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

Prognosis of laparoscopic surgery for colorectal cancer in middle-aged patients


 Department of General Surgery, Mianyang Central Hospital, School of Medicine, University of Electronic Science and Technology of China, Mianyang, Sichuan, China

Date of Submission21-Feb-2022
Date of Decision11-Apr-2022
Date of Acceptance29-Apr-2021
Date of Web Publication20-Jul-2022

Correspondence Address:
Jian-Ying Shang,
Department of General Surgery, Mianyang Central Hospital, School of Medicine, University of Electronic Science and Technology of China, 12 Changjia Lane, Jingzhong Street, Mianyang, 621000, Sichuan
China
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jmas.jmas_81_22

PMID: 35915539

  Abstract 


Background: The prognosis of middle-aged patients with colorectal cancer (CRC) treated by laparoscopic resection (LR) is unclear. This study aimed to evaluate the survival outcomes of LR compared with open resection (OR) for middle-aged patients with CRC.
Patients and Methods: This retrospective cohort study used the data from a database of all consecutive colorectal resections performed between January 2009 and December 2017. Propensity score matching (PSM) was performed to handle the selection bias based on age, gender, body mass index, tumour location, AJCC stage and admission year. Univariate and multivariate COX regression model was used to identify risk factors of overall survival (OS) and disease-free survival (DFS).
Results: After PSM, 154 patients were included in each group. Compared with the OR group in the total cohort, there were better survival outcomes in the LR group for 5-year OS and 5-year DFS (both P < 0.001). These differences were observed for Stage II and III diseases and for all CRC, irrespective of location. The multivariate analysis showed that tumour ≥5 cm (hazard ratio [HR] = 1.750, 95% confidence interval [CI]: 1.026–2.986, P = 0.040), Stage III (HR = 14.092, 95% CI: 1.894–104.848, P = 0.010) and LR (HR = 0.300, 95% CI: 0.160–0.560, P < 0.001) were independently associated with OS. Pre-operative carcinoembryonic antigen ≥5 ng/ml (HR = 3.954, 95% CI: 1.363–11.473, P = 0.011), Stage III (HR = 6.206, 95% CI: 1.470–26.200, P = 0.013) and LR (HR = 0.341, 95% CI: 0.178–0.653, P = 0.001) were independently associated with DFS.
Conclusions: In middle-aged patients with CRC, LR achieves better survival than OR. Complications are similar, except for less blood loss and shorter post-surgical hospital stay with LR.


Keywords: Colorectal cancer, laparoscopy, middle-aged, prognosis, surgical oncology



How to cite this URL:
Bao F, Wu LR, Deng ZG, Xiang CH, Shang JY. Prognosis of laparoscopic surgery for colorectal cancer in middle-aged patients. J Min Access Surg [Epub ahead of print] [cited 2022 Aug 14]. Available from: https://www.journalofmas.com/preprintarticle.asp?id=351256





  Introduction Top


Colorectal cancer (CRC) is the third-most common cancer type globally.[1] It is also the fifth-leading cause of cancer death in China, and its incidence is rapidly increasing.[2] The management of CRC involves a multidisciplinary strategy that includes surgery, systemic therapy and radiotherapy.[1] Depending on the extent and characteristics of the lesion and the patient's condition, surgery can be performed by endoscopy, laparoscopy or open surgery.[1]

Laparoscopy is widely used in the surgical management of CRC.[1] The advantages of laparoscopic procedures include less pain, quicker recovery, shorter hospital stay and better quality of life than open surgery.[3] Data from randomised trials and a meta-analysis definitively established that laparoscopic colon surgery is at least equivalent to open surgery.[4] Compared with open surgery, laparoscopic resection (LR) minimises the surgical stress and systemic inflammatory response after surgery.[4] Consequently, the post-operative immune function is better preserved with laparoscopic surgery, which may significantly increase the patient's resistance to cancer and maybe have advantages regarding the long-term outcomes.[5]

