Total gastrectomy is not necessary for proximal gastric cancer Lawrence E. Harrison, MD, Martin S. Karpeh, MD, and Murray F. Brennan, MD, New York, N.Y.
Background. Although there is an increasing incidence of proximal gastric cancers in the United States, the appropriate extent of resection for proximal gastric cancer is not known. This study addresses whether the type of operation (total gastrectomy [TG] vs proximal gastrectomy [PG]) affects outcome for proximal gastric adenocarcinoma. Methods. Review of the prospective gastric database at Memorial Sloan–Kettering Cancer Center from July 1985 to August 1995 identified 391 patients with proximal gastric cancer. Of those patients, 98 underwent curative TG or PG through an exclusively abdominal approach. Patients undergoing esophagogastrectomy (n = 293) were excluded from analysis. Data are expressed as medians and ranges. Results. The length of hospital stay was the same for patients undergoing resection for PG (16.5 days [range 8 to 55]) and for TG (18 days [range 8 to 48]). In addition, hospital mortality rates for PG (6.0%) were similar to those for TG (3.0%). There was no significant difference in tumor differentiation and overall stage between the groups that underwent TG and those that underwent PG. There was no significant difference in time to recurrence between the two operative groups (PG, 15.7 months, versus TG, 18 months). In addition, there was no association between first site of recurrence and type of procedure. The overall 5-year survival rate for proximal gastric cancer was 43% (median survival 46 months), whereas the 5-year survival rate for TG was 41% (median survival 51 months; difference not significant). Conclusions. The extent of resection for proximal gastric cancer does not affect long-term outcome. TG and PG have similar overall survival rates and time and rate of recurrence, and both procedures can be accomplished safely. (Surgery 1998;123:127-30.) From the Department of Surgery, Memorial Sloan–Kettering Cancer Center, New York, N.Y.
ALTHOUGH THERE IS AN INCREASING incidence of proximal gastric cancer in the United States, the appropriate extent of resection for proximal gastric cancer is unknown. Proponents of total gastrectomy (TG) suggest that a complete resection achieves a tumor-free proximal margin and allows for a more extended lymphadenectomy.1 Alternatively, others argue that proximal gastrectomy (PG) achieves a survival rate equivalent to that of TG, with preservation of physiologic function of the gastric remnant.2 The purpose of this study is to present a 10-year experience with proximal gastric adenocarcinomas from one institution treated by either TG or PG. Comparisons of hospital stay and mortality, recurrence, and survival rates are presented.
Accepted for publication May 15, 1997. Reprint requests: Murray F. Brennan, MD, Department of Surgery, Memorial Sloan–Kettering Cancer Center, 1275 York Ave., New York, NY 10021. Copyright © 1998 by Mosby, Inc. 0039-6060/98/$5.00 + 0 11/56/83277
METHODS Definitions. Proximal gastric cancer was defined as adenocarcinoma of the proximal one third of the stomach or gastroesophageal junction. TG included resection of the duodenum and a segment of abdominal esophagus without an extraabdominal incision. A PG was an abdominal-only operation that used an esophageal-to-distal stomach anastomosis. An esophagogastrectomy was an operation that resected the thoracic esophagus proximally and used either a thoracic or neck incision for access to the proximal anastomosis. Methods. A review of the prospective database for gastric adenocarcinoma at Memorial Sloan–Kettering Cancer Center between July 1985 and August 1995 identified 391 patients who underwent resection for proximal gastric cancer. Patients requiring an esophagogastrectomy were excluded from analysis (n = 293). Length of proximal and distal margins from the tumor were determined retrospectively by review of the pathology report (54 of 98 patients were evaluable). Data are expressed as median values and ranges. Survival was calculated by the method of SURGERY 127
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Fig. 1. Comparsion of overall survival rates of patients undergoing TG and PG (difference not significant).
