Original Articles Open Access
Copyright ©The Author(s) 2001. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. Apr 15, 2001; 7(2): 281-284
Published online Apr 15, 2001. doi: 10.3748/wjg.v7.i2.281
Clinicopathological analysis of patients with gastric cancer in 1200 cases
Wei-Xin Niu, Xin-Yu Qin, Cheng-Pei Wang, Han-Liu, Surgical Department, Zhongshan Hospital, Fu Dan University Medical Center, Shanghai 200032, China
Wei-Xin Niu, graduated from Shanghai Medical University as postgraduate in 1991, now associate professor of surgery, having 16 papers published.
Author contributions: All authors contributed equally to the work.
Correspondence to: Dr. Wei-Xin Niu, Surgical Department, Zhongshan Hospital, Fu Dan University Medical Center, 136 Yixueyuan Road,Shanghai 200032, China
Telephone: +86-21-64041990 Ext.2810 or 2276
Received: November 15, 2000
Revised: November 25, 2000
Accepted: November 30, 2000
Published online: April 15, 2001

Abstract
Key Words: stomach neoplasms/pathology, stomach neoplasms/surgery, lymphatic metastasis, neoplasm invasiveness, gastrectomy



INTRODUCTION

Gastric cancer is one of the most common fatal malignancies in the world. The prognosis is generally poor in advanced gastric cancer. The low survival is related to delayed diagnosis, metastasis and recurrence after operation. The aim of this paper was to find correlation between clinical factors and biologic behavior of gastric cancer in a series of 1200 patients undergoing surgical resection.

PATIENTS AND METHODS

Between November 1992 and December 1999, 1200 patients with stomach cancer confirmed by pathology underwent radical operations. The mean patient age at operation was 54.2 (range 22-89) years, 836 patients were male and 364 were female, with a mean postoperative hospitalization of 16.2 (range 6-127) days.

We analyzed the following clinicopathologic and surgical factors: age, sex, hemoglobin, operation manners, operation time, amount of transfusion during operation, postoperative hospital stay, postoperative complications, positive proximal margin, location of tumor, tumor size, differentiation, depth of tumor invasion, lymph nodes and lymphatic metastasis rate. Frequency of positive lymph nodes = numbers of metastatic lymph nodes / all lymph nodes excised × 100%.

Statistics

All data were analyzed by SPSS statistics program. The comparisons were made by Chi-square test, one-way ANOVA, linear and multivariate regression analysis, P < 0.05 was considered as significant.

RESULTS

Of these 1200 patients, 768 (64%) underwent distal gastrectomy, 72 (6%) proximal gastrectomy via abdomen and 264 (22%) via thorax, and 96 (8%) underwent total gastrectomy. Distal and total gastrectomy had more numbers of clearances of lymph nodes than the other operational approaches. The postoperative complications occurred in 96 patients (96/1200, 8%), including gastric retention in 22 (22/96, 23%), anastomotic leakage in 18 (18/96, 18.7%), infection of incision in 16 (16/96, 14.6%), disruption of wound in 8 (8/96, 8.3%), and thoracic cavity effusion in 8(8/96, 8.3%). The complication was most common in proximal gastrectomy via abdomen (16/96, 17% patients) (Table 1). The overall mortality was 0.4% (5/1200).

Table 1 Comparison of operation manner with numbers of lymph nodes, time for operation, amount of blood transfusion during operation, hospitalization days and complications (-x±sx).
Manners of operationN (1200)Numbers lymph nodesTime for operation (h)Amount of blood transfusion (mL)Hospitalization stays (days)Complication (%)Positive resection margin (%)
Distal gastrectomy76811.7 ± 0.3*3.3 ± 0.04426.5 ± 17.1*16.9 ± 0.79.13.8
Proximal gastrectomy via abdomen729.6 ± 0.44.0 ± 0.1*629.5 ± 43.3*18.3 ± 1.517*8.2*
Proximal gastrectomy via thorax2648.2 ± 0.23.3 ± 0.03771.5 ± 19.515.5 ± 0.61.68.7*
Total gastrectomy9613.8 ± 0.7*4.6 ± 0.1*768.2 ± 47.619.8 ± 1.712.99.3*
P< 0.0001< 0.0001< 0.0001> 0.05< 0.001= 0.01