The CRC incidence is about 13/100,000 individuals aged 20–49 years, 70/100,000 for the 50–64 years of age group, 125/100,000 for those aged 65–74 years and 225/100,000 individuals >75 years.[6] The incidence of CRC peaks at 74–80 years of age, and the median age at diagnosis is 70 years,[7] but patients with predisposing genetic conditions will have a young onset.[8] Since these middle-aged patients represent a small proportion of the patients with CRC and since many studies exclude patients with a high risk of CRC, they are underrepresented in the literature, and few reliable data are available about them. There are specific risk factors for CRC development in middle-aged individuals, including obesity, physical inactivity, alcohol consumption, early adulthood cigarette smoking, red meat consumption and low intake of folic acid.[9] On the other hand, some factors might be associated with a better prognosis of CRC in middle-aged patients. Indeed, middle-aged patients are often more fit to undergo chemotherapy than elderly patients.[10] In addition, middle-aged patients often have a better socio-economic status and have fewer comorbidities, and they might have a stronger desire for survival and adjuvant therapy.[10] Few reports examined the advantages of laparoscopic surgery compared with open surgery for CRC in middle-aged patients. The prognostic advantages of laparoscopic surgery in this particular population are unclear. Furthermore, most available data are from Western countries, and data are lacking for China.

Therefore, this study aimed to evaluate the survival outcomes of laparoscopic surgery compared with open surgery for Chinese patients with CRC and 45–65 years of age.


  Patients and Methods Top


Study design and patients

This retrospective cohort study used the data from a database of all consecutive colorectal resections performed in the Department of General Surgery of the authors' hospital, Sichuan Province, China, between January 2009 and December 2017. The study followed the ethical standards of the Declaration of Helsinki, as revised in 2013. This study was approved by the ethics committee of the authors' hospital. The requirement for individual consent was waived by the committee because of the retrospective nature of this study.

The inclusion criteria were (1) colon or rectal cancer localised above the peritoneal reflection; (2) radical (R0) D3 lymphadenectomy (tumour, node, metastasis [TNM] Stage I-III); (3) histopathologically proven primary CRC; (4) 45–65 years of age (based on the quartiles of onset age of CRC in the hospital database);[8] (5) no history of cancer before the CRC included in this study; (6) histological type included adenocarcinoma, signet-ring cell carcinoma and mucinous adenocarcinoma and (7) American Society of Anaesthesiologists Class I-III.

The exclusion criteria were (1) emergency surgery; (2) synchronous tumours; (3) familial adenomatous polyposis (FAP) or (4) inflammatory bowel diseases.

Surgery and grouping

The patients were grouped according to LR or open resection (OR). Patients for whom the LR was converted into OR were analysed as part of the OR group. All operations were performed or assisted by one of the team's six colorectal surgeons (experienced in open surgery and with >50 CRC laparoscopic operations/year for more than 5 years) using standardised techniques. The choice of the procedure was based on the patient's preference after an informed, comprehensive discussion. If the length of the incision exceeded 10 cm, LR was considered a conversion to OR.[11] According to the Japanese Society for Cancer of the Colon and Rectum, all patients underwent D3 lymphadenectomy.[12] All laparoscopic procedures were performed through a standardised medial-to-lateral approach.[13]

Adjuvant therapy

According to the patient's post-operative general condition or compliance and the physicians' experience, the patients with T3-4 or Stage III disease were considered for 5-fluorouracil-based chemotherapy.[14]

Post-operative complications

Post-operative complications were those occurring within 30 days after surgery. Anastomosis-related complications (leakage, stenosis or intraluminal bleeding) were confirmed by X-ray, endoscopy or angiography. Intra-abdominal collections and abscesses were proven by ultrasound or computed tomography scans and concomitant systemic inflammatory response lasting ≥24 h. Post-operative haemorrhage was defined as a blood loss of >300 mL according to the drainage volume. The severity of post-operative complications was assessed according to the Clavien–Dindo classification.[15]

Data collection

Pre-operative variables (age, gender, tumour location and pre-operative carcinoembryonic antigen [CEA]), intra-operative data (operation time, blood loss and the number of lymph nodes harvested) and post-operative data (largest tumour diameter, American Joint Committee on Cancer (AJCC) stage, histological grade, post-operative complications and length of post-operative hospital stay) were recorded.

The tumour was staged according to the seventh AJCC TNM classification.[16] Tumour location was classified as right-sided tumours (cecum, ascending colon, hepatic flexure and transverse colon), left-sided tumours (splenic flexure, descending colon and sigmoid colon) and rectal cancer.

