Introduction

The typical manifestation of canine heartworm infection includes the presence of heartworms within the pulmonary artery and, occasionally, the right ventricle.¹ However, adult worms have been reported in aberrant locations as early as 1856.² Such locations include the eye, peritoneal cavity, subcutis, skeletal muscle, systemic arteries and central nervous system.^3–15 Three case reports in dogs have documented the presence of an adult heartworm in the epidural space, causing paresis or paralysis.^11–13 These reports have relied on survey radiographs and myelography to diagnose the lesion prior to surgery. A recent report of dirofilariasis in the epidural space of a cat was diagnosed using magnetic resonance imaging (MRI).¹⁶ This is the first report of an intradural heartworm in a dog, and the first reported MRI findings associated with spinal canine dirofilariasis.

Case Report

A 7 yr old female spayed Yorkshire terrier presented for 5 mo of chronic waxing and waning cervical spinal pain manifested as low head carriage, reluctance to use the stairs, a stiff gait, and hyperpathia. The dog had no prior longstanding history of illness, no travel history, and was up to date with vaccines. The dog was prescribed monthly selamectin^a as heartworm preventative, but the owner occasionally missed doses. She had last been normal 5 mo earlier when she fell while playing ball, and was suspected to have an acute injury. The original physical exam performed by the referring veterinarian showed consistent cervical spinal pain. The patient weighed 2.5 kg and was started on methocarbamol^b 25 mg/kg per os q 12 hr for 14 days. A mild improvement was seen, but signs continued to wax and wane. Complete blood count and serum biochemistry values were all within normal limits. Survey thoracic radiographs that incorporated the cervical spine did not show vertebral body abnormalities or disc space compression to explain the underlying cause. The cardiac silhouette was normal, but the pulmonary arteries were interpreted as mildly enlarged. A mild diffuse bronchiolar pattern was present. The dog was then started on prednisone^c 0.5 mg/kg per os q 12 hr and tramadol^d 5 mg/kg per os q 12 hr in addition to the methocarbamol for several wk. No improvement was noted, and the dog was referred to the neurology service at the author's practice. Physical exam was normal and neurologic exam demonstrated cranial cervical hyperpathia but no neurologic deficits.

The dog was anesthetized for cervical MRI evaluation. A high field (1.5 T) magnet^e was used to obtain turbo spin-echo T2-weighted and spin-echo T1-weighted sequences in the sagittal and transverse planes. Spin-echo T1-weighted sequences after intravenous injection of contrast medium^f were also performed. MRI revealed a discrete 1.2cm x 0.2cm x 0.6cm (LxWxH), broad based, complexly intense intradural extramedullary lesion at the left lateral aspect of the vertebral canal at the level of C2 vertebra. The lesion was hyperintense on T2-weighted images. In the sagittal view, the lesion appears as a hyperintense blush along the left dorsal and lateral margin of the cord above C2, extending slightly caudal to C2-C3 articulation. On the transverse view, the lesion had an isolated irregular hyperintense focus that contained several pinpoint isointensities scattered within. Mild spinal cord compression was seen in this view with no associated signal change (Figure 1). The lesion was faintly hyperintense on T1-weighted images. After intravenous contrast administration, the lesion enhanced strongly and unevenly. On the sagittal view, there was a broad-based area of contrast enhancement along the left lateral cord that contained curvilinear filling defects present in a serpentine pattern. On the post-contrast transverse view, the lesion was again hyperintense with tiny circular filling defects seen within the contrast (Figure 2). Based on the MRI findings, the primary differential was a meningioma. Meningiomas are the most common tumor in the intradural/extramedullary location and typically have strong uniform contrast enhancement.^17,18 Other differentials for the MRI findings included a malignant nerve sheath tumor, lymphoma, sarcoma, secondary metastatic tumor, or granuloma.^17,19,20

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The patient was hospitalized and administered methylprednisolone sodium succinate^g 7.5 mg/kg IV q 12 hr, gabapentin^h 40 mg/kg per os q 12 hr, and tramadol 2 mg/kg per os q 12 hr as symptomatic treatment until surgery could be performed. A left-sided hemilaminectomy at the level of C2 was performed. A long, narrow, white nematode emerged after durotomy (Figure 3) and was gently removed. The dura was not thickened and no other abnormalities with the spinal cord were noted after worm removal. Complete decompression was achieved. The parasite was submitted for identification and was confirmed to be an adult male D. immitis. A heartworm antigen test was also submitted and tested positive for female heartworm antigens.

