Volume 2(2); Pages: 240-246, 2022 | DOI: 10.21873/cdp.10100

Distance of Peritoneum to Inferior Mesenteric Artery Predicts the Operation Time During Laparoscopic Colectomy for Sigmoid or Rectosigmoid Colon Cancer

TAKAFUMI SAEKI, YASUNORI OTOWA, YUTA YAMAZAKI, KEISUKE ARAI, TAKASHI SHIMIZU, YASUHIKO MII, KEITARO KAKINOKI, SHIGETERU OKA, TETSU NAKAMURA, DAISUKE KURODA

Abstract

Background/Aim: Obesity is a major technical limiting factor for laparoscopic surgery because abundant visceral fat is known to extend the operation time. However, special hardware is needed to assess it. We hypothesized that the depth from the peritoneum to the bifurcation of the inferior mesenteric artery (IMA) defined as ‘peritoneum to IMA distance (PID)’ might be a simple predictive factor for extended operation time during laparoscopic colectomy. Patients and Methods: One hundred twenty-four patients who were diagnosed with sigmoid or rectosigmoid colon cancer and underwent laparoscopic colectomy were included. The patients were divided into two groups based on the operation time (210 min). The vertical distance from the peritoneum to the bifurcation of the inferior mesenteric artery was defined as PID. The factors eliciting an operation time longer than 210 min were investigated. Results: There was significant difference in sex, BMI, cT, cN, and PID between the Early group (210 min) and Late group (≥210 min). Less blood loss was observed in the Early group than in the Late group. Multivariate analysis showed that PID was the only independent factor that affected operation time (p0.001). Conclusion: PID predicts the operation time during laparoscopic colectomy for sigmoid or rectosigmoid colon cancer.

Colorectal cancer (CRC) is one of the most common malignancies (1). Among CRC, sigmoid colon cancer and rectosigmoid cancer are the most frequently operated diseases in Japan (2, 3). Several studies have reported that laparoscopic surgery has benefits in short-term outcomes over open surgery with comparable long-term outcomes (2, 4-7). Therefore, laparoscopic surgery is now more often performed. However, obesity is a major technical limiting factor for laparoscopic surgery because abundant visceral fat is known to extend the operation time (8, 9). Furthermore, it is clear that extended operation time is correlated with higher complications (10, 11).

The body mass index (BMI) is used as a simple measure tool to assess obesity. Several studies have shown that BMI is correlated with extended operation time and complications, while others did not (12-15). This is because no clear distinction was made between subcutaneous fat from visceral fat (16, 17). Some studies showed that visceral fat area (VFA) is more strongly associated with postoperative morbidity than BMI (16-19). Recent studies have utilized quantitative computed tomography (CT) to determine visceral obesity by measuring VFA; however, special hardware is needed to assess it (16, 17).

Preoperative contrast-enhanced CT (CECT) is performed generally to determine the stage of the tumor and to check the running pattern of the blood vessel. Goto et al. reported that the depth from the skin to the bifurcation of the celiac artery measured by CECT is more strongly associated with operation time during laparoscopic distal gastrectomy than BMI (20). Here, we hypothesized that the depth from the peritoneum to the bifurcation of the inferior mesenteric artery (IMA) defined as ‘peritoneum to IMA distance (PID)’ might better associate with extended operation time and surgical difficulty than BMI as in the previous study. Therefore, this study aimed to clarify the usefulness of measuring PID as a simple predictive factor for extended operation time during laparoscopic colectomy in patients with sigmoid or rectosigmoid colon cancer.

Patients and Methods

Patients. During December 2013 to December 2019, 134 patients diagnosed with sigmoid or rectosigmoid colon cancer underwent laparoscopic colectomy at the Kita-Harima Medical Center, Japan. Among the 134 patients, 10 patients were excluded: two patients were converted to laparotomy and eight patients had a resection of another major organ. A total of 124 patients who underwent laparoscopic colectomy were ultimately included (Figure 1). Of these patients, 56 patients were treated by surgeons who were board certified by the Japanese Society of Endoscopic Surgery (JSES). This system was established in 2004 to maintain quality and educate trainers by the JSES (21, 22). To be a qualified surgeon of the JSES, an applicant is required to perform more than 20 laparoscopic major organ surgeries within 3 years. The applicant is also required to submit a non-edited video of these surgeries for review by at least two board-qualified referees.

