Retrospective Cohort Study Open Access
Copyright ©The Author(s) 2020. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastrointest Surg. Oct 27, 2020; 12(10): 425-434
Published online Oct 27, 2020. doi: 10.4240/wjgs.v12.i10.425
Narrow pelvic inlet plane area and obesity as risk factors for anastomotic leakage after intersphincteric resection
Akira Toyoshima, Toshihiro Nishizawa, Eiji Sunami, Ryuji Akai, Takahiro Amano, Akiyoshi Yamashita, Shin Sasaki, Takeshi Endo, Yoshihiro Moriya, Osamu Toyoshima
Akira Toyoshima, Ryuji Akai, Takahiro Amano, Shin Sasaki, Department of Colorectal Surgery, Japanese Red Cross Medical Center, Tokyo 150-8935, Japan
Toshihiro Nishizawa, Department of Gastroenterology, International University of Health and Welfare, Narita Hospital, Narita 286-8520, Japan
Toshihiro Nishizawa, Osamu Toyoshima, Department of Gastroenterology, Toyoshima Endoscopy Clinic, Tokyo 157-0066, Japan
Eiji Sunami, Department of Surgery, The University of Kyorin, Tokyo 113-8655, Japan
Akiyoshi Yamashita, Department of Radiology, Japanese Red Cross Medical Center, Tokyo 150-8935, Japan
Takeshi Endo, Tokyo Midtown Clinic, Tokyo 107-6206, Japan
Yoshihiro Moriya, Miki Hospital, Iwate 029-4201, Japan
ORCID number: Akira Toyoshima (0000-0002-5697-6251); Toshihiro Nishizawa (0000-0003-4876-3384); Eiji Sunami (0000-0002-3637-9732); Ryuji Akai (0000-0001-7241-6265); Takahiro Amano (0000-0002-0489-7519); Akiyoshi Yamashita (0000-0002-3519-084X); Shin Sasaki (0000-0003-3489-6821); Takeshi Endo (0000-0002-3394-0213); Yoshihiro Moriya (0000-0002-7865-8748); Osamu Toyoshima (0000-0002-6953-6079).
Author contributions: Toyoshima A is the lead investigator, performed operations, collected and analyzed the data, and wrote the manuscript; Nishizawa T performed the literature search and statistical analysis and wrote the manuscript; Sunami E performed the operations; Akai R and Amano T assisted the operations; Yamashita A drafted the conception; Sasaki S supervised the study and approved the final manuscript; Toyoshima O contributed to data management, interpretation, and revision.
Institutional review board statement: This retrospective study was approved by the ethics review board of the Japanese Red Cross Medical Center on July 31, 2019.
Informed consent statement: Patients were not required to give informed consent to the study because the analysis used anonymous clinical data that were obtained after each patient agreed to treatment by written consent.
Conflict-of-interest statement: No conflict of interest.
Data sharing statement: No additional data are available.
STROBE statement: The manuscript was revised according to the STROBE Statement.
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Corresponding author: Akira Toyoshima, MD, Doctor, Department of Colorectal Surgery, Japanese Red Cross Medical Center, 4-1-22 Hiroo, Shibuya-ku, Tokyo 150-8935, Japan. toyosanaa@yahoo.co.jp
Received: June 19, 2020
Peer-review started: June 19, 2020
First decision: July 30, 2020
Revised: August 12, 2020
Accepted: September 14, 2020
Article in press: September 14, 2020
Published online: October 27, 2020

Abstract
BACKGROUND

Intersphincteric resection (ISR) has been increasingly used as the ultimate sphincter-preserving procedure in extremely low rectal cancer. The most critical complication of this technique is anastomotic leakage. The incidence rate of anastomotic leakage after ISR has been reported to range from 5.1% to 20%.

AIM

To investigate risk factors for anastomotic leakage after ISR based on clinicopathological variables and pelvimetry.

METHODS

This study was conducted at Department of Colorectal Surgery, Japanese Red Cross Medical Center, Tokyo, Japan, with a total of 117 patients. We enrolled 117 patients with extremely low rectal cancer who underwent laparotomic and laparoscopic ISRs at our hospital. We conducted retrospective univariate and multivariate regression analyses on 33 items to elucidate the risk factors for anastomotic leakage after ISR. Pelvic dimensions were measured using three-dimensional reconstruction of computed tomography images. The optimal cutoff value of the pelvic inlet plane area that predicts anastomotic leakage was determined using a receiver operating characteristic (ROC) curve.

