FREE NEJM E-TOC    HOME   |   SUBSCRIBE   |   CURRENT ISSUE   |   PAST ISSUES   |   COLLECTIONS   |   Search Term  Advanced Search

Sign in | Get NEJM's E-Mail Table of Contents — Free | Subscribe

Previous Volume 340:908-914 March 25, 1999 Number 12 Next

Abstract PDF Editorial by Brennan, M. F. Letters Add to Personal Archive Add to Citation Manager Notify a Friend E-mail When Cited PubMed Citation

ABSTRACT

Background Curative resection is the treatment of choice for gastric cancer, but it is unclear whether this operation should include an extended (D2) lymph-node dissection, as recommended by the Japanese medical community, or a limited (D1) dissection. We conducted a randomized trial in 80 Dutch hospitals in which we compared D1 with D2 lymph-node dissection for gastric cancer in terms of morbidity, postoperative mortality, long-term survival, and cumulative risk of relapse after surgery.

Methods Between August 1989 and July 1993, a total of 996 patients entered the study. Of these patients, 711 (380 in the D1 group and 331 in the D2 group) underwent the randomly assigned treatment with curative intent, and 285 received palliative treatment. The procedures for quality control included instruction and supervision in the operating room and monitoring of the pathological results.

Results Patients in the D2 group had a significantly higher rate of complications than did those in the D1 group (43 percent vs. 25 percent, P<0.001), more postoperative deaths (10 percent vs. 4 percent, P= 0.004), and longer hospital stays (median, 16 vs. 14 days; P<0.001). Five-year survival rates were similar in the two groups: 45 percent for the D1 group and 47 percent for the D2 group (95 percent confidence interval for the difference, –9.6 percent to +5.6 percent). The patients who had R0 resections (i.e., who had no microscopical evidence of remaining disease), excluding those who died postoperatively, had cumulative risks of relapse at five years of 43 percent with D1 dissection and 37 percent with D2 dissection (95 percent confidence interval for the difference, –2.4 percent to +14.4 percent).

Conclusions Our results in Dutch patients do not support the routine use of D2 lymph-node dissection in patients with gastric cancer.

Reported rates of survival after gastric resection are consistently higher in Japan than in the West.¹ Japanese and Western surgeons differ in their approach to lymph-node dissection during surgery for stomach cancer. D2 lymph-node dissection has never gained widespread popularity in the West, because of the associated morbidity and in-hospital mortality described in early studies.² The Southwest Oncology Group, in a recent study of adjuvant treatment for gastric cancer, found that even though the surgeons and pathologists participating in the study were required to document curative resection, only half of them reported dissection of the lymph nodes.³

The Japanese Research Society for the Study of Gastric Cancer (JRSGC) has standardized lymph-node dissection for gastric cancer. The JRSGC regards gastric resection without a formal clearance of the D2 lymph nodes as an insufficient procedure, except for palliation.⁴ D2 lymph-node dissection is now performed more often in Western centers, and improved outcomes after the procedure have been reported.^5,6,7,8 To bring further evidence to the debate about D2 dissection, two major randomized trials comparing D1 with D2 dissection in patients undergoing potentially curative resection were conducted, one by the Medical Research Council in the United Kingdom⁹ and the other by the Dutch Gastric Cancer Group in the Netherlands.^10,11

Both trials found that the rates of short-term morbidity and in-hospital mortality were substantially higher among the patients who underwent D2 dissection. We now report the long-term survival rate and the cumulative risk of relapse in the Dutch trial and assess the overall value of D2 dissection in our patients with gastric cancer.

Methods

Eligibility and Randomization

Subjects were enrolled in the study between August 1989 and July 1993. To be eligible for participation, patients had to have histologically confirmed adenocarcinoma of the stomach without evidence of distant metastasis. They had to be younger than 85 years and in adequate physical condition for D1 or D2 lymph-node dissection. Patients were excluded if they had previous or coexisting cancer or had undergone gastrectomy for benign tumors. Randomization was performed before surgery so as to allow scheduling for the presence of specially trained supervising surgeons. If a supervising surgeon could not attend a planned operation, the patient was considered ineligible. The 80 participating centers registered patients by means of telephone calls to the central office of the trial, where randomization in blocks of six and with stratification according to center was conducted.

All patients were evaluated every three months during the first year and every six months thereafter. In accordance with common practice in the Netherlands, a clinical diagnosis was considered sufficient evidence of relapse; for the majority of patients, however, radiologic or endoscopic confirmation was sought. The trial was approved by the medical ethics committees of the Leiden University Medical Center and the other participating hospitals.

Surgery

The JRSGC has provided guidelines for the standardization of surgical treatment and pathological evaluation.⁴ These guidelines, also recommended by the American Joint Committee on Cancer and the International Union against Cancer in the fourth edition of their manual for the staging of cancer,¹² formed the basis of our protocol. These guidelines recognize 16 different lymph-node compartments (stations), numbered 1 through 16, that surround the stomach.

In general, the perigastric lymph-node stations along the lesser curvature (stations 1, 3, and 5) and the greater curvature (stations 2, 4, and 6) of the stomach are grouped together as N1, and the nodes along the left gastric artery (station 7), the common hepatic artery (station 8), the celiac artery (station 9), and the splenic artery (stations 10 and 11) are grouped together as N2. These groupings can be modified slightly, depending on the location of the primary tumor. Researchers in Japan have described further lymph-node stations (12 through 16) and groups (N3 and N4), but these were outside the scope of our trial. A D1 dissection entails the removal of the involved distal part of the stomach or the entire stomach (distal or total resection), including the greater and lesser omenta. For a D2 dissection, the omental bursa is removed, along with the front leaf of the transverse mesocolon, and the mentioned arteries are cleared completely.

At the time the trial was designed, resection of the spleen and the tail of the pancreas was regarded as necessary for the adequate removal of D2 lymph-node stations 10 and 11 in proximal tumors; in a D1 dissection, the spleen and tail of the pancreas were resected only when removal was necessitated by tumor invasion. Our protocol followed these conventions. Assessment of the curability of the tumor was always performed by the supervising surgeon at laparotomy. Patients were regarded as able to undergo resection with curative intent and underwent the randomly assigned type of dissection (D1 or D2) if at laparotomy they had a tumor that was macroscopically completely removable, no peritoneal spread or liver metastases, and no distant lymph-node metastases. The fulfillment of these criteria had to be confirmed by examination of frozen sections of one or two para-aortic lymph nodes. The patients who met these criteria constituted the group treated with curative intent. To detect free abdominal tumor cells, analysis of abdominal fluid obtained by irrigation of the abdominal cavity immediately after laparotomy was recommended. The results were not used for immediate assessment of curability.¹³

The type of gastrectomy performed (distal or total) was independent of randomization. Distal gastrectomy was allowed if there was a tumor-free margin of 5 cm beyond the proximal resection line. All other patients underwent total gastrectomy. Reconstruction of the alimentary tract was done principally by the local surgeon, who used the method he or she preferred. Histologic examination of the resected specimens was performed by the local pathologist, and the results were reviewed by a panel of supervising pathologists. After the final pathological examination, the operation was classified as R0 if the microscopical evidence indicated complete tumor removal, if there was no involvement of distant lymph nodes, and if there were no malignant cells in the abdominal-washing fluid. None of the patients treated curatively underwent adjuvant radiotherapy or chemotherapy.

