A 16-week-old 1.5-kg (3.3-lb) sexually intact male Ragdoll kitten with ascites was referred to the Oregon State University Veterinary Teaching Hospital for diagnostic workup of abdominal distension. The abdominal distension was initially noted at 7 weeks of age. The cat had no other clinical signs and was active and eating normally according to the owner. Results of a PCR assay for feline coronavirus run on a sample of peritoneal fluid were negative. Results of fecal flotation were also negative. Additionally, the cat was negative for both circulating FIV antibody and FeLV antigen.
Prior to the referral evaluation, hematologic and serum biochemical testing revealed no abnormalities. Repeated abdominocentesis yielded a yellow, hazy fluid with a total protein content of 3.4 g/dL and 1,412 nucleated cells/μL with no evidence of infectious agents, consistent with a modified transudate. Abdominal ultrasonography performed by a board-certified veterinary internist revealed a markedly distended CVC and hepatic vessels. A board-certified veterinary cardiologist performed echocardiography, which revealed no structural heart disease, and thoracic radiography, which revealed a normal cardiac silhouette with no pulmonary disease. The cat subsequently underwent a CT evaluation.
At the initial teaching hospital evaluation, physical examination abnormalities included severe abdominal distension and panting. Under anesthesia, abdominal CT angiography was performed with a 64-detector CT scannera before and after IV injection of iodinated contrast medium (2 mL of iopamidolb/kg [0.91 mL/lb]). Following contrast medium administration, CT images were acquired in arterial, portal, and venous vascular phases with the following conditions: voxel size, 0.5 mm; rotation speed, 0.5 seconds; matrix, 512 × 512; current, 250 mA; and voltage peak, 120 kV. The volume data were reconstructed in bone and soft tissue algorithms and in isovolumetric transverse, sagittal, and dorsal planes at a slice thickness of 1 mm. The images revealed that the liver was markedly enlarged with rounded and lobular margins and extended caudally to the level of vertebral body L3. At the cranial margin of the liver, the CVC focally tapered in diameter from 5 to 6 mm to 2 mm. At this focal tapering, there was a persistent curvilinear void in the contrast medium within the CVC, most clearly seen in the portal and venous phases (Figures 1 and 2). Multiple abnormal, tortuous, markedly dilated hepatic veins (up to 9 mm in diameter) were evident. These hepatic veins communicated with the CVC at multiple abnormal locations throughout the cranial to caudal extent of the liver. The communication points were all located caudal to the focal CVC narrowing. The portal vein appeared normal. There was a marked amount of non–contrast-enhancing fluid within the peritoneal cavity. Six days after the cat underwent abdominal CT angiography, selective vena caval angiography was performed under general anesthesia by advancing a 60-cm, 4F balloon wedge pressure catheterc into the CVC via the jugular vein under fluoroscopic guidance. Approximately 2 cm caudal to the diaphragm, advancement of the catheter met resistance. A 2-mL contrast medium bolus (1:1 ratio of iohexold and saline [0.9% NaCl] solution with heparin) was hand injected through the catheter, with the balloon inflated to assist retrograde flow. As a result, stenosis of the CVC approximately 5 cm caudal to the diaphragm (Figure 3) was confirmed. Pressure measurements were obtained at and cranial to the level of the stenosis, indicating a pressure difference of approximately 14 mm Hg. Despite several attempts, the catheter could not be maneuvered across the stenotic region into the caudal region of the CVC. The right jugular vein was ligated following the procedure, and the subcutaneous and cutaneous tissue layers were closed routinely.
Computed tomographic angiography images of the abdomen of a 16-week-old 1.5-kg (3.3-lb) sexually intact male Ragdoll kitten with a 9-week history of marked modified transudate ascites. Images were acquired in the venous (A) and portal phase (B) following IV injection of iodinated contrast medium. A—Sagittal image in which the diameter of the CVC is observed to taper at the cranial margin of the liver (arrow). B—Dorsal image depicting the tapering of the CVC (arrow). Notice the curvilinear filling defect in the contrast medium within the CVC, suggestive of a congenital malformation.