RESULTS

We observed anastomotic leakage in 10 (8.5%) of the 117 patients. In the multivariate analysis, we identified high body mass index (odds ratio 1.674; 95% confidence interval: 1.087-2.58; P = 0.019) and smaller pelvic inlet plane area (odds ratio 0.998; 95% confidence interval: 0.997-0.999; P = 0.012) as statistically significant risk factors for anastomotic leakage. According to the receiver operating characteristic curves, the optimal cutoff value of the pelvic inlet plane area was 10074 mm2. Narrow pelvic inlet plane area (≤ 10074 mm2) predicted anastomotic leakage with a sensitivity of 90%, a specificity of 85.9%, and an accuracy of 86.3%.

CONCLUSION

Narrow pelvic inlet and obesity were independent risk factors for anastomotic leakage after ISR. Anastomotic leakage after ISR may be predicted from a narrow pelvic inlet plane area (≤ 10074 mm2).

Key Words: Intersphincteric resection, Anastomotic leakage, Pelvimetry, Pelvic dimensions, Pelvic inlet plane area, Rectal cancer

Core Tip: Intersphincteric resection (ISR) is the ultimate sphincter-preserving procedure in extremely low rectal cancer. We investigated risk factors for anastomotic leakage after ISR based on clinicopathological variables and pelvimetry. Narrow pelvic inlet and obesity were independent risk factors for anastomotic leakage after ISR. Anastomotic leakage after ISR may be predicted from a narrow pelvic inlet plane area (≤ 10074 mm2).



INTRODUCTION

Since Schiessel et al[1] first introduced intersphincteric resection (ISR) in 1994, the procedure has been increasingly accepted as the ultimate sphincter-preserving procedure in extremely low rectal cancer. ISR preserves the natural anus and avoids permanent colostomy. However, ISR is performed in the deep and funnel-shaped pelvic cavity, where access and visualization of the narrow pelvis is difficult[2,3]. Anastomotic leakage is the most critical complication that can cause reduced function or narrowing of the anal sphincter, possibly warranting a permanent colostomy[4-6]. According to a report from a committee (chaired by N Saito) sponsored by the Ministry of Health, Labour and Welfare of Japan, anastomotic leakage occurred in 23 (10.2%) of 225 patients after ISR[7]. The incidence rate of anastomotic leakage after ISR has been reported to range from 5.1% to 20%[8-10].

Akasu et al[11] have reported on the risk factors for anastomotic leakage after ISR but have not analyzed pelvic size. Pelvic anatomy is a determinant factor of rectal dissection, as the narrow pelvic cavity and bony structures surrounding the rectum may hinder dissection maneuvers[12]. Pelvimetry is famous for its use in predicting obstetric risk. In this study, we used pelvimetry to measure the inlet and outlet plane areas, particularly pelvic dimensions, to investigate risk factors for anastomotic leakage after ISR.

MATERIALS AND METHODS
Ethics

This retrospective study was approved by the ethics review board of the Japanese Red Cross Medical Center on July 31, 2019.

Subjects

This study included subjects who underwent laparotomic and laparoscopic ISR as treatment for extremely low rectal adenocarcinoma with inferior margins less than 5 cm from the anal verge at the Japanese Red Cross Medical Center between 2005 and 2019. The spread of the rectal cancer was quantified in accordance with the clinical tumor-node-metastasis (TNM) classification (8th edition)[13]. Liver metastases were detected in all patients with stage IV cancer. The patients with peritoneal metastasis, multivisceral resection, gastrointestinal stromal tumor, and carcinoid were excluded.

Our indications for ISR included: (1) An inferior tumor margin less than 5 cm from the anal verge; (2) A moderate- to well-differentiated adenocarcinoma; (3) Local spread restricted to the internal sphincter without involvement of striated muscle; (4) The presence of some amount of T4 tumor (vaginal invasion); (5) Patients with resectable metastases to the liver or lungs; and (6) Normal sphincter function.

Surgical procedure

The surgical procedure was performed in accordance with the method by Schiessel et al[1]. Laparotomy was performed with a small incision below the umbilicus, considering minimally invasive surgery. Under either laparotomy or laparoscopy, the inferior mesenteric artery (IMA) root was generally preserved, and the superior rectal artery was severed at the branching site of the left colic artery (LCA) or first branch of the sigmoid colic artery (SCA). When the IMA root was preserved, the lymph node around IMA root was separately resected to improve the curability. If tension was present at the anastomotic site or the color of the colon indicated an inadequate blood supply, the IMA was severed at the root and splenic flexure was mobilized. The rectum was divided transanally, removing a part or the entirety of the internal sphincter. Reconstruction was performed with a hand-sewn coloanal anastomosis from the anus. A closed suction drain was inserted in the left side of the pelvis and brought out at the lower angle of the wound. In some cases, an anal bougie (transanal drain) was inserted. Anastomotic leakage occurred in the second patient; thus, in all the subsequent patients, we constructed a covering stoma. The diverting stoma was closed 3-6 mo after surgery. Before the closure, we performed colonoscopy, contrast enema radiography, or computed tomography (CT). CT was performed each time there was a complication. The operations were performed by 3 staff surgeons (A, B, and C).

