Definition and grading of anastomotic stricture/stenosis following low anastomosis after total mesorectal excision: A single-center study

doi:10.21203/rs.3.rs-2071399/v1

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Definition and grading of anastomotic stricture/stenosis following low anastomosis after total mesorectal excision: A single-center study

https://doi.org/10.21203/rs.3.rs-2071399/v1

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BACKGROUND: Anastomotic stricture/stenosis is an alarming complication after colorectal surgery, and there is still no recognized definition for anastomotic stricture/stenosis. This study aimed to determine the status and change of anastomotic stricture/stenosis after rectal surgery using a special anastomotic stricture/stenosis definition and grading system, discuss various risk factors for anastomotic stricture/stenosis, and explore the effect of different degrees of anastomotic stricture/stenosis on bowel function.

METHODS: This study included patients with confirmed rectal cancer who underwent total mesorectal excision between May 2014 and May 2021. A five-degree special anastomotic stricture/stenosis definition and grading system was used to determine anastomotic stricture/stenosis status, and clinical outcomes and risk factors for anastomotic stricture/stenosis were investigated. Furthermore, the low anterior resection syndrome score was used to assess bowel function.

RESULTS: A total of 473 patients were enrolled in this study. The low anterior resection syndrome assessment showed that the more severe the anastomotic stricture/stenosis, the more severe the low anterior resection syndrome (all p<0.001). Univariate and multivariate analyses of patient-related and technical risk factors for anastomotic stricture/stenosis were performed 3 months postoperatively. For univariate analysis, female sex was a lower risk factor for anastomotic stricture/stenosis. Defunctioning stoma, neoadjuvant chemoradiotherapy, chemotherapy, and anastomotic leakage were higher risk factors for anastomotic stricture/stenosis (all p<0.05). For multivariate analysis, only neoadjuvant chemoradiotherapy, chemotherapy, and anastomotic leakage were still higher risk factors for anastomotic stricture/stenosis (all p<0.05).

CONCLUSIONS: Through a special anastomotic stricture/stenosis definition and grading system’s evaluation, we noted the anastomotic stricture/stenosis severity significantly affected bowel function, and multivariate analysis showed that neoadjuvant chemoradiotherapy, chemotherapy, and anastomotic leakage were the higher risk factors for anastomotic stricture/stenosis.

anastomotic stricture/stenosis

total mesorectal excision

rectal cancer

Anastomotic stricture/stenosis (AS) is a common complication after colorectal and coloanal anastomosis, possibly resulting in severe anorectal dysfunctions[1]. The incidence of AS reported in the literature varies widely, with 2–30% cited most commonly[1–6]. However, this wide range is mainly due to no recognized definition for AS. Most studies defined AS the difficulty in passage of an endoscope through the anastomosis, but the diameter of the endoscope used varied widely (11–20 mm)[4–8]. As a result, there are few comparisons between different studies on AS, and analysis of risk factors for AS have also yielded mixed results. Notably, most studies on AS have focused on rectal surgery, and the main reason was that the incidence of AS was significantly higher in rectal surgery than in colon surgery[1, 2, 9]. Rectal surgery accounts for approximately 70% of AS cases, which could be diagnosed simply using digital examination[10]. It is convenient, fast, and easily repeatable to perform the digital examination, and many AS cases can simultaneously be alleviated through digital dilation. Then we provided a special definition and grading system for AS[11], which uses only digital examination and dilation to classify all anastomoses after low rectal surgery.

In this study, we summed up our single-center experience using the special AS definition and grading system to determine the status and change of AS after rectal surgery, discuss various risk factors for AS, and explore the effect of different degrees of AS on bowel function.

Patients

The study procedures reported were approved by the ethics committee of the Shengjing Hospital of China Medical University. Written informed consent was obtained from all patients.

The clinical records of all consecutive patients with rectal cancer who underwent total mesorectal excision (TME) performed by three experienced surgeons (Jinchun Cong, Hong Zhang, and Chunsheng Chen; each author performed > 100 TME operations per year) at Shengjing Hospital of China Medical University between May 2014 and May 2021 were reviewed. In this study, the inclusion criteria were as follows: (1) colorectal or coloanal anastomosis after TME for rectal cancer; (2) the anastomosis could be assessed using the index finger on digital examination; and (3) no history of colorectal surgery. The exclusion criteria were as follows: (1) lost anastomosis; (2) emergency surgery for intestinal perforation or obstruction; (3) simultaneously executed the lateral lymph node dissection; and (4) local recurrence or loss of follow-up within 6 months after surgery.

