Superselective transcatheter arterial embolization for acute small bowel bleeding: clinical outcomes and prognostic factors for ischemic complications

Abstract

Background

Small bowel bleeding (SBB) accounts for 5%–10% of all cases of acute gastrointestinal bleeding. Transcatheter arterial embolization (TAE) plays an important role in the treatment of SBB.

Purpose

To evaluate the safety and efficacy of superselective TAE exclusively for SBB and to assess factors associated with clinical outcomes.

Material and Methods

From January 2006 to April 2017, 919 patients were admitted with signs and symptoms of gastrointestinal bleeding; 74 patients (mean age = 57.5 years; age range = 14–82 years) with positive angiographic findings for SBB were retrospectively analyzed. The technical success of TAE and clinical outcomes, including recurrent bleeding, major complications, and in-hospital mortality were evaluated. The associations of various clinical and technical factors with clinical outcomes were analyzed.

Results

The bleeding foci were in the ileum in 48 (65%) patients and the jejunum in 26 (35%). Technical success was achieved in 72 (97%) patients. The rates of recurrent bleeding, major complications, and in-hospital mortality were 12% (7/57), 21% (15/71), and 25% (18/72), respectively. Superselective embolization was a significant prognostic factor associated with fewer major complications (OR = 0.069; P = 0.003). The increased number of embolized vasa recta was significantly associated with a higher probability of major complications (OR = 2.64; P < 0.001). The use of N-butyl cyanoacrylate was associated with lower rates of major complication (OR = 0.257; P = 0.027).

Conclusion

TAE is a safe and effective treatment modality for SBB. In addition, whenever possible, TAE should be performed in a superselective manner to minimize ischemic complications.

Keywords

Gastrointestinal hemorrhage small intestine therapeutic embolization treatment outcome postoperative complications

Introduction

Gastrointestinal bleeding (GIB) is the most common discharge diagnosis from hospital admissions due to gastrointestinal disease in the United States (1). Among them, small bowel bleeding (SBB) is relatively uncommon, accounting for 5%–10% of all cases of acute GIB (2). The majority of patients with SBB require multiple hospital visits and frequent blood transfusion, because of its intermittent nature and recurrent episodes (2,3). Recently, the advent of deep enteroscopy made it possible to achieve endoscopic hemostasis, in addition to diagnostic work-up (4). However, endoscopic treatment has limitations in patients with SBB, such as its invasive nature, prolonged procedure time, and the need for complete bowel preparation, compared with upper GIB (UGIB) or colorectal bleeding (3). Therefore, transcatheter arterial embolization (TAE) plays an important role in the treatment of SBB; it has been used for the treatment of SBB for decades. However, there is still some concern over advertent bowel infarction after TAE, as the small bowel supplies blood flow from only the superior mesenteric artery (SMA), which lacks a collateral network. Several studies have recently shown the safety and efficacy of TAE with the use of advanced tools and techniques for lower GIB (LGIB), including small bowel bleeding (5 –10). However, in most of the cases in these studies, treatment was performed for bleeding sources outside of the small bowel and the studies were limited by small sample sizes for SBB.

The aim of the present study was to evaluate the safety and efficacy of superselective TAE exclusively for SBB and to assess factors associated with clinical outcomes.

Material and Methods

Patient selection

The Institutional Review Board approved this single-center retrospective study, waiving the usual informed consent requirement (IRB no. 2020-0797-001). Between January 2006 and April 2017, 919 consecutive patients were admitted hospital with signs and symptoms of GIB. Of these, patients with UGIB (n = 496) and variceal bleeding (n = 149) were excluded based on clinical symptoms and imaging findings on computed tomography (CT), endoscopy, and nuclear bleeding scan. A total of 274 patients underwent diagnostic angiography for LGIB, and all patients with positive angiographic findings for SBB (n = 74) were included for analysis. Some of these patients have been previously reported on (5).

Definitions

The patient data used for this study were obtained from electronic medical records and the picture archiving and communication system. Various factors including patient characteristics, etiology of bleeding, hemodynamic status, transfusion of packed red blood cells, use of inotropic drugs, laboratory findings, and details of the angiographic findings and embolization procedure were obtained for analysis.

