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10.1245/ASO.2005.03.065
Annals of Surgical Oncology 12:347-353 (2005)
© 2005 Society of Surgical Oncology
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Original Article

The Value of Peritoneal Cytology as a Preoperative Predictor in Patients With Gastric Carcinoma Undergoing a Curative Resection

David Bentrem, MD1, Andrew Wilton, MS2, Madhu Mazumdar, PhD2, Murray Brennan, MD1 and Daniel Coit, MD1

1 Department of Surgery, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, New York 10021
2 Department of Epidemiology and Biostatistics, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, New York 10021

Correspondence: Address correspondence and reprint requests to: Daniel Coit, MD; E-mail: coitd{at}mskcc.org.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Although positive peritoneal cytology is associated with poor prognosis, it has not been found to be independently predictive of outcome when evaluated in context of post-resection pathologic T and N stage. This study was undertaken to evaluate the predictive value of positive cytology in context of other prognostic factors available prior to surgery in patients undergoing R0 resection for gastric cancer, to assess its role in selecting patients for appropriate treatment prior to surgical resection.

Methods: Clinical variables for all patients undergoing R0 resection for gastric adenocarcinoma at Memorial Sloan-Kettering Cancer Center from 1993–2002 were reviewed from a prospective database. Patients underwent preoperative assessment of T and N stage with CT scan, laparoscopy, and endoscopic and/or laparoscopic ultrasound. Peritoneal cytology was obtained in all patients.

Results: Patients with gastric cancer (n = 371) underwent R0 resection and staging laparoscopy with peritoneal washings; 24 patients (6.5%) had positive peritoneal cytology. Positive cytology was associated with advanced T stage (P = 0.02) but not with nodal positivity (P = 0.11). Median survival of patients with positive cytology was 14.8 months vs. 98.5 months for patients with negative cytology (P < 0.001). Multivariate analysis identified preoperative T stage, preoperative N stage, site, and cytology as significant predictors of outcome. Positive cytology was the preoperative factor most predictive of death from gastric cancer (RR 2.7, P < 0.001).

Conclusions: Positive cytology is information potentially available preoperatively that identifies a patient population at very high risk for early recurrence and death after curative resection of gastric cancer.

Key Words: Cytology • Stomach neoplasm • Staging • Metastasis • Peritoneal lavage


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
More than 22,000 new cases of gastric cancer were diagnosed in the United States in 2003, and there were more than 14,000 deaths.1 In the absence of metastatic disease, resection of all gross disease with negative microscopic margins offers the only chance for long-term survival.2,3 Unfortunately, recurrence is common4 even after a curative resection. Multimodality therapy has been used with the goal of extending overall survival for high-risk patients.5 Risk stratification before definitive therapy is an important challenge in the management of patients with gastric cancer, with the goal of selecting high-risk patients for whom more aggressive multimodality therapy might be appropriate.

Compared with conventional imaging, pre-resection staging laparoscopy is the most accurate method for detecting clinically unsuspected M1 disease. Detection of subradiological metastases by laparoscopy can spare those patients unnecessary open exploration.6 More accurate pretreatment staging allows identification of patients at high risk for recurrence even after optimal resection and postoperative adjuvant chemoradiotherapy. In the United States, laparoscopy has been adopted into virtually all guidelines for initial work-up of patients with gastric cancer. However, the timing and specific indications for laparoscopy and the practice of obtaining peritoneal washings during the procedure vary widely. Although obtaining peritoneal cytology has been advocated by Japanese and Dutch investigators,7,8 this is not a uniform practice in other Western centers.

Positive peritoneal cytology is associated with poor prognosis.8–10 However, it has not been found to be consistently predictive of outcome when evaluated in the context of pathologic T and N stage8,11 after an R0 resection. In a previous study from our institution of cytology in 22 stage III curative resections, we found that positive cytology in 3 patients was a significant but not independent predictor of survival.9 Postoperative pathologic T and N stage are well-known predictors of survival after curative resection for gastric adenocarcinoma.12–14 The correlation between pre-resection clinical variables and post-resection variables has been examined.15,16 Less is known about the direct relationship between the assessment of pre-resection variables, including peritoneal cytology status, and the predicted risk of recurrence after curative resection.

