDespite a decline in its incidence, gastric carcinoma re-mains one of the most common malignant tumors in theworld.

In Europe and the US, curative resection is performedin less than 60% of all gastric cancers, because most

Table 1. Diagnostic Accuracy of Laparoscopy in Gastric Cancer

Firstauthor Year

No. ofpatients

Preoperativeimaging

M1undetected

disease(%)

Accuracy(%)

Avoidedexploratory

laparotomies(%)

Gross3 1984 46 NR 57 NR NRPossik4 1986 360 US/liver scintigraphy 34 89, 96* NRKriplani5 1991 40 US/CT 13 92 NRLowi6 1996 71 CT 23 94, 33* 17Stell7 1996 103 US/CT NR 94, 99* 20Burke8 1997 110 CT 37 94 22D’Ugo9 1997 100 US/CT 21 100† 21

*Peritoneal metastases and liver metastases, respectively.†Accuracy for M staging.CT, computed tomography; NR, not reported; US, ultrasonography.


patients are locally advanced or metastatic at presenta-tion. Surgical therapy still represents the treatment ofchoice for gastric cancer, but, with locally advanced tu-mors, surgery alone seems to have reached its limits interms of the rate of curative resections and longtermsurvival.

Multimodal treatment options have preliminarilyshown promising results, but a precise evaluation ofthese treatments is strictly dependent on an accuratepatient selection with a reliable staging of tumor exten-sion, lymphonodal involvement, and the site of distantmetastases.19

To date, the introduction of videolaparoscopy andendoscopic ultrasonography have radically modifiedconventional imaging methods for gastric cancer stag-ing: videolaparoscopy has already shown considerablybetter results in the detection of unstaged metastaticdisease; preoperative laparoscopy in the prevention ofunnecessary surgical exploration has been evaluated bypreviously discussed reports4,5,7,29 and it certainly repre-sents a powerful diagnostic tool to avoid “open andclose” operations,32 since M� disease should not be re-sected in the absence of obstruction or bleeding.16 Thereis some evidence that laparoscopy permits a more accu-rate staging of extraserosal tumors (T3–T4) and, to date,an even more crucial task is assigned to preoperativelaparoscopy; indeed, after 30 years of adjuvant treatmenttrials, it has been ascertained that patients who present

locally advanced but resectable diseases (T3–T4, any N,M0) have a low chance of cure after a complete surgicalresection followed by an adjuvant chemotherapeuticregimen. Conversely, when a preoperative treatmentprotocol is applied, laparoscopy represents a useful toolfor patient selection, ruling out any unhelpful delay ofsurgery in nonadvanced cases.23,33 An increasing numberof institutions throughout the world are consequentlyrecommending neoadjuvant treatment protocols for lo-cally advanced gastric cancer, provided the disease is“properly staged.”34

Some authors have published their decision-makingflow charts6,9,29 on patient selection for a possible enroll-ment in a preoperative chemotherapy trial. In all ofthem, diagnostic laparoscopy played a crucial role (Figs.6–8).

It is our opinion that further trials of neoadjuvanttreatment for both resectable and unresectable gastriccarcinomas are needed. These experiences must be re-stricted to controlled studies that include a thoroughenrollment of homogeneously selected cases through aconstant application of laparoscopic staging modalities.

Recently, some articles have focused on the impact ofstaging laparoscopy on the clinical decision-making pro-cess, weighing the rate at which this procedure alters theclinical stage, thus determining a fallback on the treat-ment strategy.18,19

We evaluated how frequently diagnostic laparoscopy

Figure 6. Treatment algorithm for gastric cancer. (Reprinted from: Conlon KC, Karpeh MS.Laparoscopy and laparoscopic ultrasound in the staging of gastric cancer. Semin Oncol 1996;23:347–351, with permission.)


modifies conventional clinical T and M staging and itsconsequent impact on treatment strategies for gastriccancer. In a subset of 91 gastric cancer patients conven-tionally staged as M0 who underwent pretherapeuticlaparoscopic staging, the results of laparoscopy modifiedthe clinically established T and M values in 58.2% of thetotal number of patients; previously undetected metas-tases were evidenced in 13.1% of patients and the Tvalue was upgraded in 32% and downgraded in 13.1%of the patients.

