Background

AVF is an aberrant direct link between an artery and a vein that bypasses the capillary bed and can be acquired or congenital [1]. Despite the early report of AVF in 1947, fistula of the superior mesenteric artery (SMA) and inferior mesenteric artery (IMA) are still considered rare entities [2], which are easily misdiagnosed [3]. Splanchnic AVFs have been recorded in hundreds of cases, primarily between the hepatic, splenic, and superior mesenteric arteries, with only a few examples of superior and inferior mesenteric AVFs reported in the literature [4,5,6,7,8,9,10,11,12,13,14]. Simultaneous occurrence of SMA and IMA fistula is the rarest of the rare in the literature, especially treated with an endovascular approach. None of the reviewed articles in this study described the co-occurrence of SMA and IMA AVFs.

Trauma or intestinal surgery may have occurred recently or in the distant past, spanning between hours to decades [15,16,17,18,19,20,21]. The clinical presentation of SMA and IMA AVF is atypical and depends on the size and location of the fistula, from asymptomatic to abdominal pain with or without diarrhea, portal hypertension, liver impairment, and even gastrointestinal bleeding [22], causing secondary severe portal hypertension [23].

Multidetector computed tomographic (MDCT) and conventional angiography have developed as an important imaging tool in assessing the mesenteric vasculature. Endovascular therapy techniques are gaining popularity, providing a safer, more efficient approach. There have been some rare case reports of effective endovascular therapy. We were fortunate to see a successful instance of transarterial embolization of iatrogenic SMA and IMA AVF. There are no large case series or controlled trials that can be used to support this therapy method. In order to make any conclusions about this therapy, we did a systematic literature review to investigate published accounts of similarly treated cases.

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Case 1

A 46-year-old male presented with multiple episodes of bleeding and the passage of clots per rectum for a day. The patient has been a known case of EHPVO (Extrahepatic portal venous obstruction) since childhood and had a surgical history of splenectomy 20 years back. On admission, his BP was 90/60 mmHg and his pulse rate was 92 beats/min. Examination of the abdomen revealed generalized tenderness with no evidence of mass per abdomen, shifting dullness, or bruit. Anemia was discovered in the laboratory. An upper gastrointestinal endoscopy revealed minor esophageal and fundal varices with no current bleeding. Colonoscopy was inconclusive due to poor visual field secondary to bleeding. Sclerotherapy was done for the rectal varices (Fig. 1).

Fig. 1.
figure 1

46-year-old male, s/p Splenectomy, presented with melena, on CECT, and conventional angiography showing multiple superior and inferior mesenteric arteriovenous malformations. A: showing AVF between SMA & SMV, B, C, D, E, F: showing AVF between IMA & IMV (Red arrow: Artery, Blue arrow: vein, Black arrow: Fistulous arteriovenous malformation)

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MDCT was performed to determine the extent of the thrombus and the site of active bleeding. MDCT demonstrated diffuse hepatic atrophy with compensatory caudate lobe hypertrophy, thrombosis of the intrahepatic portal vein extending into the retro pancreatic splenic vein, and portosplenic confluence with dilatation of the intrahepatic biliary radicles. There are numerous tortuous gastric, mesenteric, colonic, and jejunal varices, with thrombosis within a few of them. The MDCT also detected a superior mesenteric artery aneurysm that drains into the superior mesenteric vein via a convoluted fistulous tract. Fistulous connections between inferior mesenteric artery branches and inferior mesenteric vein tributaries, as well as aneurysmal dilatations near the fistulous tract's origin, were seen in the arterial phase. Dilated feeding arteries and heavily opacified early draining ectatic veins were also visible. Other CT findings were mild to severe ascites, a complicated kidney cyst, and a small pleural effusion on the left side. These findings were consistent with those predicted for an arteriovenous fistula caused by SMA or IMA.

