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Staging Laparoscopy in the Management of GastricCancer: A Population-Based AnalysisPaul J Karanicolas, MD, PhD, Elena B Elkin, PhD, Lindsay M Jacks, MSc, Coral L Atoria, MPH,

ivian E Strong, MD, FACS, Murray F Brennan, MD, FACS, Daniel G Coit, MD, FACS

BACKGROUND: Staging laparoscopy can detect radiographically occult peritoneal metastases and prevent futilelaparotomy in patients with gastric adenocarcinoma. We sought to assess the use of staginglaparoscopy for gastric adenocarcinoma in a cohort of older patients and to compare outcomesafter laparoscopy alone with nontherapeutic laparotomy.

STUDY DESIGN: Using Surveillance, Epidemiology and End Results (SEER) population-based cancer registrydata linked with Medicare claims, we identified patients aged 65 or older diagnosed with gastricadenocarcinoma between 1998 and 2005. We defined staging laparoscopy as a laparoscopicprocedure from 1 month before the date of diagnosis until death and futile laparotomy as alaparotomy in the absence of a therapeutic intervention. We examined trends in the use ofstaging laparoscopy and compared outcomes between patients who underwent staging laparos-copy alone and those who had a futile laparotomy.

RESULTS: Of 11,759 patients with gastric adenocarcinoma, 6,388 (54.3%) had at least 1 surgical proce-dure. Staging laparoscopy was performed in 506 (7.9%) patients who had any surgery, and 151(29.8%) of these patients did not have a subsequent therapeutic intervention. Patients whounderwent staging laparoscopy alone had a significantly lower rate of in-hospital mortality(5.3% vs 13.1%, p � 0.001) and shorter length of hospitalization (2 vs 10 days, p � 0.001)than patients who had futile laparotomy.

CONCLUSIONS: Our findings in this large, population-based cohort suggest that staging laparoscopy is usedinfrequently in the management of older patients with gastric adenocarcinoma. Increased use ofstaging laparoscopy could reduce the substantial morbidity and mortality associated with non-therapeutic laparotomy. (J Am Coll Surg 2011;213:644–651. © 2011 by the American Collegeof Surgeons)

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More than 21,000 new cases of gastric cancer are diagnosedannually in the United States.1 The overall prognosis for pa-tients with advanced disease is poor. The extent of disease atpresentation is the most important predictor of prognosis andis a key determinant of the appropriate therapeutic modality.In the absence of metastases, resection of all gross disease withnegative microscopic margins offers the only chance for cure.2,3

Preoperative staging typically includes a combination ofendoscopy, cross-sectional imaging (CT scan or MRI), en-

Disclosure Information: Authors have nothing to disclose. Timothy J Eber-lein, Editor-in-Chief, has nothing to disclose.Abstract presented at the American College of Surgeons 96th Annual ClinicalCongress, Surgical Forum, Washington, DC, October 2010.

Received May 20, 2011; Revised July 20, 2011; Accepted July 20, 2011.From the Departments of Surgery (Karanicolas, Strong, Brennan, Coit) andEpidemiology and Biostatistics (Elkin, Jacks, Atoria), Memorial Sloan-Kettering Cancer Center, New York, NY.Correspondence address: Paul J Karanicolas, MD, PhD, Department of Sur-gery, Memorial Sloan-Kettering Cancer Center, 1275 York Ave, New York,
NY, 10065. email: [email protected]
644© 2011 by the American College of SurgeonsPublished by Elsevier Inc.

doscopic ultrasound, and PET scan. Despite appropriatestaging with these modalities, up to 30% of patientswith no preoperative evidence of metastatic disease harboroccult intra-abdominal metastases (peritoneal, liver, ornonregional lymph nodes) at the time of operation (Table1).4-12 In these patients, resection yields no improvement inurvival and is rarely needed for palliation of symptomsmost commonly, obstruction or bleeding).13 Staging lap-roscopy may detect occult metastatic disease and spare theatient an unnecessary laparotomy, resulting in fewer com-lications, less operating room time, and shorter hospitaltay.14 Staging laparoscopy may be particularly advanta-

geous in older patients, who are at higher risk of sufferingcomplications from laparotomy.15

