International Journal of Colorectal Disease

, Volume 33, Issue 6, pp 755–762 | Cite as

Standardization of surgical procedures to reduce risk of anastomotic leakage, reoperation, and surgical site infection in colorectal cancer surgery: a retrospective cohort study of 1189 patients

  • Ken Eto
  • Mitsuyoshi Urashima
  • Makoto Kosuge
  • Masahisa Ohkuma
  • Rota Noaki
  • Kai Neki
  • Daisuke Ito
  • Yasuhiro Takeda
  • Hiroshi Sugano
  • Katsuhiko Yanaga
Original Article



Anastomotic leakage (AL) and surgical site infection (SSI) are prevalent complications of colorectal surgery. To lower this risk, we standardized our surgical procedures in 2012, with a preferential use of laparoscopic approach (LS) for both colon and rectal surgery, combined with triangulating anastomosis (TA) for colon surgery and defunctioning ileostomy (DI) for low anterior resection. Our aim was to evaluate the outcomes of our standardized procedures.


The incidence rate of AL (primary outcome) and of reoperation and SSI (secondary outcome) was compared before (early period, n = 648) and after (late period, n = 541) standardization, through a retrospective analysis.


The incidence rate of AL (6.6 versus 1.8%; P = 0.001), reoperation (3.5 versus 0.7%; P = 0.0012), and SSI (7.7 versus 4.6%; P = 0.029) was lower in late than in the early period. For colon cancer, TA and LS reduced the risk of AL (2.1 versus 0.3%, P = 0.020, for TA, and 3.2 versus 0.4%, P = 0.0027, for LS) and reoperation (2.9 versus 0.3%, P = 0.003, for TA, and 2.5 versus 0.2%, P = 0.0040, for LS). For rectal cancer, the incidence of all adverse outcomes (AL, reoperation, and SSI) was lower in cases treated by LS. However, the incidence of AL was lower in the late than in early period (P = 0.002) and with LS (P = 0.002). On multivariate analysis, late period and LS were independent factors of a lower risk of adverse outcomes.


Our surgical standardization seems to be effective in lowering the risks of AL, reoperation, and SSI after colorectal cancer surgery.


Anastomotic leakage Reoperation Surgical site infections Laparoscopic surgery 


In colorectal surgery, anastomotic leakage (AL) is a particularly serious complication, with 63 to 95% of cases requiring reoperation [1, 2, 3]. As well, AL is associated with an increased risk of colorectal cancer recurrence and lower overall survival [4, 5]. Surgical site infection (SSI) is also a prevalent postoperative complication of colorectal surgery, with an incidence rate of 11 to 25% [6, 7, 8, 9], which is associated with extended postoperative hospital stay and higher medical costs [10, 11]. Therefore, strategies to reduce AL, reoperation, and SSI would be important to improve overall outcomes of tumor resection in patients with colorectal cancer.

The risk for AL is closely related to the method of anastomosis. In current practice, mechanical anastomosis has almost completely replaced hand-sutured anastomosis [12]. However, the evidence regarding the utility of mechanical anastomosis remains controversial, with some studies having reported an increase in the incidence of AL after mechanical anastomosis, while other studies have reported that the mechanical anastomosis shortens operative time without increasing the risk for AL [13]. As a result of this controversy, the method of anastomosis remains largely dependent on a surgeon’s experience and preference.

Lowering the risk of AL is of particular significance for patients with rectal cancer, as the risk of AL after rectal surgery (6–15%) [5, 14, 15, 16, 17] is double the risk after colon surgery for tumor resection [2, 3, 18, 19]. Retrospective studies have identified the following risk factors for AL and SSI after colorectal surgery: tumor location and size, male sex, preoperative use of steroids, operative time, intraoperative blood loss, and non-creation of a defunctioning ileostomy (DI) [2, 14, 15, 16, 17, 18]. Among these factors, surgical factors are modifiable. Therefore, we focused on standardizing our surgical methods as a means of lowering the risk for AL. Specifically, we selected to perform a triangulating anastomosis (TA) for surgical resection of colon cancer and the creation of a DI for low anterior resections of rectal cancer. TA is an end-to-end mechanical anastomosis, for which we use one linear stapler over one third of the circumference of the anastomosis, with three linear staplers needed to complete the entire anastomosis, which includes crossover stapling between each linear stapler, resulting in a triangular-shaped anastomosis. Between 2004 and 2012, no cases of AL were identified among patients treated with a TA. Of note, this outcome was not supported by a controlled trial [20]. There is also good evidence in the literature supporting the utility of a DI for rectal tumor resection to reduce the risk for AL [14, 18, 21]. However, the preventive benefit of laparoscopic surgery (LS) in lowering the risk for AL and SSI remains controversial [1, 10, 22, 23]. Specifically, it has been argued that as LS generally prolongs operative time, compared to open surgery, LS could increase the risk for AL and SSI. However, as LS is generally associated with a lower volume of bleeding, a shorter postoperative stay, and a lower rate of early postoperative complications than open surgery [15], LS could offer protection against AL and SSI. Based on the clinical advantages of LS over an open approach, we preferentially adopted a laparoscopic approach for colorectal tumor resection in our standardized procedures. Therefore, since 2012, we have standardized the following three procedures for patients with colorectal cancer: LS for both colon and rectal surgery, TA for colon surgery, and DI for low anterior rectal surgery. The purpose of this study was to evaluate the significance of these standardized procedures, with AL as the primary outcome and reoperation and SSI as secondary outcomes.

