• Users Online: 228
  • Print this page
  • Email this page


 
 Table of Contents  
ORIGINAL ARTICLE
Year : 2021  |  Volume : 33  |  Issue : 3  |  Page : 288-293

Evaluating the benefit of adjuvant radiotherapy after extensive lymph node dissection for gastric cancer: a single-institute retrospective study


1 Department of Radiation Oncology, Taipei Tzu Chi Hospital, Buddhist Tzu Chi Medical Foundation, New Taipei, Taiwan
2 Department of Hematology/Oncology, Taipei Tzu Chi Hospital, Buddhist Tzu Chi Medical Foundation, New Taipei, Taiwan
3 Department of Radiation Oncology, Taipei Tzu Chi Hospital, Buddhist Tzu Chi Medical Foundation, New Taipei; Department of Radiology, School of Medicine, Tzu Chi University, Hualien, Taiwan
4 Department of Hematology/Oncology, Taipei Tzu Chi Hospital, Buddhist Tzu Chi Medical Foundation, New Taipei; Department of Oncology, School of Medicine, Tzu Chi University, Hualien, Taiwan
5 Department of Research, Taipei Tzu Chi Hospital, Buddhist Tzu Chi Medical Foundation, New Taipei, Taiwan
6 Department of General Surgery, Taipei Tzu Chi Hospital, Buddhist Tzu Chi Medical Foundation, New Taipei; Department of Surgery, School of Medicine, Tzu Chi University, Hualien, Taiwan

Date of Submission03-Sep-2020
Date of Decision06-Oct-2020
Date of Acceptance03-Nov-2020
Date of Web Publication22-Feb-2021

Correspondence Address:
Chao-Chuan Wu
Department of General Surgery, Taipei Tzu Chi Hospital, Buddhist Tzu Chi Medical Foundation, 289, Jianguo Road, Xindian District, New Taipei
Taiwan
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/tcmj.tcmj_230_20

Rights and Permissions
  Abstract 


Objective: This study aimed to evaluate whether adjuvant radiotherapy (RT) can improve the treatment outcome of patients with locally advanced gastric cancer who underwent extensive lymph node dissection (ELND). Materials and Methods: This retrospective study included patients with gastric cancer pathological stages IIA–IIIC at Taipei Tzu Chi Hospital between 2008 and 2015. Patients (a) aged >80 years, (b) with distant metastasis at diagnosis, (c) with coexisting malignancies, (d) who did not complete the prescribed RT course, and (e) who died 1 month after surgery were excluded. Among 420 patients diagnosed with gastric cancer, 98 were included. Results: The median follow-up was 24.5 months. Of 39 patients who underwent adjuvant RT, 38 also received adjuvant chemotherapy (CT). Of 59 patients who did not receive adjuvant RT, only 34 received adjuvant CT. ELND was performed in 67.3% of the patients. The 5-year overall survival (OS) rate was 40%. In the univariate analyses, adjuvant CT regimen, 5-fluorouracil + leucovorin, was associated with worst outcome, while TS-1 was associated with better survival outcome (P = 0.018). The number of involved lymph nodes was strongly related to the OS and disease-free survival (DFS) (P < 0.001). We tried using different numbers of involved lymph nodes as a cutoff point and found that adjuvant RT significantly improved both OS and DFS in patients whose involved lymph nodes were ≥4 (OS, P = 0.017; DFS, P = 0.015). In multivariate analyses, better DFS was associated with negative surgical margin (P = 0.04), earlier disease stage (P = 0.001), adjuvant radiotherapy (P = 0.045), and adjuvant CT regimen TS-1 (P = 0.001). Conclusion: Adjuvant RT could improve DFS of patients with locally advanced gastric cancer with or without ELND. When the number of involved lymph nodes is ≥4, adjuvant RT is strongly suggested.

