Home About us Editorial board Ahead of print Current issue Search Archives Submit article Instructions Subscribe Contacts Login 


 
 Table of Contents  
ORIGINAL ARTICLE
Year : 2018  |  Volume : 14  |  Issue : 9  |  Page : 288-294

The total number of lymph nodes harvested from pathological T3N0 rectal cancer patients: Prognostic significance and potential indication for postoperative radiotherapy


1 Department of Radiation Oncology, Sun Yat-Sen University Cancer Center, State Key Laboratory of Oncology in South China; State Key Laboratory of Oncology in South China, Collaborative Innovation Center of Cancer Medicine, Guangzhou, Guangdong 510060, China
2 Department of Oncology, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou, Guangdong 510060, China
3 State Key Laboratory of Oncology in South China, Collaborative Innovation Center of Cancer Medicine; Department of Colorectal Cancer, Sun Yat-Sen University Cancer Center, State Key Laboratory of Oncology in South China, Guangzhou, Guangdong 510060, China

Date of Web Publication29-Jun-2018

Correspondence Address:
Yuan-Hong Gao
651, East Dongfeng Road, Guangzhou, Guangdong 510060
China
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0973-1482.235343

Rights and Permissions
 > Abstract 

Background: Lymph node status is important in staging colorectal cancer. The use of combination treatment for pathological T3N0 (pT3N0) rectal cancer patients has been controversial. We aimed to explore the prognostic significance of the total number of lymph nodes harvested from pT3N0 rectal cancer patients.
Methods: Between June 2004 and November 2011, 289 pT3N0 rectal cancer patients who received total mesorectal excision (TME) with or without postoperative chemotherapy were retrospectively reviewed. The main independent variable was the total number of harvested lymph nodes, and the endpoints included local recurrence-free survival (LRFS), disease-free survival (DFS), and overall survival (OS).
Results: The patients had a median of 13 lymph nodes harvested. When compared with patients who had < 12 lymph nodes harvested, patients who had ≥12 lymph nodes harvested had higher 5-year LRFS (84.7% vs. 98.0%, P < 0.001), DFS (71.4% vs. 86.8%, P < 0.001), and OS (77.6% vs. 94.9%, P < 0.001) rates. Multivariate analysis demonstrated that the patients who had ≥12 lymph nodes harvested had a significantly lower risks of local relapse (hazard ratio [HR], 0.099; P < 0.001), treatment failure (HR: 0.291; P < 0.001), and death (HR: 0.231; P < 0.001) when compared with patients who had <12 lymph nodes harvested.
Conclusions: The number of lymph nodes harvested was independently associated with local relapse, treatment failure, and OS rates in pT3N0 rectal cancer patients who received initial TME with or without postoperative chemotherapy. Postoperative radiotherapy should not be omitted for pT3N0 rectal cancer patients who had <12 lymph nodes harvested.

Keywords: Prognostic significance, radiotherapy, rectal cancer, T3N0, total number of lymph nodes


How to cite this article:
Xiao WW, Zhang LN, You KY, Huang R, Yu X, Chang H, Ding PR, Gao YH. The total number of lymph nodes harvested from pathological T3N0 rectal cancer patients: Prognostic significance and potential indication for postoperative radiotherapy. J Can Res Ther 2018;14:288-94

How to cite this URL:
Xiao WW, Zhang LN, You KY, Huang R, Yu X, Chang H, Ding PR, Gao YH. The total number of lymph nodes harvested from pathological T3N0 rectal cancer patients: Prognostic significance and potential indication for postoperative radiotherapy. J Can Res Ther [serial online] 2018 [cited 2018 Jul 16];14:288-94. Available from: http://www.cancerjournal.net/text.asp?2018/14/9/288/235343


 > Introduction Top


Colorectal cancer is the third most common malignancy in China. In Guangzhou, one of the most developed areas of China, colorectal cancer has already become the second most frequently diagnosed cancer.