Preoperative laparoscopy provided no additionalfindings compared with the clinical stage in 54.9%, butit modified preoperative therapeutic strategy in 49 of 91patients (53.8%), confirming its crucial role in staginggastric carcinoma.35

FUTURE DEVELOPMENTSPeritoneal cytologyBurke and coworkers8 had examined the therapeutic im-pact of peritoneal lavage cytology obtained at the time oflaparoscopic staging. Laparoscopic washings were ob-

tained from 127 consecutive patients with gastric cancer.A correlation between the extent of the disease and theprevalence of positive cytology was observed. No patientwith early disease (T1–T2, M0) revealed positive cytol-ogy. In contrast, 10% of patients with T3–T4, M0 and59% of patients with M1 disease had positive cytology.

Notably, even in the absence of macroscopic meta-static disease, patients with positive cytology showed aprognosis identical to those with macroscopically obvi-ous metastatic disease, showing that positive lavage cy-tology indicates microscopic peritoneal metastatic dis-ease. It is our belief that these patients behave like thosewith macroscopic peritoneal or hepatic metastases, andso should be staged as M1.

Ribeiro and colleagues36 recently reported similar re-sults in a study of 49 consecutive patients with gastriccancer who underwent laparoscopic staging. Lavage cy-tology was performed when ascites was absent. In theabsence of macroscopic peritoneal carcinomatosis, pos-itive cytology was observed in 29%. Positive cytologywas correlated with the depth of invasion, histologicalsubtype, advanced Borrmann class, and stage IV tumors.These authors suggested that cytology added sensitivityto the laparoscopic examination and that it might signif-icantly alter the therapeutic approach. More recently,Bryan and coworkers37 evaluated the prognostic impactof peritoneal lavage in a series of 88 patients who under-went diagnostic laparoscopy for esophagus and stomachcancer. In 11 patients with free peritoneal tumor cells,

Figure 8. Treatment algorithm for gastric cancer. (Reprinted from:D’Ugo DM, Persiani R, Caracciolo F, et al. Selection of locallyadvanced gastric carcinoma by preoperative staging laparoscopy.Surg Endosc 1997;11:1159–1162, with permission.)

Figure 7. Treatment algorithm for gastric cancer. (Reprinted fromLowy AM, Mansfield PF, Steven D, et al. Laparoscopic staging forgastric cancer. Surg 1996;119:611–614, with permission.)


median survival was 122 days, with only 1 patient sur-viving for more than 1 year. Among patients who did notshow free peritoneal tumor cells, median survival was378 days; this difference was statistically significant(p � 0.001). These results led the authors to concludethat the presence of free peritoneal tumor cells representsa contraindication for a curative resection.

Second-look laparoscopyAs far as the efficacy of any kind of presurgical inductiontherapy is concerned, it is crucial to establish precisecriteria for an accurate evaluation of the tumor responseafter preoperative treatment.

In our series of neoadjuvant chemotherapy for locallyadvanced resectable gastric carcinoma patients,38 evalu-ation of the response is preliminarily performed by mor-phometric comparison of pretreatment imaging (endos-copy and CT scan and laparoscopic staging) withimmediate preoperative imaging and intraoperative tu-mor restaging. All patients belonging to this categoryundergo surgery. Under such circumstances (resectableadvanced disease) the primary objectives of the multi-modal treatment are the increase of the R0 resection rateand possibly an improvement in longterm survival;second-look laparoscopy is not applied in this patientgroup.

