Introduction

Cestodiasis is common among domestic dogs in the United States resulting from a tapeworm infection in either the adult or larval form. Dogs are considered a definitive host and become infected through ingestion of an infected intermediate host, such as a flea or rabbit. The most common species of cestodes to infect canines are Dipylidium caninum, Taenia pisiformis, and Taenia hydatigena.¹ Intestinal cestodiasis is often asymptomatic, but sometimes scooting is seen as the dog tries to remove the proglottids from the perianal skin.¹ Diagnosis is made by identifying proglottids in the feces, and treatment with an appropriate anthelmintic such as praziquantel is curative. Cysticercosis, in contrast, is rare in domestic dogs because it typically consists of ingestion of the tapeworm eggs being shed from the gastrointestinal tract of a definitive host (e.g., foxes), which are then consumed by a rodent intermediate host (e.g., groundhog), resulting in a tissue infection (most commonly in subcutaneous tissues, brain, and eyes).² Only a few cases of cysticercosis from Taenia solium, Taenia crassiceps, Spirometra spp., and Mesocestoides spp. have been reported in dogs.^3–6

This case report describes the successful treatment of T crassiceps cysticercosis in an 11 yr old mixed-breed dog. This case is unique in that the dog was subjected to a thorough workup before diagnosis, including multiple fine needle aspirates and biopsy samples, which were inconclusive. The dog was also receiving long-term oclacitinib maleate^a and intermittent prednisone for environmental allergies.

Case Report

An 11 yr old 9.3 kg male castrated mixed-breed dog was initially presented to the primary veterinarian for a 2 × 3 cm mass on the right dorsal hip, which was noticed 2 wk after the dog fell down several stairs. Prior medical history included suspected food allergies managed on a novel protein diet and environmental allergies medically managed on long-term oclacitinib maleate (0.6 mg/kg per os [PO] q 24 hr for ∼5 yr) and intermittent prednisone for flare ups (0.5 mg/kg PO q 24 hr for 7 days). On two separate occasions, while the mass was present, fecal flotation was performed by the primary care veterinarian, but no ova or parasites were recorded.

On physical exam, the dog was bright, alert, and responsive with vital parameters within normal limits. A 2 × 3 cm semimovable and nonpainful mass on the right dorsal hip region was noted. No lameness or neurological deficits were reported. Orthogonal radiographs of the pelvis, hips, and stifles were reported to have no significant findings; however, they were not reviewed by a radiologist. Fine needle aspirate^b of the mass was performed and interpreted by a board-certified clinical pathologist as chronic, mixed inflammation, consisting mainly of degenerate neutrophils, macrophages, a moderate numbers of plasma cells, and small numbers of lymphocytes with no evidence of neoplasia or visible microorganisms. The dog was administered a glucosamine supplement^c (PO q 24 hr) and amoxicillin/clavulanate acid^d (13.4 mg/kg PO q 12 hr for 7 days). Over the subsequent 5 mo, the mass continued to increase in size. Because of the increasing size of the mass, the dog was re-presented to the primary care veterinarian for evaluation. No lameness or pain was reported. Physical exam revealed an 8 cm subcutaneous mass on the right dorsal hip region that was partially fixed to the deeper tissues. Fine needle aspirate was repeated, and the results were similar, including marked mixed inflammation with proteinaceous material consistent with a cyst or edema. Routine complete blood count and serum chemistry panel were unremarkable.

Three-view thoracic radiographs revealed no abnormalities. Contrast computed tomography (CT) of the abdomen and pelvis was performed for surgical planning and staging, revealing an 8.0 × 5.0 × 3.0 cm, well-marginated, heterogeneous, subcutaneous soft-tissue mass overlying the dorsolateral aspect of the gluteal muscles (Figure 1A). Extending from the margins medially were tracts of contrast enhancement described as “tendrils” extending into the adjacent fat (Figure 1B). The adjacent middle gluteal muscle contained isoattenuating nodules, which strongly contrast-enhanced (Figure 1C). No lymphadenopathy of the caudal abdominal and sublumbar lymph nodes or signs of infection were reported by the radiologist. Based on the CT, the primary differential diagnosis was neoplasia such as soft-tissue sarcoma.

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A 14G needle-core biopsy^a from the central portion of the mass was performed at the time of CT. Histopathology of the needle-core biopsy, using standard hematoxylin and eosin staining methods, showed chronic granulomatous inflammation with no evidence of neoplasia, infectious agents, or foreign material and were consistent with a vaccine reaction. Vaccination in the right hind region had last occurred 2 yr prior when the dog received a rabies booster.

