Korean J Vet Res > Volume 62(4); 2022 > Article
Park, Ahn, Chung, Lee, Park, and Choi: Vicarious excretion of contrast medium to small intestine in a dog with Toxocara canis infection

Abstract

A male mixed-breed dog of unknown age was presented with a history of bloody diarrhea and cachexia. Toxocara canis in vomitus was identified by a parasitologist. Hematology revealed low hematocrit, eosinophilia, and low albumin. Computed tomography (CT) revealed an enlarged pulmonary artery with an irregular wall, micronodules in the lung, and vicarious excretion of contrast medium to small intestine. CT scan was helpful for identifying lung lesions and the central organs of larval migration and also show vicarious excretion of contrast medium to the small intestine in T. canis infection.

Toxocara spp. is important gastrointestinal parasites in dogs and cats and have been studied with interest by not only veterinarians but also researchers in human medicine because of their zoonotic potential [1]. The reported infection rates in Western Europe vary from 3.5% to 34% for Toxocara canis in dogs and from 8% to 76% for Toxocara cati in cats [2,3]. The definitive hosts of Toxocara spp. are mainly dogs and cats, and the prevalence of patent Toxocara spp. infections is higher in puppies and kittens than in the adult animals [3,4].
T. canis infection can cause gastrointestinal and respiratory symptoms, including diarrhea, constipation, vomiting, coughing, dyspnea, and nasal discharge [1,3], and the degree of host damage depends on the tissues invaded [4].
The radiographic findings in T. cati-infected cats are primarily bronchial or/and interstitial infiltration in the lung [5]. On ultrasonography, the adult worms are detected as 2 hyperechoic lines with a hypoechoic center line, representing the outer walls of the worm [6]. In human medicine, the toxocariasis lesions in the liver and lung parenchyma have been studied using computed tomography (CT) [7-10]. In general, contrast medium injected intravenously is mainly excreted by glomerular filtration, and vicarious excretion of contrast medium (VECM) is defined as excretion via an alternative route such as the biliary tract or gastrointestinal tract, i.e. [11]. To the authors’ knowledge, there is no veterinary report for VECM to the small intestine on CT. This report describes CT images and VECM in a dog that was diagnosed to have T. canis infection.
A male mixed-breed stray dog of unknown age was presented for diagnosis and treatment of diarrhea and cachexia. Two weeks earlier, the dog had arrived for care in a shelter, where the diarrhea was observed immediately. The dog unexpectedly vomited during physical examination by a hospital veterinarian, and worms were seen in the vomitus. The worms were about 5 to 10 cm in length and yellowish in color. They were microscopically confirmed to be adult T. canis worms by a parasitologist (Fig. 1). The sex of the worms was identified by their size and reproductive system (female worms are 5 to 15 cm long and have a genital pore at the posterior end whereas male worms are about 5 cm long and have a tubular testis at the posterior end). T. canis eggs were identified microscopically on fecal testing (Fig. 1E). A complete blood count revealed low hematocrit (32.2%, reference interval [RI], 37.3% to 61.7%), eosinophilia (1.67 K/μL; RI, 0.06 to 1.23 K/μL), neutrophilia (17.67 K/μL; RI, 2.95 to 11.64 K/μL), and monocytosis (1.75 K/μL; RI, 0.16 to 1.12 K/μL). The serum biochemical profile was notable for hypocholesterolemia (104 mg/dL; RI, 110 to 320 mg/dL) and slightly low albumin (2.4 g/dL; RI, 2.3 to 4.0 g/dL).
The radiographic findings were unremarkable. Abdominal ultrasonography detected adult T. canis worms with the diameter of 2.4 mm in the duodenum. Considering the cachexic condition and low albumin, CT was performed to determine the distribution of the lesions caused by T. canis infection and to evaluate a possibility of protein losing enteropathy. CT (Alexion; Canon, Japan) was performed with 120 kV, 150 mA, 1 mm slice thickness, 0.75 seconds rotation time and 0.938 collimation beam pitch in sternal recumbency under general anesthesia. Pre-contrast imaging was acquired first, after which the arterial and portal venous phase images were sequentially obtained following 10 mL contrast medium (300 mg/mL, Omnipaque, iohexol; GE Healthcare, Ireland) was injection at a rate of 2 mL/sec. The delayed phase was scanned at 10 minutes after injection of the contrast medium. The CT images showed dilated pulmonary arteries with an irregular wall and micronodules in the subpleural area (Fig. 2). In the small intestine, distinct mucosal contrast enhancement in arterial phase and mucosal washout in portal phase were seen (Fig. 3). In delayed phase, most of the contrast medium was identified to be in the kidney, ureter, and urinary bladder, but also to be diffuse on the luminal surface of the small intestine of the duodenum, jejunum, and ileum (Fig. 3D). This CT finding was interpreted as VECM to the small intestine. The distribution of lesions was identified mainly in the lung and intestine by CT images and was consistent with the life cycle of T. canis. The patient was treated with an oral combination tablet containing mebendazole 100 mg and praziquantel 25 mg once daily for 3 days. The patient’s diarrhea disappeared after 3 days of hospital care. The dog was then discharged, and had a good outcome when reviewed 6 months later.