The aims of this study were to determine the incidence of positive peritoneal cytology in patients undergoing curative R0 resection for gastric cancer, to identify risk factors for positive peritoneal cytology, and to evaluate the predictive value of positive cytology in the context of other prognostic factors available before surgery, at a time when pretreatment risk assessment and treatment planning take place.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
By using the prospectively maintained gastric cancer database at Memorial Sloan-Kettering Cancer Center, a retrospective search identified patients who underwent staging laparoscopy with cytology followed by an R0 resection of primary gastric cancer between September 1993 and December 2002. Patients underwent pre-resection clinical assessment of T and N stage with computed tomographic (CT) scan, laparoscopy, and endoscopic and/or laparoscopic ultrasound scan. Laparoscopic staging was performed with patients under general anesthesia immediately before planned resection. The patient was placed supine, and a 10- to 12-mm port was placed below the umbilicus. An angled 30° telescope was used for exploration. The liver, diaphragm, serosal surfaces, peritoneum, omentum, bowel, mesentery, and pelvic organs were systematically inspected. The perigastric nodes were inspected along the greater and lesser curvature, on the gastrohepatic ligament, and at the hepatic hilum. Ascitic fluid, if present, was aspirated and sent for cytology. In the absence of ascites, 50 to 100 mL of normal saline was instilled into the subhepatic space, the left upper quadrant, and the pelvis, and washings were collected. Specimens were centrifuged, filter prepared, and stained by the Papanicolaou technique. A patient was considered to have positive peritoneal cytology if adenocarcinoma cells were detected, regardless of the number of cancer cells. Curative resection was performed in the absence of clinically evident peritoneal disease but without knowledge of cytology status.

A cross-tabulation analysis of patient-related variables (age, sex, and race) and tumor-related variables (T stage, N stage, site, and American Joint Committee on Cancer [AJCC] stage) with cytology status was performed by using Fisher’s exact test. Survival curves were generated by the Kaplan-Meier method and were compared by nonparametric survival analyses by using the log-rank test. Multivariate Cox proportional hazards analysis was performed on all variables found significant by univariate analysis. Relative risk with 95% confidence intervals was calculated as a measure of association. Differences of P < .05 were considered significant. Statistical analysis was performed with S-PLUS software (Mathsoft Inc., Cambridge, MA).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
During the study, 1777 patients with gastric cancer were admitted to Memorial Sloan-Kettering Cancer Center, of whom 1102 underwent surgical exploration. Seven hundred seven patients were identified who underwent an R0 resection of primary gastric cancer, of whom 450 underwent staging laparoscopy. Peritoneal lavage cytology was performed in 371 patients undergoing laparoscopy (Fig. 1Go). Of the 371 patients, 241 patients had a documented CT scan, 111 patients had an endoscopic ultrasound examination, and 156 patients had a laparoscopic ultrasound evaluation. Because this was a retrospective review, not all patients undergoing R0 resection had laparoscopy, and not all patients undergoing laparoscopy had peritoneal cytology performed. There was no intentional selection of patients for either laparoscopy or peritoneal cytology; patients reported in this series had a stage distribution very similar to contemporary R0 patients who did not undergo laparoscopy or have peritoneal cytology performed. The distribution of patient- and tumor-related variables for the study population is shown in Table 1Go. Overall, positive cytology was found in 24 patients (6.5% of the entire group).


Figure 1
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  		FIG. 1. Schema of patients undergoing laparoscopic peritoneal lavage cytology.

 

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  		TABLE 1. Distribution of patient and tumor variables
 
No patient-related variables correlated with positive cytology. Evidence of serosal invasion (preoperative T3 and T4 tumors) before resection and advanced preoperative AJCC stage were both associated with an increased probability of positive peritoneal cytology. Nineteen (10%) of 181 patients with preoperative T3 or T4 tumors had positive cytology in the absence of macroscopic M1 disease, compared with only 4 (2%) of 176 patients with preoperative T1 or T2 tumors (P = .02). Positive cytology was identified in 14 (11%) of 127 patients with preoperative AJCC stage III disease, compared with 6 (7%) of 90 patients with AJCC stage II disease and only 3 (2%) of 152 patients with AJCC stage I disease (P = .002). Evidence of nodal positivity before resection and the site of the primary tumor did not predict positive cytology (Table 2Go).


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  		TABLE 2. Incidence of positive cytology and correlation analysis
 
At a median follow-up of 36 months, the median overall survival for the entire group has not been reached (Fig. 2Go). On univariate analysis, preoperative T stage, preoperative N stage, preoperative AJCC stage, primary tumor site, and cytology status were significant predictors of survival (Table 3Go). The median survival for patients without serosal invasion was not reached, compared with a median survival of 59 months for patients with a preoperative stage of T3/4. The median survival for patients without nodal metastases identified before surgery has not been reached, and it was 54 months for those in whom nodal disease was detected on preoperative staging. The median survival of patients with positive cytology was only 15 months (Fig. 3Go). On multivariate analysis, preoperative T stage, preoperative N stage, primary tumor site, and peritoneal cytology status remained significant independent preoperative predictors of survival (Table 4Go). Of these factors, positive cytology was the most significant, with a risk ratio of 2.7.


Figure 2
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  		FIG. 2. Overall survival of patients with gastric carcinoma undergoing a curative resection, with 95% confidence limits (median follow-up, 36 months).

