Retrospective Study Open Access
Copyright ©The Author(s) 2025. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastrointest Surg. Jan 27, 2025; 17(1): 98269
Published online Jan 27, 2025. doi: 10.4240/wjgs.v17.i1.98269
Laparoscopic intracorporeal anastomosis vs open anastomosis for ileostomy reversal in Crohn's disease: A single center retrospective study
Wei-Hang Liu, Mao Xiong, Guo-Qing Chen, Zhui Long, Chao Xu, Li Zhu, Jing-Song Wu, Department of General Surgery, Chongqing General Hospital, Chongqing 401120, China
ORCID number: Zhui Long (0009-0002-0139-880X); Jing-Song Wu (0009-0008-2341-5045).
Co-first authors: Wei-Hang Liu and Mao Xiong.
Author contributions: Liu WH and Xiong M contribute equally to this study as co-first author; Wu JS, Liu WH, Xiong M and Chen GQ contributed to the conception and design of the study; Wu JS, Liu WH and Xiong M completed laparoscopic surgery; Li Z is accountable for the ongoing management of stoma care for patients in the long term; Liu WH, Xiong M and Long Z collected clinical data; Liu WH performed the statistical analysis and wrote the manuscript; Chen GQ and Wu JS reviewed the manuscript; all authors contributed to the manuscript and approved the submitted version.
Supported by Chongqing Municipal Health Commission Medical Research Project, No. 2023WSJK104.
Institutional review board statement: Ethical approval was obtained from the Ethics Committee of Chongqing General Hospital, Chongqing, People's Republic of China (approval No. KY S2022-101-01).
Informed consent statement: In consideration of the retrospective design of this study, the requirement for informed patient consent was waived.
Conflict-of-interest statement: The author declares that there are no conflicts of interest regarding the publication of this article.
Data sharing statement: No additional data are available.
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: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Jing-Song Wu, PhD, Professor, Department of General Surgery, Chongqing General Hospital, No. 118 Starlight Avenue, Chongqing 401120, China. wjsrmyy@163.com
Received: June 22, 2024
Revised: October 24, 2024
Accepted: November 12, 2024
Published online: January 27, 2025
Processing time: 187 Days and 23.9 Hours

Abstract
BACKGROUND

There is an increased maturation of laparoscopic intracorporeal anastomosis techniques. However, research on its application for small bowel stoma reversal in patients with Crohn's disease (CD) is limited. Therefore, in this study, we compared the perioperative outcomes between laparoscopic intracorporeal ileostomy reversal (LIIR) and open ileostomy reversal (OIR).

AIM

To compare the safety, feasibility, bowel function recovery, and short- and long-term LIIR and OIR outcomes in patients with CD.

METHODS

This study included patients who underwent ileal reversal for CD between January 2021 and January 2023 at our institution. The baseline data, postoperative recovery, and complication indicators were retrospectively analyzed. Logistic regression analysis was conducted to explore factors that significantly influenced the development of enteral nutrition intolerance-related symptoms.

RESULTS

Notably, 15 of the 45 patients in this study underwent OIR, and the remaining 30 received LIIR. Notably, no statistically significant differences were found between the two groups regarding clinical baseline characteristics, operation time, intraoperative hemorrhage, anastomotic site, enterolysis range, first postoperative flatus, postoperative complications, reoperation rate, or incidence of postoperative enteral nutrition intolerance. Compared with the OIR group, the LIIR group had a shorter postoperative hospital stay (P = 0.045), lower incidence of enteral nutrition intolerance symptoms (P = 0.019), and earlier postoperative total enteral nutrition initiation (P = 0.033); however, it incurred higher total hospital costs (P = 0.038). Furthermore, multivariate logistic regression analysis revealed that the duration of surgery and anastomotic technique were independent risk factors for postoperative symptoms of enteral nutrition intolerance (P < 0.05).

CONCLUSION

Laparoscopic intracorporeal anastomosis for ileostomy reversal is safe and feasible. Patients who underwent this technique demonstrated improved tolerance to postoperative enteral nutrition and quicker resumption of total enteral nutrition.