SBB was defined as acute bleeding from the gastrointestinal tract distal to the ligament of Treitz to the terminal ileum. Enteritis included infectious or ischemic enteritis, diverticulitis and inflammatory bowel disease. Vascular lesions included angiodysplasia, Dieulafoy’s lesion, arteriovenous malformation (AVM), and vasculitis. Coagulopathy was defined by the following parameters: (i) prolonged prothrombin time (international normalized ratio > 1.5); (ii) thrombocytopenia (platelet count < 80,000/mL); or (iii) activated partial thromboplastin time > 45s (5). Hemodynamic instability was defined as hypotension (systolic pressure < 100 mmHg) and/or tachycardia (heart rate > 100 beats/min). Superselective embolization was defined as fewer than three embolized vasa recta.

Angiography and embolization procedure

A 5-F vascular access sheath (Terumo Corp, Tokyo, Japan) was inserted to the right common femoral artery under ultrasound guidance. A 0.035-inch hydrophilic guide wire (Terumo) and a 5-F angiographic catheter (RH catheter or RHR catheter; Cook Medical, Bloomington, IN, USA) were used to perform SMA angiography. Celiac or inferior mesenteric artery (IMA) angiography was also performed when the source of bleeding was not localized to the small bowel before TAE. When the active bleeding focus was located, a microcatheter (Progreat Alpha; Terumo or Renegade; Boston Scientific, Natick, MA, USA) was advanced coaxially for embolization. To avoid non-target embolization, the microcatheter was advanced as close to the bleeding foci as possible. For embolization, various materials including N-butyl cyanoacrylate (NBCA) glue (Histoacryl; B. Braun, Melsungen, Germany), absorbable gelatin sponge particles (Spongostan; Ferrosan, Søborg, Denmark), or microcoils (Tornado or Micronestor; Cook) were used according to the following conditions. NBCA was used as a primary embolic agent when a bleeding branch was superselected with a microcatheter. The NBCA was mixed with lipiodol (Guerbet, Aulnay-Sous-Bois, France) at different ratios ranging from 1:1 to 1:3, depending on the distance between the target vessel and the tip of the microcatheter and the operators’ experience. If the bleeder could not be superselected, absorbable gelfoam sponges or microcoils were used as the primary embolic agents. Completion angiography was performed to confirm cessation of arterial bleeding and to evaluate the extent of embolization.

Technical and clinical outcomes

Technical success was determined based on the immediate angiographic findings and defined as complete cessation of blood flow from the bleeding artery. Technical failure was defined as previously described (5). Clinical success was defined as the achievement of hemostasis without recurrent bleeding, major complication as a result of surgery, or in-hospital mortality within 30 days after embolization. Rebleeding was defined as the recurrence of bleeding signs requiring immediate treatment during the first 30 days after the TAE procedure. Procedure-related complications were classified as major or minor according to the reporting standards of the Society of Interventional Radiology (SIR) (11). In-hospital mortality was defined as death from any cause during the admission period associated with the TAE procedure.

Statistical analysis

All statistical analyses were performed using R software (version 3.4.1; The R Project for Statistical Computing, Vienna, Austria; www.r-project.org). Predictors for recurrent bleeding, major complications, and in-hospital mortality were evaluated using univariate and multivariate logistic regression analyses. Variables with a P value < 0.1 in the univariate analysis were selected for multivariate analysis. A two-sided P value < 0.05 was considered statistically significant. The odds ratios (OR) and 95% confidence intervals (CI) were calculated.

Results

Patient characteristics

Fig. 1 demonstrates the study flowchart and Table 1 shows the patients’ baseline characteristics. Among 919 patients who presented with gastrointestinal bleeding, 74 patients (mean age = 57.5 years; age range = 14–82 years) underwent TAE for SBB. On pre-angiographic examinations, small bowel bleeding was identified by contrast-enhanced computed tomography (CT) in 41 (60.3%) patients, endoscopy in 6 (8.8%) patients, and nuclear bleeding scan in 6 (8.8%) patients. The remaining 15 (22.1%) patients underwent immediate angiography, because of unstable vital signs with clinical suspicion of LGIB. Bleeding foci were located in the ileum in 48 (64.9%) patients and the jejunum in 26 (35.1%) patients. The most common cause of SBB was unspecified (37.8%) and 16 (21.6%) patients had underlying coagulopathy. Of the 74 patients, 60 were hemodynamically unstable and inotropic agents were used in 25 of them. The mean hemoglobin level was 6.9 ± 0.173 g/dL (range = 4.1–10.9 g/dL) and 69 patients underwent transfusion.

