J Minim Invasive Surg 2016; 19(4): 148-155  https://doi.org/10.7602/jmis.2016.19.4.148
Long-term Oncologic Outcomes of Obesity after Laparoscopic Surgery for Colorectal Cancer in Asian Patients
Jung Hak Kwak1, Ji Won Park1,2,3, Byung Kwan Park1, Eon Chul Han1, Jeong-Ki Kim1, Yoon-Hye Kwon1, Seung-Bum Ryoo1, Seung-Yong Jeong1,2,3, and Kyu Joo Park1,3
1Department of Surgery, Seoul National University College of Medicine, Seoul, Korea,
2Cancer Research Institute, Seoul National University, Seoul, Korea,
3Colorectal Cancer Center, Seoul National University Cancer Hospital, Seoul, Korea
Correspondence to: Ji Won Park, Colorectal Cancer Center, Seoul National University Cancer Hospital, 101 Daehak-ro, Yeongeon-dong, Jongno-gu, Seoul 03080, Korea Tel: +82-2-2072-2325 Fax: +82-2-766-3975 E-mail: sowisdom@gmail.com
Received: August 22, 2016; Revised: October 24, 2016; Accepted: October 24, 2016; Published online: December 15, 2016.
© Journal of Minimally Invasive Surgery. All rights reserved.

cc This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Abstract

Purpose:

The adverse effects of obesity on short-term surgical outcomes after laparoscopic colorectal surgery have been reported. However, the influence of obesity on long-term oncological outcomes after laparoscopic surgery in Asian patients has not been well understood. The aim of this study was to evaluate the effect of obesity on long-term oncologic outcomes in patients who underwent laparoscopic surgery for colorectal cancer.

Methods:

Overall, 424 consecutive patients who underwent laparoscopic resection for colorectal cancer between January 2005 and July 2012 were included in this retrospective study. Patients were classified as non-obese (body mass index [BMI] <25.0 kg/m2) and obese (BMI ≥25.0 kg/m2) according to the categories proposed by the International Obesity Task Force. A survival analysis was performed using clinicopathologic characteristics, including obesity.

Results:

Of the 424 patients, 325 (76.7%) were classified as non-obese and 99 (23.3%) as obese. The clinicopathologic characteristics of the obese and non-obese groups were similar, except that there were more underlying comorbidities, a lower frequency of smoking, and fewer tumors in rectum in the obese group. Results of the multivariate analysis showed that older age, elevated serum carcinoembryonic antigen, high-grade histology, advanced tumor stage, and perineural invasion were associated with poorer disease-free survival and overall survival. Obesity was not significantly associated with disease-free survival (hazard ratio [HR], 1.196; 95% confidence interval [CI], 0.686~2.086; p=0.528) or overall survival (HR, 1.156; 95% CI, 0.584~2.289; p=0.677).

Conclusion:

Laparoscopic surgery for colorectal cancer seems to be safe and feasible for obese patients in terms of long-term oncologic outcomes.

Keywords: Obesity, Body mass index, Laparoscopic surgery, Colorectal cancer
INTRODUCTION

As obesity is a growing public health concern, numerous studies have been conducted to evaluate its effects on surgical outcomes. It has been suggested to be a risk factor that contributes to adverse surgical outcomes, including longer hospital stays, longer operative times, higher conversion rates, and wound complications.1-3 Furthermore, obesity has been suggested to be a risk factor for wound infections and dehiscence, incisional hernias, stoma complications, obstructions, strictures, and anastomotic leaks.4-6

In Korea, the prevalence of obesity has increased from 26.9% (in 1998) to 32.0% (in 2011), according to the Korea National Health and Nutrition Examination Survey reports.7 Considering the increasing population of obese patients, there is a need for an approach that maintains the inherent benefits of minimally invasive surgery while improving outcomes for the obese after colorectal surgery.4 Regarding long-term oncologic outcomes, several studies have revealed that the long-term outcomes of laparoscopic surgery for colorectal cancer in obese Western patients were similar to those in non-obese patients.6 However, there are differences among ethnic populations in obesity prevalence and body fat distributions. To date, little is known about the long-term outcomes of laparoscopic colorectal surgery with respect to obesity in Asians.

The aim of this study was to compare long-term outcomes between obese and non-obese Asian patients who underwent laparoscopic surgery for colorectal cancer.