Keywords: Adjuvant, Chemotherapy, Dissection, Gastric cancer, Radiotherapy


How to cite this article:
Wang YN, Chang SY, Hwang JM, Chang YK, Kao WY, Wan HL, Tzeng IS, Wu CC. Evaluating the benefit of adjuvant radiotherapy after extensive lymph node dissection for gastric cancer: a single-institute retrospective study. Tzu Chi Med J 2021;33:288-93

How to cite this URL:
Wang YN, Chang SY, Hwang JM, Chang YK, Kao WY, Wan HL, Tzeng IS, Wu CC. Evaluating the benefit of adjuvant radiotherapy after extensive lymph node dissection for gastric cancer: a single-institute retrospective study. Tzu Chi Med J [serial online] 2021 [cited 2021 Aug 2];33:288-93. Available from: https://www.tcmjmed.com/text.asp?2021/33/3/288/309933




  Introduction Top


The standard treatment for locally advanced gastric cancer differs between Western countries and Asian countries. Perioperative chemotherapy (CT)[1] or postoperative chemoradiation (CRT)[2] are recommended for resectable gastric cancer in Europe and North America, while postoperative CT is the standard treatment according to the Adjuvant Chemotherapy Trial of TS-1 for Gastric Cancer[3] and adjuvant capecitabine plus oxaliplatin for gastric cancer after D2 gastrectomy (CLASSIC)[4] trials in Asian countries. The different attitudes toward adding radiotherapy (RT) to the adjuvant treatment are partly related to the extent of lymph node dissection. The INT-0116 study[2], which was conducted in the US, was criticized mainly because only 10% of patients received D2 dissections, while in Asian published studies, D2 dissection remained the mainstream surgical treatment for gastric cancer. Although the added value of postoperative chemoradiotherapy after a D2 dissection has been established in various studies[5],[6], it remains unclear whether adjuvant CT or CRT is the best form of adjuvant therapy.

To answer the question, in 2012, the Adjuvant Chemoradiation Therapy in Stomach Cancer (ARTIST) trial[7] reported that the addition of RT to adjuvant CT did not significantly reduce recurrence after D2 dissection. However, in the large subgroup of node-positive patients (86.5%), postoperative chemoradiotherapy improved patients' outcome[8]. By contrast, the CT versus chemoradiotherapy after surgery and preoperative chemotherapy for resectable gastric cancer (CRITICS) study claimed that postoperative chemoradiotherapy did not provide better survival outcomes compared with postoperative CT[9], which adjuvant treatment modality is optimal after D2 dissection remains inconclusive. This study aimed to review the treatment details and outcomes of patients with locally advanced gastric cancer at Taipei Tzu Chi Hospital, Taiwan.


  Materials and methods Top


Patients

In this retrospective study, we included patients with pathologically confirmed gastric adenocarcinoma who underwent curative surgical resection at Taipei Tzu Chi Hospital from January 2008 to September 2015. Tumor staging was performed according to the AJCC/UICC TNM staging manual, 7th edition, and lesions staged as IIA–IIIC were included.

Patients (a) aged >80 years, (b) with distant metastasis at diagnosis, (c) with coexisting malignancies, (d) who did not complete the prescribed RT course, and (e) who died 1 month after surgery were excluded.

In the period of our study, 420 patients were diagnosed with gastric cancer at our hospital and 98 were selected for analysis based on the abovementioned criteria.

Treatment regimen

Surgery

Patients who had curative and en bloc tumor resection were eligible for inclusion of our study. Due to the heterogeneity of the operative records, the exact lymphadenectomy D level cannot be specified. The median number of nodes examined after performing D2 lymphadenectomies at the National Cancer Center Hospital in Tokyo, Japan, and at Seoul National University Hospital in South Korea was >25–30[10]. In a series of 367 patients with recurrent gastric adenocarcinoma from the Memorial Sloan Kettering Cancer Center, 81% of the patients had a D2 or more extensive lymphadenectomy and the median number of lymph nodes removed was 22[11]. As an alternative to D2 dissection, extensive lymph node dissection (ELND) was defined as dissection of ≥25 nodes or more in our study.

Chemotherapy

Thirty-one patients in our study did not receive any CT. Meanwhile, 29 patients received high-dose fluorouracil and leucovorin-based CT[12] alone (n = 7) or combined with oxaliplatin (n = 13), carboplatin (n = 2), or cisplatin (n = 7). Oral TS-1 (tegafur + gimeracil + oteracil), 2 caps, PO, BID, was administered in 17 patients, while oral UFT (tegafur 100 mg and uracil 224 mg) 1 cap, PO, TID, was administered in 14 patients.