Figure 1. Consort flow diagram of the study.

In this retrospective study, the Union for International Cancer Control TNM staging system was used for staging (23). The lymph node stations and tumor locations were defined using the Japanese Society for Cancer of the Colon and Rectum (JSCCR) (24). The clinical, surgical, and pathological records of the patients were obtained from our database and individual electronic medical records. Postoperative complications were graded according to the Clavien–Dindo classification, and cases with a classification higher than grade II were defined as having a postoperative complication. The data collection and analysis were approved by the Institutional Review Board of the Kita-Harima Medical Center (03-22).　

Surgical technique. Laparoscopic colectomy was performed using five trocars. The first 12-mm trocar was inserted transumbilically and the 12-mm port was placed in the lower right abdomen, and a 5 mm port was placed in upper side of both abdomen and lower left abdomen. The carbon dioxide pneumoperitoneum was maintained at 10 mmHg, and the patients were positioned on the operating table with the lithotomy position and head-right downed. Lymph node dissection was performed using an ultrasonically activated device through the trocars. The definition of D3 lymph node dissection was consistent with the JSCCR guidelines (24). Laparoscopic coagulation system was used in all cases. For the anastomosis technique, we selected Double Stapling Technique or functional end to end anastomosis according to the tumor location.

Definition of the depth of the inferior mesenteric artery from the peritoneum surface. We reviewed the preoperative CECT images of all patients and identified the peritoneum surface and the IMA bifurcation using the axial view. In all cases, we determined cancer stage using CECT in the supine position. The vertical distance from the peritoneum to the bifurcation from the aorta was defined as ‘peritoneum to IMA distance (PID)’ (Figure 2).

Figure 2. Findings of enhanced computed tomography and fat around inferior mesenteric artery in thin (A, B) and obese (C, D) patients.

Statistical analysis. Statistical analysis was carried out using the EZR software. The relation between two variables was assessed using the Fisher exact test or chi-squared test and Student’s T-test or Mann–Whitney U-test. Variables with a p-value 0.05 in a univariate analysis were further evaluated in a multivariate analysis using the logistic regression model to assess the confounding variables. The optimal cut-off level of PID and thickness of subcutaneous fat (TSF) was determined by receiver operating characteristics (ROC) analysis. In all analyses, a p0.05 was accepted as statistically significant.

Results

The median (range) operation time was 213.5 (117-460) minutes. So, we classified patients into two groups according to the operation time: Early group (210 min) and Late group (≥210 min). Patient characteristics are summarized in Table I. Higher rate of female sex and lower BMI were observed in the Early group than in the Late group (p=0.002 and p=0.021, respectively). Also, lower cT and cN stage were observed in the Early group than in the Late group (p=0.013 and p=0.022, respectively). PID was 46.9 mm in the Early group and 56.5 mm in the Late group (p=0.001).

Surgical outcomes are summarized in Table II. Significantly less blood loss was observed in the Early group than in the Late group (p=0.001). There was a trend of less left mobilization and more qualified surgeon operating in the Early group than in the Late group, although the difference was not significant. Postoperative complications were similar between the two groups.

We further examined factors that affected the operation time. The optimal cut-off levels and area under the curve (AUC) of PID and TSF were determined by ROC curve and were 54.5 mm (AUC 0.696) and 14.1 mm (AUC 0.549), respectively (Figure 3A and B). Univariate analyses showed that sex, cT, cN, and PID affected operation time. Multivariate analysis showed that PID was the only independent factor that affected operation time (p0.001) (Table III). Several studies showed that technical proficiency level would affect the operation time (25, 26). Therefore, we examined whether factors affecting the operation time differed between operator’s skill. Table IV and Table V show the results regarding the factors affecting the operation time for non-qualified surgeon and qualified surgeon, respectively. PID was the factor affecting the operation time in both non-qualified and qualified surgeon (p=0.032 and p=0.007, respectively).

Figure 3. Receiver operating characteristics curve of peritoneum to IMA distance for an operation time longer than 210 min.