Key Words: Crohn’s disease; Ileostomy reversal; Laparoscopic intracorporeal anastomosis; Enteral nutrition intolerance; Total enteral nutrition

Core Tip: The maturation of laparoscopic intracorporeal anastomosis techniques is on the rise. However, there is limited research on its application in small bowel stoma reversal for patients with Crohn's disease. This study aims to investigate perioperative outcomes associated with laparoscopic intracorporeal ileostomy reversal compared to open ileostomy reversal. The use of laparoscopic intracorporeal anastomosis for ileostomy reversal is both safe and feasible. The results showed that patients undergoing this technique demonstrate improved tolerance to postoperative enteral nutrition and a quicker resumption of total enteral nutrition.



INTRODUCTION

Crohn's disease (CD), a chronic non-specific inflammatory disease with a lifelong recurrence tendency, can affect the entire gastrointestinal tract, and surgical intervention often results in complications, such as perforations, fistulas, and strictures[1-3]. Following ileocolonic resection, the incidence of anastomotic fistulae is notable, leading to the adoption of protective ileostomy in a significant proportion of patients[4]. However, ileostomies are associated with increased complications and pose greater difficulties in terms of care[5]. Consequently, many patients strongly desired stomatal reversal.

Previous studies have shown that patients who underwent ileostomy reversal through laparoscopic intracorporeal anastomosis experienced improved short-term postoperative outcomes compared with those who underwent conventional open surgery[6,7]. Therefore, surgical release of abdominal adhesions is frequent in patients with CD[8]. The laparoscopic technique proves effective in enterolysis and avoids the extension of incisions and exposure of the bowel outside the body when addressing fibrous strictures and intestinal fat crawls. However, few studies have investigated the laparoscopic intracorporeal anastomosis technique for ileostomy reversal in patients with CD. Therefore, in this study, we primarily aimed to evaluate the safety and feasibility of laparoscopic intracorporeal anastomosis for ileostomy reversal in patients with CD.

MATERIALS AND METHODS
Patient’s clinical characteristics

This study included 55 patients with CD who underwent ileostomy reversal surgery at our institution between January 2021 and January 2023. Ethical approval was obtained from the Ethics Committee of Chongqing General Hospital, Chongqing, People's Republic of China (approval No. KY S2022-101-01), and adhered to the ethical standards outlined in the Declaration of Helsinki. Before ileostomy reversal therapy, all patients underwent preoperative colonoscopy and small intestinal computed tomography enterography to assess the viability of the procedure. A senior operator who is an experienced surgeon dedicated to the surgical management of CD performed the surgeries. Notably, patients who underwent concomitant bowel resection or stricture plasty were excluded from the study (Figure 1).

Figure 1
Figure 1 Flow chart.

Furthermore, all participants had prior experience with preoperative enteral nutrition through the use of nasogastric tubes. They could successfully perform enteral nutrition independently or with the assistance of a nurse. The clinical characteristics of the patients included sex, age, body mass index (BMI), American Society of Anesthesiology (ASA) score, surgical history, stoma duration, and preoperative blood indicators (Table 1).

Table 1 Baseline clinical characteristics of patients.
Characteristics
OIR
LIIR
P value
Age (years)28 (25-33)26.5 (18.75-32)0.242
Sex0.526
Male6 (40)15 (50)
BMI (kg/m2)19.5 (17.4-21.3)18.55 (17.85-19.375)0.166
ASA 0.092
    I-II10 (66.67)12 (40)
    III-IV5 (33.33)18 (60)
Duration of ileostomy retention (months)8 (6-9)6.5 (6-10)0.836
Medication0.446
Immunosuppressant2 (13.33)1 (3.33)
Biologics12 (80)27 (90)
5-ASA1 (6.7)2 (6.67)
WBC (109/L)6.150 ± 1.4056.198 ± 1.5220.92
NE (109/L)4.221 ± 1.3773.802 ± 1.5890.389
LYM (109/L)1.2 (1.01-1.38)1.315 (1.18-1.538)0.393
PLT (109/L)271.27 ± 59.977247.33 ± 62.6430.227
Hb (g/L)131.13 ± 6.312135.10 ± 9.7670.161
ALB (g/L)44.267 ± 6.34444.043 ± 4.1780.888
CRP (mg/L)1.22 (0.79-2.58)0.885 (0.77-8.158)0.895
ESR (mm)15 (8-18)10.5 (6-15.25)0.091