Fig. 1.

Study flow chart.

Table 1.

Baseline characteristics of 74 patients in relation to origin of bleeding.

	All (n = 74)	Jejunum (n = 26)	Ileum (n = 48)
Mean age (years)	57.5 ± 17.6	63.0 ± 13.3	54.9 ± 18.9
Sex
Male	52 (70.3)	20 (76.9)	32 (66.7)
Female	22 (29.7)	6 (23.1)	16 (33.3)
Hypertension	32 (43.2)	12 (46.2)	20 (41.7)
Diabetes mellitus	28 (37.8)	10 (38.5)	18 (37.5)
Chronic renal disease	9 (12.2)	2 (7.7)	7 (14.6)
Etiology of bleeding
Recent surgery	18 (24.3)	8 (30.8)	10 (20.8)
Enteritis	18 (24.3)	13 (50)	5 (10.4)
Vascular disease	7 (9.5)	3 (11.5)	4 (8.3)
Malignancy	3 (4.1)	1 (3.8)	2 (4.2)
Unspecified	28 (37.8)	10 (38.5)	18 (37.5)
Coagulopathy	16 (21.6)	6 (23.1)	10 (20.8)
Pre-angiographic examination
CT	47 (63.5)	15 (57.7)	32 (66.7)
Endoscopy	6 (8.1)	3 (11.5)	3 (6.3)
Bleeding scan	6 (8.1)	1 (3.8)	5 (10.4)
Clinical symptom	15 (20.2)	6 (23.1)	9 (18.8)
PRBC transfusion
Yes	69 (93.2)	25 (96.2)	44 (91.7)
No	5 (6.8)	1 (3.8)	4 (8.3)
Tachycardia
Yes	60 (81.1)	24 (92.3)	36 (75)
No	14 (18.9)	2 (7.7)	12 (25)
Inotropic drug
Yes	25 (33.8)	12 (46.2)	13 (27.1)
No	49 (66.2)	14 (53.8)	35 (72.9)

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

CT, computed tomography; PRBC, packed red blood cell.

Technical and clinical outcomes

The details of embolization are summarized in Table 2. Technical success was achieved in 72 (97.3%) patients. Of the two technical failures (2.8%), superselection was not feasible in one patient because of a small and tortuous feeding vessel, for which the patient subsequently underwent surgery. In the other patient, bleeding foci disappeared as a result of vasospasm during the selection of the feeding artery. This patient underwent conservative management and SBB was spontaneously resolved without evidence of recurrent bleeding.

Table 2.

Embolization details in patients with technical success.

	Total (n = 72)	Jejunum (n = 26)	Ileum (n = 46)
Number of embolized vasa recta
1	27 (37.5)	14 (53.8)	13 (28.3)
2	18 (25)	6 (23.1)	12 (26.1)
3	4 (5.6)	0 (0)	4 (8.7)
4	19 (26.4)	6 (23.1)	13 (28.3)
5	3 (4.2)	0 (0)	3 (6.5)
6	1 (1.4)	0 (0)	1 (2.2)
Embolic material
NBCA	43 (59.7)	18 (69.2)	25 (54.3)
Gelatin sponge particles	25 (34.7)	5 (19.2)	20 (43.5)
Microcoil	4 (5.6)	3 (11.5)	1 (2.2)

Values are given as n (%).

NBCA, N-butyl cyanoacrylate.