Follow-up

The patients were routinely followed at 3-month intervals for the first 2 years, at 6-month intervals for the next 3 years and then annually. The last follow-up was in December 2020. Local recurrence was defined as a recurring tumour limited to the previous tumour resection site or adjacent organs. Distant recurrence was defined as any tumour recurrence outside the primary site of the disease. Overall survival (OS) was measured from the date of surgery to death from any cause. Disease-free survival (DFS) was measured from the time of operation to the date of progression or death from any cause. Lost to follow-up was defined as the complete impossibility of seeing or contacting the patients, either by phone, mail or e-mail.

Propensity score matching

To mitigate the selection bias due to the retrospective nature of this study, propensity score matching (PSM) was done to handle the selection bias and estimate the two groups' prognosis. Propensity scores were obtained by logistic regression analysis of age, gender, body mass index (BMI), tumour location, AJCC stage and admission year. One-to-one pair matching without replacement and a nearest-neighbour matching algorithm with callipers <0.05 were performed using SPSS 26 (IBM, Armonk, NY, USA).

Statistical analysis

Data were presented as means ± standard deviations for continuous variables and as numbers and percentages for categorical variables. The characteristics of the two groups were compared using the independent t-test for continuous variables and either the Chi-square test or Fisher's exact test for the categorical variables. Survival analysis was performed using the Kaplan–Meier method and compared using the log-rank test. The patients lost to follow-up were censored at their last visit. Variables with P < 0.10 in the univariate analyses were entered into a multivariate Cox regression analysis using the enter method. Statistical analyses were performed using SPSS 26.0 (IBM, Armonk, NY, USA). Two-sided P < 0.05 were considered statistically significant.


  Results Top


Clinicopathological characteristics and perioperative outcomes

[Supplementary Figure S1] presents the flow chart of the patients' enrolment. A total of 1319 patients were identified as potentially eligible. Patients with emergency surgery (e.g. acute intestinal obstruction or perforation and acute bleeding) (n = 5), FAP (n = 4), synchronous tumours (n = 1), inflammatory bowel diseases (n = 5), other types of cancers (n = 5) (except for adenocarcinoma, signet-ring cell carcinoma and mucinous adenocarcinoma), Stage IV disease (n = 171) and lesion below the peritoneal reflection (n = 468) were excluded. Finally, 660 patients were included.



The LR and OR groups included 405 (61.4%; 55.9 ± 5.9 years of age) and 255 (38.6%; 56.0 ± 5.8 years of age) patients, respectively. Before matching, BMI (22.9 ± 3.3 vs. 21.7 ± 3.4 kg/m2, m P = 0.021), frequency of admission in 2014–2017 (88.4% vs. 43.1%, P < 0.001), rectal tumour (32.1% vs. 16.5%, P < 0.001), right-sided tumours (28.6% vs. 43.1%, P = 0.001), tumour size (4.4 ± 2.5 vs. 5.0 ± 2.2 cm, P = 0.013), operation time (153.2 ± 47.7 vs. 165.7 ± 53.5 min, P = 0.002), blood loss (78 ± 75 vs. 157 ± 104 ml, P < 0.001), post-surgical hospital stay (9.9 ± 5.4 vs. 12.4 ± 5.5 days, P < 0.001), number of retrieved LNs (15.5 ± 16.0 vs. 12.7 ± 8.4, P = 0.009) and the use of adjuvant therapy (42.0% vs. 70.6%, P < 0.001) were significantly different between the two groups [Supplementary Table S1].



After PSM, there were 154 pairs of patients. The only significant differences between the two groups were blood loss (78 ± 67 vs. 155 ± 107 ml, P < 0.001) and post-surgical hospital stay (10.0 ± 6.5 vs. 12.5 ± 6.2 days, P < 0.001).

Survival

With a median follow-up of 36 months (range: 3–135) in the total cohort (before matching), 11 patients (4.3%) in the OR group and 16 patients (4.0%) in the LR group were lost to follow-up (P = 0.819).

