Conference 01 - 2014 Case: 01 20140903

Signalment:

A 7-year-old intact male German shepherd dog.A 7-year-old intact male German shepherd dog was presented with hind limb paresis of 3 days duration and back pain. The referring veterinarian had treated the dog with prednisone and cephalexin for 3 days but the dog had deteriorated neurologically despite treatment. Neurological examination at presentation revealed paralysis of the right hind limb and paresis with minimal voluntary movement of the left hind limb. The dog appeared to be mainly in pain during postural shifts. All spinal reflexes were absent in the right hind limb. A weak withdrawal reflex was detected in the left hind limb. The neuroanatomic diagnosis was a lesion located in L4-S1 spinal cord segments and more severe on the right side. MRI examination was done 4 days post-admission and demonstrated an intramedullary increased signal intensity from the conus medularis to the level of L1. A surgical intervention was attempted but the dogs condition continued to deteriorate and it was euthanized. Most of the slides submitted are from this case (Ex57G). Additional slides are from another dog with a history of acute progressive paraparesis and severe back pain beginning 3 days before presentation (Ex57B).

Gross Description:

At necropsy, following incision of the dura, a single nematode was found embedded in the spinal parenchyma at L1 L2 spinal segments on the left. Transverse sections of the spinal cord showed macroscopic changes from the caudal thoracic to the lumbar area. There were multiple, randomly distributed foci of hemorrhage and necrosis with or without cavitation involving the gray and white matter. The lumbar segment was the most severely affected. Many necrohemorrhagic foci were continuous through multiple transverse sections and formed one or more tracts. The lesion was mostly located on the right side of the cord but moved to the left at L1-L2. Similar lesions were seen in the second case.

Histopathologic Description:

In a random distribution within the white matter, there are several foci of necrosis and acute hemorrhage with mild gitter cell and variable neutrophilic infiltration. In the tissue around the tract, astrocytes show mild hypertrophy. Scattered vacuoles, some containing swollen axons (spheroids) and other cellular debris, are present in the white matter near the necrotic foci as well as further away. There is slight hemorrhage and mild gitter cell infiltration in the meninges within the ventral median fissure of one sample (lumbar intumescence). In another sample, there is widespread hemorrhage in the connective tissue external to the dura mater. There are several sections of a nematode with a smooth cuticle, coelomyarian-polymyarian muscles, large lateral hypodermal chords, abundant amphophilic to basophilic fluid in the pseudocoelom and an intestine composed of individual cuboidal cells, each with a prominent brush border. These features are typical of an adult spirurid, including Spirocerca lupin. Unfortunately, the parasite was dislodged during tissue processing. Sections from the second block (Ex57B) show a similar lesion but in this sample the tracts are present in the gray and white matter and there is mild to moderate inflammatory infiltration. Within one of the tracts there is a single transverse section at the level of the esophagus of a nematode with morphologic features as described above.

Morphologic Diagnosis:

Spinal cord: Multifocal necrosis and hemorrhage with mild acute histiocytic and neutrophilic meningomyelitis and intralesional spirurid nematode.

Lab Results:

CBC and serum biochemistry were unremarkable. Serological tests for Toxoplasma gondii and Neospora caninum were negative. Fecal flotation yielded S. lupi eggs. CSF analysis revealed mild mixed pleocytosis (40 cells/μl, reference interval: 0-8 cells/μl) with neutrophils (65%) and eosinophils (35%), and protein concentration of 22 mg/dl (RI: <25 mg/dl). Endoscopy demonstrated 3 typical S. lupi nodules in the caudal esophagus.

Condition:

Spirocerca lupi

Contributor Comment:

Spirocerca lupin is primarily a parasite of dogs. Its distribution is worldwide but it is most prevalent in warm climates. Adult parasites live in a nodular mass in the esophageal wall of the host. The female lays embryonated eggs which are transferred through a tract in the nodules and excreted with feces. The eggs are ingested by an intermediate host, corprophagus beetles, and develop to infective L3 within 2 months.

Carnivores are infected by ingestion of the beetles or a variety of paratenic hosts (birds, lizards, mice, rabbits etc.). In the carnivore host, the infective larvae penetrate the gastric mucosa and migrate within the walls of the gastric arteries to the thoracic aorta. About 3 months post-infection the larvae leave the aorta and migrate to the esophagus where they incite the development of fibro-inflammatory tissue (granulomas) as they mature to adults over the next 3 months. Lesions associated with S. lupi infestation are mainly due to migration and persistence of the parasite in tissues. Esophageal nodular masses (granulomas) and aortic scars and aneurysms are the most common lesions. Other lesions include spondylitis and spondylosis of the caudal thoracic vertebrae, neoplastic transformation of the esophageal granulomas, hypertrophic osteopathy, and aberrant migration into a wide variety of tissues including thoracic viscera, GIT, urinary system and subcutaneous tissue.(5)

More recently, several reports from Israel and South Africa describe aberrant migration into the spinal cord.(1,2,3) In one report (n=4) S. lupi was located in the extradural space and elicited signs typical of thoracolumbar IVD prolapse or spinal trauma.(2) In the remaining cases (n=5), tracts were present within the spinal cord as in the two cases used here.(2,3) Although confirmation of the diagnosis is difficult in cases which recover, the neurologists at the Veterinary School of the Hebrew University estimate that in the past 2-3 years, approximately 10-15 cases are seen annually (Dr. Orit Chai, personal communication). The reason for the increase in the occurrence of this form of canine spirocercosis is unknown but it may in part be attributable to failure in making the correct diagnosis in the past. Currently, a tentative diagnosis is based on the neurological signs, eosinophilic CSF pleocytosis and evidence of S. lupi infection in other tissues (by thoracic radiography, esophagoscopy and fecal floatation). The presenting signs of an acute nonsymmetrical paraparesis / plegia and high CSF eosinophil counts, observed in the present case, are similar to previously reported spinal intramedullary spirocercosis cases.(1)