The patient characteristics included age, body mass index (BMI), sex, diabetes, angiocardiopathy, neoadjuvant chemoradiotherapy (NCRT), chemotherapy, pathological T and N stage, defunctioning stoma, ligation site of the inferior mesenteric artery (IMA), blood perfusion evaluated using indocyanine green (ICG), surgical approach, anastomotic method, distance from anastomosis to the anal verge, and anastomotic leakage (AL).

Surgical procedures

All patients underwent TME, as described by Heald[12]. The choice of laparoscopy or open surgery is not random but mainly according to the patient's wishes. High or low ligation IMA and whether blood perfusion was evaluated using intraoperative ICG fluorescence angiography were also not random but mainly depended on the habits and perceptions of the surgeons at the time. All anastomoses were end-to-end, and no pouches were created. For stapled anastomosis, a 28 mm EEA circular stapler (Medtronic PLC, Dublin, Ireland) or 29 mm (Ethicon Endo-Surgery Inc, Albuquerque, NM, USA) was used. A 4 − 0 Vicryl Rapide suture was used for the manual anastomosis. Regarding the defunctioning stoma, a temporary protective diverting ileostomy was created based on the operator’s discretion, and the stoma was usually reversed between 3‒6 months after surgery.

Definition of AS

AS was defined as “the intestinal canal at the anastomotic site could not achieve the diameter and/or elasticity as that of the adjacent healthy bowel at either side of the anastomosis.” The grading of AS severity was classified during digital examination and dilation. Briefly, five degrees were included in this grading system, and the severity was graded from 0 to 3[11]:

Grade 0: the index finger readily passes through the anastomosis, which could be dilated like the normal bowel; no inflammatory or fibrotic adhesions in the anastomosis.

Grade 1: the index finger readily passes through the anastomosis, which has a fixed diameter and could not be dilated further; no inflammatory or fibrotic adhesions in the anastomosis.

Grade 2a: the presence of resistance at the anastomosis, and the patient experienced pain or discomfort; the anastomosis contains inflammatory adhesions that could be broken by digital dilation, and the index finger could pass through the anastomosis before or after the dilation.

Grade 2b: the presence of resistance at the anastomosis, and the patient experienced pain or discomfort; fibrotic adhesions in the anastomosis that could not be broken by digital dilation, the index finger could pass through the anastomosis, and no proximal bowel distention was observed radiographically.

Grade 3: the index finger could not pass through the anastomosis with any effort or degree 2b with proximal bowel distention observed radiographically.

All degrees of AS were judged by three surgeons (Jinchun Cong, Hong Zhang, and Chunsheng Chen; all of whom were "blinded" to the patients’ characteristics). Any disagreement regarding degree 2a was ultimately resolved by the first examiner, and other disputes were resolved by the majority rule. All patients judged as grade 2b or 3 underwent imageological examination.

Bowel function assessment

The bowel function was assessed using a low anterior resection syndrome (LARS) score at 1, 3, and 6 months postoperatively for the patients with restored intestinal continuity. The score consists of five questions and ranges from 0–42 points, in which patients were classified into no LARS (0–20 points), minor LARS (21–29 points), or major LARS (30–42 points)[13, 14].

Statistical analysis

The SPSS software (version 22.0, IBM Corp, Armonk, NY, USA) was used to examine the data. Quantitative data with a normally distributed range were reported as mean ± standard deviation and analyzed using two independent sample t-test methods. Qualitative data that were not normally distributed were presented as median (range) using the Mann–Whitney U test. In addition, categorical data were reported as the number of patients (percentage) and analyzed using Fisher’s exact test, χ2 test, and rank-sum test. The heterogeneity analysis was determined using the kappa test, and ordinal logistic regression was used for multivariate analysis. All tests were two-sided, and a p-value of < 0.05 was considered statistically significant.