Patients who did not meet these criteria constituted the group not treated curatively. They underwent a palliative surgical procedure or exploratory laparotomy at the discretion of the surgeon and irrespective of the assigned treatment.

Quality Control

Participating surgeons received a videotape and booklet about the technique and were instructed in the operating room by an expert gastric-cancer surgeon from Japan. The expert was present during the first four months of the intake period, which served as an instruction period, and regularly thereafter. All operations involving D2 dissection were attended by one of eight surgeons, from eight regions, who had been specially trained in D2 dissection. The study coordinator attended nearly all D1 operations. These supervising surgeons monitored the technique and the extent of lymph-node dissection, and after the operation, they divided the perigastric tissue into the proper lymph-node stations. Regular meetings about the technique were held with the supervising surgeons, the study coordinator, and the instructing surgeon.

Quality control was carried out by relating the number and location of lymph nodes detected at pathological examination to the guidelines of our protocol.¹⁴ If at pathological examination lymph nodes were detected in stations other than those specified by the protocol, this violation of the protocol was called "contamination." If the pathologist could not detect lymph nodes in stations that should have been dissected, this violation was called "noncompliance." These violations could occur in both D1 and D2 dissections, but contamination in the D1 group and noncompliance in the D2 group could theoretically blur the distinction between the two operative methods. There is considerable variation in the number of lymph nodes in each station, and the defined lymph-node stations may not contain any lymph nodes.¹⁵ To account for this biologic variation, we allowed one missing station. If the discrepancies exceeded one lymph-node station, however, we considered this deviation from the protocol relevant.

Statistical Analysis

The sample size was based on an expected five-year survival rate of 20 percent for the patients undergoing surgery with a D1 dissection with curative intent and 32 percent for those undergoing surgery with a D2 dissection with curative intent.¹⁶ Using a significance level of 0.05 (two-sided) and a power of 0.90, and expecting 40 percent of the patients to be treated palliatively, we calculated that we needed to enroll 1100 patients. Survival rates were calculated from the time of enrollment in the study until death (event) or the last follow-up contact (if data were censored). For calculating the cumulative risk of relapse, the event was defined as relapse; data on a patient were censored when at the last follow-up contact the patient was alive with no evidence of disease or had died of diseases other than gastric cancer without evidence of a recurrence. Both survival and cumulative risk of recurrence were studied. The primary analysis of survival included all patients eligible for treatment (intention-to-treat analysis), including those who had undergone palliative treatment, whereas subsequent analyses focused on the patients operated on with curative intent. Because only the patients with an R0 resection who had not died in the hospital were at risk for recurrence, this group was used to study the cumulative risk of relapse. The effect of prognostic variables was studied in a univariate analysis. The log-rank test was used to evaluate the survival curves, although the assumption of proportional hazards was not always satisfied. The hazard ratios presented compare the results after D2 surgery with the results after the reference treatment, D1 surgery.

Results

Between August 1989 and July 1993, we enrolled 1078 patients and randomly assigned them to either the D1 group or the D2 group (Table 1). Eighty-two patients (8 percent) were not eligible, 35 because no reference surgeon could attend the operation and the remainder because of secondary cancers, lack of adenocarcinoma, or inadequate physical condition. Of the 996 eligible patients, 285 (29 percent) were found to have peritoneal, hepatic, or distant lymph-node metastases or locally unresectable tumors at the time of surgery. These 285 patients with incurable disease underwent palliative gastrectomy (53 percent), gastric bypass (19 percent), or exploratory surgery only (28 percent). No gross evidence of metastatic disease was detected in 711 (71 percent) of the eligible patients, who underwent curative resection with D1 (380 patients) or D2 (331 patients) lymph-node dissection. Of these 711 patients, 632 fulfilled our criteria for an R0 resection. The D1 and D2 groups were well balanced, except in terms of associated pancreatectomy and splenectomy, a difference that was expected because of the protocol, and in terms of the type of gastrectomy (P<0.05) (Table 2). Pathological stage T1 tumors (defined as early gastric cancer) were found in 26 percent of the patients.

View this table: [in this window] [in a new window]   Table 1. Results of Randomization and Assessment of Eligibility of 1078 Patients with Gastric Cancer.

 

View this table: [in this window] [in a new window]   Table 2. Characteristics of 711 Patients and Tumors after Resection with Curative Intent.

 
Follow-up continued until January 1998. In all eligible patients the median follow-up period was 72 months (range, 47 to 98 months). Of the 711 patients who were treated with curative intent, 398 died. Forty-seven patients died of complications soon after surgery and never left the hospital (Table 3). During follow-up, 47 patients died of cardiopulmonary disease, and the remaining 304 died of infections not related to the operation or of secondary cancers. Death with recurrence of gastric cancer occurred in 289 patients. Of the 313 surviving patients in the curative group, 7 had recurrence. D2 dissection was associated with substantially more complications, more in-hospital deaths, and a longer median hospital stay than was D1 dissection (Table 3).^10,11

View this table: [in this window] [in a new window]   Table 3. Short-Term Outcome after Resection with Curative Intent in 711 Patients.

 
Figure 1 summarizes the long-term survival of all patients eligible for participation in the study and of the patients who were treated with curative intent. According to a proportional-hazards analysis, the hazard ratio comparing the risk of death within five years after D2 surgery with the risk of death within five years after D1 surgery for the eligible patients was 1.09 (95 percent confidence interval, 0.94 to 1.27). For the patients in the curative group, this hazard ratio was 1.00 (95 percent confidence interval, 0.82 to 1.22). The mean (±SE) five-year survival rates for all eligible patients were 34±2.1 percent in the D1 group and 33±2.2 percent in the D2 group (difference in five-year survival rates, 1 percent; 95 percent confidence interval, –5 percent to +7 percent). For the patients in the curative group, these figures were 45±2.6 percent for the D1 group and 47±2.8 percent for the D2 group (difference, –2 percent; 95 percent confidence interval, –9.6 percent to +5.6 percent).

View larger version (4K): [in this window] [in a new window]   Figure 1. Survival among All Eligible Patients and Those Treated with Curative Intent. Of the 996 patients eligible for participation, 513 underwent D1 dissection and 483 underwent D2 dissection. Of the 711 patients treated with curative intent, 380 underwent D1 dissection and 331 underwent D2 dissection.

 
The cumulative risk of relapse, calculated for the cohort of 589 patients who had an R0 resection but did not die in the hospital, was lower for patients with D2 dissections than for those with D1 dissections (hazard ratio 0.84; 95 percent confidence interval, 0.65 to 1.09). The risks of relapse by five years after surgery were 43 percent for the D1 group and 37 percent for the D2 group (Figure 2). The curves for the cumulative risk of relapse diverged two years after surgery, but the difference did not reach statistical significance (P=0.22). The estimated difference of 6 percent at seven years had a standard error of 4.2 percent and was associated with a 95 percent confidence interval of –2.4 percent to +14.4 percent.

View larger version (4K): [in this window] [in a new window]   Figure 2. Survival and Cumulative Risk of Relapse among the Patients with R0 Resection, Excluding In-Hospital Deaths. Of these 589 patients, 324 underwent D1 dissection and 265 underwent D2 dissection.