Treatment options were explained to the patient along with the high risk of an open surgical invasion because of secondary adhesions and the possibility of massive bleeding from numerous collateral arcades. Hence, the patient was taken for conventional angiography and transarterialglue embolization of AVF. Through the right femoral artery, a celiac, SMA, and IMA angiogram was performed, revealing a normal celiac axis with multiple fistulous malformations of SMA and IMA as focal areas of abnormal blush with multiple collateral arcade formations. Angiogram confirmed the previously reported contrast-enhanced CT findings. Multiple fistulous communications between the distal SMA and SMV, IMA and IMV were confirmed with contrast opacifications of the dilated SMV and IMV documented during the early arterial phase. Using a catheter wire system, the feeding vessels of culprit arcades were selectively cannulated and embolized with 30% glue (n-butyl-2-cyanoacrylate-lipiodol combination). The AV fistulas of SMA and IMA were embolized serially under DSA (Digital Subtraction Angiography) guidance. A postembolization angiogram revealed the cessation of opacifications of the aneurysmal malformations and AVF tract.

The patient was strictly monitored for immediate post-embolization syndrome and signs of bowel ischemia. Post-procedure CT showed complete occlusion of the aneurismal dilatation and fistulous tracts of SMA and IMA. The tortuous varicosities of the prior studies were not visualized in the post-procedure study (Fig. 2).

Fig. 2
figure 2

Post-transcatheter Glue embolization of the secondary SMA & IMA AVF in coronal CECT and DSA images (white arrow)

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Data acquisition and methodology

A systematic analysis of the literature was conducted in order to identify all documented examples of endovascular repair of mesenteric AVFs, which are described as abnormal connections between the superior and inferior mesenteric arteries and veins. The authors conducted an exhaustive Web-based review using the terms "Endovascular with inferior mesenteric fistula, superior mesenteric fistula." The recovered literature's references and related articles were also scoped. Articles written in languages other than English have been translated. The online search included all relevant peer-reviewed journal articles published up to September 2019 in the following databases: Elsevier, Wiley online, Springer Link, PubMed, Researchgate, Science Direct, and Google Scholar. The search yielded 40 articles describing 40 individuals with mesenteric AVFs who were treated with various endovascular techniques. In addition to our example, a total of 41 individuals were included in the study (Table 1). The inclusion criteria were case report publications that used a unique endovascular procedure as the primary therapy. Book chapters and systematic reviews, as well as four papers reporting on a hybrid strategy, were excluded from our review (combining endovascular and surgical). Technical success (fistula obliteration with or without problems and without the necessity for open surgical conversion), perioperative, and 90-day mortality were the primary end measures. Procedure-related problems, which are classified as minor and require surveillance or reintervention, as well as the operator's retrospective personal overall improvement, the following therapy was prescribed: The secondary outcome measures were strongly in favor, in favor but with caution, awaiting further recommendations before suggesting the procedure, and no or negative advice. Finally, a comparative subanalysis was conducted to evaluate mortality and complication rates between patients getting elective therapy (defined as a procedure that is scheduled) and patients who require urgent therapy (defined as patients requiring urgent intervention due to a critical state or hemodynamic instability).

Table 1 Published case reports of Superior and Inferior mesenteric AVMs treated with an endovascular approach
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Results of data analysis

The average age of the cases examined was 50 years (age range 16–84). There were 31 males (59%) and 10 females (41%) among the 41 patients. The superior mesenteric segment was the site of the fistula in 80.4% of patients (33 of 41), the inferior mesenteric segment in 12.1% (5 of 41), and the superior and inferior mesenteric segments in 2.4% of patients (1 of 41). In 7.3% (3 of 41) of patients who had successful treatments, complications occurred. None of the patients had major problems. The symptomatic strategy was beneficial in managing those problems. All minor issues were handled with caution. In reflection, the authors were mainly in favor of endovascular treatment. The therapy modality received strong support from 41 authors, including us. Five writers were enthusiastic, but cautioned that the therapy should be used with caution and in conjunction with a multidisciplinary approach.