The treatment of rectal cancer has rapidly evolved during the last 15 years. The use of preoperative chemoradiotherapy for locally advanced disease has increased, which has markedly improved the quality of life and the survival of rectal cancer patients. However, the benefit of additional radiotherapy and chemotherapy on the survival of pathological T3N0 (pT3N0) rectal cancer patients remains controversial;[1],[2] the National Comprehensive Cancer Network (NCCN) guideline only recommends postoperative chemotherapy for pT3N0 rectal cancer patients who received upfront total mesorectal excision (TME), whereas the European Society of Medical Oncology consensus recommends postoperative radiotherapy for all pT3N0 rectal cancer patients. Identifying the risk factors for treatment failure is essential to optimize treatment for pT3N0 rectal cancer patients.

The total lymph node number (TLNN) harvested by surgery is one of the most widely studied pathological factors in malignant tumors. The prognostic significance of the TLNN is widely advocated in breast cancer,[3] gastric cancer,[4] and esophageal squamous cell carcinoma.[5] The TLNN is also a significant pathological feature of undefined colorectal cancer.[6],[7] However, whether the TLNN can be utilized as a criterion to select postoperative radiotherapy for pT3N0 patients remains unknown.

The purpose of this retrospective study was to explore the prognostic significance of the TLNN in pT3N0 rectal cancer patients by reviewing the archives of pT3N0 rectal cancer patients.


 > Methods Top


Patients and database

The data from rectal cancer patients who were treated with TME at the Sun Yat-sen University Cancer Center in Guangzhou between January 2004 and December 2011 were collected. Before 2005, the standardized neoadjuvant/adjuvant chemoradiotherapy for rectal cancer was not well-established in our hospital; some patients who received a diagnosis of locally advanced rectal cancer also received upfront TME. Meanwhile, the pathological stages of some stage I patients were upgraded to pT3N0 after TME, leading to the absence of preoperative chemotherapy or radiotherapy.

For the purpose of this study, the patient selection criteria were as follows: (1) Did not receive preoperative therapy or postoperative radiotherapy; (2) underwent TME surgery; (3) had pathologically confirmed T3N0 rectal adenocarcinoma according to the American Joint Committee on Cancer (AJCC) and International Union Against Cancer;[8] and (4) had no evidence of distant metastases at initial diagnosis.

After the medical and pathological records were carefully reviewed, data from a total of 296 pT3N0 rectal cancer patients were collected. Seven patients were excluded due to a lack of follow-up after treatment. A total of 289 patients with pT3N0 rectal cancer were included in the study.

The protocol complies with the declaration of Helsinki and with National Laws and was approved by the Protocol Review Board of the Institution. All patients provided written informed consent before participation.

Patient assessment and follow-up

All patients were asked to follow-up every 3 to 6 months after treatment in the first 3 years and every 6 to 12 months thereafter. A digital examination and serum carcinoembryonic antigen (CEA) tests were performed at each follow-up session. Radiologic exams and colonoscopies were performed every 6 to 12 months or when clinically indicated. In addition to their scheduled follow-up, all surviving patients received follow-up phone calls until July 2014.

Local recurrence-free survival (LRFS) was calculated from the time of diagnosis to the time of recurrence in the surgical bed or pelvis. Disease-free survival (DFS) was calculated from the time of diagnosis to the time of either local or distant tumor recurrence. Overall survival (OS) was calculated from the time of diagnosis to the time of death due to any reason or to the time of the last follow-up.

Statistical methods

Actuarial survival rates were calculated using the Kaplan–Meier method, and the log-rank test was used to compare variables in the univariate analysis. Multivariate analysis was performed with Cox regression, and hazard ratios (HRs) were calculated including the 95% confidence interval (CI) to determine independent risk factors. All statistical analyses were performed using the SPSS software package ( Version 19.0, SPSS Inc., Chicago, Illinois, USA). Two-sided P < 0.05 was considered as significant.


