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 ¤  Abstract
 ¤ Introduction
 ¤ Patients and Methods
 ¤ Results
 ¤ Discussion
 ¤ Conclusion
 ¤  References
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 Table of Contents     
Year : 2018  |  Volume : 14  |  Issue : 2  |  Page : 134-139

Outcomes according to body mass index following laparoscopic surgery in patients with colorectal cancer

1 Department of Surgery, Chonnam National University Hospital, Gwangju, Korea
2 Department of Surgery, Korea University Anam Hospital, Seoul, Korea

Date of Submission06-Apr-2017
Date of Acceptance03-Jul-2017
Date of Web Publication12-Mar-2018

Correspondence Address:
Prof. Seon-Hahn Kim
73, Inchon-ro, Seongbuk-gu, Seoul 02841
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jmas.JMAS_68_17

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 ¤ Abstract 

Purpose: Body mass index (BMI) may not be appropriate for different populations. Therefore, the World Health Organization (WHO) suggested 25 kg/m2 as a measure of obesity for Asian populations. The purpose of this report was to compare the oncologic outcomes of laparoscopic colorectal resection with BMI classified from the WHO Asia-Pacific perspective.
Patients and Methods: All patients underwent laparoscopic colorectal resection from September 2006 to March 2015 at a tertiary referral hospital. A total of 2408 patients were included and classified into four groups: underweight (n = 112, BMI <18.5 kg/m2), normal (n = 886, 18.5–22.9 kg/m2), pre-obese (n = 655, 23–24.9 kg/m2) and obese (n = 755, >25 kg/m2). Perioperative parameters and oncologic outcomes were analysed amongst groups.
Results: Conversion rate was the highest in the underweight group (2.7%, P < 0.001), whereas the obese group had the fewest harvested lymph nodes (21.7, P < 0.001). Comparing oncologic outcomes except Stage IV, the underweight group was lowest for overall (P = 0.007) and cancer-specific survival (P = 0.002). The underweight group had the lowest proportion of national health insurance but the highest rate of medical care (P = 0.012).
Conclusion: The obese group had the fewest harvested lymph nodes, whereas the underweight group had the highest estimated blood loss, conversion rate to open approaches and the poorest overall and cancer-specific survivals.

Keywords: Asian population, body mass index, colorectal cancer, laparoscopy, short- and long-term outcomes

How to cite this article:
Kwak HD, Ju JK, Kang DW, Baek SJ, Kwak JM, Kim J, Kim SH. Outcomes according to body mass index following laparoscopic surgery in patients with colorectal cancer. J Min Access Surg 2018;14:134-9

How to cite this URL:
Kwak HD, Ju JK, Kang DW, Baek SJ, Kwak JM, Kim J, Kim SH. Outcomes according to body mass index following laparoscopic surgery in patients with colorectal cancer. J Min Access Surg [serial online] 2018 [cited 2021 Sep 29];14:134-9. Available from:

 ¤ Introduction Top

Body mass index (BMI) is a universal parameter derived from the weight and height of an individual. It is easily calculated as weight in kilogrammes divided by square of height in metres and has high specificity. According to BMI, people with obesity have increased risk of diseases such as type 2 diabetes, hypertension, heart attack and hyperlipidaemia, which can cause poor surgical outcomes.[1] Obesity in adulthood is also associated with short life expectancy and is a predictor of mortality at old ages.[2] However, the impact of being underweight is not well known or only for external causes such as increased risk of dying.[3]

The criteria for classifying obesity using BMI are reported to possibly not be appropriate for different populations. Risks of even low BMI can be increased in Asians who are diagnosed with visceral or abdominal obesity. Therefore, the World Health Organization (WHO) redefined obesity as 25 kg/m2 for Asia-Pacific populations in 2000.[4] In 2004, WHO Expert Consultation also proposed a BMI cut-off of 23 kg/m2 for determining public health and clinical action in Asia.[5] The outcomes of this new standard and its oncologic outcomes have not been reported, especially for low BMI patients.

Therefore, this study was designed to compare short- and long-term outcomes of underweight, normal range, pre-obese and obese patients using BMI for Asians following laparoscopic resection for colorectal cancer.

 ¤ Patients and Methods Top

A total 2640 patients underwent laparoscopic R0 resection for colorectal cancer from September 2006 to March 2015 at a tertiary referral hospital. Data were collected prospectively and analysed retrospectively.