The cause of aberrant migration of S. lupi is unknown. It has been suggested that aberrant migration occurs when a worm in the thoracic arterial wall enters the intercostal arteries and through their spinal branches arrives at the extradural space. To enter the spinal cord it must then further penetrate the dura mater and the leptomeninges. The location reported in most intradural and extradural cases is T4-L1. In this region the aorta lies closely parallel to the vertebral column and the intercostal arteries supply the spinal branches that enter the spinal canal via the intervertebral foramina.(3)

Verminous encephalomyelitis may arise from aberrant wanderings of a parasite within its normal host (e.g., Dirofilaria immitis in the CNS of dogs and cats and Strongylus vulgaris in the brain of horses); or more commonly, infection of an aberrant host (e.g., Paralephastrongylus tenuis, the meningeal worm of white-tailed deer infesting sheep, goats and other herbivores). Other than regions where S. lupi is prevalent, cerebrospinal helminthosis is uncommon in dogs and cats. Nematodes, which may cause aberrant migration into the CNS of dogs include Angiostrongylus cantonensis in Australia, Angiostrongylus vasorum and Dirofilaria immitis.(6) There is a report of neurologic dysfunction in 3 dogs due to intracranial hemorrhage from consumptive coagulopathy associated with Angiostrongylus vasorum infection of the lung.(3)

JPC Diagnosis:

Spinal cord: Meningomyelitis, necrotizing, eosinophilic, multifocal, marked, with adult spirurid nematode.

Conference Comment:

This is an excellent example of aberrant migration in a normal host of a common and readily identifiable nematode. Conference participants reviewed the features of nematodes on histologic section of which they used the coelomyarian-polymyarian musculature that projects into the pseudocoelom, prominent lateral chords and eosinophilic material within the pseudocoelom in the present case to facilitate identification of a spirurid nematode, specifically Spirocerca lupi. Other spirurids of veterinary importance include: Trichospirura leptostoma inhabiting pancreatic ducts of the common marmoset, Physaloptera spp. residing in the stomach of many mammals, Draschia megastoma in the stomach of horses, and Gongylonema spp. found in the many different tissues and species.

The contributor provides an excellent overview of the complex pathogenesis of Spirocerca and appropriately conveys the tremendous variety of lesions associated with infection. Of significance is the pathognomonic lesion of thoracic spondylitis and its ability to induce malignant transformation, with esophageal fibrosarcoma or osteosarcoma being most characteristic.(7) This ability is not exclusive to Spirocerca, however. The acronym SOCCS-T is often used at JPC to facilitate remembering the following neoplasm-inducing parasites: Spirocerca lupi, Opisthorchis felineus (cholangiocarcinoma in cats and people), Cysticercus fasciolaris (hepatic sarcoma in rats), Clonorchis sinensis (cholangiocarcinoma in cats and people), Schistosoma hematobium (transitional cell carcinoma of urinary bladder in people) and Trichosomoides crassicauda (papillomas of rat urothelium).

Just as the contributor noted, it is the extensive migration of Spirocerca which most commonly causes lesions, as was the case in this dramatic example. Up to 80% of the section of spinal cord was affected in some slides, leading participants to speculate on how rapid the migration must have occurred to cause such extensive lesions in a relatively short period of time. Conference participants also discussed the clinicopathologic findings of pleocytosis, along with elevated neutrophils, eosinophils and protein, as expected findings of a cerebrospinal fluid analysis in this case. This is to contrast with an albuminocytologic dissociation, in which elevated protein levels does not accompany pleocytosis (seen with neoplastic or degenerative diseases such as Guillain-Barre syndrome in people).

References:

1. Chai O, Shelef I, Brenner O, Dogadkin O, Aroch I, Shamir MH. Magnetic resonance imaging findings of spinal intramedullary sprocercosis. Vet Radiol Ultrasound. 2008;49:456-9.

2. Du Plessis CJ, Keller N, Millward IR. Aberrant extradural spinal migration of Spirocerca lupi: four dogs. J Small Anim Pract. 2007;48:275-278.

3. Dvir E, Perl S, Loeb E, et al. Spinal intramedullary aberrant Spirocerca lupi migration in three dogs. J Vet Intern Med. 2007;21:860-864.

4. Garosi LS, Platt SR, McConnell JF, Wray JD, Smith KC. Intracranial hemorrhage associated with Angiostrongylus vasorum infection in three dogs. J Small Anim Pract. 2005;46:93-99.

5. Mazaki-Tovi M, Baneth G, Aroch I, et al. Canine spirocercosis: Clinical, diagnostic, pathologic and epidemiologic characteristics. Vet Parasitol. 2002;107:235-250.

6. Summers BA. Inflammatory diseases of the central nervous system. In: Summers BA, Cummings JF, de LaHunta A, eds. Veterinary Neuropathology. St. Louis, MO: Mosby-Year Book; 1995:159-162.

7. Van der Merwe LL, Kirberger RM, Clift S, Williams M, Keller N, Naidoo V. Spirocerca lupi infection in the dog: a review. Vet J. 2008;176(3):294-309.