Colocolic intussusception in children: A case series and literature review


 Background

Colocolic intussusceptions is a rare subtype of intussusception mostly caused by juvenile polyps. The treatment of colocolic intussusception caused by other pathologic lead points remains poorly understood.
Methods

A systematic literature review between January 2000 and June 2021 was performed to characterize the comprehensive treatment of colocolic intussusception in children. This report also included 10 patients admitted to our center between 2010 and 2020 not previously reported in the literature.
Results

We identified 27 patients in 20 studies in addition to 10 patients from our center for a total of 37 patients (median age, 4.0 years; 54.1% male). The lead point was identified in 33 patients (33/37, 89.2%). The most common lead point was juvenile polyps (16/33, 48.5%). A therapeutic enema was performed in 12 patients with colocolic intussusception caused by juvenile polyps and was successful in 8 patients (8/12, 66.7%). Colonoscopic polypectomy was subsequently performed in 7 patients and was successful in 6 patients (6/7, 85.7%). The other patient had undergone laparoscopic exploration, and no abnormality was found. Subsequently, the patient underwent open surgery. The patients with colocolic intussusception caused by other pathologic lead points almost underwent surgical treatment (14/17, 82.4%), including 12 open surgeries and 2 laparoscopic surgeries.
Conclusion

A therapeutic enema followed by colonoscopic polypectomy is feasible to treat colocolic intussusception caused by juvenile polyps unless the patient has bowel perforation; however, open surgery is sometimes needed. For patients with colocolic intussusception caused by other pathologic lead points, open surgery may be preferable to laparoscopic surgery.


Abstract Background
Colocolic intussusceptions is a rare subtype of intussusception mostly caused by juvenile polyps. The treatment of colocolic intussusception caused by other pathologic lead points remains poorly understood.

Methods
A systematic literature review between January 2000 and June 2021 was performed to characterize the comprehensive treatment of colocolic intussusception in children. This report also included 10 patients admitted to our center between 2010 and 2020 not previously reported in the literature.

Results
We identi ed 27 patients in 20 studies in addition to 10 patients from our center for a total of 37 patients (median age, 4.0 years; 54.1% male). The lead point was identi ed in 33 patients (33/37, 89.2%). The most common lead point was juvenile polyps (16/33, 48.5%). A therapeutic enema was performed in 12 patients with colocolic intussusception caused by juvenile polyps and was successful in 8 patients (8/12, 66.7%). Colonoscopic polypectomy was subsequently performed in 7 patients and was successful in 6 patients (6/7, 85.7%). The other patient had undergone laparoscopic exploration, and no abnormality was found. Subsequently, the patient underwent open surgery. The patients with colocolic intussusception caused by other pathologic lead points almost underwent surgical treatment (14/17, 82.4%), including 12 open surgeries and 2 laparoscopic surgeries. Conclusion A therapeutic enema followed by colonoscopic polypectomy is feasible to treat colocolic intussusception caused by juvenile polyps unless the patient has bowel perforation; however, open surgery is sometimes needed. For patients with colocolic intussusception caused by other pathologic lead points, open surgery may be preferable to laparoscopic surgery.

Background
Intussusception is one of the most common abdominal emergencies in children. It often occurs near the ileocecal junction and rarely only involves the colon [1,2]. Approximately 90% of ileocolic intussusception cases are idiopathic, and most can be resolved by nonoperative reduction with therapeutic enema [2,3]. However, almost all colocolic intussusceptions are caused by pathologic lead points and should be treated with surgical interventions, including colonoscopic polypectomy, open surgery or laparoscopic surgery [4][5][6][7][8]. The most common lead point in colocolic intussusception is juvenile polyps [6].
The available literature on colocolic intussusception is sparse, at best, and consists mainly of case reports. Some case reports have shown that a successful therapeutic enema followed by colonoscopic polypectomy is feasible to treat colocolic intussusception caused by a juvenile polyp, but open surgery is still used in most cases [6,7,9]. Additionally, the effect of laparoscopic surgery on colocolic intussusception is controversial and that the treatment of colocolic intussusception caused by other lead points remians still poorly understood. Thus, we performed this retrospective study to summarize the clinical features of colocolic intussusception using the largest sample size in China and a review of the literature to provide evidence that could be used to improve treatment in clinical practice [10].

Study population
After approval by the Ethics Committee of Beijing Children's Hospital (approval number [2021]-E-090-R), the medical records of all children diagnosed with intussusception and admitted to Beijing Children's Hospital between January 2010 and December 2020 were retrospectively reviewed. Patients diagnosed with colocolic intussusception and con rmed by colonoscopy or open surgery were included. The collected data included demographics, clinical symptoms, accompanying malformations, imaging data, clinical interventions, and pathological data.