Patients and methods

Study design

We conducted a retrospective analysis of the clinical data of patients with a diagnosis of colorectal cancer who underwent primary tumor resection at our Department of Surgery, between January 2008 and December 2015. For analysis, we divided patients into two groups: the early period group, formed of patients who underwent tumor resection prior to the standardizing of surgical procedure (January 2008 to January 2012, n = 648), and the late period group, formed of patients who underwent tumor resection after standardization of our surgical procedures (February 2012 to December 2015, n = 541). We then compared the risk of AL and other outcomes, before and after February 2012, as the cutoff date of implementation of our standardized surgical procedures, as a historical control study. Prior to this standardization, decisions regarding surgical and anastomosis methods and the creation of a DI were based on each surgeon’s experience and preference.

All patients and their families were informed of the possible risks and benefits of performing these surgical procedures and provided written consent. The study protocol was reviewed and approved by the ethics committee and Institutional Review Board (27-283 8168).

Patients and outcomes

We included patients who had a pathological diagnosis of colorectal cancer and who underwent primary tumor resection. Tumor staging for all patients was based on the TNM classification by means of colonoscopy examination, chest and abdominal computerized tomography (CT), or magnetic resonance (MR) imaging. We identified 1189 consecutive patients meeting our inclusion criteria, from medical records, between January 2008 and December 2015, for analysis. Postoperative complications were defined as those occurring within 30 days postsurgery. In the event of fecal discharge from the drain or suspicious symptoms of AL postoperatively, patients underwent abdominal CT imaging, gastrografin enema, and bacterial culture for diagnosis of AL as the primary outcome. Wound surveillance was performed by the infection control team (nurses and doctors). Diagnosis of incisional or organ/space SSI was based on the Centers for Disease Control and Prevention National Nosocomial Infections Surveillance system criteria [24] and analyzed as a secondary outcome. Reoperation within 30 days after the index surgery was also included as a secondary outcome.

Standardized surgical procedures

As standardized procedures, the following three surgical techniques have preferentially been used for the treatment of patients with colorectal cancer since February 2012. First, LS was to be considered as the primary surgical procedure selected. At their discretion, attending surgeons could select to perform an open surgical procedure for patients for whom general anesthesia or pneumoperitoneum was contraindicated, for patients with intestinal obstruction or for patients who had undergone multiple surgeries. Second, TA was to be used as the method of anastomosis, to the extent possible, for colon tumor resection. Third, a DI was to be created for low anterior resections of rectal tumors.

Clinical variables

The following variables were also extracted from the medical records for analysis: sex, age, body mass index (BMI), American Society of Anesthesiologists score (ASA), tumor location (colon or rectum), the UICC-TNM classification, anesthesia (general or local), emergency or elective procedure, open or laparoscopic approach, anastomotic method (TA, functional end-to-end anastomosis, double stapling technique, hand-sewn anastomosis, stump anastomosis, or no anastomosis), presence or absence of a DI, operative time (min), volume of intraoperative blood loss (mL), and length of hospital stay (days).