Between May 2014 and May 2021, 1564 patients with rectal cancer underwent TME at Shengjing Hospital of China Medical University. Among them, 65 patients lost anastomosis, 93 simultaneously executed the lateral lymph node dissection, 38 underwent emergency surgery for perforation or obstruction, 3 had local recurrence, 151 could not be clearly assessed for the anastomosis using digital examination, and 741 lost regular follow-up from the designated examiners in 6 months postoperatively. These patients were excluded from the study. The demographics of the remaining 473 patients are shown in Table 1.

Table 1

Demographic characteristics of the 473 patients
Clinicopathological variables
Age (years), mean ± SD	61.3 ± 8.7
BMI (kg/m²), mean ± SD	24.1 ± 3.3
Gender, n (%)
Female	175 (37.0)
Male	298 (63.0)
Diabetes, n (%)
No	430 (90.9)
Yes	43 (9.1)
Angiocardiopathy, n (%)
No	419 (88.6)
Yes	54 (11.4)
Neoadjuvant chemoradiotherapy, n (%)
No	368 (77.8)
Yes	105 (22.2)
Chemotherapy, n (%)
No	243 (51.4)
Yes	230 (48.6)
Pathological T stage, n (%)
T0/T1/T2	307 (64.9)
T3/T4	166 (35.1)
Pathological N stage, n (%)
N0	346 (73.2)
N+	127 (26.8)
Defunctioning stoma, n (%)
No	178 (37.6)
Yes	295 (62.4)
Ligation site of IMA, n (%)
High	329 (69.6)
Low	144 (30.4)
Blood perfusion evaluated with ICG, n (%)
No	313 (66.2)
Yes	160 (33.8)
Surgical approach, n (%)
Laparoscopic	332 (70.2)
Open	141 (29.8)
Anastomotic method, n (%)
Stapled	386 (81.6)
Manual	87 (18.4)
Distance from anastomosis to anal verge (cm), mean ± SD	3.4 ± 0.8
Anastomotic leakage, n (%)
No	455 (96.2)
Yes	18 (3.8)
Anastomotic stenosis/stricture, n (%)
at 1 month
Grade 0	45 (9.5)
Grade 1	158 (33.4)
Grade 2a	161 (34.0)
Grade 2b	91 (19.2)
Grade 3	18 (3.8)
at 3 months
Grade 0	55 (11.6)
Grade 1	163 (34.5)
Grade 2a	133 (28.1)
Grade 2b	98 (20.7)
Grade 3	24 (5.1)
at 6 months
Grade 0	64 (13.5)
Grade 1	261 (55.2)
Grade 2a	23 (4.9)
Grade 2b	103 (21.8)
Grade 3	22 (4.7)
ICG, indocyanine green; IMA, inferior mesenteric artery; BMI, body mass index;

The degrees of AS were judged by three surgeons, and the consistency test was carried out 3 months postoperatively for the heterogeneity analysis between the three examiners. The average kappa value was 0.985 (0.983, 0.989, and 0.983 between each other, p = 0.007, 0.006, and 0.007, respectively). The degrees, change in AS, and the conversion between each other in the follow-up are shown in Table 1 and Fig. 1. Between 1‒6 months after surgery, AS’s severity gradually decreased (p < 0.001). In the process, grade 0 maintained the degree at all times. Grade 1 partially changed to grade 0, and the vast majority maintained the degree. Grade 2a changed to grade 1 or 2b or maintained the degree, and the most obvious change occurred 6 months postoperatively, where 80.5% of grade 2a changed to grade 1. Grade 2b and 3 changed between each other; however, neither grade 2b nor 3 could downgrade to a lower level than grade 2a.

The relationship between AS and bowel function was analyzed for patients with restored intestinal continuity at 1, 3, and 6 months postoperatively. No stoma was reversed 3 postoperatively, and stoma could not still be reversed in 19 cases 6 months postoperatively (11 cases due to anastomotic complications and the other 8 for individual reasons). There were 454 patients who gained LARS scores at this time. Table 2 shows the association between AS and LARS severity, and the results showed that the more severe the AS, the more severe the LARS (all p < 0.001). As for the change in the LARS scores, the LARS severity gradually decreased over time, p = 0.022.