Outcomes

Anastomotic leakage was defined as the presence of an anastomosis fistula during the first postoperative endoscopy or gastrografin enema. In addition, anastomotic leakages were classified into three categories according to the clinical management by Rahbari et al[14] as follows: Grade A requires no active therapeutic intervention; Grade B, an active therapeutic intervention without operation; and Grade C, re-laparotomy.

We conducted retrospective univariate and multivariate regression analyses on 33 items to elucidate the risk factors for anastomotic leakage after ISR. These items were categorized into three groups as follows: Surgery, tumor, and patient related. The surgery-related factors were operation type (laparotomy or laparoscopic surgery), circumferential resection margin (CRM +/−), site of IMA ligature (IMA/LCA or SCA), splenic flexure mobilization (with/without), construction of a diverting stoma (with/without), insertion of an anal bougie (with/without), blood loss, transfusion (with/without)[15], surgeon (A, B, and C), surgical duration, and curability (A, B, or C). Tumor-related factors were tumor size, distance from the anal verge to the inferior margin of the tumor, patient categorization as clinical TNM classification, preoperative radiotherapy (with/without), and neoadjuvant chemotherapy (with/without). The patient related factors were age, sex, body mass index (BMI), American Society of Anesthesiologists Physical Status (ASA-PS; I, II, or III), serum total protein level, hemoglobin level, prognostic nutritional index[7], diabetes (hemoglobin A1c >/≤ 5.8 g/dL), and nine pelvimetry measurements.

Pelvimetry

We used the Synapse Vincent magnifying viewer (Fujifilm Medical Co., Ltd., Tokyo, Japan) to convert CT images into three-dimensional images. By using this imaging system, the anteroposterior (AP) diameter, transverse diameter, and total area were measured at the pelvic inlet and outlet. The length of the pubic symphysis and distance from the sacral promontory to the coccyx were measured to determine the anterior and posterior depths of the pelvis (Figure 1A-C). The lumbosacral (tortuosity) angle at the sacral promontory was also measured (Figure 1D).

Figure 1
Figure 1 Variables identified with three-dimensional pelvimetry. A: Lateral view; B: pelvic inlet plane; C: Pelvic outlet plane; D: Lateral view. 1: Anteroposterior pelvic inlet diameter; 2: Anteroposterior pelvic outlet diameter; 3: Length of the pubic symphysis; 4: Distance from the sacral promontory to the coccyx; 5: Transverse pelvic inlet diameter; 6: Pelvic inlet area; 7: Transverse pelvic outlet diameter; 8: Pelvic outlet area; 9: Lumbosacral (tortuosity) angle at the sacral promontory.
Statistical analyses

Differences between the leakage and non-leakage groups were detected using the Welch’s t-test or Student t-test for continuous data. The χ2 test was used for categorical secondary outcomes. The predictors found to be associated with anastomotic leakage in the univariate analysis (P < 0.05) were analyzed by subsequent multiple logistic regression method to identify independent factors. If both diameter and area were statistically significant, the area was preferentially used in the multivariate analysis. The optimal cutoff value of the pelvic inlet plane area for predicting anastomotic leakage was determined using the receiver operating characteristic curve. P values of < 0.05 were considered statistically significant in this study.

RESULTS

We enrolled 117 patients [89 men; mean age, 61.3 years (range, 26-86 years)]. We observed anastomotic leakage in 10 (8.5%) of the 117 patients as follows: Grade A in 3 patients (30%), grade B in 5 (50%), and grade C in 2 (20%). In the 3 cases with grade A leakage, it was cured by conservative treatment such as antibiotic treatment. In the 5 patients with grade B leakage, the fistulae were closed using an alpha-cyanoacrylate monomer (Aron Alpha A Sankyo, Toagosei Co., Ltd., Tokyo, Japan), a tissue adhesive. Two patients with grade C leakage needed re-operation. One patient underwent permanent colostomy, and the other underwent nephrostomy for vesicorectal fistula. Closure of the diverting stoma was possible in 8 (80%) of the 10 patients. No operative deaths occurred.

