Left inferior phrenic arterial malformation mimicking gastric varices: A case report and review of literature

Abstract

BACKGROUND

Gastric submucosal arterial dilation resulting from splenic artery occlusion represents an exceedingly rare etiology of acute upper gastrointestinal bleeding (UGIB). Although endoscopy is a widely utilized diagnostic and therapeutic modality for gastrointestinal bleeding, it has limitations in detecting arterial abnormalities.

CASE SUMMARY

This report presents a rare case of massive UGIB in a 57-year-old male with a tortuous left inferior phrenic artery accompanied by splenic artery occlusion. “Gastric varices” was identified during the patient's endoscopy one year before hemorrhage. Despite initial hemostasis by endoscopic clipping, the patient experienced massive rebleeding after one month, requiring intervention with transcatheter arterial embolization (TAE) to achieve hemostasis.

CONCLUSION

This is the first case to report UGIB due to a tortuous left inferior phrenic artery. This case highlights the limitations of endoscopy in identifying arterial abnormalities and emphasizes the potential of TAE as a viable alternative for the management of arterial bleeding in the gastrointestinal tract.

Key Words: Upper gastrointestinal bleeding; Left inferior phrenic artery; Splenic artery occlusion; Gastrointestinal endoscopy; Digital subtraction angiography; Case report

Core Tip: Endoscopy has become a widely used diagnostic and therapeutic tool for gastrointestinal bleeding, effectively screening for gastric varices and achieving hemostasis. However, arteries can mimic varices, and their ruptures require multidisciplinary discussion and alternative therapeutic options. Gastric submucosal arterial dilation due to splenic artery occlusion constitutes an exceptionally rare cause of acute upper gastrointestinal bleeding (UGIB). This is the first documented instance of UGIB originating from the left inferior phrenic artery. The study provides valuable insights into the clinical diagnosis and management of this rare and challenging condition.

INTRODUCTION

Acute upper gastrointestinal bleeding (UGIB) is a severe medical emergency with significant global incidence and in-hospital mortality rates[1]. UGIB can be categorized into variceal UGIB and non-variceal UGIB (NVUGIB)[2], with the former frequently observed in patients with liver cirrhosis or portal hypertension[3]. The incidence of NVUGIB is substantially higher than that of variceal UGIB, and it is associated with a mortality rate of 1%-5%[4]. Erosive gastritis, esophagitis, peptic ulcers, Dieulafoy lesions, neoplasms, and angiodysplasia are the leading causes of NVUGIB[5,6]. Vascular abnormalities are critical pathophysiologies of NVUGIB and can cause severe hemorrhage in cases of arterial lesions[4]. The absence of the splenic artery as an etiology for NVUGIB is rare. Here, we present a rare case of NVUGIB caused by a tortuous left inferior phrenic artery running through the gastric wall due to splenic artery occlusion. Our discussion of this case, its diagnosis, and treatment aims to provide informative insights into the management of such hemorrhages.

CASE PRESENTATION

Chief complaints

A 57-year-old man presented to black stools, dizziness, epigastric discomfort, hypodynamia, and anorexia in the emergency room of our hospital.

History of present illness

The patient had black stools 5-6 times a day for three days. He experienced a brief loss of consciousness in the emergency room. Upon feeling faint, he had a heart rate of 59 bpm and an oxygen saturation of 99%. His blood pressure (BP) was 8.4/5.6 kPa.

History of past illness

The patient denied any history of liver cirrhosis or the use of anticoagulant drugs or anti-inflammatory drugs. “Gastric varices” were identified during the patient's endoscopy one year prior (Supplementary Figure 1).

Personal and family history

The patient denied personal and family history.

Physical examination

The patient appeared anemic but not jaundiced and had a soft abdomen with no tenderness or rebound tenderness. The liver and spleen were impalpable, and no edema was observed in the patient's lower limbs.

