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Abstract

The mortality rate of gastric varices bleeding can reach 20% within 6 weeks. Isolated gastric varices (IGVs) refer to gastric varices without esophageal varices and typically arise as a common complication of left portal hypertension. Although IGVs commonly form in the setting of splenic vein occlusion, the combination of antiphospholipid syndrome and protein S deficiency leading to splenic vein occlusion is rare. We herein present a case of a 28-year-old woman with intermittent epigastric pain and melena. She was diagnosed with antiphospholipid syndrome based on the triad of pregnancy morbidity, unexplained venous occlusion, and positive lupus anticoagulant. Laparoscopic splenectomy and pericardial devascularization were performed for the treatment of IGVs. During the 6-month postoperative follow-up, repeated endoscopy and contrast-enhanced computed tomography revealed disappearance of the IGVs. This is the first description of splenic vein occlusion associated with both antiphospholipid syndrome and protein S deficiency. We also provide a review of the etiology, clinical manifestations, diagnosis, and treatment methods of IGVs.

Keywords

Isolated gastric varices hemorrhage left-sided portal hypertension antiphospholipid syndrome protein S deficiency splenic vein occlusion case report

Introduction

Isolated gastric varices (IGVs) refer to gastric varices without esophageal varices. IGVs occur less frequently than esophageal varices¹ and are associated with higher morbidity and mortality rates. Portal hypertension associated with liver cirrhosis is the most common etiology of both gastroesophageal varices and IGVs. However, the presence of IGVs in noncirrhotic patients is thought to be highly suggestive of regional portal hypertension, also known as left-sided portal hypertension (LSPH). Clinical manifestations of IGVs are extremely heterogeneous and vary from severe forms of acute variceal bleeding to the complete absence of symptoms. IGVs caused by LSPH should be considered as a differential diagnosis for patients presenting with upper gastrointestinal bleeding, especially those with no background of cirrhosis. Endoscopy, endoscopic ultrasonography, and contrast-enhanced computed tomography (CECT) are helpful in diagnosing these disorders. IGVs secondary to splenic vein occlusion should be individually managed on the basis of any underlying diseases. Endoscopic treatment, radiologic treatment, and surgical approaches are available to control bleeding. In the present report, we describe the first known case of IGVs secondary to splenic vein occlusion associated with both antiphospholipid syndrome (APS) and protein S deficiency. We except that this report will provide a reference for the clinical diagnosis and treatment of similar conditions.

Case presentation

On 19 April 2022, a 28-year-old woman was admitted to our hospital from the outpatient department with a 4-year history of intermittent epigastric pain and melena. She had received no special treatment for the pain or melena. Four years previously, the patient had presented to a local hospital for evaluation of melena, and upper gastrointestinal endoscopy revealed IGVs. Conservative treatment for the IGVs was implemented. The patient’s medical history included third trimester induction (35 weeks) in December 2021 with unknown reason or circumstances surrounding the induction, as well as a diagnosis of thrombophilia. She denied a history of liver disease and alcohol abuse.

On arrival, the patient’s vital signs were as follows: body temperature, 36.3°C; heart rate was 83 beats per min; respiratory was 20 breaths per minute; and blood pressure was 123/71 mmHg. Physical examination revealed tenderness in the epigastric region. Laboratory tests showed mild anemia (hemoglobin of 10.2 g/L), and the activated partial prothrombin time was 44.9 seconds (reference range, 28.0–43.5 seconds). No abnormality in liver function was found. Upper endoscopy demonstrated tortuous veins at the body of the stomach with a red wale sign. According to the Sarin classification, the varicose vein type was IGV2 (Figure 1(a), (b)). Abdominal CECT revealed splenomegaly (123 × 110 ×67 mm), occlusion of the distal splenic vein and main splenic artery, and markedly dilated gastric veins (Figure 2(a), (b)) but no signs of liver cirrhosis or pancreatic disease. To further clarify the collateral circulation of the portal vein, three-dimensional models of the portal, splenic, and superior mesenteric veins reconstructed from the CECT images were created. These images demonstrated that collateral circulation had been established between the spleen and stomach (Figure 2(c)); however, there were no signs of underlying diseases involving splenic vein occlusion. After common conditions had been ruled out, the patient was suspected to have splenic vein occlusion as a complication of a hypercoagulable disease. Upon review of her medication use and medical history, we found that during her last induction, her protein S concentration had been 23.3% (reference range, 55%–140%) on 13 December 2021.