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The dog's cervical pain improved rapidly after surgery. She was discharged from the hospital 3 days postoperatively with oral buprenorphineⁱ 0.015 mg/kg q 8 hr. Due to the heartworm infection, one dose of selamectin^a 30mg was administered topically and 30 days of doxycycline^j 10 mg/kg q 24 hr was prescribed. Recheck physical exam 10 days following surgery was normal, and the dog was acting normally at home.

Two wk following surgery, an echocardiogram was performed to evaluate for the presence of additional heartworms and to obtain additional recommendations regarding heartworm treatment. Measurement of all cardiac chambers and valvular function were normal. There was no evidence of pulmonary hypertension. At least two heartworms were visualized in the distal main pulmonary artery. In addition to the doxycycline prescribed previously, a split adulticide protocol using melarsomine dichlorhydrate^k was recommended. Follow-up phone communication was performed 1 mo later. The owner reported the dog felt normal, but had not scheduled adulticide treatment.

Discussion

Similar to the previous report of canine cervical spinal D. immitis in which the dog had chronic recurrent tetraparesis, this dog had chronic recurring pain with a fast and complete recovery following surgery.¹¹ In the other two cases, the dogs developed acute non-ambulatory paraparesis.^12,13 The location of the parasite in these dogs was the thoracolumbar spine, and the site of surgery in each of these dogs had extensive inflammatory lesions associated with the infection. One dog was ambulatory following surgery; the other was euthanized due to lack of neurologic improvement postoperatively. Overall, dogs are able to recover well after surgery, regardless of the chronicity of infection. The outcome appears to be dependent on the severity of inflammation associated with the infection and the severity of the neurologic deficits at presentation.

The route of entry of D. immitis into the dura of this dog could not be determined by MRI or at surgery. The mechanism for how adult worms migrate to aberrant locations has yet to be elucidated. Third and fourth stage larvae are thought to be too large to flow through a capillary bed, but adult heartworms lack the mechanical structures necessary to penetrate and migrate through vessel walls.^2,5 Hypotheses regarding the route of entry into the epidural space have included recent migration as an adult or larval migration to the vicinity with the last molt and subsequent local maturation.^11,12 In cats, the occurrence of D. immitis in the brain is well documented.^15,21–23 However, there is only one report of its presence within the spinal cord.¹⁶ It was proposed in that report that the smaller size of cat spinal vessels prevent filarial nematode migration.

Reported locations of adult D. immitis in the central nervous system of dogs are limited to cerebral ventricles, cerebral subarachnoid space, posterior communicating artery, anterior middle and posterior cerebral arteries, the basilar artery, and the spinal epidural space.^{11–13,15,21,24} The three cases of spinal D. immitis were reported in the 1980s, during which time the most effective diagnostic imaging tools were limited to survey radiographs and contrast myelography, but MRI is the current and preferred diagnostic tool to investigate the CNS. To the author's knowledge, the only MRI description of an aberrant heartworm infection is in the epidural space of the lumbar spine of a cat.¹⁶ This lesion was described as a hyperintense extradural mass on T2-weighted images.¹⁶ It was a well-defined, heterogeneous hypointensity on T1-weighted images, and had heterogeneous contrast enhancement.¹⁶ In this dog, the contrast has tiny, hole-like filling defects that are suspected to represent the worm coiled up within the dura. Therefore, it could be argued that the heterogeneity and complexity of the enhancement should raise the clinician's suspicion of heartworm infection.

In the United States, heartworm prevention is considered part of routine veterinary care, which has minimized the prevalence of heartworm infection. However, active D. immitis infections are still commonly seen in the United States, and the occurence of infection is increasing throughout the world.²⁶ Veterinarians should be aware of the new manifestations of heartworm disease, including signs of aberrant infection and migration.

Conclusion

The imaging findings in this case of D. immitis infection show an irregular, complexly intense soft tissue lesion that strongly enhances with contrast. Unlike tumors that typically have more uniform enhancement, this lesion had unique filling defects within the contrast.¹⁸ These complexities in shape and enhancement may be considerations to include D. immitis infection to the more common list differentials for lesions in the intradural extramedullary location. A positive heartworm test may also raise the index of suspicion. However, surgical exploration is necessary to obtain a definitive diagnosis. Clinical improvement described in the current patient is similar to prior reports, supporting the author's belief that this infection can have a favorable prognosis with surgical treatment.