Citation: Journal of the American Veterinary Medical Association 245, 4; 10.2460/javma.245.4.414
A 3-D reconstruction of the soft tissue window images acquired in the venous phase following IV injection of iodinated contrast medium from the cat in Figure 1. Notice the filling defect in the CVC at the level of the stenosis (arrow).
Citation: Journal of the American Veterinary Medical Association 245, 4; 10.2460/javma.245.4.414
Fluoroscopic image acquired during selective catheterization of the CVC of the cat in Figure 1 following injection of a 2-mL bolus of iohexol and saline (0.9% NaCl) solution with heparin (1:1 ratio). The arrow indicates the stenotic area.
Citation: Journal of the American Veterinary Medical Association 245, 4; 10.2460/javma.245.4.414
On the basis of the pressure gradient at the CVC narrowing, it was determined that the cat might benefit from vascular stenting of the affected CVC region. Preoperative blood typing was performed by use of a commercial kit.e A week after selective vena caval angiography, the cat was anesthetized and the abdominal cavity was accessed via median celiotomy to locate the CVC. An 18-gauge IV catheter was placed caudal to the left and right renal veins to insert a 0.035-mm-diameter hydrophilic guidewiref into the CVC. When trying to advance the guidewire through the CVC narrowing, slight resistance located approximately 2.5 cm cranial to the right phrenicoabdominal vein was felt. With a mild increase in the amount of cranially directed force, the guidewire was advanced beyond the stenotic area. The catheter was removed, and a 6F introducerf was placed over the guidewire into the vena cava. The guidewire was removed, and a 6F 8 × 24-mm biliary stentf was advanced into the stenotic area under fluoroscopic guidance. A single dose of heparin (35 U/kg [15.9 U/lb], IV) was administered preceding the deployment of the vascular stent. The stent was expanded with saline solution under maintained fluoroscopic guidance to a pressure of 6 atm, as measured with a handheld pressure gauge. Electrocardiographic monitoring of the cat detected a transient decrease in heart rate from 200 to 180 beats/min accompanied by the appearance of 4 ventricular premature complexes during deployment of the intravascular stent, which resolved without intervention once the balloon of the expanding stent was deflated. The venotomy site was closed with 6–0 polydioxanone sutureg in a simple continuous pattern following removal of the introducer. The cat had moderate to severe hypotension (mean arterial pressure, 30 to 60 mm Hg) throughout the procedure, which necessitated treatment with constant rate infusions of dopamine (5 to 10 μg/kg/min [2.3 to 4.5 μg/lb/min], IV) and dobutamine (1 μg/kg/min [0.45 μg/lb/min], IV), hetastarch (6%; 2 mL/kg [0.9 mL/lb], IV, over a period of 10 minutes), and vasopressin (0.013 U/kg [0.006 U/lb], IV, once). The liver was diffusely nodular in appearance, and 4-mm punch biopsy specimens were obtained from right and left lateral liver lobes. The remainder of the intra-abdominal organs were grossly normal. The abdomen was lavaged and the incision routinely closed.
Stent placement in the abdominal CVC caudal to the diaphragm was confirmed with 2-view postoperative abdominal radiography. The stent extended from the caudal thoracic portion of the CVC to the cranial to mid aspect of the liver (ie, from the caudal aspect of the T11 vertebra to the midbody of the T13 vertebra). The cat recovered from anesthesia uneventfully and was hospitalized for 3 nights following the procedure.
Histologic examination of the liver biopsy specimens revealed focal areas of sinusoidal congestion with attenuation of hepatic cords. The amount of loose connective tissue within the liver capsule was greater than that considered normal and was accompanied by moderate vascular ectasia. Compared with findings typical of a healthy cat's liver, there was a moderate increase in portal collagen content with scattered, generally moderate dissection into the surrounding lobules, consistent with moderate fibrosis.
Recheck examinations at 3.5 and 7.5 months after surgery revealed that the cat was growing rapidly and its activity level was considered normal. The owner had no concerns regarding the cat's well-being except for intermittent soft feces. The cat was mildly overconditioned with a body condition score of 7 of 9, and mild distension of the abdomen was noted during both recheck examinations. A CBC and serum biochemical profile performed at each recheck examination revealed no remarkable findings. Serum alanine aminotransferase activity remained mildly high at the 3.5- and 7.5-month recheck examinations (180 and 73 U/L, respectively; reference range, 5 to 65 U/L). No peritoneal fluid was detected during recheck abdominal ultrasonography at 3.5 months after surgery.