Figure 1.

Endoscopic images. (a, b) Numerous tortuous veins were observed at the body of the stomach with stigmata and a red wale sign (yellow arrow) and (c, d) endoscopic image after laparoscopic splenectomy and pericardial devascularization revealed disappearance of the isolated gastric varices.

Figure 2.

Abdominal contrast-enhanced computed tomography images. (a) The splenic vein was occluded (yellow arrow). (b) The body of the gastric veins was markedly dilated (yellow arrows). (c) Three-dimensional computed tomography revealed an abnormal vascular mass in the gastric fundus (yellow arrow) and occlusion of the splenic vein (yellow arrow) and (d) contrast-enhanced computed tomography after splenectomy showed disappearance of the abnormal collateral vessels in the gastric fundus.

Considering the patient’s reproductive history, we performed a further diagnostic work up that included tests for inherited and acquired hypercoagulable conditions (including proteins C and S and antithrombin) as well as tests for lupus anticoagulant and antiphospholipid antibody. Notably, lupus anticoagulant was positive at the silica clotting time, and the protein S concentration was 33.6% (reference range, 55%–140%). With the triad of pregnancy morbidity, unexplained venous occlusion, and positive lupus anticoagulant, APS was highly suspected. Based on her history of recurrent melena, secondary prevention for IGVs was recommended. Splenic artery embolization was not performed because the middle section of the main splenic artery was occluded. Finally, the patient underwent laparoscopic splenectomy and pericardial devascularization. Histopathological examination of the spleen confirmed chronic congestive splenomegaly. The patient underwent treatment with hypodermic injection of low-molecular-weight heparin (2500 U) for 3 days after surgery. She recovered well and was discharged on postoperative day 6 with oral aspirin.

The patient underwent regular follow-ups to rule out false-positive lupus anticoagulant. During the follow-up, lupus anticoagulant tested positive again on 8 August 2022 (interval of >12 weeks), and the diagnosis of APS with protein S deficiency was established. Furthermore, the diagnosis of IGVs secondary to splenic vein occlusion associated with APS and protein S deficiency was confirmed. The patient continued to receive long-term follow-up and oral aspirin therapy. During the next 6 months of follow-up, repeated endoscopy and CECT revealed disappearance of the IGVs (Figure 1(c), (d); Figure 2(d)).

Discussion

IGVs can be observed in 5% of patients with cirrhosis and up to 10% of patients with noncirrhotic portal hypertension.² Templeton³ first described IGVs in 1944, and Samuel⁴ subsequently stated in 1948 that any obstruction to splenic blood flow by a pancreatic tumor or splenic vein thrombosis tends to produce varices in the gastric fundus. Since then, case reports and case series of IGVs have been continuously reported. The most widely used classification system of IGVs was originally proposed by Sarin et al.¹ in 1992. Using this system, IGVs can be categorized into two types based on their location within the stomach: IGV1, which are located in the fundus of the stomach (2% of all gastric varices), and IGV2, which are located anywhere in the stomach except the fundus (4% of all gastric varices). Another classification system is based on whether IGVs appear at the initial presentation or develop after obliteration of esophageal varices and other gastric varices. In this system, secondary IGVs account for approximately 85%, whereas primary IGVs account for approximately 15%.²

From an anatomical and pathophysiological viewpoint, the etiology of IGVs can be divided into three categories: cirrhotic portal hypertension, noncirrhotic portal hypertension, and anatomic variation. Cirrhotic portal hypertension has been thoroughly described in previous reports and is beyond the scope of this article. Anatomic variation is rare since the short gastric vein drains into the splenic vein, and any structural abnormality that impedes venous return may lead to the formation of gastric varices. In noncirrhotic portal hypertension, the increase in resistance mainly occurs at the presinusoidal level. The elevation of portal venous pressure in noncirrhotic portal hypertension is attributed to histological changes in the portal vein branches, including sclerosis, narrowing or dilation of the lumen, occlusion of the lumen, and herniation in the lobule. LSPH is a localized form of extrahepatic portal hypertension that accounts for approximately 5% of cases. LSPH usually occurs as a result of splenic vein occlusion, including splenic vein stenosis, thrombosis, or external compression caused by a surrounding structure. Pancreatic diseases are the most common etiology because of the proximity in location between the splenic vein and pancreas; such diseases include pancreatitis, pseudocysts, abscesses, arterial aneurysms, and pancreatic neoplasms. Chronic pancreatitis is reportedly the most common cause, with a prevalence ranging from 5% to 22%.⁵ Other diseases have rarely been described; these include metastatic malignancies (renal cancer, gastric cancer, and colonic adenocarcinoma), lymphoma, surgical manipulations, retroperitoneal fibrosis, hypercoagulability disorders, umbilical vein catheterizations, and myeloproliferative diseases.

