Int J Colorectal Dis DOI 10.1007/s00384-013-1803-9
ORIGINAL ARTICLE
The impact of visceral obesity on surgical outcomes of laparoscopic surgery for colon cancer Jun Watanabe & Kenji Tatsumi & Mitsuyoshi Ota & Yusuke Suwa & Shinsuke Suzuki & Akira Watanabe & Atsushi Ishibe & Kazuteru Watanabe & Hirotoshi Akiyama & Yasushi Ichikawa & Satoshi Morita & Itaru Endo
Accepted: 19 November 2013 # Springer-Verlag Berlin Heidelberg 2013
Abstract Purpose Although obesity is considered as a risk factor for postoperative morbidity in abdominal surgery, its effect on the outcomes of laparoscopic-assisted colectomy (LAC) is still unclear. The technical difficulty and risk factor for postoperative complication in LAC are thought to be influenced by visceral obesity. The aim of this prospective study was to evaluate the impact of visceral fat on the surgical outcomes of LAC. Methods Between April 2005 and December 2010, consecutive patients with preoperatively diagnosed colon cancer, excluding medium and low rectal cancer, who underwent LAC, were enrolled. Their visceral fat area (VFA) and body mass index (BMI) were prospectively collected. The VFA was assessed by Fat Scan software. The patients were classified into two groups as follows: VFA nonobese with VFA 30 kg/m2 is only 2–3 % in the Japanese population. On the other hand, it is 10– 20 % in Europe and the USA [25, 30, 31]. In our study, there were only four patients (1.2 %) with BMI ≧30 kg/m2. Thus, it is not practical to evaluate the influence of BMI >30 kg/m2 on LAC in the population of Japan. However, there are differences in obesity prevalence and body fat distribution between ethnic populations, and Asian population tends to accumulate visceral fat without developing generalized obesity, relative to Caucasians [32]. In general, the percentage of fat volume in Asians is 3–5 % higher than that in Caucasians for the same BMI [33]. Therefore, different cutoff points are needed for different populations. The Steering Committee of the WHO Western Pacific Region has recommended different ranges for the Asia-Pacific region based on risk factors and morbidities. In Asians, the cutoff line for obesity is >25 kg/m2, which is lower than the WHO cutoff line of >30 kg/m2 [32]. Based on this criteria, BMI >25 kg/m2 has been validated in our population by Japan Society for the Study of Obesity [25]. Therefore, we adopted the criteria of BMI ≧25 kg/m2 in this study. Although the BMI is very simple and useful, it does not always reflect the degree of obesity in the visceral cavity because distribution of adipose tissue has large individual differences [17]. In LAC, the essential operation procedure is performed within the abdominal cavity [17]. Therefore, the impact on surgical outcomes of LAC may be influenced by visceral obesity. In the present study, although BMI was used as a predictive factor for postoperative complications and SSI based on a multivariate analysis, there was greater significant difference in VFA than in BMI. Moreover, multivariate analysis showed that the risk factor for the development of anastomotic leakage is only VFA. In colorectal surgery, previous reports have shown that an anastomotic leakage, which is a critical complication, occurs in 1–20 % of patients, and the risk factors for an anastomotic leakage are low-level anastomosis, male gender, smoking, preoperative chemoradiotherapy, and excessive alcohol consumption [34]. Among the previous studies that analyzed the risk factors for anastomotic leakage, there are a few studies that had examined the obesity factor. A Finnish study [35] concluded that obesity is significantly associated with anastomotic leakage (OR 2.32), and a Spanish group [36] also showed that the risk factor of leak is obesity (OR 9). In this study, there was no significant difference in the leakage rate between obese (BMI ≧25 kg/m2) and nonobese (BMI 30 procedures) and was 32.1 % with respect to beginner surgeon (30? A case-matched comparative study with open colectomy. Dis Colon Rectum 48:975–981 15. Dostalík J, Martínek L, Vávra P et al (2005) Laparoscopic colorectal surgery in obese patients. Obes Surg 15:1328–1331 16. Scheidbach H, Benedix F, Hu¨gel O (2008) Laparoscopic approach to colorectal procedures in the obese patient: risk factor or benefit? Obes Surg 18:66–70