The diameter of the neoplasm was positively correlated with the depth of infiltration and lymphatic metastasis rate while hemoglobin was the opposite. One hundred and seventy-nine (14.9%) of 1200 were early gastric carcinoma (EGC) with metastasis of lymph nodes in 21 patients (21/179, 11.7%). The frequency of positive lymph nodes in these patients was 3%-4% less than in advanced gastric cancer (Table 2). In linear regression analysis, age and diameter of the tumor were negatively correlated with the preoperative hemoglobin (P < 0.001). The diameter of the tumor was positively correlated with age and the frequency of positive lymph nodes (P < 0.01).

Table 2 Comparison of depth of infiltration with age, diameter, hemoglobin, and lymphatic metastasis rate (-x±sx).
Depth of invasionN (1200)Age (yrs)Diameter (cm)Hemoglobin(g/L)Lymphatic metastasis rate (%)
pT1(m)11451.6 ± 1.22.3 ± 0.412.1 ± 0.33.2 ± 0.8
pT1(ms)6555.7 ± 1.5*2.5 ± 0.711.3 ± 0.4*4.1 ± 1.3
pT29156.8 ± 1.4*3.1 ± 0.311.2 ± 0.1*9.8 ± 1.6*
pT39557.1 ± 1.2*4.2 ± 0.6*11.4 ± 0.2*20.4 ± 2.9*
pT483556.9 ± 0.3*5.6 ± 0.1*11.2 ± 0.1*37.1 ± 1.2*
P< 0.003< 0.0001< 0.001< 0.0001

The patients with tumor of bad differentiation were younger than the other groups, who had larger tumor diameter and higher frequency of positive lymph nodes. The degree of differentiation was not related with the depth of tumor invasion on the gastric wall (Table 3). The tumor diameter on the corpus and fundus was larger than the others, which had higher frequency of positive lymph nodes (Table 4). The proximal gastric cancer, bad differentiation and frequency > 30% positive lymph nodes were more common in female than in male (Table 5).

Table 3 Comparison of differentiation with age, diameter, hemoglobin and lymphatic metastasis rate (-x±sx).
DifferentiationN (1200)Age (yrs)Diameter (cm)Hemoglobin (g/L)Lymphatic metastasis rate (%)
I3761.4 ± 1.43.5 ± 0.210.7 ± 0.410.3 ± 3.2*
II16157.9 ± 0.84.1 ± 0.311.1 ± 0.126.1 ± 2.5
III32958.6 ± 0.74.2 ± 0.211.2 ± 0.322.7 ± 1.4
IV67353.2 ± 0.3*4.9 ± 0.3*11.8 ± 0.1*33.6 ± 1.2*
P< 0.0001= 0.004= 0.01< 0.0001
Table 4 Comparison of tumor site with age, diameter, hemoglobin and positive lymph node rate (-x±sx).
Location of tumorN (1200)Age (yrs)Diameter (cm)Hemoglobin (g/L)Lymphatic metastasis rate (%)
Pylorus2754.3 ± 2.93.9 ± 0.712.6 ± 0.713.9 ± 3.2
Antrum37956.6 ± 0.5*4.6 ± 0.211.5 ± 0.326.3 ± 1.4
Incisura37254.2 ± 0.43.3 ± 0.412.5 ± 0.122.5 ± 1.3
Corpus9155.2 ± 1.26.4 ± 0.5*12.2 ± 0.438.3 ± 4.2*
Fundus33159.8 ± 0.6*5.6 ± 0.2*12.8± 0.235.1 ± 1.9*
P< 0.0001< 0.0001> 0.005< 0.001
Table 5 Comparison of sex with tumor location, differentiation, depth of invasion and positive lymph node rate (-x±sx).
SexLocation (%)
Differentiation (%)
Depth of invasion (%)
Frequency of metastatic lymph node (%)
ProximalMiddleDistalWellMiddleBadpT1pT2pT3< 30> 30
Male (836)31240183052148786436
Female (364)40325132166157785644
P< 0.001< 0.001> 0.05= 0.01

Multiple analysis demonstrated that sex, location of tumor, tumor diameter, depth of tumor invasion and differentiation play an important role in the metastasis of lymph nodes (Table 6).