 
In the univariate analysis, none of the prognostic variables shown in Table 4 changed the overall results in the two groups. Patients who needed resection of the spleen or the tail of the pancreas had a lower survival rate than those who did not require these resections, but the difference between the D1 and D2 groups was not significant. Univariate analysis of the cumulative risk of relapse among patients with R0 resections showed a marginally significant difference for patients who did not require splenectomy or pancreatectomy (cumulative risk of relapse at five years, 41 percent for the D1 group and 29 percent for the D2 group; P=0.02).

View this table: [in this window] [in a new window]   Table 4. Univariate Analysis of Survival Rates among 711 Patients Five Years after Resection with Curative Intent, According to Selected Prognostic Variables.

 
The degree of adherence to the protocol is shown in Table 5. The quality-control system effectively prevented dissection beyond the limits of the protocol (contamination) in nearly all cases, but in 36 percent of the patients in the D1 group and in 51 percent of the patients in the D2 group, the pathologist could not detect lymph nodes in stations that should have been dissected (noncompliance).

View this table: [in this window] [in a new window]   Table 5. Adherence to the Protocol for Lymph-Node Dissection in the 711 Patients Who Underwent Resection with Curative Intent.

 
Discussion

For most solid tumors, en bloc removal of regional lymph nodes is part of the surgical treatment, although it is unclear whether this procedure improves survival or merely refines staging.¹⁸ For gastric cancer, the JRSGC has consistently recommended extended (D2) lymph-node dissection. In most countries outside Asia this procedure is performed less often, however, mainly because the morbidity associated with D2 dissection is higher than in Japan. Furthermore, the evidence of better survival after D2 surgery in Japan is based solely on observational studies. Large Western institutions tend to perform D2 dissections, but the justification for this operation also rests solely on retrospective evidence.^5,6,7,8

The results of our randomized trial comparing limited (D1) and extended (D2) lymph-node dissections do not confirm the experience with these dissections in Japan. Our earlier report of increased short-term morbidity and in-hospital mortality among patients who underwent D2 dissection¹⁰ has been confirmed in a separate trial performed by the Medical Research Council.⁹ There was no long-term improvement in survival or decrease in the risk of relapse among patients in our trial who had a D2 dissection. For these reasons, we cannot recommend extended lymph-node dissection for Western patients.

When our results are compared with historical data, it can be seen that long-term survival has improved. At the start of the trial, we had expected the five-year survival rates to be 20 percent for the patients who had D1 dissection and 32 percent for the patients who had D2 dissection with curative intent.^1,16 The observed five-year survival rates were 45 percent and 47 percent, respectively. This improvement is certainly related to the unexpectedly high proportion of pathological stage T1 tumors (26 percent) and pathological stage T2 tumors (47 percent), which have a relatively good prognosis, but it is also a reflection of more refined staging. Before the trial, N4 (distant) lymph-node involvement was not evaluated, and the criteria for defining a potentially curative resection were less restrictive. In this trial, 89 of the 996 eligible patients were regarded as having incurable disease because of N4 lymph-node involvement.

The incidence of gastric cancer in any Western country is so low that a randomized trial requires the cooperation of many surgeons. To make sure that the surgeons understood the sometimes fine distinction between D1 and D2 dissections, and to ensure the quality of surgery, we implemented a strict quality-control system, in which supervising surgeons were required to attend the operations.¹⁴ We had hoped that this system would reduce the risk of complications, but D2 dissection was nevertheless associated with relatively high morbidity and in-hospital mortality. As compared with patients in Japan, even our patients who underwent D1 dissection had more complications. These differences might result from the Western habitus, which diminishes accessibility of the abdomen, and from the amount of intraabdominal fatty tissue. Western patients also frequently have underlying diseases. For instance, of the 109 patients who died after curative resection without signs of recurrence, more than half died of cardiovascular and pulmonary diseases.

To guarantee that the assigned D1 and D2 dissections were carried out, supervising surgeons in the operating room prevented crossover to the alternative treatment, with a degree of success that is evidenced by the mean number of lymph nodes harvested. However, because the JRSGC protocol describes in detail which lymph-node stations have to be dissected for each tumor location, we felt that additional measures of adherence to the protocol were needed. These measures, contamination and noncompliance, have never been used in the context of a surgical trial, so our results cannot be directly compared with those of other trials.

In earlier reports on protocol adherence, the number and site of the lymph nodes detected at pathological investigation were related to the protocol of the JRSGC.¹⁴ However, our study protocol differed slightly from that of the JRSGC, because we did not perform proximal gastrectomy and we required a different indication for pancreaticosplenectomy. As a consequence, the indicated lymph-node stations in all proximal tumors differ between the JRSGC and Dutch protocols. Furthermore, we did not account for the biologic variation in the numbers of lymph nodes per station.¹⁵ The data presented here, adjusted for these variables, show that surgeons did confine the operation to the indicated dissection. Noncompliance seems serious, but it is merely a reflection of suboptimal division of the fatty tissue into lymph-node stations and incomplete detection of lymph nodes by the pathologist.¹⁹

Performing splenectomy and distal pancreatectomy as part of surgery for gastric cancer has been criticized, mainly because of the immunologic properties of the spleen.²⁰ To dissect the D2 lymph nodes along the tail of the pancreas and in the hilum of the spleen, resection of these organs was required in the protocol for proximal tumor sites with invasion beyond the muscularis propria (stage T3 or T4). We found that resection of the spleen was an independent risk factor for surgical complications¹¹ and was associated with reduced survival in both the D1 and the D2 groups. Although this conclusion rests on an independent observation based on a subgroup analysis outside the scope of the trial, we concur with reports that splenic resection (and concomitant pancreatic resection) should not be part of standard gastrectomy for cancer.^11,20,21

It is difficult to compare our results with the results obtained in Japan. In our patients, lymph-node dissection was clearly defined and depended solely on the involved area of the stomach. In Japan, however, the approach is much more individualistic, with lymph-node dissection tailored according to various preoperative selection criteria. Furthermore, the outcome of curative resections in Japanese patients may have been modified by the frequent use of adjuvant chemotherapy; in Western patients, adjuvant chemotherapy after gastric resection is given only in clinical trials. In our trial, adjuvant therapy was not used in patients in the curative group.

It is well known that stage migration, in which diagnostic information leads to refined staging without actually altering the prognosis of patients with cancer, is one of the reasons for the discrepancy between the long-term results of surgery for gastric cancer in Japan and the results in the West, because additional information on lymph nodes is available only for patients with D2 dissection. Stage migration occurred in our trial in 30 percent of the D2 group.²² If we use the observed five-year survival rates, we can calculate that stage migration in the D2 group led to a drop in the patients' stage-specific survival rates of 3 percent for International Union against Cancer (UICC) stage I disease, 8 percent for stage II, 6 percent for stage IIIA, and 12 percent for stage IIIB. For comparisons of limited and extended lymph-node dissections, therefore, we recommend the use of pathological tumor staging. The subgroup analyses of five-year survival rates for pathological stage T1, T2, and T3 tumors are shown in Table 4. The five-year cumulative risks of relapse (restricted to patients who underwent R0 resections and not including in-hospital deaths) for patients with pathological stage T1, T2, and T3 tumors, respectively, were 14 percent, 48 percent, and 83 percent for D1 dissection and 11 percent, 40 percent, and 72 percent for D2 dissection.