Kaplan-Meier and compared by log-rank test. Other comparisons were made by unpaired t or chi-squared test, with statistical significance defined as p less than 0.05. RESULTS Clinical factors. Of the 98 patients undergoing resection for proximal gastric cancer, 65 underwent PG and 33 underwent TG. There was a male predominance among patients with proximal gastric cancer (65:33). The age of the patients undergoing PG (66 years [range 33 to 89 years]) was no different from that of patients undergoing TG (68 years [range 26 to 92 years]). TG was associated with splenectomy significantly more often than was PG (45% versus 26%; p < 0.02). The length of hospital stay was the same for patients undergoing resection for PG (16.5 days [range 8 to 55 days]) or TG (18 days [range 8 to 48 days]). In addition, the hospital mortality rate for PG (6.0%) was similar to that of TG (3.0%) (Table I). Pathologic factors. There were no significant differences in tumor differentiation and overall stage between groups that underwent TG and those that underwent PG. The tumor size was significantly larger in patients undergoing TG (7 cm [range 0.6 to 15 cm]) compared with PG (4 cm [range 0.5 to 10.8 cm]; p = 0.02). The extent of nodal dissection was greater in the group that underwent TG as determined by the total number of lymph nodes dissected (26 nodes [range four to 72] versus 18 nodes [range one to 65]). There was no difference in distribution of node-negative tumors between the two groups. However, when patients with positive nodal disease were compared, those undergoing TG (n = 21) had a significantly increased number of positive nodes (four nodes [range one to 21]) over those undergoing PG (n = 35; seven nodes [range one to 60]). The proximal margin (mean ± SD) was not significantly
Surgery February 1998 different between PG (2.4 ± 0.8 cm) and TG (2.9 ± 0.5 cm). However, as expected, the distal margin was significantly longer for TG (6.5 ± 1.2 cm) compared with PG (3.9 ± 0.5 cm; p < 0.05) (Tables I and II). Survival. After a mean follow-up of 30 months, 35 of the 98 patients had recurrences either locally or at distant sites. There was no significant difference in time to recurrence between the two operative groups (PG, 15.7 months, versus TG, 18 months). In addition, there was no association between first site of recurrence and type of procedure (Table III). The overall survival rate for PG was equal to that of TG (Fig. 1). The overall 5-year survival rate of proximal gastric cancer was 43% (median survival 46 months), whereas the 5-year survival rate for TG was 41% (median survival 51 months). DISCUSSION Although the overall incidence of gastric cancer has remained stable in the West, there is a well-documented shift from distal to proximal lesions.3 The clinical relevance of this shift is that the overall prognosis for patients with proximal gastric cancer is worse than for those with distal tumors.4 The optimal treatment for these proximal tumors is unknown. In an attempt to determine an optimal extent of resection, we analyzed data from 98 patients with proximal gastric cancer from one institution during a 10-year period. We demonstrated that, for patients with proximal gastric cancer, the type of resection, either TG or PG, did not influence recurrence rates and overall survival rates. In addition, both resections could be performed safely, with a low mortality rate. The surgical management of patients with proximal gastric cancer remains controversial with regard to extent of resection. Papachristou and Fortner1 suggested that the objectives of surgical treatment of adenocarcinoma of the proximal stomach included (1) removal of tumor and prevention or relief of obstruction of the esophagus, (2) obtaining tumor-free margins around the primary neoplasm, and (3) removal of those regional lymph nodes that are likely to be involved by metastasis. They concluded that TG fulfilled these criteria and offered survival rates superior to those of PG.1 On the basis of these guidelines, the rates of recurrence and survival should be positively influenced by the more complete resection of TG. However, a positive impact by TG on outcome has not been supported by clinical reports. Jakl et al.2 analyzed 125 patients undergoing either TG (n = 50) or PG (n = 75) and reported that the 5-year survival rates were equivalent between the two groups.
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Surgery Volume 123, Number 2 Table I. Patient data for TG versus PG Factor Clinical Age (yr) (range) M/F ratio LOS (days) (range) Splenectomy (n) Hospital mortality (n/%) Pathologic Tumor size (cm) (range) Proximal margin + (n/%) Distal margin + (n/%) Total no. of nodes (range) N+ (no. positive nodes) (range) Grade (%) Well Moderate Poor
PG (n = 65)
TG (n = 33)
p Value
66 (42-89) 43:22 16.5 (8-56) 17 4/6
67 (33-86) 22:11 18 (8-48) 15 1/3
NS NS NS 0.05 NS
4 (0.5-10.8) 4/6.2 1/1.5 18 (1-65) 4 (1-21)
7 (0.6-15) 3/8.5 1/3.0 26 (4-72) 7 (1-60)
0.02 NS NS 0.001 0.001
23 37 40
3 45 52
NS
NS, Not significant; LOS, length of hospital stay.