Search strategy
The study was performed in accordance with the PRISMA guidelines. The following databases were searched through June 30, 2021: PubMed, Web of Science and the Cochrane Library. Search strings included colocolic intussusception, pediatric, child and children ( Table 1). The reference lists of the relevant studies were manually-searched to identify other potentially appropriate studies. Retrospective studies, including case reports and case series that assessed the treatment of colocolic intussusception, were included. Studies investigating adults, reviews, studies not written in English, studies lacking complete data, and studies without the outcomes of interest were excluded. Additionally, to explore the progress of the treatment of colon intussusception and provide evidence that would be useful in clinical practice, studies published before 2000 were also excluded.

Authors' cases
A total of 1278 patients were diagnosed with intussusception and admitted to Beijing Children's Hospital between January 2010 and December 2020. Among these patients, 10 (0.8%) were diagnosed with colocolic intussusception; these patients are listed in Table 2.
The median age at presentation was 3.3 (2.8, 5.7) years, and 3 patients were male. Six patients had been misdiagnosed at other hospitals. Abdominal ultrasound was performed in all patients, with a positive rate of 100.0%. Juvenile polyps were identi ed as the lead point in 8 patients, and 6 had polyps situated in the left colon. Therapeutic air enema was performed in 6 patients diagnosed with colonic polyps by ultrasound that successfully reduced intussusception in 5 patients. Among the patients in whom therapeutic air enema was successful, 4 with pedunculated polyps underwent colonoscopic polypectomy, and the other patient, who had a sessile polyp, underwent segmental colonic resection. The patient in whom the therapeutic enema was unsuccessful was treated with segmental colonic resection. Colon duplication was identi ed as the lead point on ultrasound in 2 patients, and surgical reduction with segmental colonic resection was subsequently performed. Total colonic duplication a The patient underwent resection of the duplicated colon distal to the ascending colon and a side-to-end colon anastomosis due to total colon duplication at 2 months
The diagnosis and treatment of patients are summarized in