Radiotherapy

The timing for adjuvant RT ranged from 2 to 6 weeks after the surgery. We used computerized tomography simulation and conformal treatment planning such as intensity-modulated radiation therapy (IMRT) or intensity-modulated arc therapy to deliver a lower dose of radiation to the organs at risk (e.g., heart, lungs, liver, kidneys, and small bowel). Patients were instructed to avoid taking heavy meal 3 h before simulation and treatment. They were treated in the supine position. Uncertainties from variations in stomach filling and respiratory motion were also considered. The clinical target volume (CTV) was individualized based on the extent and location of the primary tumor and involved lymph nodes and the type of surgery performed. The lymphatic drainage areas in the radiation fields included perigastric, celiac, splenic hilar, suprapancreatic, porta hepatis, pancreaticoduodenal, and local para-aortic nodes. In patients with tumors located at the gastroesophageal junction, paracardial and paraesophageal lymph nodes were included in the radiation fields, while pancreaticoduodenal region was not irradiated. The planning target volume consisted of the CTV with a 1-cm margin. The 45 Gy of radiation was delivered in 25 fractions, 5 days per week, to the tumor bed, regional nodes, and 2 cm beyond the proximal and distal margins of resection.

Statistical methods

Overall survival (OS) was recorded from the date of radical surgery until death of any cause or last contact with the patient or any family member. Disease-free survival (DFS) was measured from the date of radical surgery to the date of the first disease recurrence. Locoregional recurrence was defined as recurrence at the anastomosis site, duodenal stump, tumor bed, remnant stomach, or regional lymph nodes within the RT field. Distant metastasis was defined as lymph node recurrence outside of the RT field, peritoneal seeding, liver metastasis, or metastasis to other extra-abdominal sites.

The Chi-square test and Student's t-test were used to compare the characteristics between with adjuvant RT group and without adjuvant RT group. The Kaplan–Meier method was used to estimate survival, while the log-rank test was used to determine significance. A Cox proportional-hazards model was used to estimate the prognostic factors for survival. SPSS software for Windows version 24.0 (SPSS, Chicago, IL, USA) was used for statistical analysis. Statistical significance was assumed when the P value fell below 0.05.

Ethical approval

This study has been approved by the Taipei Tzu Chi Hospital, Buddhist Tzu Chi Medical Foundation Institutional Review Board on Nov., 17, 2016 (IRB No. 05-X27-090). The constitution and operation of this review board are according to the guidelines of ICH-GCP. The informed patient consent was waived by the IRB.


  Results Top


Patients' characteristics

Patients' characteristics are shown in [Table 1]. Among the 98 patients in the study, 66 were men and their median age was 64 years (range: 28–80). Meanwhile, 66 patients underwent ELND. The median number of dissected nodes was 31 (range: 3–90). Seventy patients had regional nodal involvement and 9 had close or involved margins. Sixty-seven patients underwent adjuvant CT and 39 had adjuvant RT.
Table 1: Patients' characteristics

Click here to view


Patients who received adjuvant RT and those who did not receive adjuvant RT were compared. Of 39 patients who underwent adjuvant RT, only 38 received adjuvant CT. Of 59 patients who did not receive adjuvant RT, only 34 received adjuvant CT.

Those who underwent RT were significantly younger (55.62 vs. 67.46 years, P < 0.001), with more involved lymph nodes (11.28 vs. 3.95, P < 0.001), and with more advanced disease (P = 0.003). The CT regimen in the RT group was mostly 5-fluorouracil (5-FU) + leucovorin (26 of 39), while more than half of the group without RT did not receive CT (30 of 59).

Survival and relapse

The median follow-up was 24.5 months (range: 3–106 months). A total of 51 patients died; of them, 38 died due to disease recurrence (local, 8; regional, 11; and distant, 19), while 13 died due to other causes. Overall, the 5-year survival rate was 40% and the median OS was 44.7 months. The 5-year DFS rate was 40% and the median DFS was 39.1 months.

The prognostic factor for both OS and DFS identified in the univariate analysis is adjuvant CT [Table 2]. The regimen 5-FU + leucovorin was associated with worst outcome, while TS-1 was associated with better survival outcome. Whether patients had ELND or adjuvant RT did not show a significant difference.
Table 2: Univariate analysis

Click here to view


As shown in [Table 3], in the multivariate analysis, better OS was associated with earlier disease stage (P = 0.003), adjuvant RT (P = 0.058), and adjuvant CT regimen TS-1 (P = 0.001). Better DFS was associated with negative surgical margin (P = 0.04), earlier disease stage (P = 0.001), adjuvant RT (P = 0.045), and adjuvant CT regimen TS-1 (P = 0.001) or UFT (P = 0.034).
Table 3: Prognostic factors based on multivariate analyses (n=98)