They concluded that the extent of resection for proximal gastric cancer was not an independent factor for survival.2 Moreaux and Msika5 compared overall survival rates of 54 patients undergoing PG and 27 patients undergoing TG. They noted that there was no significant difference in outcome. Even after stratifying for nodal status, a survival advantage for either operation could not be revealed.5 This series also supports the equivalence of TG and PG in terms of survival. The 5-year survival rates were identical after TG and PG. Although the median survival time was slightly longer after TG, this was not statistically significant. Overall, TG was not shown to produce superior survival results for proximal gastric cancer compared with PG. On the basis of equivalence of survival between TG and PG, the local recurrence rate and safety become the next important discriminators for the type of resection for proximal gastric cancer. For local control of disease, classic oncologic dictum would predict that wide margins and extended lymphadenectomy for nodal basins at risk should confer an advantage in terms of local recurrence. Although the level of proximal resection is the same for TG and PG, TG provides a longer distal margin and a more extensive lymphadenectomy. As predicted, there was no difference in length of proximal margin when TG was compared with PG. In addition, the incidence of positive proximal margins was equivalent. On the other hand, the length of distal margins was significantly longer for TG than for PG. Despite this, there was only one positive distal margin in each group. This relatively low rate probably reflects the surgeon’s judgment to convert a planned PG to a TG to achieve ade-
Table II. TNM staging PG (n = 65) T stage (n) TIS T1 T2 T3 T4 N stage (n) N0 N1 N2 Stage (n) 0 I II III IV
TG (n = 33)
1 17 12 32 3
0 4 15 12 2
30 23 12
12 10 11
1 19 17 27 1
0 10 5 17 1
Table III. First site of recurrence Procedure PG TG
Local (n) 18 7
Distant (n) 6 5
Time to recurrence (mo) 15.7 18
quate tumor clearance distally, thus avoiding a positive distal margin. This rationale is supported by the larger tumor size noted in the group undergoing TG. The extent of lymphadenectomy is another consideration when TG and PG are compared. Although extended lymphadenectomy for gastric cancer has been emphasized,1,6 recent data are less convincing.7,8 Inarguably, TG enables a more com-
130 Harrison, Karpeh, Brennan
plete and extensive nodal dissection. This study demonstrated that the number of nodes overall, as well as the average number of positive nodes in patients with N+ nodes, was significantly greater in the patients undergoing TG. Although TG provides a longer distal margin and a more complete lymphadenectomy, the clinical relevance of these factors is uncertain. This study indicates that the time to recurrence and the site of first recurrence were not influenced by the type of operation. The clinical importance of a TG is probably related to more complete staging by the lymphadenectomy, rather than providing a survival advantage. TG and PG can be performed safely, with minimal morbidity and death in most hands. Because both TG and PG require an esophageal anastomosis, no difference in morbidity should be expected. We noted that the hospital stay was equivalent for both types of resection, despite an increase in splenectomy rates for patients undergoing TG. In addition, the postoperative mortality rates were similar. In summary, the extent of resection for proximal gastric cancer does not affect long-term outcome. Although TG achieves a longer distal margin, no differences in the rate of margin-positive nodes are noted. TG and PG have similar overall survival rates
Surgery February 1998
and time and rate of recurrence, and both procedures can be accomplished safely. Further studies should focus on the postoperative function and patient quality of life to discriminate the resection of choice for proximal gastric cancer. REFERENCES 1. Papachristou DN, Fortner JG. Adenocarcinoma of the gastric cardia: the choice of gastrectomy. Ann Surg 1996;192:58-64. 2. Jakl RJ, Miholic J, Koller R, Markis E, Wolner E. Prognostic factors in adenocarcinoma of the cardia. Am J Surg 1995;169:316-9. 3. Blot WJ, Devesa SS, Kneller RW, Fraumeni J. Rising incidence of adenocarcinoma of the esophagus and gastric cardia. JAMA 1991;265:1287-9. 4. Salvon-Harman JC, Cady B, Nikulasson S, Khettry U, Stone M, Lavin P. Shifting proportions of gastric adenocarcinomas. Arch Surg 1994;129:381-9. 5. Moreaux J, Msika S. Carcinoma of the gastric cardia: surgical management and long-term survival. World J Surg 1988;12:229-35. 6. Siewert JR, Roder JD, Bottcher K, Busch R, Hermanek P, Meyers HJ. Prognostic relevance of systemic lymph node dissection in gastric carcinoma. Br J Surg 1993;80:1015-8. 7. Robertson CS, Chung SCS, Woods SDS, Raimes SA, Lau JTF, Li AKC. A prospective randomized trial comparing R1 subtotal gastrectomy with R3 total gastrectomy for antral cancer. Ann Surg 1994;220:176-82. 8. Dent DM, Madden MV, Price SK. Randomized comparison of R1 and R2 gastrectomy for gastric carcinoma. Br J Surg 1988;75:110-2.
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