Table 2

The association between AS and LARS severity
	total	Grade 0	Grade 1	Grade 2a	Grade 2b	Grade 3	P value
1 month	N = 178 (100)	N = 28 (15.7)	N = 80 (44.9)	N = 39 (21.9)	N = 25 (14.0)	N = 6 (3.4)	p < 0.001
Major LARS	57 (32.0)	0 (0)	18 (22.5)	17 (43.6)	16 (64.0)	6 (100)
Minor LARS	73 (41.0)	9 (32.1)	37 (46.3)	18 (46.2)	9 (36.0)	0(0)
No LARS	48 (27.0)	19(67.9)	25(31.3)	4(10.3)	0(0)	0 (0)
3 months	N = 178 (100)	N = 31 (17.4)	N = 86 (48.3)	N = 21 (11.8)	N = 30 (16.9)	N = 10 (5.6)	p < 0.001
Major LARS	62 (34.8)	1 (3.2)	19 (22.1)	12 (57.1)	20 (66.7)	10 (100)
Minor LARS	60 (33.7)	11 (35.5)	30 (34.9)	9 (42.9)	10 (33.3)	0 (0)
No LARS	56 (31.5)	19 (61.3)	37 (43.0)	0 (0)	0 (0)	0 (0)
6 months	N = 454 (100)	N = 132 (29.1)	N = 201 (44.3)	N = 38 (8.4)	N = 68 (15.0)	N = 15 (3.3)	p < 0.001
Major LARS	118 (26.0)	6 (4.5)	31 (15.4)	21 (55.3)	45 (66.2)	15(100)
Minor LARS	167 (36.8)	47 (35.6)	82 (40.8)	15 (39.5)	23 (33.8)	0 (0)
No LARS	169 (37.2)	79 (59.8)	88 (43.8)	2 (5.3)	0 (0)	0 (0)
LARS, low anterior resection syndrome; AS, anastomotic stricture

Univariate and multivariate analyses of patient-related and technical risk factors for AS 3 months postoperatively are shown in Table 3. For the univariate analysis, the female sex was a lower risk factor for AS. In contrast, defunctioning stoma, NCRT, chemotherapy, and AL were the higher risk factors for AS (all p < 0.05), and there was no statistical difference in age, BMI, diabetes, angiocardiopathy, ligation site of IMA, blood perfusion evaluated using ICG, surgical approach, anastomotic method, and distance from anastomosis to anal verge (all p > 0.05). For the multivariate analysis, NCRT, chemotherapy, and AL were still the higher risk factors for AS (all p < 0.05); however, sex and defunctioning stoma showed no statistical difference (both p > 0.05).

Table 3

Univariate and multivariate analyses of patient-related and technical risk factors for AS at 3 months after the operation
Factor category	Univariate analysis				Multivariate analysis
Factor category	β	OR	95% CI	P	β	OR	95% CI	P
Sex (Female)	-0.264	0.768	0.629–0.938	0.01	-0.063	0.939	0.752–1.172	0.577
Age	-0.003	0.997	0.986–1.008	0.551
BMI	-0.003	0.997	0.969–1.026	0.841
Diabetes	-0.211	0.810	0.582–1.127	0.212
Angiocardiopathy	0.081	1.084	0.803–1.467	0.597
Surgical approach	0.055	1.057	0.857–1.302	0.605
Ligation site of IMA	-0.035	0.966	0.784–1.188	0.738
Blood perfusion evaluated with ICG	0.088	1.092	0.892–1.338	0.393
Distance from anastomosis to anal verge	0.072	1.075	0.959–1.206	0.216
Anastomotic method	0.14	1.150	0.899–1.473	0.263
Defunctioning stoma	0.528	1.696	1.385–2.075	< 0.001	0.015	1.015	0.797–1.292	0.905
Neoadjuvant chemoradiotherapy	1.598	4.943	3.626–6.733	< 0.001	2.433	11.393	6.646–19.550	< 0.001
Chemotherapy	1.121	3.068	2.465–3.819	< 0.001	0.524	1.689	1.314–3.819	< 0.001
Anastomotic leakage	3.115	22.533	7.050-71.952	< 0.001	4.725	112.730	30.784-412.815	< 0.001
ICG, indocyanine green; IMA, inferior mesenteric artery; BMI, body mass index; OR, odds ratio; CI, confidence interval; AS, anastomotic stricture

AS after rectal surgery is a common complication that may lead to impaired function, such as fecal urgency, incontinence, and bowel obstruction[1]. In this study, using a specific definition and grading system, we displayed the status and change of AS after TME. The results showed that the severity of AS significantly affects bowel function, and multivariate analysis showed that NCRT, chemotherapy, and AL were higher risk factors for AS.