APS, an acquired hypercoagulable disorder, is characterized by pregnancy morbidity and systemic arterial and venous thrombosis. Deep venous thrombosis is the most common clinical manifestation, accounting for approximately one-third of cases. APS-associated splenic vein occlusion is a rare entity. According to a study by Kaushik et al.,⁶ splenic vein thrombosis accounts for only 18% of APS-induced abdominal vascular thrombosis. To our knowledge, only eight other case reports of APS causing splenic vein thrombosis have been published to date (Table 1).^7–14

Table 1.

Summary of eight cases of splenic vein thrombosis caused by APS.

Title and reference	Publication year	Thrombosis site	Etiology	Varices	Variceal bleeding	Therapy
Antiphospholipid antibodies and splenic thrombosis in a patient with idiopathic myelofibrosis (Bregani et al.⁸)	1992	Spleen	Idiopathic myelofibrosis, antiphospholipid antibodies	No mention	No	Heparin
Splenic vein thrombosis with pancytopenia and fever: antiphospholipid antibody syndrome (Adducchio et al.¹⁴)	1997	Splenic vein	Antiphospholipid antibody syndrome	No mention	No	Not available
Acute Budd-Chiari syndrome, portal and splenic vein thrombosis in a patient with ulcerative colitis associated with antiphospholipid antibodies and protein C deficiency (Junge et al.⁷)	2000	Axillary, subclavian, popliteal, portal, and splenic veins	Thrombocytosis, protein C deficiency, antiphospholipid antibodies	Fundic and antral varices	Yes	Long-term anticoagulation, transplantation
Portal vein thrombosis associated with a myeloproliferative disorder, prothrombin G20210A mutation, antiphospholipid syndrome, with repermeation during anticoagulant therapy (Diaz et al.¹⁰)	2001	Portal and splenic veins	Myeloproliferative disorder, antiphospholipid syndrome, factor II G202101 mutation	None	No	Anticoagulant treatment
Coexistence of homozygous factor V Leiden mutation and antiphospholipid antibodies in two patients presented with Budd-Chiari syndrome (Diz-Kucukkaya et al.⁹)	2002	Hepatic, portal, and splenic veins	Homozygous factor V Leiden mutation, antiphospholipid antibodies	Case 1: grade 1 esophageal and fundic varicesCase 2: grade -1 fundic varices	No	Warfarin
Primary antiphospholipid syndrome: a cause of fever of unknown origin (Ozaras et al.¹¹)	2003	Splenic, superior mesenteric, and portal veins	Primary antiphospholipid syndrome	No mention	No	Low-molecular-weight heparin and warfarin
Relapsing splenic vein thrombosis associated with antiphospholipid antibodies in a patient with Wegener granulomatosis (Steen et al.¹²)	2007	Relapsing splenic vein thrombosis	Wegener granulomatosis, antiphospholipid syndrome	No mention	No	Heparin and oral warfarin
Spontaneous splenorenal shunt in a patient with antiphospholipid syndrome (Cacciapaglia et al.¹³)	2007	Total portal, mesenteric, and splenic veins	Antiphospholipid syndrome, deficiency of C and S protein, heterozygous MTHFR mutation	Grade F3 esophageal varices	No	Low-molecular-weight heparin and beta-antagonist

In this case, abdominal CECT showed splenic vein occlusion with no obvious intravascular low density and no signs of acute thrombosis. We hypothesized that the splenic vein occlusion had been caused by chronic thrombosis or vasculitis related to APS. Unfortunately, because pathologic examination of the splenic vein was not performed, splenic vein occlusion caused by chronic thrombosis or vasculitis can only be highly suspected. However, the patient’s chronic disease course and the rich network of collateral vessels in the splanchnic circulation suggest that the development of splenic vein occlusion is a chronic process, supporting the above assumption to some extent.