One of the arguments for D2 dissection is its ability to reduce rates of local recurrence, thereby increasing the quality of life. The distressing finding of local recurrence, usually in a terminal phase of the disease, often leads to second operations to restore gastrointestinal continuity. In our trial, there was a tendency toward a reduced cumulative risk of relapse after D2 dissection, but the rate of relapse remained high and the difference from D1 dissection was not significant. A subgroup analysis indicated a significant or marginally significant difference for patients with disease in UICC stages II and IIIA, but this difference was attributable largely to stage migration.

Supported by grants from the Dutch Health Insurance Funds Council and the Netherlands Cancer Foundation.

We are indebted to the participating surgeons and pathologists of the Dutch Gastric Cancer Group and to the data center of the surgery department at the Leiden University Medical Center for its contribution to this trial, especially that of its head, Elma Klein Kranenbarg.

^* Centers participating in the Dutch Gastric Cancer Group are listed in the Appendix.

Source Information

From the Department of Surgery, Leiden University Medical Center, Leiden, the Netherlands (J.J.B., C.J.H.V.), the Department of Medical Statistics, Leiden University, Leiden, the Netherlands (J.H.), and the National Cancer Center Hospital, Tokyo, Japan (M.S.). Other authors were K. Welvaart and I. Songun (Leiden University Medical Center); S. Meyer (University Hospital Amsterdam Vrije University); J.T.M. Plukker (University Hospital Groningen); P. Van Elk (Geertruiden Hospital Deventer); H. Obertop, D.J. Gouma, J.J.B. van Lanschot, and C.W. Taat (Amsterdam Academic Medical Center); P.W. de Graaf (Reinier de Graaf Hospital Delft); M.F. von Meyenfeldt (University Hospital Maastricht); and H. Tilanus (University Hospital Dijkzigt Rotterdam) — all in the Netherlands.

Address reprint requests to Prof. van de Velde at the Department of Surgery, Leiden University Medical Center, P.O. Box 9600, 2300 RC Leiden, the Netherlands, or at velde{at}surgery.azl.nl.

References

1. Akoh JA, Macintyre IMC. Improving survival in gastric cancer: review of 5-year survival rates in English language publications from 1970. Br J Surg 1992;79:293-299. [Medline]
2. McNeer G, Lawrence W Jr, Ortega LG, Sunderland DA. Early results of extended total gastrectomy for cancer. Cancer 1956;9:1153-1159. [Medline]
3. Estes NC, MacDonald JS, Touijer K, Benedetti J, Jacobson J. Inadequate documentation and resection for gastric cancer in the United States: a preliminary report. Am Surg 1998;64:680-685. [Medline]
4. Kajitani T, Japanese Research Society for the Study of Gastric Cancer. The general rules for gastric cancer study in Surgery and Pathology. Jpn J Surg 1981;11:127-145. [CrossRef][Medline]
5. Pacelli F, Doglietto GB, Bellantone R, Alfieri S, Sgadari A, Crucitti F. Extensive versus limited lymph node dissection for gastric cancer: a comparative study of 320 patients. Br J Surg 1993;80:1153-1156. [Medline]
6. Roder JD, Böttcher K, Siewert JR, et al. Prognostic factors in gastric carcinoma: results of the German Gastric Carcinoma Study 1992. Cancer 1993;72:2089-2097. [CrossRef][Medline]
7. Smith JW, Shiu MH, Kelsey L, Brennan MF. Morbidity of radical lymphadenectomy in the curative resection of gastric carcinoma. Arch Surg 1991;126:1469-1473. [Abstract]
8. Sue-Ling HM. Radical surgery is essential for treating gastric cancer. Eur J Surg Oncol 1994;20:179-182. [Medline]
9. Cuschieri A, Fayers P, Fielding J, et al. Postoperative morbidity and mortality after D1 and D2 resections for gastric cancer: preliminary results of the MRC randomised controlled surgical trial. Lancet 1996;347:995-999. [CrossRef][Medline]
10. Bonenkamp JJ, Songun I, Hermans J, et al. Randomised comparison of morbidity after D1 and D2 dissection for gastric cancer in 996 Dutch patients. Lancet 1995;345:745-748. [CrossRef][Medline]
11. Sasako M. Risk factors for surgical treatment in the Dutch Gastric Cancer Trial. Br J Surg 1997;84:567-571. 
12. Beahrs OH, Henson DE, Hutter RVP, Kennedy BJ, eds. Manual for staging of cancer. 4th ed. Philadelphia: J.B. Lippincott, 1992.
13. Bonenkamp JJ, Songun I, Hermans J, van de Velde CJH. Prognostic value of positive cytology findings from abdominal washings in patients with gastric cancer. Br J Surg 1996;83:672-674. [Medline]
14. Bunt AMG, Hermans J, Boon MC, et al. Evaluation of the extent of lymphadenectomy in a randomized trial of Western- versus Japanese-type surgery in gastric cancer. J Clin Oncol 1994;12:417-422. [Abstract]
15. Wagner PK, Ramaswamy A, Ruschoff J, Schmitz-Moormann P, Rothmund M. Lymph node counts in the upper abdomen: anatomical basis for lymphadenectomy in gastric cancer. Br J Surg 1991;78:825-827. [Medline]
16. Bonenkamp JJ, van de Velde CJH, Kampschöer GHM, et al. Comparison of factors influencing the prognosis of Japanese, German, and Dutch gastric cancer patients. World J Surg 1993;17:410-415. [CrossRef][Medline]
17. Hermanek P, Hutter RVP, Sobin LH, Wagner G, Wittekind C, eds. TNM atlas. 4th ed. Berlin, Germany: Springer-Verlag, 1997.
18. Cady B. Lymph node metastases: indicators, but not governors of survival. Arch Surg 1984;119:1067-1072. [Abstract]
19. Bonenkamp JJ, Hermans J, Sasako M, van de Velde CJH. Quality control of lymph node dissection in the Dutch randomized trial of D1 and D2 dissection for gastric cancer. Gastric Cancer (in press).
20. Griffith JP, Sue-Ling HM, Martin I, et al. Preservation of the spleen improves survival after radical surgery for gastric cancer. Gut 1995;36:684-690. [Free Full Text]
21. Wanebo HJ, Kennedy BJ, Winchester DP, Stewart AK, Fremgen AM. Role of splenectomy in gastric cancer surgery: adverse effect of elective splenectomy on longterm survival. J Am Coll Surg 1997;185:177-184. [CrossRef][Medline]
22. Bunt AMG, Hermans J, Smit VTH, van de Velde, Fleuren GJ, Bruijn JA. Surgical/pathologic-stage migration confounds comparisons of gastric cancer survival rates between Japan and Western countries. J Clin Oncol 1995;13:19-25. [Free Full Text]