MATERIALS AND METHODS

A total of 424 consecutive patients who underwent laparoscopic resection for colorectal cancer between January 2005 and July 2012 at Seoul National University Hospital were included in this study. The medical records of these patients were reviewed retrospectively. The collected data included clinicopathologic variables and surgical outcomes. The clinicopathologic data included age, sex, body mass index (BMI), social history, history of abdominal surgeries, presence of comorbidities, American Society of Anesthesiologists (ASA) score, tumor location, and carcinoembryonic antigen (CEA) level; these were reviewed and compared with pathologic results. Surgical outcomes included conversion rates, intraoperative events, operative time, length of the postoperative hospital stay, recurrence, overall survival, and disease-free survival. This study was approved by the Institutional Review Board of the Seoul National University Hospital. Patients were divided into an obese group and a non-obese group on the basis of their BMI, in accordance with the categories proposed by the World Health Organization’s International Obesity Task Force (BMI <25 kg/m2, non-obese; BMI ≥25 kg/m2, obese).7

Laparoscopic colorectal surgery was performed as a standardized procedure. Generally, five trocars were inserted, as follows: one 11-mm, two or three 5-mm, and one or two 12-mm trocars. An 11-mm umbilical trocar was used as the camera port using a 30° angled scope. Ligation of the vessel and mobilization of the colon or rectum was performed laparoscopically. The specimen was extracted through an extended incision of the port in the lower left quadrant, umbilicus, or perineum. In the case of anterior resection or low anterior resection, anastomosis was performed extracorporeally with a circular stapler. In the case of right or left colectomy, anastomosis was performed extracorporeally with two linear staplers.

All patients underwent a postoperative follow-up examination every 3 or 6 months for the first 5 years and every year thereafter that comprised a physical examination, serum CEA measurements, chest radiographs, and abdominal and pelvic computed tomographic scanning. Colonofibroscopic examinations were performed every 1 or 2 years after surgery. Overall survival was defined as the time from surgery to death from any cause. Disease-free survival was defined as the time from surgery to a recurrence or death from any cause.

Data are presented as the number of patients and percentages or as means with standard deviations. Depending on the nature of the data, the chi-squared test, Fisher’s exact test, Student’s t-test, or Mann-Whitney U-test was used for comparisons. A survival comparison was performed using the log-rank test of the Kaplan-Meier analysis. A multivariable analysis of survival outcomes was performed with a Cox regression analysis. Statistical analysis was performed using SPSS software, version 19.0 (SPSS, Chicago, IL). A two-tailed p value <0.05 was the criterion for statistical significance.

RESULTS

Among the 424 patients, 325 (76.7%) were classified as non-obese and 99 (23.3%) were classified as obese. The clinicopathological characteristics of patients according to their obesity statuses are presented in Table 1. There were no significant differences in clinicopathological characteristics between groups, with the exception of the presence of comorbid diseases, smoking history, and location of the tumor. The obese group had more comorbid diseases, a lower frequency of smoking, and a lower prevalence of colonic tumors than did the non-obese group.

Clinicopathological characteristics of patients

Characteristics Non-obese, no. (%)  Obese, no. (%) p value 
No. of patients325 (76.7)99 (23.3)
Age0.338
 <65 years177 (54.5)50 (50.5)
 ≥65 years148 (45.5)49 (49.5)
Gender0.376
 Male200 (61.5)56 (56.6)
 Female125 (38.5)43 (43.4)
ASA ≥311 (3.4)0 (0.0)0.075
Presence of comorbid disease128 (39.4)56 (56.6)0.003
Smoking history45 (13.8)5 (5.1)0.018
Alcohol history84 (25.8)21 (21.2)0.350
Location0.042
 Colon186 (57.2)68 (68.7)
 Rectum139 (42.8)31 (31.3)
Elevated serum CEA (≥5 ng/ml)37 (11.5)11 (11.3)0.967
Conversion to open13 (4.0)1 (1.0)0.204
Number of tumor ≥26 (1.8)2 (2.0)0.911
Histologic grade0.407
 Low grade312 (96.0)93 (93.9)
 High grade13 (4.0)6 (6.1)
TNM stage0.346
 I116 (35.7)26 (26.3)
 II90 (27.7)29 (29.3)
 III109 (33.5)40 (40.4)
 IV10 (3.1)4 (4.0)
Harvested LN19.5±9.918.9±9.70.647
Angiolymphatic invasion65 (20.0)24 (24.2)0.364
Venous invasion25 (7.7)5 (5.1)0.369
Perineural invasion48 (14.8)10 (10.1)0.237
Adjuvant treatment186 (57.2)65 (65.7)0.135
Follow-up duration (month)45.7±19.548.4±17.40.205

ASA = American Society of Anesthesiologist; CEA = carcinoembryogenic antigen; LN = lymph node.