17. Bouchard C, Despres JP, Mauriege P (1993) Genetic and nongenetic determinants of regional fat distribution. Endocr Rev 14:72–93 18. Wajchenberg BL (2000) Subcutaneous and visceral adipose tissue: their relation to the metabolic syndrome. Endocr Rev 21:697–738 19. Maurovich-Horvat P, Massaro J, Fox CS et al (2007) Comparison of anthropometric, area- and volume-based assessment of abdominal subcutaneous and visceral adipose tissue volumes using multi-detector computed tomography. Int J Obes (London) 31: 500–506 20. Poirier P, Despres JP (2003) Waist circumference, visceral obesity, and cardiovascular risk. J Cardiopulm Rehabil 23:161–169 21. Pou KM, Massaro JM, Hoffmann U et al (2009) Patterns of abdominal fat distribution: the Framingham Heart Study. Diabetes Care 32: 448–481 22. Seki Y, Ohue M, Sekimoto M et al (2007) Evaluation of the technical difficulty performing laparoscopic resection of a rectosigmoid carcinoma: visceral fat reflects technical difficulty more accurately than body mass index. Surg Endosc 21:929–934 23. Tsujinaka S, Konishi F, Kawamura YJ et al (2008) Visceral obesity predicts surgical outcomes after laparoscopic colectomy for sigmoid colon cancer. Dis Colon Rectum 51:1757–1765 24. Ishii Y, Hasegawa H, Nishibori H et al (2005) Impact of visceral obesity on surgical outcome after laparoscopic surgery for rectal cancer. Br J Surg 92:1261–1262 25. Japan Society for the Study of Obesity (2002) The Examination Committee of Criteria for Obesity Disease in Japan. Circ J 66: 987–992 26. Yoshizumi T, Nakamura T, Yamane M et al (1999) Abdominal Fat: standardized technique for measurement at CT. Radiology 211:283– 286 27. Kunisaki C, Makino H, Takagawa R et al (2009) Predictive factors for surgical complications of laparoscopy-assisted distal gastrectomy for gastric cancer. Surg Endosc 23:2085–2093 28. Miransky J, Ruo L, Nicoletta S et al (2001) Impact of a surgeontrained observer on accuracy of colorectal surgical site infection rates. Dis Colon Rectum 44:1100–1105 29. Konishi T, Watanabe T, Kishimoto J et al (2006) Elective colon and rectal surgery differ in risk factors for wound infection: results of prospective surveillance. Ann Surg 244:758–763 30. Inoue M, Sobue T, Tsugane S et al (2004) Impact of body mass index on the risk of total cancer incidence and mortality among middleaged Japanese: data from a large-scale population-based cohort study—the JPHC study. Cancer Causes Control 15:671–680 31. Yoshiike N, Seino F, Tajima S et al (2002) Twenty-year changes in the prevalence of overweight in Japanese adults: the National Nutrition Survey 1976–95. Obes Rev 3:183–190 32. WHO/IASO/IOTF. (2000) The Asia-Pacific Perspective. Redefining obesity and its treatment. Australia: Health Communications Australia Pty Ltd, (WWW document.) ISBN #0-9577082-1-1. (full document available at: http://www.idi.org.au/obesity_report.htm) 33. Deurenberg P, Deurenberg-Yap M, Guricci S (2002) Asians are different from Caucasians and from each other in their body mass index/body fat per cent relationship. Obes Rev 3:141–146 34. Kelly A, Gendall SR, Ross K et al (2007) The impact of obesity on outcome after major colorectal surgery. Dis Colon Rectum 50:2223– 2237 35. Makela JT, Kiviniemi H, Laitinen S (2003) Risk factors for anastomotic leakage after left-sided colorectal resection with rectal anastomosis. Dis Colon Rectum 46:653–660 36. Biondo S, Pares D, Kreisler E et al (2005) Anastomotic dehiscence after resection and primary anastomosis in left-sided colonic emergencies. Dis Colon Rectum 48:2272–2280 37. Makino T, Shukla PJ, Rubino S et al (2012) The impact of obesity on perioperative outcomes after laparoscopic colorectal resection. Ann Surg 255:228–236