Table 6 Multi-factors analysis of lymphatic metastasis in gastric patients.
Related factorsRegression coefficientStandard errorStandard regression coefficientP
Constant-24.37.10.001
Age-0.0061440.079-0.220.438
Sex-6.4892.027-0.0920.001
Tumor location2.3260.7800.0870.003
Diameter of tumor2.3680.4590.1650.0001
Depth of invasion7.0430.7860.2850.0001
Differentiation3.6871.1460.0940.001
DISCUSSION

Gastric cancer remains one of most common causes of death. Although the etiology of gastric cancer is still unclear, but studies have shown that many factors are associated with the development, metastasis of gastric cancer, and recurrence after operation[1-9]. Recent studies suggest that infection with Helicobacter pylori may play an important role in the development of gastric cancer[10-15]. It has been proposed that Helicobacter pylori infection may produce acute and chronic gastritis, intestinal metaplasia, dysplasia, and eventually resulting in gastric cancer. Some abnormal expression[16-18] in gene is involved in carcinogenesis of gastric cancer such as matrix metalloproteinases gene, p53 gene and dinucleotide repeat sequence gene. Abnormal contents of some trace elements may also be one of the risk factors in gastric cancer[19,20].

Early gastric cancer (EGC) has been considered to be a form of gastric malignancy with a relatively good long-term prognosis compared to that of advanced gastric cancer because of rare metastasis in lymph nodes[21-26]. In Japan, EGC is diagnosed in 30%-50%, due to partly at least the extensive use of endoscopy and mass screening programs[27-29]. In this study, the proportion of EGC diagnosed in all patients is 14.9%, similar to the proportion in the United States and Europe[30,31]. In recent years, endoscopic treatment has become increasingly popular as an alternative to surgical treatment of patients with EGA in hope of offering superior quality of life (QOL)[32]. However, because of presence of metastasis in 10%-20% and skip metastasis of lymph nodes, whether the rationale for a standard resection with systematic lymphadenectomy is necessary is still a controversial issue[33-37].

Different operative approaches were carried out according to the different locations of the tumor. In our study, the number of lymph nodes excised were the largest in total gastrectomy, followed by distal gastrectomy which may be related to the resection of all or most parts of omentum. The number of lymph nodes excised in proximal gastrectomy via a transabdomen was similar to via transthorax. There was shorter time for operation and lower frequency of complication in proximal gastrectomy via transthorax while lower blood transfusion in proximal gastrectomy via transabdomen. The postoperative hospitalization stay and the positive resection margin was same between them. The complications varied among different operations: gastric retention was common in distal gastrectomy while thorax effusion and infection of lung were mainly found in total gastrectomy.

Although the overall incidence of gastric cancer has remained stable in the West, there is well-documented shift from distal to proximal lesion. The clinical relevance of this shift is that the overall prognosis for patients with proximal gastric cancer is worse than for those with distal tumor. This difference in survival may be attributed to a variety of factors, ranging from an increased biologic aggressiveness of proximal tumors to an advanced stage of presentation[38,39]. In study, a higher frequency of positive lymph nodes was found in gastric cancer located on corpus and the fundus which may be associated with the larger diameter of the tumor in corpus and the fundus. In tumors with larger diameters there were worse differentiation, deeper infiltration, and higher frequency of positive lymph nodes. Apparently, the prognosis will be worse in these patients. The present results also show that the more proximal lesions, bad differentiation, and the higher > 30% frequency of positive lymph nodes can be found in female than in male.