Perioperative parameters and oncologic outcomes were analysed according to four groups using the WHO Asia-Pacific perspective:[4] under 18.5 kg/m2 as the underweight group, between 18.5 and 22.9 kg/m2 as the normal range group, 23–24.9 kg/m2 as the pre-obese group and over 25 kg/m2 as the obese group. Open conversion cases were included to analyse whether it was due to obesity. A total of 2408 patients were included and classified as the underweight (n = 112), normal range (n = 886), pre-obese (n = 655) and obese (n = 755). All surgeries were performed by two senior colorectal surgeons with extensive laparoscopic experience.

Post-operative complications and mortality were defined as complications or death occurring within 30 days following surgery or during hospitalisation. Oncologic outcomes were measured as recurrence (local and distant metastasis), overall survival and cancer-specific survival. Recurrence was defined as a recurrent lesion detected by radiologic, clinical, intraoperative or pathologic method.

Statistical analyses

Differences between groups were estimated with one-way analysis of variance, Kruskal–Wallis test for continuous data and linear-by-linear association for categorical data. Probability of recurrence and survival was estimated by Kaplan–Meier curve analysis with the exception of Stage IV. Statistical analyses used SPSS (IBM, SPSS Statistics, Version 20, Armonk, NY, USA). P < 0.05 was considered statistically significant.

 ¤ Results Top

From our colorectal database of 2408 patients, there were 1477 (61.3%) men and 931 women (38.7%) with a mean age of 61.9 years. Mean BMI for total patients was 23.6 kg/m2. No significant differences were observed between groups in age, sex, cancer location and pre-operative CEA as pre-operative parameters. Although the proportion of diabetes mellitus did not show significant differences, the rate of hypertension increased with BMI (P< 0.001) [Table 1].
Table 1: Demographics and characteristics

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By analysis of operative outcomes, the underweight group had higher estimated blood loss than the other groups (P = 0.019). Conversion rate was the highest in the underweight group (2.7%, P < 0.001). Causes of conversion from minimally invasive surgery to an open conversion were bulky tumours such as T4 cancers (0.7%, 17 of 2408) with or without obstruction, fatty obesity (n = 4, 0.2%), adhesions from previous operations (n = 3, 0.1%), uncontrolled bleeding (n = 3, 0.1%) and poor visualisation resulting from instrument or assistant error (n = 17, 0.7%) [Table 2].
Table 2: Operative outcomes

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The obese group had the fewest harvested lymph nodes (mean 21.7, P < 0.001). No significant differences were seen in post-operative complications or length of post-operative hospital stay. There were also no differences in TNM staging, adjuvant chemotherapy and radiation therapy [Table 3].
Table 3: Post-operative outcomes

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Comparison of oncologic outcomes except for Stage IV showed that median follow-up was 34–37 months. The underweight group had the highest recurrence rate (29.5%, P = 0.050), the poorest overall survival (P = 0.007) and cancer-specific survival (P = 0.002) [Table 4] and [Figure 1].
Table 4: Long-term outcomes except Stage IV (n=2082)

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Figure 1: Kaplan–Meier curves of recurrence-free survival, overall survival and cancer-specific survival classified by obesity status

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Analysis of poor oncologic outcomes showed no significant differences in occupation or educated level of the patients. However, the underweight group had the lowest proportion of national health insurance and the highest medical care (P = 0.012) [Table 5].
Table 5: Socioeconomic status except Stage IV

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 ¤ Discussion Top

Analysis using the new BMI classification from the WHO Asia-Pacific perspective for Asians showed hypertension increased with BMI, and a group of obese patients had a longer operative duration and fewer harvested lymph nodes than other groups. The underweight group had higher estimated blood loss during the surgery and also higher conversion rate than other groups. The underweight group had the poorest long-term outcomes for overall survival and cancer-specific survival, which might be linked to their health insurance.

The impact of obesity on short-term outcomes was first introduced in 2000.[6] Since then, relevant discussions have included cross-ethnic population studies for Asians in China, Hong Kong, India, Japan, Korea, Malaysia and Singapore.[5],[7],[8] A Japanese study investigated the influence of obesity on short-term and long-term outcomes after laparoscopic colonic surgery in 2014. However, the BMI criteria for obesity were 30 kg/m2.[9] Due to inaccurate results, several studies from Japan used visceral obesity as a parameter instead of BMI. Ishii et al. showed visceral obesity (odds ratio 1.0, 95% confidence interval: 1.2–84.5, P = 0.035) as an independent risk factor along with low rectal cancer and smoking.[10] Tsujinaka et al. concluded that visceral fat area is a more useful standard than BMI for patients over 25 kg/m2.[11] A prospective, randomised trial of oncologic outcomes associated with BMI and colorectal cancer showed that only obese women (BMI >30 kg/m2) had worse overall mortality but had no significant difference in recurrence.[12] The effect of adjuvant chemotherapy on BMI for colon cancer is controversial. Patients with BMI over 35 kg/m2 experienced increased risk of recurrence and death though they received adjuvant chemotherapy for colon cancer.[13] However, increased BMI during adjuvant chemotherapy was not related to a high recurrence of death in a cohort study of Stage III colon cancer.[14]

