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Outcome of Rectal Arterial Embolization for Rectal Bleeding in 34 Patients: A Single-Center Retrospective Study over 20 Years
CLINICAL STUDY
Outcome of Rectal Arterial Embolization for Rectal Bleeding in 34 Patients: A Single-Center Retrospective Study over 20 Years Suyoung Park, MD, Yook Kim, MD, Ji Hoon Shin, MD, Woo Jin Yang, MD, Seung Yeon Noh, MD, Hee Ho Chu, MD, Cheng Shi Chen, MD, and Hyun-Ki Yoon, MD ABSTRACT Purpose: To report the efficacy of rectal artery embolization (RAE) for the treatment of rectal bleeding and the prognostic factors related to recurrent bleeding. Materials and Methods: A total of 34 patients in a single center who underwent RAE for treatment of rectal bleeding between September 1998 and December 2018 were retrospectively reviewed. Procedure details including angiographic findings and embolic materials used, technical success rate, bleeding control rate during hospital stay, major adverse event rate, and prognostic factors associated with recurrent bleeding were evaluated. Results: Technical success rate was 97.1% (33 of 34). Bleeding control during hospital stay was achieved in 64.7% of patients (n ¼ 22). The most common bleeding focus was in the superior rectal artery. Recurrent bleeding occurred in 11 patients. Incomplete initial angiography with only an inferior mesenteric or internal iliac angiogram had been performed in 90.9% of patients with recurrent bleeding (10 of 11) and 52.2% of patients with bleeding control (12 of 23; P ¼ .053). The use of N-butyl-2-cyanoacrylate was related to a significantly lower incidence of recurrent bleeding (P ¼ .014), whereas coagulopathy (P ¼ .001) and transfusion of > 10 U of packed red blood cells (PRBCs; P ¼ .003) were related to higher recurrent bleeding rates. One patient had a puncture site–related complication, and no bowel infarction was noted during follow-up. Conclusions: RAE was feasible and safe. The use of N-butyl-2-cyanoacrylate, presence of coagulopathy, and transfusion of > 10 U of PRBCs were significant factors related to recurrent bleeding. Bilateral inferior mesenteric artery and internal iliac artery angiography is highly recommended in the initial RAE session to achieve a high rate of bleeding control.
ABBREVIATIONS IIA ¼ internal iliac artery, IMA ¼ inferior mesenteric artery, NBCA ¼ N-butyl-2-cyanoacrylate, PRBC ¼ packed red blood cell, RAE ¼ rectal arterial embolization
Rectal bleeding makes up 9%–10% of cases of lower gastrointestinal bleeding (1,2). Underlying conditions include hemorrhoids, radiation proctitis, benign rectal ulcer, or colorectal cancer (3). Although most rectal bleeding
resolves spontaneously with conservative management, aggressive therapy, such as endoscopy, surgery, or transcatheter embolization of the rectal artery may be needed if the bleeding is life-threatening.
From the Department of Radiology (S.P.), Gachon University Gil Medical Center, Incheon, Korea; Department of Radiology (Y.K.), Chungbuk National University Hospital, Cheongju, Korea; Department of Radiology and Research Institute of Radiology (J.H.S., H.H.C., H.-K.Y.), Asan Medical Center, University of Ulsan College of Medicine, Olympic-ro 43gil, Seoul 05505, Korea; Department of Radiology (W.J.Y.), Korea University Guro Hospital, Seoul, Korea; Department of Radiology (S.Y.N.), Soon Chun Hyang University Seoul Hospital, Seoul, Korea; and Department of Radiology (C.S.C.), The Affiliated Cancer Hospital of Zhengzhou University, Zhengzhou, China. Received February 6, 2019; final revision received May 8, 2019; accepted May 12, 2019. Address correspondence to J.H.S.; E-mail: [email protected]
S.P. and Y.K. contributed equally to this work. None of the authors have identified a conflict of interest. © SIR, 2019 J Vasc Interv Radiol 2019; ▪:1–8 https://doi.org/10.1016/j.jvir.2019.05.013
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EDITORS’ RESEARCH HIGHLIGHTS This single-center 20-year retrospective study identified 34 patients with rectal bleeding who underwent embolization; the results highlight the rarity of the clinical context, ie, fewer than 2 procedures per year. The complexity of the clinical scenario of rectal hemorrhage and the complexity of rectal arterial supply is evident: despite successful embolization in 97% of patients (33 of 34), recurrent bleeding occurred in one third (n ¼ 11). This was mostly a result of patient-related factors, especially coagulopathy (P ¼ .001) and transfusion requirement of > 10 U of packed red blood cells (P ¼ .003). The dual arterial supply to the rectum from the inferior mesenteric artery (IMA) and both internal iliac arteries (IIAs) affected outcomes, as patients who underwent selective angiography of all vessels had better outcomes than those who underwent only IMA or IIA angiography (P ¼ .053). Use of liquid embolic agents such as N-butyl2-cyanoacrylate was correlated with less recurrent bleeding (P ¼ .014) without adverse events such as bowel ischemia or nontarget embolization. This success and safety may be a result of the high proportion of patients with coagulopathy (17.6%), hemodynamic instability (23.5%), and multiplicity of collateral vessels supplying the rectum. Study limitations include the small sample size, variations in angiographic protocols, patients lost to follow-up, and inconsistent postembolization sigmoidoscopy performed to assess potential rectal wall injury.
Endoscopic procedures constitute the initial diagnostic and treatment modalities because the rectum is easily examined by endoscopy (4). However, when the endoscopic treatment is insufficient, ie, if endoscopic access is unsuccessful because of a large amount of fresh blood, another treatment modality should be considered. Because surgical treatment is associated with significant morbidity as a result of surgery-related complications, rectal arterial embolization (RAE) can be considered as an alternative treatment modality. Transcatheter arterial embolization is valuable in identifying the specific bleeding site and achieving hemostasis by exclusion of the bleeding artery (5–7). In particular, RAE was introduced as a treatment modality for acute rectal bleeding (8–13) as well as for hemorrhoids, ie, the so-called emborrhoid technique (14). Bilateral internal iliac arteries (IIAs) and the inferior mesenteric artery (IMA) supply the rectum as the superior rectal artery from the IMA and the middle and inferior rectal arteries from the IIA (15–17). The purpose of the present study is to report the efficacy and safety of RAE for the treatment of rectal bleeding and to determine the prognostic factors related to recurrent bleeding based on the treatment of 34 patients in a single institution.
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MATERIALS AND METHODS This study was approved by the institutional review board, and the requirement for informed consent was waived in view of the retrospective study design. All patients with rectal bleeding detected by diagnostic angiography at a single institution from September 1998 to December 2018 were analyzed retrospectively. Thirty-four patients (13 women, 21 men; mean age, 66.1 y; age range, 31–96 years) were included in the study who had been referred for diagnostic angiography for suspicion of rectal bleeding based on clinical symptoms and signs, contrast-enhanced computed tomography (CT), and/or endoscopic findings. In the authors’ hospital, if lower gastrointestinal bleeding, including rectal bleeding, is clinically suspected, endoscopic workup with treatment is considered to be the first choice of treatment modality. However, if a patient is in hemodynamically unstable condition or sigmoidoscopy is not available, the patient is referred for RAE or surgical management first.