On the other hand, when preoperative chemotherapyis applied to similarly locally advanced but technicallyunresectable cancers, second-look laparoscopy mightrepresent a powerful tool in ruling out from an unhelp-ful delayed exploration those patients who do not re-spond to medical treatment and do not warrant pallia-tion for stenosis or bleeding.

Laparoscopic palliation of unresectablegastric cancerPatients with incurable malignant disease accompaniedby distal gastric obstruction have a very poor prognosis.A few decades ago, the only therapeutic possibility forpalliation and relief from symptoms (gastric outlet ob-struction or jaundice or both) was gastroenterostomy orbilioenteric anastomosis via laparotomy, or both.39 Thisoperation, though providing satisfying functional re-sults, remains quite invasive. It is related to a consider-able period of hospitalization and to pain, discomfort,and possible complications. Open gastroenterostomy

for palliation of malignancies has been associated withdelayed gastric emptying in up to 16% of cases and withmorbidity and mortality rates, respectively, of 25% and8% to 17%.40 The effort to reduce operative trauma inunresectable cancer patients resulted in the developmentof minor access or laparoscopic palliative operations.While laparoscopic surgery with curative intention formalignant disease has already been shown to be highlycontroversial,41,42 palliative laparoscopic proceduresare certainly particularly beneficial for patients whogenerally have a very short life expectancy. Some ofthe advantages offered by laparoscopic palliative surgeryare reduced pain, a short recovery time, and a shorthospital stay, allowing the surgical procedure to interfereas little as possible with the quality of life. For this rea-son, over the last few years, several authors have startedto perform gastroenterostomy routinely via laparoscopicaccess.43,44

Brune and coworkers,45 performed laparoscopic gas-trojejunostomy in 16 patients with gastrointestinal ma-lignancies. Laparoscopic gastrojejunostomy was per-formed as an antecolic isoperistaltic side-to-sideanastomosis with a 30-mm Endo-GIA stapler (UnitedStates Surgical Corp) with an enterostomy 25 cm belowthe gastrojejunostomy to assure sufficient biliary drain-age from the afferent loop and to avoid exposure of thegastric anastomosis to bile acids.

In conclusion, preoperative staging laparoscopy is asafe, simple, and relatively cheap procedure at mostmedical institutions. For locally advanced gastric cancer,our data support the belief that, to date, laparoscopyplays two fundamental roles: On one hand, it undoubt-edly represents the most specific method for detectingpreviously unsuspected M� disease, sparing unresect-able cases from unnecessary surgical exploration. On theother hand, following the increasing application of neo-adjuvant treatment protocols for stage IIIa–IIIb tumors,we have seen that laparoscopy permits the most reliableand accurate selection of T3 and T4 patients, avoidingan unhelpful delay of surgery in nonadvanced cases. Ac-curate staging by preoperative videolaparoscopy allowsfor a more homogeneous evaluation of the treatmentresults in the context of research studies. Finally, theapplication of “second-look” laparoscopy in selectedcases might offer a chance to verify a possible tumordownstaging and to detect the sites of residual diseaseafter neoadjuvant treatment.


REFERENCES

1. Jacobaeus HC. Kurze Ubersicht uber meine Erfahrungen mitder Laparoskopie. Munch Med Wochenschr 1911;58:2017–2019.

2. Greene FL. Laparoscopy in malignant disease. Surg Clin NorthAm 1992;72:1125–1136.

3. Gross E, Bancewicz J, Ingram G. Assessment of gastric cancer bylaparoscopy. Br Med J (Clin Res Ed) 1984;288:1577.

4. Possik RA, Franco EL, Pires DR, et al. Sensitivity, specificity andpredictive value of laparoscopy for the staging of gastric cancerand for the detection of liver metastases. Cancer 1986;58:1–6.

5. Kriplani AK, Kapur BML. Laparoscopy for pre-operative stag-ing and assessment of operability in gastric carcinoma. Gastro-intest Endosc 1991;37:441–443.