Discussion
Colocolic intussusceptions in children are far less common than ileocolic intussusceptions, occurring in less than 5% of most case series except on the African continent, and most have a pre-existing colonic pathology acting as a lead point [5,6,25,26]. The incidence of colocolic intussusception was 0.8% at our center, a value lower than that reported in the literature. The reason might be related to ethnic and geographic differences. Additionally, patients with intussusception treated successfully by air enema at the outpatient department were not included in our case series, which affected the incidence. A review of the studies published in the past 20 years showed that unlike the male predominance reported in previous studies on all types of intussusception, no such predominance was identi ed among patients with colocolic intussusception, as reported in previous surveys [26]. Our study also con rmed that the age at the development of colocolic intussusception was older on average than that of patients with ileocolic intussusception [27,28]. The reason might be associated with pathologic lead points, such as juvenile polyps, which occur most commonly in children older than 2 years of age [29].
The clinical symptoms of abdominal pain, bloody stool and vomiting are often considered the main features of intussusception.
However, less than 25% of patients have this classic triad, leading to a delayed diagnosis or misdiagnosis [30]. Among patients with colocolic intussusception in our study, the proportion with the above classic triad was as high as 43.2%, but 37.8% were still misdiagnosed. The reason was mainly related to the less severe symptoms of the patients at the initial visit, lack of imaging examination or successive occurrence of the above symptoms [5,6]. Our study also con rmed that, unlike patients with ileocolic intussusception who almost always had abdominal masses, a signi cantly lower proportion of patients with colonic intussusception had abdominal masses, most of which were located in the left abdomen; instead, patients with colonic intussusception had a signi cantly higher incidence of rectal masses or prolapse. Both ultrasound and computed tomography are useful tools to diagnose intussusception [31]. Ultrasound is recommended rst and should be used at the initial visit for all children with the above symptoms and a clinical suspicion of intussusception, including colocolic intussusception [32].
Given the pathologic lead points found in most colocolic intussusceptions, therapeutic enemas, especially hydrostatic barium enemas, were previously considered to be avoided, and these patients often required open surgery [33]. However, treating colocolic intussusception caused by a pathologic lead point is currently considered the same as treating those without a pathologic lead point, involving a careful attempt at reduction using a minimally invasive approach [7]. Similar to the ndings in the recent systematic review of intussusception, our study suggested that for colocolic intussusception, without peritonitis (e.g., diffuse abdominal tenderness), a therapeutic enema could be performed rst [34]. The success rates of a therapeutic enema to the treat colon intussusception with and without pathologic lead points in our study were 52.9% (9/17) and 75.0% (3/4), respectively. A colonoscopy can be performed to investigate the colon wall and identify the pathologic lead point in patients with successful therapeutic enemas and performing a colonoscopy can sometimes help reduce intussusception in patients in whom the therapeutic enema has been unsuccessful [6, 7].
As described in most studies in the literature, active intervention is required for colocolic intussusception caused by pathologic lead points because the presence of lead points may impair complete reduction of intussusception and the recurrence rate is still high even after a successful therapeutic enema [6, 10,33]. According to our study, juvenile polyps are the most common lead point in patients with colocolic intussusception, and using a therapeutic enema followed by colonoscopic polypectomy was found to be a feasible intervention to treat these patients. Among the 7 patients with successful therapeutic enemas who underwent colonoscopy subsequently, 6 (6/7, 85.7%) had their polyps successfully removed, and 1 with a sessile polyp found during colonoscopy underwent segmental colonic resection. Additionally, to our best knowledge, the current study reported the largest variety of pathologic lead points of colocolic intussusception other than juvenile polyps and found that all patients with colocolic intussusception caused by other pathologic lead points had received surgical interventions (12 open surgeries, 2 laparoscopic surgeries and 2 colonoscopic polypectomies), except for 1 with colocolic intussusception caused by hereditary angioneurotic edema. The main reasons for the increased use of open surgery may be as follows. First, most pathologic lead points were rare, and clinicians lacked the awareness and treatment experience of these intussusception types. Second, even if the intussusception was successfully reduced by therapeutic enema, some pathologic lead points, such as synovial sarcoma and lipoblastoma, could not be removed by colonoscopy.
Third, after successful reduction by therapeutic enema, some pathologic lead points located outside the colon could not be observed by colonoscopy, such as the ileal invagination of the sigmoid colon [12,23,24]. Additionally, Abrahams et al. reported 1 patient with colocolic intussusception caused by a juvenile polyp who had undergone laparoscopic exploration after a successful therapeutic enema, but no abnormality was found; the patient had undergone open surgery subsequently because of the recurrence of symptoms [10]. Thus, open surgery remains the primary treatment in patients with colocolic intussusception and may be preferable to laparoscopic surgery. However, the identi cation rate of pathological lead points by open surgery also did not reach 100.0%. For example, the case of colocolic intussusception caused by capillary hemangioma reported by Utsumi et al. could only be accurately resolved by open surgery with colonoscopic assistance [17]. Further studies with larger samples are needed to con rm this nding.
With advances in ultrasound and computed tomography, an increasing number of patients can be diagnosed with or without pathologic lead points [17,33]. If the colocolic intussusception caused by pathologic lead points was reduced by therapeutic enema, we recommended that patients be hospitalized for a period of time to relieve bowel edema and receiving adequate bowel preparation before deciding the best way to manage the pathologic lead points, an approach that could be helpful for reasonable surgical selection and improve the overall prognosis [7]. However, except for juvenile polyps, identifying the speci c type of lead points preoperatively remains challenging. No study has reported the differences in imaging ndings between different pathologic lead points, which would be helpful to develop a standard diagnosis and treatment procedure for colocolic intussusception in the future.
The study has several limitations. First, all the included studies were retrospective, and the patient population was small. Second, some studies had not fully reported the results, which may have confounded the ndings. Finally, literature reviews did not include all published studies (before 2000), leading to potential bias. A multicenter prospective study of colocolic intussusception is recommended in the future.

Conclusion
A therapeutic enema followed by colonoscopic polypectomy is feasible as a treatment for colocolic intussusception caused by juvenile polyps unless the patient has signs of peritonitis due to bowel perforation; However, open surgery is sometimes needed. For patients with colocolic intussusception caused by other pathologic lead points, colonoscopy can be used as a diagnostic method, and open surgery remains the primary treatment. The role of laparoscopic surgery in colocolic intussusception is debatable.

Declarations Ethics approval and consent to participate
This study adheres to the ethical principles of the Declaration of Helsinki. It was approved by the Ethics Committee of Beijing Children's Hospital ([2021]-E-090-R). For the presented retrospective data, the requirement to obtain informed consent was waived in accordance with the vote of the Ethics Committee of Beijing Children's Hospital.

Consent for publication
Not applicable.

Availability of data and materials
All data generated or analyzed during this study are included in this published article.

Figure 2
Details of the treatment for patients with colocolic intussusception (N = 37)