Patient Characteristics The study flow is outlined in Figure 1, and patient characteristics are displayed in Table 1. The most common etiology of rectal bleeding was a benign ulcer (n ¼ 16; 47.1%), followed by tumor (n ¼ 7; 20.6%), postoperative status (n ¼ 5; 14.7%), radiation proctitis (n ¼ 2; 5.9%), postpolypectomy status (n ¼ 1; 2.9%), and unknown causes (n ¼ 3; 8.8%). The incidence of benign ulcer was higher among patients in an immobilized state (as detailed later; 13 of 20; 65.0%) than in those in a mobilized state (3 of 14; 21.4%; P ¼ .016). Among the study patients, 50.0% (n ¼ 17) had undergone sigmoidoscopy and 29.4% (n ¼ 10) had undergone a preprocedural contrast-enhanced abdominopelvic CT scan. A total of 35.3% of patients (n ¼ 12) underwent immediate angiography without preangiography CT scan or sigmoidoscopy because of hemodynamically unstable condition. The most common cause of failure of sigmoidoscopic treatment was incomplete treatment as a result of massive bleeding (41.2%; 7 of 17), followed by lack of visibility as a result of poor bowel preparation (35.3%; 6 of 17) and incomplete treatment as a result of failed localization of bleeding focus (23.5%; 4 of 17). Findings of CT scans were contrast agent extravasation (40.0%; 4 of 10), pseudoaneurysm (20.0%; 2 of 10), and hematoma without evidence of active bleeding (40.0%; 4 of 10). Transfusion of packed red blood cells (PRBCs) was performed in 29 patients (85.3%). The mean volume of transfused PRBCs before RAE was 5.1 U (range, 0–30 U). Bleeding tendency, defined as an International Normalized Ratio of more than 1.5 and/or a platelet count of less than 50,000/μL at initial presentation before RAE, and hemodynamic instability, defined as hypotension with systolic blood pressure less than 90 mm Hg despite the use of vasopressor(s), were present in 6 (17.6%) and 8 (23.5%) patients, respectively (18–21).
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Figure 1. Study flowchart. (§Three patients died as a result of hypovolemic shock and metabolic acidosis within 1 week of embolization.)
Angiography and Embolization Technique Four experienced interventional radiologists (with 22, 18, 18, and 13 y of experience, respectively) performed angiography and embolization procedures. Angiography of the suspected arteries, including the IMA and/or IIA, was performed to identify the bleeding focus. Superior mesenteric artery angiography was performed if clinically needed. Positive angiographic findings included contrast agent extravasation (64.8%; n ¼ 22), pseudoaneurysm (2.9%; n ¼ 1), both contrast agent extravasation and pseudoaneurysm (11.8%; n ¼ 4), and hypervascularity (20.6%; n ¼ 7). If the bleeding was identified, the bleeding artery was superselectively embolized with the use of a 2.0–2.2-F microcatheter (Progreat; Terumo, Tokyo, Japan). The choice of embolic agent used for embolization was based on operator preference and included N-butyl-2cyanoacrylate (NBCA; B. Braun, Melsungen, Germany), microcoils (Hilal or Tornado; Cook, Bloomington, Indiana), and/or gelatin sponge particles (Spongostan; Johnson & Johnson, New Brunswick, New Jersey).
Technical success was defined as the occlusion and exclusion of the bleeding focus without evidence of active arterial bleeding on completion angiography. Bleeding control was defined as cessation of bleeding after the RAE without any evidence of recurrent bleeding that required further treatment during the hospital stay. Recurrent bleeding was defined as recurrent rectal bleeding during the clinical follow-up period or no improvement of the clinical signs and symptoms that prompted RAE, and required immediate treatment such as repeated RAE or endoscopic or surgical treatment. Incomplete angiography was defined as only IMA or IIA angiography performed during the initial RAE session. Multifocal bleeding was defined as cases in which the bleeding focus was multifocal, with embolization performed at 2 or more sites. The evidence of major complications including bowel ischemia/infarction was obtained by reviewing the electronic medical report and follow-up CT scan if available.
Statistical Analysis Study Endpoints and Definition Electronic medical records of the patients were reviewed to collect data on patient demographic characteristics; coagulation profile; number of transfusions before RAE; angiographic findings, including bleeding sites, technical success rate, and evidence of recurrent bleeding on followup records; and procedure-related major complications such as bowel infarction. Patients were considered to be in an immobilized state if they were confined to bed by neurologic or orthopedic diseases or any other condition that required an intensive care unit stay longer than 1 week.
Fisher exact test and analysis of variance were used to determine the prognostic factors associated with recurrent bleeding. All statistical analyses were performed with SPSS software (version 20.0; SPSS, Chicago, Illinois) for Windows (Microsoft, Redmond, Washington).
RESULTS The details of RAE are summarized in Table 2. The arteries examined in the initial session of RAE were the IMA (n ¼ 16; 47.0%), IIA (n¼ 6; 17.6%), and IMA andbilateral IIAs(n ¼ 12; 35.3%). A single type of embolic material was used in 24
4 ▪ Retrospective Study of Rectal Arterial Embolization for Bleeding
Table 1. Characteristics of Study Patients (N ¼ 34)
Table 2. Characteristics and Outcomes of Rectal Arterial Embolization
Characteristic
Value
Mean age (y)
66.1
Sex Female Male
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13 (38.2) 21 (61.8)
Cause
Characteristic
Incidence
Examined artery on initial session* IMA
16 (47.0)
IIA
6 (17.6)
IMA and bilateral IIAs
12 (35.3)
Angiographic finding
Benign ulcer
16 (47.1)
Tumor
7 (20.6)
Extravasation
Postoperative Radiation proctitis
5 (14.7) 2 (5.9)
Pseudoaneurysm
1 (2.9)
Extravasation and pseudoaneurysm
4 (11.8)
Postpolypectomy
1 (2.9)
Unknown
3 (8.8)
SRA
Transfusion of PRBCs Yes No
29 (85.3)
Single
5 (14.7)
Both MRA
Bleeding tendency Yes No
Hypervascularity Embolized artery in all sessions†
6 (17.6) 28 (82.4)
Hemodynamic instability* Yes
8 (23.5)
No
26 (76.5)
Immobilized state†
Single
22 (64.8)
7 (20.6) 23 (67.6) 22 1 4 (11.8) 4
Both
0
IRA Single
4 (11.8) 3
Both SRA and MRA
1 1 (2.9)
Yes
20 (58.8)
SRA and IRA
0
No
14 (41.2)
MRA and IRA
1 (2.9)
SRA, MRA, and IRA
1 (2.9)
In-hospital mortality caused by rectal bleeding Yes‡ No
Embolic materials 3 (8.8) 31 (91.2)
Single type of embolic materials Microcoils GSP
Overall in-hospital mortality Yes§
4 (11.8)
No
30 (88.2)
Note–Values in parentheses are percentages. PRBC ¼ packed red blood cell. *Defined as hypotension with systolic blood pressure of less than 90 mm Hg. † Patients confined to bed and required intensive care stay longer than 1 week. ‡ Three patients died of hypovolemic shock directly related to recurrent bleeding. § The remaining patient died 21 days after the procedure as a result of pneumonia.
patients,andmultipletypesofembolicmaterialwereusedinthe remaining 10. The embolic materials used most commonly were gelatin sponge particles (n ¼ 12; 35.3%; Fig 2), followed by a combination of microcoils with gelatin sponge (n ¼ 9; 26.5%), NBCA (n ¼ 9; 26.5%; Fig 3), or microcoils (n ¼ 3; 8.8%) and a combination of microcoils, gelatin sponge, and NBCA(n¼1;2.9%). The technical success rate was 97.1% (33 of 34). The technically unsuccessful case had a severe stenosis at the origin of the IMA. The bleeding focus was supplied by collateral flow from the superior mesenteric artery. A microcatheter could not be advanced to the bleeding focus because of the long and tortuous course of the supplying artery. Persistent bleeding was observed on completion
NBCA Multiple types of embolic materials
24 (70.6) 3 12 9 10 (29.4)
Microcoils and GSP
9
Microcoils, GSP and NBCA
1
Technical success Yes No
33 (97.1) 1 (2.9)
Bleeding control during hospital stay Yes
22 (64.7)
No
12 (35.3)
Major complications Yes
1 (2.9)
No
33 (97.1)
Note–Data in parentheses are percentages. GSP ¼ gelatin sponge particle; IIA ¼ internal iliac arteries; IMA ¼ inferior mesenteric artery; IRA ¼ inferior rectal artery; MRA ¼ middle rectal artery; NBCA ¼ N-butyl-2-cyanoacrylate; SRA ¼ superior rectal artery. *Diagnostic angiography for identifying the bleeding focus during the initial session of RAE. † Embolization of bleeding arteries in all sessions of RAE including initial and repeated sessions.
angiography despite embolization at the proximal portion of the superior rectal artery. Subsequent endoscopic bleeding control was performed, but it was insufficient and bleeding recurred. The patient was finally treated with surgical repair.
