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ORIGINAL ARTICLE
Year :   |  Volume :   |  Issue :   |  Page :
 

Proper surgical extent for clinical Stage I right colon cancer


1 Department of Surgery, Chonnam National University Hospital, Chonnam National University College of Medicine, Gwangju, South Korea
2 Department of Surgery, Chonnam National University Hospital, Gwangju, South Korea
3 Department of Surgery, Chonnam National University Hwasun Hospital, Chonnam National University College of Medicine, Gwangju, South Korea

Date of Submission06-Jan-2021
Date of Decision22-Apr-2021
Date of Acceptance24-May-2021
Date of Web Publication06-Sep-2021

Correspondence Address:
Hyeong Rok Kim,
322 Seoyang-ro, Hwasun-eup, Hwasun-gun, Jeonnam 58128
South Korea
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jmas.JMAS_9_21

  Abstract 


Purpose: Pre-operative evaluation identifying clinical-stage affects the decision regarding the extent of surgical resection in right colon cancer. This study was designed to predict a proper surgical resection through the prognosis of clinical Stage I right colon cancer.
Patients and Methods: We included patients who were diagnosed with clinical and pathological Stage I right-sided colon cancer, including appendiceal, caecal, ascending, hepatic flexure and proximal transverse colon cancer, between August 2010 and December 2016 in two tertiary teaching hospitals. Patients who underwent open surgeries were excluded because laparoscopic surgery is the initial approach for colorectal cancer in our institutions.
Results: Eighty patients with clinical Stage I and 104 patients with pathological Stage I were included in the study. The biopsy reports showed that the tumour size was larger in the clinical Stage I group than in the pathological Stage I group (3.4 vs. 2.3 cm, P < 0.001). Further, the clinical Stage I group had some pathological Stage III cases (positive lymph nodes, P = 0.023). The clinical Stage I group had a higher rate of distant metastases (P = 0.046) and a lower rate of overall (P = 0.031) and cancer-specific survival (P = 0.021) than the pathological Stage I group. Compared to pathological Stage II included in the period, some of the survival curves were located below the pathological Stage II, but there was no statistical difference.
Conclusion: The study results show that even clinical Stage I cases, radical resection should be considered in accordance with T3 and T4 tumours.


Keywords: Clinical stage, outcome, pathological stage, right colon cancer, Stage I



How to cite this URL:
Kwak HD, Chung JS, Ju JK, Lee SY, Kim CH, Kim HR. Proper surgical extent for clinical Stage I right colon cancer. J Min Access Surg [Epub ahead of print] [cited 2021 Dec 9]. Available from: https://www.journalofmas.com/preprintarticle.asp?id=325623





  Introduction Top


Despite innovative changes in surgical treatment and global standardisation, unexpected recurrence and metastasis have been reported in potentially curable colon cancer, even in the early stages of the disease. The surgical treatment for right-sided colon cancer has been standardised;[1] however, treatment for early colon cancer is controversial, varying from endoscopic management to radical surgical resection. Excessive lymphatic dissection in the early stages of the disease can cause post-operative complications, while insufficient resection in the advanced stages of the disease can increase the risk of recurrence. Therefore, predicting the exact cancer stage preoperatively is important for determining the extent of surgical resection. This study was designed to predict the proper surgical extent through the prognosis of clinically early right-sided colon cancer.


  Patients And Methods Top


The study included patients diagnosed with right-sided colon cancer classified as clinical Stage I and pathological Stage I. All patients underwent surgical treatment at OOO hospital and OOOO hospital between 2010 and 2016, and the parameters were prospectively collected. The disease was staged according to the eighth edition of the tumour, node and metastasis classification of colon cancer proposed by the Union for International Cancer Control (UICC) and the American Joint Committee on Cancer. Appendiceal, caecal, ascending colon, hepatic flexure colon and proximal transverse colon cancer were included as right-sided colon cancer. Clinical Stage I was defined as T1 and T2 on abdominal computed tomography (CT) with negative lymph node metastasis. All the included cases were confirmed to have no metastasis on abdominal and chest CT. Radical lymph node dissection was performed on all patients, which refers to the case in which the principal nodes were included according to the Japanese Society for Cancer of the Colon and Rectum (JSCCR) guidelines.[2] In these institutions, open surgeries performed in <5% of patients; therefore, this study only included patients who underwent laparoscopy.