Int J Colorectal Dis 38. Goodpaster BH, Kelley DE, Wing RR et al (1999) Effects of weight loss on regional fat distribution and insulin sensitivity in obesity. Diabetes 48:839–847 39. Ross R, Dagnone D, Jones PJ et al (2000) Reduction in obesity and related comorbid conditions after diet-induced weight loss or exercise-induced weight loss in men. A randomized, controlled trial. Ann Intern Med 133:92–103 40. Cawthorn SJ, Gibbs NM, Marks CG (1986) Clearance technique for the detection of lymph nodes in colorectal cancer. Br J Surg 73:58–60 41. Kim CS, Lee SC, Kim YM et al (2008) Visceral fat accumulation induced by a high-fat diet causes the atrophy of mesenteric lymph nodes in obese mice. Obesity 16:1261–1269 42. Tepper JE, O’Connell MJ, Niedzwiecki D et al (2001) Impact of number of nodes retrieved on outcome in patients with rectal cancer. J Clin Oncol 19:157–163 43. Chang GJ, Rodriguez-Bigas MA, Skibber JM et al (2007) Lymph node evaluation and survival after curative resection of colon cancer: systematic review. J Natl Cancer Inst 99:433–441 44. Ribeiro-Filho FF, Faria AN, Azjen S et al (2003) Methods of estimation of visceral fat: advantages of ultrasonography. Obes Res 11: 1488–1494
45. Sass DA, Schoen RE, Weissfeld JL et al (2004) Relationship of visceral adipose tissue to recurrence of adenomatous polyps. Am J Gastroenterol 99:687–693 46. Park HS, Lee K (2005) Greater beneficial effects of visceral fat reduction compared with subcutaneous fat reduction on parameters of the metabolic syndrome: a study of weight reduction programs in subjects with visceral and subcutaneous obesity. Diabet Med 22:266–272 47. von Eyben FE, Mouritsen E, Holm J et al (2003) Intra-abdominal obesity and metabolic risk factors: a study of young adults. Int J Obes Relat Metab Disord 27:941–949 48. Rossner S, Bo WJ, Hiltbrandt E et al (1990) Adipose tissue determinations in cadavers: a comparison between crosssectional planimetry and computed tomography. Int J Obes 14:893–902 49. Tokunaga K, Matsuzawa Y, Ishikawa K et al (1983) A novel technique for the determination of body fat by computed tomography. Int J Obes 7:437–445 50. Kvist H, Chowdhury B, Sjostrom L et al (1988) Adipose tissue volume determination in males by computed tomography and 40 K. Int J Obes 12:249–266
ORIGINAL ARTICLE
The impact of visceral obesity on surgical outcomes of laparoscopic surgery for colon cancer Jun Watanabe & Kenji Tatsumi & Mitsuyoshi Ota & Yusuke Suwa & Shinsuke Suzuki & Akira Watanabe & Atsushi Ishibe & Kazuteru Watanabe & Hirotoshi Akiyama & Yasushi Ichikawa & Satoshi Morita & Itaru Endo
Accepted: 19 November 2013 # Springer-Verlag Berlin Heidelberg 2013
Abstract Purpose Although obesity is considered as a risk factor for postoperative morbidity in abdominal surgery, its effect on the outcomes of laparoscopic-assisted colectomy (LAC) is still unclear. The technical difficulty and risk factor for postoperative complication in LAC are thought to be influenced by visceral obesity. The aim of this prospective study was to evaluate the impact of visceral fat on the surgical outcomes of LAC. Methods Between April 2005 and December 2010, consecutive patients with preoperatively diagnosed colon cancer, excluding medium and low rectal cancer, who underwent LAC, were enrolled. Their visceral fat area (VFA) and body mass index (BMI) were prospectively collected. The VFA was assessed by Fat Scan software. The patients were classified into two groups as follows: VFA nonobese with VFA 30 kg/m2 is only 2–3 % in the Japanese population. On the other hand, it is 10– 20 % in Europe and the USA [25, 30, 31]. In our study, there were only four patients (1.2 %) with BMI ≧30 kg/m2. Thus, it is not practical to evaluate the influence of BMI >30 kg/m2 on LAC in the population of Japan. However, there are differences in obesity prevalence and body fat distribution between ethnic populations, and Asian population tends to accumulate visceral fat without developing generalized obesity, relative to Caucasians [32]. In general, the percentage of fat volume in Asians is 3–5 % higher than that in Caucasians for the same BMI [33]. Therefore, different cutoff points are needed for different populations. The Steering Committee of the WHO Western Pacific Region has recommended different ranges for the Asia-Pacific