Discussion

We showed that PID was a favorable factor predicting operation time. Obesity is known to prolong the operation time, and BMI is often used to define obesity (27). However, abdominal shape is sexually dimorphic. Men accumulate more visceral fat whereas women accumulate more subcutaneous fat (28). Several studies showed that abundant subcutaneous fat is not associated with higher complications whereas abundant visceral fat is strongly associated with it (19, 29, 30). Also, Goto et al. showed that TSF did not reflect the operation time which was similar to our results. The results of these studies suggest that subcutaneous fat does not affect the difficulty of the operation. Therefore, BMI does not always reflect the difficulty and operation time.

There are several benefits of predicting the operation time using PID. First, it will help predict the difficulty of the operation (31). Surgical difficulty is known to relate with anastomotic leakage (32). Thus, it would be safer for difficult cases to be operated by skilled surgeons. Second, long operation times may cause surgeons to lose concentration, experience fatigue, and increase the number of intraoperative errors (33, 34). Taking short breaks during surgery is known to preserve performance without prolonging the operation time (35, 36). Therefore, surgeons can prevent excessive fatigue by taking breaks whenever the operation is thought to be long. Third, no special instruments are needed to measure the distance. Generally, CT is taken before the operation to determine the stage of the tumor, whether operation is appropriate, and to check the running pattern of the blood vessel. PID can be measured by using this CT, while special software is needed to assess VFA (16, 17). Last, PID can be applied by all surgeons despite the skill. We showed that PID was a factor affecting the operation time in both non-qualified and qualified surgeons.

In this study, qualified surgeons had a trend of shorter operation time than non-qualified surgeons (205 min vs. 226 min, p=0.083) and there was no difference in patient characteristics between qualified and non-qualified surgeon (data not shown). However, operation by qualified surgeon was not a factor affecting the operation time among all cases. This might be because a qualified surgeon always attends laparoscopic colectomy at our hospital. Several studies showed that novice surgeons can maintain surgical quality under supervision by senior surgeons. Among these studies, Langhoff et al. reported that the operation time was similar when operated by either senior or novice surgeons (37). Also, Ichikawa et al. showed that non-qualified surgeon’s operation time reached plateau at the 18th case of laparoscopic colectomy (38). We therefore believe that quality of surgery was maintained by the attendance of a qualified surgeon and this was the reason qualified surgeon was not a factor affecting the operation time among all cases.

There are several limitations for this study. This is a retrospective study at a single institution, so the sample size is small. In addition, we could not measure VFA, since we did not have the hardware to assess it. Therefore, we still do not know whether PID correlates with VFA. Further studies are necessary to clarify this point.

In conclusion, PID is a simple factor that can predict the operation time despite the skills of the surgeon. PID longer than 54.5 mm is a risk of prolonged operation time over 210 min.

Conflicts of Interest

All Authors have no conflicts of interest to declare in relation to this study.

Authors’ Contributions

All Authors performed surgery and perioperative management on the patients. Takafumi Saeki, Yasunori Otowa and Keitaro Kakinoki conceived the study. Takafumi Saeki, Yuta Yamzaki and Takashi Shimizu collected data. Takafumi Saeki, Keisuke Arai and Yasuhiko Mii performed the data analysis. Takafumi Saeki and Yasunori Otowa wrote the manuscript. Shigeteru Oka, Tetsu Nakamura and Daisuke Kuroda revised the manuscript. All Authors approved the final version of the article.

