Computed tomographic features of focal lipogranulomatous lymphangitis for differentiating from malignant intestinal lesions in a dog

Abstract

An eight-year-old Maltese dog presented with diarrhea and anorexia. Ultrasonography revealed marked focal wall thickening with loss of layering in the distal ileum. Contrast-enhanced computed tomography (CT) revealed a preserved wall layer with hypoattenuating middle wall thickening. In some segments of the lesion, small nodules protruding toward the mesentery from the outer layer were observed. Histopathology revealed focal lipogranulomatous lymphangitis (FLL) with lymphangiectasia. This is the first report to describe the CT features of FLL in a dog. CT features of preserved wall layers with hypoattenuating middle wall thickening and small nodules can assist in diagnosing FLL in dogs.

INTRODUCTION

Focal lipogranulomatous lymphangitis (FLL) is defined as a focal or regional inflammation of the lymphatic vessels and intestinal wall without a clear etiology [1,2]. It is characterized by transmural granulomatous inflammation with lipogranulomas appearing as small white nodules of the intestinal wall or mesentery [1,3]. Although histological evaluation is required to definitively diagnose FLL, some reports have described the ultrasonographic features of FLL in dogs. However, to the best of our knowledge, only 20 cases have been reported to date, and no studies have described the computed tomography (CT) features of FLL [1,3,4]. In this report, we describe the imaging features of FLL in a dog including ultrasound and CT, and the usefulness of CT for evaluating FLL lesions.

CASE PRESENTATION

An eight-year-old, 1.7-kg, spayed female Maltese dog presented with chronic diarrhea. The complete blood count was unremarkable. Serum chemistry revealed hypoalbuminemia (1.4 g/dL; reference interval: 2.2–3.9 g/dL) and hypoproteinemia (2.9 g/dL; reference interval: 5.2–8.2 g/dL). There were no abnormalities on thoracic radiographs. On abdominal radiographs, serosal detail was diffusely decreased, and it was difficult to assess abdominal organs.

Abdominal ultrasonography (Apilio 500; Canon Medical System, Japan) revealed marked focal and circumferential thickening of the distal ileum at about 8 mm (Fig. 1). The wall of the ileum was heterogeneously hypoechoic, with multiple hyperechoic speckles within the thickened wall. The wall layering had completely disappeared at the center of the lesion. There was no distinct margin between the lesion and the adjacent normal intestinal wall. Hyperechoic mesenteric fat edema and anechoic peritoneal effusion were observed. Based on ultrasonography, a primary intestinal tumor, such as adenocarcinoma, leiomyosarcoma, or severe inflammatory bowel disease (IBD) such as eosinophilic or lymphocytic-plasmocytic enteritis with lymphangiectasia was suspected. CT was performed using a 16-channel multi-detector CT (GE Revolution ACT 16; GE Healthcare, USA) to evaluate the extent of the lesion and the presence of metastasis to the lymph node or lung.

Fig. 1. Ultrasonography images of the distal ileum (A), and jejunum (B) of the dog. Focal and marked circumferential irregular thickening of the distal ileum with loss of layering (A, yellow arrows) are observed (A and B). Multiple hyperechoic speckles are observed in the thickened wall (A). The wall of the jejunum has a normal thickness and layering (B).

General anesthesia was induced using alfaxalone (2 mg/kg i.v.; Alfaxan®, Careside, Korea), and maintained with isoflurane (1.5–2.5) and oxygen (1 L/min) after endotracheal tube intubation. A ventilator was used during anesthesia, which was temporarily stopped during CT scanning to induce apnea. The scanning parameters were as follows: 120 kV, 130 mA, 1.25 mm thickness, and 1 s rotation time. After placing the dog in sternal recumbency, thoracic and abdominal CT images were acquired before and after the iohexol injection (Omnipaque 300; GE Healthcare, Norway, 600 mgI/kg; i.v.; 2 m/sec). Triple-phase CT images of the abdomen were obtained at arterial (5 sec), venous (25 sec), and delayed (150 sec) phases after performing a test-bolus scan with an injection of iohexol (150 mgI/kg; i.v.; 2 mL/sec) at the level of porta hepatis. Thoracic CT images were obtained only in the delayed phase.

Abdominal CT revealed segmental and circumferential thickening of the distal ileum about 5 cm in length (Fig. 2). The thickened wall showed a stratified enhancement pattern with a three-layer appearance in the arterial, portal, and delayed phases: a strongly enhanced inner layer, a hypoattenuating thickened middle layer, and a mildly enhanced outer layer. Each wall layer exhibited relatively homogeneous enhancement. In contrast to the thickened walls, the normal intestinal segments showed homogeneous enhancement without distinction between each wall layer in the venous and delayed phases. In some segments of the distal ileum, small nodules protruding toward the mesentery from the outer layer were suspected (Fig. 3). No evidence of lymphadenopahty or metastasis was observed.

Fig. 2. Computed tomography images of transverse pre-contrast (A), arterial (B), venous (C), delayed phase (D) and dorsal plane venous phase (E). The distal ileum is circumferentially and irregularly thickened (thickness: 5−6 mm, yellow arrows). The thickened wall shows a stratified enhancement pattern; a strongly enhanced inner layer, a hypoattenuating inner layer, and a mildly enhanced outer layer. Other normal intestinal segments show a hyper-enhanced inner layer, but no distinction with the middle and other layers in the arterial phase, and show homogeneous enhancement without wall layering in the venous and delayed phases.