The following centers took part in the study: Medisch Centrum Alkmaar, Rijnoord Alphen, De Lichtenberg Amersfoort, Ziekenhuis Amstelveen, Academisch Medisch Centrum Amsterdam, Academisch Ziekenhuis Vrije Universiteit Amsterdam, Antoni van Leeuwenhoekhuis Amsterdam, St. Lucas Amsterdam, Bovenij Amsterdam, Slotervaart Amsterdam, Gooi Noord Blaricum, Ziekenhuis Centrum Apeldoorn, Rijnstate Arnhem, Diaconessenhuis Arnhem, Wilhelmina Assen, Rode Kruis Beverwijk, St. Ignatius Breda, St. Gregorius Brunssum, Reinier de Graaf Gasthuis Delft, Delfzicht Delfzijl, Geertruiden Deventer, Nij Smellinghe Drachten, Catharina Eindhoven, Diakonessenhuis Eindhoven, Dr. Jansen Emmeloord, Scheperziekenhuis Emmen, St. Anna Geldrop, Bleuland Gouda, Bronovo 's-Gravenhage, Westeinde 's-Gravenhage, Rode Kruis 's-Gravenhage, Leyenburg 's-Gravenhage, Academisch Ziekenhuis Groningen, Martini Groningen, Johannes de Deo Haarlem, Elisabeth Gasthuis Haarlem, Röpcke Zweers Hardenberg, Oranjeoord Harlingen, Spaarne Heemstede, Tjongerschans Heerenveen, Elkerliek Helmond, Streekziekenhuis Midden Twente Hengelo, Groot Ziekengasthuis 's-Hertogenbosch, Bethesda Hoogeveen, Westfries Gasthuis Hoorn, Zeeweg IJmuiden, Medisch Centrum Leeuwarden, Diaconessenhuis Leiden, Academisch Ziekenhuis Leiden, St. Antoniushove Leidschendam, IJsselmeerziekenhuizen Lelystad, Academisch Ziekenhuis Maastricht, Diaconessen Inrichting Meppel, Canisius-Wilhelmina Nijmegen, Academisch Ziekenhuis Nijmegen, St. Laurentius Roermond, Academisch Ziekenhuis Dijkzigt Rotterdam, St. Franciscus Gasthuis Rotterdam, St. Clara Rotterdam, Antonius Sneek, Ruwaard van Putten Spijkenisse, Rivierenland Tiel, St. Elisabeth Tilburg, Academisch Ziekenhuis Utrecht, Diakonessen Utrecht, Overvecht Utrecht, St. Joseph Veghel, St. Elisabeth Venray, Streekziekenhuis Walcheren Vlissingen, Diaconessenhuis Voorburg, St. Jans Gasthuis Weert, St. Lucas Winschoten, Streekziekenhuis Koningin Beatrix Winterswijk, 't Lange Land Zoetermeer, 't Nieuwe Spittaal Zutphen, Sophia Zwolle, and De Weezenlanden Zwolle.

Abstract PDF Editorial by Brennan, M. F. Letters Add to Personal Archive Add to Citation Manager Notify a Friend E-mail When Cited PubMed Citation

Related Letters:

Surgery for Gastric Cancer
Pacelli F., Sgadari A., Doglietto G.B., Bonenkamp J.J., Sasako M., van de Velde C.
Extract | Full Text  
N Engl J Med 1999; 341:538-539, Aug 12, 1999. Correspondence

This article has been cited by other articles:

• Pacelli, F., Papa, V., Rosa, F., Tortorelli, A. P., Sanchez, A. M., Covino, M., Bossola, M., Doglietto, G. B. (2008). Four Hundred Consecutive Total Gastrectomies for Gastric Cancer: A Single-Institution Experience. Arch Surg 143: 769-775 [Abstract] [Full Text]  
• Sasako, M., Sano, T., Yamamoto, S., Kurokawa, Y., Nashimoto, A., Kurita, A., Hiratsuka, M., Tsujinaka, T., Kinoshita, T., Arai, K., Yamamura, Y., Okajima, K., the Japan Clinical Oncology Group, (2008). D2 Lymphadenectomy Alone or with Para-aortic Nodal Dissection for Gastric Cancer. NEJM 359: 453-462 [Abstract] [Full Text]  
• Bilimoria, K. Y., Talamonti, M. S., Wayne, J. D., Tomlinson, J. S., Stewart, A. K., Winchester, D. P., Ko, C. Y., Bentrem, D. J. (2008). Effect of Hospital Type and Volume on Lymph Node Evaluation for Gastric and Pancreatic Cancer. Arch Surg 143: 671-678 [Abstract] [Full Text]  
• Wilkinson, N. W., Howe, J., Gay, G., Patel-Parekh, L., Scott-Conner, C., Donohue, J. (2008). Differences in the Pattern of Presentation and Treatment of Proximal and Distal Gastric Cancer: Results of the 2001 Gastric Patient Care Evaluation. Ann. Surg. Oncol. 15: 1644-1650 [Abstract] [Full Text]  
• Milne, A N A, Carvalho, R, Jansen, M, Kranenbarg, E K, van de Velde, C J H, Morsink, F M, Musler, A R, Weterman, M A J, Offerhaus, G J A (2008). Cyclin E low molecular weight isoforms occur commonly in early-onset gastric cancer and independently predict survival. J. Clin. Pathol. 61: 311-316 [Abstract] [Full Text]  
• Pritchard, S A (2008). Best practice in macroscopic examination of gastric resections. J. Clin. Pathol. 61: 172-178 [Abstract] [Full Text]  
• Izzo, J. G., Ajani, J. A. (2007). Thinking In and Out of the Box When It Comes to Gastric Cancer and Cyclooxygenase-2. JCO 25: 4865-4867 [Full Text]  
• de Maat, M. F.G., van de Velde, C. J.H., Umetani, N., de Heer, P., Putter, H., van Hoesel, A. Q., Meijer, G. A., van Grieken, N. C., Kuppen, P. J.K., Bilchik, A. J., Tollenaar, R. A.E.M., Hoon, D. S.B. (2007). Epigenetic Silencing of Cyclooxygenase-2 Affects Clinical Outcome in Gastric Cancer. JCO 25: 4887-4894 [Abstract] [Full Text]  
• Lee, J. H., Kim, Y.-W., Ryu, K. W., Lee, J. R., Kim, C. G., Choi, I. J., Kook, M. C., Nam, B.-H., Bae, J.-M. (2007). A Phase-II Clinical Trial of Laparoscopy-Assisted Distal Gastrectomy with D2 Lymph Node Dissection for Gastric Cancer Patients. Ann. Surg. Oncol. 14: 3148-3153 [Abstract] [Full Text]  
• Iddings, D. M., Bilchik, A. (2007). Gastric carcinoma: applying the sentinel node paradigm to improve the understanding of metastatic patterns and the possible role of selective lymphadenectomy.. Ann. Surg. Oncol. 14: 2432-2434 [Full Text]  
• Guo, E., Chen, L., Xie, Q., Chen, J., Tang, Z., Wu, Y. (2007). Serum HDL-C as a Potential Biomarker for Nodal Stages in Gastric Cancer. Ann. Surg. Oncol. 14: 2528-2534 [Abstract] [Full Text]  
• Pedrazzani, C., de Manzoni, G., Marrelli, D., Giacopuzzi, S., Corso, G., Minicozzi, A. M., Rampone, B., Roviello, F. (2007). Lymph node involvement in advanced gastroesophageal junction adenocarcinoma. J. Thorac. Cardiovasc. Surg. 134: 378-385 [Abstract] [Full Text]  
• De Vita, F, Giuliani, F, Orditura, M, Maiello, E, Galizia, G, Di Martino, N, Montemurro, F, Carteni, G, Manzione, L, Romito, S, Gebbia, V, Ciardiello, F, Catalano, G, Colucci, G (2007). Adjuvant chemotherapy with epirubicin, leucovorin, 5-fluorouracil and etoposide regimen in resected gastric cancer patients: a randomized phase III trial by the Gruppo Oncologico Italia Meridionale (GOIM 9602 Study). Ann Oncol 18: 1354-1358 [Abstract] [Full Text]  
• Lee, J. H., Paik, Y. H., Lee, J. S., Ryu, K. W., Kim, C. G., Park, S. R., Kim, Y. W., Kook, M. C., Nam, B.-h., Bae, J.-M. (2007). Abdominal Shape of Gastric Cancer Patients Influences Short-Term Surgical Outcomes. Ann. Surg. Oncol. 14: 1288-1294 [Abstract] [Full Text]  
• Barbour, A. P., Rizk, N. P., Gonen, M., Tang, L., Bains, M. S., Rusch, V. W., Coit, D. G., Brennan, M. F. (2007). Lymphadenectomy for Adenocarcinoma of the Gastroesophageal Junction (GEJ): Impact of Adequate Staging on Outcome. Ann. Surg. Oncol. 14: 306-316 [Abstract] [Full Text]  
• Schwarz, R. E., Smith, D. D. (2007). Clinical impact of lymphadenectomy extent in resectable gastric cancer of advanced stage. Ann. Surg. Oncol. 14: 317-328 [Abstract] [Full Text]  
• Nishikawa, T., Maetani, S. (2007). Evaluation of Intensive Adjuvant Chemotherapy in Gastric Cancer Using Life Expectancy Compared with Log-Rank Test as a Measure of Survival Benefit. Ann. Surg. Oncol. 14: 348-354 [Abstract] [Full Text]  
• Gee, D. W., Rattner, D. W. (2007). Management of Gastroesophageal Tumors. The Oncologist 12: 175-185 [Abstract] [Full Text]  
• Marrelli, D., Pedrazzani, C., Neri, A., Corso, G., DeStefano, A., Pinto, E., Roviello, F. (2007). Complications after Extended (D2) and Superextended (D3) Lymphadenectomy for Gastric Cancer: Analysis of Potential Risk Factors. Ann. Surg. Oncol. 14: 25-33 [Abstract] [Full Text]  
• Lee, J. H., Ryu, K. W., Lee, J.-H., Park, S. R., Kim, C. G., Kook, M. C., Nam, B.-H., Kim, Y.-W., Bae, J.-M. (2006). Learning Curve for Total Gastrectomy with D2 Lymph Node Dissection: Cumulative Sum Analysis for Qualified Surgery. Ann. Surg. Oncol. 13: 1175-1181 [Abstract] [Full Text]  
• Cunningham, D., Allum, W. H., Stenning, S. P., Thompson, J. N., Van de Velde, C. J.H., Nicolson, M., Scarffe, J. H., Lofts, F. J., Falk, S. J., Iveson, T. J., Smith, D. B., Langley, R. E., Verma, M., Weeden, S., Chua, Y. J., the MAGIC Trial Participants, (2006). Perioperative chemotherapy versus surgery alone for resectable gastroesophageal cancer.. NEJM 355: 11-20 [Abstract] [Full Text]  
• Costa, M. L. V., de Cassia Braga Ribeiro, K., Machado, M. A. C., Costa, A. C. L. V., Montagnini, A. L. (2006). Prognostic Score in Gastric Cancer: The Importance of a Conjoint Analysis of Clinical, Pathologic, and Therapeutic Factors. Ann. Surg. Oncol. 13: 843-850 [Abstract] [Full Text]  
• Ohtsu, A., Yoshida, S., Saijo, N. (2006). Disparities in Gastric Cancer Chemotherapy Between the East and West. JCO 24: 2188-2196 [Abstract] [Full Text]  
• Black, E., Niamat, J., Boddu, S., Martin-Ucar, A., Duffy, J. P., Morgan, W. E., Beggs, F. D. (2006). Unplanned splenectomy during oesophagectomy does not affect survival. Eur. J. Cardiothorac. Surg. 29: 244-247 [Abstract] [Full Text]  