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Figure 2. Images from a 50-year-old man who presented with acute rectal bleeding from a benign rectal ulcer. (a) Inferior mesenteric angiography shows contrast medium extravasation (arrow) at the distal branch of the left superior rectal artery. (b) Postembolization angiography shows no further bleeding focus after embolization of the left distal superior rectal artery with the use of gelatin sponge particles. The patient presented again with acute rectal bleeding 1 day after the initial embolization. (c) Left internal iliac angiography shows contrast medium extravasation (arrow) at the distal branch of the left obturator artery. (d) Postembolization angiography shows no further bleeding focus after embolization of the left distal obturator artery with the use of gelatin sponge particles.
Bleeding control was achieved in 64.7% of patients (n ¼ 22). Among patients with bleeding control, 4 were lost to follow-up before 1 month: 1 died 21 days after the procedure as a result of underlying pneumonia, 1 underwent abdominoperineal excision 7 days after the procedure to treat rectal cancer, and the remaining 2 were transferred to another hospital 7 days after the procedure. Among the 11 patients with recurrent bleeding (32.4%), 3 underwent repeated RAE, which controlled the bleeding. Bleeding control rates of the initial RAE session and combined initial and repeated sessions were 64.7% (22 of 34) and 73.5% (25 of 34), respectively. Patients with and without recurrent bleeding after RAE (Table 3) were matched with respect to sex, cause of bleeding, bleeding tendency, transfusion of more than 10 U of PRBCs, immobilized state, multiplicity of embolized arteries, and evidence of active bleeding on CT (Fisher
exact test, P > .05). The use of an embolic agent other than NBCA was significantly correlated with recurrent bleeding (Fisher exact test, P ¼ .014; odds ratio, 0.565). The most common cause of recurrent bleeding was estimated to be incomplete initial angiography (90.9%; 10 of 11) with (n ¼ 2) or without (n ¼ 8) multifocal bleeding, followed by only multifocal bleeding (9.1%; 1 of 11). Among 10 patients with incomplete initial angiography, 6 underwent IMA angiography only and the remaining 4 underwent IIA angiography only. Among these 10 patients, 2 underwent a second RAE session and a complementary angiogram was obtained, which identified the bleeding focus, and bleeding control was achieved (Fig 2). The embolization procedures were well-tolerated, although a major complication occurred in 1 patient (2.9%): thrombosis developed in the punctured right common femoral artery approximately 6 hours after RAE,
6 ▪ Retrospective Study of Rectal Arterial Embolization for Bleeding
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Figure 3. Images from a 62-year-old man who presented with acute rectal bleeding 2 weeks after a lower anterior resection for rectal cancer. (a) Enhanced CT scan shows a pseudoaneurysm (arrow) in the right perirectal space. Right internal iliac (b) and selective (c) angiography show a pseudoaneurysm (arrow, b) in the distal branch of the right middle rectal artery. The right middle rectal artery was embolized with the use of NBCA. (d) No further visualization of the bleeding focus is shown on right internal iliac angiography.
massive hematochezia occurred during surgical thrombectomy, and the patient died 1 day after the procedure. There was no evidence of bowel infarction during follow-up on contrast-enhanced CT (20.6%; 7 of 34) and sigmoidoscopy (35.3%; 12 of 34) or based on electronic medical report review.
DISCUSSION The present study of 34 patients who underwent RAE to treat rectal bleeding showed that RAE is safe and feasible, with a high technical success rate of 97.1%. The result corresponds with those of several other studies of gastrointestinal bleeding (2,6,22–25), in which technical success rates range from 90% to 100%. In the present study, technical failure of RAE was encountered in 1 patient in whom
the microcatheter could not be advanced to the bleeding focus because of the long and tortuous course of the supplying artery. Previous studies (12,22,25) have reported 2 clinical failures caused by target vessel disappearance during selection of the supplying artery and severe atherosclerosis precluding a microcatheter approach to the bleeding focus. In the present study, the most frequent cause of rectal bleeding was a benign ulcer (47.1%), corresponding with other studies (12,22,25). Several reports (8,26) indicated that the risk factors for the development of benign rectal ulcers included prolonged convalescence, constipation, rectal instrumentation, and anticoagulation. In general, these conditions are commonly observed in immobilized patients. Therefore, benign rectal ulcers tend to occur more frequently in immobilized patients, as in 65.0% of the
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Table 3. Characteristics of Patients with or without Recurrent Bleeding after Embolization Characteristic
Recurrent Bleeding Yes (n ¼ 11)
No (n ¼ 23)
Sex Female
4
9
Male
7
14
Ulcer
8
8
Other
3
15
3
3
8
20
Yes
11
11
No
0
12
Yes
7
13
No
4
10
0 11
10 13
1
11
10
12
1
8
18
>1
3
5
1.000
Cause of bleeding
.066
Bleeding tendency Yes No Transfusion of > 10 U PRBCs
.001
.003
Immobilized state
1.000
Embolic materials NBCA Other
.014
Initial angiography† Complete Incomplete
.053
Embolized artery
Bleeding on preembolization CT Yes
P Value*
1.000
.169‡ 1
8
No
1
4
CT not taken
9
11
CI ¼ confidence interval; NBCA ¼ N-butyl cyanoacrylate; OR ¼ odds ratio; PRBC ¼ packed red blood cell. *Determined by Fisher exact test unless otherwise noted. † Complete angiography means the inferior mesenteric and bilateral internal iliac arteriograms were obtained at the initial session of RAE. Incomplete angiography means that one of the inferior mesenteric and bilateral internal iliac arteriograms were not obtained at the initial session of RAE. ‡ Analysis of variance.