There is still no recognized definition for AS, due to the differences in equipment used, it is impossible to have a fixed diameter to distinguish the presence or absence of AS. The most important point of the actual meaning of no AS is that the upstream intestinal contents could pass through the anastomosis without any hindrance, and none of the existing definitions could denote this idea. In this study, we defined AS as the anastomotic intestinal canal being positioned at any degree inferior to the adjacent healthy bowel. This is based on the consensus of comparing with the healthy bowel of the same patient, which is considered the most accurate metric for comparison[15]. This setting should not omit any degree of AS; however, nearly all anastomoses are assumed to appear as AS, so we divide AS into five degrees: grade 0 indicated sufficient proximity to a healthy bowel with perfect diameter and elasticity, and grade 1 indicated a sufficiently large lumen but decreased elasticity. In grade 2a, inflammatory adhesions (mainly involved mucosal and submucosal layers in gross pathology[15, 16]) occurred at the anastomosis. In grades 2b and 3, the fibrotic adhesions (involved muscularis mucosa and muscularis propria[15, 16]) developed at the anastomosis. In clinical practice, grades 2a, 2b, and 3 can all manifest as a failure to pass the endoscope; however, the impact on patients varies widely, which is the main reason for the inconsistent clinical results. Our definition and grading system could perfectly explain clinical problems associated with AS, such as why some AS are easily disrupted by digital dilation[17](because they belong to grade 2a) and some had reduced remission success rates even after instrument dilation[5] (because they belong to grade 2b or 3). The main doubt about this definition and grading system may be whether it is affected by individual differences among examiners. Therefore, we performed a consistency analysis, and there were no significant differences among the examiners.

There are few independent studies discussing the effect of AS on bowel function, and if there is any, it is usually mentioned in the studies on AL and bowel function[18]; the main reason is still the definition of AS. All these yes or no criteria for defining AS should miss many cases of poor passage, leading to significant deviation in functional studies. Whereas our definition and grading system perfectly accommodate all cases and can comprehensively evaluate the effect of AS on bowel function. The LARS score was used in this study to evaluate bowel function. A major advantage of the validated LARS score is that it can easily identify patients with impaired bowel function and quality of life[14], and it is easier to use and more objective than the other scoring systems that have been used to evaluate functional outcomes after low anterior resection[19]. This study is the first to evaluate the correlation between AS and LARS severity. In our study, as time passed, the severity of AS gradually decreased, and the severity of LARS decreased accordingly. Generally, more severe LARS mean more severe AS, and low AS levels also indicate mild LARS. Our findings may help to optimize the management of these cases postoperatively. A poor LARS score usually indicates the need for early intervention for AS, especially for grade 2a. The earlier the intervention, the easier the transition to a lower level and the alleviative LARS.