Clinical outcomes are summarized in Table 3. Clinical success was achieved in 56/72 (77.8%) patients. Recurrent bleeding within 30 days of the procedure occurred in 7/57 (12.3%) patients (15/72 patients were excluded because their follow-up periods were < 30 days). These patients were treated with surgery (n = 3), repeated TAE (n = 2), or endoscopic hemostasis (n = 2). Major complications after TAE occurred in 15/71 (21.1%) patients: one of the 72 patients was excluded because of early death within 30 days not associated with complications. The median interval between TAE and observation of a major complication was five days (range = 1–17 days). Five patients had transient bowel ischemia managed with conservative treatment; these patients were included in the clinical success category. By contrast, the remaining 10 patients developed a transmural infarction and either underwent surgery (n = 7) or died (n = 3) within 30 days (Fig. 2). The overall in-hospital mortality rate was 25% (18/72 patients). Of the 18 deaths, 3 (16.7%) were related to recurrent bleeding, and another 3 (16.7%) patients died of complication after TAE. The remaining 12 (66.7%) patients died due to underlying conditions, including disseminated intravascular coagulopathy (n = 2), cardiovascular disease (n = 4), malignancy (n = 3), or pneumonia (n = 3), despite successful TAE.

Table 3.

Clinical outcomes according to organ and embolization-related factors.

	Clinical success	Recurrent bleeding*	Major complication^†
	Clinical success	Recurrent bleeding*	Total	Conservative treatment	Surgery or death
Total (n = 72)	56 (77.8)	7/57 (12.3)	15/71 (21.1)	5 (7)	10 (14.1)
Jejunum (n = 26)	19 (65.5)	2/16 (12.5)	4/26 (15.4)	1 (3.8)	3 (11.5)
Ileum (n = 46)	37 (80.4)	5/41 (12.2)	11/45 (24.4)	4 (8.9)	7 (15.6)
Angiographic finding
Extravasation (n = 55)	45 (81.8)	4/44 (9.1)	10/54 (18.5)	3 (5.6)	7 (12.9)
Others (n = 17)^‡	11 (64.7)	3/13 (23.1)	5/17 (29.4)	2 (11.8)	3 (17.6)
Embolization material
NBCA (n = 43)	36 (83.7)	3/35 (8.6)	5/42 (11.9)	2 (4.8)	3 (7.1)
Gelfoam sponge particles (n = 25)	17 (68)	4/20 (20)	9/25 (36)	3 (12)	6 (25)
Microcoil (n = 4)	3 (75)	0/2 (0)	1/4 (25)	0 (0)	1 (25)
Number of embolized vasa recta
1 (n = 27)	23 (85.2)	1/21 (4.8)	1/26 (3.8)	1 (3.8)	0 (0)
2 (n = 18)	15 (83.3)	2/16 (12.5)	2/18 (11.1)	1 (5.6)	1 (5.6)
3 (n = 4)	4 (100)	0/4 (0)	1/4 (25)	0 (0)	1 (25)
>3 (n = 23)	14 (60.9)	4/16 (25)	11/23 (47.8)	3 (13)	8 (34.8)

Values are given as n (%).

*Total number of patients with recurrent bleeding was 57 after the exclusion of 15 patients with follow-up periods <30 days.

^†Total number of patients with major complication was 71 after the exclusion of one patient who died early within 30 days; the death was not associated with complications.

^‡Pseudoaneurysm, vascular blush, and angiodysplasia.

NBCA, N-butyl cyanoacrylate.

Fig. 2.

A 60-year-old woman presented with hematochezia of unknown etiology. (a) Contrast-enhanced CT scan showed an active bleeding focus at the terminal ileum (arrow). (b) SMA angiography demonstrated extravasation of contrast medium (arrow) from the culprit vasa recta of the ileocolic artery (arrowheads). (c) Selective angiography of the ileocolic artery via microcatheter (black arrow) shows active bleeding (arrow) and multiple vasa recta (arrowheads) from the marginal artery. (d) Final angiography after NBCA embolization shows absence of active bleeding and solidified NBCA in the culprit vasa recta (arrow) and marginal artery (arrowheads). The solidified NBCA involves four vasa recta. (e) Follow-up CT image obtained 3 days after TAE showed infarction of the terminal ileum (arrowhead). Lower right inset is maximal intensity projection image of the terminal ileum. The four vasa recta and marginal artery solidified by NBCA were seen as high density. CT, computed tomography; NBCA, N-butyl cyanoacrylate; SMA, superior mesenteric artery; TAE, transcatheter arterial embolization.