6. Lowy AM, Mansfield PF, Steven D, et al. Laparoscopic stagingfor gastric cancer. Surg 1996;119:611–614.

7. Stell DA, Carter CR, Stewart I, et al. Prospective comparison oflaparoscopy, ultrasonography and computed tomography in thestaging of gastric cancer. Br J Surg 1996;86:1260–1262.

8. Burke EC, Karpeh MS, Conlon KC, et al. Laparoscopy in themanagement of gastric adenocarcinoma. Ann Surg 1997;225:262–267.

9. D’Ugo DM, Persiani R, Caracciolo F, et al. Selection of locallyadvanced gastric carcinoma by preoperative staging laparoscopy.Surg Endosc 1997;11:1159–1162.

10. Nduka CC, Monson JRT, Menzies-Gow N, et al. Abdominalwall metastases following laparoscopy. Br J Surg 1994;81:648–652.

11. Taffinder NJ, Champault G. Port site metastases after laparo-scopic colorectal surgery for cure of malignancy. Br J Surg 1996;83:133.

12. Ishida H, Murata N, Yamada H, et al. Influence of trocar place-ment and CO2 pneumoperitoneum on port site metastases.Surg Endosc 2000;14:193–197.

13. Wittich P, Marquet RL, Kazemier G, et al. Port site metastasesafter CO2 laparoscopy. Is the aerosolization of tumor cells apivotal factor? Surg Endosc 2000;14:189–192.

14. Reymond MA, Schneider C, Kastl S, et al. The pathogenesis ofport site recurrences. J Gastrointest Surg 1998;2:406–414.

15. Pearlstone DB, Feig BW, Mansfield PF. Port site recurrencesafter laparoscopy for malignant disease. Semin Surg Oncol1999;16:307–312.

16. D’Ugo DM, Coppola R, Persiani R, et al. Immediately preop-erative laparoscopic staging for gastric cancer. Surg Endosc1996;10:996–999.

17. Wanebo HJ, Kennedy BJ, Chmiel J, et al. Cancer of the stom-ach. A patient care study by the American College of Surgeons.Ann Surg 1993;218:583–592.

18. Yano M, Tsujinaka T, Shiozaki H, et al. Appraisal of treatmentstrategy by staging laparoscopy for locally advanced gastric can-cer. World J Surg 2000;24:1130–1136.

19. Feussner H, Omote K, Fink U, et al. Pretherapeutic laparoscopicstaging in advanced gastric carcinoma. Endoscopy 1999;31:342–347.

20. Sobin LH, Fleming ID. TNM classification of malignant tu-mors. 5th ed. Union Internationale Contre le Cancer and theAmerican Joint Committee on Cancer. Cancer 1997;80:1803–1804.

21. D’Ugo D, Pacelli F, Persiani R, et al. Impact of latest TNMclassification for gastric cancer: retrospective analysis on 94 D2gastrectomies. World J Surg 2002;6:672–677.

22. Charukhchyan SA, Lucas GW. Laparoscopy and lesser sac en-doscopy in gastric carcinoma operability assessment. Am Surg1998;64:160–164.

23. Fink U, Stein HJ, Schuhmacher C, et al. Neoadjuvant chemo-therapy for gastric cancer: an update. World J Surg 1995;19:509–516.

24. Ascher SM, Evans SRT, Zeman RK. Laparoscopic cholecystec-tomy: intraoperative ultra-sound of the extra-hepatic biliary treeand the natural history of postoperative transabdominal ultra-sounds findings. Semin Ultrasound 1993;14:331–337.

25. Marugiah M, Paterson-Brown S, Winsdor JA, et al. Early expe-rience of laparoscopic ultrasonography in the management ofpancreatic carcinoma. Surg Endosc 1993;7:119–124.

26. Cuesta MA, Mejer S, Borgstein PJ, et al. Laparoscopic ultra-sonography for hepato-biliary and pancreatic malignancy. Br JSurg 1993;80:1571–1574.

