Multidetector computed tomography diagnosis of small bowel intussusceptions in adults: observations in a 10-year single-center study

Abstract

Background

The etiologies of small bowel intussusception (SBI) in adults are varied.

Purpose

To investigate multidetector computed tomography (MDCT) characteristics in adults with neoplastic and non-neoplastic SBI.

Material and Methods

Clinical data and MDCT images diagnosed with SBI in adults from January 2010 to May 2020 were retrospectively reviewed.

Results

The study included a total of 71 patients. Forty-two patients had a combined total of 55 neoplastic intussusceptions, including 29 patients with benign tumors and 13 patients with malignant tumors. Twenty-nine patients had a combined total of 36 non-neoplastic intussusceptions, of which the condition was idiopathic in 23 patients and cased by non-neoplastic benign lesions in six patients. There were no significant differences in patient age or sex ratio in the neoplastic and non-neoplastic groups. In the non-neoplastic group the intussusceptions were shorter in length (3.6 cm vs. 13.2 cm, P<0.05) and smaller in transverse diameter (2.8 cm vs. 4.2 cm, P<0.05), and less likely to be associated with intestinal obstruction (2 vs. 18, P<0.05). The percentage of patients with multiple intussusceptions was greater in the neoplastic group (10/42, 23.8% vs. 4/29, 13.8%). In the non-neoplastic group only one lead point was detected (in a patient with Meckel’s diverticulum), whereas lead points were detected in all 55 intussusceptions in the neoplastic group.

Conclusion

There are differences in the clinical and MDCT manifestations of adult neoplastic and non-neoplastic SBIs. Whether a lead point is present or not has implications with regard to deciding on the most appropriate treatment and avoiding unnecessary surgery.

Keywords

Adults computed tomography intestinal disease intussusceptions small bowel

Introduction

Intussusception is relatively rare in adults, only accounting for an estimated 5% of all intussusceptions and 1% of the causes of intestinal obstruction, and its causes are varied (1 –4). Previous studies based on discharge diagnoses and surgical results suggest that 80%–90% of adult intussusceptions have an underlying cause, approximately 65% are due to malignant neoplasm, and the colon is involved in intussusceptions more often than the small bowel (2). Multidetector computed tomography (MDCT) is the most commonly used imaging modality for the detection of intussusceptions, and it can provide valuable information about the location of the intussusception, the intestinal segments involved, and the extent of the intussusceptions (5). Our recent experience suggests that non-neoplastic intussusception of the small bowel in adults is more common than previously reported. The aim of the present study was to investigate the diagnostic value of MDCT for determining the etiology of small bowel intussusception in adults, and to compare clinical and imaging parameters in neoplastic and non-neoplastic intussusceptions.

Material and Methods

Patients

This retrospective study was approved by the relevant ethics committee, and the requirement of written informed consent was waived. A total of 220 patients aged ≥18 years were diagnosed with intussusception via MDCT between January 2010 and May 2020 and managed at our hospital. Seventy-one patients (44 men, 27 women; mean age = 45.6 years; age range = 18–81 years) had small bowel intussusceptions that were confirmed via surgical pathology and follow-up MDCT examinations were included in this study. The other 149 patients with neoplastic colon intussusception confirmed via surgery were excluded.

Computed tomography

Computed tomography (CT) examinations were performed using three different systems: Aquillion 64-detector spiral CT (Toshiba Medical Systems, Tokyo, Japan) (n = 43); Somatom Emotion 16-detector slice spiral CT (Siemens Medical Systems, Erlangen, Germany) (n = 17); and Somatom Force CT (Siemens Medical Systems) (n = 11). Six patients only underwent plain CT of the abdomen and pelvis, and 65 patients underwent plain and contrast-enhanced CT of arterial and venous phases. The scanning parameters were tube voltage 120 kV, automatic tube current milliamps, pitch 1, field of view = 35 × 35 cm to 45 × 45 cm, matrix = 512 × 512, axial imaging with a slice thickness and interval of 3 mm.

The contrast medium iohexol (300 mg/mL) (Yangzijiang Pharmaceutical Co., Ltd., Jiangsu, PR China) was injected at a dosage of 1.8 mL/kg at a rate of 3 mL/s. The arterial and venous phases were scanned at 30 s and 70 s after the initiation of contrast medium injection. Coronal and sagittal multiplanar reformation images were performed conventionally with slice thickness and spacing of 3 mm. In patients with a longer range of intussusception, curved planar reconstruction was conducted along the intestine.