 > Results Top


Patient characteristics and outcomes

The clinicopathological characteristics of the patient population are shown in [Table 1]. The median age in our series was 62 years (range: 32–86 years). High rectal lesions, with tumors (distal edge) located 5 cm above the anus, were found in 214 (74%) of the 289 patients. A total of 201 patients (70%) underwent postoperative chemotherapy with the 5-fluorouracil (FU)-based regimens, according the chief physician's decision.
Table 1: Clinicopathologic characteristics and outcomes of the 289 patients with pT3N0 rectal cancer

Click here to view


Within a median follow-up time of 50.47 months (range: 0.5–106.37 months) for all patients, 32 patients (11%) had died (11 from local recurrence, 20 from distant failure, and 1 from respiratory disease). Local or distant recurrence was observed in 49 patients (17%), of whom 10 patients had local recurrence only, 30 had distant metastasis only, and 9 had synchronous local and distant recurrence. Of all 289 patients, the 5-year LRFS, DFS, and OS rates were 93.6%, 80.4%, and 87.9%, respectively.

Characteristics of dissected lymph nodes

The lymph node status was confirmed by a pathologist via microscopic examination to reconfirm the N status. The TLNN distribution is shown in [Figure 1]. The median TLNN was 13 (range: 0–34 lymph nodes dissected).
Figure 1: Histogram of the distribution of the total lymph node number of all 289 pathological T3N0 rectal cancer patients. The median total lymph node number was 13 (range: 0–34 lymph nodes dissected)

Click here to view


Prognostic significance of the total lymph node number for LRFS, disease-free survival, and overall survival

The prognostic significance of the TLNN and other clinicopathological variables was analyzed. The 5-year LRFS, DFS, and OS rates were compared for each variable in univariate analysis [Table 1]. Significantly lower 5-year LRFS, DFS, and OS rates were observed in patients with a TLNN <12 when compared with patients and a TLNN ≥ 12 [84.7% vs. 98.0%, P < 0.001; 71.4% vs. 86.8%, P < 0.001; 77.6% vs. 94.9%, P < 0.001, respectively; [Figure 2]. The 5-year LRFS and DFS rates were significantly lower in the elevated CEA group when compared with the normal CEA group (86.9% vs. 97.1%, P = 0.001; 74.2% vs. 84.8%, P = 0.007, respectively), whereas no significant difference was found for OS (85.4% vs. 90.0%, P = 0.707). Other significant prognostic factors revealed by univariate analysis included sex (DFS favoring female patients, P = 0.036), age (LRFS favoring patients < 62-year-old, P = 0.046), and tumor location (LRFS favoring high rectal lesions, P = 0.038), as shown in [Table 1].
Figure 2: Stratified analyses of all 289 pathological T3N0 rectal cancer patients using the total lymph node number (<12 vs. ≥12) to compare local recurrence-free survival (a), Disease-free survival (b), and overall survival (c)

Click here to view


Survival rates were further compared between subgroups according to the CEA level, tumor location and treatment regimen. As shown in [Table 2], in patients with normal CEA levels, satisfactory local control rates were achieved in both patients with a TLNN < 12 and patients with a TLNN ≥ 12, and DFS did not significantly differ between these groups; however, a significant difference between these groups was observed for OS [Figure 3] and [Table 2]. For patient with elevated CEA levels, a TLNN < 12 correlated with significantly lower LRFS, DFS, and OS rates [Figure 3] and [Table 2]. Survival analysis showed that the TLNN was significantly correlated with LRFS, DFS and OS in both low and high rectal cancer patients, but greater differences were noted between cancer patients with low rectal lesions with a TLNN < 12 and those with a TLNN ≥ 12 [Figure 4] and [Table 2]. The patients were also divided into two groups according to the treatment regimen (surgery alone vs. surgery + postoperative chemotherapy). In patients who received surgery alone, a TLNN ≥ 12 was a favorable prognostic factor for LRFS and DFS but not for OS [Figure 5] and [Table 2]. In the patients who received surgery with postoperative chemotherapy, those with a TLNN ≥ 12 had significant increased LRFS, DFS and OS rates compared with those of patients with a TLNN < 12 [Figure 5] and [Table 2].
Table 2: Comparison of patients with TLNN<12 vs. ≥12 in subgroups