The surgical outcomes included operative time, estimated hemorrhage, anastomotic site, enterolysis, mechanical exhaust time, postoperative complications, length of hospitalization, and hospital costs. Additionally, the total enteral nutrition time, symptoms of enteral nutrition intolerance and enteral nutrition intolerance were recorded. Symptoms of enteral nutrition intolerance were defined as abdominal pain, bloating, nausea, vomiting, diarrhea, and an enteral nutrition tolerance score ≥ 3[9]. Enteral nutrition intolerance was characterized by an enteral nutrition tolerance score ≥ 5 and the interruption of enteral nutrient supply for > 24 hours[9].

Incision infections were defined as superficial or deep subcutaneous infections occurring within 7 days postoperatively[10]. Postoperative intestinal obstruction was defined as nausea/vomiting, abdominal distension, and gastrointestinal radiography or computed tomography scans showing a dilated intestinal lumen with gas and fluid accumulation[11]. Enterolysis is classified into two distinct categories: Enterolysis confined solely to the peri-ileostomy region and enterolysis extending proximally and distally from the ileostomy site.

Surgical procedure and postoperative enteral nutrition

Laparoscopic intracorporeal ileostomy reversal group: Notably, a 10 mm trocar was created as an observation hole, with approximately two transverse fingers (approximately 2-4 cm) below the navel (Figure 2A). Furthermore, to minimize the risk of intestinal puncture injuries due to abdominal adhesions, we preferred to create a visual aperture under direct open observation as opposed to directly puncturing the abdomen. Therefore, a 12 mm trocar and a 5 mm trocar were established on the left side of the abdomen. If abdominal and pelvic adhesions hindered the insertion of a 5 mm trocar on the right side, the successful creation of the right trocar was achieved through initial enterolysis (Figure 2B). In addition, adequate separation of abdominal adhesions around the stoma and distal bowel was performed to achieve sufficient anastomotic length and avoid tension (Figure 3A). The proximal segment of the intestine adjacent to the stoma was cut off (Figure 3B). Following the skin around the stoma was incised, and the intestinal tube attached to the cutaneous surface was removed. The entire gastrointestinal tract was examined for the presence of fibrous strictures, and surgical interventions such as partial bowel resection or stricture plasty were performed in cases deemed necessary. An intestinal side-to-side anastomosis was performed using a universal cutting stapler (Figure 3C). Laparoscopic closure of the common opening was achieved using a 3-0 absorbable suture, simultaneously reinforcing the anastomosis and the common opening (Figures 3D and E).

Figure 2
Figure 2 Establishment of pneumoperitoneum and initial enterolysis. A: Location of pneumoperitoneum and trocar puncture; B: In the abdominal cavity, adhesions obstructed the right 5 mm trocar puncture, and initial enterolysis assisted the trocar puncture.
Figure 3
Figure 3 Brief surgical procedure. A: Laparoscopic enterolysis; B: Cutting off the proximal intestine of the stoma and closure of the bowel stump; C: Isoperistaltic side-to-side anastomosis; D: Absorbable barbed suture is used to close the common opening; E: Suture closure of mesenteric lacunae; F: Minimally invasive abdominal incision.

Open ileostomy reversal group: Open surgery involved creating an incision in the midline or right paracentral midline of the abdomen, followed by enterolysis and extra-incisional examination of the bowel under direct visual guidance. The incision was extended to an appropriate length based on the requirements for enterolysis. The anastomosis was performed using the same method as that used in the laparoscopic surgery group, conducting an isoperistaltic side-to-side anastomosis with the mesentery of the anastomotic segments of the intestine opposing each other[12].