Predictors for clinical outcomes

Table 4 shows the associations of selected clinical and technical parameters with clinical outcomes. There were no factors associated with recurrent bleeding. Univariate analysis showed that superselective embolization (OR = 0.099; 95% CI = 0.027–0.368; P = 0.001) and the use of NBCA (OR = 0.257; 95% CI = 0.077–0.859; P = 0.027) were related to major complications. Results from multivariate analysis showed that superselective embolization had a negative association with major complications (OR = 0.069; 95% CI = 0.012–0.406; P = 0.003). Fig. 3 demonstrates that the increased number of embolized vasa recta was significantly associated with a higher probability of major complications (OR = 2.64; 95% CI = 1.55–4.52; P < 0.001).

Table 4.

Univariate and Multivariate Analysis of Various Prognostic Factors for Clinical Outcomes.

	Univariate		Multivariate
	OR (95% CI)	P value	OR (95% CI)	P value
Complication
Recent GI surgery	0.164 (0.020–1.348)	0.093	0.097 (0.009–1.098)	0.059
Superselection embolization	0.099 (0.027–0.368)	0.001	0.069 (0.012–0.406)	0.003
Embolization materials (NBCA)	0.257 (0.077–0.859)	0.027	1.303 (0.221–7.674)	0.770
In-hospital mortality
Enteritis	0.153 (0.019–1.253)	0.080	0.791 (0.636–0.981)	0.034
Hemodynamic instability	11.636 (2.428–55.764)	0.002	1.391 (1.153–1.679)	0.001
Inotropics use	3.250 (1.077–9.803)	0.036	1.142 (0.933–1.397)	0.192
Hemoglobin level (< 7)	1.450 (1.220–1.723)	0.015	1.069 (0.829–1.380)	0.602
Bleeding focus (jejunum)	2.969 (0.990–8.900)	0.052	1.154 (0.952–1.399)	0.141

CI, confidence interval; GI, gastrointestinal; NBCA, N-butyl cyanoacrylate; OR, odds ratio.

Fig. 3.

(a) Box and whisker plot showing distribution of the number of embolized vasa recta in patients with and without of major complications. The median number of embolized vasa recta was significantly higher in patients with a major complication (P < 0.001). (b) Graph showing the predicted probabilities of major complication as a function of the number of embolized vasa recta. Shaded area indicates 95% CI. Increased number of embolized vasa recta was associated with a significantly higher probability of major complication (OR = 2.64; 95% CI = 1.55 – 4.52; P < 0.001). CI, confidence interval; OR, odds ratio.

In-hospital mortality was associated with hemodynamic instability (OR = 0.741; 95% CI = 0.633–0.867; P = 0.015), inotropic use (OR = 3.250; 95% CI = 1.077–9.803; P = 0.036), and a hemoglobin level < 7 g/dL before TAE (OR = 11.636; 95% CI = 2.428–55.764; P = 0.002). The presence of hemodynamic instability before TAE (OR = 1.391; 95% CI = 1.153–1.679; P = 0.001) and enteritis (OR = 0.791; 95% CI = 0.636–0.981; P = 0.034) were independently related to in-hospital mortality according to the multivariate analysis.

Discussion

The present study of 74 patients is one of the largest studies describing the technical and clinical success rates for TAE to treat SBB as well as the predictors associated with clinical outcomes. The rate of technical success was 97.3% (72/74) and the rates of recurrent bleeding, major complications, and in-hospital mortality were 12.3% (7/57), 21.1% (15/71), and 25% (18/72), respectively.