The numbers of metastatic lymph nodes play an important role in the long-term outcome after curative resection[40-43]. Thus it is suggested that extended lymphadenectomy should be performed in advanced gastric cancer[44-47]. Our multivariate analysis indicated that among six clinicopathologic variables (age, sex, location of tumor, tumor diameter, depth of invasion and differentiation), the depth of invasion was the most important factor influencing metastasis of lymph node.

In conclusion, this retrospective study has shown that clinicopathological characters in gastric cancer varied with sex, location, and diameter of the tumor. The depth of invasion plays a very important role in metastasis of lymph node. The prognosis in female with gastric cancer may be worse than in man. Because metastasis of lymph nodes may occur even in patients with EGC, radical gastrectomy witi lymphadenectomy may be necessary in all stages of gastric cancer.

Footnotes

Edited by Ma JY

References
1.  Deng DJ. progress of gastric cancer etiology: N-nitrosamides 1999s. World J Gastroenterol. 2000;6:613-618.  [PubMed]  [DOI]  [Cited in This Article: ]
2.  Sun GY, Liu WW, Zhou ZQ, Fang DC, Men RP, Luo YH. Free radicals in development of experimental gastric carcinoma and precancerous lesions induced by Nmethyl-N' nitro-N-nitrosoguanidine in rats. Huaren Xiaohua Zazhi. 1998;6:219-221.  [PubMed]  [DOI]  [Cited in This Article: ]
3.  Ma JL, Liu WD, Zhang ZZ, Zhang L, You WC, Chang YS. Rela-tionship between gastric cancer and precancerous lesions. Huaren Xiaohua Zazhi. 1998;6:222-223.  [PubMed]  [DOI]  [Cited in This Article: ]
4.  Liu HF, Liu WW, Fang DC. Study of the relationship between apoptosis and proliferation in gastric carcinoma and its precan-cerous lesion. Shijie Huaren Xiaohua Zazhi. 1999;7:649-651.  [PubMed]  [DOI]  [Cited in This Article: ]
5.  Zhang X, Wang YJ, Geng M, Ding JY. nm23 and c-erbB-2 proto oncogene protein expression in gastric recurrent carcinoma. Huaren Xiaohua Zazhi. 1998;6:227-228.  [PubMed]  [DOI]  [Cited in This Article: ]
6.  Xiong MM, Jiang JR, Liang WL, Meng XL, Zhang CL, Peng C. A study on vasoactive intestinal peptide in serum, carcinomatous tissue and its surrounding mucosa in patients with gastric cancer. Huaren Xiaohua Zazhi. 1998;6:121-122.  [PubMed]  [DOI]  [Cited in This Article: ]
7.  Tao HQ, Lin YZ, Wang RN. Significance of vascular endothelial growth factor messenger RNA expression in gastric cancer. World J Gastroenterol. 1998;4:10-13.  [PubMed]  [DOI]  [Cited in This Article: ]
8.  Xia JZ, Zhu ZG, Liu BY, Yan M, Yin HR. Significance of immunohistochemically demonstrated micrometastases to lymph nodes gastric carcinomas. Shijie Huaren Xiaohua Zazhi. 2000;8:1113-1116.  [PubMed]  [DOI]  [Cited in This Article: ]
9.  Xu L, Zhang SM, Wang YP, Zhao FK, Wu DY, Yan X. Relationship between DNA ploidy,expression of ki-67 antigen and gastric cancer metastasis. World J Gastroenterol. 1999;5:10-11.  [PubMed]  [DOI]  [Cited in This Article: ]
10.  He XX, Wang JL, Wu JL, Yuan SY, Ai L. Telomerase expression, Hp infection and gastric mucosal carcinogenesis. Shijie Huaren Xiaohua Zazhi. 2000;8:505-508.  [PubMed]  [DOI]  [Cited in This Article: ]
11.  Guo CQ, Wang YP, Liu GY, Ma SW, Ding GY, Li JC. Study on Helicobacter pylori infection and p53, c-erbB-2 gene expression in carcinogenesis of gastric mucosa. Shijie Huaren Xiaohua Zazhi. 1999;7:313-315.  [PubMed]  [DOI]  [Cited in This Article: ]