Studies have shown the benefits of enteral nutrition in children and adults with CD[13]. Guidelines, including those from the European Society for Clinical Nutrition and Metabolism and the European Crohn's and Colitis Organization, recommend the use of enteral nutrition whenever possible to induce remission in patients with CD[14,15]. Therefore, in addition to appropriate water intake after the passage of flatus during the postoperative period, it is crucial to gradually increase the intake of enteral nutritional preparations rather than normal food. The specific method involves pumping Enteral Nutritional Emulsion (TP, 500 mL/bag) through the nasogastric tube using an enteral feeding pump, starting at an initial rate of 20 mL/hour and gradually increasing to 100-150 mL/hour, adjusting the dosage based on the patient's tolerance until complete enteral nutrition is achieved to meet daily energy requirements. Symptoms such as abdominal pain or bloating, nausea or vomiting, diarrhea, and a tolerance score ranging from 3 to 4 required a reduction in nasal feed and reassessment after 2 hours. Tolerance scores ≥ 5 necessitate the suspension of enteral nutrition, pending reassessment, and gradual reintroduction of enteral feeding.

Statistical analysis

Data were statistically analyzed utilizing SPSS27. The t-test was employed for continuous variables that exhibited a normal distribution and satisfied the criteria of homoscedasticity. However, the Mann-Whitney U test was used for variables that did not meet these conditions. Categorical variables were analyzed using the χ2 or Fisher's exact tests. Univariate logistic regression analysis was performed on the candidate variables, and significant parameters were further verified using multivariate logistic regression analysis. Statistical significance was set at P values < 0.05.

RESULTS

Among all the patients, 30 underwent laparoscopic surgery, 15 underwent open surgery, and there were no conversions in the laparoscopic group. The statistical analysis revealed no statistically significant differences between the two groups regarding age, sex, BMI, ASA classification, stoma carrying duration, medication usage, and hematologic examination (P > 0.05; Table 1). Similarly, there were no statistically significant differences between the two groups regarding operative time, intraoperative hemorrhage, anastomotic site, extent of enterolysis, or first postoperative flatus time (P > 0.05; Table 2). Regarding surgical complications, the laparoscopic intracorporeal ileostomy reversal (LIIR) group exhibited a comparatively lower complication rate than the open ileostomy reversal (OIR) group; however, the difference between the two groups did not reach statistical significance (P > 0.05; Table 2). Regarding hospitalization expenditure, the OIR group demonstrated significantly lower than the LIIR group (34111 RMB vs 36211 RMB, P = 0.038). Subgroup analysis revealed a lower incidence of feeding intolerance symptoms in the LIIR group than in the OIR group (14.29% vs 53.85%, P = 0.019).

Table 2 Intraoperative and postoperative outcomes.
Variables
OIR
LIIR
P value
Operation time, minutes194.4 ± 23.194191.4 ± 34.1520.761
Intraoperative hemorrhage (mL)100 (70-100)70 (60-100)0.091
anastomotic site0.118
Ileum-ileum4 (26.67)16 (53.33)
Ileum-colon11 (73.33)14 (46.67)
Enterolysis range0.14
Around ileostomy5 (33.33)17 (56.67)
Distal and proximal bowel10 (66.67)13 (43.33)
First postoperative flatus, days2 (2-3)2 (1-2.25)0.128
Postoperative complication4 (26.67)5 (16.67)0.454
Anastomotic hemorrhage0 (0)2 (6.67)0.545
Anastomotic leakage0 (0)0 (0)1
Wound infection2 (13.33)1 (3.3)0.254
Postoperative ileus2 (13.33)2 (6.67)0.591
Reoperation0 (0)2 (6.67)0.545
Postoperative days in the hospital, days13 (11-16)11 (10-12.25)0.045
Total hospitalization costs (RMB)34111 (31240-37892)36211 (33220.25-40116.75)0.038