immobilized patients (13 of 20) in the present study. Hur et al (12) reported that an immobilized state was of the significant risk factors in patients with rectal bleeding (67.5%), as opposed to those with small bowel (33.1%) and colon (11.1%) bleeding. In addition, an immobilized state was related to recurrent bleeding after embolization for lower gastrointestinal bleeding in the study by Hur et al (12), whereas the relationship between recurrent bleeding and benign rectal ulcer as a cause of bleeding was not statistically significant. It is important to be familiar with the prognostic factors related to recurrent bleeding because recurrent bleeding was
a major cause of patient mortality in the present study. In the present study, the use of NBCA was related to a significantly lower incidence of recurrent bleeding. This result may be explained by 2 factors. First, the use of NBCA can not only achieve complete embolization of the target artery, but NBCA also fills the adjacent potential collateral vessels. Therefore, more complete embolization is expected in the rectum, where there are multiple collateral vessels. Second, NBCA occludes the vessel by a polymerization mechanism, regardless of coagulation (9,12,27–29). Considering that patients with rectal bleeding are more likely to be in an immobilized state, accompanied by complex medical problems such as coagulopathy, NBCA can be considered as a useful material in embolization of rectal bleeding. In addition, there were no bowel infarctions after embolization with NBCA in the present study, as in previous studies (9,12,29). These results show that embolization with the use of NBCA is technically feasible, safe, and effective for the treatment of rectal bleeding. The average number of bleeding foci in rectal bleeding is known to be more than that in small or large bowel bleeding (12,22,25). This could be explained by the fact that the rectum has an abundant vascular supply and multiple potential collateral channels (10,17). There was a relatively low bleeding control rate in the present study compared with studies of bleeding in the small bowel (range, 74%–88%) and large bowel (75%–89%) (6,12,14,22). An understanding of possible multifocality in rectal bleeding is important because it is one of the main causes of treatment failure of RAE and therefore provides a rationale for comprehensive angiography, including at least the IMA and IIA. In the present study, IIA angiography was not performed as the initial angiography study in almost half of the patients (44.1%), and only 35.3% of the patients (12 of 34) underwent IMA and IIA angiography during the initial RAE session. Considering that the bleeding focus can also originate from the middle or inferior rectal arteries (38.2% of cases in the present study) and that multiple bleeding foci could be related to recurrent bleeding, it is highly recommended to perform complete angiography (ie, of the IMA and IIA) at the time of the initial session. The present study has several limitations. First, it is a retrospective study, and the standard protocol of diagnostic angiography in patients with acute rectal bleeding had not been not established during the study period. Second, hematologic parameters, time interval between the onset of bleeding and embolization, and long-term clinical outcomes were not included in the analysis. Third, embolizationrelated adverse events such as bowel infarction were evaluated by clinical record only. Sigmoidoscopy was not performed in all patients after embolization to assess potential rectal wall injury. Finally, analyses of all predictors were performed with unadjusted statistical tests not controlling for confounding. In conclusion, RAE is technically feasible and safe in the treatment of rectal bleeding. Use of embolic agents other
8 ▪ Retrospective Study of Rectal Arterial Embolization for Bleeding
than NBCA, coagulopathy, and transfusion of more than 10 U of PRBCs were significant factors related to recurrent bleeding. Angiography of bilateral IIAs as well as the IMA is highly recommended in the initial RAE session to achieve a high rate of bleeding control.
REFERENCES 1. Lee EW, Laberge JM. Differential diagnosis of gastrointestinal bleeding. Tech Vasc Interv Radiol 2004; 7:112–122. 2. Longstreth GF. Epidemiology and outcome of patients hospitalized with acute lower gastrointestinal hemorrhage: a population-based study. Am J Gastroenterol 1997; 92:419–424. 3. Adelstein BA, Macaskill P, Chan SF, Katelaris PH, Irwig L. Most bowel cancer symptoms do not indicate colorectal cancer and polyps: a systematic review. BMC Gastroenterol 2011; 11:65. 4. Van Rosendaal GM, Sutherland LR, Verhoef MJ, et al. Defining the role of fiberoptic sigmoidoscopy in the investigation of patients presenting with bright red rectal bleeding. Am J Gastroenterol 2000; 95:1184–1187. 5. Miller M Jr, Smith TP. Angiographic diagnosis and endovascular management of nonvariceal gastrointestinal hemorrhage. Gastroenterol Clin North Am 2005; 34:735–752. 6. Teng HC, Liang HL, Lin YH, et al. The efficacy and long-term outcome of microcoil embolotherapy for acute lower gastrointestinal bleeding. Korean J Radiol 2013; 14:259–268. 7. Shin JH. Recent update of embolization of upper gastrointestinal tract bleeding. Korean J Radiol 2012; 13(suppl 1):S31–S39. 8. Costouros NG, Niho H, Mahadevan U, Kerlan RK Jr, Bloom AI. Angiographic embolization for control of life-threatening hemorrhage from benign rectal ulcers. J Vasc Interv Radiol 2009; 20:561–562. 9. Syed MI, Chaudhry N, Shaikh A, Morar K, Mukerjee K, Damallie E. Catheter-directed middle hemorrhoidal artery embolization for lifethreatening rectal bleeding. Can J Gastroenterol 2007; 21:117–123. 10. Morar KN, Syed MI, Patel JK, Shaikh A. Embolization of middle hemorrhoidal artery in the management of life-threatening rectal bleeding. Cardiovasc Intervent Radiol 2006; 29:128–129. 11. Pichon N, Francois B, Pichon-Lefievre F, Mathonnet M, Maubon A, Vignon P. Embolization of rectal arteries: an alternative treatment for hemorrhagic shock induced by traumatic intrarectal hemorrhage. Cardiovasc Intervent Radiol 2005; 28:515–517. 12. Hur S, Jae HJ, Lee M, Kim HC, Chung JW. 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.
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13. Lee JH, Lee KH, Chung WS, Hur J, Won JY, Lee DY. Transcatheter embolization of the middle sacral artery: collateral feeder in recurrent rectal bleeding. AJR Am J Roentgenol 2004; 182:1055–1057. 14. Vidal V, Sapoval M, Sielezneff Y, et al. Emborrhoid: a new concept for the treatment of hemorrhoids with arterial embolization: the first 14 cases. Cardiovasc Intervent Radiol 2015; 38:72–78. 15. Bilhim T, Pereira JA, Tinto HR, et al. Middle rectal artery: myth or reality? Retrospective study with CT angiography and digital subtraction angiography. Surg Radiol Anat 2013; 35:517–522. 16. Schuurman JP, Go PM, Bleys RL. Anatomical branches of the superior rectal artery in the distal rectum. Colorectal Dis 2009; 11:967–971. 17. Ayoub SF. Arterial supply to the human rectum. Acta Anat 1978; 100: 317–327. 18. O’Connor SD, Taylor AJ, Williams EC, Winter TC. Coagulation concepts update. AJR Am J Roentgenol 2009; 193:1656–1664. 19. Malloy PC, Grassi CJ, Kundu S, et al. Consensus guidelines for periprocedural management of coagulation status and hemostasis risk in percutaneous image-guided interventions. J Vasc Interv Radiol 2009; 20(7 suppl):S240–S249. 20. Strauss RG. Pretransfusion trigger platelet counts and dose for prophylactic platelet transfusions. Curr Opin Hematol 2005; 12:499–502. 21. Shander A, Goodnough LT. Update on transfusion medicine. Pharmacotherapy 2007; 27(part 2):57s–68s. 22. Kickuth R, Rattunde H, Gschossmann J, Inderbitzin D, Ludwig K, Triller J. Acute lower gastrointestinal hemorrhage: minimally invasive management with microcatheter embolization. J Vasc Interv Radiol 2008; 19: 1289–1296.e2. 23. Kwak HS, Han YM, Lee ST. The clinical outcomes of transcatheter microcoil embolization in patients with active lower gastrointestinal bleeding in the small bowel. Korean J Radiol 2009; 10:391–397. 24. Tan KK, Wong D, Sim R. Superselective embolization for lower gastrointestinal hemorrhage: an institutional review over 7 years. World J Surg 2008; 32:2707–2715. 25. Kuo WT, Lee DE, Saad WE, Patel N, Sahler LG, Waldman DL. Superselective microcoil embolization for the treatment of lower gastrointestinal hemorrhage. J Vasc Interv Radiol 2003; 14:1503–1509. 26. Hendrickson RJ, Diaz AA, Salloum R, Koniaris LG. Benign rectal ulcer: an underground cause of inpatient lower gastrointestinal bleeding. Surg Endosc 2003; 17:1759–1765. 27. Koo HJ, Shin JH, Kim HJ, 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. 28. Valji K. Cyanoacrylates for embolization in gastrointestinal bleeding: how super is glue? J Vasc Interv Radiol 2014; 25:20–21. 29. Frodsham A, Berkmen T, Ananian C, Fung A. Initial experience using Nbutyl cyanoacrylate for embolization of lower gastrointestinal hemorrhage. J Vasc Interv Radiol 2009; 20:1312–1319.