Image analyses

Patients were divided into a neoplastic intussusception group and a non-neoplastic intussusception group based on CT findings and surgical results or clinical follow-up observations. Neoplastic intussusception is defined as an intussusception secondary to the obstruction of intestinal benign or malignant neoplastic lesions. Non-neoplastic intussusception includes intussusception caused by non-neoplastic benign lesions and idiopathic intussusception. Idiopathic intussusception is defined as with or without mild abdominal pain that disappeared without surgical removal, or intermittent intussusceptions detected in a series of CT scans, with no demonstrable underlying cause or bowel wall thickening evident via CT or during surgery (2). If the intestine proximal to intussusception is dilated with a transverse diameter ≥3 cm accompanied by intestinal effusion or gas-fluid level, distal intestinal atrophy is considered with small bowel obstruction.

Two radiologists with >5 years of experience in abdominal imaging diagnosis read the images on a picture archiving and communication system together, and recorded the number of intussusceptions, lead points, intussusception type (jejunojejunal type, jejunoileal type, ileoileal type), and the number of cases involving intestinal obstruction. The length and transverse diameter of the intussusception at the mid-point were measured independently, and the average value was recorded.

Statistical analysis

SPSS 20.0 statistical software (SPSS, Inc., Chicago, IL, USA) was used for statistical analysis. The independent samples t-test was used to compare patient age, intussusceptions length, and transverse intussusception diameter in the neoplastic and non-neoplastic groups. The chi-square test was used to compare the sex ratios of patients with neoplastic and non-neoplastic intussusceptions, and Fisher’s exact test was used to compare the numbers of cases with single and multiple intussusceptions, and the numbers of cases with intestinal obstruction. P < 0.05 was considered statistically significant.

Results

Patient data

There were 42 patients in the neoplastic intussusception group, of which 39 reported abdominal pain, five of whom also exhibited hematochezia. In the other three patients, intussusception was discovered incidentally. There were 29 patients in the non-neoplastic intussusception group, including 13 who had mild abdominal pain and 16 whom intussusceptions were discovered incidentally via abdominal CT performed for other reasons. There were no statistically significant differences in patient age or sex ratio between the two groups (P > 0.05) (Table 1).

Table 1.

Clinical and intussusception data.

	Non-neoplastic intussusception (n = 29)	Neoplastic intussusception (n = 42)	Statistic	P value
Age (years)	45.9 ± 14.0	45.7 ± 19.3	t = 0.046	0.963
Sex ratio (M:F)	19:10	25:17	x² = 0.261	0.609
Number of intussusceptions (cases of single : multiple)	35 (25:4)	55 (32:10)	x² = 1.072	0.301*
Number of intestinal obstructions	2	18	x² = 10.809	<0.05
Intussusception width (cm)	2.8 ± 0.6 (1.5–4.2)	4.2 ± 1.1 (2.2–7.5)	t = –7.263	<0.05
Intussusception length (cm)	3.6 ± 2.1 (1.5–11.0)	13.2 ± 8.4 (4.6–45.7)	t = –6.651	<0.05

Values are given as n or mean ± SD (range).

P value derived by comparing patient numbers with single vs. multiple intussusceptions in the two groups.

CT characteristics of small bowel intussusception

There were 55 intussusceptions in the neoplastic group and 36 intussusceptions in the non-neoplastic group. The types of intussusceptions in the two groups are shown in Table 2.

Table 2.

Numbers of intussusceptions in the small intestine.

	Jejunojejunal	Jejunoileal	Ileoileal	Total
Non-neoplastic intussusception	28	0	8	36
Neoplastic intussusception	17	10	28	55

In the neoplastic intussusception group, there were 29 patients with 39 intussusceptions secondary to benign tumors, including 22 patients with single intussusceptions (Fig. 1). Of the seven patients with multiple intussusceptions, five patients had two intussusceptions, one patient had with three intussusceptions, and one patient had four intussusceptions (Fig. 2). There were 13 patients with 16 intussusceptions secondary to malignant tumors, including 10 patients with single intussusceptions (Fig. 3) and three patients with two intussusceptions. A lead point was evident in all 55 neoplastic intussusceptions on preoperative CT.

Fig. 1.