 

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  		TABLE 3. Preoperative predictors of survival
 

Figure 3
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  		FIG. 3. Overall survival by cytology status.

 

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  		TABLE 4. Independent preoperative predictors of survival on multivariate analysis
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The overall incidence of positive cytology reported depends very much on the cohort of patients being studied. Bando et al.17 found positive cytology in 311 (24%) of 1297 patients with gastric cancer. This series included patients with advanced gastric cancer (296 patients with peritoneal metastasis and 77 patients with T4 tumors), and this accounted for the higher incidence of positive cytology. Ribeiro et al.18 reported a 41% incidence of positive cytology in a series of 49 patients with both localized and metastatic gastric cancer. When other series evaluated patients without advanced disease undergoing a curative resection, the incidence of positive peritoneal cytology was approximately 5% (Table 5Go). This overall incidence is quite similar to the 6.5% reported in this study.


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  		TABLE 5. Summary of studies reporting the prevalence of positive cytology in gastric cancer patients
 
Our previous study and others have shown a correlation between the extent of disease, as determined by postoperative staging, and the prevalence of positive cytology.8,9,18 Peritoneal carcinomatosis is associated with a very high likelihood, but not a certainty, of positive cytology, with a reported incidence of 59% to 69%.9,19 In patients without carcinomatosis, the postoperative pathologic depth of the primary tumor invasion has been found to correlate most consistently with positive cytology. The incidence of positive peritoneal cytology ranges from 0% to 4% in patients with pathologic T1/2 tumors, compared with 10% to 12% in those with serosal invasion.8,9 However, postoperative predictors of an important prognostic factor are not all that useful, especially if that factor could be known before resection and used for pretreatment planning. In this study, we attempted to identify preoperative predictors of peritoneal cytology status, at a time when the information could be incorporated into an appropriate and relevant treatment plan. In this study, the prevalence of positive cytology with serosal invasion or with AJCC stage III, both determined before resection, was 10% to 11%.

More thorough evaluations of the cytology sample are also under investigation to increase the yield of peritoneal cytology for early detection of clinically occult malignant cells. Several groups21,22 have used immunohistochemistry (IHC) or quantitative reverse transcriptasepolymerase chain reaction (PCR) for expression of carcinoembryonic antigen messenger RNA (mRNA)23–25 or trypsinogen mRNA19 in peritoneal washes to more accurately identify free malignant cells. Schott et al.22 found positive peritoneal cytology in 33 (53%) of 62 patients with stage I to IV gastric cancer by using a panel of IHC stains. Patients with positive cytology by that method had a significantly worse prognosis by univariate analysis. Because there was a very strong association between cytology status and pathologic stage, it was not clear that cytology status was an independent predictor of outcome, in contrast to this study. Furthermore, because conventional cytology (CY) was not performed in the Schott study, the incremental yield and clinical significance of IHC positivity over the more conventional Papanicolaou stain were not reported. Benevolo et al.21 evaluated peritoneal washings for tumor cells in 144 patients with stage I to III gastric cancer by using both CY and IHC. IHC improved the yield for identifying positive cytology over conventional staining (35% positive with IHC vs. 21% positive by conventional staining). Among 80 patients with a minimum 2-year follow-up, positive cytology by either conventional staining or IHC was a significant univariate predictor of poor survival. In the Benevolo study, patients with positive cytology by IHC only (n = 12) had a survival intermediate between those with positive cytology by conventional staining (n = 12) and those with negative cytology (n = 56). Again, in contrast to the current series, the authors were unable to make any statement about the independent predictive value of positive cytology in their study.

Oyama et al.26 described their experience with real-time quantitative reverse transcriptase-PCR for carcinoembryonic antigen mRNA expression in patients with gastric cancer. Thirty (18%) of 163 patients undergoing curative resection had positive cytology by PCR. In their series, positive peritoneal cytology was an independent predictor of peritoneal recurrence, as well as of relapse-free and overall survival. Their overall survival rates were somewhat better than those reported in our series. Although all of our patients with positive cytology by conventional staining were dead by 3 years, their estimated 3-year survival with positive cytology by PCR was 75%.

Kodera et al.24 reported on their experience with a very similar real-time quantitative reverse transcriptase-PCR assay for expression of carcinoembryonic antigen mRNA in 189 patients with gastric cancer. They specifically considered the incremental value of the molecular technique (PCR) over CY. Among the entire cohort of 189 patients, 135 patients (71.5%) were CY–/PCR–, 19 patients (10%) were CY–/PCR+, and 35 patients (18.5%) were CY+/PCR+. PCR– patients had a much better outcome than PCR+ patients, and PCR+ patients fared poorly regardless of CY status. Among 150 patients who underwent curative resection, positive PCR status of the peritoneal washings was the most powerful independent predictor of overall survival.