Click here to view
Figure 3: Stratified analyses using the total lymph node number (<12 vs. ≥12) of 169 pathological T3N0 rectal cancer patients with normal carcinoembryonic antigen levels to compare local recurrence-free survival (a), Disease-free survival (b), and overall survival (c), and of 120 patients with elevated carcinoembryonic antigen levels using the total lymph node number to compare local recurrence-free survival (d), disease-free survival (e), and overall survival (f)

Click here to view
Figure 4: Stratified analyses using the total lymph node number (<12 vs. ≥12) of 75 pathological T3N0 rectal cancer patients with low rectal lesions to compare local recurrence-free survival (a), Disease-free survival (b), and overall survival (c), and of 214 patients with high rectal lesions to compare local recurrence-free survival (d), disease-free survival (e), and overall survival (f)

Click here to view
Figure 5: Stratified analyses using the total lymph node number (<12 vs. ≥12) of 88 pathological T3N0 rectal cancer patients treated with total mesorectal excision alone to compare local recurrence-free survival (a), Disease-free survival (b), and overall survival (c), and of 201 patients treated with total mesorectal excision and adjuvant chemotherapy to compare local recurrence-free survival (d), disease-free survival (e), and overall survival (f)

Click here to view


The variables analyzed by univariate analysis were included in multivariate analysis with the Cox regression method. As shown in [Table 3], TLNN remained an independent risk factor for predicting LRFS (HR: 0.096; 95% CI: 0.028–0.333; P < 0.001), DFS (HR: 0.291; 95% CI: 0.161–0.527; P < 0.001), and OS (HR: 0.231; 95% CI: 0.107–0.501; P < 0.001). The CEA level was found to be an independent risk factor for predicting LRFS (HR: 6.258; 95% CI: 2.059–19.017; P = 0.001) and DFS (HR: 2.330; 95% CI: 1.312–4.136; P = 0.004) but not OS. Female sex was associated with a significantly better LRFS (HR: 0.320; 95% CI: 0.105–0.974; P = 0.045) and DFS (HR: 0.457; 95% CI: 0.237–0.880; P = 0.019) but not OS.
Table 3: Multivariate analysis of prognostic factors of LRFS, DFS and OS

Click here to view



 > Discussion Top


Merchant et al. reported the 5-year actuarial LR rate was 12% for T3N0 rectal cancer patients who underwent resection with sharp mesorectal excision without postoperative therapy in the 1980s and 1990s.[9] Another report from the University of Erlangen of Germany demonstrated that the 5-year LR rates were 4.4%, 14.7%, and 18.0% for pT3a/bN0, pT3cN0, and pT3dN0 patients, respectively, during the same period.[10] Several trials have reported that TME surgery alone can reduce the LR rate and improve the survival rate for stage II cancer patients. Studies have reported an LR rate of approximately 10% for pT3N0 patients undergoing TME alone.[11],[12],[13] Similar to previously reported results, our study found that the actuarial 5-year LR rate was 6.4%. Due to the low risk of LR in pathological stage T3N0 rectal cancer and considering the limited survival benefit, the value of postoperative radiotherapy in the treatment of pT3N0 cancer has been questioned. Park et al. did not find a significant difference in the LR rates between patients who did and did not receive postoperative radiotherapy in 390 pT3N0 cancer patients.[14] In addition, the NCCN guideline only recommends postoperative chemotherapy for pT3N0 rectal cancer patients.

The use of tri-modality treatment (surgery plus radiation and chemotherapy) for all pT3N0 cancer patients may be excessive, but surgery with or without postoperative chemotherapy may not be enough for some patients in this stage. The negative result of Park et al.'s study may be because pT3N0 rectal cancer represents a heterogeneous group of more and less aggressive tumors. In clinical practice, the challenge is determining which patients cannot be spared from postoperative chemoradiotherapy as a treatment component.