A 71-year-old man with a small intestine leiomyoma secondary to an ileoileal-type intussusception and small bowel obstruction. Coronal multiplanar reconstruction image depicted a soft mass as a lead point located at the ileum (a) that exhibited uneven enhancement (thin arrow). Typical intussusception (b) was observed in the proximal intestine (thick arrow).

Fig. 2.

A 20-year-old man with small intestinal Peutz-Jeghers polyps secondary to multiple intussusceptions. Two ileoileal-type intussusceptions (thick arrows) are shown in the transverse images (a, b) and coronal multiplanar reconstruction images (c, d). Multiple significantly enhanced soft tissue nodules were observed in the small intestine (thin arrows), of which two were lead points of the intussusceptions (c).

Fig. 3.

A 44-year-old man with a small bowel intussusception secondary to the metastatic melanoma. The intussusceptions presented as a typical “target sign” in the axial imaging (a), a soft tissue nodule (thin arrow) was observed in the lumen, and coronal multiplanar reconstruction (b) depicted a wide range of intussusception (thick arrow) in the proximal small intestine.

In the non-neoplastic intussusception group, there were 23 patients with 29 idiopathic intussusceptions, including 20 patients with a single intussusception (Fig. 4), one patient with two, one patient with three, and one patient with four intussusceptions. There were five patients with six intussusceptions secondary to non-neoplastic benign lesions, including intestinal anastomotic orifice (n = 2) (Fig. 5), ectopia of the gastric mucosa (n = 1), Meckel’s diverticulum (n = 1), small bowel inflammation (n = 1), and pregnancy (n = 1, with two intussusceptions) (Fig. 6). One a patient with Meckel’s diverticulum exhibited a lead point (Fig. 7), but no lead points were detected in any other patients in the non-neoplastic intussusception group.

Fig. 4.

Axial (a) and coronal (b) multiplanar reconstruction images of a 44-year-old man with right renal calculus, hydronephrosis, and idiopathic jejunojejunal intussusception without a lead point (arrows).

Fig. 5.

A 46-year-old woman with a history of small intestinal gastrointestinal stromal tumor surgery. In axial (a) and coronal (b) multiplanar reconstruction images, an intussusception (thick arrow) was evident at the anastomosis orifice, without a lead point and with no small bowel obstruction.

Fig. 6.

A 28-year-old six-months pregnant woman. Coronal (a) and sagittal (b) multiplanar reconstruction images depicted two jejunojejunal intussusceptions (thick arrows) in the left upper abdomen accompanied by proximal small intestinal obstruction. A fetus is seen in the pelvic cavity (thin arrow).

Fig. 7.

A 35-year-old man with a Meckel’s diverticulum secondary to ileoileal-type intussusceptions. An oval cystic mass (a) in the distal ileum (thin arrow) and an intussusception (b) (thick arrow) was observed in the coronal multiplanar reconstruction images in the proximal bowel accompanied by small bowel obstruction.

The intussusceptions in the non-neoplastic group were significantly shorter (3.6 cm vs. 13.2 cm, P < 0.05) and smaller in transverse diameter (2.8 cm vs. 4.2 cm, P < 0.05) than those in the neoplastic group. In the non-neoplastic group, the mean intussusception length in the 23 patients with idiopathic intussusception (2.9 cm, range = 1.5–4.8 cm) was shorter than that in the six patients with non-idiopathic intussusception (7.1 cm, range = 3.3–11.0 cm).

The incidence of small bowel obstruction in the neoplastic intussusception group (18/42, 42.9%) was greater than that in the non-neoplastic intussusception group (2/29, 6.9%) (P < 0.05). Multiple intussusceptions were detected in 10/42 (23.8%) patients in the neoplastic group and 4/29 (13.8%) in the non-neoplastic group, but this difference was not statistically significant (Table 1).

Clinical follow-up and pathology

In 23 patients of idiopathic intussusception in the non-neoplastic group, the intussusceptions no longer evident in follow-up CT performed at time points ranging from two weeks to three months after initial detection without surgery. In the other six patients, surgery was performed. All the 42 patients of neoplastic intussusception were confirmed via surgery, including 29 patients of benign tumors and 13 patients of malignant tumors (Table 3).

Table 3.

Clinical and etiological characteristics of the neoplastic and non-neoplastic intussusceptions of the small intestine.