Recently, the advent of endoscopic technique has enabled treatment of SBB (2,3). However, endoscopic hemostasis for patients with urgent case of SBB is still limited because of its invasive nature, prolonged procedure time, and the need for complete bowel preparation (12). For patients who are unable to undergo endoscopy, other therapeutic options include surgery or TAE. Emergency surgery has mortality rates as high as 15%–30% (5,6). Moreover, when the bleeding focus is not localized, the surgery-related mortality rate increases up to 50% (5). The latest, the American College of Gastroenterology guidelines strongly recommended angiography in unstable patients as the first-line procedure in those presenting with massive SBB (3,13). Furthermore, small bowel endoscopy cannot be performed on patients with prior surgeries and intestinal adhesions (3). However, in the present study, 24.3% (18/74) of patients had previous surgeries, yet all patients underwent successful TAE.

There are several studies that have reported the technical and clinical outcomes of TAE for LGIB, including SBB (5 –10). However, the TAE procedure for SBB has several differences compared to that for colorectal bleeding. First, there is less collateral vascular supply in the small bowel than in the colorectum, especially in the rectum (5). Therefore, superselective embolization is required to avoid ischemic complication. Second, the arteries supplying the small bowels, especially the jejunal branches, are more tortuous than those supplying the colon. Thus, it is more technically difficult to achieve superselection. The technical success rate in the present study was 97.3%, which is comparable to the rates reported in previous studies on TAE for LGIB, including colorectal bleeding (89.5%–100%) (5,7,9,14 –17). In addition, there were no technical failures in patients with jejunal bleeding. Third, SBB has an intermittent nature (3). Therefore, angiography should be performed when the patient develops symptoms, in order to find the bleeding focus. Unfortunately, in the present study, the time interval between symptom presentation and angiography was not investigated, and thus further study is needed.

The overall recurrent bleeding rate in the present study was 12.3%, which is comparable to rates reported in previous studies on LGIB (8.8%–26%) (5,7,9,14 –17) and lower in comparison with that of endoscopic hemostasis (20%–33.8%) (18 –21). Several factors are known to affect recurrent bleeding after TAE or endoscopic hemostasis, including coagulopathy, vascular lesions, blood transfusion, and low hemoglobin levels (5,9,21,22). In particular, vascular lesions, including angiodysplasia, AVM, or Dieulafoy’s lesion, show high rebleeding rates after endoscopic hemostasis (30%–45%) (21,23,24). In the present study, of the seven patients with vascular lesions, the recurrent bleeding rate was 14.3% (1/7 patients), which is lower than that of endoscopic hemostasis.

The main concern in performing TAE for SBB is ischemic complication due to poor collateral circulation (25). In previous studies regarding TAE for traditionally defined LGIB, the ischemic complication rate was in the range of 3.3%–18.3% (5,7,9,10,25). In the present study, the major complication rate was 21.1% (15/71 patients), which is slightly higher than that reported in previous studies. Patients with major complications were defined as those who required in-hospital management regardless of whether they were treated with conservative treatment of not. Indeed, 5/15 patients with major complications achieved complete recovery after conservative management. Therefore, the complication rate may be overestimated.

Superselective embolization for SBB is one of the important factors related to complications. In previous studies, it has been shown that superselective embolization involving four or more vasa recta resulted in an increased risk of ischemic bowel damage (15,26,27). This is in line with findings of the present study, that the major complication rate was significantly lower in the superselective embolization group (OR = 0.069; P = 0.003). Additionally, the increased number of embolized vasa recta was significantly associated with a higher probability of major complications (OR =2.64; P < 0.001). This study is one of the largest studies describing the safety and outcome of TAE only for SBB and unique in providing data on the clinical implication of the number of embolized vasa recta on human subjects. While the number of embolized vasa recta that do not cause ischemic bowel damage cannot be determined with certainty, the result of the present study suggests that three or fewer vasa recta would be a safe number for the majority of SBB cases.

NBCA has been reported as an effective embolic material with favorable outcome for LGIB (5,9,25). In particular, NBCA showed a lower complication rate than did other embolic materials in patients with LGIB (5,9). This can be explained by the characteristics of NBCA, which can prevent the embolic agent from propagating too far distally into the capillary bed. Thereby, circulation in the post-embolic tissue is preserved after TAE via collateral channels in the intramural microcirculation (25). Furthermore, NBCA mixture with lipiodol is radio-opaque, allowing for easier control under fluoroscopy, compared with other embolic materials (5). In the present study, although the use of NBCA had no independent relationship, it was associated with lower rates of major complication (OR = 0.257; P = 0.027).