Despite the demonstrated benefits of staging laparos-copy, the uptake of this management approach in prac-tice is unclear. We sought to explore trends in the useand outcomes of staging laparoscopy for gastricadenocarcinoma in a population-based cohort of older
adults.
ISSN 1072-7515/11/$36.00doi:10.1016/j.jamcollsurg.2011.07.018

mailto:[email protected]

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645Vol. 213, No. 5, November 2011 Karanicolas et al Staging Laparoscopy for Gastric Cancer

METHODSDataThe primary data source was the Surveillance, Epidemiol-ogy and End Results (SEER) cancer registry data linkedwith Medicare claims and enrollment records. SEER is theNational Cancer Institute (NCI)-sponsored program ofcancer registries in selected geographic regions coveringabout 25% of the US population.16 The SEER registriescollect data regarding site and extent of disease, first courseof cancer-directed therapy, and sociodemographic charac-teristics, with active follow-up for date and cause of death.Medicare is the primary health insurer for 97% of the USpopulation 65 years or older. Hospitalization informationfor those eligible for Medicare Part A is available from theMedicare Provider Analysis and Review files. Outpatientand physician or supplier Medicare files for services ren-dered in physicians’ offices and hospital outpatient depart-ments are available for the 95% of Medicare beneficiarieswho elect Part B coverage. Approximately 93% of SEERpatients 65 years or older have been successfully linkedwith their Medicare claims.16 The SEER-Medicare files

ere used in accordance with a data-use agreement fromhe NCI, and the study was approved by the Institutionaleview Board at Memorial Sloan-Kettering Cancer Center.

CohortWe identified all patients aged 65 or over with primarygastric adenocarcinoma diagnosed between January 1,1998 and December 31, 2005. Based on Medicare claimsfor surgical procedures from 1 month before the date ofdiagnosis until death, we restricted the cohort to patientswho had an operative procedure for gastric cancer (Appen-dix, online only, for procedure codes). We excluded pa-tients diagnosed only at the time of death, who had a his-tory of another malignancy, who lacked Parts A or B of

Table 1. Summary of Studies Examining the Rate of Intra-abdominal Occult Metastases at the Time of Staging Lapa-roscopy in Patients with Gastric CancerFirstauthor Year n

Preoperativeworkup

Occultmetastases, %

Possik8 1986 360 US 34Kriplani6 1991 40 US CT 13Lowy7 1996 71 CT 23Stell11 1996 103 US,CT 34Ascencio4 1997 76 US,CT 41D’Ugo5 1997 100 US,CT 21Romijn9 1998 20 US,CT 40Yano12 2000 32 US,CT 34Sarela10 2006 657 CT 31

US, ultrasound.

Medicare, and those enrolled in a managed care plan.

Outcomes and predictorsThe primary endpoint was type of gastric cancer surgeryreceived from 1 month before diagnosis through the date ofdeath or end of follow-up. Therapeutic intervention wasdefined by the presence of a claim for gastric resection orgastric bypass (Fig. 1). A patient was classified as havinglaparotomy alone if there was a claim for laparotomy in theabsence of a therapeutic intervention on the same day orearlier. If a patient had a therapeutic intervention at a laterdate, we assumed that metastatic disease was identified atthe initial laparotomy and the subsequent therapeutic in-tervention was needed for palliation of symptoms. Addi-tional endpoints were in-hospital mortality (defined as dis-charge status of dead) and length of hospital stay (for thefirst chronological procedure in patients who had multipleoperations).

Several patient and disease characteristics were as-sessed. Demographic characteristics included patientage, race, marital status, geographic location, and resi-dence in a metropolitan vs a nonmetropolitan county.Clinical characteristics included location of the cancerwithin the stomach, tumor stage, grade, and nodal in-volvement. Comorbidity was estimated using the Charl-son comorbidity index based on inpatient claims in the12 months before cancer diagnosis.17 We assessed the useof neoadjuvant chemotherapy by identifying claims forchemotherapy between the month of cancer diagnosisand the date of resection.

