Abstract
Background/Aim
In rectal cancer surgery, anastomotic leakage (AL) is the most important complication and has a reported frequency of 11-15%. The causes of AL leakage are complex, and AL prevention should be performed in multiple directions. Thus, this study examined the usefulness of the comprehensive and multifaceted AL preventive measures.
Patients and Methods
In total, 164 rectal surgery patients who had low rectal staple anastomosis below the peritoneal reflection were enrolled. The patients were divided into two groups: (i) the multifaceted AL prevention group (MP group, n=34) and (ii) the insufficient AL prevention group (IP group, n=130). Multifaceted AL prevention was defined as intestinal blood flow evaluated via indocyanine green (ICG)-fluorescence imaging (FI), the use of a single-staple technique (SST) without intersecting stapling lines or “dog ears”, the use of transanal suture reinforcement according to the air leakage test, and the use of a transanal tube for anatomical decompression and a diverting stoma for diverting the fecal stream. The AL rates were retrospectively compared between the two groups. The data are expressed as the median and interquartile range.
Results
The rate of AL was significantly lower in the MP group (0%) than in the IP group (11.54%) (p=0.0423).
Conclusion
Multifaceted AL prevention, including ICG-FI and SST, achieved a zero incidence of AL. Multifaceted prevention significantly lessened AL more than inadequate prevention did. Therefore, if the weight of each preventive measure cannot be clearly identified, to avoid AL, it is important to take all preventive measures from multiple aspects.
Keywords: ICG, fluorescence, single-staple technique, rectum, anastomotic leakage
In rectal cancer surgery, anastomotic leakage (AL) is the most important complication. The frequency of leakage is in the range of 11-15% (1-4). It has been reported that AL during rectal surgery not only puts the patient at risk for death due to peritonitis but also leads to early adverse consequences for bowel function and quality of life even when leakage is cured (5).
Additionally, AL adversely affects oncologic outcomes, such as increasing local recurrence and impeding the initiation of adjuvant chemotherapy (6-8). The causes of AL are complex, and many risk factors have been reported. In particular, important factors for anastomosis include intestinal blood flow (IBF), completeness of the anastomosis itself, tension on the intestine around the anastomosis, and the background of the individual patient (9-13).
In terms of IBF, near-infrared fluorescence imaging has attracted increasing attention. Since the PILLAR 2 study (14), there have been many reports on the potential of indocyanine green (ICG) fluorescence imaging (FI) to reduce AL in rectal surgery (15-22).
In a phase III comparative study, the EssentiAL trial showed for the first time that ICG was effective at reducing AL (23). This study revealed that the leakage rate was 7.6%, which is a very low score. However, ICG-FI may not yield zero AL. To eradicate AL, comprehensive and multifaceted prevention, including ICG-FI, is necessary.
Recently, during surgery involving lower rectal anastomosis conducted at our institution, single-staple ICG-FI anastomosis with transanal reinforcement, a transanal tube, and a diverting stoma were performed to prevent AL. In this study, we investigated whether, compared with insufficient measures, our measures to prevent AL would reduce the incidence of AL in operated patients.
Patients and Methods
Patient selection. Rectal surgery with anastomosis via a stapler was performed in a total of 261 patients at our institution from January 2017 to December 2023. Among these patients, 164 patients who had low rectal staple anastomosis below the peritoneal reflection were enrolled.
Comparison between the surgery with multifaceted AL prevention and insufficient AL prevention groups. The 164 patients with lower rectal anastomosis were divided into two groups: (i) the multifaceted AL prevention group (MP group, n=34) and (ii) the insufficient AL prevention group (IP group, n=130). Multifaceted AL prevention in the MP group was defined as follows.
1. IBF evaluation with ICG-FI was performed (Figure 1).
Figure 1.
Observation of the oral side of the intestine with indocyanine green fluorescence imaging. A) The planned anastomotic line indicated by the white arrow was highly fluorescent. The surgical plan was not changed. B) The planned anastomotic line indicated by the white arrow was not fluorescent. The anastomotic line was changed to the position indicated by the black arrow.