Furthermore, the total enteral nutrition intolerance symptoms were less prevalent in the LIIR group (P = 0.019); however, the subgroups of nutrition intolerance symptoms including abdominal pain/bloating, nausea/vomiting, and diarrhea between the two groups was not statistically significant (P > 0.05; Table 3). In the postoperative analysis of long-term complications, it was observed that two patients in the LIIR group underwent reoperation; however, this outcome was not statistically significant (P > 0.05). The median time to start postoperative total enteral nutrition was 6 days in both groups; however, the LIIR group started postoperative total enteral nutrition earlier than the OIR group (P = 0.033; Table 3). Logistic one-way analysis of variance indicated that enterolysis range, operation time, OIR, and LIIR were associated with the development of postoperative enteral nutrition intolerance symptoms (P < 0.05; Table 4). The multifactorial analysis highlighted that operation time and OIR or LIIR were critical factors causing symptoms of postoperative enteral nutrition intolerance in patients (P < 0.05; Table 4).

Table 3 Clinical outcomes for enteral nutrition intolerance.
Variables
OIR
LIIR
P value
Total symptoms of feeding intolerance7 (53.85)4 (14.29)0.019
Abdominal distension/pain5 (38.46)3 (10.71)0.084
Nausea/vomiting2 (15.38)0 (0)0.095
Diarrhea5 (38.46)4 (14.29)0.113
Enteral nutrition intolerance3 (23.08)3 (10.71)0.361
Time to total enteral nutrition (days)6 (6-8.5)6 (5-6)0.033
Table 4 Logistic multifactorial regression analysis of postoperative symptoms of enteral nutrition intolerance.
Variables
Univariate analysis
Multivariate analysis
OR (95%CI)
P value
OR (95%CI)
P value
Sex1.750 (0.422-7.253)0.44
Age0.988 (0.908-1.073)0.768
BMI1.342 (0.875-2.059)0.178
Duration of stoma retention1.309 (0.980-1.748)0.068
anastomotic site5.143 (0.947-27.921)0.058
Enterolysis range4.606 (1.007-21.072)0.0491.673(0.250-11.217)0.596
Operation time1.054 (1.013-1.095)0.0091.059(1.005-1.115)0.031
anastomotic technique0.143 (0.031-0.653)0.0120.120(0.017-0.862)0.035
DISCUSSION

With the advancement of laparoscopic techniques, intracorporeal anastomosis has become widely used in gastrointestinal surgery. Therefore, in this retrospective analysis, we aimed to compare the safety and feasibility of LIIR and OIR. Our results showed that both surgical methods took longer and had similar durations. Royds et al[16] reported that the reversal time for laparoscopic ileostomy was longer than that for open surgery (65 minutes vs 50 minutes); however, this difference was not statistically significant. Furthermore, during laparoscopic-assisted surgery for ileostomy reversal in patients with CD, the operation time was shorter compared with open surgery (128.2 ± 41.7 minutes vs 142.5 ± 41.7 minutes); however, this difference was not statistically significant[17]. This disparity may be attributed to the higher frequency of adhesion enterolysis required for ileostomy reversal in patients with CD compared with that after proctocolectomy and the need for extensive intraoperative examination of the small intestine before intracorporeal anastomosis, resulting in a prolonged operation time. The LIIR group exhibited higher inpatient costs than the OIR group, potentially because of the elevated expenses associated with laparoscopic surgery and surgical instruments compared with open surgery.

Furthermore, in this study, there was no statistically significant difference between the two groups regarding the time to the first postoperative flatus. Previous studies have found that patients who undergo totally laparoscopic ileostomy have an earlier first flatus and faster return of bowel function after surgery[6,18]. Laparoscopic surgery is associated with reduced surgical trauma and enables early mobilization of patients. Moreover, laparoscopic intracorporeal anastomosis minimizes manipulation of the mesentery, which is a critical factor in promoting postoperative bowel function recovery[19]. The results of our study demonstrated a significantly shorter duration of hospitalization in the LIIR group compared with the OIR group, which is consistent with previous research findings[6,20-22].

Previous research has demonstrated the advantages of intracorporeal laparoscopic ileostomy reversal in reducing postoperative complications compared with open surgery[6,16,21]. The postoperative complication rates for OIR and LIIR in our study were 26.67% and 16.67%, respectively, which is consistent with previous findings from scholarly reports[18,23]. The primary postoperative complications included incisional infection and postoperative bowel obstruction. Factors contributing to incisional infections include the extension of open surgical incisions, irritant dermatitis surrounding small bowel stomas, and nutritional risks. Additionally, some patients experience delayed recovery of bowel function postoperatively and may even develop postoperative ileus.