AnalysisAssociations between patient and disease characteristicsand receipt of staging laparoscopy were assessed using chi-square tests. We used multivariable logistic regression anal-ysis to evaluate potential predictors of staging laparoscopy,including only characteristics that would be known preop-eratively: age, sex, race, marital status, comorbidity, geo-graphic region, and site of the tumor within the stomach.Similar analyses were performed to assess predictors of re-section. We explored time trends in the use of staging lap-aroscopy using the Cochran-Armitage test for trend. Dif-ferences in the rate of in-hospital mortality and medianlength of hospital stay were compared between those re-ceiving staging laparoscopy alone and laparotomy aloneusing the chi-square test and Wilcoxon rank-sum test, re-spectively. All statistical analyses were performed using SASversion 9.2 (SAS Institute Inc) software.

RESULTSDuring the 8-year study period, 11,759 patients were di-agnosed with gastric adenocarcinoma and 6,388 patients
underwent an operative procedure. Staging laparoscopy

a

cedur

646 Karanicolas et al Staging Laparoscopy for Gastric Cancer J Am Coll Surg

was performed in 506 (8%) patients who had any opera-tion (Fig. 2). Of these patients, 151 (30%) did not have afurther operative intervention (ie, staging laparoscopyalone) and 306 (60%) proceeded to have a therapeuticintervention (resection in 97% of patients). Of the 5,882patients who did not have laparoscopy as part of their man-agement, 5,304 (90%) had a therapeutic intervention (re-section in 94% of these patients).

The use of staging laparoscopy increased over the studyperiod from 5.5% in 1998 to 11.1% in 2005 (p � 0.01,Fig. 3).The rate of staging laparoscopy alone also increased,from 1.7% to 3.1% (p � 0.01), and the rate of laparotomylone was stable over time (p � 0.52).

Figure 1. Pro

Figure 2. Classification of cohort by ty

Patients who had staging laparoscopy were more likely tobe young, white, married, have less comorbidity, be treatedin the Northeast, and have proximal tumors, comparedwith those who did not have laparoscopy (Table 2). Only4% of patients received neoadjuvant chemotherapy, andthis proportion did not vary by use of staging laparoscopy(data not shown). In multivariable analysis, significant pre-dictors of staging laparoscopy were younger age, white race,lower comorbidity score, Northeast region, and proximaltumors (Table 3). Significant predictors of resection com-pared with any other gastric operation were Asian race,being married, and having a distal tumor (Table 4). Amongpatients who had any therapeutic intervention the most

e definitions.

pe of gastric cancer procedures.

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common procedure was distal gastrectomy, independent ofthe use of staging laparoscopy (Table 5).

Patients who had laparoscopy alone had a shorter lengthof hospital stay (2 days vs 10 days, p � 0.01) and a lowern-hospital mortality rate (5.3% vs 13.1%, p � 0.01) com-ared with patients who had laparotomy alone.

DISCUSSIONThis large, population-based analysis of patients over theage of 65 years who underwent gastric cancer surgery in theUS highlights several important findings. Despite clearbenefits of staging laparoscopy in patients without radio-logic evidence of metastases, only 8% of patients had stag-ing laparoscopy during the course of their manage-ment.13,14 In patients who did undergo laparoscopy, 30%did not have a later therapeutic intervention, presumablydue to occult metastases identified at the time of laparos-copy. In an additional 10% of patients a laparotomy wasperformed without therapeutic intervention, likely due tooccult metastases or locally unresectable disease that wasnot identified at the time of laparoscopy. The low currentuse of staging laparoscopy in the US suggests an opportu-nity to improve patient selection and thereby reduce themorbidity of futile laparotomy in this group of patients.