Laboratory examinations

The laboratory findings upon admission revealed a white blood cell count of 6.32 × 10⁹/L, a hemoglobin level of 121.0 g/L, and a platelet count of 204.0 × 10⁹/L. The liver function test results revealed alanine aminotransferase 41 U/L, aspartate aminotransferase 40 U/L, gamma-glutamyl transpeptidase 72 U/L, total protein 61.5 g/L, albumin 38.1 g/L, total bilirubin 33.8 µmol/L, direct bilirubin 13.6 µmol/L, and indirect bilirubin 20.2 µmol/L. The patient had normal coagulation function and tested negative for hepatitis B and C viral markers.

Imaging examinations

Abdominal ultrasound indicated that the liver was fatty but that there were no apparent abnormalities in the portal vein. Upon admission to the hospital, the patient experienced an acute episode of massive hematemesis, followed by dark red bloody stools, resulting in a decreased hemoglobin level of 81.0 g/L and a BP of 66/35 mmHg. Emergency upper gastrointestinal endoscopy (GIE) revealed the presence of a bleeding vessel with ulcerative lesions in the fundus (Figure 1 and Video), massive blood clots, and a visible thrombus. Endoscopic clipping effectively achieved hemostasis.

Figure 1 Emergency endoscopy findings during haematemesis. A: Active bleeding and blood clots in the fundus and body of the stomach; B and C: A giant thrombus head in the stomach dome by reversing the patient’s position and several varice-like vessels around the thrombus; D: The base of the thrombus clipped using four metal clips.

Further hospital course

Nonetheless, one month later, the patient experienced rebleeding of similar severity as the initial episode. Transcatheter arterial embolization (TAE) was utilized to achieve hemostasis, and digital subtraction angiography revealed occlusion of the splenic artery. The spleen was supplied by the tortuous left inferior phrenic artery and dorsal pancreatic artery, which originated from the celiac trunk (Figure 2). The left inferior phrenic artery was observed to bifurcate, with one branch supplying the left diaphragmatic muscle and the other running close to the gastric wall before entering the spleen, which was clamped by clips. Coil embolization led to the disappearance of the tortuous variant artery, and bleeding ceased. Computed tomography (CT) venography revealed occlusion of the splenic artery (Figure 3A-C). Further spiral CT 3D image reconstruction revealed that collateral circulation was established through two variant arteries stemming from the celiac trunk to supply the spleen (Figure 3D-F). One of these arteries travels in front of the pancreas, whereas the other divides into two branches with one passing through the stomach wall and into the spleen.

Figure 2 Abdominal angiography findings. A: Two arteries from the celiac trunk supplying the spleen; B: The bleeding artery is one branch (indicated by green arrows) from the left inferior phrenic. Another branch (indicated by blue arrow) supplies the left diaphragmatic muscle; C: After transcatheter embolization with metallic coils (yellow arrow); D: Selective arteriography showed that the remaining dorsal pancreatic artery still supplies the spleen (yellow arrow).

Figure 3 Portal vein computed tomography venography images. A: Tortuous vessels supplying the spleen observed in the coronal view; B: The splenic artery occlusion indicated by yellow arrows; C: A tortuous artery running through the gastric wall indicated by green arrow; D: A three-dimensional computed tomography image shows the absence of the splenic artery; E and F: The tortuous artery running through the gastric wall (indicated by green arrows), which along with the enlarged dorsal pancreatic artery (indicated by blue arrows), supplies the spleen. The image shows the placement of clips on the gastric wall.

FINAL DIAGNOSIS

NVUGIB due to a tortuous left inferior phrenic artery accompanied by splenic artery occlusion.

TREATMENT

TAE was utilized to achieve hemostasis. Coil embolization led to the disappearance of the tortuous variant artery, and bleeding ceased.

OUTCOME AND FOLLOW-UP

Regular follow-up examinations revealed no further instances of bleeding in the patient. After nine months, the patient underwent an upper GIE evaluation, showing an absence of tortuous vessels or noteworthy abnormalities in the gastric wall. CT angiography (CTA) (Supplementary Figure 2) did not detect the emergence of novel compensatory arteries that supply the spleen. Medical timeline of the patient is shown in Figure 4.

Figure 4 Medical timeline of the patient with acute upper gastrointestinal bleeding. GIE: Gastrointestinal endoscopy; CTV: Computed tomography venography; DSA: Digital subtraction angiography; TAE: Transcatheter arterial embolization.