References

1. Siegel RL, Miller KD and Jemal A: Cancer statistics, 2020. CA Cancer J Clin 70(1): 7-30, 2020. PMID: 31912902. DOI: 10.3322/caac.21590
2. Kitano S, Inomata M, Mizusawa J, Katayama H, Watanabe M, Yamamoto S, Ito M, Saito S, Fujii S, Konishi F, Saida Y, Hasegawa H, Akagi T, Sugihara K, Yamaguchi T, Masaki T, Fukunaga Y, Murata K, Okajima M, Moriya Y and Shimada Y: Survival outcomes following laparoscopic versus open D3 dissection for stage II or III colon cancer (JCOG0404): a phase 3, randomised controlled trial. Lancet Gastroenterol Hepatol 2(4): 261-268, 2017. PMID: 28404155. DOI: 10.1016/S2468-1253(16)30207-2
3. Miyamoto K, Wakabayashi M, Mizusawa J, Nakamura K, Katayama H, Higashi T, Inomata M, Kitano S, Fujita S, Kanemitsu Y and Fukuda H: Evaluation of the representativeness and generalizability of Japanese clinical trials for localized rectal/colon cancer: Comparing participants in the Japan Clinical Oncology Group study with patients in Japanese registries. Eur J Surg Oncol 46(9): 1642-1648, 2020. PMID: 32340817. DOI: 10.1016/j.ejso.2020.04.005
4. Green BL, Marshall HC, Collinson F, Quirke P, Guillou P, Jayne DG and Brown JM: Long-term follow-up of the Medical Research Council CLASICC trial of conventional versus laparoscopically assisted resection in colorectal cancer. Br J Surg 100(1): 75-82, 2013. PMID: 23132548. DOI: 10.1002/bjs.8945
5. Veldkamp R, Kuhry E, Hop WC, Jeekel J, Kazemier G, Bonjer HJ, Haglind E, Påhlman L, Cuesta MA, Msika S, Morino M, Lacy AM and COlon cancer Laparoscopic or Open Resection Study Group (COLOR): Laparoscopic surgery versus open surgery for colon cancer: short-term outcomes of a randomised trial. Lancet Oncol 6(7): 477-484, 2005. PMID: 15992696. DOI: 10.1016/S1470-2045(05)70221-7
6. Colon Cancer Laparoscopic or Open Resection Study Group, Buunen M, Veldkamp R, Hop WC, Kuhry E, Jeekel J, Haglind E, Påhlman L, Cuesta MA, Msika S, Morino M, Lacy A and Bonjer HJ: Survival after laparoscopic surgery versus open surgery for colon cancer: long-term outcome of a randomised clinical trial. Lancet Oncol 10(1): 44-52, 2009. PMID: 19071061. DOI: 10.1016/S1470-2045(08)70310-3
7. Jayne DG, Thorpe HC, Copeland J, Quirke P, Brown JM and Guillou PJ: Five-year follow-up of the Medical Research Council CLASICC trial of laparoscopically assisted versus open surgery for colorectal cancer. Br J Surg 97(11): 1638-1645, 2010. PMID: 20629110. DOI: 10.1002/bjs.7160
8. Hourigan JS: Impact of obesity on surgical site infection in colon and rectal surgery. Clin Colon Rectal Surg 24(4): 283-290, 2011. PMID: 23204944. DOI: 10.1055/s-0031-1295691
9. Senagore AJ, Delaney CP, Madboulay K, Brady KM and Fazio VW: Laparoscopic colectomy in obese and nonobese patients. J Gastrointest Surg 7(4): 558-561, 2003. PMID: 12763416. DOI: 10.1016/s1091-255x(02)00124-5
10. Telem DA, Chin EH, Nguyen SQ and Divino CM: Risk factors for anastomotic leak following colorectal surgery: a case-control study. Arch Surg 145(4): 371-6; discussion 376, 2010. PMID: 20404288. DOI: 10.1001/archsurg.2010.40
11. Kingham TP and Pachter HL: Colonic anastomotic leak: risk factors, diagnosis, and treatment. J Am Coll Surg 208(2): 269-278, 2009. PMID: 19228539. DOI: 10.1016/j.jamcollsurg.2008.10.015
12. Makino T, Trencheva K, Shukla PJ, Rubino F, Zhuo C, Pavoor RS and Milsom JW: The influence of obesity on short- and long-term outcomes after laparoscopic surgery for colon cancer: a case-matched study of 152 patients. Surgery 156(3): 661-668, 2014. PMID: 24947645. DOI: 10.1016/j.surg.2014.03.023