12.  Liu HF, Liu WW, Fang DC, Men RF, Wang ZH. Apoptosis and its relationship with Fas ligand expression in gastric carcinoma and its precancerous lesion. Shijie Huaren Xiaohua Zazhi. 1999;7:561-563.  [PubMed]  [DOI]  [Cited in This Article: ]
13.  Pan KF, Liu WD, Ma JL, Zhou T, Zhang L, Chang YS, You WC. Infection of Helicobacter pylori in children and mode of transmission in a high-risk area of gastric cancer. Huaren Xiaohua Zazhi. 1998;6:42-44.  [PubMed]  [DOI]  [Cited in This Article: ]
14.  Zhang L, Jiang J, Pan KF, Liu WD, Ma JL, Zhou T, Perez-Perez GI, Blaser MJ, Chang YS, You WC. Infection of H.pylori with cagA strain in a high-risk area of gastric cancer. Huaren Xiaohua Zazhi. 1998;6:40-41.  [PubMed]  [DOI]  [Cited in This Article: ]
15.  Harry XH. Association between Helicobacter pylori and gastric cancer: current knowledge and future research. World J Gastroenterol. 1998;4:93-96.  [PubMed]  [DOI]  [Cited in This Article: ]
16.  Li N, Xu CP, Song P, Fang DC, Yang SM, Meng RP. Overpression of matrix metalloproteinases gene in human gastric carcinoma. Huaren Xiaohua Zazhi. 1998;6:118-120.  [PubMed]  [DOI]  [Cited in This Article: ]
17.  Zhou XD, Fang DC. Clinical implication of dinucleotide repeat sequence instability at D17S261 and D17S799 in gastric cancer. Huaren Xiaohua Zazhi. 1998;6:318-320.  [PubMed]  [DOI]  [Cited in This Article: ]
18.  Zhang QX, Dou YL, Shi XY, Ding Y. Expression of somatostatin mRNA in various differentiated types of gastric carcinoma. World J Gastroenterol. 1998;4:48-51.  [PubMed]  [DOI]  [Cited in This Article: ]
19.  Lu HD, Wang ZQ, Pan YR, Zhou TS, Xu XZ, Ke TW. Comparison of serum Zn, Cu and Se contents between healthy people and patients in high,middle and low incidence areas of gastric cancer of Fujian Province. World J Gastroenterol. 1999;5:84-86.  [PubMed]  [DOI]  [Cited in This Article: ]
20.  Cao GH, Yan SM, Yuan ZK, Wu L, Liu YF. A study of the relationship between trace element Mo and gastric cancer. World J Gastroenterol. 1998;4:55-56.  [PubMed]  [DOI]  [Cited in This Article: ]
21.  Yu W, Whang I, Suh I, Averbach A, Chang D, Sugarbaker PH. Prospective randomized trial of early postoperative intraperitoneal chemotherapy as an adjuvant to resectable gastric cancer. Ann Surg. 1998;228:347-354.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 135]  [Cited by in F6Publishing: 144]  [Article Influence: 5.5]  [Reference Citation Analysis (0)]
22.  Tsujitani S, Oka S, Saito H, Kondo A, Ikeguchi M, Maeta M, Kaibara N. Less invasive surgery for early gastric cancer based on the low probability of lymph node metastasis. Surgery. 1999;125:148-154.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 112]  [Cited by in F6Publishing: 116]  [Article Influence: 4.6]  [Reference Citation Analysis (0)]
23.  Ohgami M, Otani Y, Kumai K, Kubota T, Kim YI, Kitajima M. Curative laparoscopic surgery for early gastric cancer: five years experience. World J Surg. 1999;23:187-192; discussion 192-193.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 187]  [Cited by in F6Publishing: 193]  [Article Influence: 7.7]  [Reference Citation Analysis (0)]
24.  Ohwada S, Nakamura S, Ogawa T, Izumi M, Tanahashi Y, Sato Y, Ikeya T, Iino Y, Morishita Y. Segmental gastrectomy for early cancer in the mid-stomach. Hepatogastroenterology. 1999;46:1229-1233.  [PubMed]  [DOI]  [Cited in This Article: ]
25.  Tomita R, Takizawa H, Tanjoh K. Physiologic effects of cisapride on gastric emptying after pylorus-preserving gastrectomy for early gastric cancer. World J Surg. 1998;22:35-40; discussion 40-41.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 26]  [Cited by in F6Publishing: 28]  [Article Influence: 1.1]  [Reference Citation Analysis (0)]