DISCUSSION

UGIB is a common and potentially fatal condition. Endoscopic hemostasis remains the mainstay of therapy for achieving hemostasis and preventing rebleeding[7]. Although the incidence and mortality of NVUGIB have decreased in the past two decades due to effective prevention and management, it remains a significant clinical problem[4,8]. Gastroduodenal peptic ulcers remain the most common cause of NVUGIB, and angiodysplasia has become an increasingly recognized cause[5,9]. Vascular lesions in arteries are more likely to cause severe bleeding because of the strong pulsation of the vessel. Dieulafoy syndrome is an example of an arterial abnormality in which the artery penetrates the submucosa, runs a tortuous course, and protrudes into the submucosa[10]. Once the overlying epithelium is damaged, the artery is exposed to the gastrointestinal lumen, resulting in massive hemorrhage.

UGIB caused by congenital absence of the splenic artery or splenic artery occlusion is a rare clinical condition. We have summarized previously reported cases in Table 1, including their symptoms and GIE findings. Most cases (6 of 10 cases) involved the left gastric artery as a compensatory artery due to the absence or occlusion of the splenic artery[11-14], whereas 1 case reported a cluster of arterial vessels branching from the occluded splenic artery[15]. The left gastric artery is a significant supplier of blood to the gastroesophageal junction and is commonly employed as a compensatory artery in the absence of the splenic artery. In the present case, the patient was initially misdiagnosed with gastric varices on the basis of previous endoscopic findings. However, further investigation revealed that the patient had no history of chronic liver disease and was instead suffering from NVUGIB due to an abnormality in the left inferior phrenic artery. This condition is exceptionally rare because the tortuous artery, which runs through the gastric wall, is a branch of the left inferior phrenic artery that normally supplies the spleen. Previous studies reported only two cases of UGIB originating from the left inferior phrenic artery, one caused by iatrogenic reasons[16] and one caused by cirrhosis[17]. Our case is the first to report that the left inferior phrenic artery supplies the spleen rather than the left gastric artery, as observed in previous cases. Furthermore, in this case, the dorsal pancreatic artery was enlarged and supplied the spleen, whereas the gastric artery remained normal.

Table 1 Summary of reports about acute upper gastrointestinal bleeding due to the absence of splenic artery.

Age/sex	Symptoms	GIE findings	Bleeding vessel	Splenic artery	Treatment	Rebleeding	Ref.
13/M	Hematemesis	-	Left gastric artery	Congenital SA absence	Ligation + Splenectomy	No	Durrans et al[22]
31/M	Hematemesis	Erosive gastritis and duodenitis with hemorrhagic gastritis	Left gastric artery or short gastric arteries	Congenital SA absence	Vagotomy + pyloroplasty + Splenectomy	Yes (Achieved hemostasis by partial gastrectomy)	Spriggs[19]
50/F	Dizziness and tarry stools	A bleeding vessel in the gastric mucosa	Variant left gastric artery	The absence of the SA	Endoscopic clipping	Yes (Achieved hemostasis by TAE)	Namikawa et al[11]
60/M	Hematemesis	Varicose-shaped submucosal vessels with a small erosion	Arterial cluster arising from the left gastric artery and left gastroepiploic artery	Complete SA thrombosis	Endoscopic clipping followed by TAE	No	Martino et al[12]
52/M	Hematemesis and cold sweats	Large amount of clotted blood	-	SA occlusion	-	Death	Arslan et al[30]
69/M	Recurrent UGIB	A varicose shaped submucosal vessel located at the funds of the stomach	Left gastric artery	Idiopathic SA thrombosis	Splenectomy + dissection of the arteries	No	von Trotha et al[13]
36/M	Dizziness and melena	3-mm polypoid lesion in the gastric body of the stomach on the lesser curve	-	SA occlusion	Splenectomy + partial gastric devascularization	No	Baron et al[20]
66/M	Melena and fatigue	A submucosal lesion consistent with a vascular malformation in the fundus of the stomach	A cluster of arterial vessels branching from the occluded splenic artery	SA occlusion	TAE	No	Mnatzakanian et al[15]
49/M	Massive hematemesis	Prominent submucosal variceal-like structure	Enlarged left gastric artery	Chronic occlusion of the mid-SA	TAE	Yes (Achieved hemostasis by Splenectomy + ligation of the artery)	Al-Balas et al[14]
68/F	Black stools	A tortuous, submucosal mass with an overlying red spot	Collateral vessels arose from the proximal splenic artery	Aneurysmectomy	Ligation + Splenectomy	No	Worthley et al[21]
57/M	Black stools and dizziness	A bleeding vessel with ulcerative lesions in the fundus	Left inferior phrenic artery	The absence of the SA	Endoscopic clipping + ECGI	Yes (Achieved hemostasis by TAE)	Our case