ICG was administered after IMA ligation, rectal transection and division of the oral mesentery. IBF assessment with the ICG FI was performed on the oral side of the intestine. The ICG injection dose was 5 mg for patients with a body weight less than 75 kg, and 7.5 mg of ICG was used for patients who weighed 75 kg or more. The infusion route was flushed with 20 ml of saline.
The fluorescence observation camera used was a VISERA ELITE2 or VISERA ELITE3 system (Olympus, Tokyo, Japan), and the distance between the beam camera and the intestine was approximately 5-10 cm. Vascular perfusion via the ICG was not shown with the planned anastomotic line on the oral side, and the anastomotic line was changed. In the case of delayed vascular perfusion, the surgical plan was also changed.
2. Anastomosis was performed via the single-staple technique (SST) (Figure 2).
Figure 2.
Anastomosis via the single-staple technique. A) A purse-string suture was circumferentially performed doubly on the rectal cuff. B) A circular stapler was inserted with the guidance of a nelaton catheter. C) The circular stapler was fired. D) Transanal hand-sewn suture reinforcement sutures were added circumferentially.
We employed abdominal double purse-string circular stapled anastomosis for the SST after TaTME (24). First, purse-string suturing was circumferentially performed doubly on the rectal cuff with a 2-0 monofilament nonabsorbable suture. A nelaton catheter (10 Fr) was inserted transanally, and the rectal cuff was manually closed. We used a 28 mm or 29 mm circular stapler. The center shaft was connected to the nelaton catheter and guided from within the rectum to the pelvis. The anvil was connected to the center shaft, and a circular stapler was used for firing. After confirming the presence of a complete ring of the circular stapler and performing the air leakage test, transanal hand-sewn suture reinforcement sutures were added circumferentially to strengthen the anastomosis. If there was an incomplete ring or a positive air leakage test, suture reinforcement was mandatory, and at least 16 knotted sutures were used.
3. Transanal tube insertion.
The transanal tube was placed beyond the anastomosis and into the intestinal tract on the oral side. The tube used was a SILASCON® Duple Drain (Outer Diameter 8 mm) (KANEKA MEDICAL Products, Osaka, Japan).
4. A diverting stoma was created. Loop ileostomy was performed.
Patients who did not complete any of these AL preventive measures were assigned to the IP group. Data on patient demographics, comorbidities, neoadjuvant treatment, preoperative parameters, and disease details, such as TNM classification (25), intraoperative findings, postoperative hospital stay and postoperative morbidity according to the Clavien–Dindo classification (CD) (26), were obtained and compared retrospectively between the two groups. The primary outcome was: all CD grade AL rate. The secondary outcomes were CD Grade IIIa overall AL and CD Grade IIIb overall AL.
Analysis of ICG-FI. A total of 164 patients with lower rectal anastomosis were divided into the ICG+ group (n=103), in which ICG was used for IBF evaluation, and the ICG- group (n=61), in which ICG was not used. The AL rate was compared between the two groups and in the ICG+ group, it was evaluated whether the planned anatomical line was changed after ICG-FI.
Statistical analysis. The data are shown as the median and interquartile range. Statistical analysis was performed with the Mann–Whitney U-test and Fisher’s exact test, and all differences were determined to be significant at p<0.05. Statistical analysis was performed via JMP (JMP, Inc., Cary, NC, USA).
This study was approved by the Research Ethics Committee of the Kawaguchi Municipal Medical Center (Saitama, Japan) (approval number: 2019-42) and conformed to the provisions of the Declaration of Helsinki. Informed consent was obtained from all patients.