The following pre-operative data were evaluated: age, gender, body mass index (BMI), American Society of Anaesthesiologists (ASA) score, past medical history, previous abdominal surgery and pre-operative carcinoembryonic antigen (CEA) level. Further, the following intra-operative parameters were assessed: tumour location, extent of surgical resection, operating time, and estimated blood loss. The following pathological factors were evaluated: tumour size, length of proximal/distal margins, number of retrieved/pathological lymph nodes, presence of vascular/lymphatic/neural invasion and type of differentiation. In addition, the following post-operative outcomes were assessed: post-operative CEA level, date of first flatus/defecation/diet, length of hospital stay and type of post-operative complications (the Clavien–Dindo classification). The 5-year disease-free survival (DFS), overall survival, and cancer-specific survival (CSS) were analysed based on the presence or absence of local and systemic recurrence and metastasis. The patients visited the hospitals quarterly for the first 2 years and semiannually thereafter for 3 years. During follow-up, serum CEA tests and abdomen and chest CT were performed semiannually and total colonoscopy was performed annually. Recurrence was defined as a pathologically identified or radiologically proven local or systemic metastasis. The study was approved by the Institutional Review Board of OOO Hospital (CNUH-2019-119).

Statistical analysis

The groups were compared using Student's t-test or the Mann–Whitney U-test for continuous data and the Chi-square test or Fisher's exact test for categorical data. The recurrence and survival rates were estimated using Kaplan–Meier curve analyses. Statistical analyses were performed using SPSS (IBM, SPSS Statistics, Version 20, Armonk, NY, USA). A P ≤ 0.05 was considered statistically significant.


  Results Top


Patients' characteristics and operative outcomes

Eighty patients were diagnosed with clinical Stage I right-sided colon cancer, and 104 were diagnosed with pathological Stage I right-sided colon cancer. There was no difference in the groups in terms of age, gender, BMI, ASA score, past medical history (hypertension and diabetes mellitus) and previous abdominal surgery. Further, the tumour location, extent of surgical resection, operation time and estimated blood loss did not differ between the groups. None of the cases required conversion to open surgery [Table 1].
Table 1: Patients' characteristics and operative outcomes

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Pathologic outcomes

The tumour size was larger in the clinical Stage I group than in the pathological Stage I group (2.3 vs. 3.4 cm; P < 0.001). The frequency of neural invasion was higher in the clinical Stage I group than in the pathological Stage I group (15% [12 cases] vs. 5.8% [6 cases]; P = 0.037). Of the 184 patients included in the study, 154 (83.7%) patients had undergone radical lymph node dissection, including the principal node [Table 2].
Table 2: Pathologic outcomes

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Short-and long-term outcomes

There was no difference between the groups in terms of short-term post-operative outcomes. The length of the hospital stay was 8 days. There was no difference in post-operative complications, such as surgical site infection, intra-abdominal bleeding, anastomotic bleeding, anastomosis leakage, ileus and urinary retention, between the groups. No death was recorded till post-operative day 30 [Table 3].
Table 3: Post-operative outcomes

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The median follow-up period after surgery was 33.6 months, which did not differ between the groups. The rate of local recurrence did not differ between the groups (P = 0.874), but the rate of distant metastasis statistically differed (3 [2 hepatic and 1 pulmonary] cases in the clinical Stage I group vs. 0 cases in the pathological Stage I group; P = 0.046). No statistical difference was seen in the 5-year DFS between the clinical Stage I group and the pathological Stage I group (94.3 vs. 94.9; P = 0.386); however, statistical difference was seen in the 5-year OS (85.4 vs. 95.3; P = 0.031) and CCS (92 vs. 99, P = 0.021). Compared to pathological Stage II, some of the survival curves of clinical Stage I were located below the pathological Stage II, although there did not statistically differ (DFS: 94.3 vs. 95.4%; P = 0.140, OS: 85.4 vs. 87.2; P = 0.292, CSS: 92 vs. 96%; P = 0.163) [Table 3] and [Figure 1].
Figure 1: Oncologic outcomes between clinical Stage I, pathological Stage I, and pathological Stage II: (a) recurrence-free survival, (b) overall survival and (c) cancer-specific survival

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  Discussion Top


The study revealed significant differences in several parameters between clinical and pathological Stages I right-sided colon cancer. The clinical Stage I group had a larger tumour size, higher frequency of neural invasion (which denotes a poorer prognosis), and lower survival rate in some survival analyses than the pathological Stage I group. In particular, survival curves of clinical Stage I were similar to those of pathological Stage II.