Interpreting the findings from patients who did not un-dergo a staging laparoscopy as part of their management ismore difficult. Based on the proportion of patients whounderwent staging laparoscopy or laparotomy alone afterlaparoscopy, one might expect 40% of patients who did not

Figure 3. Trends in use of staging laparoscalone.

undergo staging laparoscopy to have a futile laparotomy. In

actuality, 90% of these patients underwent a therapeuticintervention, with only 10% having a laparotomy alone.There are at least 2 possible explanations for this apparentdiscrepancy. It is possible that surgeons effectively stratifiedpatient risk of occult metastases and appropriately selectedpatients at higher risk for metastatic disease to undergostaging laparoscopy. However, the similar tumor and nodalstages between patients who had laparoscopy and thosewho did not have laparoscopy suggest this was not the case.Another, more compelling explanation is that a substantialproportion of these patients underwent therapeutic inter-vention in the setting of metastatic disease. It is likely thatin some cases, having subjected patients to the morbidity oflaparotomy, surgeons chose to perform a “palliative” resec-tion or bypass despite metastases. The higher ratio of by-pass to resection in patients who did not undergo staginglaparoscopy supports this hypothesis. Although some sur-geons may justify laparotomy in the setting of metastaticdisease to perform a bypass, in a series of 165 patients withoccult metastases detected at the time of laparoscopy, only12% subsequently required laparotomy for symptoms.13

Given the substantially increased morbidity and mortalityfrom laparotomy compared with laparoscopy, this ap-proach should be discouraged.

Although the stage of disease was similar betweengroups, there were some differences in the characteristics ofpatients who underwent staging laparoscopy comparedwith those who did not. Patients who had staging laparos-copy were generally younger and had less comorbidity than

taging laparoscopy alone, and laparotomy
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patients who did not. This trend is counterintuitive be-

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Table 2. Characteristics of Study Cohort by Use of Staging Laparoscopy

Characteristic

All patients(n � 6,388)

Staging laparoscopy(n � 506)

No staging laparoscopy(n � 5,882) p

Valuen % n % n %

Age at diagnosis, y

65 – 69 1,232 19 140 28 1,092 19 �0.01

70 – 74 1,534 24 139 27 1,395 24

75 – 79 1,617 25 110 22 1,507 26

80 � 2,005 31 117 23 1,888 32

ex

Male 3,649 57 298 59 3,351 57 0.40

Female 2,739 43 208 41 2,531 43

ace

White 4,282 67 387 76 3,895 66 �0.01

Black 712 11 47 9 665 11

Asian 733 11 29 6 704 12

Hispanic 264 4 17 3 247 4

Other/unknown 397 6 26 5 371 6

arital status

Married 3,612 57 309 61 3,303 56 �0.01

Not married 2,564 40 173 34 2,391 41

Unknown 212 3 24 5 188 3

harlson Comorbidity Score

0 3,216 50 268 53 2,948 50 �0.01

1 – 2 1,735 27 153 30 1,582 27

3� 1,437 23 85 17 1,352 23

egion

West 3,171 50 211 42 2,960 50 �0.01

Midwest 881 14 71 14 810 14

Northeast 1,554 24 165 33 1,389 24

South 782 12 59 12 723 12

ocation in the stomach

Cardia/fundus 1,452 23 129 25 1,323 22 �0.01

Body 535 8 52 10 483 8

Antrum/pylorus 2,005 31 104 21 1,901 32

Lesser curve 720 11 48 9 672 11

Greater curve 328 5 32 6 296 5

Overlapping/other 1,348 21 141 28 1,207 20

Stage

T0/Tis/T1 1,348 21 112 22 1,236 21 �0.01

T2a 594 9 35 7 559 10

T2b 1,735 27 100 20 1,635 28

T3 835 13 60 12 775 13

T4 737 12 55 11 682 12

TX 1,139 18 144 28 995 17

ymph nodes

Negative 2,416 38 174 34 2,242 38 �0.01

Positive 3,197 50 210 42 2,987 51

Unknown 775 12 122 24 653 11

rade

Well differentiated 303 5 18 4 285 5 �0.01

Moderately differentiated 1,722 27 126 25 1,596 27

Poor/undifferentiated 3,723 58 275 54 3,448 59

Unknown 640 10 87 17 553 9

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cause elderly patients with comorbidities are likely to ben-efit most from avoidance of nontherapeutic laparotomy.Surgeons selected patients with more proximal tumors forlaparoscopy, which is appropriate given the increased inci-dence of occult metastases in patients with proximal tu-mors.10 Patients with distal tumors would also be moreamenable to palliative bypass, which could influence sur-geons away from performing staging laparoscopy. Greateruse of laparoscopy in married patients and white patientssuggests that social support and socioeconomic status mayalso influence surgical decisions.