Non-neoplastic intussusception	Patients	Number	Neoplastic intussusception	Patients	Number
Idiopathic and transient	23	29	Benign tumors or tumor-like lesions
Pregnancy	1	2	Single polyp	8	8
Ectopia of gastric mucosa	1	1	Multiple polyps	6	15
Inflammation	1	1	Villous tubular adenoma	2	3
Anastomotic astium	2	2	Lipoma	12	12
Meckel’s diverticulum	1	1	Leiomyoma	1	1
			Malignant tumors
			Tubular adenocarcinoma	2	2
			Diffuse large B cell lymphoma	4	5
			Gastrointestinal stromal tumor	1	1
			Leiomyosarcoma	2	2
			Metastatic carcinoma or tumor	4	6
Total	29	36	Total	42	55

Discussion

In adults, the colonic intussusceptions are usually caused by lipoma or adenocarcinoma, but the causes of small bowel intussusceptions are varied (6). Idiopathic small bowel intussusceptions are usually transient and are often absent in follow-up examinations and the pathophysiological mechanisms involved in their development and resolution are unclear. Non-neoplastic small bowel intussusception can be caused by local inflammation, ectopic pancreas, postoperative adhesions, bowel hematoma from coagulopathy, Meckel’s diverticulum, mesenteric lymph node hyperplasia, and abdominal trauma, among other things (2 –7). Benign tumors that can cause small bowel intussusception in adults include polyp, adenomas, lipoma, leiomyoma, and hemangioma. Malignant tumors such as adenocarcinoma and melanoma are the most common causes, but others include gastrointestinal stromal tumor, adenomatous polyp, leiomyosarcoma, carcinoid, neuroendocrine tumor, lymphoma, leukemia, metastasis, and Kaposi's sarcoma (1 –6). All of these factors may reduce the intestinal peristalsis or lead to an intestinal obstruction; thus, the intussusception occurs as peristalsis is increased in proximal intestine (1 –4).

In the adults in the present study, small bowel intussusceptions accounted for 32.5% (71/220) of all cases of intussusception at our hospital between January 2010 and May 2020, and the incidence was much smaller than that of intussusceptions in the colon. The non-neoplastic intussusception account for 40.8% (29/71) in all small bowel intussusceptions, and most of them are idiopathic. Pregnancy is a rare cause of small bowel intussusceptions in adults and may be related to the associated increased intra-abdominal pressure and enhancement of intestinal peristalsis. One pregnant patient in the present study had two intussusceptions in the distal jejunum and accompanying intestinal obstruction. Intussusceptions caused by ectopia of the gastric mucosa or anastomotic orifice are also rarely reported as causes for small bowel intussusceptions in adults, and in the present study there was only one case caused by gastric mucosa ectopia and two cases caused by anastomotic orifice. This differs from a previous study in which approximately 65% of adult intussusceptions were due to malignant neoplasm (2). In the present study, the number of intussusceptions caused by benign tumors (29/42, 69%) was greater than the number caused by malignant tumors (13/42, 31%).

The clinical diagnosis of intussusception in adults is challenging because it can be asymptomatic, and where they are present the symptoms are varied. They can be acute, intermittent, or chronic (4). Most intussusceptions in adults are chronic and characterized by incomplete intestinal obstruction. Clinical symptoms can include abdominal pain, nausea, vomiting, abdominal distension, and blood in the stool (2 –4,8).

Due to increased awareness of intussusception, idiopathic small bowel intussusceptions are now reported more frequently. In the present study, the incidence of idiopathic small bowel intussusceptions in the non-neoplastic group was 23 of 29 (79.3%), and intussusceptions was detected incidentally via CT performed due to mild abdominal pain or other reasons in 23 of 71 patients (32.4%). Twenty-three patients had no intestinal obstruction or bloody stool, and all of these patients were managed via non-operative techniques and exhibited complete resolution at follow-up examinations conducted at time points ranging from two weeks to three months after initial diagnosis. This suggests that this form of intussusception is more prevalent in some asymptomatic populations than has previously been reported. Accurate diagnosis of idiopathic/transient intussusceptions is important because it can facilitate the avoidance of unnecessary surgery.