Click here to view


To determine whether adjuvant CT or RT is indicated after ELND, we performed a multivariate analysis in this group of patients [Table 4]. Negative surgical margin (P = 0.013), earlier disease stage (P = 0.002), adjuvant RT (P = 0.009), and adjuvant CT regimen TS-1 (P < 0.001) or UFT (P = 0.04) were associated with better OS. Better DFS was associated with negative surgical margin (P = 0.004), earlier disease stage (P = 0.001), adjuvant RT (P = 0.008), and adjuvant CT regimen TS-1 (P < 0.001).
Table 4: Prognostic factors based on multivariate analyses in patients who underwent extensive lymph node dissection (n=66)

Click here to view


We also observed that the number of involved lymph nodes was strongly related to the OS and DFS (P < 0.001). However, as there was considerable overlap between this factor and disease stage, we did not use it in the multivariate analyses. We tried using different numbers of involved lymph nodes as a cutoff point and found that adjuvant RT significantly improved both OS and DFS in patients whose number of involved lymph nodes were ≥4 (univariate analysis: OS, P = 0.017; DFS, P = 0.015). The process and results are presented in [Table 5].
Table 5: The effect of radiotherapy on different groups of patients with regional lymph nodes involved

Click here to view



  Discussion Top


In the present retrospective study, patients who underwent adjuvant CT or RT were significantly younger, with more lymph nodes dissected, and with more advanced disease. Simply put, the more advanced disease was treated more aggressively. Such an uneven distribution might explain why some treatment-related factors did not show statistical significance in the univariate analysis. However, it is noteworthy that oral TS-1 provided significantly better outcome even in such an uneven distribution. TS-1 is usually prescribed for locally advanced gastric cancer patients who have undergone a D2 dissection in Japan. Sakuramoto et al. demonstrated its survival benefit as an adjuvant treatment versus surgery alone[3]. In a systematic review, four studies supported that S-1 regimens slightly improve the OS (by less than an additional month) versus 5-FU-containing regimens[13].

Our multivariate analysis showed that adjuvant RT significantly improved DFS and TS-1 significantly improved both OS and DFS [Table 3]. Some previous randomized controlled trials (RCTs) showed similar outcomes favoring adjuvant RT. In INT-0116, surgery alone had significantly worse OS (HR = 1.35, P = 0.005) and higher recurrence rate (HR = 1.52, P < 0.001) than surgery followed by CRT. The role of adjuvant CRT after D2 dissection has also been established by several studies. A Korean retrospective study showed that the addition of adjuvant CRT was superior to surgery alone (95.3 months vs. 62.6 months, P = 0.02)[5]. Jácome et al. also published a study showing that adjuvant CRT was associated with a lower risk of death in gastric cancer patients treated with D2 dissection[6]. With regard to the debates on adjuvant CT or CRT, Zhu et al.[14] compared adjuvant CRT with CT. The CRT arm showed better 5-year RFS (45.2% vs. 35.8%, P = 0.029) and OS (48.4% vs. 41.8%, P = 0.122), although the benefit on OS was not statistically significant.

On the contrary, the results of the ARTIST trial did not encourage the use of adjuvant RT. The 5-year OS of adjuvant CRT was similar to that of adjuvant CT alone (75% vs. 73%, P = 0.484). The advantage of adding RT has been shown to provide better 3-year DFS (78.2% vs. 74.2%, P = 0.0862) but diminished its association with 7-year DFS (P = 0.74). Another Korean RCT reported that adjuvant CRT was not significantly better than adjuvant CT (5-year RFS: 45.2% vs. 35.8%, P = 0.029; 5-year OS: 48.4% vs. 41.8%, P = 0.122)[15].

However, in the following subgroup analysis[8] of node-positive patients in the ARTIST trial, postoperative chemoradiotherapy significantly lowered regional recurrence (23 in the CT arm; 5 in the CRT arm; P < 0.001).

It is noteworthy that the RT technique used in the two Korean RCTs mentioned above was traditional AP-PA fields. Boda-Heggemann et al.[16] conducted a cohort study consisting of 27 patients treated with 3D-CRT with 5-FU and leucovorin and 33 patients treated with IMRT and capecitabine plus oxaliplatin. Patients in the IMRT group had a 30% absolute improvement in 2-year OS (67% vs. 37%; P = 0.0492). It was possible that advanced RT could provide more benefits with more accurate radiation delivery and less adverse effects.

