Clinical, imaging and surgical outcomes of secondary intussusceptions in children: a retrospective analysis based on the benign and malignant pathologic lead points

Introduction

Intussusception is a common condition in the pediatric emergency department (1). While most cases are spontaneous, secondary intussusception accounts for only about 6% of cases (2). Secondary intussusception is defined as an intussusception caused by a pathological lead point (PLP). The PLPs causing secondary intussusception include a variety of diseases, such as Meckel’s diverticulum, intestinal duplication, intestinal polyps, Peutz-Jeghers syndrome, and lymphoma. Meckel’s diverticulum is the most frequently encountered PLP (3). Most PLPs are benign, with only a small proportion being malignant. Lymphoma accounted for a small proportion (6%) of PLPs in intussusception surgeries (4). Analysis of surgical intussusception cases identified lymphoma as the third most common comorbidity in children ≥6 years, present in 17.9% of cases. Due to the rarity of malignant PLPs, clinicians may misdiagnose them.

Air-contrast enema (ACE) is standard for ileo-colic intussusception but usually ineffective for secondary cases, where PLP resection is needed. Malignant PLPs require prompt chemotherapy. England et al. (5) found that combined surgery and chemotherapy achieve favorable outcomes in intussusception secondary to intestinal lymphoma. Given that delayed diagnosis raises complication risks (1), early differentiation of benign and malignant PLPs is critical.

While spontaneous intussusception at Children’s Hospital of Fudan University is usually treated successfully with air enema without admission, this study specifically focuses on inpatients with secondary intussusception, all of whom were confirmed by surgical pathology. This study is the first to conduct a stratified analysis of PLPs based on benign and malignant PLPs. Its aim was to evaluate clinical features, imaging examinations, and intraoperative characteristics of secondary intussusception in order to improve the diagnosis of benign and malignant PLPs. We present this article in accordance with the STROBE reporting checklist (available at https://tp.amegroups.com/article/view/10.21037/tp-2025-533/rc).

Methods

The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the research ethics board of Children’s Hospital of Fudan University (approval No. 2021-252) and individual consent for this analysis was waived due to the retrospective nature. This study is a single-center design. We searched our hospital’s electronic medical record (EMR) system for patients hospitalized with a diagnosis of “intussusception” between January 2012 and December 2023. Our inclusion criteria specifically targeted those patients who received a diagnosis of intussusception during this defined study period. Exclusion criteria: Patients were excluded if they either (I) did not undergo surgery at our hospital (e.g., intussusception resolved with air enema or referred to another hospital), or (II) no PLP was found or resected during surgery. Flow diagram of was shown in Figure 1. We reviewed the clinical records, imaging studies, and intraoperative findings of these 75 patients, all pathologically diagnosed with intussusception secondary to PLPs at our institution.

Figure 1 Flow diagram of patients’ selection. ACE, air-contrast enema; PLP, pathological lead point.

The following clinical and imaging data were collected and analyzed for each patient (Table 1): (I) demographic and clinical characteristics, presence of hematochezia, frequency of intussusception episodes, and recurrence rate of intussusception prior to surgical intervention; (II) primary imaging examinations; (III) Intraoperative findings documented by the operating surgeons; (IV) the success rate of ACE reduction for intussusception; (V) pathological diagnoses; and (VI) postoperative prognoses. Three main types and nine subtypes of intussusception were identified. Three main types included small bowel-small bowel, small bowel-large bowel, and large bowel-large bowel. The nine subtypes of intussusception included jejuno-jejunal, jejuno-jejuno-ileal, jejuno-ileal, ileo-ileal, ileo-cecal, ileo-ileo-colic, ileo-colic, ceco-colic, and colo-colic subtypes. PLPs were located in four primary regions: the jejunum, ileum, ileocecal region, and colon. The success rate of ACE reduction for intussusception was defined as the number of successful reductions divided by the total number of cases in which ACE detected intussusception. However, among the 75 patients, data were missing for 2 patients on intussusception type, 9 patients on PLP location and distance, and 8 patients on PLP size. Missing values that occurred in a certain subgroup analysis were excluded from that group’s analysis.

The examinations of ultrasound were performed by sonographers with 3–20 years of experience in diagnostics. The diagnosis of our computed tomography (CT) images undergoes a two-step process: an initial report by an attending physician and a final report reviewed by a senior. The technical details of ultrasound (US) and CT were shown on Appendix 1.