27. John TG, Greig JD, Carter DC, et al. Carcinoma of the pancre-atic head and periampullary region: tumor staging with laparos-copy and laparoscopic ultrasonography. Ann Surg 1995;221:156–164.

28. Velasco JM, Rossi H, Hieken TJ, Fernandez M. Laparoscopicultrasound enhances diagnostic laparoscopy in the staging ofintra-abdominal neoplasms. Am Surg 2000;66:407–411.

29. Conlon KC, Karpeh MS. Laparoscopy and laparoscopic ultra-sound in the staging of gastric cancer. Semin Oncol 1996;23:347–351.

30. Van Dijkum JN, De Wit LTH, Van Delden OM, et al. Staginglaparoscopy and laparoscopic ultrasonography in more than 400patients with upper gastrointestinal carcinoma. J Am Coll Surg1999;189:459–465.

31. Lehnert T, Rudek B, Kienle P, et al. Impact of diagnostic lapa-roscopy on the management of gastric cancer: prospective studyof 120 consecutive patients with primary gastric adenocarci-noma. Br J Surg 2002;89:471–475.

32. Picciocchi A, D’Ugo D, Ronconi P, et al. The impact of staginglaparoscopy on the treatment of locally advanced gastric cancer.J Exp Clin Cancer Res 1997;16:84–86.

33. Sendler A, Dittler HJ, Feussner H. Preoperative staging of gas-tric cancer as a precondition for multimodal treatment. WorldJ Surg 1995;19:501–508.

34. Siewert JR, Maruyama K. What’s new in gastric cancer? WorldJ Surg 1995;19:483.

35. Persiani R, Pende V, Picciocchi A, et al. Laparoscopic staging ofgastric carcinoma; diagnostic and therapeutic approach. Proc4th Int Cong EAES, Nice, France, 2000.

36. Ribeiro U, Gama-Rodrigues JJ, Bitelman B, et al. Value ofperitoneal lavage cytology during laparoscopy staging of pa-tients with gastric carcinoma. Surg Laparosc Endosc 1998;8:132–135.

37. Bryan RT, Cruickshank NR, Needham SJ, et al. Laparoscopicperitoneal lavage in staging gastric and oesophageal cancer. EurJ Surg Oncol 2001;27:291–297.

38. D’Ugo D, Persiani R, Pende V, et al. Neoadjuvant chemother-apy for locally advanced gastric cancer: results on an ongoingphase II study. Proc 4th Int Gastric Cancer Cong, New York,2001.

39. Watanapa P, Williamson RCN. Surgical palliation for pancre-atic cancer: developments during the past two decades. Br J Surg1992;79:1348.

40. De Roij PD, Rogatko A, Brennan M. Evaluation of palliativesurgical procedures in unresectable pancreatic cancer. Br J Surg1991;78:1053–1058.


41. Rosin D, Brasesco O, Rosenthal RJ. Laparoscopy for gastrictumors. Surg Oncol Clin N Am 2001;10:511–529.

42. Azagra JS, Goergen M, De Simone P, et al. Minimally invasivesurgery for gastric cancer. Surg Endosc 1999;13:351–357.

43. Nathanson LK. Laparoscopic colecisto-jejunostomy and gastro-enterostomy for malignant disease. Surg Oncol 1993;2[suppl1]:19–24.

44. Sosa JL, Zalewski M, Puente I. Laparoscopic gastro-jejunostomy technique: case report. Laparoendosc Surg 1994;4:215–220.

45. Brune IB, Feussner H, Neuhaus H, et al. Laparoscopic gastro-jejunostomy and endoscopic biliary stent placement for pallia-tion of incurable gastric outlet obstruction with cholestasis. SurgEndosc 1997;11:834–837.


Documents

Laparoscopic staging of gastric cancer: an overview