Table 3. Predictors of Staging Laparoscopy

PredictorAdjustedodds ratio 95% CI p Value

Age at diagnosis, y65 – 69 Ref �0.0170 – 74 0.76 0.59 – 0.9875 – 79 0.56 0.43 – 0.7380 � 0.49 0.37 – 0.64

exMale Ref 0.56Female 1.06 0.87 – 1.30

aceWhite Ref �0.01Black 0.75 0.54 – 1.05Asian 0.50 0.33 – 0.75Hispanic 0.75 0.45 – 1.16Other/unknown 0.71 0.46 – 1.09arital StatusMarried Ref 0.06Not married 0.83 0.67 – 1.02Unknown 1.33 0.84 – 2.08

harlson ComorbidityScore

0 Ref �0.011 – 2 1.18 0.96 – 1.463� 0.76 0.59 – 0.99

egionWest Ref �0.01Midwest 1.09 0.81 – 1.46Northeast 1.50 1.19 – 1.89South 1.00 0.72 – 1.37

ocation in the stomachAntrum/pylorus Ref �0.01Cardia/fundus 1.44 1.09 – 1.90Body 1.89 1.33 – 2.68Lesser curve 1.27 0.89 – 1.81Greater curve 1.81 1.19 – 2.75Overlapping/other 1.96 1.50 – 2.56

Ref, reference group.

Despite the overall low use of staging laparoscopy in this

population, there is reason for optimism: the rate of staginglaparoscopy doubled between 1998 and 2005.This rise wasmirrored by an increase in the rate of staging laparoscopyalone, suggesting that despite increasing use of laparoscopyoccult metastases were identified in a similar proportion ofpatients. Even in the most recent year the majority of pa-tients still did not undergo staging laparoscopy, and the rateof futile laparotomy was stable. Enhanced education andoutreach to surgeons may help further increase the use ofstaging laparoscopy in practice.

The findings from this population-based study are sup-ported by previous institutional series in which the rate ofoccult metastases ranged from 13% to 41%.4-12 Despitedvances in cross-sectional imaging, the ability of stagingaparoscopy to identify peritoneal-based disease remainsnsurpassed, particularly with adjuncts for micrometasta-

Table 4. Predictors of Resection

PredictorAdjustedodds ratio 95% CI p Value

Age at diagnosis, y65 – 69 Ref 0.6570 – 74 1.01 0.83 – 1.2375 – 79 1.08 0.89 – 1.3180 � 1.11 0.92 – 1.35

SexMale Ref 0.13Female 1.12 0.97 – 1.29

RaceWhite Ref �0.01Black 1.19 0.95 – 1.48Asian 1.62 1.26 – 2.09Hispanic 0.89 0.65 – 1.22Other/unknown 1.38 1.02 – 1.88

Marital statusMarried Ref �0.01Not married 0.78 0.68 – 0.90

Charlson Comorbidity Score0 Ref 0.601 – 2 1.06 0.91 – 1.243� 0.97 0.82 – 1.14

RegionWest Ref 0.61Midwest 1.09 0.88 – 1.34Northeast 1.06 0.90 – 1.26South 0.94 0.76 – 1.16

Location in the stomachAntrum/pylorus Ref �0.01Cardia/fundus 0.71 0.59 – 0.86Body 0.94 0.72 – 1.23Other 0.67 0.57 – 0.79

Ref, reference group.

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ses such as peritoneal cytology and reverse transcriptasepolymerase chain reaction analysis for tumor markers.18,19

The optimal study design to address the benefits of staginglaparoscopy would be a randomized controlled trial of stag-ing laparoscopy compared with no staging laparoscopy. Toour knowledge no such trial has been conducted and giventhe existing evidence, such a trial is unlikely to be con-ducted in the future. However, the consistent findings inprevious single-institutional studies of frequent occult me-tastases (Table 1), the strong data suggesting that patientswith metastatic disease (occult or otherwise) do not benefitfrom resection,13 and the minimal morbidity of staginglaparoscopy argue strongly in favor of its widespread adop-tion in the management of patients with gastric cancer.