Compared with the OR group in the total cohort, there were better survival outcomes in the LR group for 5-year OS (P = 0.035) and 5-year DFS (P = 0.013); these differences were observed after PSM (P < 0.001 and P < 0.001) [Figure 1]. Subgroup analyses revealed no significant difference between the two groups for Stages I disease (both before and after PSM) for 5-year OS and DFS (all P > 0.05). For Stage II disease, the difference in OS was significant after PSM (P = 0.013) but not before (P = 0.373), just like for DFS (before: P = 0.282; after: P = 0.009). For Stage III disease, the differences in OS and DFS were significant before (OS: P = 0.021; DFS: P = 0.003) and after (OS: P = 0.002; DFS: P = 0.010) PSM [Figure 2] and [Figure 3].
Figure 1: OS and DFS curves of the two groups before (a and c) and after (b and d) PSM. OS: Overall survival, DFS: Disease-free survival, PSM: Propensity score matching

Click here to view
Figure 2: OS curves of the two groups according to cancer stage before (a, c and e) and after (b, d and f) PSM. OS: Overall survival, PSM: Propensity score matching

Click here to view
Figure 3: The DFS curves of the two groups according to cancer stage before (a, c and e) and after (b, d and f) PSM. DFS: Disease free survival, PSM: Propensity score matching

Click here to view


For right-sided colon cancer, the differences in OS were not significant before PSM (P = 0.166) but were significant after PSM (P = 0.005). In contrast, the differences in DFS were significant before (P = 0.007) and after (P = 0.003) PSM. For left-sided colon cancer, the differences in OS and DFS were not significant before PSM (OS: P = 0.104; DFS: P = 0.090) but were significant after PSM (OS: P = 0.005; DFS: P = 0.023). Finally, for rectal cancer, the 5-year OS (P = 0.725) and DFS (P = 0.720) were not significantly different before PSM, but the differences were significant after PSM (P = 0.021 and P = 0.031) [Supplementary Figure S2] and [Figure 4].

Figure 4: The DFS curves of the two groups according to cancer location before (a, c and e) and after (b, d and f) PSM. DFS: Disease free survival, PSM: Propensity score matching

Click here to view


Prognostic factors

The multivariate analysis showed that tumour ≥5 cm (hazard ratio [HR] = 1.750, 95% confidence interval [CI]: 1.026–2.986, P = 0.040), Stage III (HR = 14.092, 95% CI: 1.894–104.848, P = 0.010) and LR (HR = 0.300, 95% CI: 0.160–0.560, P < 0.001) were independently associated with OS. Pre-operative CEA ≥5 ng/ml (HR = 3.954, 95% CI: 1.363–11.473, P = 0.011), Stage III (HR = 6.206, 95% CI: 1.470–26.200, P = 0.013) and LR (HR = 0.341, 95% CI: 0.178–0.653, P = 0.001) were independently associated with DFS [Supplementary Table S2].




  Discussion Top


The incidence of CRC peaks at 74–80 years of age, and patients with a genetic condition have a young onset. Therefore, the prognosis of middle-aged patients with CRC treated by LR is unclear. This study aimed to evaluate the survival outcomes of LR compared with OR for patients with CRC and 45–65 years of age. The results suggest that in middle-aged patients with CRC, LR has better survival outcomes than OR.

In this study of middle-aged patients with CRC, OS and DFS in all patients were better for LR than OR after matching for age, gender, BMI, tumour location, AJCC stage and admission year. LR has become an accepted therapeutic option for CRC patients, providing at least similar OS and DFS compared with OR in Stages I–III disease.[17] Previous studies in patients with CRC (irrespective of age, but most studies included older patients) showed that LR was at least comparable to OR, as shown by two meta-analyses.[4] Chern et al.[17] reported that LR maximised the short-term outcomes compared with OR without comprising the long-term outcomes. Long-term results by Green et al.[18] also support the use of LR for CRC. On the other hand, Cianchi et al.[5] reported that the 5-year cancer-related survival after LR was significantly higher than that after OR, and similar results were reported by Law et al.,[19] both supporting the present study. Park et al.[20] reported similar outcomes between LR and OR in T4 tumours but a tendency for better outcomes with LR in tumours <4 cm. Hence, contradictory results can be observed in the literature. LR is known to minimise the surgical stress and systemic inflammatory response after surgery,[4] which is conducive to reducing complications and improving recovery. Hypotheses have been proposed to explain this beneficial oncological role of LR in the treatment of CRC. One possible reason is that the number of LNs harvested by laparoscopy was higher than by OR,[5] as observed in the present study.