The ESMO clinical practice guidelines recommend wide surgical resection and anastomosis for Stage I colon cancer.[3] The National Comprehensive Cancer Network does not provide clear recommendation for early-stage colon cancer.[4] The JSCCR guidelines 2016 recommend that at least D2 dissection for clinical T2 cancer and that D3 dissection may be needed in approximately 1% of case with a possibility of principal lymph node metastasis. However, this guideline provides insufficient evidence regarding the extent of lymph node dissection in cT2 cancers.[2] Although there are recent expert consensus recommendations, complete mesocolic excision in early colon cancer is controversial.[5]

In a study on the necessity of IMA ligation in T1 left-sided colon cancer including 121 patients, 12 had a nodal involvement, of whom 11 were diagnosed with lymph node metastases limited to the pericolic area. Therefore, IMA, the principal lymph node, can be preserved in T1 tumours.[6] However, in the case of right-sided colon cancer, lymphadenectomy is technically challenging and there is a variable distribution of blood vessels and lymph nodes. For all colorectal cancers, several studies on early stage have been published. In these studies, 13% of patients with T1 colorectal cancer had lymphatic metastasis, and lymphovascular invasion (P = 0.005), sm3 depth (P = 0.001) and lower rectum (P = 0.007) were identified as risk factors.[7] In a study on submucosal invasive colorectal cancer (SICC), lymph node metastasis was found in 14.3% of patients, and sm3, poorly differentiated cancer (P = 0.028) and tumour cell dissociation (P = 0.045) were identified as risk factors. According to the authors, local excision should be considered carefully.[8] In another pathological study on SICC, lymph node metastasis was found in 14.3% of patients, and lymphatic invasion (P < 0.01), tumour differentiation (P < 0.01), and tumour budding (P < 0.01) were significantly associated with lymph node metastasis.[9] Some of the authors included in our study also recommended that lymph node metastasis was higher in the case of lymphovascular invasion (P < 0.001) or perineural invasion (P = 0.004) in T1 and T2 colorectal cancer.[10] A systemic review and meta-analysis reported a 13% risk of lymph node metastasis in T1 cancers (95% confidence interval: 11.5%–15.4%) and the lowest risk of nodal metastasis in case of a depth of invasion ≤1,000 μm from the muscularis mucosa, good differentiation, absence of lymphatic and vascular invasion and the absence of tumour budding. However, it revealed the risk was not zero (1.9%), and the quality of evidence was poor.[11]

The reliability of CT in evaluating the staging preoperatively is questionable. In a study that reviewed 150 CT scans, CT failed to identify 18% of primary cancers, with an overall accuracy of only 63%. Overstaged and understaged clinical T stage were 23.7% and 48.3%, and clinical nodal stage were 28.7% and 53.0%, respectively.[12] Thus, MRI may be a more valuable tool than CT in the pre-operative staging of colon cancer.[13]

In a recent study by these authors, only 43.8% of clinical Stage I right-sided colon cancers were diagnosed as pathological Stage I. Risk factors for migration to overstaging include tumour size (P = 0.010) and the number of retrieved lymph nodes (P = 0.046).[14] In a study comparing complete (D3) and standard (D2) mesenteric excision with Stage I and II cancers, the D3 group had a higher 3-year OS (88.1% vs. 79.0%, P = 0.003) and DFS (82.1% vs. 74.3%, P = 0.026) than the D2 group.[15] In another study, the complete mesocolic excision (CME) group had better 4-year DFS rates (85.8% vs. 73.4%, P = 0.0014) and a higher UICC Stage I disease (100% vs. 89.8%, P = 0·046) than the non-CME group after propensity score matching.[16] This should be clarified and more accurate in upcoming studies.[17]

This study has some limitations. The radiological reports of pre-operative images may have different results depending on the institution. However, it is not thought to be beyond the range of standard radiologic reports because the institutions are responsible for more than 500 cases of colorectal cancer surgeries per year. The small sample size included in this study and retrospective design can also be limitations. However, the data were collected prospectively. Therefore, a large-sized multicentre trial is required to confirm the study results.


  Conclusion Top


Even in the case of clinical Stage I, radical resection should be considered in accordance with T3 and T4 tumours.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
West NP, Hohenberger W, Weber K, Perrakis A, Finan PJ, Quirke P. Complete mesocolic excision with central vascular ligation produces an oncologically superior specimen compared with standard surgery for carcinoma of the colon. J Clin Oncol 2010;28:272-8.  Back to cited text no. 1
    
2.
Watanabe T, Muro K, Ajioka Y, Hashiguchi Y, Ito Y, Saito Y, et al. Japanese Society for Cancer of the Colon and Rectum (JSCCR) guidelines 2016 for the treatment of colorectal cancer. Int J Clin Oncol 2018;23:1-34.  Back to cited text no. 2
    