CT images of dogs infected with T. canis have not been reported previously. A veterinary study documenting the imaging features of experimental T. cati infection and several human case reports were referenced when interpreting the findings in our patient [5-10,12]. The occurrence and distribution of lesions were predicted based on the histopathological characteristics and life cycle of T. canis infection. The severity of lesions varies according to the degree of infection; however, this is difficult to judge because of the lack of a clear standard. The life cycle of T. canis includes the larvae needing to complete either tracheal or somatic migration before they become adult worms in the gastrointestinal tract. T. canis eggs first appear in dog feces at 4 to 5 weeks following infection [2,3]. In our case, given that the adult worms in the intestine were detected both macroscopically and ultrasonographically and that shedding of T. canis eggs in the feces was identified during the hospitalization period, it is presumed that larval migration has already been completed and that the dog had been infected for at least 4 to 5 weeks. Based on these findings, we predicted that CT would detect parenchymal lesions consistent with the route of migration, e.g., the lung, liver, and intestine. Liver lesions were not detected in our patient. However, pulmonary lesions and atypical excretion of contrast medium through the wall of the small intestine were identified.
In a course of migration, the larvae reach the lung via the pulmonary vessels and penetrate the alveoli before migrating to the trachea. The lesions in the pulmonary vessels and parenchyma appear as increased attenuation on radiographic and CT images. In human medicine, pulmonary lesions caused by T. canis infection can be radiographically categorized as ground-glass opacities, solid nodules, consolidations, or linear opacities [8]. The most common pattern is ill-defined ground-glass opacities, defined as hazy areas of increased attenuation in the lung without obscuration of the underlying pulmonary vessels [8,10]. The pulmonary lesions tend to involve 3 or more lung lobes on the initial CT scan and the major location is the subpleural area of the lung [8]. In 2 studies, these lesions were found to have either disappeared or migrated on follow-up CT [8,10]. Radiographs of cats with experimentally induced T. cati infection show a diffuse bronchial-interstitial pattern and enlarged pulmonary arteries, and these lung lesions can also be identified by CT [5]. The lung lesions in our case were detected on CT images but not on radiographs, as described in the previous veterinary and human literature. This suggests that the lesions were not large enough to be detected by radiography and that CT is a better modality for evaluating the distribution of lesions caused by T. canis infection.
To evaluate the conspicuity of the mucosal layer of the intestinal wall, we compared the same intestinal segment at the same transverse level in the different phases (Fig. 3). Typically, upon washout of contrast from the luminal surface, the outer gastrointestinal wall shows homogeneous enhancement [13]. However, in our case, the contrast medium was seen again in the lumen in the delayed phase. Given that washout of contrast medium was confirmed in the portal phase, the intraluminal appearance of contrast medium in the delayed phase can be interpreted as VECM in the small intestine.
VECM generally occurs in the presence of impaired renal function [14]. VECM occurring by enteropathy has not been reported yet, but an iodinated contrast induced in the bowel was excreted via the urinary system in a human with Crohn’s disease [15]. In the present dog, there was no evidence of renal dysfunction or obstruction, and it is suspected VECM was occurred by enteropathy caused by T. canis infection. However, histopathology was not performed in our case, and more research is needed on leak of contrast through the gastrointestinal wall. Nevertheless, it is significant to note that delayed phase scans can detect VECM. Our case showed that VECM occurred in a T. canis-infected dog in the absence of renal dysfunction.
The CT images in this case were helpful for identifying lung lesions and the central organs of larval migration and also suggested the possibility of VECM in T. canis infection through leak of contrast medium across the intestinal barrier in the delayed phase.

Acknowledgments

This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (NRF-2017R1C1B5073755).

Fig. 1.
Microphotographs of adult Toxocara canis found in vomitus (A-D, bar: 300 µm) and T. canis egg found in feces (E, bar: 80 µm). (A) The cervical alae at the anterior end. (B) Three large lips on the anterior end. (C) The tail end of a male T. canis worm. (D) The tail end of a female T. canis worm. (E) A T. canis egg.
kjvr-20220026f1.jpg
Fig. 2.
(A, B) Transverse plane computed tomography (CT) images with lung window. (A) An enlarged pulmonary vessel (arrow) with an irregular wall in the accessory lung lobe. (B) Micronodules are observed in the subpleural area (arrowheads). (C) Three-dimensional reconstructed CT image. Small lung lesions are observed throughout the lung (arrows).
kjvr-20220026f2.jpg
Fig. 3.
Transverse pre-contrast (A), arterial phase (B), portal phase (C), and delayed phase 10 minutes after injection of contrast medium (D). Note the intraluminal appearance of contrast medium in the small intestine (arrows).
kjvr-20220026f3.jpg

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