13. Mustain WC, Davenport DL, Hourigan JS and Vargas HD: Obesity and laparoscopic colectomy: outcomes from the ACS-NSQIP database. Dis Colon Rectum 55(4): 429-435, 2012. PMID: 22426267. DOI: 10.1097/DCR.0b013e31823dfb17
14. Leroy J, Ananian P, Rubino F, Claudon B, Mutter D and Marescaux J: The impact of obesity on technical feasibility and postoperative outcomes of laparoscopic left colectomy. Ann Surg 241(1): 69-76, 2005. PMID: 15621993. DOI: 10.1097/
    sla.0000150168.59592.b9
15. Singh A, Muthukumarasamy G, Pawa N, Riaz AA, Hendricks JB and Motson RW: Laparoscopic colorectal cancer surgery in obese patients. Colorectal Dis 13(8): 878-883, 2011. PMID: 20553315. DOI: 10.1111/j.1463-1318.2010.02348.x
16. Cakir H, Heus C, van der Ploeg TJ and Houdijk AP: Visceral obesity determined by CT scan and outcomes after colorectal surgery; a systematic review and meta-analysis. Int J Colorectal Dis 30(7): 875-882, 2015. PMID: 25772271. DOI: 10.1007/s00384-015-2174-1
17. Ozoya OO, Siegel EM, Srikumar T, Bloomer AM, DeRenzis A and Shibata D: Quantitative assessment of visceral obesity and postoperative colon cancer outcomes. J Gastrointest Surg 21(3): 534-542, 2017. PMID: 28101721. DOI: 10.1007/s11605-017-3362-9
18. Tanaka K, Miyashiro I, Yano M, Kishi K, Motoori M, Seki Y, Noura S, Ohue M, Yamada T, Ohigashi H and Ishikawa O: Accumulation of excess visceral fat is a risk factor for pancreatic fistula formation after total gastrectomy. Ann Surg Oncol 16(6): 1520-1525, 2009. PMID: 19267237. DOI: 10.1245/s10434-009-0391-y
19. Tokunaga M, Hiki N, Fukunaga T, Ogura T, Miyata S and Yamaguchi T: Effect of individual fat areas on early surgical outcomes after open gastrectomy for gastric cancer. Br J Surg 96(5): 496-500, 2009. PMID: 19358176. DOI: 10.1002/bjs.6586
20. Goto H, Kanaji S, Yasuda T, Oshikiri T, Yamamoto M, Matsuda T, Nakamura T, Suzuki S, Fujino Y, Tominaga M and Kakeji Y: The depth from the skin to the celiac artery measured using computed tomography is a simple predictive index for longer operation time during laparoscopic distal gastrectomy. World J Surg 42(4): 1065-1072, 2018. PMID: 29018909. DOI: 10.1007/s00268-017-4282-2
21. Kimura T, Mori T, Konishi F and Kitajima M: Endoscopic surgical skill qualification system in Japan: Five years of experience in the gastrointestinal field. Asian Journal of Endoscopic Surgery 3(2): 66-70, 2021. DOI: 10.1111/j.1758-5910.2009.00034.x
22. Mori T, Kimura T and Kitajima M: Skill accreditation system for laparoscopic gastroenterologic surgeons in Japan. Minim Invasive Ther Allied Technol 19(1): 18-23, 2010. PMID: 20095893. DOI: 10.3109/13645700903492969
23. Brierley JD, Gospodarowicz MK and Wittekind C: TNM Classification of Malignant Tumours, 8th Edition. Hoboken, Wiley-Blackwell, 2016.
24. Japanese Society for Cancer of the Colon and Rectum: Japanese classification of colorectal, appendiceal, and anal carcinoma: the 3d English edition [secondary publication]. J Anus Rectum Colon 3(4): 175-195, 2019. PMID: 31768468. DOI: 10.23922/jarc.2019-018
25. Akagi T, Endo H, Inomata M, Yamamoto H, Mori T, Kojima K, Kuroyanagi H, Sakai Y, Nakajima K, Shiroshita H, Etoh T, Saida Y, Yamamoto S, Hasegawa H, Ueno H, Kakeji Y, Miyata H, Kitagawa Y and Watanabe M: Clinical impact of Endoscopic Surgical Skill Qualification System (ESSQS) by Japan Society for Endoscopic Surgery (JSES) for laparoscopic distal gastrectomy and low anterior resection based on the National Clinical Database (NCD) registry. Ann Gastroenterol Surg 4(6): 721-734, 2020. PMID: 33319163. DOI: 10.1002/ags3.12384