Interpretation and discussion

Splanchnic AVFs can be found in a variety of places. The celiac artery or its branches, particularly the hepatic (45%) and splenic (30%) arteries, are responsible for the majority of cases. In decreasing order of frequency, the superior mesenteric, gastroduodenal, and inferior mesenteric arteries are involved [1, 16, 19]. AVF involving the superior and inferior mesenteric vessels is uncommon in only about 41 cases collectively in the literature [3,4,5,6,7,8,9,10,11,12,13,14]. SMA and IMA AVFs are abnormal communication between the SMA, SMV, and IMA, IMV, respectively. SMAVFs are most commonly caused by a traumatic event, such as a surgical colon resection. The hemodynamics of the AVF is most likely to blame for the substantial difference in the time it takes for mesenteric AVFs to manifest clinically. A large and rapid flow of blood from the arterial to the venous circulation characterizes high-flow fistulas [14]. According to one study, the duration between surgery and the beginning of clinical SMAVF can be as long as 25 years [24]. Our patient had a history of splenectomy 20 years ago.

The intestine's arteriovenous fistula is a rare cause of gastrointestinal hemorrhage. Gastrointestinal bleeding can occur from a variety of sources. The origins of bleeding in Pietri et al.’s [19] series included esophageal or cardiac varices due to portal hypertension, massive hematochezia due to cecal AVF rupture, hemobilia due to hepatic biopsy, and bloody diarrhea due to colonic ischemia. The most common sign of mesenteric AVFs is increasing stomach pain, which may be accompanied by malabsorption symptoms [25]. Untreated fistulas, despite the usual delayed and inconspicuous clinical manifestation of SMA and IMA AVF, can have fatal consequences, with a reported mortality rate of up to 25% [26]. Certain instances of mesenteric AVFs are asymptomatic for a long time before presenting with symptoms. PHTN (Portal hypertension) develops over time when blood is shunted from the arterial to the venous systems, resulting in refractory ascites and severe GI bleeding [25].

Abdominal ultrasound scanning, CT, or MRI are usually the first to reveal vascular deformity [23]. MDCT angiography has recently gained popularity as a method for assessing the mesenteric vasculature. Because of its superior spatial resolution and faster acquisition periods, it allows for the imaging of normal vascular anatomy and gives reliable diagnostic information, allowing assessment of the peripheral visceral branches [27,28,29]. The gold standard for determining the precise anatomic site and amount of mesenteric vascular involvement is DSA. However, this operation is usually reserved mainly for treatment purposes.

SMAVF surgical ligation is a well-known therapeutic option. However, due to problematic bowel mobilization and adhesions from previous abdominal surgery, the operation can be technically tough. Surgical procedures have a 18% fatality risk [27]. Percutaneous endovascular embolization of the feeding artery is becoming more popular as an option to surgery [17, 19, 21]. It's less invasive, and it's becoming more popular for occluding mesenteric AVFs [30]. Occlusion of AVFs has been accomplished with metal coils, stent-grafts, amplatzer vascular plugs, Onyx, and detachable coils with N-butyl-2-cyanoacrylate glue [31]. Recently, percutaneous endovascular treatment of such AVFs has been increasingly performed, using covered stents or embolization [30, 32, 33]. Metallic coil embolization could be problematic when the fistula's flow rate is high and its diameter is greater than 8 mm because of the likelihood of migration into the portal venous system [34]. Embolization may be challenging in situations with congenital or multiple iatrogenic AVFs, as it is only effective if all active and quiescent shunts are closed.

Conclusions

Finally, we provide a case of upper GI bleed caused by several superior and inferior mesenteric AVFs, which was easily and consistently visualized by MDCT and validated by traditional angiography. In the case of suspected mesenteric arteriovenous malformations, we recommend MDCT angiography as the primary study. For the evaluation of possible interventions, conventional angiography can be used. AVF can be misdiagnosed because the patients' unique clinical symptoms are typically nonspecific, and physical examination may not indicate the existence of abdominal bruit. A differential of arteriovenous malformations should be evaluated in the presence of secondary indications of portal hypertension and a history of abdominal surgery. Endovascular embolization can be safely performed with outstanding results. Endovascular glue embolization (n-butyl-2cyanoacrylate and lipiodol combination) can be the choice of endovascular intervention in high flow arterio-venous malformation and in patients with multiple co-morbidities or high risk patients. It is also an economical option, thus making it the treatment of choice even for patients of lower economic strata and in low socio-economic countries as well.