Our results showed that the underweight, not the obese group, had the lowest overall and cancer-specific survival compared to other groups. A study showed that underweight patients (BMI <20 kg/m2) with colon cancer had increased mortality although the study concluded that the cause of death was not related to cancer,[15] which phenomenon had been introduced in the previous year as the obesity paradox.[16] Roh et al.[3] reported that only external causes such as frailty, alcohol or drug abuse increase the risk of dying for underweight individuals in a census-linked cohort of 21,578 individuals with up to 32 years of follow-up. Studies of Western[17] and Eastern[18] populations on whether underweight can be a risk factor for death have not clearly been explained and is still a matter of debate.

Health seems to result from a mixture of biological, environmental and behavioural factors rather than from a single cause. However, recently, sociological papers have found that socioeconomic status has a strong relationship with health, even when controlling for economic resources and access to healthcare.[19] Although income and employment were not exactly analysed in this study, a review article from Japan showed a positive relationship between educational and occupational class and health.[20] Therefore, a reasonable hypothesis is that, in this study, the poorest outcomes in the underweight group might have been linked to socioeconomic status.

The rate of open conversion cases was extremely low (1.8%, 43 of 2408), but the underweight group had the highest conversion rate (2.7%, P < 0.001) in this study. The main factor which caused the highest conversion rate in the underweight group was bleeding during the surgery, which also related with the highest estimated blood loss in the underweight group. However, statistical differences appear to be due to very low incidence rates in this study. The relationship between BMI and conversion rate is also a matter of debate. A prospective study from Germany showed no significance in conversion rate based on BMI (7.3% in the obese vs. 9.5% in the non-obese group, P > 0.05).[21] However, a study from 2002 on stability with high BMI using laparoscopy for colorectal cancer showed higher conversion rate (39 vs. 13.5%, P = 0.01) in the obese group.[22] Their consecutive results also showed a higher conversion rate (23.7 vs. 10.9%, no P value provided).[23]

Although we showed that fewer lymph nodes were harvested from patients in the pre-obese and obese groups than other groups, other studies found no significant difference between non-obese and obese groups.[24],[25],[26] A Japanese case-matched study analysing 152 patients also reported that the median number of harvested lymph nodes was not affected by obesity (high vs. low BMI, 17 vs. 17, P = 0.97).[9] In the area of gastric resection, Dhar et al.[27] in a study on 787 patients showed that significantly fewer lymph nodes were removed following D2 (high vs. low BMI, 21 vs. 28, P = 0.002) and D3 (31 vs. 37, P = 0.023) dissections.

This study has several limitations. First, it was a retrospective study of prospectively collected data. Therefore, important parameters might have been missed in the analysis. The design may also have led to selection bias despite the use of prospectively collected data. Second, the number of patients in the normal range was one-third (36.8%) of the study population, whereas obesity was 31.4% (755 of 2408 patients). These percentages were comparable or higher than Western populations.[6],[23] Pre-operative BMI might not reflect weight loss or malnutrition in patients who received neoadjuvant or adjuvant treatment. Third, the collected data for an analysis of socioeconomic status had limitations; patients' incomes or property and states of employment were not collected. Therefore, mean age over 65 just marked as retirement or unemployed state.

 ¤ Conclusion Top

The obese group had the fewest harvested lymph nodes, whereas the underweight group had the highest estimated blood loss, conversion rate to open approaches and the poorest overall and cancer-specific survivals.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