Notably, some studies have suggested that extracorporeal anastomosis is a more reliable approach because of the frequent presence of mesenteric and vascular thickening in CD cases[17]. However, our surgical observations revealed that enlarged lymph nodes or mesenteric thickening were not observed around the bowel in all cases, which is consistent with previous findings[24]. Moreover, thickened mesentery and enlarged lymph nodes did not increase the risk of complications[24]. During the anastomotic procedure, we ensured adequate freeing of the proximal and distal bowels to preserve the optimal anastomotic length and minimize tension. Therefore, by employing the isoperistaltic side-to-side anastomosis technique, the mesentery of the anastomotic segments is positioned opposite each other, effectively preventing anastomotic and mesenteric hemorrhage while ensuring that the anastomosis aligns with the intestinal peristalsis (Figure 3C-F).

Enteral nutrition therapy has gained consensus as an effective approach for mitigating intestinal inflammatory responses and treating CD[13,25]. Notably, some studies have shown that total parenteral nutrition is crucial in optimizing nutritional status, regulating intestinal flora, and protecting epithelial barrier function in patients with CD postoperatively[26,27]. Previous studies have also demonstrated that early enteral nutrition during laparoscopic colorectal surgery is associated with reduced hospitalization duration and accelerated recovery compared with open surgery[28]. In the long term, total enteral nutrition demonstrated significant efficacy in reducing the occurrence of surgical recurrence after CD surgery[29-31]. Therefore, the early administration of enteral nutritional preparations following ileostomy reversal is imperative for patients with CD. However, research has shown that early enteral nutrition after intestinal surgery increases the incidence of postoperative vomiting[32]. This may cause patients to experience symptoms of enteral nutrition intolerance. However, the etiology of enteral nutrition intolerance remains unclear and may be associated with systemic inflammatory responses, metabolic imbalances, and diminished gastrointestinal motility[33,34]. In our study, the incidence of postoperative symptoms associated with enteral nutrition intolerance was lower in the LIIR group than in the OIR group, and total enteral nutrition was resumed earlier during the postoperative period.

Furthermore, our study revealed a higher incidence of enteral nutrition intolerance symptoms following ileocolonic anastomosis compared with that observed after ileal-ileal anastomosis, which may be associated with the absence of the ileocecal valve[35]. We also found that the prolonged operative duration and open surgical procedures were associated with postoperative symptoms of enteral nutrition intolerance in patients. Therefore, a shorter operation time can reduce the impact of anesthesia and surgery and is beneficial for the recovery of the patient's intestinal function postoperatively[36]. As mentioned above, LIIR helps postoperative patients receive early full enteral nutrition and alleviates symptoms of enteral nutrition intolerance.

This is the first study to examine the safety and feasibility of the laparoscopic intracorporeal anastomosis technique for ileostomy reversal in patients with CD. The limitations of this study are its retrospective nature and small sample size, potentially introducing bias into the results. Therefore, prospective multicenter studies are required to verify the generalizability of our results.

CONCLUSION

The laparoscopic intracorporeal anastomosis technique for ileostomy reversal is safe and viable. Moreover, it facilitates the recuperation of bowel function in patients, thereby promoting earlier attainment of total enteral nutrition. However, this was a single-center retrospective study; therefore, further multicenter prospective studies are required.

Footnotes

Provenance and peer review: Unsolicited article; Externally peer reviewed.

Peer-review model: Single blind

Specialty type: Gastroenterology and hepatology

Country of origin: China

Peer-review report’s classification

Scientific Quality: Grade A, Grade C

Novelty: Grade A, Grade B

Creativity or Innovation: Grade B, Grade B

Scientific Significance: Grade A, Grade B

P-Reviewer: Abdelsamad A S-Editor: Lin C L-Editor: A P-Editor: Xu ZH

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