Table 1 shows the correlation between the postoperative anastomotic leakage and clinicopathological variables. The univariate analysis revealed a statistically significant relationship between anastomotic leakage and higher BMI, smaller pelvic inlet area, shorter AP diameter of the inlet plane, shorter transverse diameter of the inlet plane, shorter AP diameter of the outlet plane, longer pubic symphysis, greater lumbosacral angle, and larger amount of bleeding.

Table 1 Univariate analyses of clinicopathological variables related to anastomotic leakage after intersphincteric resection.

No leakage
Leakage
P value
Patients number10710
Age in yr61.1 ± 12.764.3 ± 9.90.436
Male sex, n (%)80 (74.8)9 (90)0.489
Body mass index22.4 ± 3.325.6 ± 2.70.004
Anesthesiologists physical status0.569
1 293
2757
330
Serum total protein level, g/dL6.9 ± 0.57.1 ± 0.50.351
Blood hemoglobin level, g/dL13.5 ± 1.814.6 ± 1.40.055
Prognostic nutritional index49.7 ± 6.352.4 ± 4.90.205
Diabetes mellitus0.326
No937
Yes143
Inlet plane: Antero-posterior diameter, mm110.3 ± 10.8100 ± 7.90.002
Inlet plane: Transverse diameter, mm156.3 ± 35.4136.4 ± 17.70.008
Area of the inlet plane, mm211330 ± 12799428 ± 636.1< 0.001
Outlet plane: Antero-posterior diameter, mm97.8 ± 8.990.6 ± 10.40.018
Outlet plane: Transverse diameter, mm103.4 ± 10.1102.8 ± 4.40.739
Area of the outlet plane, mm29572 ± 15019323 ± 9990.487
Length of the pubic symphysis, mm41.9 ± 5.645.7 ± 5.20.044
Distance from the sacral promontry to the coccyx, mm125.5 ± 13.3131.3 ± 14.80.193
Tortuosity angle 131.7 ± 8.7140.4 ± 11.40.004
Tumors
Tumor size, mm41.3 ± 25.233.3 ± 19.70.335
Distance from the anal verge, mm16.8 ± 19.220.4 ± 14.60.563
TNM stage0.056
031
I356
II231
III341
IV121
Preoperative radiotherapy0.972
No909
Yes171
Neoadjuvant chemotherapy0.341
No8910
Yes180
Surgery0.341
Laparotomy8910
Laparoscopic surgery180
Circumferential resection margin0.809
No1009
Yes71
Ligated site of the artery0.583
Inferior mesenteric artery50
Left colonic artery413
Sigmoid colon artery617
Mobilization of the splenic flexure0.738
No999
Yes81
Diverting stoma0.401
No11
Yes1069
Anal bougie0.341
No8910
Yes180
Bleeding amount, mL645 ± 7091380 ± 11660.004
Blood transfusion, mL8 ± 60292 ± 6210.181
Operator0.418
X879
T91
S110
Operation time in min367 ± 156387 ± 1670.698
Curativity0.54
A 869
B80
C131

In the multivariate analysis, we identified high BMI (odds ratio 1.674; 95% confidence interval: 1.087-2.58; P = 0.019) and smaller pelvic inlet plane area (odds ratio 0.998; 95% confidence interval: 0.997-0.999; P = 0.012) as statistically significant risk factors for anastomotic leakage (Table 2).

Table 2 Multivariate analyses of clinicopathological variables related to anastomotic leakage after intersphincteric resection.
Variables
Multivariate analysis
Odds ratio
95%CI
P value
Body mass index1.6741.087-2.580.019
Area of the inlet plane 0.9980.997-0.9990.012
Outlet plane: Antero-posterior diameter0.9050.811-1.0080.07
Length of the pubic symphysis 1.1250.883-1.4350.341
Tortuosity angle 1.0490.941-1.170.39
Bleeding amount1.0010.999-1.0030.144

According to the receiver operating characteristic curves, the optimal cutoff value of the pelvic inlet plane area was 10074 mm2 (Figure 2). Narrow pelvic inlet area (≤ 10074 mm2) predicted anastomotic leakage with a sensitivity of 90%, a specificity of 85.9%, and an accuracy of 86.3%. The positive predictive value was 37.5%, and the negative predictive value was 98.9%.

Figure 2
Figure 2 Receiver operating characteristic curve for predicting anastomotic leakage based on the pelvic inlet plane area.
DISCUSSION

Narrow pelvic inlet and obesity were independent risk factors for anastomotic leakage after ISR. This is the first report of increased anastomotic leakage due to narrow pelvic inlet. Narrow pelvic inlet hinders the surgical procedures with the approach from the abdominal cavity, and the difficulty might lead to anastomotic leakage.

