Left-Sided Portal Hypertension Induced by Splenic Arteriovenous Malformation: A Case Report

Introduction

Left-sided portal hypertension (LSPH), also known as splenic venous hypertension, is a rare condition that results from elevated splenic venous pressure. LSPH can cause gastric varices, which often present as gastrointestinal hemorrhage. Unlike conventional portal hypertension, LSPH does not tend to be associated with abnormalities of hepatic function or esophageal varices. The main causes of LSPH include splenic vein compression by benign tumors, adenocarcinoma, or neurofibroma; primary stenosis of the splenic vein; secondary stenosis of the splenic vein caused by pancreatitis; splenic vein thrombosis or embolism; and Whipple’s surgery impacting the splenic vein [1]. However, reports of LSPH arising from vascular malformations are scarce in the literature. In this case report, we describe our experience with a patient with LSPH caused by a splenic vein malformation.

Case Report

A 53-year-old man reported having melena for 2 weeks. He had a history of hypertension for more than 10 years, with poor blood pressure control. He had a history of neurofibroma between the second and third lumbar vertebrae, which was surgically removed 2 months prior to the current presentation. The tumor did not impair abdominal venous return and the surgical approach was not trans-abdominal. He denied any history of pancreatitis, abdominal trauma, and other related surgeries. Gastroscopy performed at another hospital revealed gastric varices (Figure 1), in which patchy erosion with fresh red blood traces was observed on the varicose veins near the cardia. Abdominal contrast-enhanced CT showed gastric fundal varices and splenic vascular malformation (Figure 2). The patient was admitted to our hospital for further examination and all vital signs were stable on admission. Physical examination revealed that the liver and spleen were not palpable under the ribs, and the abdomen was flat and soft without obvious pressure or rebound pain. No signs of cirrhosis, such as jaundice, spider angioma, and abdominal wall varicose veins, were observed. Preoperative laboratory tests revealed that hemoglobin was slightly low (117 g/L) due to digestive tract bleeding and the remaining complete blood count (CBC) parameters were within normal limits, such as the platelet count (166×109/L) and white blood cell count (3.7×109/L). High-density lipoprotein cholesterol was also low (0.78 mmol/L), and liver function test results (aspartate transaminase, alanine transaminase) were normal. Albumin (45.8 g/L), which is suggestive of chronic liver disease, was also within the normal range. Relevant hepatitis antibody and autoimmune liver disease antibody were normal. After ruling out these possible liver diseases, fibrosis marker tests were not performed. Imaging of the portal vein by contrast-enhanced CT revealed portal hypertension, a tortuous vascular cluster between the splenic artery and vein (a mixed pattern of hypodense and hyperdense areas), marked dilatation of the left gastric vein, and numerous collateral vascular branches surrounding the perigastric area and splenomegaly, with no signs of cirrhosis and gastro-renal shunt or splenic-renal shunt (Figure 3). Contrast-enhanced MRI confirmed portal hypertension, esophageal and gastric varices, splenic varices, splenomegaly, and the absence of cirrhosis (Figure 4).

Based on the examination findings, we suspected he had LSPH caused by splenic arteriovenous malformation. To improve the melena, we performed splenectomy and Hassab’s operation. The main procedural steps were the following. We first dissected the gastro-splenic ligament, then transected and ligated the left gastroepiploic vessels along with all short gastric arteries and veins. The splenic artery was isolated and ligated, followed by division of the surrounding ligaments. After allowing the spleen to fully decompress, it became significantly smaller and softer. The splenic artery and vein were then suture-ligated. The tortuous vascular structures and the spleen were mobilized, then the specimen was removed. The posterior gastric vein was dissected, along with the cardia, gastric fundus, and the lower esophagus (approximately 7 cm above the cardia). The surrounding variceal veins were transected and ligated. Intraoperative exploration showed a normal liver with no obvious cirrhosis, and a normal but slightly enlarged spleen with obvious dilatation of the gastric coronary vein and splenic vein, as well as visible tortuous vessels around the splenic vein (Figure 5). Postoperative histopathological examination revealed thickening and degeneration of the splenic venous vascular wall with calcification and atheromatous plaque formation. Splenomegaly and chronic congestion of the spleen were also noted. Elastic fiber staining showed irregular thickening of the tunica intima of the splenic vein, interrupted and disrupted elastic fiber layers, and both fractured and intact elastic layers in the splenic arterial wall. A sample of the lesion was immunoglobulin G4 negative eliminating the possibility of IgG4-related vasculitis (Figure 6). Based on the pathology results, there are clear discontinuities in the elastic layer of the intima of the vessel wall, indicating high-flow vascular malformations and we definitively diagnosed arteriovenous malformation.

Postoperatively, he recovered well and did not experience any symptoms, including gastrointestinal bleeding. Hydroxyurea was given to reduce platelets after splenectomy.

Discussion

LSPH is a relatively rare disease that can manifest with upper gastrointestinal hemorrhage and is often caused by stenosis, compression, or embolism of the splenic vein, with splenic vein embolism being the most common etiology. We report a rare case of LSPH caused by a high-flow vascular malformation. To the best of our knowledge, there has been only 1 has previously reported case of LSPH secondary to splenic arteriovenous fistula, which was caused by chronic pancreatitis [2].