ACE was performed using Essenta RC (Philips, Hamburg, Germany) and Uni-Vision (Shimadzu, Kyoto, Japan) digital gastrointestinal fluoroscopy systems. No sedatives were used before enema administration. A Foley catheter was inserted into the child’s rectum and inflated to secure it in place and prevent air leakage. Under fluoroscopy using a gastrointestinal X-ray machine, air was slowly injected through the catheter using a pressure gauge. The initial pressure was maintained at ≤8 kPa, with a maximum therapeutic pressure of 12 kPa. Radiographs were taken to record the position of the intussusception shadow. The procedure was successful when the intussusception disappeared under fluoroscopy and air entered the small intestine. We usually have reduction attempts twice per session. If the initial ACE fails, we usually allow the patient to rest for 2 to 3 hours before attempting a second delayed air enema reduction.

Statistical analysis

Statistical analyses were performed using SPSS software (version 27.0). Categorical variables were summarized as frequencies and percentages, while continuous variables were presented as means and medians. The Mann-Whitney U test was employed for data that did not follow a normal distribution. Categorical data were analyzed using the chi-squared or Fisher’s exact test where appropriate. P<0.05 was considered to be statistically significant.

Results

All included patients were divided into benign and malignant groups based on their pathological diagnoses. The benign group comprised 62 cases (62/75, 82.7%), while the malignant group included 13 cases (13/75, 16.3%). Meckel’s diverticulum was the most common etiology in the benign group, accounting for 31 cases (31/62, 50%), whereas lymphoma was predominant in the malignant group, representing 12 cases (12/13, 92.3%). Among the 12 lymphoma cases, 7 were Burkitt lymphoma, 4 were diffuse large B-cell lymphoma, and 1 lacked pathological classification. Other frequent PLPs included intestinal duplication, Peutz-Jeghers syndrome, Henoch-Schönlein purpura, and juvenile polyps, while rarer causes involved hemangioma, perivascular epithelioid cell tumor, leiomyoma, small bowel polyps, and fibrosarcoma (Table 2).

The duration of illness was longer in the malignant group than in the benign group (22 vs. 3.5 days, P=0.02). The overall recurrence rate of intussusception was 37.3% (28/75), with a recurrence rate of 30.6% (19/62) in the benign group and 69.2% (9/13) in the malignant group (P=0.02). The malignant group exhibited a significantly higher frequency of intussusception episodes than the benign group, with a median of 2 episodes versus 1 episode (P=0.02) (Table 3). No statistically significant differences were observed in sex, age, or the incidence of hematochezia in the two groups. The male-to-female ratio was 37:25 in the benign group and 10:3 in the malignant group. The median age in the benign group was 52 months (range, 1–192 months), compared to 72 months (range, 7–185 months) in the malignant group.

Among all 75 patients, more patients in the benign group underwent ultrasound, more average times of examinations per patient using ultrasound compared to CT, and more intussusceptions were observed on ultrasound (Table 4). No significant differences were found between the benign and malignant PLP groups in multifactor analysis of ultrasound or CT. Polyps of the small intestine, juvenile polyps, and duplication cysts ranked among the top three in the detection rate for PLPs in both the ultrasound and CT groups (Table 5). The difference was that CT detected more duplication cysts (80%) and fewer juvenile polyps (62.5%), while ultrasound detected more juvenile polyps (80%) and fewer duplication cysts (66.7%). Among the diseases ranked 4th to 6th in detection rate using the two modalities, CT performed better (with detection rates of at least 50%, Figure 2), while the ultrasound group had rates of only 20% to 33.3% (Figure 3). The detection rates of Meckel’s diverticulum, hematoma, and perivascular epithelial cell tumor were low on ultrasound and CT (Figure 4).

Figure 2 Jejuno-jejunal intussusception secondary to Peutz-Jeghers syndrome in a 12-year-old boy. (A) Axial enhanced CT image shows a polyp (arrows) causing the intussusception. The polyp appears as a bright area on the image. (B) Oblique axial enhanced CT image shows the common bile duct herniating into the intussusception, causing dilation of the pancreatic duct (star). CT, computed tomography.

Figure 3 Colo-colic intussusceptions secondary to lymphoma in a 4-year-old boy. (A) Sagittal ultrasound image shows the intussusception as a “sleeve sign” (arrows). A dark area to the left of the intussusception (star) suggests a pathological lead point. (B) Transverse power color Doppler image shows the intussusception as a “target sign” (arrows). The same dark area is visible, indicating a potential lead point. (C) Sagittal power color Doppler image shows increased blood flow in the dark area (star), suggesting a pathological lead point. (A) is composed of two consecutive sagittal images stitched together for clarity.

Figure 4 Ileo-colic intussusceptions secondary to Meckel’s diverticulum in a 2-year-old girl. (A) Coronal non-contrast CT image shows the intussuscepted bowel and mesentery (arrows). (B) Axial non-contrast CT image shows the intussuscepted bowel and mesentery (arrows). CT, computed tomography.