Results
The patient backgrounds are presented in Table I. When comparing the MP group and IP group, the pathological N stage (pN) values (0:1:2:3) were significantly different (16:15:2:0 vs. 83:28:16:2) (p=0.0434); and 7 (20.59%) and 7 (5.38%) patients received neoadjuvant chemoradiotherapy, respectively (p=0.0047). With respect to operative factors, in the IP group, ICG-FI was performed for 53.08%, SST was performed for 0.77% and a diverting stoma was used in 52.31% of the patients. There were 14 (10-16) knotted sutures in the MP group and 1 (0-2) knotted suture in the IP group, and these differences were significant (p<0.0001) (Table II). In the MP group, there was no AL (CD of any grade) (Table III). The rate of AL (all CD grades) was significantly lower in the MP group (0%) than in the IP group (11.54%) (p=0.0423). The rates of AL (CD grade IIIa over) were 0 and 14 (10.77%), and the rates of AL (CD grade IIIb over) were 0 and 6 (4.62%), with no significant difference. The postoperative hospital stay durations were 16 (9-22) and 11 (9-15) days, respectively, with no significant difference.
Table I. Patient characteristics.
FAP: Familial adenomatous polyposis; UC: ulcerative colitis; CRT: chemo-radiotherapy. MP group: Multifaceted AL prevention group; IP: insufficient AL prevention group; is: in situ. Values are presented as the median [interquartile range] or as n (%).
Table II. Operative factors.
Values are presented as the median [interquartile range] or as n (%). *Number of stiches. ICG-FI: Indocyanine green fluorescence imaging; SST: single-staple technique; MP group: Multifaceted AL prevention group; IP: insufficient AL prevention group.
Table III. Short-term outcomes.
Values are presented as the median [interquartile range] or as n (%). CD: Clavien–Dindo classification; MP group: Multifaceted AL prevention group; IP: insufficient AL prevention group.
No significant difference in complications classified as Clavien–Dindo grade III or higher was noted, with two patients in the MP group (5.9%, stoma outlet obstruction) and 20 patients in the IP group (15.4%, two with small intestinal penetration, one with a duodenal ulcer, one with small intestinal obstruction, two with an abdominal abscess, and 14 with AL).
Analysis of ICG-FI. Comparative analysis showed that the percentages of ALs (all CD grades) were 9 (8.74%) and 6 (9.84%); the percentages of ALs (CD grade IIIa) were 8 (7.8%) and 5 (8.2%); and the percentages of ALs (CD grade IIIb) were 2 (1.94%) and 4 (6.56%) in the ICG+ group and ICG- group, respectively, with no significant difference (Table IV). However, in the ICG+group, surgical planning was changed because of ICG in 11 (10.7%) patients. A stoma was added in two (1.9%) patients, resulting in no AL. Nine patients (8.7%) experienced planed anastomotic line changes, 7 (7.6%) of whom avoided AL. The change in the planned anastomosis line by ICG-FI was 3 [2-5.25] cm.
Table IV. Percentages of anastomotic leakages in the indocyanine green (ICG)+ and ICG- groups.
CD: Clavien–Dindo classification. Values are presented as n (%).
Discussion
The ICG-FI has been shown to reduce the incidence of AL (23). In this study, AL could be prevented in nine patients by changing the surgical plan according to the ICG-FI. Although there was a trend toward fewer ALs resulting in reoperation with ICG-FI, the small number of our patients at a single institution did not indicate a significantly different rate of AL reduction. The causes of AL are complex, and preventive measures must be taken from multiple aspects.
Among the anastomotic techniques, the most common method in rectal surgery is DST, which was first reported in 1980 and is a simple, safe, reliable, and rapid procedure (27). However, it has been argued that DST carries the risk of AL, intersecting stapling lines and the formation of “dog ears”, which are the corners of the rectal stump with a potentially poor blood supply (28,29). SST was expected to overcome these problems.
Although the literature published more than a decade ago revealed no significant difference in the AL rate between SST and DST, recent studies on the SST have reported the superiority of the AL rate over the DST rate (30,31).