For the same reasons mentioned above, the risk factors analysis based on whether they could pass the endoscope is also prone to inconsistent results. In this study, male sex, defunctioning stoma, NCRT, chemotherapy, and AL were the higher risk factors for AS based on the univariate analysis; however, sex and defunctioning stoma showed no significant difference in the multivariate analysis. First, regarding sex, one study identified the male sex as a higher risk factor for AS[20], and another reported that the female sex was associated with an approximately 2-fold increased risk of developing AS[21]. In this study, the multivariate analysis failed to confirm sex as a risk factor for AS, indicating that sex -related differences in AS may be associated with other factors such as AL. Second, regarding defunctioning stoma, some studies suggest that defunctioning stoma leads to more AS[8, 22]; however, in this study, the multivariate analysis also failed to confirm defunctioning stoma as a higher risk factor for AS. The main reason might be that the defunctioning stoma increases the proportion of grade 2a (41.4% vs. 21.9% at 1 month, 38.0% vs. 11.8% at 3 months, both p < 0.001), which would sometimes manifest as an inability to pass through an endoscope if no digital dilation was performed before endoscopy[20]. Third, regarding NCRT, most studies have confirmed that NCRT is a high-risk factor for AS[4, 5, 7, 23], consistent with our study's result. For our special grading system, the results showed that more severe grades of AS were present in patients who received NCRT, especially in grades 2b and 3 (70.5% VS. 6.5% and 16.2% VS. 1.9% for the patients with and without NCRT, both p < 0.001). Fourth, regarding chemotherapy, few studies investigated the effect of chemotherapy on anastomotic healing. One study showed that preoperative chemotherapy was significantly associated with the development of AL[24]. In this study, we did not separate preoperative and postoperative chemotherapy because the chemotherapy’s effects on anastomosis may be gradual and delayed, and the results showed that chemotherapy was a higher risk factor for AS. Fifth, regarding AL, AL will inevitably cause hyperplasia and fibrosis around the anastomosis, which would gradually aggravate AS’s severity. In this study, all patients with AL showed severe AS, which was significantly more severe than that in patients without AL, consistent with existing studies[4, 25]. Finally, age, BMI, diabetes, angiocardiopathy, ligation site of IMA, blood perfusion evaluated with ICG, surgical approach, anastomotic method, and distance from anastomosis to anal verge did not show a significant effect on AS in this study. All of these factors have been studied to see if they can affect AS; some are considered significant, some are not, and some are similarly controversial. The typical factor is an anastomotic method. One study showed that stapled anastomosis is considered to cause more severe AS than handsewn anastomosis[26], and another showed that AS was significantly less frequent in the stapled than handsewn anastomosis[27]. Regarding other factors, such as age, Greenwald found that age is a risk factor for AS due to the reduced blood flow linked to atherosclerosis and the decline in perfusion in elderly patients[28]. Furthermore, factors such as the ligation site of IMA have also been studied; studies found that low ligation may result in a reduced rate of AS following colorectal cancer surgeries and then suggest that low ligation should be preferred over high ligation[22, 29]. Another factor is blood perfusion evaluated using ICG, which significantly reduces AL and AS rates[30]. However, none of these factors thought to influence AS was identified as meaningful in this study.

This study has some limitations. First, this system is only suitable for rectal surgery. Second, this study lacked further follow-up data; the longer the time, the more loss in follow-up by the designated examiners. Finally, some factors were not studied due to the limitation of the single center. Typical examples are stapler sizes. One study showed that 25–29 mm EEA staplers were associated with an increased rate of AS compared with 30–33 mm staplers[31]. In contrast, another showed that using 25 mm circular staplers is safe and does not increase the risk of AS compared with larger staplers[17]. Since all the staplers we used were 28 or 29 mm, there is no analysis of the factors of stapler size in this study.

In conclusion, in this study, a special AS definition and grading system was used to determine low anastomosis after TME. Through the evaluation of this system, we noted that the severity of AS significantly affected bowel function, and multivariate analysis showed that NCRT, chemotherapy, and AL were higher risk factors for AS.

Author contribution Study conception and design: Jinchun Cong,Hong Zhang and Chunsheng Chen. Acquisition of data: Jinchun Cong,Hong Zhang and Chunsheng Chen. Analysis and interpretation of data: Jinchun Cong. Drafting of manuscript: Jinchun Cong. Critical revision: Jinchun Cong,Hong Zhang and Chunsheng Chen.

Fund/Support: None

Declarations

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All authors have read and approved the manuscript.

Conflict of interest

The authors declare no competing interests.

Disclaimers, for example, conflicts of interest, use of off-label or unapproved drugs or products, use of previously copyrighted material:

The authors declare that they have no conflict of interest.

Source(s) of support (i.e. grants, equipment, drugs) or state if there is no funding:

None

State if manuscript has been or will be a podium or poster meeting presentation:

This manuscript has not been published or presented elsewhere in part or in entirety and is not under consideration by another journal.

Category of the paper:

Colorectal/Anal neoplasia

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No competing interests reported.

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Definition and grading of anastomotic stricture/stenosis following low anastomosis after total mesorectal excision: A single-center study

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Abstract

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Introduction

Patients And Methods

Patients

Surgical procedures

Definition of AS

Bowel function assessment

Statistical analysis

Results

Discussion

Conclusion

Declarations

References

Additional Declarations

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