Intraoperative findings of intussusception and PLPs were documented (Table 6). The median distance between PLPs and the ileocecal region was shorter in the malignant group compared to the benign group (11 vs. 35 cm, P=0.002). Among the three main types of intussusceptions, small bowel-large bowel was the most common type in both the benign (51.7%, 31/60) and malignant (61.5%, 8/13) groups. Small bowel-small bowel was the second common type in the benign group (40.0%, 24/60). The most commonly observed subtype in the benign group was ileo-ileal (22/60, 36.7%). In contrast, ileo-colic (6/12, 50%) was the predominant subtype in the malignant group. For the location of the PLP, the ileum was the most common site, occurring in both benign (49/60, 81.7%) and malignant (8/13, 61.5%) groups (P>0.05). No significant difference was found in the size of PLPs between groups (6.375 vs. 13.72 cm³, P=0.052).

Preoperative ACE was performed in 65 patients (65/72, 90.3%), including 52 (52/62, 83.9%) in the benign group and 12 (12/13, 92.3%) in the malignant group. The success rate of ACE reduction for intussusception was 44.4% (64/144) in the benign group and 59.2% (29/49) in the malignant group (P=0.07). PLPs were identified during ACE in 5 benign patients (5/52, 9.6%) and 2 malignant patients (2/12, 16.7%).

Among the 75 patients, 2 experienced postoperative complications, specifically intestinal obstruction. No complications before or after non-surgical reduction of intussusception (ACE) were observed in patients. No patients had a recurrence of intussusception after the operation.

Discussion

According to previous reports, Meckel’s diverticulum is the most common cause of secondary intussusception (6,7), while lymphoma is the most frequently observed (8). Our findings aligned with those in the literature, with Meckel’s diverticulum accounting for 41.3% of all cases and 50% of benign cases. In our malignant group, lymphoma was the predominant cause (92%).

Recurrence may occur in intussusception, and the recurrence rate has been reported as high as 9% (9). In our study, the recurrence rates of secondary intussusception were higher, at 30.6% in the benign group and 69.2% in the malignant group. It is still controversial whether secondary intussusception is associated with the recurrence of intussusception. Niramis et al. (10) mentioned that the proportion of PLP was nearly three times higher in recurrent than in non-recurrent intussusception patients. Fisher et al. (11) indicated that recurrence of intussusception was not a predictor for PLP. In our study, the frequency of intussusception episodes was higher in the malignant group compared to the benign group (2 vs. 1 episode). This finding highlights the potential role of malignant PLPs in driving recurrent intussusception, suggesting clinicians should maintain a high index of suspicion for malignancy in cases with frequent recurrences.

Some studies have reported that the duration of intussusception secondary to small bowel tumors and lymphomas is broader, with a higher maximum range than that caused by Meckel’s diverticulum (Meckel’s diverticulum: 1–10 days; lymphomas: 35–90 days; small bowel tumors: 1–90 days) (6,8). According to our data, the duration of illness and time to surgical diagnosis for secondary intussusception was significantly longer in the malignant group compared to the benign group (22 vs. 3.5 days). This prolonged duration in malignant cases may reflect the challenges in diagnosing these lesions, particularly in the context of overlapping imaging findings and nonspecific clinical presentations. We hypothesize that this difference may be related to the pathological morphology of benign versus malignant PLPs. In lymphoma cases, intestinal involvement was often characterized by submucosal dysplasia, with the lesions typically appearing as localized eminence. Burkitt lymphoma, for instance, often presents as an ileocecal mass or with thickened folds and narrowing of the distal ileum (12).

Compared with CT, ultrasound is considered the preferred imaging modality for diagnosing intussusception due to its high sensitivity, specificity, and absence of radiation exposure (13). Other examination methods (such as endoscopy and magnetic resonance enterography) place high demands on pediatric patient cooperation. Endoscopy is an invasive procedure that children often have difficulty tolerating, while magnetic resonance enterography requires sedation and contrast agent administration through a nasojejunal tube (14). Therefore, these modalities are generally not included in diagnosis pathways in the first place, but as examinations for further diagnosis. Next, the incidence of intussusception detected by ultrasound was higher, which may be because ACE is generally performed after ultrasound and before CT, meaning that intussusception may no longer be present during CT examination. Moreover, our study revealed large variabilities in detecting different PLPs using different image modalities. In previous literature reports, the detection rate of secondary intussusception by ultrasound varies greatly, ranging from approximately 6.2% to 65.7% (3,6,7,15). CT is reserved for patients whose diagnosis remains unclear or for further evaluation of PLPs, especially in cases where malignancy is suspected. In our study, the difference in detection rates of PLP between ultrasound and CT suggests that these two examination methods can be used complementarily, such as juvenile polyps, duplication cyst, Henoch-Schonlein purpura, lymphoma, and Peutz-Jeghers syndrome. However, the diagnosis of PLPs in secondary intussusception remains challenging. Extensive ischemic changes and transmural necrosis further complicate diagnosis via ultrasound and CT (6,16). Our study observed low detection rates of Meckel’s diverticulum, hematoma, and perivascular epithelial cell tumor on both ultrasound and CT. This finding underscores the need for complementary imaging modalities. From previous literature, in secondary intussusception, endoscopy plays a positive role in diagnosing intestinal lymphoma (3,17-19), while Technetium-99m pertechnetate imaging and magnetic resonance enterography are beneficial for diagnosing Meckel’s diverticulum (14,20).