Retrospective data [15],[16],[17],[18] suggest that there may be a favorable subset of patients with pT3N0 rectal cancer (defined as having well to moderately differentiated histology, extending 2 mm or less into the perirectal fat, lacking lymphatic or vascular invasion, being located in the upper rectum, and having adequate node dissection) who may not benefit from postoperative treatment. Other adverse effects for this subset of patients include elevated CEA levels [11] and perineural invasion.[13]

Whether the TLNN should be regarded as a prognostic factor and a selective criterion for postoperative chemoradiotherapy in pT3N0M0 rectal cancer patients remains unknown, and two studies have reported controversial results.[13],[19] In the current study, we analyzed the prognostic value of the TLNN in TME-treated pT3N0 rectal cancer patients.

Lymph node retrieval and assessment is critical in rectal cancer staging and can impact further decisions on interventions such as postoperative radiotherapy and chemotherapy. A positive lymph node is more likely to be identified if more lymph nodes are harvested, and patients with lymph node-negative rectal cancer have, on average, fewer lymph nodes harvested than do patients with lymph node-positive cancer.[20] The AJCC staging system recommends that at least 12 lymph nodes should be surgically removed to accurately identify early-stage colorectal cancer. However, the number of lymph nodes retrieved can vary significantly, and only 58.8% of the patients in our study had ≥12 lymph nodes harvested.

In Scandolaro et al. study of 71 pT3N0 patients, no significant differences were found in the 5-year RFS and OS when comparing patients with <12 harvested nodes and >12 harvested nodes.[19] In contrast, in 173 pT3N0 rectal cancer patients analyzed by Peng et al., patients with ≥12 harvested lymph nodes had significantly lower 5-year LR and higher 5-year DFS and OS rates.[13] However, those studies had smaller cohorts when compared with the current study and may have lower statistical power to detect an association. To the best of our knowledge, the current study is the largest study to specifically evaluate the association between the number of lymph nodes harvested and prognosis among pT3N0 rectal cancer patients after TME. The TLNN was independently associated with the LRFS, DFS and OS rates in both univariate and multivariate proportional hazard models. The LRFS, DFS, and OS rates of patients who had <12 lymph nodes harvested were only 84.7%, 71.4%, and 77.6%, respectively; these rates are substantially low, indicating that these patients require further therapeutic intervention.

Factors such as the extent of surgery, type of surgical procedure, thoroughness of the pathological assessment, tumor location, tumor size, histological grade, and patient age can have a significant impact on the TLNN.[21],[22],[23] Additional important factors that may influence the TLNN are the inflammatory and immunologic responses of the human body to cancer. A lower TLNN may be correlated with a suppressed immune reaction and, consequently, a higher relapse probability.

The CEA level has been indicated as a useful prognostic factor for colorectal cancer. In patients with normal CEA levels, patients with a TLNN < 12 still have excellent local control and a very low disease relapse rate; these findings are comparable to those in patients with a TLNN ≥ 12. This result indicates that even if the lymph node dissection is not thorough enough, micrometastasis may not exist yet, and postoperative chemoradiotherapy may not be needed. In patients with elevated CEA levels, the differences in 5-year LRFS, DFS, and OS between the patients with <12 and ≥12 lymph nodes harvested were all approximately 25%. The lower survival rates of patients with <12 lymph nodes harvested indicates that some patients may have been under-staged on pathological staging or that micrometastasis likely already existed in the regional lymph nodes. Postoperative chemoradiotherapy is strongly required for these patients.

Further subgroup analysis showed that in both low and high rectal cancer, the TLNN was a significant prognostic factor for LRFS, DFS, and OS, favoring the examination of ≥12 lymph nodes. The median TLNN for low and high rectal cancer (using 5 cm from the anus as the cut-off) was 12 and 13, respectively. Tumor location did not correlate with the TLNN.

A portion of patients received 5-FU-based postoperative chemotherapy according the chief physician's decision. In this study, regardless of whether the patient received postoperative chemotherapy, patients with a TLNN ≥12 had significantly higher 5-year LRFS and DFS rates than those with a TLNN < 12, with a difference of approximately 10–20%. However, a difference in OS was only found in the patients who received postoperative chemotherapy, possibly due to the small sample size in the subgroup who received surgery alone. Although postoperative chemotherapy could help to overcome the adverse impact of inadequate lymph node examination, postoperative radiotherapy remains strongly required for patients with <12 lymph nodes harvested.