As a surrogate of D2 dissection, extensive LN dissection did not show a superior survival benefit in our multivariate analysis. This result indicates that the number of dissected LNs alone is probably not of significant importance. The nodal stations at risks need to be dissected thoroughly to achieve better locoregional control. The Dutch[17] and MRC[18] trials showed that D2 dissection was associated with increased postoperative mortality and morbidity and the survival outcome was not superior to D1 dissection. It is noteworthy that surgical morbidity and mortality rates for gastric adenocarcinoma are generally much higher in the United States than that in South Korea and Japan[10].

Nodal status is an important prognostic factor. Previous studies have proposed N-ratio, the ratio between metastatic and dissected lymph nodes, and the results showed that it is an independent prognostic factor for OS and DFS[19],[20]. In the present study, we did not use the number of involved lymph nodes for multivariate analysis because it has already been included in the AJCC stage. To determine the patients who would benefit the most from adjuvant RT, we tried using different numbers of involved lymph nodes as a cutoff point. The univariate analysis result showed that in patients whose involved LNs were greater or equal to four, adjuvant RT significantly improved both OS (median: 46.8 vs. 14.27 months, P = 0.017) and DFS (median: 51.8 vs. 8.37 months, P = 0.015).

The major limitation of our retrospective study is the use of various treatment modalities with uneven patient distribution. Patients who underwent adjuvant CT or RT were significantly younger, with more lymph nodes dissected, and with more advanced diseases. Besides, due to the heterogeneity of the operative records, we used extensive LN dissection as the surrogate of D2 dissection and failed to show its locoregional control benefit.


  Conclusion Top


Our study indicates that adjuvant RT significantly improved DFS after gastrectomy with or without extensive LN dissection. When the number of involved LNs was ≥4, adjuvant RT is strongly suggested for better locoregional control.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Cunningham D, Allum WH, Stenning SP, Thompson JN, Van de Velde CJ, Nicolson M, et al. Perioperative chemotherapy versus surgery alone for resectable gastroesophageal cancer. N Engl J Med 2006;355:11-20.  Back to cited text no. 1
    
2.
Macdonald JS, Smalley SR, Benedetti J, Hundahl SA, Estes NC, Stemmermann GN, et al. Chemoradiotherapy after surgery compared with surgery alone for adenocarcinoma of the stomach or gastroesophageal junction. N Engl J Med 2001;345:725-30.  Back to cited text no. 2
    
3.
Sakuramoto S, Sasako M, Yamaguchi T, Kinoshita T, Fujii M, Nashimoto A, et al. Adjuvant chemotherapy for gastric cancer with S-1, an oral fluoropyrimidine. N Engl J Med 2007;357:1810-20.  Back to cited text no. 3
    
4.
Bang YJ, Kim YW, Yang HK, Chung HC, Park YK, Lee KH, et al. Adjuvant capecitabine and oxaliplatin for gastric cancer after D2 gastrectomy (CLASSIC): A phase 3 open-label, randomised controlled trial. Lancet 2012;379:315-21.  Back to cited text no. 4
    
5.
Kim S, Lim DH, Lee J, Kang WK, MacDonald JS, Park CH, et al. An observational study suggesting clinical benefit for adjuvant postoperative chemoradiation in a population of over 500 cases after gastric resection with D2 nodal dissection for adenocarcinoma of the stomach. Int J Radiat Oncol Biol Phys 2005;63:1279-85.  Back to cited text no. 5
    
6.
Jácome AA, Wohnrath DR, Scapulatempo Neto C, Fregnani JH, Quinto AL, Oliveira AT, et al. Effect of adjuvant chemoradiotherapy on overall survival of gastric cancer patients submitted to D2 lymphadenectomy. Gastric Cancer 2013;16:233-8.  Back to cited text no. 6
    
7.
Lee J, Lim DH, Kim S, Park SH, Park JO, Park YS, et al. Phase III trial comparing capecitabine plus cisplatin versus capecitabine plus cisplatin with concurrent capecitabine radiotherapy in completely resected gastric cancer with D2 lymph node dissection: The ARTIST trial. J Clin Oncol 2012;30:268-73.  Back to cited text no. 7
    
8.
Yu JI, Lim DH, Ahn YC, Lee J, Kang WK, Park SH, et al. Effects of adjuvant radiotherapy on completely resected gastric cancer: A radiation oncologist's view of the ARTIST randomized phase III trial. Radiother Oncol 2015;117:171-7.  Back to cited text no. 8
    