Protein S is a vitamin K-dependent anticoagulant, and a decrease in the protein S concentration has been reported as a primary cause of portal vein thrombosis. The annual incidence rate of venous thrombosis is approximately 0.50% to 1.65% in patients with protein S deficiency. In a study from North America, protein S deficiency was more common in patients with splanchnic vein thrombosis than in those with deep vein thrombosis.¹⁵ Protein S deficiency existing in the context of APS is a rare syndrome, and the underlying mechanism is unclear. However, it may be due in part to impairment of the physiologic anticoagulant functions of protein S by the binding of antiphospholipid antibodies. The coexistence of lupus anticoagulant and protein S deficiency greatly aggravated the patient’s thrombophilia in this case. The coexistence of both conditions is reportedly more common in patients with systemic lupus erythematosus and acquired immune deficiency syndrome.¹⁶

Although an association between APS and splenic vein occlusion and between IGVs and splenic vein occlusion has been shown in the literature, the coexistence of these three conditions has been reported in only one other case besides this report.¹⁷ However, this report is the first description of IGVs secondary to splenic vein occlusion associated with both APS and protein S deficiency.

When the splenic vein is occluded, the blood flow in the short gastric vein and gastroepiploic vein, which normally drains through the splenic vein, begins draining through the coronary vein into the portal vein or the superior mesentery. The reversal of flow in these veins results in increased blood flow and pressure, submucosal structures consequently dilate, leading to the formation of gastric varices. When the coronary vein drains distal to the obstruction in the splenic vein, esophageal varices may occur alone or in combination with gastric varices. IGVs form in the setting of splenic vein thrombosis, have been well known, and one study showed that the gastric variceal bleeding rate was 12% in patients with splenic vein thrombosis.¹⁸

Most IGVs are asymptomatic and found incidentally in the process of diagnosing related diseases. In one study, chronic abdominal pain and variceal bleeding were observed in 89% and 50% of patients with LSPH, respectively.⁵ Bradley¹⁹ reported that the first clinical manifestation of LSPH was generally acute or chronic gastrointestinal bleeding. Other studies showed that gastrointestinal bleeding was the presenting symptom in 45% to 72% of patients with LSPH.^20,21

The presence of IGVs without liver cirrhosis is considered highly suggestive of splenic vein obstruction. When IGVs are suspected on an upper gastrointestinal series, routine biochemistry tests should be performed to exclude hepatogenic portal hypertension. Endoscopy is the most widely used modality, but its sensitivity depends on the endoscopist’s experience because gastric varices hidden by rugal folds at the gastric body may be easily overlooked. The use of endoscopic ultrasonography makes it possible to precisely visualize IGVs and evaluate the patency of the splenic vein. CECT can not only identify a significant number of gastric varices but also show the portal vein collateral circulation. A prospective study of 102 patients confirmed that CT had a sensitivity of 87% for the detection of gastric varices. In addition, CT identified periesophageal varices and extraluminal pathology that are essential for establishing optimal treatment.²² Magnetic resonance angiography has been shown to be a promising noninvasive method for the diagnosis of patency or thrombosis of the portal venous system.

Because of their distinct anatomy and etiology compared with gastric varices associated with portal hypertension, IGVs secondary to splenic vein occlusion should be individually managed on the basis of underlying diseases. The management of patients with LSPH aims to target the underlying disease on the one hand and to prevent bleeding complications on the other. In the acute phase of bleeding, initial resuscitation (including intravenous fluid resuscitation and the administration of blood products, antibiotics, and vasoactive drugs) should start as early as possible. Once hemodynamics are stabilized, other options become available to control bleeding (e.g., endoscopic treatment, radiologic treatment, and surgical approaches).

Endoscopic treatments, such as gastric variceal sclerotherapy, gastric variceal band ligation, endoscopic cyanoacrylate injection, and endoscopic ultrasound-guided coil/glue application, can be performed to control acute bleeding from gastric varices. In a retrospective study, Kozieł et al.²³ reported technical success of endoscopic ultrasound-guided treatment of gastric varices using coils and cyanoacrylate glue injections in 15 of 16 patients (94.0%). In a case series, Japanese endoscopists demonstrated an 87.5% clinical success rate of endoscopic ultrasound-guided coil deployment with sclerotherapy for IGVs, and long-term nonrecurrence was achieved.²⁴ However, these techniques do not resolve the underlying cause of bleeding, thereby resulting in high rebleeding rates.