Outcome of Rectal Arterial Embolization for Rectal Bleeding in 34 Patients: A Single-Center Retrospective Study over 20 Years Suyoung Park, MD, Yook Kim, MD, Ji Hoon Shin, MD, Woo Jin Yang, MD, Seung Yeon Noh, MD, Hee Ho Chu, MD, Cheng Shi Chen, MD, and Hyun-Ki Yoon, MD ABSTRACT Purpose: To report the efficacy of rectal artery embolization (RAE) for the treatment of rectal bleeding and the prognostic factors related to recurrent bleeding. Materials and Methods: A total of 34 patients in a single center who underwent RAE for treatment of rectal bleeding between September 1998 and December 2018 were retrospectively reviewed. Procedure details including angiographic findings and embolic materials used, technical success rate, bleeding control rate during hospital stay, major adverse event rate, and prognostic factors associated with recurrent bleeding were evaluated. Results: Technical success rate was 97.1% (33 of 34). Bleeding control during hospital stay was achieved in 64.7% of patients (n ¼ 22). The most common bleeding focus was in the superior rectal artery. Recurrent bleeding occurred in 11 patients. Incomplete initial angiography with only an inferior mesenteric or internal iliac angiogram had been performed in 90.9% of patients with recurrent bleeding (10 of 11) and 52.2% of patients with bleeding control (12 of 23; P ¼ .053). The use of N-butyl-2-cyanoacrylate was related to a significantly lower incidence of recurrent bleeding (P ¼ .014), whereas coagulopathy (P ¼ .001) and transfusion of > 10 U of packed red blood cells (PRBCs; P ¼ .003) were related to higher recurrent bleeding rates. One patient had a puncture site–related complication, and no bowel infarction was noted during follow-up. Conclusions: RAE was feasible and safe. The use of N-butyl-2-cyanoacrylate, presence of coagulopathy, and transfusion of > 10 U of PRBCs were significant factors related to recurrent bleeding. Bilateral inferior mesenteric artery and internal iliac artery angiography is highly recommended in the initial RAE session to achieve a high rate of bleeding control.
ABBREVIATIONS IIA ¼ internal iliac artery, IMA ¼ inferior mesenteric artery, NBCA ¼ N-butyl-2-cyanoacrylate, PRBC ¼ packed red blood cell, RAE ¼ rectal arterial embolization
Rectal bleeding makes up 9%–10% of cases of lower gastrointestinal bleeding (1,2). Underlying conditions include hemorrhoids, radiation proctitis, benign rectal ulcer, or colorectal cancer (3). Although most rectal bleeding
resolves spontaneously with conservative management, aggressive therapy, such as endoscopy, surgery, or transcatheter embolization of the rectal artery may be needed if the bleeding is life-threatening.
From the Department of Radiology (S.P.), Gachon University Gil Medical Center, Incheon, Korea; Department of Radiology (Y.K.), Chungbuk National University Hospital, Cheongju, Korea; Department of Radiology and Research Institute of Radiology (J.H.S., H.H.C., H.-K.Y.), Asan Medical Center, University of Ulsan College of Medicine, Olympic-ro 43gil, Seoul 05505, Korea; Department of Radiology (W.J.Y.), Korea University Guro Hospital, Seoul, Korea; Department of Radiology (S.Y.N.), Soon Chun Hyang University Seoul Hospital, Seoul, Korea; and Department of Radiology (C.S.C.), The Affiliated Cancer Hospital of Zhengzhou University, Zhengzhou, China. Received February 6, 2019; final revision received May 8, 2019; accepted May 12, 2019. Address correspondence to J.H.S.; E-mail: [email protected]
S.P. and Y.K. contributed equally to this work. None of the authors have identified a conflict of interest. © SIR, 2019 J Vasc Interv Radiol 2019; ▪:1–8 https://doi.org/10.1016/j.jvir.2019.05.013
2 ▪ Retrospective Study of Rectal Arterial Embolization for Bleeding
EDITORS’ RESEARCH HIGHLIGHTS This single-center 20-year retrospective study identified 34 patients with rectal bleeding who underwent embolization; the results highlight the rarity of the clinical context, ie, fewer than 2 procedures per year. The complexity of the clinical scenario of rectal hemorrhage and the complexity of rectal arterial supply is evident: despite successful embolization in 97% of patients (33 of 34), recurrent bleeding occurred in one third (n ¼ 11). This was mostly a result of patient-related factors, especially coagulopathy (P ¼ .001) and transfusion requirement of > 10 U of packed red blood cells (P ¼ .003). The dual arterial supply to the rectum from the inferior mesenteric artery (IMA) and both internal iliac arteries (IIAs) affected outcomes, as patients who underwent selective angiography of all vessels had better outcomes than those who underwent only IMA or IIA angiography (P ¼ .053). Use of liquid embolic agents such as N-butyl2-cyanoacrylate was correlated with less recurrent bleeding (P ¼ .014) without adverse events such as bowel ischemia or nontarget embolization. This success and safety may be a result of the high proportion of patients with coagulopathy (17.6%), hemodynamic instability (23.5%), and multiplicity of collateral vessels supplying the rectum. Study limitations include the small sample size, variations in angiographic protocols, patients lost to follow-up, and inconsistent postembolization sigmoidoscopy performed to assess potential rectal wall injury.
Endoscopic procedures constitute the initial diagnostic and treatment modalities because the rectum is easily examined by endoscopy (4). However, when the endoscopic treatment is insufficient, ie, if endoscopic access is unsuccessful because of a large amount of fresh blood, another treatment modality should be considered. Because surgical treatment is associated with significant morbidity as a result of surgery-related complications, rectal arterial embolization (RAE) can be considered as an alternative treatment modality. Transcatheter arterial embolization is valuable in identifying the specific bleeding site and achieving hemostasis by exclusion of the bleeding artery (5–7). In particular, RAE was introduced as a treatment modality for acute rectal bleeding (8–13) as well as for hemorrhoids, ie, the so-called emborrhoid technique (14). Bilateral internal iliac arteries (IIAs) and the inferior mesenteric artery (IMA) supply the rectum as the superior rectal artery from the IMA and the middle and inferior rectal arteries from the IIA (15–17). The purpose of the present study is to report the efficacy and safety of RAE for the treatment of rectal bleeding and to determine the prognostic factors related to recurrent bleeding based on the treatment of 34 patients in a single institution.
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MATERIALS AND METHODS This study was approved by the institutional review board, and the requirement for informed consent was waived in view of the retrospective study design. All patients with rectal bleeding detected by diagnostic angiography at a single institution from September 1998 to December 2018 were analyzed retrospectively. Thirty-four patients (13 women, 21 men; mean age, 66.1 y; age range, 31–96 years) were included in the study who had been referred for diagnostic angiography for suspicion of rectal bleeding based on clinical symptoms and signs, contrast-enhanced computed tomography (CT), and/or endoscopic findings. In the authors’ hospital, if lower gastrointestinal bleeding, including rectal bleeding, is clinically suspected, endoscopic workup with treatment is considered to be the first choice of treatment modality. However, if a patient is in hemodynamically unstable condition or sigmoidoscopy is not available, the patient is referred for RAE or surgical management first.