9.
Cats A, Jansen EP, van Grieken NC, Sikorska K, Lind P, Nordsmark M, et al. Chemotherapy versus chemoradiotherapy after surgery and preoperative chemotherapy for resectable gastric cancer (CRITICS): An international, open-label, randomised phase 3 trial. Lancet Oncol 2018;19:616-28.  Back to cited text no. 9
    
10.
Schmidt B, Yoon SS. D1 versus D2 lymphadenectomy for gastric cancer. J Surg Oncol 2013;107:259-64.  Back to cited text no. 10
    
11.
D'Angelica M, Gonen M, Brennan MF, Turnbull AD, Bains M, Karpeh MS. Patterns of initial recurrence in completely resected gastric adenocarcinoma. Ann Surg 2004;240:808-16.  Back to cited text no. 11
    
12.
Ardalan B, Chua L, Tian EM, Reddy R, Sridhar K, Benedetto P, et al. A phase II study of weekly 24-hour infusion with high-dose fluorouracil with leucovorin in colorectal carcinoma. J Clin Oncol 1991;9:625-30.  Back to cited text no. 12
    
13.
Wagner AD, Syn NL, Moehler M, Grothe W, Yong WP, Tai BC, et al. Chemotherapy for advanced gastric cancer. Cochrane Database Syst Rev 2017;8:CD004064.  Back to cited text no. 13
    
14.
Zhu WG, Xua DF, Pu J, Zong CD, Li T, Tao GZ, et al. A randomized, controlled, multicenter study comparing intensity-modulated radiotherapy plus concurrent chemotherapy with chemotherapy alone in gastric cancer patients with D2 resection. Radiother Oncol 2012;104:361-6.  Back to cited text no. 14
    
15.
Kim TH, Park SR, Ryu KW, Kim YW, Bae JM, Lee JH, et al. Phase 3 trial of postoperative chemotherapy alone versus chemoradiation therapy in stage III-IV gastric cancer treated with R0 gastrectomy and D2 lymph node dissection. Int J Radiat Oncol Biol Phys 2012;84:e585-92.  Back to cited text no. 15
    
16.
Boda-Heggemann J, Hofheinz RD, Weiss C, Mennemeyer P, Mai SK, Hermes P, et al. Combined adjuvant radiochemotherapy with IMRT/XELOX improves outcome with low renal toxicity in gastric cancer. Int J Radiat Oncol Biol Phys 2009;75:1187-95.  Back to cited text no. 16
    
17.
Songun I, Putter H, Kranenbarg EM, Sasako M, van de Velde CJ. Surgical treatment of gastric cancer: 15-year follow-up results of the randomised nationwide Dutch D1D2 trial. Lancet Oncol 2010;11:439-49.  Back to cited text no. 17
    
18.
Cuschieri A, Weeden S, Fielding J, Bancewicz J, Craven J, Joypaul V, et al. Patient survival after D1 and D2 resections for gastric cancer: Long-term results of the MRC randomized surgical trial. Surgical Co-operative Group. Br J Cancer 1999;79:1522-30.  Back to cited text no. 18
    
19.
Marchet A, Mocellin S, Ambrosi A, Morgagni P, Garcea D, Marrelli D, et al. The ratio between metastatic and examined lymph nodes (N ratio) is an independent prognostic factor in gastric cancer regardless of the type of lymphadenectomy: Results from an Italian multicentric study in 1853 patients. Ann Surg 2007;245:543-52.  Back to cited text no. 19
    
20.
Coimbra FJ, Costa WL Jr., Montagnini AL, Diniz AL, Ribeiro HS, Silva MJ, et al. The interaction between N-category and N-ratio as a new tool to improve lymph node metastasis staging in gastric cancer: Results of a single cancer center in Brazil. Eur J Surg Oncol 2011;37:47-54.  Back to cited text no. 20
    



 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]



 

Top
 
 
  Search
 
Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
Access Statistics
Email Alert *
Add to My List *
* Registration required (free)

 
  In this article
Abstract
Introduction
Materials and me...
Results
Discussion
Conclusion
References
Article Tables

 Article Access Statistics
    Viewed554    
    Printed12    
    Emailed0    
    PDF Downloaded33    
    Comments [Add]    

Recommend this journal


[TAG2]
[TAG3]
[TAG4]