The results from this study should be interpreted with caution. Because the data on lymphovascular invasion and perineural invasion were incomplete, they were not included in the multivariate analysis. Furthermore, the study was conducted on patients who received treatment over an 8-year period, and it is possible that surgical and pathological techniques changed over that time.


 > Conclusions Top


The examination of <12 lymph nodes is a common pathological feature in this patient subset. The number of lymph nodes harvested was independently associated with local control, disease relapse, and OS in patients with pT3N0 rectal cancer who received TME with or without postoperative chemotherapy. The pT3N0 rectal cancer patients with <12 lymph nodes harvested should be considered for postoperative radiotherapy, especially those patients with elevated CEA levels at diagnosis.

Acknowledgments

This study was supported by the National Natural Science Foundation of China (No. 81071891) and the Science and Technology Planning Project of Guangdong Province, China (No. 2010B0807017).

Financial support and sponsorship

This study was supported by the National Natural Science Foundation of China (No. 81071891) and the Science and Technology Planning Project of Guangdong Province, China (No. 2010B0807017).

Conflicts of interest

There are no conflicts of interest.

 
 > References Top

1.
Guillem JG, Díaz-González JA, Minsky BD, Valentini V, Jeong SY, Rodriguez-Bigas MA, et al. cT3N0 rectal cancer: Potential overtreatment with preoperative chemoradiotherapy is warranted. J Clin Oncol 2008;26:368-73.  Back to cited text no. 1
    
2.
Wo JY, Mamon HJ, Ryan DP, Hong TS. T3N0 rectal cancer: Radiation for all? Semin Radiat Oncol 2011;21:212-9.  Back to cited text no. 2
[PUBMED]    
3.
Yi M, Meric-Bernstam F, Ross MI, Akins JS, Hwang RF, Lucci A, et al. How many sentinel lymph nodes are enough during sentinel lymph node dissection for breast cancer? Cancer 2008;113:30-7.  Back to cited text no. 3
[PUBMED]    
4.
Chen S, Zhao BW, Li YF, Feng XY, Sun XW, Li W, et al. The prognostic value of harvested lymph nodes and the metastatic lymph node ratio for gastric cancer patients: Results of a study of 1,101 patients. PLoS One 2012;7:e49424.  Back to cited text no. 4
[PUBMED]    
5.
Zhu Z, Chen H, Yu W, Fu X, Xiang J, Li H, et al. Number of negative lymph nodes is associated with survival in thoracic esophageal squamous cell carcinoma patients undergoing three-field lymphadenectomy. Ann Surg Oncol 2014;21:2857-63.  Back to cited text no. 5
[PUBMED]    
6.
Chandrasinghe PC, Ediriweera DS, Hewavisenthi J, Kumarage S, Deen KI. Total number of lymph nodes harvested is associated with better survival in stages II and III colorectal cancer. Indian J Gastroenterol 2014;33:249-53.  Back to cited text no. 6
[PUBMED]    
7.
Huh JW, Kim CH, Kim HR, Kim YJ. Factors predicting oncologic outcomes in patients with fewer than 12 lymph nodes retrieved after curative resection for colon cancer. J Surg Oncol 2012;105:125-9.  Back to cited text no. 7
[PUBMED]    
8.
Edge SB, Byrd DR, Compton CC, Fritz AG, Greene FL, Trotti A, editors. AJCC Cancer Staging Manual. 7th ed. New York: Springer; 2010.  Back to cited text no. 8
    