26. Ichikawa N, Homma S, Funakoshi T, Ohshima T, Hirose K, Yamada K, Nakamoto H, Kazui K, Yokota R, Honma T, Maeda Y, Yoshida T, Ishikawa T, Iijima H, Aiyama T and Taketomi A: Impact of technically qualified surgeons on laparoscopic colorectal resection outcomes: results of a propensity score-matching analysis. BJS Open 4(3): 486-498, 2020. PMID: 32207580. DOI: 10.1002/bjs5.50263
27. Hotouras A, Ribas Y, Zakeri SA, Nunes QM, Murphy J, Bhan C and Wexner SD: The influence of obesity and body mass index on the outcome of laparoscopic colorectal surgery: a systematic literature review. Colorectal Dis 18(10): O337-O366, 2016. PMID: 27254110. DOI: 10.1111/codi.13406
28. Krotkiewski M, Björntorp P, Sjöström L and Smith U: Impact of obesity on metabolism in men and women. Importance of regional adipose tissue distribution. J Clin Invest 72(3): 1150-1162, 1983. PMID: 6350364. DOI: 10.1172/JCI111040
29. Kunisaki C, Makino H, Takagawa R, Sato K, Kawamata M, Kanazawa A, Yamamoto N, Nagano Y, Fujii S, Ono HA, Akiyama H and Shimada H: Predictive factors for surgical complications of laparoscopy-assisted distal gastrectomy for gastric cancer. Surg Endosc 23(9): 2085-2093, 2009. PMID: 19116746. DOI: 10.1007/s00464-008-0247-8
30. Hagiwara M, Miyajima A, Hasegawa M, Jinzaki M, Kikuchi E, Nakagawa K and Oya M: Visceral obesity is a strong predictor of perioperative outcome in patients undergoing laparoscopic radical nephrectomy. BJU Int 110(11 Pt C): E980-E984, 2012. PMID: 22642302. DOI: 10.1111/j.1464-410X.2012.11274.x
31. Akiyoshi T, Kuroyanagi H, Oya M, Konishi T, Fukuda M, Fujimoto Y, Ueno M, Miyata S and Yamaguchi T: Factors affecting the difficulty of laparoscopic total mesorectal excision with double stapling technique anastomosis for low rectal cancer. Surgery 146(3): 483-489, 2009. PMID: 19715805. DOI: 10.1016/j.surg.2009.03.030
32. Sparreboom CL, van Groningen JT, Lingsma HF, Wouters MWJM, Menon AG, Kleinrensink GJ, Jeekel J, Lange JF and Dutch ColoRectal Audit group: Different risk factors for early and late colorectal anastomotic leakage in a nationwide audit. Dis Colon Rectum 61(11): 1258-1266, 2018. PMID: 30239395. DOI: 10.1097/DCR.0000000000001202
33. Gawande AA, Zinner MJ, Studdert DM and Brennan TA: Analysis of errors reported by surgeons at three teaching hospitals. Surgery 133(6): 614-621, 2003. PMID: 12796727. DOI: 10.1067/msy.2003.169
34. Goitein L, Shanafelt TD, Wipf JE, Slatore CG and Back AL: The effects of work-hour limitations on resident well-being, patient care, and education in an internal medicine residency program. Arch Intern Med 165(22): 2601-2606, 2005. PMID: 16344417. DOI: 10.1001/archinte.165.22.2601
35. Dorion D and Darveau S: Do micropauses prevent surgeon’s fatigue and loss of accuracy associated with prolonged surgery? An experimental prospective study. Ann Surg 257(2): 256-259, 2013. PMID: 22824853. DOI: 10.1097/SLA.0b013e31825efe87
36. Engelmann C, Schneider M, Kirschbaum C, Grote G, Dingemann J, Schoof S and Ure BM: Effects of intraoperative breaks on mental and somatic operator fatigue: a randomized clinical trial. Surg Endosc 25(4): 1245-1250, 2011. PMID: 20835716. DOI: 10.1007/s00464-010-1350-1
37. Langhoff PK, Schultz M, Harvald T and Rosenberg J: Safe laparoscopic colorectal surgery performed by trainees. J Surg Educ 70(1): 144-148, 2013. PMID: 23337684. DOI: 10.1016/j.jsurg.2012.06.027
38. Ichikawa N, Homma S, Yoshida T, Ohno Y, Kawamura H, Kamiizumi Y, Iijima H and Taketomi A: Supervision by a technically qualified surgeon affects the proficiency and safety of laparoscopic colectomy performed by novice surgeons. Surg Endosc 32(1): 436-442, 2018. PMID: 28664430. DOI: 10.1007/s00464-017-5701-z