In terms of short-term outcomes, the conversion rates, operative times, transfusion rates, and complication rates were not significantly different between the obese and non-obese groups (Table 2). The length of hospitalization was shorter and the estimated blood loss was greater in the obese group than in the non-obese group.

Short-term outcomes in non-obese and obese groups

Characteristics Non-obese, no. (%)  Obese, no. (%)p value 
No. of patients325 (76.7)99 (23.3)
Conversion to open16 (4.9)2 (2.0)0.210
Operative time (minutes) 167.9±65.6175.2±81.20.361
Transfusion12 (3.7)4 (4.0)0.874
Hospital stay (days)9.0±7.97.7±2.20.007
Complication86 (26.5)24 (24.2)0.659
EBL (ml)123.2±131.1158.3±143.10.045

EBL = Estimated blood loss.


The mean follow-up duration for patients was 46.3±19.1 (range: 0.6~97.7) months. Table 3 shows the results of the analysis of the risk factors for disease-free survival. In the univariate analysis, older age, elevated serum CEA level, high-grade histology, advanced Tumor-Node-Metastasis (TNM) stage, lymphovascular invasion, venous invasion, and perineural invasion were associated with poor disease-free survival. In the multivariable analysis, age, serum CEA level, histologic grade, TNM stage, and perineural invasion were independent significant risk factors for disease-free survival. In the univariate analysis for overall survival, older age, high ASA score, elevated serum CEA level, high-grade histology, advanced TNM stage, lymphovascular invasion, venous invasion, and perineural invasion were associated with poor overall survival (Table 4). In the multivariable analysis, age, ASA, serum CEA level, histologic grade, TNM stage, and perineural invasion were independent significant risk factors for overall survival.

Univariate and multivariable analysis for disease free survival

CharacteristicsUnivariateMultivariable analysis


 5YR-DFSR (%) p value HR95% CIp value 
Age0.0180.047
 <65 years82.21
 ≥65 years76.21.627 1.006~2.630 
Gender0.281
 Male80.0
 Female83.5
ASA0.112
 1, 281.7
 ≥368.6
BMI0.6940.528
 Non-obese81.11
 Obese82.11.1960.686~2.086
Presence of comorbidities0.205
 No83.9
 Yes77.7
Tumor location0.196
 Colon83.2
 Rectum78.7
Secum CEA level0.0010.005
 <5 ng/ml83.31
 ≥5 ng/ml64.72.3301.299~4.178
Adjuvant treatment0.072
 No87.5
 Yes77.5
Number of tumor0.460
 Single 81.3
 Multiple 80.0
Histologic grade<0.001<0.001
 Low grade83.21
 High grade39.13.8081.802~8.047
TNM stage<0.0010.027
 I92.61
 II85.61.3860.628~3.060
 III72.82.0670.995~4.290
 IV28.64.2431.565~11.506
Number of Harvested LN0.639
 <1280.7
 ≥1281.4
Lymphovascular invasion<0.0010.099
 No86.01
 Yes64.31.5780.918~2.714
Venous invasion0.0020.877
 No83.11
 Yes59.10.9430.449~1.981
Perineural invasion<0.0010.006
 No86.01
 Yes53.42.2361.263~3.958