9.
Merchant NB, Guillem JG, Paty PB, Enker WE, Minsky BD, Quan SH, et al. T3N0 rectal cancer: Results following sharp mesorectal excision and no adjuvant therapy. J Gastrointest Surg 1999;3:642-7.  Back to cited text no. 9
[PUBMED]    
10.
Sauer R. Adjuvant and neoadjuvant radiotherapy and concurrent radiochemotherapy for rectal cancer. Pathol Oncol Res 2002;8:7-17.  Back to cited text no. 10
[PUBMED]    
11.
Nissan A, Stojadinovic A, Shia J, Hoos A, Guillem JG, Klimstra D, et al. Predictors of recurrence in patients with T2 and early T3, N0 adenocarcinoma of the rectum treated by surgery alone. J Clin Oncol 2006;24:4078-84.  Back to cited text no. 11
[PUBMED]    
12.
Zhu J, Xu Y, Gu W, Peng J, Cai G, Cai G, et al. Adjuvant therapy for T3N0 rectal cancer in the total mesorectal excision era- identification of the high risk patients. Radiat Oncol 2010;5:118.  Back to cited text no. 12
[PUBMED]    
13.
Peng J, Sheng W, Huang D, Venook AP, Xu Y, Guan Z, et al. Perineural invasion in pT3N0 rectal cancer: The incidence and its prognostic effect. Cancer 2011;117:1415-21.  Back to cited text no. 13
[PUBMED]    
14.
Park IJ, Kim HC, Yu CS, Kim TW, Jang SJ, Kim JC. Effect of adjuvant radiotherapy on local recurrence in stage II rectal cancer. Ann Surg Oncol 2008;15:519-25.  Back to cited text no. 14
[PUBMED]    
15.
Lopez-Kostner F, Lavery IC, Hool GR, Rybicki LA, Fazio VW. Total mesorectal excision is not necessary for cancers of the upper rectum. Surgery 1998;124:612-7.  Back to cited text no. 15
[PUBMED]    
16.
Willett CG, Badizadegan K, Ancukiewicz M, Shellito PC. Prognostic factors in stage T3N0 rectal cancer: Do all patients require postoperative pelvic irradiation and chemotherapy? Dis Colon Rectum 1999;42:167-73.  Back to cited text no. 16
[PUBMED]    
17.
Willett CG. Sphincter preservation in rectal cancer. Local excision followed by postoperative radiation therapy. Semin Radiat Oncol 1998;8:24-9.  Back to cited text no. 17
[PUBMED]    
18.
Frasson M, Garcia-Granero E, Roda D, Flor-Lorente B, Roselló S, Esclapez P, et al. Preoperative chemoradiation may not always be needed for patients with T3 and T2N+rectal cancer. Cancer 2011;117:3118-25.  Back to cited text no. 18
    
19.
Scandolaro L, Cazzaniga LF, Bianchi E, Cagna E, Prina M, Valli MC, et al. Postoperative adjuvant radio (chemo) therapy for rectal cancer: An appraisal. Tumori 2004;90:208-15.  Back to cited text no. 19
[PUBMED]    
20.
Tepper JE, O'Connell MJ, Niedzwiecki D, Hollis D, Compton C, Benson AB 3rd, et al. Impact of number of nodes retrieved on outcome in patients with rectal cancer. J Clin Oncol 2001;19:157-63.  Back to cited text no. 20
    
21.
Sigurdson ER. Lymph node dissection: Is it bdiagnostic or therapeutic? J Clin Oncol 2003;21:965-7.  Back to cited text no. 21
[PUBMED]    
22.
Görög D, Nagy P, Péter A, Perner F. Influence of obesity on lymph node recovery from rectal resection specimens. Pathol Oncol Res 2003;9:180-3.  Back to cited text no. 22
    
23.
Thorn CC, Woodcock NP, Scott N, Verbeke C, Scott SB, Ambrose NS. What factors affect lymph node yield in surgery for rectal cancer? Colorectal Dis 2004;6:356-61.  Back to cited text no. 23
[PUBMED]    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]



 

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)

  >Abstract>Introduction>Methods>Results>Discussion>Conclusions>Article Figures>Article Tables
  In this article
>References

 Article Access Statistics
    Viewed96    
    Printed7    
    Emailed0    
    PDF Downloaded20    
    Comments [Add]    

Recommend this journal


[TAG2]
[TAG3]
[TAG4]