Statistical analysis

All data were expressed as a median (25–75th percentile) or number (%). The Mann-Whitney’s U test and the chi-squared test were used to evaluate between-group differences for continuous and categorical variables, respectively. Logistic regression analysis was used to assess associations between exposure to non-standardized or standardized surgical procedures and outcomes. Multivariate adjustments were performed for the following variables: sex, age, BMI, ASA, the UICC-TNM classification, open or laparoscopic approach, anastomotic methods, DI (yes or no), operative time, and intraoperative blood loss. All reported P values were two-sided with a P value < 0.05 considered significant. All analyses were performed by M.U. who did not examine the patients and was not involved in data collection. Stata 14.0 (StataCorp LP, College Station, TX) was used for all analyses.


Patients’ characteristics

Relevant patient characteristics and surgical outcomes, stratified by early and late period, are summarized in Table 1. After the standardization of surgical procedures, the incidence rate of LS, TA, and DI increased from 48.0 to 82.8, 38.7 to 70.6, and 16.9 to 35.8%, respectively. Of note, compared to the early period group, the late period group had a higher prevalence of patients with an ASA score of II, less patients with stage IV, a smaller proportion of patients who required epidural anesthesia, and smaller volumes of bleeding, but longer operative times. There was no difference between the groups with regard to the length of hospital stay.
Table 1

Patient characteristics and clinical variables between the early and late period by univariate analysis


Early period (N = 648)

Late period (N = 541)

P value

Standardized procedures


< 0.001c

 1. Laparoscopic surgery (LS)

311 (48.0%)

448 (82.8%)


 2. Anastomotic method (n = 737d)


< 0.001c

  Triangulating anastomosis (TA)

159 (38.7%)

230 (70.6%)


  Functional end-to-end anastomosis

89 (21.6%)

14 (4.3%)


  Double stapling technique

50 (12.2%)

7 (2.1%)


  Hand-sewn anastomosis

87 (21.2%)

55 (16.9%)


  Stump anastomosis

22 (5.3%)

16 (4.9%)


  No anastomosis

4 (1.0%)

4 (1.2%)


 3. Defunctioning ileostomy (DI) (n = 452e)

40 (16.9%)

77 (35.8%)

< 0.001c

Patients’ characteristics

 Age (years)

66.0 (59–74)a

68.0 (59.0–75.0)


 Sex ratio (male/female)




 Body mass index (kg/m2)

22.7 (20.6–25.0)

22.7 (20.4–25.0)




222 (34.3%)

134 (24.4%)

< 0.001c


392 (60.5%)

378 (69.9%)



34 (5.2%)

31 (5.7%)


Tumor location




411 (63.4%)

326 (60.3%)



232 (35.8%)

209 (38.6%)


 Both colon and rectum

5 (0.8%)

6 (1.1%)


TNM classification


33 (5.1%)

20 (3.7%)



185 (28.6%)

173 (31.9%)



151 (23.3%)

135 (25.0%)



192 (29.6%)

168 (31.1%)



87 (13.4%)

45 (8.3%)






633 (97.7%)

539 (99.6%)



15 (2.3%)

2 (0.4%)






23 (3.6%)

22 (4. 1%)



625 (96.4%)

519 (95.9%)


Surgical results

 Operative time (min)

199 (150–258)

245 (192–312)

< 0.001b

 Intraoperative blood loss (mL)

50 (0–245)

0 (0–50)

< 0.001b

 Hospital stay (days)

11 (8–18)

11 (8–16)


aMedian (25–75th percentile)

bMann-Whitney’s U test

cChi-squared test

dColon cancer alone

eRectal cancer alone and simultaneous rectal and colon cancer

Risk comparison before and after standardization of procedures

The incidence rate of AL, reoperation, incisional SSI, and organ/space SSI in the early period and late period is reported in Table 2. Among the 27 patients who underwent reoperation, 15 (55.6%) were diagnosed with AL. Only one patient from the early period group died within the 30-day period postsurgery, due to pulmonary edema following blood transfusion, with no deaths identified for the late period group.
Table 2

Risk comparison before and after standardization of procedures


Early period (N = 648)

Late period (N = 541)


95% CI

P valuea

Primary outcome

 Anastomosis leakage (AL)

43 (6.6%)

10 (1.8%)




Secondary outcome


23 (3.5%)

4 (0.7%)




 Incisional SSI

107 (16.5%)

79 (14.6%)




 Organ/Space SSI

50 (7.7%)

25 (4.6%)




SSI surgical site infection

aChi-squared test

The incidence rate of AL, the primary outcome, decreased to one fourth after standardization of surgical procedures: odds ratio (OR), 0.26 (95% confidence interval (CI), 0.12 to 0.54; P = 0.0001). Both reoperations and organ/space SSI were also significantly less frequent after standardization: OR, 0.20 (95% CI, 0.05 to 0.60; P = 0.0012) and OR, 0.58 (95% CI, 0.34 to 0.97; P = 0.029), respectively, although there was no significant difference in incisional SSI.