Overall in-hospital mortality rate after TAE was 25% in the present study, which was similar to rates reported in previous studies on TAE for LGIB (9%–27%) (5,9,14,16,28). Many factors are known to affect mortality after TAE, including hemodynamic instability, low hemoglobin levels, blood transfusion, and inotropic use, and these have been found to be negatively correlated with survival rates (5,28,29). This is in line with results of the present study that found the in-hospital mortality rate to be significantly higher in those with hemodynamic instability before TAE (OR = 1.391; P = 0.001). Another significant prognostic factor was enteritis, which showed a negative relationship with in-hospital mortality (OR = 0.791; P = 0.032). One possible explanation is that enteritis is a condition which can be treated by conservative management.

The current study has a few limitations. First, this study has a retrospective design. Second, the embolic agent was not randomly chosen. Further study is warranted to compare outcomes based on randomized selection of embolic materials. Third, bowel ischemic change was determined by follow-up CT only in clinically suspicious patients. Owing to the retrospective study design, the selection of follow-up modality and its implementation were determined by the gastroenterologists based on the clinical circumstances of each patient. However, complications without clinical symptoms are classified as a minor complication and are considered to have no effect on clinical outcomes of the patients.

In conclusion, TAE is a safe and effective treatment modality for SBB. In addition, whenever possible, superselective embolization should be used to avoid major complications.

Footnotes

Declaration of conflicting interests

The author(s) declared the following potential conflicts of interest with respect to the research, authorship, and/or publication of this article: Data on the patients described in this current study were extracted from our gastrointestinal bleeding registry. Some of these patients were reported in previous work from this institution (European Radiology 2019; 29: 57–67).

Funding

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

ORCID iDs

Joon Ho Kwon

Man-Deuk Kim

Gyoung Min Kim

References

Peery

Crockett

Barritt

, et al. Burden of Gastrointestinal, Liver, and Pancreatic Diseases in the United States. Gastroenterology 2015; 149:1731–1741.e1733.

Chetcuti Zammit

Sidhu

Small bowel bleeding: cause and the role of endoscopy and medical therapy. Curr Opin Gastroenterol 2018; 34:165–174.

Gerson

Fidler

Cave

, et al. ACG Clinical Guideline: Diagnosis and Management of Small Bowel Bleeding. Am J Gastroenterol 2015; 110:1265–1287; quiz 1288.

Ell

May

Mid-gastrointestinal bleeding: capsule endoscopy and push-and-pull enteroscopy give rise to a new medical term. Endoscopy 2006; 38:73–75.

Kwon JH, Kim MD, Han K, et al. Transcatheter arterial embolisation for acute lower gastrointestinal haemorrhage: a single-centre study. Eur Radiol 2019;29:57–67.

Barnert

Messmann

Diagnosis and management of lower gastrointestinal bleeding. Nat Rev Gastroenterol Hepatol 2009; 6:637–646.

Huang

Lee

Hsiao

, et al. N-butyl cyanoacrylate embolization as the primary treatment of acute hemodynamically unstable lower gastrointestinal hemorrhage. J Vasc Interv Radiol 2011; 22:1594–1599.

Yata

Ihaya

Kaminou

, et al. Transcatheter arterial embolization of acute arterial bleeding in the upper and lower gastrointestinal tract with N-butyl-2-cyanoacrylate. J Vasc Interv Radiol 2013; 24:422–431.

Hur

Jae

Lee

, et al. Safety and efficacy of transcatheter arterial embolization for lower gastrointestinal bleeding: a single-center experience with 112 patients. J Vasc Interv Radiol 2014; 25:10–19.

10.

Koo

Shin

Kim

, et al. Clinical outcome of transcatheter arterial embolization with N-butyl-2-cyanoacrylate for control of acute gastrointestinal tract bleeding. AJR Am J Roentgenol 2015; 204:662–668.

11.

Sacks

McClenny

Cardella

, et al. Society of Interventional Radiology clinical practice guidelines. J Vasc Interv Radiol 2003; 14:S199–202.

12.