In the present study, LR showed an advantage over OR in Stages II and III after PSM. The present study is supported by Day et al.,[21] who reported 665 resections (457 LR and 208 OR) for CRC, and the 5-year OS for non-Stage IV disease in the LR group was significantly better than in the open group (79.4% vs. 74.0%, P = 0.03).

LR was independently associated with better OS and DFS in the multivariable analyses. These results are supported by studies on elderly patients.[22] In addition, one study suggests that LR achieved similar outcomes among elderly and middle-aged patients with rectal cancer.[23] The present study is supported by the literature because it is known that middle-aged patients have specific risk factors[9] and a better prognosis because of better access to treatments and fewer comorbidities.[10]

In this study, LR showed an advantage over OR in rectal cancer after PSM. In rectal cancer, some studies revealed that LR and OR have similar effects on long-term survival.[24] On the other hand, Nonaka et al.[25] reported that DFS was better in the LR group than in the OR group. Ng et al.[26] reported a trend towards a lower recurrence rate at 10 years after LR than after OR among patients with Stage III rectal cancer (P = 0.078). These points will have to be examined in future studies because the number of rectal cancer patients was small in this study.

The complications were similar between LR and OR in this study, supported by the general principle of LR[4] and by a previous meta-analysis[27] and a cohort study.[28] A recent study showed that LR and OR were safe both in elderly and non-elderly patients.[29] These differences in complications might play a role in the difference in survival. The conversion rate was 2.6%, similar to that of a previous study (2%).[17]

There are some limitations that are inherent to retrospective studies (such as missing data and various biases), but the present study used the PSM approach, which allows for a more robust analysis by reducing confounders,[30] but without completely mitigating all sources of bias of non-randomised studies. This is particularly useful when a randomised controlled trial is impossible due to practical, medical or ethical issues. Moreover, this study was based on a single-institution series, and the generalisability of the results might be limited. Performing a prospective observational study at multiple centers would be needed to confirm the conclusions of this study.


  Conclusions Top


LR in patients with CRC and aged 45–65 years achieves better OS and DFS than OR. Complications are similar, except for less blood loss and shorter post-surgical hospital stay with LR.

Ethics approval

Studies involving human subjects (including research on identifiable human material and data) must have been performed with the appropriate participants' informed consent in compliance with the Helsinki Declaration. This study was approved by the Ethics Committee of Mianyang Central Hospital.

Informed consent

The need for individual consent was waived by the committee because of the retrospective nature of this study.

Data availability statement

All data generated or analysed during this study were included in this manuscript and its supplemental files.

Reporting guidelines

Reporting guidelines for Original Research Articles: STROBE (2007).

Financial support and sponsorship

This work was supported by the Mianyang Technology agency program (17YFHM002) and the research project of the Sichuan Provincial Health Planning Committee (No. 16PJ191). The funder was not involved in the study design, collection, analysis, interpretation of data, the writing of this article or the decision to submit it for publication.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

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Jeong SY, Park JW, Nam BH, Kim S, Kang SB, Lim SB, et al. Open versus laparoscopic surgery for mid-rectal or low-rectal cancer after neoadjuvant chemoradiotherapy (COREAN trial): Survival outcomes of an open-label, non-inferiority, randomised controlled trial. Lancet Oncol 2014;15:767-74.  Back to cited text no. 3
    
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Theophilus M, Platell C, Spilsbury K. Long-term survival following laparoscopic and open colectomy for colon cancer: A meta-analysis of randomized controlled trials. Colorectal Dis 2014;16:O75-81.  Back to cited text no. 4
    
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Cianchi F, Trallori G, Mallardi B, Macrì G, Biagini MR, Lami G, et al. Survival after laparoscopic and open surgery for colon cancer: A comparative, single-institution study. BMC Surg 2015;15:33.  Back to cited text no. 5
    
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Rawla P, Sunkara T, Barsouk A. Epidemiology of colorectal cancer: Incidence, mortality, survival, and risk factors. Prz Gastroenterol 2019;14:89-103.  Back to cited text no. 6
    