Effect of TA and LS on outcomes in colon cancer

Since TA is used only for patients with colon cancer, effects of TA and LS on outcomes were analyzed only in patients with colon cancer (Table 3). TA significantly reduced the risk of AL (P = 0.020) and reoperation (P = 0.0030), but did not lower the risk of incisional and organ/space SSI. Moreover, compared to an open procedure, LS significantly decreased the risk for AL (P = 0.0027), reoperation (P = 0.004), and SSI organ/space (P = 0.0027), but not incisional SSI.
Table 3

Effect of triangulating anastomosis (TA) and laparoscopic surgery (LS) on outcomes in colon cancer


Without TA (N = 340)

With TA (N = 389)


95% CI

P valuea

Open surgery (N = 282)

LS (N = 455)


95% CI

P valuea

Primary outcome

 Anastomosis leakage (AL)

7 (2.1%)

1 (0.3%)




9 (3.2%)

2 (0.4%)




Secondary outcome


10 (2.9%)

1 (0.3%)




7 (2.5%)

1 (0.2%)




 Incisional SSI

36 (10.6%)

93 (11.1%)




39 (13.8%)

42 (9.2%)




 Organ/space SSI

9 (2.6%)

8 (2.1%)




13 (4.6%)

5 (1.1%)




Colon cancer alone

SSI surgical site infection

aChi-squared test

Effect of DI and LS on outcomes in rectal cancer

Since DI is used only for patients with rectal cancer, effects of DI and LS on outcomes were analyzed only in patients with rectal cancer and those with both rectal and colon cancer (Table 4). No reoperation was performed in patients in whom a DI was created, whereas 4.8% of patients without a DI required reoperations: OR, 0.0 (95% CI, 0.00 to 0.66; P = 0.016). Incisional SSI was also less frequent with than without a DI (P = 0.038). Compared to an open procedure, LS significantly reduced risks of AL (P = 0.0019), reoperations (P = 0.04), incisional SSI (P < 0.0001), and organ/space SSI (P = 0.029).
Table 4

Effect of defunctioning ileostomy (DI) and laparoscopic surgery (LS) on outcomes in rectal cancer


Without DI (N = 335)

With DI (N = 117)


95% CI

P valuea

Open surgery (N = 148)

LS (N = 304)


95% CI

P valueb

Primary outcome

 Anastomosis leakage (AL)

33 (9.9%)

12 (10.3%)




24 (16.2%)

21 (6.9%)




Secondary outcome


16 (4.8%)

0 (0.0%)




9 (6.1%)

7 (2.3%)




 Incisional SSI

86 (25.7%)

19 (16.2%)




56 (37.8%)

49 (16.1%)



< 0.0001

 Organ/space SSI

42 (12.5%)

15 (12.8%)




31 (20.9%)

26 (8.6%)




Rectal cancer alone and simultaneous rectal and colon cancer

SSI surgical site infection

aChi-squared test

Effect of standardized surgical procedures on AL by multivariate analysis

Finally, a multivariate analysis was used to identify factors in our standardized procedures which effectively reduced AL, after controlling for age, sex, BMI, ASA, TNM stage, operative time, and intraoperative blood loss (Table 5). For colorectal cancer, both late period and LS independently decreased the risk of AL. However, for rectal cancer, DI did not influence the risk of AL, whereas late period and LS remained as significant preventive factors. For colon cancer, no factors were significantly associated with the risk of AL.
Table 5

Effect of standardized surgical procedures on anastomosis leakage (AL) in patients with colorectal cancer assessed by multivariate analysis


Overall (N = 1189)

Rectal cancera (N = 452)

Colon cancer (N = 737)


95% CI

P value


95% CI

P value


95% CI

P value

Late period






























Adjusted with age, gender, BMI, ASA, TNM stage, operation time, and intraoperative blood loss in relation to late period, laparoscopic surgery (LS), and defunctioning ileostomy (DI) or triangulating anastomosis (TA)

aRectal cancer alone and simultaneous rectal and colon cancer


Since both late period and LS were independently associated with lowering the risk of AL in patients with colorectal cancer, the use of LS could specifically decrease the risk of AL. The number of the patients who underwent open surgery decreased in the late period. This fact would have a great influence on the good results in late period, which, we believe, is the part of effect of our standardization.