The length of hospitalization (median 2 days) and in-hospital mortality rate (5.3%) after staging laparoscopyalone appear remarkably high at first glance. Indeed, stag-ing laparoscopy is frequently performed as an outpatientprocedure and the anticipated mortality rate should be low.However when this is compared with the correspondingdata for laparotomy alone (10 days and 13.1%, respec-tively), the advantages are clear. Furthermore, it is impor-tant to consider that this represents a group of elderly pa-tients (over age 65) with metastatic gastric cancer. Therelatively poor outcomes in these patients reflect the under-lying disease process and highlight the importance ofavoiding nontherapeutic interventions when possible.

The use of staging laparoscopy for gastric cancer in rou-tine practice in the US has not been well described. Coburnand colleagues20 recently assessed patterns of gastric cancer

anagement in Ontario, Canada. Among 2,399 patientsho underwent gastric cancer surgery between 2000 and005, 308 (12.8%) had staging laparoscopy. Interestingly,espite the similar overall rate of staging laparoscopy,6.6% of patients who underwent staging laparoscopy inhe Canadian analysis did not have a subsequent therapeu-ic intervention. This remarkably high rate of laparoscopy

Table 5. First Operative Procedure in Patients who ReceivedTherapeutic Intervention by Use of Staging Laparoscopy

Procedure

Anytherapeuticintervention(n � 5,610)

Staginglaparoscopy

(n � 306)

No staginglaparoscopy(n � 5,304)

n % n % n %

Total gastrectomy 1,354 24 100 33 1,254 24Distal gastrectomy 2,991 53 141 46 2,850 54Proximal

gastrectomy539 10 31 10 508 10

Other resection 242 4 16 5 226 4Bypass 366 7 10 3 356 7

lone suggests that Ontario surgeons applied laparoscopy

ore selectively to patients at high risk of metastaticisease.Several limitations of our study warrant mention. Our

indings may not be applicable to patients younger than 65ears. It is conceivable that surgeons perform staging lapa-oscopy more frequently in younger patients, although el-erly patients and those with comorbidities are the most

ikely to benefit due to the increased risk of complicationsrom laparotomy. Although we were able to control forotential confounding by a number of important sociode-ographic and disease characteristics, other factors thatay be associated with surgical decision making, such as

he patient’s functional status and patient and physicianreferences, are not available in the SEER-Medicare data-et, so could not be evaluated. Surgical intent (palliative orurative operation) was inferred retrospectively based onhe timing of procedures relative to each other. Therefore,e cannot precisely distinguish elective futile laparotomies

rom urgent exploratory laparotomies in patients who pre-ented with gastric outlet obstruction or bleeding. Despitehis limitation, our results support the primary conclusionhat staging laparoscopy is infrequently used in the man-gement of patients with gastric adenocarcinoma.

CONCLUSIONSIn summary, staging laparoscopy is performed infrequentlyin older patients with gastric adenocarcinoma in the US.Our findings, in combination with those from other stud-ies, suggest that up to 30% of patients could avoid futilelaparotomy if staging laparoscopy was performed. Un-equivocally, futile laparotomy is associated with substan-tially longer hospitalization and higher perioperative mor-tality than staging laparoscopy. Surgeons should beencouraged to offer patients with gastric adenocarcinomastaging laparoscopy before initiating laparotomy.

Author ContributionsStudy conception and design: Karanicolas, Elkin, Jacks,

Brennan, CoitAcquisition of data: Karanicolas, Elkin, JacksAnalysis and interpretation of data: Karanicolas, Elkin,

Jacks, Atoria, Strong, Brennan, CoitDrafting of manuscript: Karanicolas, ElkinCritical revision: Karanicolas, Elkin, Jacks, Atoria, Strong,

Brennan, Coit

Acknowledgment: The authors gratefully acknowledge theApplied Research Program, NCI; the Office of InformationServices and Office of Strategic Planning, Centers for Medi-care & Medicaid Services (CMS); Information Management
Services, Inc; and the SEER Program tumor registries for cre-


ation of the SEER-Medicare dataset. The authors acknowl-edge Nicole M Ishill, MSc, for assistance with statisticalprogramming.

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