• Nitti, D., Wils, J., Dos Santos, J. G., Fountzilas, G., Conte, P. F., Sava, C., Tres, A., Coombes, R. C., Crivellari, D., Marchet, A., Sanchez, E., Bliss, J. M., Homewood, J., Couvreur, M. L., Hall, E., Baron, B., Woods, E., Emson, M., Van Cutsem, E., Lise, M. (2006). Randomized phase III trials of adjuvant FAMTX or FEMTX compared with surgery alone in resected gastric cancer. A combined analysis of the EORTC GI Group and the ICCG. Ann Oncol 17: 262-269 [Abstract] [Full Text]  
• Baxter, N. N., Tuttle, T. M. (2005). Inadequacy of Lymph Node Staging in Gastric Cancer Patients: A Population-Based Study. Ann. Surg. Oncol. 12: 981-987 [Abstract] [Full Text]  
• Smith, D. D., Schwarz, R. R., Schwarz, R. E. (2005). Impact of Total Lymph Node Count on Staging and Survival After Gastrectomy for Gastric Cancer: Data From a Large US-Population Database. JCO 23: 7114-7124 [Abstract] [Full Text]  
• Yun, M., Lim, J. S., Noh, S. H., Hyung, W. J., Cheong, J. H., Bong, J. K., Cho, A., Lee, J. D. (2005). Lymph Node Staging of Gastric Cancer Using 18F-FDG PET: A Comparison Study with CT. JNM 46: 1582-1588 [Abstract] [Full Text]  
• Kollmannsberger, C., Budach, W., Stahl, M., Schleucher, N., Hehr, T., Wilke, H., Schleicher, J., Vanhoefer, U., Jehle, E. C., Oechsle, K., Trarbach, T., Boehlke, I., Kanz, L., Hartmann, J. T., Bokemeyer, C. (2005). Adjuvant chemoradiation using 5-fluorouracil/folinic acid/cisplatin with or without paclitaxel and radiation in patients with completely resected high-risk gastric cancer: two cooperative phase II studies of the AIO/ARO/ACO. Ann Oncol 16: 1326-1333 [Abstract] [Full Text]  
• Ajani, J.A., Mansfield, P.F., Crane, C.H., Wu, T.T., Lunagomez, S., Lynch, P.M., Janjan, N., Feig, B., Faust, J., Yao, J.C., Nivers, R., Morris, J., Pisters, P.W. (2005). Paclitaxel-Based Chemoradiotherapy in Localized Gastric Carcinoma: Degree of Pathologic Response and Not Clinical Parameters Dictated Patient Outcome. JCO 23: 1237-1244 [Abstract] [Full Text]  
• Lee, W.-J., Kappas, A. M., Fatouros, M., Roukos, D. H. (2005). It Is Still Not the Time to Change Surgical Strategy for Gastric Cancer. Ann. Surg. Oncol. 12: 194-196 [Full Text]  
• Kappas, A. M., Fatouros, M., Roukos, D. H. (2004). Editorial: Is it Time to Change Surgical Strategy for Gastric Cancer in the United States?. Ann. Surg. Oncol. 11: 727-730 [Full Text]  
• Ajani, J.A., Mansfield, P.F., Janjan, N., Morris, J., Pisters, P.W., Lynch, P.M., Feig, B., Myerson, R., Nivers, R., Cohen, D.S., Gunderson, L.L. (2004). Multi-Institutional Trial of Preoperative Chemoradiotherapy in Patients With Potentially Resectable Gastric Carcinoma. JCO 22: 2774-2780 [Abstract] [Full Text]  
• Birkmeyer, J. D. (2004). Understanding Surgeon Performance and Improving Patient Outcomes. JCO 22: 2765-2766 [Full Text]  
• Mansfield, P. F. (2004). Lymphadenectomy for Gastric Cancer. JCO 22: 2759-2761 [Full Text]  
• Weitz, J., Jaques, D. P., Brennan, M., Karpeh, M. (2004). Association of Splenectomy With Postoperative Complications in Patients With Proximal Gastric and Gastroesophageal Junction Cancer. Ann. Surg. Oncol. 11: 682-689 [Abstract] [Full Text]  
• Hartgrink, H.H., van de Velde, C.J.H., Putter, H., Bonenkamp, J.J., Klein Kranenbarg, E., Songun, I., Welvaart, K., van Krieken, J.H.J.M., Meijer, S., Plukker, J.T.M., van Elk, P.J., Obertop, H., Gouma, D.J., van Lanschot, J.J.B., Taat, C.W., de Graaf, P.W., von Meyenfeldt, M.F., Tilanus, H., Sasako, M. (2004). Extended Lymph Node Dissection for Gastric Cancer: Who May Benefit? Final Results of the Randomized Dutch Gastric Cancer Group Trial. JCO 22: 2069-2077 [Abstract] [Full Text]  
• Dicken, B.J., Saunders, L.D., Jhangri, G.S., de Gara, C., Cass, C., Andrews, S., Hamilton, S.M. (2004). Gastric Cancer: Establishing Predictors of Biologic Behavior with Use of Population-Based Data. Ann. Surg. Oncol. 11: 629-635 [Abstract] [Full Text]  
• Bollschweiler, E. H., Monig, S. P., Hensler, K., Baldus, S. E., Maruyama, K., Holscher, A. H. (2004). Artificial Neural Network for Prediction of Lymph Node Metastases in Gastric Cancer: A Phase II Diagnostic Study. Ann. Surg. Oncol. 11: 506-511 [Abstract] [Full Text]  
• Ajani, J. A. (2004). Operate on My Stomach Cancer? Oh, No--Not You, or Not Yet!. JCO 22: 1763-1764 [Full Text]  
• van Beek, J., zur Hausen, A., Klein Kranenbarg, E., van de Velde, C. J.H., Middeldorp, J. M., van den Brule, A. J.C., Meijer, C. J.L.M., Bloemena, E. (2004). EBV-Positive Gastric Adenocarcinomas: A Distinct Clinicopathologic Entity With a Low Frequency of Lymph Node Involvement. JCO 22: 664-670 [Abstract] [Full Text]  
• Roukos, D. H. (2004). Early-Stage Gastric Cancer: A Highly Treatable Disease. Ann. Surg. Oncol. 11: 127-129 [Full Text]  
• Weitz, J., D'Angelica, M., Gonen, M., Klimstra, D., Coit, D. G., Brennan, M. F., Karpeh, M. S. (2003). Interaction of Splenectomy and Perioperative Blood Transfusions on Prognosis of Patients With Proximal Gastric and Gastroesophageal Junction Cancer. JCO 21: 4597-4603 [Abstract] [Full Text]  
• Peeters, K.C.M.J., van de Velde, C.J.H. (2003). Improving Treatment Outcome for Gastric Cancer: The Role of Surgery and Adjuvant Therapy. JCO 21: 272s-273 [Full Text]  
• Sasako, M. (2003). Principles of Surgical Treatment for Curable Gastric Cancer. JCO 21: 274s-275 [Full Text]  
• Nitti, D., Marchet, A., Olivieri, M., Ambrosi, A., Mencarelli, R., Belluco, C., Lise, M. (2003). Ratio Between Metastatic and Examined Lymph Nodes Is an Independent Prognostic Factor After D2 Resection for Gastric Cancer: Analysis of a Large European Monoinstitutional Experience. Ann. Surg. Oncol. 10: 1077-1085 [Abstract] [Full Text]  
• Shimoyama, S., Mafune, K.-i., Kaminishi, M. (2003). Indications for a Pylorus-Preserving Gastrectomy for Gastric Cancer With Proper Muscle Invasion. Arch Surg 138: 1235-1239 [Abstract] [Full Text]  
• Park, S. H., Kim, D. Y., Heo, J. S., Lim, D. H., Park, C. K., Lee, K. W., Choi, S. H., Sohn, T. S., Kim, S., Noh, J. H., Kim, Y. I., Park, J. O., Kim, K., Kim, W. S., Jung, C. W., Im, Y. H., Lee, M. H., Park, K., Park, C. H., Kang, W. K. (2003). Postoperative chemoradiotherapy for gastric cancer. Ann Oncol 14: 1373-1377 [Abstract] [Full Text]  
• van de Velde, C. J.H., Peeters, K. C.M.J. (2003). The Gastric Cancer Treatment Controversy. JCO 21: 2234-2236 [Full Text]  
• Gill, S., Shah, A., Le, N., Cook, E. F., Yoshida, E. M. (2003). Asian Ethnicity-Related Differences in Gastric Cancer Presentation and Outcome Among Patients Treated at a Canadian Cancer Center. JCO 21: 2070-2076 [Abstract] [Full Text]  