Balloon retrograde transvenous obliteration, partial splenic embolization (PSE), splenic vein stenting, and percutaneous trans-splenic embolization are radiologic treatments that represent another short-term therapeutic option with a high rate of successful bleeding control. Kobayakawa et al.²⁵ reported that balloon retrograde transvenous obliteration achieved success in 76.9% to 100% of patients with acute gastric varices; however, it is used to treat gastric varices only in the presence of a gastro-renal or gastro-caval shunt. El Kininy et al.²⁶ suggested that splenic vein stenting, an emerging treatment, was effective; however, more trials with longer follow-up are needed. Percutaneous trans-splenic embolization is a promising approach, and several studies have shown that the success rates of this approach range from 91.6% to 96.0%.²⁷ PSE improves hypersplenism and reduces portal hypertension by decreasing blood flow from the splenic vein, thereby reducing episodes of variceal rupture. The most important advantage of PSE over splenectomy is the preservation of splenic function. If splenectomy is avoided because of its invasiveness, PSE can also be performed with similarly good outcomes for IGVs.²⁸

Splenectomy with or without gastric devascularization may be required in cases of uncontrolled bleeding or when extensive varices are present.²⁹ However, the role of surgery in asymptomatic patients remains controversial. In the present case, the middle section of the main splenic artery was occluded, and the distal splenic artery branch was connected to the right gastroepiploic artery and left subphrenic artery. Hence, splenic artery embolization was not suitable. Finally, more aggressive splenectomy and gastric devascularization were performed.

This report highlights the complex course and arising clinical challenges of LSPH due to severe thrombophilia, and there are three important points to mention regarding the diagnosis and treatment in this case. First, the local hospital did not consider the presence of the IGVs to be of serious concern at the time of the patient’s initial visit, and no further investigations into the underlying cause or treatments were carried out because she had no history of chronic liver disease. This suggests that clinicians are not paying enough attention to varices associated with noncirrhotic portal hypertension. Second, when screening for the etiology of IGVs, we did not note the patient’s history of induced abortion or the presence of protein S deficiency. Systemic hypercoagulable states should be screened to identify non-pancreatic causes of LSPH, especially in women of reproductive age. Third, the treatment of APS varies depending on the risk stratification, and the 2006 Sydney Guidelines recommend low-dose aspirin for primary prevention. The patient had no acute thrombosis, and the diagnosis of chronic thrombosis in the splenic vein and splenic artery was unclear; therefore, she received regular follow-up and oral aspirin therapy. If she plans to become pregnant in the future, anticoagulant therapy will be required.

Conclusion

In the present case, we described a rare case of IGVs secondary to splenic vein occlusion associated with APS and protein S deficiency, this is the first known report of this specific condition. We also systematically reviewed the etiology, clinical manifestations, diagnosis, and treatment methods of IGV, which we hope will provide a reference for the clinical diagnosis and treatment of similar patients. Overall, this case report demonstrates the clinical challenges of patients with LSPH related to severe thrombophilia.

The reporting of this study conforms to the CARE guidelines.³⁰

Footnotes

Acknowledgement

The authors thank the patient for her cooperation and permission to publish this case.

Author contributions

Xueyan Li reviewed the literature and drafted the manuscript. Ying Liu, Jiandi Wu, and Feifei Fang substantially contributed to the design of this study. Wewei Jiang, Gangping Li, and Jun Song revised the manuscript for important intellectual content. All authors have read and approved the final manuscript.

Consent

The patient provided written consent for publication of this report.

Data availability statement

Any inquiries regarding the data of the report beyond the information provided in the article can be directed to the corresponding author.

Ethics approval

This study was a case report and literature review and did not involve human or animal subjects. Therefore, ethics approval was not required.

Declaration of conflicting interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Funding

No funding was received for the present study.

ORCID iD

Jun Song

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Isolated gastric varices associated with antiphospholipid syndrome and protein S deficiency: a case report and review of the literature