Univariate and multivariable analysis for overall survival

CharacteristicsUnivariateMultivariable analysis


 5YR-OSR (%) p value HR95% CIp value 
Age0.0020.003
 <65 years90.91
 ≥65 years82.2 2.536  1.379~4.662 
Gender0.352
 Male86.2
 Female88.3
ASA0.0100.012
 1, 287.51
 ≥368.65.0461.426~17.860
BMI0.7440.677
 Non-obese87.01
 Obese87.31.1560.584~2.289
Presence of comorbidities0.179
 No89.9
 Yes82.6
Tumor location0.585
 Colon88.4
 Rectum84.9
Secum CEA level0.0030.013
 <5 ng/ml88.41
 ≥5 ng/ml75.92.4481.208~4.962
Adjuvant treatment0.946
 No89.2
 Yes86.2
Number of tumor0.143
 Single87.2
 Multiple80.0
Histologic grade<0.001<0.001
 Low grade88.81
 High grade42.74.9572.044~12.018
TNM stage<0.0010.033
 I94.81
 II90.00.9790.372~2.576
 III82.31.5620.646~3.779
 IV42.94.6871.426~15.409
Number of Harvested LN0.759
 <1290.3
 ≥1286.0
Lymphovascular invasion0.0010.374
 No90.81
 Yes73.51.3600.691~2.678
Venous invasion0.0130.868
 No88.11
 Yes73.01.0800.434~2.685
Perineural invasion<0.0010.019
 No90.11
 Yes68.92.4291.157~5.102

Importantly, in the univariate analysis, obesity was not significantly associated with disease-free survival (5-year disease-free survival, 81.1% in the non-obese group versus 82.1% in the obese group; p=0.694; Fig. 1) or with overall survival (5-year overall survival, 87.0% in the non-obese group versus 87.3% in the obese group; p=0.744; Fig. 2). In the multivariable analysis, obesity was also not a significant risk factor for disease-free survival (hazard ratio, 1.196; 95% confidence interval, 0.686~2.086; p=0.528) or overall survival (hazard ratio, 1.156; 95% confidence interval, 0.584~2.289; P=0.677).

Fig. 1.

Disease-free survival graph according to obesity (p value=0.694).


Fig. 2.

Overall survival graph according to obesity (p value=0.744).


DISCUSSION

This study showed no significant differences between obese and non-obese patients in long-term survival after laparoscopic colorectal cancer surgery. In terms of short-term outcomes, several studies have shown that obese patients have unfavorable surgical outcomes, such as longer operative times, increased conversion rates, increased postoperative complication rates, and prolonged hospital stays.1-3 These unfavorable short-term outcomes may affect long-term outcomes for obese patients with colorectal cancer. However, some studies in Western patients showed that long-term outcomes for obese patients were not different from those for non-obese patients.3,5,6,8 The present study in Asians showed similar results. Thus, considering the results for long-term survival, laparoscopic colorectal surgery appears to be acceptable for obese Asians.

In Asia, lifestyle and dietary changes have resulted in increased rates of obesity, as more Western-style eating habits are now favored.7 During the last decade, the overall prevalence of obesity has also increased in Korea.7 With this trend, the penetration rates for laparoscopic resection for colorectal cancer have increased in Korea.9 Thus, a greater number of obese patients could undergo laparoscopic surgery for colorectal cancer. The evaluation of outcomes following laparoscopic colorectal cancer surgery in obese patients is therefore urgently required.

A recent systematic review and meta-analysis reported that approximately 20% of all malignancies were associated with obesity.10 Mortality associated with cancer in obese patients has increased to 24% with the worldwide increased prevalence of obesity over time.11 Published data have shown that obesity and overweight are the cause of about 20% of deaths from cancer in women, while the rate is around 14% in men.12 The mechanisms underlying the association between obesity and cancer are not fully understood. A high BMI is known to be a risk factor that increases insulin resistance, hyperinsulinemia, and free insulin-like growth factor (IGF)-I.13 Chronic hyperinsulinemia is associated with decreased concentrations of IGF-binding protein-1 and -2, which increase free IGF-I with concomitant changes in the cellular environment that favor tumor formation.14,15 Likewise, obesity itself may affect outcomes following cancer. In addition, tumor resection can be difficult in obese patients. Obstacles to performing laparoscopic surgery in obese patients include difficulties in obtaining an adequate operative field and difficulties in the intra-abdominal maneuvering of instruments in a restricted working area.2,16 These difficulties may also affect oncologic outcomes following colorectal cancer. However, this study showed no adverse effect of obesity on survival following laparoscopic colorectal cancer surgery.