Patient Characteristics The study flow is outlined in Figure 1, and patient characteristics are displayed in Table 1. The most common etiology of rectal bleeding was a benign ulcer (n ¼ 16; 47.1%), followed by tumor (n ¼ 7; 20.6%), postoperative status (n ¼ 5; 14.7%), radiation proctitis (n ¼ 2; 5.9%), postpolypectomy status (n ¼ 1; 2.9%), and unknown causes (n ¼ 3; 8.8%). The incidence of benign ulcer was higher among patients in an immobilized state (as detailed later; 13 of 20; 65.0%) than in those in a mobilized state (3 of 14; 21.4%; P ¼ .016). Among the study patients, 50.0% (n ¼ 17) had undergone sigmoidoscopy and 29.4% (n ¼ 10) had undergone a preprocedural contrast-enhanced abdominopelvic CT scan. A total of 35.3% of patients (n ¼ 12) underwent immediate angiography without preangiography CT scan or sigmoidoscopy because of hemodynamically unstable condition. The most common cause of failure of sigmoidoscopic treatment was incomplete treatment as a result of massive bleeding (41.2%; 7 of 17), followed by lack of visibility as a result of poor bowel preparation (35.3%; 6 of 17) and incomplete treatment as a result of failed localization of bleeding focus (23.5%; 4 of 17). Findings of CT scans were contrast agent extravasation (40.0%; 4 of 10), pseudoaneurysm (20.0%; 2 of 10), and hematoma without evidence of active bleeding (40.0%; 4 of 10). Transfusion of packed red blood cells (PRBCs) was performed in 29 patients (85.3%). The mean volume of transfused PRBCs before RAE was 5.1 U (range, 0–30 U). Bleeding tendency, defined as an International Normalized Ratio of more than 1.5 and/or a platelet count of less than 50,000/μL at initial presentation before RAE, and hemodynamic instability, defined as hypotension with systolic blood pressure less than 90 mm Hg despite the use of vasopressor(s), were present in 6 (17.6%) and 8 (23.5%) patients, respectively (18–21).
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Figure 1. Study flowchart. (§Three patients died as a result of hypovolemic shock and metabolic acidosis within 1 week of embolization.)
Angiography and Embolization Technique Four experienced interventional radiologists (with 22, 18, 18, and 13 y of experience, respectively) performed angiography and embolization procedures. Angiography of the suspected arteries, including the IMA and/or IIA, was performed to identify the bleeding focus. Superior mesenteric artery angiography was performed if clinically needed. Positive angiographic findings included contrast agent extravasation (64.8%; n ¼ 22), pseudoaneurysm (2.9%; n ¼ 1), both contrast agent extravasation and pseudoaneurysm (11.8%; n ¼ 4), and hypervascularity (20.6%; n ¼ 7). If the bleeding was identified, the bleeding artery was superselectively embolized with the use of a 2.0–2.2-F microcatheter (Progreat; Terumo, Tokyo, Japan). The choice of embolic agent used for embolization was based on operator preference and included N-butyl-2cyanoacrylate (NBCA; B. Braun, Melsungen, Germany), microcoils (Hilal or Tornado; Cook, Bloomington, Indiana), and/or gelatin sponge particles (Spongostan; Johnson & Johnson, New Brunswick, New Jersey).
Technical success was defined as the occlusion and exclusion of the bleeding focus without evidence of active arterial bleeding on completion angiography. Bleeding control was defined as cessation of bleeding after the RAE without any evidence of recurrent bleeding that required further treatment during the hospital stay. Recurrent bleeding was defined as recurrent rectal bleeding during the clinical follow-up period or no improvement of the clinical signs and symptoms that prompted RAE, and required immediate treatment such as repeated RAE or endoscopic or surgical treatment. Incomplete angiography was defined as only IMA or IIA angiography performed during the initial RAE session. Multifocal bleeding was defined as cases in which the bleeding focus was multifocal, with embolization performed at 2 or more sites. The evidence of major complications including bowel ischemia/infarction was obtained by reviewing the electronic medical report and follow-up CT scan if available.
Statistical Analysis Study Endpoints and Definition Electronic medical records of the patients were reviewed to collect data on patient demographic characteristics; coagulation profile; number of transfusions before RAE; angiographic findings, including bleeding sites, technical success rate, and evidence of recurrent bleeding on followup records; and procedure-related major complications such as bowel infarction. Patients were considered to be in an immobilized state if they were confined to bed by neurologic or orthopedic diseases or any other condition that required an intensive care unit stay longer than 1 week.
Fisher exact test and analysis of variance were used to determine the prognostic factors associated with recurrent bleeding. All statistical analyses were performed with SPSS software (version 20.0; SPSS, Chicago, Illinois) for Windows (Microsoft, Redmond, Washington).
RESULTS The details of RAE are summarized in Table 2. The arteries examined in the initial session of RAE were the IMA (n ¼ 16; 47.0%), IIA (n¼ 6; 17.6%), and IMA andbilateral IIAs(n ¼ 12; 35.3%). A single type of embolic material was used in 24
4 ▪ Retrospective Study of Rectal Arterial Embolization for Bleeding
Table 1. Characteristics of Study Patients (N ¼ 34)
Table 2. Characteristics and Outcomes of Rectal Arterial Embolization
Characteristic
Value
Mean age (y)
66.1
Sex Female Male
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13 (38.2) 21 (61.8)
Cause
Characteristic
Incidence
Examined artery on initial session* IMA
16 (47.0)
IIA
6 (17.6)
IMA and bilateral IIAs
12 (35.3)
Angiographic finding
Benign ulcer
16 (47.1)
Tumor
7 (20.6)
Extravasation
Postoperative Radiation proctitis
5 (14.7) 2 (5.9)
Pseudoaneurysm
1 (2.9)
Extravasation and pseudoaneurysm
4 (11.8)
Postpolypectomy
1 (2.9)
Unknown
3 (8.8)
SRA
Transfusion of PRBCs Yes No
29 (85.3)
Single
5 (14.7)
Both MRA
Bleeding tendency Yes No
Hypervascularity Embolized artery in all sessions†
6 (17.6) 28 (82.4)
Hemodynamic instability* Yes
8 (23.5)
No
26 (76.5)
Immobilized state†
Single
22 (64.8)
7 (20.6) 23 (67.6) 22 1 4 (11.8) 4
Both
0
IRA Single
4 (11.8) 3
Both SRA and MRA
1 1 (2.9)
Yes
20 (58.8)
SRA and IRA
0
No
14 (41.2)
MRA and IRA
1 (2.9)
SRA, MRA, and IRA
1 (2.9)
In-hospital mortality caused by rectal bleeding Yes‡ No
Embolic materials 3 (8.8) 31 (91.2)
Single type of embolic materials Microcoils GSP
Overall in-hospital mortality Yes§
4 (11.8)
No
30 (88.2)
Note–Values in parentheses are percentages. PRBC ¼ packed red blood cell. *Defined as hypotension with systolic blood pressure of less than 90 mm Hg. † Patients confined to bed and required intensive care stay longer than 1 week. ‡ Three patients died of hypovolemic shock directly related to recurrent bleeding. § The remaining patient died 21 days after the procedure as a result of pneumonia.
patients,andmultipletypesofembolicmaterialwereusedinthe remaining 10. The embolic materials used most commonly were gelatin sponge particles (n ¼ 12; 35.3%; Fig 2), followed by a combination of microcoils with gelatin sponge (n ¼ 9; 26.5%), NBCA (n ¼ 9; 26.5%; Fig 3), or microcoils (n ¼ 3; 8.8%) and a combination of microcoils, gelatin sponge, and NBCA(n¼1;2.9%). The technical success rate was 97.1% (33 of 34). The technically unsuccessful case had a severe stenosis at the origin of the IMA. The bleeding focus was supplied by collateral flow from the superior mesenteric artery. A microcatheter could not be advanced to the bleeding focus because of the long and tortuous course of the supplying artery. Persistent bleeding was observed on completion
NBCA Multiple types of embolic materials
24 (70.6) 3 12 9 10 (29.4)
Microcoils and GSP
9
Microcoils, GSP and NBCA
1
Technical success Yes No
33 (97.1) 1 (2.9)
Bleeding control during hospital stay Yes
22 (64.7)
No
12 (35.3)
Major complications Yes
1 (2.9)
No
33 (97.1)
Note–Data in parentheses are percentages. GSP ¼ gelatin sponge particle; IIA ¼ internal iliac arteries; IMA ¼ inferior mesenteric artery; IRA ¼ inferior rectal artery; MRA ¼ middle rectal artery; NBCA ¼ N-butyl-2-cyanoacrylate; SRA ¼ superior rectal artery. *Diagnostic angiography for identifying the bleeding focus during the initial session of RAE. † Embolization of bleeding arteries in all sessions of RAE including initial and repeated sessions.
angiography despite embolization at the proximal portion of the superior rectal artery. Subsequent endoscopic bleeding control was performed, but it was insufficient and bleeding recurred. The patient was finally treated with surgical repair.