A study by Foppa et al. reported that the AL rate was significantly lower in the SST group than in the DST group (6.48% vs. 15.28%; p=0.002) (32). With respect to the difference in AL between the SST and DST, other studies conducted by Harji et al. (33), Spinelli et al. (34), and Brunner et al. (35) reported 8.6% vs. 20.9% (p=0.028), 2% vs. 17.3% (p=0.01), and 3% vs. 9% (p=0.04), respectively.
Transanal hand-sewn reinforcement for stapled anastomosis also has the potential to decrease the AL rate. The AL rate in rectal anastomosis with suture reinforcement has been reported to be 0-5.9% (36-38).
Enomoto et al. reported that if the SST after Ta-TME results in an incomplete ring, hand-sewn reinforcement all around the stapled line reduces the occurrence of AL (36). Endoluminal pressure reduction via a transanal tube is also expected to be an AL preventive measure after rectal surgery.
Xiao et al. (39) reported that the incidence of AL with a transanal tube was significantly lower than that without a transanal tube (3.7% vs. 9.3%; p=0.028). However, another earlier study conducted by Zhao et al. reported that there was no significant difference in the incidence of AL between patients treated with transanal tubs and those treated without transanal tubs (6.4% vs. 6.8%, p=0.87) (40).
Two randomized clinical trials have reached different conclusions, and these findings are controversial. In the study by Zhao et al., 280 patients with a transanal tube had no bleeding or iatrogenic colonic perforations (40). This procedure method was deemed safe and did not appear to have the least adverse effect on anastomotic healing. A diverting stoma is the most common method used for AL prevention in clinical practice.
However, it is argued that diverting stomas cannot eliminate the AL risk but can surely minimize surgical complications related to AL and reduce the rate of reoperation (41-44). In addition to these, as a measure against AL, attempts to predict AL with the level of C-reactive protein (CRP) in drainage fluid or The side-to-side rectal anastomosis technique using a circular stapler to prevent AL have been reported (45-46). The side-to-side rectal anastomosis also does not cause intersecting stapling lines or “dog ears”, but is not indicated for lower rectal cancer.
The causes of AL are complex, and it is difficult to prove that any single AL preventive measure clearly reduces AL.
In this study, multifaceted AL prevention, including IBF evaluation with ICG-FI, SST without intersecting stapling lines, “dog ears” formation, transanal suture reinforcement, the use of a transanal tube for anatomical decompression, and a diverting stoma for diverting the fecal stream, achieved a zero incidence of AL. Multifaceted prevention significantly reduced the AL incidence compared with inadequate prevention. If the weight of each measure for AL prevention cannot be clearly identified, then it is important to take comprehensive and multifaceted preventive measures to avoid AL.
Study limitations. The limitations of this research include its retrospective single-center design, small sample size, and possible selection and historical bias. Because the study included only ALs of clinical significance, if there were no clinical problems in the early postoperative period, aggressive imaging studies to search for ALs were not performed.
Conclusion
It is important to take comprehensive and multifaceted preventive measures to avoid AL.
Conflicts of Interest
The Authors have no competing interests to declare that are relevant to the content of this article.
Authors’ Contributions
Shunjin Ryu contributed to the conception and design of the study and analyzed the data. Data collection and analysis were performed by Shunjin Ryu, Yuta Imaizumi, Keisuke Goto, Sotaro Iwauchi, Takehiro Kobayashi, and Ryusuke Ito. The first draft of the manuscript was written by Shunjin Ryu, and all the authors commented on previous versions of the manuscript. All the Authors read and approved the final manuscript. Yukio Nakabayashi supervised the study.
Acknowledgements
The Authors would like to thank Hiroya Enomoto (Department of Surgery, The Jikei University School Daisan Hospital, Tokyo) for his assistance with the introduction of Ta-TME. The Authors also express their appreciation to the operating room staff of the Kawaguchi Municipal Medical Center, especially Ms. Keika Iijima, for her assistance with the colorectal cancer database. This work was supported by JSPS KAKENHI Grant Number 22K16524.
Funding
This work was supported by JSPS KAKENHI Grant Number 22K16524.
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