Simple vascular malformations can be categorized into low-flow and high-flow types based on their hemodynamic characteristics. The low-flow type includes capillary malformations, common venous malformations, and common lymphatic malformations. High-flow types include arteriovenous malformations and arteriovenous fistulas. Arteriovenous malformations result from the direct connection of malformed arteries and veins or the presence of abnormal primitive vascular connections between veins and arteries. Arteriovenous malformations are often present with dissection of the tunica intima and arterialized thick-walled veins [3,4]. Arteriovenous malformations result in elevated venous pressure, vasodilatation, and other changes due to the lack of normal capillary structure and direct influx of arterial blood into the veins. Our patient probably had a congenital splenic arteriovenous malformation, as well as poor control of long-term hypertension, which led to the direct effect of high-dynamic blood flow on the venous wall, causing dilatation of the venous wall, arterialization, and elevated splenic venous pressure. These occurred secondary to other changes, including gastric fundal varices and splenic venous varicose veins (gastric varices).

One study [5] showed that elastic fiber staining helps to differentiate between high-flow and low-flow vascular malformations, despite the lack of preoperative imaging of typical arteriovenous malformations. Therefore, we used elastic fiber staining to definitively identify the high-flow vascular malformation causing high LSPH based on the presence of fractures in the intimal–medial elastic layer. This conclusion was reached after excluding thromboembolism and vascular stenosis of the splenic vein.

Our patient exhibited massive peri-splenic tortuous vascularization and gastric fundal varices, indicating a long-term disease course. To solve this problem, we considered direct embolization of the perispherical tortuous vessels and gastric varices, or splenectomy combined with ligation of gastroesophageal varices. However, the embolization approach was ultimately abandoned for 2 primary reasons. First, the numerous and anatomically complex tortuous vessels around the spleen posed a high risk of incomplete embolization, which could potentially lead to postoperative recurrence. Second, directly embolizing the splenic artery to reduce blood flow to these perispherical vessels carried a significant risk of postoperative splenic infarction, which could lead to complications such as splenic abscess and ultimately result in a poorer prognosis. To address the perigastric varices, we considered balloon-occluded retrograde transvenous obliteration (BRTO). However, contrast-enhanced CT of the portal venous system failed to identify a gastro-renal shunt. Consequently, this interventional approach was also deemed not feasible for managing the perigastric variceal veins. Finally, we performed splenectomy and Hassab’s operation. If detected early and appropriately managed, the patient may not have progressed to LSPH and endured the immense trauma of surgery. Early detection could potentially prevent the development of gastroesophageal varices. Therapeutic efforts would therefore be directed solely toward the primary lesion (splenic arteriovenous malformation), which would reduce the extent of surgical intervention required. Furthermore, if arteriovenous malformation is identified at an early stage, which tends to worsen over time due to increased flow and collateral vessel formation, the tortuosity and proliferation of blood vessels may not be as complex, potentially allowing for treatment via splenic vein embolization instead of open surgery. Therefore, the importance of early detection and differentiation of vascular malformations should be emphasized. Angiography has traditionally been the gold standard diagnostic method for vascular malformation; however, it is invasive and may not be the first choice for early identification. As alternatives, ultrasound is commonly used to detect superficial vascular malformations, and MRI is commonly used to identify intracranial vascular malformations. One study suggested that dynamic contrast-enhanced MRI measurements of contrast rise time are useful to differentiate between high-flow and low-flow malformations [6]. In our case, the enhanced MRI showed low-signal changes in the peri-splenic vascular malformations on T2-weighted and diffusion-weighted imaging. This finding is largely consistent with another report indicating that high-flow lesions often exhibit flow void phenomena due to rapid blood flow, manifesting as low or signal-void areas on T2-weighted images (similar to the dark shadows characteristic of vascular flow voids). However, the author of that article also noted that the sensitivity and specificity of these signs remained suboptimal, necessitating further combination with dynamic enhancement parameters (such as slope) to improve diagnostic accuracy [7]. Unfortunately, in this case, DCE-MRA (dynamic contrast-enhanced magnetic resonance angiography) was not performed, so corresponding images could not be provided for further analysis. A recent review also indicated that magnetic resonance techniques, such as dynamic contrast-enhanced MRI, arterial spin labeling MRI, and four-dimensional flow magnetic resonance angiography, provide valuable additional information to improve the detection of vascular malformations [8]. Therefore, MRI seems to be a useful tool for the early detection and identification of visceral vascular malformations. However, use of CT for identification of vascular malformations has rarely been reported. Interestingly, in the present case, the presence of early enhancement of the periportal splenic vein in the arterial phase of contrast-enhanced CT (Figure 2A) was consistent with the rapid movement of arterial blood into the vein due to the lack of capillaries in arteriovenous malformations, but its accuracy needs further study.

Conclusions

We report a rare case of LSPH caused by an arteriovenous malformation. This case suggests the importance of early differentiation of vascular malformations and non-invasive vascular imaging in patients suspected of having LSPH.