The dog was presented to the University of Pennsylvania Ryan Veterinary Hospital’s Surgical Oncology Service 10 days after the CT and needle-core biopsy had been performed. Because of the lack of a definitive histological diagnosis, further biopsy was recommended and a marginal excision of the mass was performed. The resection included the superficial skin, subcutaneous tissue, the underlying muscle fascia, and contrast-enhancing regions of the middle gluteal muscle. The mass was excised with ∼5 mm of subcutaneous fat included in all directions to the level of the middle gluteal muscle. At no point was the lesion’s capsule penetrated during removal (Figure 1C). The region of the middle gluteal muscle was then excised en bloc from the lateral surface of the ilial wing, including the periosteum. The muscle was firm and lobular, but no overt tract was identified as was noted on CT.

After removal, the mass was incised, and a large number of cysticerci exuded from the cut surface (Figure 1D). Samples were submitted for parasitologic analysis, and the remainder of the mass and the deeper muscular samples were submitted for histopathological examination.

The dog recovered uneventfully and was discharged the following day on a 14-day course of praziquantel (5 mg/kg), pyrantel pamoate (5 mg/kg), and febantel^e (30 mg/kg) to be administered orally q 24 hr, fenbendazole^f (50 mg/kg PO q 24 hr for 7 days), carprofen (2 mg/kg PO q 12 hr for 7 days), and codeine (1.6 mg/kg PO q 8–12 hr pro re nata for 3 days). In addition, the dog was administered a consistent regiment of monthly ivermectin/pyrantel pamoate^g and fipronil/(S)-methoprene^h.

Multiple sections from the subcutaneous and deep intramuscular lesions were examined by a board-certified pathologist using standard hematoxylin and eosin staining methods. The histopathologic findings showed severe chronic pyogranulomatous cellulitis and myositis with intralesional cysticerci. Sections from the individual parasites consisted of cysticerci with calcareous corpuscles and cross sections of protoscolices (Figure 2A). Three sections from the deeper subcutaneous lesion consisted of similar sections of cysticerci, some of which contained rows of refractile hooks. The surrounding subcutaneous fat was extensively infiltrated and expanded by pyogranulomas, consisting of neutrophils surrounded by epithelioid macrophages, multinucleated giant cells, and dispersed lymphoplasmacytic infiltrate. Interconnecting bands of fibroplasia and fibrosis encased the inflammatory focus. Sections from the intramuscular region consisted of coalescing inflammatory nodules surrounded by a dense sclerotic collagenous matrix embedded in skeletal muscle. All histologic lesions were compatible with T crassiceps cysticercosis and resulting inflammation (Figure 2).

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The cysticerci found ranged in size from 1.6 to 4 mm in length (Figure 2C), and some were observed to be exogenously budding (Figure 2D). On the larger cysticerci, the protoscolex had four suckers and a rostellum with hooks arranged in two interdigitated rows. A count of the hooks in a histological section of a cysticercus (Figure 2B) showed at least 30 hooks. Four large rostellar hooks and four small hooks on one cysticercus were measured. The average length and standard deviation of the large hooks was 170.4 ± 2.0 μm, and the small hooks measured 134.4 ± 7.1 μm (Figure 2A). The exogenous budding and the number and size of the large and small hooks on the rostellum were within the range of measurements described by Hoberg and consistent with only one North American tapeworm—T crassiceps.^7,8

Recheck examination 14 days after surgery revealed the surgical incision was healing normally. A follow-up phone call with the owner 6 mo after surgery confirmed that there was no visual sign of local recurrence.

Discussion

T crassiceps is a species of tapeworm commonly found in Canada and the northern United States that typically uses rodents (e.g., groundhogs) as intermediate hosts and the gastrointestinal tract of canids (e.g., foxes) as definitive hosts.^2,8,9 The T crassiceps life cycle begins with the adult worm, which resides in the small intestines of its definitive host, typically a wild canid such as the red fox or a wolf.¹⁰ Eggs with oncospheres (usually within proglottids) are shed in the host’s feces. Intermediate hosts, typically rodents, consume the eggs. Once consumed, the oncospheres migrate through the digestive tract of the intermediate host, eventually passing through the intestinal epithelium, where they become embedded in tissues.¹⁰ At that point, the oncospheres differentiate into the larval stage (cysticercus).¹⁰ The T crassiceps life cycle differs from that of other tapeworms in that the larvae divide by budding exogenously within the host. The budding cysticeri multiply while the host walls off the area of infection, leading to, as in this case, a large subcutaneous mass fibrous tissue surrounding the many cysticerci. The life cycle is completed when the intermediate host is consumed by the definitive host (canids) and the cysticercus develops to the adult worm in the lumen of the small intestine. The prepatent period for T crassiceps is 5 wk.⁹