 ¤ References Top

Prasad US, Walker WS, Sang CT, Campanella C, Cameron EW. Influence of obesity on the early and long term results of surgery for coronary artery disease. Eur J Cardiothorac Surg 1991;5:67-72.  Back to cited text no. 1
Peeters A, Barendregt JJ, Willekens F, Mackenbach JP, Al Mamun A, Bonneux L, et al. Obesity in adulthood and its consequences for life expectancy: A life-table analysis. Ann Intern Med 2003;138:24-32.  Back to cited text no. 2
Roh L, Braun J, Chiolero A, Bopp M, Rohrmann S, Faeh D, et al. Mortality risk associated with underweight: A census-linked cohort of 31,578 individuals with up to 32 years of follow-up. BMC Public Health 2014;14:371.  Back to cited text no. 3
WHO, IOTF. The Asia-Pacific Perspective. Redefining Obesity and Its Treatment. Obesity: Preventing and Managing the Global Epidemic. Geneva: WHO; 2000.  Back to cited text no. 4
WHO Expert Consultation. Appropriate body-mass index for asian populations and its implications for policy and intervention strategies. Lancet 2004;363:157-63.  Back to cited text no. 5
Benoist S, Panis Y, Alves A, Valleur P. Impact of obesity on surgical outcomes after colorectal resection. Am J Surg 2000;179:275-81.  Back to cited text no. 6
James WP, Chunming C, Inoue S. Appropriate asian body mass indices? Obes Rev 2002;3:139.  Back to cited text no. 7
Deurenberg P, Deurenberg-Yap M. Validity of body composition methods across ethnic population groups. Acta Diabetol 2003;40 Suppl 1:S246-9.  Back to cited text no. 8
Makino T, Trencheva K, Shukla PJ, Rubino F, Zhuo C, Pavoor RS, 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;156:661-8.  Back to cited text no. 9
Ishii Y, Hasegawa H, Nishibori H, Watanabe M, Kitajima M. Impact of visceral obesity on surgical outcome after laparoscopic surgery for rectal cancer. Br J Surg 2005;92:1261-2.  Back to cited text no. 10
Tsujinaka S, Konishi F, Kawamura YJ, Saito M, Tajima N, Tanaka O, et al. Visceral obesity predicts surgical outcomes after laparoscopic colectomy for sigmoid colon cancer. Dis Colon Rectum 2008;51:1757-65.  Back to cited text no. 11
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Dignam JJ, Polite BN, Yothers G, Raich P, Colangelo L, O'Connell MJ, et al. Body mass index and outcomes in patients who receive adjuvant chemotherapy for colon cancer. J Natl Cancer Inst 2006;98:1647-54.  Back to cited text no. 13
Meyerhardt JA, Niedzwiecki D, Hollis D, Saltz LB, Mayer RJ, Nelson H, et al. Impact of body mass index and weight change after treatment on cancer recurrence and survival in patients with stage III colon cancer: Findings from Cancer and Leukemia Group B 89803. J Clin Oncol 2008;26:4109-15.  Back to cited text no. 14
Sinicrope FA, Foster NR, Sargent DJ, O'Connell MJ, Rankin C. Obesity is an independent prognostic variable in colon cancer survivors. Clin Cancer Res 2010;16:1884-93.  Back to cited text no. 15
Mullen JT, Moorman DW, Davenport DL. The obesity paradox: Body mass index and outcomes in patients undergoing nonbariatric general surgery. Ann Surg 2009;250:166-72.  Back to cited text no. 16
Ajani UA, Lotufo PA, Gaziano JM, Lee IM, Spelsberg A, Buring JE, et al. Body mass index and mortality among US male physicians. Ann Epidemiol 2004;14:731-9.  Back to cited text no. 17
Jee SH, Sull JW, Park J, Lee SY, Ohrr H, Guallar E, et al. Body-mass index and mortality in korean men and women. N Engl J Med 2006;355:779-87.  Back to cited text no. 18
Wilkinson R, Pickett K, Cato MS. The Spirit Level: Why More Equal Societies Almost Always Do Better. London: Penguin; 2009.  Back to cited text no. 19
Kagamimori S, Gaina A, Nasermoaddeli A. Socioeconomic status and health in the japanese population. Soc Sci Med 2009;68:2152-60.  Back to cited text no. 20
Schwandner O, Farke S, Schiedeck TH, Bruch HP. Laparoscopic colorectal surgery in obese and nonobese patients: Do differences in body mass indices lead to different outcomes? Surg Endosc 2004;18:1452-6.  Back to cited text no. 21
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Leroy J, Ananian P, Rubino F, Claudon B, Mutter D, Marescaux J, et al. The impact of obesity on technical feasibility and postoperative outcomes of laparoscopic left colectomy. Ann Surg 2005;241:69-76.  Back to cited text no. 24
Bège T, Lelong B, Francon D, Turrini O, Guiramand J, Delpero JR, et al. Impact of obesity on short-term results of laparoscopic rectal cancer resection. Surg Endosc 2009;23:1460-4.  Back to cited text no. 25
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Dhar DK, Kubota H, Tachibana M, Kotoh T, Tabara H, Masunaga R, et al. Body mass index determines the success of lymph node dissection and predicts the outcome of gastric carcinoma patients. Oncology 2000;59:18-23.  Back to cited text no. 27


  [Figure 1]

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


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