BMI has been broadly used as an index to show a patient’s degree of obesity.17 We used the cut-off value (25 kg/m2) suggested by the International Obesity Task Force.7 The cut-off value in Asian countries is different from that in Western countries (30 kg/m2). This study included only a small number of patients with morbid obesity (30 kg/m2) according to the Asian criteria. The outcomes of morbidly obese patients should be evaluated in a larger multi-center study that includes more morbidly obese patients. Another index for obesity is visceral adiposity. Visceral adiposity is assessed based on the amount of fat evident on abdominal computed tomography or based on waist circumference. Visceral adiposity may more accurately indicate the status of obesity than BMI can. Future studies using visceral obesity are required.

Multiple studies have shown an association between obesity and colorectal cancer. Obesity has been shown to increase the risk of developing colorectal cancer almost 2-fold, with insulin and insulin-like growth factor (IGF) postulated as important mediators in the oncogenic process. However, recent reports suggest that there is insufficient evidence of a strong association between obesity and survival in colorectal cancer.18-20 Therefore, it is unclear whether long-term surgical outcomes are adversely affected by obesity, because there have been many conflicting reports.

Recently, as obesity has become an important issue with respect to outcomes following colorectal cancer surgery, several studies have reported the effects of obesity on surgical outcomes. Obesity has been associated with poor short-term outcomes following laparoscopic colorectal surgery, including longer hospital stays, longer operative times, higher conversion rates, and wound complications. However, obesity was not associated with adverse short-term outcomes in this study, except with respect to estimated blood loss. This discrepancy may be related to differences in the definition of obesity used in the studies.

In a previous study, a greater number of metastatic regional lymph nodes was found in obese patients than in patients with normal weight. These findings suggest that obesity is an adverse prognostic variable in colorectal cancer surgery.19,21 However, several studies have shown that there were no significant differences in survival between obese and non-obese Western patients.5,22 To our knowledge, few studies have examined long-term surgical outcomes following laparoscopic colorectal cancer in Asian patients. The results of this study showed no significant differences in disease-free and overall survival between obese and non-obese patients in Asian countries.

In this study, obese patients had more comorbidities than non-obese patients did. This heterogeneity could be a confounder. To evaluate the main effects of obesity on survival, we performed a multivariable analysis that included comorbidities. After adjusting for other significant factors, including comorbidities, obesity was not a significant prognostic factor (disease-free survival: HR, 0.742; 95% CI, 0.422~1.306; p=0.301; overall survival: HR, 0.792; 95% CI, 0.398~1.575; p=0.506). In the present study, long-term outcomes did not differ between obese and non-obese patients after adjustment for comorbidities. Limitations of the study include its retrospective design and that it included data only from a single institution. Large multicenter studies will provide more definite conclusions. This study may be useful by providing baseline data for further studies.

If information regarding patient obesity is obtained before surgery, it may be useful to develop a strategy to use laparoscopic colorectal cancer surgery. With sufficient experience, laparoscopic colorectal cancer surgery in obese patients may be feasible in terms of long-term survival. Colorectal surgeons should be aware of obesity-related challenges in these patients.

In conclusion, laparoscopic surgery for colorectal cancer in obese Asian patients seems to be safe and feasible based on long-term oncologic outcomes.

ACKNOWLEDGMENTS

This research was partly supported by a grant from the National R&D Program for Cancer Control, Ministry for Health and Welfare, Republic of Korea (grant number 10515608) and partly supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT & Future Planning, Republic of Korea (grant number 2015008884). The authors thank Amanda for the English editing of the manuscript.