region based on risk factors and morbidities. In Asians, the cutoff line for obesity is >25 kg/m2, which is lower than the WHO cutoff line of >30 kg/m2 [32]. Based on this criteria, BMI >25 kg/m2 has been validated in our population by Japan Society for the Study of Obesity [25]. Therefore, we adopted the criteria of BMI ≧25 kg/m2 in this study. Although the BMI is very simple and useful, it does not always reflect the degree of obesity in the visceral cavity because distribution of adipose tissue has large individual differences [17]. In LAC, the essential operation procedure is performed within the abdominal cavity [17]. Therefore, the impact on surgical outcomes of LAC may be influenced by visceral obesity. In the present study, although BMI was used as a predictive factor for postoperative complications and SSI based on a multivariate analysis, there was greater significant difference in VFA than in BMI. Moreover, multivariate analysis showed that the risk factor for the development of anastomotic leakage is only VFA. In colorectal surgery, previous reports have shown that an anastomotic leakage, which is a critical complication, occurs in 1–20 % of patients, and the risk factors for an anastomotic leakage are low-level anastomosis, male gender, smoking, preoperative chemoradiotherapy, and excessive alcohol consumption [34]. Among the previous studies that analyzed the risk factors for anastomotic leakage, there are a few studies that had examined the obesity factor. A Finnish study [35] concluded that obesity is significantly associated with anastomotic leakage (OR 2.32), and a Spanish group [36] also showed that the risk factor of leak is obesity (OR 9). In this study, there was no significant difference in the leakage rate between obese (BMI ≧25 kg/m2) and nonobese (BMI 30 procedures) and was 32.1 % with respect to beginner surgeon (30? A case-matched comparative study with open colectomy. Dis Colon Rectum 48:975–981 15. Dostalík J, Martínek L, Vávra P et al (2005) Laparoscopic colorectal surgery in obese patients. Obes Surg 15:1328–1331 16. Scheidbach H, Benedix F, Hu¨gel O (2008) Laparoscopic approach to colorectal procedures in the obese patient: risk factor or benefit? Obes Surg 18:66–70
17. Bouchard C, Despres JP, Mauriege P (1993) Genetic and nongenetic determinants of regional fat distribution. Endocr Rev 14:72–93 18. Wajchenberg BL (2000) Subcutaneous and visceral adipose tissue: their relation to the metabolic syndrome. Endocr Rev 21:697–738 19. Maurovich-Horvat P, Massaro J, Fox CS et al (2007) Comparison of anthropometric, area- and volume-based assessment of abdominal subcutaneous and visceral adipose tissue volumes using multi-detector computed tomography. Int J Obes (London) 31: 500–506 20. Poirier P, Despres JP (2003) Waist circumference, visceral obesity, and cardiovascular risk. J Cardiopulm Rehabil 23:161–169 21. Pou KM, Massaro JM, Hoffmann U et al (2009) Patterns of abdominal fat distribution: the Framingham Heart Study. Diabetes Care 32: 448–481 22. Seki Y, Ohue M, Sekimoto M et al (2007) Evaluation of the technical difficulty performing laparoscopic resection of a rectosigmoid carcinoma: visceral fat reflects technical difficulty more accurately than body mass index. Surg Endosc 21:929–934 23. Tsujinaka S, Konishi F, Kawamura YJ et al (2008) Visceral obesity predicts surgical outcomes after laparoscopic colectomy for sigmoid colon cancer. Dis Colon Rectum 51:1757–1765 24. Ishii Y, Hasegawa H, Nishibori H et al (2005) Impact of visceral obesity on surgical outcome after laparoscopic surgery for rectal cancer. Br J Surg 92:1261–1262 25. Japan Society for the Study of Obesity (2002) The Examination Committee of Criteria for Obesity Disease in Japan. Circ J 66: 987–992 26. Yoshizumi T, Nakamura T, Yamane M et al (1999) Abdominal Fat: standardized technique for measurement at CT. Radiology 211:283– 286 27. Kunisaki C, Makino H, Takagawa R et al (2009) Predictive factors for surgical complications of laparoscopy-assisted distal gastrectomy for gastric cancer. Surg Endosc 23:2085–2093 28. Miransky J, Ruo L, Nicoletta S et al (2001) Impact of a surgeontrained observer on accuracy of colorectal surgical site infection rates. Dis Colon Rectum 44:1100–1105 29. Konishi T, Watanabe T, Kishimoto J et al (2006) Elective colon and rectal surgery differ in risk factors for wound infection: results of prospective surveillance. Ann Surg 244:758–763 30. Inoue M, Sobue T, Tsugane S et al (2004) Impact of body mass index on the risk of total cancer incidence and mortality among middleaged Japanese: data from a large-scale population-based cohort study—the JPHC study. Cancer Causes Control 15:671–680 31. Yoshiike N, Seino F, Tajima S et al (2002) Twenty-year changes in the prevalence of overweight in Japanese adults: the National Nutrition Survey 1976–95. Obes Rev 3:183–190 32. WHO/IASO/IOTF. (2000) The Asia-Pacific Perspective. Redefining obesity and its treatment. Australia: Health Communications Australia Pty Ltd, (WWW document.) ISBN #0-9577082-1-1. (full document available at: http://www.idi.org.au/obesity_report.htm) 33. Deurenberg P, Deurenberg-Yap M, Guricci S (2002) Asians are different from Caucasians and from each other in their body mass index/body fat per cent relationship. Obes Rev 3:141–146 34. Kelly A, Gendall SR, Ross K et al (2007) The impact of obesity on outcome after major colorectal surgery. Dis Colon Rectum 50:2223– 2237 35. Makela JT, Kiviniemi H, Laitinen S (2003) Risk factors for anastomotic leakage after left-sided colorectal resection with rectal anastomosis. Dis Colon Rectum 46:653–660 36. Biondo S, Pares D, Kreisler E et al (2005) Anastomotic dehiscence after resection and primary anastomosis in left-sided colonic emergencies. Dis Colon Rectum 48:2272–2280 37. Makino T, Shukla PJ, Rubino S et al (2012) The impact of obesity on perioperative outcomes after laparoscopic colorectal resection. Ann Surg 255:228–236
Int J Colorectal Dis 38. Goodpaster BH, Kelley DE, Wing RR et al (1999) Effects of weight loss on regional fat distribution and insulin sensitivity in obesity. Diabetes 48:839–847 39. Ross R, Dagnone D, Jones PJ et al (2000) Reduction in obesity and related comorbid conditions after diet-induced weight loss or exercise-induced weight loss in men. A randomized, controlled trial. Ann Intern Med 133:92–103 40. Cawthorn SJ, Gibbs NM, Marks CG (1986) Clearance technique for the detection of lymph nodes in colorectal cancer. Br J Surg 73:58–60 41. Kim CS, Lee SC, Kim YM et al (2008) Visceral fat accumulation induced by a high-fat diet causes the atrophy of mesenteric lymph nodes in obese mice. Obesity 16:1261–1269 42. Tepper JE, O’Connell MJ, Niedzwiecki D et al (2001) Impact of number of nodes retrieved on outcome in patients with rectal cancer. J Clin Oncol 19:157–163 43. Chang GJ, Rodriguez-Bigas MA, Skibber JM et al (2007) Lymph node evaluation and survival after curative resection of colon cancer: systematic review. J Natl Cancer Inst 99:433–441 44. Ribeiro-Filho FF, Faria AN, Azjen S et al (2003) Methods of estimation of visceral fat: advantages of ultrasonography. Obes Res 11: 1488–1494
45. Sass DA, Schoen RE, Weissfeld JL et al (2004) Relationship of visceral adipose tissue to recurrence of adenomatous polyps. Am J Gastroenterol 99:687–693 46. Park HS, Lee K (2005) Greater beneficial effects of visceral fat reduction compared with subcutaneous fat reduction on parameters of the metabolic syndrome: a study of weight reduction programs in subjects with visceral and subcutaneous obesity. Diabet Med 22:266–272 47. von Eyben FE, Mouritsen E, Holm J et al (2003) Intra-abdominal obesity and metabolic risk factors: a study of young adults. Int J Obes Relat Metab Disord 27:941–949 48. Rossner S, Bo WJ, Hiltbrandt E et al (1990) Adipose tissue determinations in cadavers: a comparison between crosssectional planimetry and computed tomography. Int J Obes 14:893–902 49. Tokunaga K, Matsuzawa Y, Ishikawa K et al (1983) A novel technique for the determination of body fat by computed tomography. Int J Obes 7:437–445 50. Kvist H, Chowdhury B, Sjostrom L et al (1988) Adipose tissue volume determination in males by computed tomography and 40 K. Int J Obes 12:249–266