• Gretschel, S., Christoph, F., Bembenek, A., Estevez-Schwarz, L., Schneider, U., Schlag, P. M. (2003). Body Mass Index Does Not Affect Systematic D2 Lymph Node Dissection and Postoperative Morbidity in Gastric Cancer Patients. Ann. Surg. Oncol. 10: 363-368 [Abstract] [Full Text]  
• Douglass, H. O. (2003). Gastric Cancer: D2 All Over Again. Ann. Surg. Oncol. 10: 206-207 [Full Text]  
• Sierra, A., Regueira, F. M., Hernandez-Lizoain, J. L., Pardo, F., Martinez-Gonzalez, M. A., A.-Cienfuegos, J. (2003). Role of the Extended Lymphadenectomy in Gastric Cancer Surgery: Experience in a Single Institution. Ann. Surg. Oncol. 10: 219-226 [Abstract] [Full Text]  
• Roukos, D. H., Briasoulis, E., Michos, K. M., Elisaf, M., Agnantis, N. J., Kappas, A. M. (2003). Breast and Gastric Cancer: Comparing What We Learn. Ann. Surg. Oncol. 10: 92-94 [Full Text]  
• Kitajima, M., Kitagawa, Y. (2002). Surgical Treatment of Esophageal Cancer -- The Advent of the Era of Individualization. NEJM 347: 1705-1709 [Full Text]  
• Kappas, A. M., Roukos, D. H. (2002). Quality of Surgery Determinant for the Outcome of Patient With Gastric Cancer. Ann. Surg. Oncol. 9: 828-830 [Full Text]  
• Roviello, F., Marrelli, D., Morgagni, P., de Manzoni, G., Di Leo, A., Vindigni, C., Saragoni, L., Tomezzoli, A., Kurihara, H. (2002). Survival Benefit of Extended D2 Lymphadenectomy in Gastric Cancer With Involvement of Second Level Lymph Nodes: A Longitudinal Multicenter Study. Ann. Surg. Oncol. 9: 894-900 [Abstract] [Full Text]  
• Bando, E., Yonemura, Y., Taniguchi, K., Fushida, S., Fujimura, T., Miwa, K. (2002). Outcome of Ratio of Lymph Node Metastasis in Gastric Carcinoma. Ann. Surg. Oncol. 9: 775-784 [Abstract] [Full Text]  
• Sano, T., Yamamoto, S., Sasako, M. (2002). Randomized Controlled Trial to Evaluate Splenectomy in Total Gastrectomy for Proximal Gastric Carcinoma: Japan Clinical Oncology Group Study JCOG 0110-MF. Jpn J Clin Oncol 32: 363-364 [Abstract] [Full Text]  
• McCulloch, P., Taylor, I., Sasako, M., Lovett, B., Griffin, D. (2002). Randomised trials in surgery: problems and possible solutions. BMJ 324: 1448-1451 [Full Text]  
• Allum, W H, Griffin, S M, Watson, A, Colin-Jones, D (2002). Guidelines for the management of oesophageal and gastric cancer. Gut 50 : v1-v23 [Full Text]  
• Schwarz, R. E., Zagala-Nevarez, K. (2002). Recurrence Patterns After Radical Gastrectomy for Gastric Cancer: Prognostic Factors and Implications for Postoperative Adjuvant Therapy. Ann. Surg. Oncol. 9: 394-400 [Abstract] [Full Text]  
• Yoshikawa, T., Tsuburaya, A., Kobayashi, O., Sairenji, M., Motohashi, H., Noguchi, Y. (2002). Is D2 Lymph Node Dissection Necessary for Early Gastric Cancer?. Ann. Surg. Oncol. 9: 401-405 [Abstract] [Full Text]  
• Roukos, D. H. (2002). Adjuvant Chemoradiotherapy in Gastric Cancer: Wave Goodbye to Extensive Surgery?. Ann. Surg. Oncol. 9: 220-221 [Full Text]  
• Hundahl, S. A., Macdonald, J. S., Benedetti, J., Fitzsimmons, T. (2002). Surgical Treatment Variation in a Prospective, Randomized Trial of Chemoradiotherapy in Gastric Cancer: The Effect of Undertreatment. Ann. Surg. Oncol. 9: 278-286 [Abstract] [Full Text]  
• Bajetta, E., Buzzoni, R., Mariani, L., Beretta, E., Bozzetti, F., Bordogna, G., Aitini, E., Fava, S., Schieppati, G., Pinotti, G., Visini, M., Ianniello, G., Di Bartolomeo, M. (2002). Adjuvant chemotherapy in gastric cancer: 5-year results of a randomised study by the Italian Trials in Medical Oncology (ITMO) Group. Ann Oncol 13: 299-307 [Abstract] [Full Text]  
• Shoup, M., Brennan, M. F., McWhite, K., Leung, D. H. Y., Klimstra, D., Conlon, K. C. (2002). The Value of Splenic Preservation With Distal Pancreatectomy. Arch Surg 137: 164-168 [Abstract] [Full Text]  
• Abraham, I., Dhar, P., Praseedom, R. K., Atkins, C. D., Berney, C. R., Merrett, N. D., Macdonald, J. S., Benedetti, J., Hundahl, S. A. (2002). Adjuvant Chemoradiotherapy for Gastric Cancer. NEJM 346: 210-211 [Full Text]  
• Inoue, K., Nakane, Y., Iiyama, H., Sato, M., Kanbara, T., Nakai, K., Okumura, S., Yamamichi, K., Hioki, K. (2002). The Superiority of Ratio-Based Lymph Node Staging in Gastric Carcinoma. Ann. Surg. Oncol. 9: 27-34 [Abstract] [Full Text]  
• Macdonald, J. S., Smalley, S. R., Benedetti, J., Hundahl, S. A., Estes, N. C., Stemmermann, G. N., Haller, D. G., Ajani, J. A., Gunderson, L. L., Jessup, J. M., Martenson, J. A. (2001). Chemoradiotherapy after Surgery Compared with Surgery Alone for Adenocarcinoma of the Stomach or Gastroesophageal Junction. NEJM 345: 725-730 [Abstract] [Full Text]  
• Roukos, D. H., Kappas, A. M. (2001). Limitations in Controlling Risk for Recurrence After Curative Surgery for Advanced Gastric Cancer Are Now Well-Explained by Molecular-Based Mechanisms. Ann. Surg. Oncol. 8: 620-621 [Full Text]  
• (2001). East is East and West was West: Closing the Gap in the Delivery of Gastric Cancer Surgery. Jpn J Clin Oncol 31: 469-470 [Full Text]  
• Ota, D. M. (2001). A Pilot Study of Preoperative Chemoradiation for Gastric Cancer. Ann. Surg. Oncol. 8: 482-483 [Full Text]  
• Lee, K. Y., Noh, S. H., Hyung, W. J., Lee, J. H., Lah, K. H., Choi, S. H., Min, J. S. (2001). Impact of Splenectomy for Lymph Node Dissection on Long-Term Surgical Outcome in Gastric Cancer. Ann. Surg. Oncol. 8: 402-406 [Abstract] [Full Text]  
• Schwarz, R. E., Kelsen, D. P. (2001). Postoperative Adjuvant Chemoradiation Therapy for Patients With Resected Gastric Cancer: Intergroup 116. JCO 19: 1879-1880 [Full Text]  
• Melville, A, Eastwood, A, Morris, E, Forman, D (2001). Management of upper gastrointestinal cancers. Qual Saf Health Care 10: 57-64 [Full Text]  
• Kelsen, D. P. (2000). Postoperative Adjuvant Chemoradiation Therapy for Patients With Resected Gastric Cancer: Intergroup 116. JCO 18: 32s-34 [Full Text]  
• Davis, P. A. (2000). The Management of Patients with Gastric Cancer: Can West Meet East?. Jpn J Clin Oncol 30: 463- [Full Text]  
• Cady, B. (2000). Sentinel Lymph Node Procedure in Squamous Cell Carcinoma of the Vulva. JCO 18: 2795-2797 [Full Text]  
• Doglietto, G. B., Pacelli, F., Caprino, P., Bossola, M., Stasi, C. D. (2000). Pancreas-Preserving Total Gastrectomy for Gastric Cancer. Arch Surg 135: 89-92 [Abstract] [Full Text]  
• Pacelli, F., Sgadari, A., Doglietto, G.B., Bonenkamp, J.J., Sasako, M., van de Velde, C. (1999). Surgery for Gastric Cancer. NEJM 341: 538-539 [Full Text]  
• Brennan, M. F. (1999). Lymph-Node Dissection for Gastric Cancer. NEJM 340: 956-958 [Full Text]