The poor prognosis of patients with gastric cancer with free abdominal tumor cells on cytological examination has been described in Japan17,27 and The Netherlands.8 We previously reported 127 consecutive patients with both localized and advanced gastric cancer in whom the peritoneal cytology status was known. In that series, the 3 patients undergoing R0 resection with unsuspected positive peritoneal cytology had the same dismal prognosis as the 51 patients with macroscopic peritoneal disease. In essence, for those three patients, positive cytology was prognostically equivalent to macroscopically evident M1 disease.9

The influence of positive cytology on survival for patients with gastric cancer has not been consistent, as reported from other centers. Including patients with metastatic disease, Bando et al.17 identified positive cytology and the presence of metastatic disease (peritoneal or hepatic metastasis) as independent predictors of survival. Abe et al.11 evaluated 108 patients with stage III disease. When compared with postoperative pathologic variables (extent of serosal invasion and presence of lymph node metastasis), positive cytology was not an independent predictor of survival. The authors concluded that the specificity of peritoneal cytology was low and less important than the postresection T and N stage in predicting outcome. Bonenkamp et al.8 reported on the findings of peritoneal washings performed in 457 patients undergoing a curative resection for gastric cancer as part of the Dutch randomized controlled trial for D1 versus D2 nodal dissection for gastric cancer. On univariate analysis, positive cytology was a significant predictor of poorer overall survival, but, again, it was not found to be an independent predictor when compared with postoperative pathologic T and N stage.

Preoperative assessment of T and N stage with CT scan or endoscopic ultrasound correlates with postresection T and N stage.15,16 No study to date has considered the prognostic value of preoperative T or N stage. In this study, preoperative assessment of these two factors and the primary tumor site were found to be independent predictors of survival. When peritoneal cytology is considered in this context, it is not only an independent predictor of survival, but also the most powerful piece of prognostic information available before surgery for patients who have disease that is potentially resectable for cure.

In this series, peritoneal cytology specimens were obtained immediately before resection, and the results were not available or used to guide definitive treatment planning until after surgical resection. The data suggest that positive cytology can identify a patient population at very high risk for early recurrence and death after complete resection. Whether the preoperative predictors of positive cytology can identify a group of patients who should undergo a separate pre-resection laparoscopy with peritoneal washings is beyond the scope of this review. It seems clear, however, that patients with positive cytology are unlikely to derive any meaningful benefit from gastric resection. If knowledge of cytology status would affect definitive treatment planning—i.e., prompting either preoperative or definitive chemotherapy, or postoperative intraperitoneal therapy—then it might be reasonable to have the information available before resection, especially in high-risk patients (T3/4, AJCC stage II/III). Our current practice has evolved. If a patient is believed to be at risk for positive peritoneal cytology and does not require immediate palliative resection, we consider performing a staging laparoscopy for washings as a separate procedure. When positive cytology is identified before resection, patients are considered to have stage IV disease and are offered initial systemic chemotherapy. After initial chemotherapy, if subsequent restaging reveals no progression of disease, these patients may be offered resection with postoperative intraperitoneal chemotherapy on an individual basis.

The cost-effectiveness of a separate staging laparoscopic procedure is difficult to estimate. It must be considered in the context of individual patient- and tumor-related factors and in the context of available treatment options. Although the incremental cost of a separate staging laparoscopy procedure can be estimated, it would be impossible to assess the true cost of a probably nontherapeutic gastric resection in a patient with positive cytology. Certainly the risk of positive cytology in a high-risk patient (T3/4 or AJCC stage III by preoperative assessment) is comparable to the yield of other staging procedures used to formulate a treatment plan. This would justify the practice of performing staging laparoscopy as a separate procedure. An option to a separate staging laparoscopy would be to use a rapid intraoperative cytological assay,28 although the ability to provide a quick and accurate assessment of peritoneal fluid cytology may not be a resource available at all institutions.

In summary, 6.5% of patients undergoing a curative resection for gastric cancer had positive peritoneal washings. Advanced preoperative T stage and AJCC stage were associated with an increased incidence of positive cytology (10% of patients with preoperative T3/4 tumors and 11% of preoperative AJCC stage III patients had positive cytology). In the context of other known preoperative risk factors, positive peritoneal cytology was the most powerful independent predictor of outcome, with a risk ratio of 2.7 for patients undergoing a curative resection.

This study confirms initial reports and supports the value of peritoneal cytology in the pretreatment staging of gastric cancer. Positive cytology is information available before resection that identifies a patient population at very high risk for early recurrence and death even after curative resection. For patients undergoing a potentially curative resection, for whom the treatment plan will be affected, it is important to know the peritoneal cytology status before definitive surgical treatment.


   ACKNOWLEDGMENTS
 
The authors thank Marianne Beninati for her help with data collection. Supported by a grant from the Gelb Foundation.

Received for publication March 19, 2004. Accepted for publication December 21, 2004.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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