At 7.5 months after stent placement, the cat was anesthetized and underwent abdominal CT angiography with settings similar to those used initially, except the current (300 mA) and contrast medium dose (1 mL of iopamidol/kg) were increased to account for the increased weight of the cat. Similar to initial findings, the liver remained enlarged and extended caudally to the L3 vertebra; however, the margins were less rounded and no longer lobular. The CVC stent was in a position similar to that detected radiographically after surgery and continued to bridge the location of the previous stenosis. The diameter of the CVC was 8 mm cranial to the stent, 9 mm at the level of the stent, and 4 mm caudal to the stent. The hepatic veins remained tortuous but were no longer dilated, with a maximal diameter of 5 mm. The multiple abnormal locations of entry of the hepatic veins into the intrahepatic CVC persisted. The peritoneal fluid accumulation detected at the initial evaluation had resolved. At this latter recheck examination, the portal vein at the porta hepatis was focally tortuous, which had not been detected previously. The cat recovered from the anesthetic episode uneventfully. At the time of the last telephone inquiry 13 months after stent placement, the owner reported that the cat remained free of clinical signs and continued to have a good appetite, normal energy level, and weight gain.
Discussion
Budd-Chiari syndrome in humans is characterized by an obstruction of the hepatic venous outflow, which leads to postsinusoidal portal hypertension and the associated triad of clinical signs: hepatomegaly, proteinaceous ascites, and abdominal discomfort.1–4 The obstruction that causes BCS can develop at any site between the liver and the right atrium, and the spectrum of lesions responsible includes veno-occlusive disease of the small hepatic veins as well as obstructions of the large hepatic veins or the suprahepatic portion of the inferior vena cava.2,4
In veterinary medicine, primary BCLS has mainly been reported as affecting dogs and can develop in conjunction with congenital cardiac defects (cor triatriatum dexter), blunt trauma to the CVC, and perivenular fibrosis of the hepatic veins.5–7 Secondary kinking and extraluminal obstruction of the CVC as a result of neoplasia, vehicular trauma, and cardiac disease can also lead to development of BCLS.8–10 Budd-Chiari–like syndrome in cats is a rare condition, with only 4 previously reported cases,2,11–13 to our knowledge. Two of the 4 cases were caused by obstruction of the CVC: one intrahepatic and the other extrahepatic.2,12 In cats, BCLS can also be a result of hepatic vein occlusion or stenosis.11,13 Regardless of the underlying cause, the previously described cats with BCLS had similar clinical signs.2,11,12,13 The young age of cats with fibrous membranous obstruction of the CVC but without concurrent coagulopathies or underlying hematopoietic disorders supports the conclusion that CVC obstructions are a congenital disorder.12,14 This is in contrast to the veno-occlusive disease and hepatic vein obstruction in middle-aged to older cats, in which the underlying etiopathogenesis is not completely understood.11,13
In the Western world, hepatic vein thrombosis is the most common cause of BCS in people. In most cases, an underlying hypercoagulable state can be identified.15,16 Among humans in Asian and African countries, inferior vena cava obstruction is the most common cause of BCS.3,4,15–17 Membranous obstruction of the inferior vena cava in humans was considered a congenital vascular malformation for many years, but with modern imaging and histologic evaluation, it is now also considered a complication of thrombosis.3,4
For the 4 previously reported feline cases of BCLS,2,11–13 abdominal ultrasonography was helpful in establishing a diagnosis and localizing the vascular lesion. In the cat of the present report, ultrasonography performed at a referral practice did not identify the lesion but did reveal CVC and hepatic vein distension, which are important indicators of a more cranial CVC stenosis. After consultation with a board-certified radiologist during the initial evaluation at the teaching hospital, it was decided to forego repeated abdominal ultrasonography in favor of CT angiography. This decision was based on individual preferences of the board-certified radiologist involved in this case; the procedure did successfully identify the localization and extent of the CVC stricture. Selective CVC catheterization was additionally performed to document pressure gradients across the stricture and to determine suitability of the patient for stenting of the lesion. It should be noted that the images acquired by venography during selective CVC catheterization highlighted the stenotic area very clearly.