Rullier et al[16] demonstrated that male sex and obesity were independent risk factors for anastomotic leakage after low anterior resection (LAR). The male pelvis is narrower than the female pelvis; thus, male sex as a risk factor for anastomotic leakage might be due to the narrower pelvis in males.

Zhou et al[17] evaluated the technical difficulties in LAR or abdominoperineal resection using three-dimensional reconstruction of CT images. Their multivariate analyses revealed that the AP diameter of the pelvic inlet, AP diameter of the pelvic outlet, and height of the pubic symphysis were factors that affect operative time. These results indicate that narrower and deeper pelvises could increase operating times.

Zur Hausen et al[18] also evaluated the clinical outcomes in LAR or abdominoperineal resection using CT pelvimetry. A shorter AP pelvic inlet diameter was associated with a higher rate of incomplete mesorectal excision. However, the number of cases were relatively small (n = 74), and the study failed to show the association between pelvic diameters and incidence of anastomotic leakage. The authors concluded that preoperative pelvimetry may help identify difficult pelvic dissections preoperatively.

The present study shows that narrow pelvic inlet significantly increased the incidence of anastomotic leakage after ISR. Furthermore, narrow pelvic inlet area (≤ 10074 mm2) predicted anastomotic leakage with a sensitivity of 90%, a specificity of 85.9%, and an accuracy of 86.3%. Identification of patients at high risk for anastomotic leakage may allow for the selective use of the indocyanine green fluorescence method or more-advanced access methods such as transanal total mesorectal excision or robotic-assisted laparoscopic surgery[19] for improving surgical outcomes.

In our study, obesity was also an independent risk factor for anastomotic leakage after ISR. Surgery for obese patients is generally more difficult because obesity contributes to inadequate exposure of the surgical field, which results in accidental injury. Yang et al[20] and Yamamoto et al[21] reported that obesity was a risk factor for anastomotic leakage after LAR. Rullier et al[16] reported that obesity was a risk factor for anastomotic leakage after ISR. A protective stoma is, therefore, suitable after ISR, particularly in obese patients. The first limitation of our study is that it was conducted within a single specialized institution. Second, this study was consecutive but retrospective. Third, the number of laparoscopic cases was small, and the effect of laparoscopic surgery was not determined. A follow-up study should be performed to confirm and clarify the characteristics of anastomotic leakage after ISR including laparoscopic surgery.

CONCLUSION

In conclusion, narrow pelvic inlet and high BMI were associated with anastomotic leakage after ISR. Anastomotic leakage after ISR may be predicted from a narrow pelvic inlet plane area (≤ 10074 mm2).

ARTICLE HIGHLIGHTS
Research background

Intersphincteric resection (ISR) has been increasingly used as the ultimate sphincter-preserving procedure in extremely low rectal cancer.

Research motivation

Anastomotic leakage is the most critical complication that can cause reduced function or narrowing of the anal sphincter, possibly warranting a permanent colostomy.

Research objectives

This study investigated risk factors for anastomotic leakage after ISR based on clinicopathological variables and pelvimetry.

Research methods

We enrolled 117 patients with extremely low rectal cancer who underwent laparotomic and laparoscopic ISRs. Risk factors for anastomotic leakage after ISR that were analyzed using a multivariate analysis. Pelvic dimensions were measured using three-dimensional reconstruction of computed tomography images. The optimal cutoff value of the pelvic inlet plane area that predicts anastomotic leakage was determined using a receiver operating characteristic curve.

Research results

Higher body mass index and small pelvic inlet plane area were independently associated with anastomotic leakage after ISR. According to the receiver operating characteristic curves, the optimal cutoff value of the pelvic inlet plane area was 10074 mm2. Narrow pelvic inlet plane area (≤ 10074 mm2) predicted anastomotic leakage with a sensitivity of 90%, a specificity of 85.9%, and an accuracy of 86.3%.

Research conclusions

Narrow pelvic inlet and obesity were independent risk factors for anastomotic leakage after ISR.

Research perspectives

A follow-up study should be performed to confirm and clarify the characteristics of anastomotic leakage after ISR including laparoscopic surgery.

Footnotes

Manuscript source: Unsolicited manuscript

Corresponding Author's Membership in Professional Societies: Japan Surgical Society, No. 0413910; and The Japanese Society of Gastroenterology, No. 032796.

Specialty type: Surgery

Country/Territory of origin: Japan

Peer-review report’s scientific quality classification

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P-Reviewer: Fakhr I, Vignali A, Zhao WT S-Editor: Wang JL L-Editor: Filipodia P-Editor: Li JH

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