26.  Isozaki H, Okajima K, Momura E, Ichinona T, Fujii K, Izumi N, Takeda Y. Postoperative evaluation of pylorus-preserving gastrectomy for early gastric cancer. Br J Surg. 1996;83:266-269.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 54]  [Cited by in F6Publishing: 54]  [Article Influence: 1.9]  [Reference Citation Analysis (1)]
27.  Endo M, Habu H. Clinical studies of early gastric cancer. Hepatogastroenterology. 1990;37:408-410.  [PubMed]  [DOI]  [Cited in This Article: ]
28.  Itoh H, Oohata Y, Nakamura K, Nagata T, Mibu R, Nakayama F. Complete ten-year postgastrectomy follow-up of early gastric cancer. Am J Surg. 1989;158:14-16.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 157]  [Cited by in F6Publishing: 164]  [Article Influence: 4.7]  [Reference Citation Analysis (0)]
29.  Sano T, Sasako M, Kinoshita T, Maruyama K. Recurrence of early gastric cancer. Follow-up of 1475 patients and review of the Japanese literature. Cancer. 1993;72:3174-3178.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 1]  [Reference Citation Analysis (0)]
30.  Hioki K, Nakane Y, Yamamoto M. Surgical strategy for early gastric cancer. Br J Surg. 1990;77:1330-1334.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 68]  [Cited by in F6Publishing: 70]  [Article Influence: 2.1]  [Reference Citation Analysis (0)]
31.  de Almeida JC, Bettencourt A, Costa CS, de Almeida JM. Curative surgery for gastric cancer: study of 166 consecutive patients. World J Surg. 1994;18:889-894; discussion 894-895.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 11]  [Cited by in F6Publishing: 11]  [Article Influence: 0.4]  [Reference Citation Analysis (0)]
32.  Takeshita K, Tani M, Inoue H, Saeki I, Hayashi S, Honda T, Kando F, Saito N, Endo M. Endoscopic treatment of early oesophageal or gastric cancer. Gut. 1997;40:123-127.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 137]  [Cited by in F6Publishing: 143]  [Article Influence: 5.3]  [Reference Citation Analysis (0)]
33.  Hayes N, Karat D, Scott DJ, Raimes SA, Griffin SM. Radical lymphadenectomy in the management of early gastric cancer. Br J Surg. 1996;83:1421-1423.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 26]  [Cited by in F6Publishing: 32]  [Article Influence: 1.1]  [Reference Citation Analysis (0)]
34.  Sowa M, Kato Y, Nishimura M, Kubo T, Maekawa H, Umeyama K. Surgical approach to early gastric cancer with lymph node metastasis.. World J Surg. 1989;13:630-635; discussion 630-635.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 39]  [Cited by in F6Publishing: 45]  [Article Influence: 1.3]  [Reference Citation Analysis (0)]
35.  Seto Y, Nagawa H, Muto Y, Kaizaki S, Kitayama J, Muto T. Preliminary report on local resection with lymphadenectomy for early gastric cancer. Br J Surg. 1999;86:526-528.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 30]  [Cited by in F6Publishing: 31]  [Article Influence: 1.2]  [Reference Citation Analysis (0)]
36.  Jentschura D, Heubner C, Manegold BC, Rumstadt B, Winkler M, Trede M. Surgery for early gastric cancer: a European one-center experience. World J Surg. 1997;21:845-848; discussion 849.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 27]  [Cited by in F6Publishing: 31]  [Article Influence: 1.1]  [Reference Citation Analysis (0)]