Laine

Sahota

Shah

Does capsule endoscopy improve outcomes in obscure gastrointestinal bleeding? Randomized trial versus dedicated small bowel radiography. Gastroenterology 2010; 138:1673–1680.e1671; quiz e1611–1672.

13.

Strate

Gralnek

IM.

ACG Clinical Guideline: Management of Patients with Acute Lower Gastrointestinal Bleeding.

Am J Gastroenterol 2016; 111:459–474.

14.

Maleux

Roeflaer

Heye

, et al. Long-Term Outcome of Transcatheter Embolotherapy for Acute Lower Gastrointestinal Hemorrhage. Am J Gastroenterol 2009; 104:2042–2046.

15.

Kodani

Yata

Ohuchi

, et al. Safety and Risk of Superselective Transcatheter Arterial Embolization for Acute Lower Gastrointestinal Hemorrhage with N-Butyl Cyanoacrylate: Angiographic and Colonoscopic Evaluation. J Vasc Interv Radiol 2016; 27:824–830.

16.

Tan

K-K

Strong

Shore

, et al. The Safety and Efficacy of Mesenteric Embolization in the Management of Acute Lower Gastrointestinal Hemorrhage. Ann Coloproctol 2013; 29:205–208.

17.

Kickuth

Rattunde

Gschossmann

, et al. Acute lower gastrointestinal hemorrhage: minimally invasive management with microcatheter embolization. J Vasc Interv Radiol 2008; 19:1289–1296.

18.

Aniwan

Viriyautsahakul

Rerknimitr

, et al. Urgent double balloon endoscopy provides higher yields than non-urgent double balloon endoscopy in overt obscure gastrointestinal bleeding. Endosc Int Open 2014; 2:E90–95.

19.

Ponte

Perez-Cuadrado Robles

Pinho

, et al. High short-term rebleeding rate in patients undergoing a second endoscopic therapy for small-bowel angioectasias after recurrent bleeding. Rev Esp Enferm Dig 2018; 110:88–93.

20.

Dulic-Lakovic

Dulic

Hubner

, et al. Bleeding Dieulafoy lesions of the small bowel: a systematic study on the epidemiology and efficacy of enteroscopic treatment. Gastrointest Endosc 2011; 74:573–580.

21.

Sakai

Endo

Taguri

, et al. Frequency and risk factors for rebleeding events in patients with small bowel angioectasia. BMC Gastroenterol 2014; 14:200.

22.

Pasha

Shergill

Acosta

, et al. The role of endoscopy in the patient with lower GI bleeding. Gastrointest Endosc 2014; 79:875–885.

23.

Jackson

Gerson

LB.

Management of gastrointestinal angiodysplastic lesions (GIADs): a systematic review and meta-analysis. Am J Gastroenterol 2014; 109:474–483; quiz 484.

24.

Romagnuolo

Brock

Ranney

Is endoscopic therapy effective for angioectasia in obscure gastrointestinal bleeding? A systematic review of the literature. J Clin Gastroenterol 2015; 49:823–830.

25.

Frodsham

Berkmen

Ananian

, et al. Initial experience using N-butyl cyanoacrylate for embolization of lower gastrointestinal hemorrhage. J Vasc Interv Radiol 2009; 20:1312–1319.

26.

Ikoma

Kawai

Sato

, et al. Ischemic effects of transcatheter arterial embolization with N-butyl cyanoacrylate-lipiodol on the colon in a Swine model. Cardiovasc Intervent Radiol 2010; 33:1009–1015.

27.

Jae

Chung

Kim

, et al. Experimental study on acute ischemic small bowel changes induced by superselective embolization of superior mesenteric artery branches with N-butyl cyanoacrylate. J Vasc Interv Radiol 2008; 19:755–763.

28.

Defreyne

Vanlangenhove

De Vos

, et al. Embolization as a first approach with endoscopically unmanageable acute nonvariceal gastrointestinal hemorrhage. Radiology 2001; 218:739–748.

29.

Dempsey

Burke

Reilly

, et al. Angiography in poor-risk patients with massive nonvariceal upper gastrointestinal bleeding. Am J Surg 1990; 159:282–286.