There have only been two previous reports of T crassiceps cysticercosis in dogs and one in a cat within North America. The first report featured fatal intrapleural and intraperitoneal cysticerci in an apparently immunocompromised dog.⁸ The second report described subcutaneous cysticercosis on the medial thigh in an apparently healthy adult dog.⁴ Fatal cerebral cysticercosis by T crassiceps has also been documented in a domestic cat.¹¹

The point of exposure for the dog in this report was unknown. It was suspected that the dog may have ingested contaminated fox feces, because the dog had a history of coprophagia, and the owner reported having seen foxes and fox droppings in the yard frequently.

On two separate occasions, while the mass was present, fecal flotation was performed, but no ova or parasites were detected. This is not necessarily surprising because the most commonly used fecal flotation solutions (zinc sulphate or sodium nitrate) do not rule out tapeworm infection because the eggs are usually contained within proglottids, which do not float. Additionally, Taenia eggs have a specific gravity of 1.23, making them too dense to float in some solutions.¹² As a consequence of the negative flotation results, the dog was not dewormed, and the owner reported that they stopped monitoring the dog’s stool. As stated previously, the dog was on year-round ivermectin/pyrantel pamoate and fipronil/(S)-methoprene; however, these preventives are ineffective against tapeworms.

T crassiceps exposure may occur in domestic dogs through ingestion of T crassiceps eggs present in the environment or through the ingestion of an infected rodent.⁴ Although it is thought that ingestion of cysticeri from an intermediate host will lead to adult worms in the small intestine of a dog, ingestion of eggs might lead to cysticercosis.

Published reports of subcutaneous T crassiceps cysticercosis in humans link infection with immunosuppression.¹¹ The dog reported here had a history of suspected environmental allergies that were being managed with oclacitinib maleate (0.6 mg/kg PO q 24 hr), which the dog had been receiving for ∼5 yr. Oclacitinib maleate is a small molecule inhibitor of the Janus kinase 1 and 3 tyrosine kinases, which inhibit the downstream production of inflammatory and allergy/atopy-associated cytokines such as interleukin (IL)-2, IL-4, IL-6, and IL-13 involved in allergy, inflammation, and pruritus.¹³ It is unclear what effect this drug may have had, if any, in modulating the dog’s immune system allowing the T crassiceps cysticercosis to develop and progress.

The dog was treated with anthelmintics, including an extended 2 wk course of praziquantel (5 mg/kg), pyrantel pamoate (5 mg/kg), and febantel (30 mg/kg), and a 5-day course of fenbendazole (50 mg/kg PO q 24 hr). Because there is no documented treatment recommendation for T crassiceps cysticercosis in dogs, the treatment recommendation for Taenia intestinal infections in dogs was adapted and extended in order to achieve tissue penetration. The dog remained on oclacitinib maleate during and after treatment. Recommendations to check fecal samples, monitor stool for proglottids, and watch the excision site for swelling were made.

The dog had no local recurrence or any additional concerns 6 mo after surgical excision of the mass followed by the extended course of anthelmintics. Upon surgical excision, it was noted that the mass was encapsulated; thus, it is hypothesized that anthelmintic treatment alone would not have penetrated the source of infection. The combination of surgical excision and medical management was likely needed in order to successfully treat the dog. If a diagnosis was obtained during the earlier diagnostics of fine needle aspirates or biopsy, medical management could have been attempted first, and if no improvement was observed, marginal excision of the mass could have been performed.

Conclusion

Cysticercosis should be considered as a differential diagnosis for progressively enlarging subcutaneous masses in dogs living in Canada or the northern United States with a previous history of fecal tapeworm infection or coprophagia and exposure to rodents or foxes. Making the diagnosis can be challenging because of the difficulty identifying the parasite on routine fecal flotation as well as on cytology or needle core biopsy samples. Empirical anthelmintic therapy should be considered if there is suspicion for tapeworms in the stool; however, the effectiveness of medical therapy alone for encapsulated mass lesions, as described here, is unknown. Based on the successful treatment of T crassiceps cysticercosis in this dog, marginal surgical resection combined with anthelmintic therapy is the recommended treatment.