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Figure 2. Images from a 50-year-old man who presented with acute rectal bleeding from a benign rectal ulcer. (a) Inferior mesenteric angiography shows contrast medium extravasation (arrow) at the distal branch of the left superior rectal artery. (b) Postembolization angiography shows no further bleeding focus after embolization of the left distal superior rectal artery with the use of gelatin sponge particles. The patient presented again with acute rectal bleeding 1 day after the initial embolization. (c) Left internal iliac angiography shows contrast medium extravasation (arrow) at the distal branch of the left obturator artery. (d) Postembolization angiography shows no further bleeding focus after embolization of the left distal obturator artery with the use of gelatin sponge particles.
Bleeding control was achieved in 64.7% of patients (n ¼ 22). Among patients with bleeding control, 4 were lost to follow-up before 1 month: 1 died 21 days after the procedure as a result of underlying pneumonia, 1 underwent abdominoperineal excision 7 days after the procedure to treat rectal cancer, and the remaining 2 were transferred to another hospital 7 days after the procedure. Among the 11 patients with recurrent bleeding (32.4%), 3 underwent repeated RAE, which controlled the bleeding. Bleeding control rates of the initial RAE session and combined initial and repeated sessions were 64.7% (22 of 34) and 73.5% (25 of 34), respectively. Patients with and without recurrent bleeding after RAE (Table 3) were matched with respect to sex, cause of bleeding, bleeding tendency, transfusion of more than 10 U of PRBCs, immobilized state, multiplicity of embolized arteries, and evidence of active bleeding on CT (Fisher
exact test, P > .05). The use of an embolic agent other than NBCA was significantly correlated with recurrent bleeding (Fisher exact test, P ¼ .014; odds ratio, 0.565). The most common cause of recurrent bleeding was estimated to be incomplete initial angiography (90.9%; 10 of 11) with (n ¼ 2) or without (n ¼ 8) multifocal bleeding, followed by only multifocal bleeding (9.1%; 1 of 11). Among 10 patients with incomplete initial angiography, 6 underwent IMA angiography only and the remaining 4 underwent IIA angiography only. Among these 10 patients, 2 underwent a second RAE session and a complementary angiogram was obtained, which identified the bleeding focus, and bleeding control was achieved (Fig 2). The embolization procedures were well-tolerated, although a major complication occurred in 1 patient (2.9%): thrombosis developed in the punctured right common femoral artery approximately 6 hours after RAE,
6 ▪ Retrospective Study of Rectal Arterial Embolization for Bleeding
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Figure 3. Images from a 62-year-old man who presented with acute rectal bleeding 2 weeks after a lower anterior resection for rectal cancer. (a) Enhanced CT scan shows a pseudoaneurysm (arrow) in the right perirectal space. Right internal iliac (b) and selective (c) angiography show a pseudoaneurysm (arrow, b) in the distal branch of the right middle rectal artery. The right middle rectal artery was embolized with the use of NBCA. (d) No further visualization of the bleeding focus is shown on right internal iliac angiography.
massive hematochezia occurred during surgical thrombectomy, and the patient died 1 day after the procedure. There was no evidence of bowel infarction during follow-up on contrast-enhanced CT (20.6%; 7 of 34) and sigmoidoscopy (35.3%; 12 of 34) or based on electronic medical report review.
DISCUSSION The present study of 34 patients who underwent RAE to treat rectal bleeding showed that RAE is safe and feasible, with a high technical success rate of 97.1%. The result corresponds with those of several other studies of gastrointestinal bleeding (2,6,22–25), in which technical success rates range from 90% to 100%. In the present study, technical failure of RAE was encountered in 1 patient in whom
the microcatheter could not be advanced to the bleeding focus because of the long and tortuous course of the supplying artery. Previous studies (12,22,25) have reported 2 clinical failures caused by target vessel disappearance during selection of the supplying artery and severe atherosclerosis precluding a microcatheter approach to the bleeding focus. In the present study, the most frequent cause of rectal bleeding was a benign ulcer (47.1%), corresponding with other studies (12,22,25). Several reports (8,26) indicated that the risk factors for the development of benign rectal ulcers included prolonged convalescence, constipation, rectal instrumentation, and anticoagulation. In general, these conditions are commonly observed in immobilized patients. Therefore, benign rectal ulcers tend to occur more frequently in immobilized patients, as in 65.0% of the
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Table 3. Characteristics of Patients with or without Recurrent Bleeding after Embolization Characteristic
Recurrent Bleeding Yes (n ¼ 11)
No (n ¼ 23)
Sex Female
4
9
Male
7
14
Ulcer
8
8
Other
3
15
3
3
8
20
Yes
11
11
No
0
12
Yes
7
13
No
4
10
0 11
10 13
1
11
10
12
1
8
18
>1
3
5
1.000
Cause of bleeding
.066
Bleeding tendency Yes No Transfusion of > 10 U PRBCs
.001
.003
Immobilized state
1.000
Embolic materials NBCA Other
.014
Initial angiography† Complete Incomplete
.053
Embolized artery
Bleeding on preembolization CT Yes
P Value*
1.000
.169‡ 1
8
No
1
4
CT not taken
9
11
CI ¼ confidence interval; NBCA ¼ N-butyl cyanoacrylate; OR ¼ odds ratio; PRBC ¼ packed red blood cell. *Determined by Fisher exact test unless otherwise noted. † Complete angiography means the inferior mesenteric and bilateral internal iliac arteriograms were obtained at the initial session of RAE. Incomplete angiography means that one of the inferior mesenteric and bilateral internal iliac arteriograms were not obtained at the initial session of RAE. ‡ Analysis of variance.