TAE: Transcatheter arterial embolization; ECGI: Endoscopic cyanoacrylate glue injection; SA: Splenic artery; M: Male; F: Female; UGIB: Upper gastrointestinal bleeding; GIE: Gastrointestinal endoscopy.

The etiologies of splenic artery absence vary and include congenital absence of the splenic artery[18], atherosclerosis[19], thrombosis[13], trauma[20], and surgical intervention[21]. Analysis of the patient characteristics in the table reveals a greater prevalence of older male patients, likely due to atherosclerosis- or thrombosis-induced splenic artery occlusion. Conversely, UGIB due to congenital absence of the splenic artery seems to occur at a younger age[19,22], highlighting the need for careful consideration in patients presenting with sudden hematemesis without a history of portal hypertension, gastroesophageal tumors, or gastric ulcers. In such cases, compensatory artery bleeding due to an absent splenic artery should be considered, especially in older patients with atherosclerosis or thrombosis. The patient presented in this case had no history of trauma or surgical intervention, and laboratory results indicated no evidence of atherosclerosis or thrombosis. The absence of the splenic artery in this patient was likely congenital, and the cause of the bleeding was presumed to be vascular lesions resulting from excessive drinking.

In recent decades, there have been significant advancements in the management of NVUGIB[23,24]. However, the management of this condition has become increasingly challenging because of its complex etiology and comorbidities[25]. Endoscopic treatment is considered an essential advance in the control of NVUGIB[26,27], but more careful consideration is needed when a patient has an absent splenic artery. In this case, endoscopic clipping and cyanoacrylate glue injection were attempted for hemostasis for the first time; however, the patient experienced rebleeding within one month. Ultimately, TAE was performed and successfully stopped rebleeding. Similarly, Namikawa et al[11] reported a patient with NVUGIB who underwent endoscopic clipping but subsequently experienced rebleeding. TAE was also successful in preventing rebleeding in that case. Two other studies reported that TAE was performed and achieved successful hemostasis with no rebleeding[12,15]. However, one patient experienced hemorrhage after TAE and required splenectomy and artery ligation[14]. Compared with endoscopic hemostasis, TAE appears to be a more practical option for achieving hemostasis and avoiding rebleeding in these patients. Surgical hemostasis and splenectomy may be necessary for patients who do not respond to interventional treatment. Notably, direct injection of cyanoacrylate glue into arteries carries a significant risk of systemic embolization and life-threatening adverse events[28,29]. Therefore, obtaining a definite diagnosis for NVUGIB patients before cyanoacrylate glue injection is crucial. When this option is used, it should be considered only as a last resort[30].

CONCLUSION

Endoscopists should pay attention to patients with massive hematemesis who do not have a history of portal hypertension, gastroesophageal tumors, or gastric ulcers. The absence of splenic artery-induced hemorrhage could be one cause of sudden UGIB in a patient. To obtain clinical clues, CTA is suggested for patients in stable condition. For patients with a confirmed diagnosis of splenic artery occlusion, TAE or splenectomy is recommended. After TAE, regular follow-up of the patient is necessary, particularly if splenectomy is not performed. A CTA follow-up is suggested to screen for new compensatory arteries in the future. In cases where the etiology of UGIB is uncertain, caution should be exercised when cyanoacrylate glue injection is used because of the potential for the artery to mimic gastric varices.

ACKNOWLEDGEMENTS

We thank the patient for his willingness for publication of this case report.