References
  1. Mustain WC, Davenport DL, Hourigan JS, and Vargas HD. Obesity and laparoscopic colectomy: outcomes from the ACS-NSQIP database. Dis Colon Rectum 2012;55:429-435.
    Pubmed CrossRef
  2. Park JW, Lim SW, Choi HS, Jeong SY, Oh JH, and Lim SB. The impact of obesity on outcomes of laparoscopic surgery for colorectal cancer in Asians. Surg Endosc 2010;24:1679-1685.
    Pubmed CrossRef
  3. Senagore AJ, Delaney CP, Madboulay K, Brady KM, and Fazio VW. Laparoscopic colectomy in obese and nonobese patients. J Gastrointest Surg 2003;7:558-561.
    CrossRef
  4. Keller DS, Madhoun N, Flores-Gonzalez JR, Ibarra S, Tahilramani R, and Haas EM. Effect of BMI on Short-Term Outcomes with Robotic-Assisted Laparoscopic Surgery: a Case-Matched Study. J Gastrointest Surg 2016;20:488-493.
    Pubmed CrossRef
  5. Makino T, Trencheva K, and Shukla PJ et al. The influence of obesity on short- and long-term outcomes after laparoscopic surgery for colon cancer: a case-matched study of 152 patients. Surgery 2014;156:661-668.
    Pubmed CrossRef
  6. Vignali A, De Nardi P, Ghirardelli L, Di Palo S, and Staudacher C. Short and long-term outcomes of laparoscopic colectomy in obese patients. World J Gastroenterol 2013;19:7405-7411.
    Pubmed KoreaMed CrossRef
  7. Kim CS, Ko SH, and Kwon HS et al. Prevalence, awareness, and management of obesity in Korea: data from the Korea national health and nutrition examination survey (1998-2011). Diabetes Metab J 2014;38:35-43.
    Pubmed KoreaMed CrossRef
  8. Pikarsky AJ, Saida Y, and Yamaguchi T et al. Is obesity a high-risk factor for laparoscopic colorectal surgery?. Surg Endosc 2002;16:855-858.
    Pubmed CrossRef
  9. Park SJ, Lee KY, and Lee SH. Laparoscopic Surgery for Colorectal Cancer in Korea: Nationwide Data from 2008~2013. J Minim Invasive Surg 2015;18:39-43.
    CrossRef
  10. De Pergola G, and Silvestris F. Obesity as a major risk factor for cancer. J Obes 2013;2013:291546.
    Pubmed KoreaMed CrossRef
  11. Jaggers JR, Sui X, and Hooker SP et al. Metabolic syndrome and risk of cancer mortality in men. Eur J Cancer 2009;45:1831-1838.
    Pubmed KoreaMed CrossRef
  12. Calle EE, Rodriguez C, Walker-Thurmond K, and Thun MJ. Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N Engl J Med 2003;348:1625-1638.
    Pubmed CrossRef
  13. Giovannucci E. Insulin, insulin-like growth factors and colon cancer: a review of the evidence. J Nutr 2001;131:3109s-3120s.
    Pubmed
  14. Renehan AG, Frystyk J, and Flyvbjerg A. Obesity and cancer risk: the role of the insulin-IGF axis. Trends Endocrinol Metab 2006;17:328-336.
    Pubmed CrossRef
  15. Renehan AG, Tyson M, Egger M, Heller RF, and Zwahlen M. Body-mass index and incidence of cancer: a systematic review and meta-analysis of prospective observational studies. Lancet 2008;371:569-578.
    CrossRef
  16. Lascano CA, Kaidar-Person O, Szomstein S, Rosenthal R, and Wexner SD. Challenges of laparoscopic colectomy in the obese patient: a review. Am J Surg 2006;192:357-365.
    Pubmed CrossRef
  17. WHO Expert Consultation. Appropriate body-mass index for Asian populations and its implications for policy and intervention strategies. Lancet 2004;363:157-163.
    CrossRef
  18. Parkin E, O’Reilly DA, Sherlock DJ, Manoharan P, and Renehan AG. Excess adiposity and survival in patients with colorectal cancer: a systematic review. Obes Rev 2014;15:434-451.
    Pubmed CrossRef
  19. Sinicrope FA, Foster NR, Sargent DJ, O’Connell MJ, and Rankin C. Obesity is an independent prognostic variable in colon cancer survivors. Clin Cancer Res 2010;16:1884-1893.
    Pubmed KoreaMed CrossRef
  20. Moore LL, Bradlee ML, and Singer MR et al. BMI and waist circumference as predictors of lifetime colon cancer risk in Framingham Study adults. Int J Obes Relat Metab Disord 2004;28:559-567.
    Pubmed CrossRef
  21. Greene FL, Stewart AK, and Norton HJ. A new TNM staging strategy for node-positive (stage III) colon cancer: an analysis of 50,042 patients. Ann Surg 2002;236:416-421.
    Pubmed KoreaMed CrossRef
  22. Singh A, Muthukumarasamy G, Pawa N, Riaz AA, Hendricks JB, and Motson RW. Laparoscopic colorectal cancer surgery in obese patients. Colorectal Dis 2011;13:878-883.
    Pubmed CrossRef


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