Multiple minimally invasive and surgical treatment procedures are available for relieving hepatic vein obstruction in humans. Restoration of physiologic hepatic venous drainage is thought to be preferable to procedures that result in portosystemic shunting13,18 because of theoretical benefits of lower risks of liver failure and hepatic encephalopathy. This is likely also true for veterinary patients with CVC obstructions. Thus, stenting of the CVC narrowing was considered a viable treatment option in the present case.
In a previous report of BCLS in a cat,2 medical management was described as unrewarding and balloon dilation as well as surgical shunting options were deemed too unpredictable, considering the young age of the patient and presumed future growth following the procedure. The stent chosen for the procedure in the cat of the present report was a balloon-expandable nitinol stent. Nitinol is a nickel-titanium alloy with physical properties that make it ideal for vascular stenting.19,20 Specifically, the crystalline structure of the alloy is such that it exists in a different form at higher and lower temperatures, with a thermal memory effect at higher temperatures while remaining flexible and easy to deploy at lower temperatures.19 One-time intraoperative administration of heparin (35 U/kg, IV) was justified as a prophylactic antithrombotic treatment because of the risk of thrombus formation at the site of endothelial damage following stent deployment.
Although membranous stenosis of the CVC is believed to be congenital, subacute onset of postsinusoidal portal hypertension was suspected in the cat described in the present report. This was supported by the clinical findings, which included slow onset of ascites without evidence of hepatic encephalopathy and hepatomegaly consistent with hepatic congestion. The prognosis for cats with subacute BCLS remains uncertain, given that the cat of this report appears to represent the first case of successful CVC obstruction relief by stent placement in this species with survival time and follow-up > 1 year. Increases in portal pressure generally lead to decreased portal and hepatic arterial blood flow, thereby causing hypoxic damage and centrilobular necrosis of hepatocytes.1,21 If the reduced perfusion of the liver persists, fibrosis and cirrhosis will develop in a short period, often within 6 months from onset of centrilobular congestion.1,21,22 Results of a large clinical case series to determine the effects of surgical portal decompression in humans with BCS indicate that reversal of liver damage will occur with early correction of the underlying condition.22 Fibrosis, as detected in percutaneous liver biopsy specimens, did not progress to cirrhosis in any individual in whom portal decompression was successfully achieved.22 For the cat of the present report, the persistent abdominal distension evident at the recheck examinations was believed to be mainly attributable to the body condition score of the patient. The absence of recurrent ascites detected by recheck ultrasonography and CT and resolution of the hepatic vein dilation supported the resolution of clinical postsinusoidal portal hypertension. However, the likely congenital small size of the CVC caudal to the stent as well as the tortuousity of the portal vein at the porta hepatis identified during recheck CT examination were concerning with regard to residual subclinical portal hypertension. This could account for the cat's persistent hepatomegaly detected by CT as well as the mildly high serum alanine aminotransferase activity, and progression to clinical postsinusoidal portal hypertension at a later point cannot be ruled out. Nevertheless, for the young cat of this report, the outcome of balloon-expandable nitinol stent placement as the treatment of BCLS secondary to a membranous obstruction of the CVC was considered successful. Clinicians should be aware that CT angiography can be used to determine the localization of the stenosis and monitor the effect of treatment.
ABBREVIATIONS
| BCLS | Budd-Chiari–like syndrome |
| BCS | Budd-Chiari syndrome |
| CVC | Caudal vena cava |
Toshiba Aquilion, Toshiba American Medical Systems, Tustin, Calif.
Iopamidol (300 mg of iodine/mL), Bracco Diagnostics Inc, Princeton, NJ.
AI-07121, Arrow International Inc, Reading, Pa.
Omnipaque, GE Healthcare, Waukesha, Wis.
Alvedia Quick Test A+B, Alvedia, Limonest, France.
Infinity Medical Inc, Menlo Park, Calif.
Ethicon Inc, Somerville, NJ.
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