immobilized patients (13 of 20) in the present study. Hur et al (12) reported that an immobilized state was of the significant risk factors in patients with rectal bleeding (67.5%), as opposed to those with small bowel (33.1%) and colon (11.1%) bleeding. In addition, an immobilized state was related to recurrent bleeding after embolization for lower gastrointestinal bleeding in the study by Hur et al (12), whereas the relationship between recurrent bleeding and benign rectal ulcer as a cause of bleeding was not statistically significant. It is important to be familiar with the prognostic factors related to recurrent bleeding because recurrent bleeding was
a major cause of patient mortality in the present study. In the present study, the use of NBCA was related to a significantly lower incidence of recurrent bleeding. This result may be explained by 2 factors. First, the use of NBCA can not only achieve complete embolization of the target artery, but NBCA also fills the adjacent potential collateral vessels. Therefore, more complete embolization is expected in the rectum, where there are multiple collateral vessels. Second, NBCA occludes the vessel by a polymerization mechanism, regardless of coagulation (9,12,27–29). Considering that patients with rectal bleeding are more likely to be in an immobilized state, accompanied by complex medical problems such as coagulopathy, NBCA can be considered as a useful material in embolization of rectal bleeding. In addition, there were no bowel infarctions after embolization with NBCA in the present study, as in previous studies (9,12,29). These results show that embolization with the use of NBCA is technically feasible, safe, and effective for the treatment of rectal bleeding. The average number of bleeding foci in rectal bleeding is known to be more than that in small or large bowel bleeding (12,22,25). This could be explained by the fact that the rectum has an abundant vascular supply and multiple potential collateral channels (10,17). There was a relatively low bleeding control rate in the present study compared with studies of bleeding in the small bowel (range, 74%–88%) and large bowel (75%–89%) (6,12,14,22). An understanding of possible multifocality in rectal bleeding is important because it is one of the main causes of treatment failure of RAE and therefore provides a rationale for comprehensive angiography, including at least the IMA and IIA. In the present study, IIA angiography was not performed as the initial angiography study in almost half of the patients (44.1%), and only 35.3% of the patients (12 of 34) underwent IMA and IIA angiography during the initial RAE session. Considering that the bleeding focus can also originate from the middle or inferior rectal arteries (38.2% of cases in the present study) and that multiple bleeding foci could be related to recurrent bleeding, it is highly recommended to perform complete angiography (ie, of the IMA and IIA) at the time of the initial session. The present study has several limitations. First, it is a retrospective study, and the standard protocol of diagnostic angiography in patients with acute rectal bleeding had not been not established during the study period. Second, hematologic parameters, time interval between the onset of bleeding and embolization, and long-term clinical outcomes were not included in the analysis. Third, embolizationrelated adverse events such as bowel infarction were evaluated by clinical record only. Sigmoidoscopy was not performed in all patients after embolization to assess potential rectal wall injury. Finally, analyses of all predictors were performed with unadjusted statistical tests not controlling for confounding. In conclusion, RAE is technically feasible and safe in the treatment of rectal bleeding. Use of embolic agents other
8 ▪ Retrospective Study of Rectal Arterial Embolization for Bleeding
than NBCA, coagulopathy, and transfusion of more than 10 U of PRBCs were significant factors related to recurrent bleeding. Angiography of bilateral IIAs as well as the IMA is highly recommended in the initial RAE session to achieve a high rate of bleeding control.
REFERENCES 1. Lee EW, Laberge JM. Differential diagnosis of gastrointestinal bleeding. Tech Vasc Interv Radiol 2004; 7:112–122. 2. Longstreth GF. Epidemiology and outcome of patients hospitalized with acute lower gastrointestinal hemorrhage: a population-based study. Am J Gastroenterol 1997; 92:419–424. 3. Adelstein BA, Macaskill P, Chan SF, Katelaris PH, Irwig L. Most bowel cancer symptoms do not indicate colorectal cancer and polyps: a systematic review. BMC Gastroenterol 2011; 11:65. 4. Van Rosendaal GM, Sutherland LR, Verhoef MJ, et al. Defining the role of fiberoptic sigmoidoscopy in the investigation of patients presenting with bright red rectal bleeding. Am J Gastroenterol 2000; 95:1184–1187. 5. Miller M Jr, Smith TP. Angiographic diagnosis and endovascular management of nonvariceal gastrointestinal hemorrhage. Gastroenterol Clin North Am 2005; 34:735–752. 6. Teng HC, Liang HL, Lin YH, et al. The efficacy and long-term outcome of microcoil embolotherapy for acute lower gastrointestinal bleeding. Korean J Radiol 2013; 14:259–268. 7. Shin JH. Recent update of embolization of upper gastrointestinal tract bleeding. Korean J Radiol 2012; 13(suppl 1):S31–S39. 8. Costouros NG, Niho H, Mahadevan U, Kerlan RK Jr, Bloom AI. Angiographic embolization for control of life-threatening hemorrhage from benign rectal ulcers. J Vasc Interv Radiol 2009; 20:561–562. 9. Syed MI, Chaudhry N, Shaikh A, Morar K, Mukerjee K, Damallie E. Catheter-directed middle hemorrhoidal artery embolization for lifethreatening rectal bleeding. Can J Gastroenterol 2007; 21:117–123. 10. Morar KN, Syed MI, Patel JK, Shaikh A. Embolization of middle hemorrhoidal artery in the management of life-threatening rectal bleeding. Cardiovasc Intervent Radiol 2006; 29:128–129. 11. Pichon N, Francois B, Pichon-Lefievre F, Mathonnet M, Maubon A, Vignon P. Embolization of rectal arteries: an alternative treatment for hemorrhagic shock induced by traumatic intrarectal hemorrhage. Cardiovasc Intervent Radiol 2005; 28:515–517. 12. Hur S, Jae HJ, Lee M, Kim HC, Chung JW. 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.
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13. Lee JH, Lee KH, Chung WS, Hur J, Won JY, Lee DY. Transcatheter embolization of the middle sacral artery: collateral feeder in recurrent rectal bleeding. AJR Am J Roentgenol 2004; 182:1055–1057. 14. Vidal V, Sapoval M, Sielezneff Y, et al. Emborrhoid: a new concept for the treatment of hemorrhoids with arterial embolization: the first 14 cases. Cardiovasc Intervent Radiol 2015; 38:72–78. 15. Bilhim T, Pereira JA, Tinto HR, et al. Middle rectal artery: myth or reality? Retrospective study with CT angiography and digital subtraction angiography. Surg Radiol Anat 2013; 35:517–522. 16. Schuurman JP, Go PM, Bleys RL. Anatomical branches of the superior rectal artery in the distal rectum. Colorectal Dis 2009; 11:967–971. 17. Ayoub SF. Arterial supply to the human rectum. Acta Anat 1978; 100: 317–327. 18. O’Connor SD, Taylor AJ, Williams EC, Winter TC. Coagulation concepts update. AJR Am J Roentgenol 2009; 193:1656–1664. 19. Malloy PC, Grassi CJ, Kundu S, et al. Consensus guidelines for periprocedural management of coagulation status and hemostasis risk in percutaneous image-guided interventions. J Vasc Interv Radiol 2009; 20(7 suppl):S240–S249. 20. Strauss RG. Pretransfusion trigger platelet counts and dose for prophylactic platelet transfusions. Curr Opin Hematol 2005; 12:499–502. 21. Shander A, Goodnough LT. Update on transfusion medicine. Pharmacotherapy 2007; 27(part 2):57s–68s. 22. Kickuth R, Rattunde H, Gschossmann J, Inderbitzin D, Ludwig K, Triller J. Acute lower gastrointestinal hemorrhage: minimally invasive management with microcatheter embolization. J Vasc Interv Radiol 2008; 19: 1289–1296.e2. 23. Kwak HS, Han YM, Lee ST. The clinical outcomes of transcatheter microcoil embolization in patients with active lower gastrointestinal bleeding in the small bowel. Korean J Radiol 2009; 10:391–397. 24. Tan KK, Wong D, Sim R. Superselective embolization for lower gastrointestinal hemorrhage: an institutional review over 7 years. World J Surg 2008; 32:2707–2715. 25. Kuo WT, Lee DE, Saad WE, Patel N, Sahler LG, Waldman DL. Superselective microcoil embolization for the treatment of lower gastrointestinal hemorrhage. J Vasc Interv Radiol 2003; 14:1503–1509. 26. Hendrickson RJ, Diaz AA, Salloum R, Koniaris LG. Benign rectal ulcer: an underground cause of inpatient lower gastrointestinal bleeding. Surg Endosc 2003; 17:1759–1765. 27. Koo HJ, Shin JH, Kim HJ, 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. 28. Valji K. Cyanoacrylates for embolization in gastrointestinal bleeding: how super is glue? J Vasc Interv Radiol 2014; 25:20–21. 29. Frodsham A, Berkmen T, Ananian C, Fung A. Initial experience using Nbutyl cyanoacrylate for embolization of lower gastrointestinal hemorrhage. J Vasc Interv Radiol 2009; 20:1312–1319.