Brainstem Parelaphostrongylus tenuis in a domestic sheep
Latasha Ludwig, Hugh Cai, Lisa Ledger, Brandon Lillie
Department of Pathobiology, University of Guelph, Guelph, ON (Ludwig, Lillie); Animal Health Laboratory, University of Guelph, Guelph, ON (Cai, Ledger).
AHL Newsletter 2021;25(1):8.
A 2.8-year-old, intact female Katahdin sheep presented to the Large Animal Clinic of the Ontario Veterinary College’s (OVC) Health Sciences Center with a several day history of ataxia and eventual recumbency. Initial clinical signs were reported as repeated falling to the left. The sheep was treated with oxytetracycline and thiamine with minimal improvement, and the condition progressed to lateral recumbency. Three other sheep on the farm showed similar clinical signs, one of which died prior to treatment, while two others were treated with thiamine, oxytetracycline, and multivitamins and recovered. All sheep on the farm were on a forage-only diet. Though on similar feed and housing, this animal was not in direct contact with the other affected sheep.
On presentation to OVC, the sheep was dull and obtuse but responsive to external stimuli with an elevated respiratory rate (48 breaths/minute), tacky and pale pink mucous membranes, a slightly delayed capillary refill time (~2 seconds), struggled to lift herself into sternal recumbency and had multiple cranial nerve deficits. In hospital, she repeatedly struggled with an increased respiratory rate with lung consolidation present on thoracic ultrasound which was attributed to the lateral recumbency. On the second day of hospitalization, signs consistent with a seizure began, and they occurred multiple times while in hospital. She was treated with intravenous fluids, oxytetracycline, systemic anti-inflammatories, gabapentin, diazepam, thiamine, gastroprotectants, and oxygen therapy. Approximately two days after presentation, humane euthanasia was elected due to poor prognosis.
On necropsy, there was a large amount of foam in the trachea, and the lungs were heavy and wet with some separation of the septa by edema. On the left ventral side of the caudal brainstem was an approximately 1.5 cm diameter area of hemorrhage. No other gross findings were appreciated on necropsy. Histologically, within the cerebellar peduncle of the brain, there was a focal area characterized by perivascular cuffs of eosinophils (confirmed by Luna stain), lymphocytes, and plasma cells. The neuroparenchyma in this area was vacuolated with swollen axons and aggregates of foamy macrophages. On further sectioning of the brainstem to target the area of focal hemorrhage, multiple profiles (cross and longitudinal sections) of a nematode were present focally replacing the neuroparenchyma in the cerebellar peduncle (Fig. 1). The parasite had a body cavity enclosed within a thin cuticle with accessory hypodermal cords and polymyarian-coelomyarian musculature. The intestine was large and composed of a few multinucleated cells (Fig. 1 inset) and there was also a reproductive tract. These features are consistent with Parelaphostrongylus sp., suspected to be P. tenuis based on the location.
To confirm the identity of the parasite, DNA sequencing was pursued. The formalin-fixed paraffin-embedded block was manually cored using a 0.6 mm punch to obtain the parasite with minimal surrounding ovine brain tissue. Initially, universal ribosomal internal transcribed spacer (ITS) region primers produced a positive band of the correct size by gel electrophoresis, but there was insufficient concentration to allow sequencing. Parelaphostrongylus-specific primers, as previously described (1,2) were used to obtain a sufficient product that was sent for sequencing. There was 100% sequence similarity (156/156 bp) to a partial segment of the ITS2 (second internal transcribed spaces of the ribosomal RNA gene) region of both P. tenuis and P. andersoni. This supports an etiologic diagnosis of P. tenuis since the brain, rather than muscle was affected (as would be expected with P. andersoni), and explained the clinical signs demonstrated by this sheep. It is unknown whether the other sheep were also affected by this parasite, as no follow-up testing was pursued in these animals.
P. tenuis most commonly infects white-tailed deer (Odocoileus virginianus) and generally produces no clinical signs in this species. The nematodes complete their life cycle and generate first stage larvae that are expelled in the feces. These larvae enter gastropods (slugs, snails), their intermediate hosts, where they develop into infective third stage larvae. The intermediate host is then ingested by either white-tailed deer, where they complete their cycle, or abnormal hosts, where clinical disease is most commonly seen. Following ingestion, the larvae exit the stomach and migrate aberrantly, most commonly into the spinal cord or less frequently, into the brain (3). These aberrant migrations have been reported in a variety of species, including sheep, with camelids reported to be most susceptible and cattle most resistant (3). Postmortem diagnosis can be difficult as the parasite is not commonly found in histologic sections and therefore, it is often presumptive based on clinical signs, cerebrospinal fluid analyses, response to therapy, and/or characteristic focal inflammatory lesions in the brain (2,3). AHL
Figure 1. Replacing the neuroparenchyma are multiple cross and longitudinal sections of a nematode parasite consistent with Parelaphostrongylus tenuis (inset: higher magnification of the parasite, arrows indicating the multinucleated intestine). (H&E)
1. Tanabe M et al. Molecular confirmation of Parelaphostrongylus tenuis infection in a horse with verminous encephalitis. Vet Pathol 2010;47(4):759.
2. Mitchell KJ et al. Diagnosis of Parelaphostrongylus spp. infection as a cause of meningomyelitis in calves. J Vet Diagn Invest 2011;23(6):1097-1103.
3. Nagy DW. Parelaphostrongylus tenuis and other parasitic diseases of the ruminant nervous system. Vet Clin Food Anim 2004;20:393-412.