We found the differences in some of patient characteristics and clinical variables between the early and late period. There was less stage IV colon cancer in the late period. We assume that in the late period, the referring oncologists tended to choose colonic stenting for patients with stage IV colon cancer instead of primary tumor resection not because of patient’s sickness but owing to early initiation of chemotherapy. We believe that the reason for smaller amount of intraoperative blood loss and less epidural anesthesia is related to the high incidence of laparoscopic surgery in the late group. The patients with ASA II were found more in the late period than in the early period, and the sickness of patients between the early and late period patient seems to be different. But in Table 5, OR was remained significant even after multivariate adjustment with age, gender, BMI, ASA, TNM stage, operation time, and intraoperative blood loss. Therefore, we do not believe that there was a selection bias between the early and late period. Moreover, bowel preparation, antibiotic regimens, and fast-track rehabilitation protocol has been consistent throughout the study period.

The absence of reoperation among patients with rectal cancer who underwent additional DI is in agreement with previous studies [25, 26, 27]. However, the utility of TA in lowering the risk of AL and reoperation among patients with colon cancer has only been reported in a few previous studies [20, 28, 29]. To our knowledge, there was no literature which mentioned about mechanism of TA against leakage. We need to confirm this point using animal model as a future direction. Our overall rate of AL among patients with colon cancer was low (1.1%), with an even lower failure rate among patients who underwent a TA (0.3%). As mechanical anastomosis is less influenced by a surgeon’s skill, it is easier to perform and, therefore, is likely to continue to gain popularity over hand-sutured anastomosis. Of note, we did not identify an independent effect of either DI or TA in lowering the risk of AL on multivariate analysis. This might indicate the presence of other confounding variables or that the number of cases in our analysis was insufficient to detect an effect on AL using multiple logistic regression models. We did identify a lower risk of AL, reoperation, and SSI after LS, compared to open surgery, although the reasons for this benefit of LS are not entirely clear as we used the same anastomotic instruments and methods for both open and laparoscopic procedures. It is possible that more skilled surgeons selected the LS approach or that patients who underwent an open procedure had more advanced disease status, such as with larger tumors, intestinal obstruction, and/or prior history of multiple surgeries. As these factors would implicitly bias the selection of the surgical procedure, a randomized controlled trial would be necessary to objectively evaluate the benefits of LS over an open approach in lowering the risk of AL, and to control for cancer-specific factors which could influence outcomes of LS. In the current study, although LS significantly reduced the incidence of incisional SSI among patients with rectal cancer, this benefit was only marginal among patients with colon cancer. Our methods may have influenced these outcomes. Specifically, mobilization of a tumor and dissection of blood vessels were performed laparoscopically, with the need for an open procedure determined after this point. This approach reduces the time of exposure of organs to air, which would further bias results.

In considering the clinical application of our findings, the limitations of our study need to be considered. First, we used a historical control which did not allow us to identify the mechanisms underlying the better outcomes for the late period group. Learning effects of surgeons and of the co-medical staff, as well as advances in medicine and surgical procedures, could have contributed to the improvement in outcomes in the late period, in addition to our standardization of surgical procedures. Second, even though we standardized our surgical procedures for all cases, the use of LS, DI, and TA was not applicable to all patients. In fact, although the application of these surgical procedures doubled in the late period, they remained far from being used in 100% of cases. Third, although more than 1000 patients were enrolled in our study, complications occurred in only a small proportion of cases. Specifically, AL occurred in only 1.1% of patients with colon cancer, and in only 1 of 389 cases performed in the late period. As such, computation of multivariate analyses was limited.


Standardization of our surgical procedures, including a preferential use of LS, TA, and DI, resulted in a significant lowering of the risk of AL, reoperation, and SSI organ/space associated with tumor resection in patients with colorectal cancer.


Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Ken Eto
    • 1
  • Mitsuyoshi Urashima
    • 2
  • Makoto Kosuge
    • 1
  • Masahisa Ohkuma
    • 1
  • Rota Noaki
    • 1
  • Kai Neki
    • 1
  • Daisuke Ito
    • 1
  • Yasuhiro Takeda
    • 1
  • Hiroshi Sugano
    • 1
  • Katsuhiko Yanaga
    • 1
  1. 1.Department of SurgeryJikei University School of MedicineTokyoJapan
  2. 2.Division of Molecular EpidemiologyJikei University School of MedicineTokyoJapan

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