37.  Guadagni S, Catarci M, Kinoshitá T, Valenti M, De Bernardinis G, Carboni M. Causes of death and recurrence after surgery for early gastric cancer. World J Surg. 1997;21:434-439.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 36]  [Cited by in F6Publishing: 41]  [Article Influence: 1.5]  [Reference Citation Analysis (0)]
38.  Blot WJ, Devesa SS, Kneller RW, Fraumeni JF. Rising incidence of adenocarcinoma of the esophagus and gastric cardia. JAMA. 1991;265:1287-1289.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 1287]  [Cited by in F6Publishing: 1132]  [Article Influence: 34.3]  [Reference Citation Analysis (0)]
39.  Salvon-Harman JC, Cady B, Nikulasson S, Khettry U, Stone MD, Lavin P. Shifting proportions of gastric adenocarcinomas. Arch Surg. 1994;129:381-388; discussion 381-388;.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 64]  [Cited by in F6Publishing: 66]  [Article Influence: 2.2]  [Reference Citation Analysis (0)]
40.  de Manzoni G, Verlato G, Guglielmi A, Laterza E, Genna M, Cordiano C. Prognostic significance of lymph node dissection in gastric cancer. Br J Surg. 1996;83:1604-1607.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 91]  [Cited by in F6Publishing: 97]  [Article Influence: 3.5]  [Reference Citation Analysis (0)]
41.  Fujii K, Isozaki H, Okajima K, Nomura E, Niki M, Sako S, Izumi N, Mabuchi H, Nishiguchi K, Tanigawa N. Clinical evaluation of lymph node metastasis in gastric cancer defined by the fifth edition of the TNM classification in comparison with the Japanese system. Br J Surg. 1999;86:685-689.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 52]  [Cited by in F6Publishing: 52]  [Article Influence: 2.1]  [Reference Citation Analysis (0)]
42.  Yoo CH, Noh SH, Shin DW, Choi SH, Min JS. Recurrence following curative resection for gastric carcinoma. Br J Surg. 2000;87:236-242.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 523]  [Cited by in F6Publishing: 531]  [Article Influence: 22.1]  [Reference Citation Analysis (0)]
43.  Tong ZM. Relationship between lymph node metastasis and post-operative survival in gastric cancer. Huaren Xiaohua Zazhi. 1998;6:224-226.  [PubMed]  [DOI]  [Cited in This Article: ]
44.  Maeta M, Yamashiro H, Saito H, Katano K, Kondo A, Tsujitani S, Ikeguchi M, Kaibara N. A prospective pilot study of extended (D3) and superextended para-aortic lymphadenectomy (D4) in patients with T3 or T4 gastric cancer managed by total gastrectomy. Surgery. 1999;125:325-331.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 52]  [Cited by in F6Publishing: 51]  [Article Influence: 2.0]  [Reference Citation Analysis (0)]
45.  Doglietto GB, Pacelli F, Caprino P, Sgadari A, Crucitti F. Surgery: independent prognostic factor in curable and far advanced gastric cancer. World J Surg. 2000;24:459-463; discussion 464.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 31]  [Cited by in F6Publishing: 34]  [Article Influence: 1.4]  [Reference Citation Analysis (0)]
46.  Isozaki H, Okajima K, Fujii K, Nomura E, Izumi N, Mabuchi H, Nakamura M, Hara H. Effectiveness of paraaortic lymph node dissection for advanced gastric cancer. Hepatogastroenterology. 1999;46:549-554.  [PubMed]  [DOI]  [Cited in This Article: ]
47.  Siewert JR, Kestlmeier R, Busch R, Böttcher K, Roder JD, Müller J, Fellbaum C, Höfler H. Benefits of D2 lymph node dissection for patients with gastric cancer and pN0 and pN1 lymph node metastases. Br J Surg. 1996;83:1144-1147.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 182]  [Cited by in F6Publishing: 195]  [Article Influence: 7.0]  [Reference Citation Analysis (0)]