Analyzing the types of intussusceptions and the locations and sizes of the PLPs during surgery can aid surgeons in better identifying secondary intussusception. Based on the anatomical location observed intraoperatively, intussusception can be categorized into types such as ileo-colic and colo-colic. Most pediatric intussusception cases in infants and young children are ileo-colic (21-23). However, our study showed a wide variability in the types of intussusceptions, ranging from jejuno-jejuno-ileal to colo-colic. Furthermore, ileo-ileal intussusception (40%) was the most prevalent in the benign group, whereas ileo-colic intussusception (50%) predominated in the malignant group. Malignant PLPs were closer to the ileocecal region than benign ones in our study, consistent with Kassira’s (24) finding that the ileocecal region is a common site for pediatric intestinal lymphoma due to its high lymphatic tissue concentration (25). This variability might underscore the importance of tailoring surgical approaches based on intussusception’s specific type and location, particularly in cases with suspected malignancy.

ACE is the conventional treatment for ileo-colic intussusception, with a higher success rate of 82–83% under fluoroscopic guidance (26,27). Systematic clinical data indicate that ACE remains a safe and effective treatment for children over 3 years of age with intussusception without increasing the risk of hospitalization or length of postoperative stay (28). Recent evidence indicates that sedation could improve the success of ACE for pediatric ileocolic intussusception (29). In our study, 86.7% of patients underwent ACE before surgery. However, ACE is unsuitable for small bowel-small bowel intussusception, for it can neither reveal nor treat intussusception. Small bowel-small bowel intussusception is not uncommon, accounting for 40% of the benign group and 15.6% of the malignant group in our study. Furthermore, in cases of secondary intussusception, the presence of a PLP necessitates surgical intervention for resolution (30). Clinically, performing multiple ACEs on secondary intussusception patients is often ineffective, as clinicians may not promptly recognize the existence of a PLP.

The limitations of our study include: (I) it was a single-center study with a relatively small sample size, particularly in the malignant group. Differences in CT protocols across hospitals may affect the generalizability of this study. (II) Missing intraoperative data were encountered during data collection, which may have introduced potential selection bias. (III) Some patients underwent CT after successful ACE reduction, potentially affecting the detection rate of intussusception on CT. (IV) Surgeons orders a CT scan following a PLP finding on ultrasound may introduce bias into the CT detection rates of PLP. The study spans a 12-year period of patient data, and although it is a single-center dataset, we believe it possesses a certain degree of generalizability.

Conclusions

Based on the results of 75 patients with secondary intussusception confirmed by surgical pathology, malignant PLPs have a longer duration of illness, with a higher frequency of intussusception episodes, and are closer to the ileocecal region than benign PLPs. Ultrasound and CT showed large variabilities in detecting different PLPs, which may complement each other. However, a low detection rate for some particular PLPs remains a significant challenge. Future studies should explore multimodal imaging approaches’ role in enhancing PLP detection and improving outcomes for pediatric patients with secondary intussusception. Our study provides novel insights into the distinct clinical and imaging characteristics of benign and malignant PLPs, offering a framework for improved diagnostic and therapeutic strategies.

Acknowledgments

We would like to extend our sincere gratitude to Dr. Chang Tianjiao from the Department of Ultrasonography at the Children's Hospital of Fudan University for her careful review and verification of the ultrasound images and related content in the manuscript.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://tp.amegroups.com/article/view/10.21037/tp-2025-533/rc

Data Sharing Statement: Available at https://tp.amegroups.com/article/view/10.21037/tp-2025-533/dss

Peer Review File: Available at https://tp.amegroups.com/article/view/10.21037/tp-2025-533/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://tp.amegroups.com/article/view/10.21037/tp-2025-533/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the research ethics board of Children’s Hospital of Fudan University (approval No. 2021-252) and individual consent for this analysis was waived due to the retrospective nature.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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