Fig. 3. Transverse delayed-phase computed tomography image (A), intraoperative view (B), and histology (C). Two small nodules protrude from the intestinal surface (yellow arrows); these are not connected to the vessels, and there are no surrounding structures that could cause partial volume artifact (A). In the intraoperative view, the distal ileum is thickened, and multiple small white nodules are visible along the lymphatic vessels and mesenteric border of the ileum (B). On histopathology (C), the muscularis layer (asterisk) of the small intestine is thickened with inflammation and lipogranuloma (black arrows). The wall layering of the thickened wall can be distinguished. The lymphatic vessels are severely dilated in the submucosa and mucosa layers.

On Laparotomy, the distal ileum was sampled using a punch biopsy. Grossly, milky-pink colored abdominal effusion was observed and the mesenteric lymph vessels of the distal ileum were segmentally distended. Multiple small white to pink nodules (1–2 mm) were observed at the mesenteric border of the thickened ileal wall, which was confirmed as granulomatous inflammation on histopathology (Fig. 3). In granulomas, necrosis of the smooth muscle with inflammatory cells and lipid-laden macrophages was observed. Lymphangiectasia was observed in the mucosal and submucosal layers. The final diagnosis was FLL with lymphangiectasia.

The patient recovered uneventfully post-surgery. Prednisolone (1 mg/kg, PO, SID) was administered, with progressive tapering for over 3 months. Metronidazole (10 mg/kg, PO, BID) and famotidine (0.5 mg/kg, PO, BID) were also administered. The clinical signs resolved, and protein and albumin levels were observed to be within normal limits 14 days after treatment.

DISCUSSION

This report describes the imaging features of FLL in a dog. To the best of our knowledge, this is the first report describing the CT features of FLL in a dog. The FLL lesion showed segmental wall thickening and loss of wall layering of the distal ileum and ileocolic junction on ultrasonography, mimicking the primary intestinal tumor. However, stratified layering with hypoattenuating thickening of the middle layer was observed on CT, indicating a benign lesion rather than a malignant tumor.

Previously reported ultrasonographic features of FLL include focal circumferential thickening of the intestinal wall, in which granuloma and inflammation mainly involve the muscular layer and less likely the mucosa [1,4]. These features may be one of the main ultrasonographic features of FLL and it could make FLL be differentiated from malignant tumors, which usually show focal transmural thickening with a loss of layering [1,4,5]. However, in previous studies, 37.5% (6/16) of FLL lesions were accompanied by loss of wall layering [1,4], which makes it difficult to differentiate FLL from malignant tumor, as in the present case.

In humans, contrast enhancement patterns of thickened walls on CT have been widely used to differentiate intestinal lesions [6]. Focal, irregular, asymmetric, or heterogenous wall thickening is the main feature of malignant tumor, else, stratified wall thickening commonly indicates benign lesions [6,7]. Stratified wall thickening can be divided according to the contrast enhancement pattern. The spectrum of enhancement patterns include white (uniform and avid contrast enhancement of the thickened wall), gray (limited enhancement), water halo sign (stratification within a thickened bowel wall that consists of two or three thickened layers), fat halo sign (three-layered target sign of thickened bowel in which the middle layer has a fatty attenuation) and black (equivalent of pneumatosis), respectively [6]. Differentiating these patterns will considerably narrow the diagnostic possibilities [6].

In the present case, the lesion showed a three-layered appearance on post-contrast CT, with a strongly enhanced inner layer, homogeneously hypoattenuating middle layer, and mildly enhanced outer layer. Because malignant tumors in the gastrointestinal tract of dogs generally show heterogeneous contrast enhancement without distinct wall layering on CT [8,9] and the CT features in the present case were similar to the water halo sign in humans, benign lesions rather than neoplasms were suspected [6,10]. Although further studies are required, the CT features described in this case could help differentiate FLL lesions from malignant tumors.

In the present case, unlike ultrasonography findings, wall-layering could be distinguished on CT and histology. Although the cause of this discrepancy was unknown, in the author’s opinion, the severe lymphangiectasia of the mucosal and submucosal layers and inflammatory changes of the muscular layer changed the thickness and echogenicity of the wall layer, which resulted in indistinct wall layering on ultrasonography. In CT, it was thought that each layer was distinguished due to different contrast enhancement.

FLL is a rare form of IBD. On ultrasonography, diffuse thickening of the wall and/or altering of the wall layers can be seen in FLL and other IBDs. Severe, focal thickening of the muscular layer may be the main features of FLL, however, no specific findings have been reported for the diagnosis of FLL in dogs. Although CT features of IBDs in dogs have not been well described, IBD could cause similar changes in CT as in humans. The FLL in dogs has been thought to be similar to Crohn’s disease in humans, and the CT features of the FLL lesions in the present case showed a similar appearance to the water halo signs described in Crohn’s disease. The small nodules from the outer layer, which was thought to be a granulomatous lesion confirmed by histology, may be the feature of FLL, but further studies on many cases are needed.

The location and clinical features of FLL lesion in the present case were similar to the previously reported cases, as follows. In this case, the FLL lesion was located at the distal ileum, which is the predominant location of the FLL in dogs [1,3,4]. In this case, hyperechoic foci were observed within the thickened wall on ultrasonography, which was confirmed as lymphangiectasia on histopathology, and the dog had hypoalbuminemia. Protein-losing enteropathy has been thought to be a concurrent disease of FLL and the most common laboratory findings of FLL were hypoalbuminemia and hypocobalaminemia [1,3,4]. However, FLL can occur independently of protein-losing enteropathy with a normal laboratory test result [1,3,4].

In conclusion, the FLL lesion showed focal intestinal wall thickening with loss of wall layering on ultrasonography, mimicking a focal intestinal tumor. However, on contrast-enhanced CT, a stratified wall layer and homogeneous contrast enhancement of the thickened wall layer were observed, indicating a benign lesion. These findings suggest that the use of contrast-enhanced CT to evaluate focal intestinal lesions could help differentiate FLL from malignant lesions.