The six patients with non-idiopathic intussusception in the non-neoplastic group had varying degrees of abdominal pain. One pregnant woman had two intussusceptions and accompanying with small bowel obstruction. Two patients had two intussusceptions at the anastomotic orifice had histories of surgical resection of small intestinal stromal tumor. The patient with small bowel ectopia of the gastric mucosa and the patient with inflammation had abdominal pain but no bowel obstruction. In one patient, a Meckel’s diverticulum appeared as an intraluminal cystic mass in the distal ileum and secondary intussusception was accompanied by small bowel obstruction, and it was misdiagnosed as a tumor before surgery.

In the present study, 39 of 42 patients (92.9%) in the neoplastic intussusception group reported abdominal pain or exhibit hematochezia. Of the remaining three patients in whom the intussusceptions were found incidentally, one had a history of hiccups, one had a history of abdominal aortic dissection, and one had a history of lymphoma. Patients with neoplastic intussusception were more prone to secondary intestinal wall necrosis and/or bleeding than patients with non-neoplastic intussusception, and small bowel obstruction was detected in 18 of 42 (42.9%) patients in the neoplastic intussusception group. This may be associated with the tumor leading to long-term restriction of intestinal wall movement or chronic intestinal obstruction at the same time the peristalsis of the proximal intestine is enhanced. In the present study, there were no significant differences in sex or age distribution between the neoplastic and non-neoplastic intussusception groups.

MDCT is the most effective examination tool for the diagnosis of small intestinal intussusception in adults. It can be used to accurately identify the site of intussusceptions preoperatively, assess the involvement of intestinal segments, and determine the extent of intussusception of the bowel (5). Honjo et al. (9) reported that the accuracy of preoperative diagnosis via MDCT was 95.5%. On MDCT, intussusception typically exhibits a “bowel-within-bowel” appearance, and a “target sign” or “bull’s eye sign” is depicted if the image is perpendicular to the intussusception. If the image is parallel to the long axis of the intussusception, it is depicted as “sausage mass” or “double tube sign” with multiple intestinal walls. Other signs described in previous studies include vascular involvement, renal-type shape, a banana-type shape, and a shape resembling a comet tail. MDCT has the capacity to determine the presence or absence of a lead point (10 –14).

The MDCT features of the small bowel intussusceptions in adults in the present study were concordant with previously described criteria. The CT appearances of the intussusceptions in the non-neoplastic group indicated that most were localized to the proximal intestine, however, and a lead point was only detected in a single patient with Meckel’s diverticulum. All of them had short segment intussusceptions. Al-Radaideh et al. (6) described seven patients with transitory intussusception, of which it was ≤3 cm in six patients, and 4 cm in one patient. Lvoff et al. (15) reported that intussusception is temporary and self-limiting when the length of the adjacent intestinal loop is ≤3.5 cm. The results of the present study are consistent with results reported by Al-Radaideh et al. (6) and Lvoff et al. (15), in that the mean length of idiopathic intussusceptions was 2.9 cm and no patients had a small bowel obstruction.

A solid mass at the head of the intussusception is a reliable sign of the present of a lead point in cases of neoplastic intussusceptions (10 –14). In the present study, intussusception with a lead point was evident in all patients in the neoplastic group. Al-Radaideh et al. (6) reported that MDCT facilitated reliable identification of intussusceptions in all cases, but the etiology could only be established with certainty in case of lipoma. Neoplastic intussusception can occur anywhere in the small intestine. In the present study, >50% of intussusceptions in the neoplastic group were located in the distal small bowel, and both the length and transverse diameters of intussusceptions in the neoplastic group were greater than those in the non-neoplastic group. All cases of lipoma and some cases of polyp were correctly diagnosed, but in the other cases involving benign or malignant entities, the etiology of intussusceptions could not be ascertained via MDCT.

The present study had some limitations. It was retrospective, and there was a relatively small number of non-idiopathic small bowel intussusception cases in the non-neoplastic group. Idiopathic intussusceptions may exist in some asymptomatic patients, and the incidence, mechanism, and management of this should be further evaluation. Intra-observer consistency with respect to determining the number of lead points was not evaluated. Lastly, some patients may have been missed in this retrospective study.

In conclusion, the purpose of MDCT examination in cases of potential small bowel intussusception in adults is not only to accurately clarify its presence and location, but also to determine whether there is a potential primary lesion and a lead point. The length and transverse diameter of intussusceptions, and whether a lead point is present, are key points in the differential diagnosis of neoplastic and non-neoplastic intussusceptions.

Footnotes

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iDs

Maoqing Hu

Wansheng Long

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