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Serra-Rexach JA, Jimenez AB, García-Alhambra MA, Pla R, Vidán M, Rodríguez P, et al. Differences in the therapeutic approach to colorectal cancer in young and elderly patients. Oncologist 2012;17:1277-85.  Back to cited text no. 8
    
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Flood A, Rastogi T, Wirfält E, Mitrou PN, Reedy J, Subar AF, et al. Dietary patterns as identified by factor analysis and colorectal cancer among middle-aged Americans. Am J Clin Nutr 2008;88:176-84.  Back to cited text no. 9
    
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van den Broek CB, Dekker JW, Bastiaannet E, Krijnen P, de Craen AJ, Tollenaar RA, et al. The survival gap between middle-aged and elderly colon cancer patients. Time trends in treatment and survival. Eur J Surg Oncol 2011;37:904-12.  Back to cited text no. 10
    
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Hu Y, Huang C, Sun Y, Su X, Cao H, Hu J, et al. Morbidity and mortality of laparoscopic versus open D2 distal gastrectomy for advanced gastric cancer: A randomized controlled trial. J Clin Oncol 2016;34:1350-7.  Back to cited text no. 11
    
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Watanabe T, Itabashi M, Shimada Y, Tanaka S, Ito Y, Ajioka Y, et al. Japanese Society for Cancer of the Colon and Rectum (JSCCR) Guidelines 2014 for treatment of colorectal cancer. Int J Clin Oncol 2015;20:207-39.  Back to cited text no. 12
    
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Cianchi F, Cortesini C, Trallori G, Messerini L, Novelli L, Comin CE, et al. Adequacy of lymphadenectomy in laparoscopic colorectal cancer surgery: A single-centre, retrospective study. Surg Laparosc Endosc Percutan Tech 2012;22:33-7.  Back to cited text no. 13
    
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Clavien PA, Barkun J, de Oliveira ML, Vauthey JN, Dindo D, Schulick RD, et al. The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg 2009;250:187-96.  Back to cited text no. 15
    
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Ueno H, Mochizuki H, Akagi Y, Kusumi T, Yamada K, Ikegami M, et al. Optimal colorectal cancer staging criteria in TNM classification. J Clin Oncol 2012;30:1519-26.  Back to cited text no. 16
    
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Park SS, Lee JS, Park HC, Park SC, Sohn DK, Oh JH, et al. Favorable short-term oncologic outcomes following laparoscopic surgery for small T4 colon cancer: A multicenter comparative study. World J Surg Oncol 2020;18:299.  Back to cited text no. 20
    
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Nonaka T, Fukuda A, Maekawa K, Nagayoshi S, Tokunaga T, Takatsuki M, et al. Clinical and oncological outcomes of laparoscopic versus open surgery for advanced rectal cancer. Anticancer Res 2016;36:5419-24.  Back to cited text no. 25
    
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Ng SS, Lee JF, Yiu RY, Li JC, Hon SS, Mak TW, et al. Long-term oncologic outcomes of laparoscopic versus open surgery for rectal cancer: A pooled analysis of 3 randomized controlled trials. Ann Surg 2014;259:139-47.  Back to cited text no. 26
    
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Song XJ, Liu ZL, Zeng R, Ye W, Liu CW. A meta-analysis of laparoscopic surgery versus conventional open surgery in the treatment of colorectal cancer. Medicine (Baltimore) 2019;98:e15347.  Back to cited text no. 27
    
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Tunruttanakul S, Chareonsil B, Charernsuk M. Operative outcome of laparoscopic colorectal cancer surgery in a regional hospital in a developing country: A propensity score-matched comparative analysis. Asian J Surg 2021;44:329-33.  Back to cited text no. 28
    
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Ueda Y, Shiraishi N, Kawasaki T, Akagi T, Ninomiya S, Shiroshita H, et al. Short- and long-term outcomes of laparoscopic surgery for colorectal cancer in the elderly aged over 80 years old versus non-elderly: A retrospective cohort study. BMC Geriatr 2020;20:445.  Back to cited text no. 29
    
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Austin PC. An introduction to propensity score methods for reducing the effects of confounding in observational studies. Multivariate Behav Res 2011;46:399-424.  Back to cited text no. 30
    


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