3.
Labianca R, Nordlinger B, Beretta G, Mosconi S, Mandalà M, Cervantes A, et al. Early colon cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 2013;24:vi64-72.  Back to cited text no. 3
    
4.
Benson AB, Venook AP, Al-Hawary MM, Cederquist L, Chen YJ, Ciombor KK, et al. NCCN Guidelines Insights: Colon Cancer, Version 2.2018. J Natl Compr Canc Netw 2018;16:359-69.  Back to cited text no. 4
    
5.
Zheng M, Ma J, Fingerhut A, Adamina MP, Atroschenko A, Bergamaschi R, et al. Complete mesocolic excision for colonic cancer: Society for Translational Medicine expert consensus statement. Ann Laparosc Endosc Surg 2018;3:68.  Back to cited text no. 5
    
6.
Kawamura YJ, Sakuragi M, Togashi K, Okada M, Nagai H, Konishi F. Distribution of lymph node metastasis in T1 sigmoid colon carcinoma: Should we ligate the inferior mesenteric artery? Scand J Gastroenterol 2005;40:858-61.  Back to cited text no. 6
    
7.
Nascimbeni R, Burgart LJ, Nivatvongs S, Larson DR. Risk of lymph node metastasis in T1 carcinoma of the colon and rectum. Dis Colon Rectum 2002;45:200-6.  Back to cited text no. 7
    
8.
Choi PW, Yu CS, Jang SJ, Jung SH, Kim HC, Kim JC. Risk factors for lymph node metastasis in submucosal invasive colorectal cancer. World J Surg 2008;32:2089-94.  Back to cited text no. 8
    
9.
Tateishi Y, Nakanishi Y, Taniguchi H, Shimoda T, Umemura S. Pathological prognostic factors predicting lymph node metastasis in submucosal invasive (T1) colorectal carcinoma. Mod Pathol 2010;23:1068-72.  Back to cited text no. 9
    
10.
Huh JW, Kim HR, Kim YJ. Lymphovascular or perineural invasion may predict lymph node metastasis in patients with T1 and T2 colorectal cancer. J Gastrointest Surg 2010;14:1074-80.  Back to cited text no. 10
    
11.
Mou S, Soetikno R, Shimoda T, Rouse R, Kaltenbach T. Pathologic predictive factors for lymph node metastasis in submucosal invasive (T1) colorectal cancer: A systematic review and meta-analysis. Surg Endosc 2013;27:2692-703.  Back to cited text no. 11
    
12.
Fernandez LM, Parlade AJ, Wasser EJ, Dasilva G, de Azevedo RU, Ortega CD, et al. How reliable is CT scan in staging right colon cancer? Dis Colon Rectum 2019;62:960-4.  Back to cited text no. 12
    
13.
Nerad E, Lambregts DM, Kersten EL, Maas M, Bakers FCH, van den Bosch HCM, et al. MRI for local staging of colon cancer: Can MRI become the optimal staging modality for patients with colon cancer? Dis Colon Rectum 2017;60:385-92.  Back to cited text no. 13
    
14.
Kwak HD, Ju JK, Yeom SS, Lee SY, Kim CH, Kim YJ, et al. Is radical surgery for clinical Stage I right-sided colon cancer relevant? A retrospective review. Ann Surg Treat Res 2020;98:139-45.  Back to cited text no. 14
    
15.
Storli KE, Søndenaa K, Furnes B, Nesvik I, Gudlaugsson E, Bukholm I, et al. Short term results of complete (D3) vs. standard (D2) mesenteric excision in colon cancer shows improved outcome of complete mesenteric excision in patients with TNM Stages I-II. Tech Coloproctol 2014;18:557-64.  Back to cited text no. 15
    
16.
Bertelsen CA, Neuenschwander AU, Jansen JE, Wilhelmsen M, Kirkegaard-Klitbo A, Tenma JR, et al. Disease-free survival after complete mesocolic excision compared with conventional colon cancer surgery: A retrospective, population-based study. Lancet Oncol 2015;16:161-8.  Back to cited text no. 16
    
17.
Lu JY, Xu L, Xue HD, Zhou WX, Xu T, Qiu HZ, et al. The Radical Extent of lymphadenectomy-D2 dissection versus complete mesocolic excision of LAparoscopic Right Colectomy for right-sided colon cancer (RELARC) trial: Study protocol for a randomized controlled trial. Trials 2016;17:582.  Back to cited text no. 17
    


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    Tables

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2004 Journal of Minimal Access Surgery
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Online since 15th August '04