Discussion

Among the elaphostrongyline metastrongyloid nematodes found in North America, there are 3 species of Parelaphostrongylus; all 3 are extrapulmonary parasites of definitive ungulate hosts, which include cervids and bovids.^1–3 Among these 3 parasites, P tenuis is relatively large; males are typically up to 62 mm (range, 31 to 62 mm) in length, are anatomically equipped with spicules that typically exceed 200 μm (range, 202 to 249 μm) in length, and have a gubernaculum > 100 μm (range, 89 to 137 μm) in length.⁴ In contrast, specimens of Parelaphostrongylus andersoni found in white-tailed deer (Odocoileus virginianus) are 22 mm in length and have spicules that do not reach > 115 μm in length. Mature males of Parelaphostrongylus odocoilei found in Dall's sheep (Ovis dalli) are up to 36 mm in length, but they are slightly smaller in black-tailed deer (Odocoileus hemionus columbianus). Spicule length typical of P odocoilei may approach that observed in P tenuis, but they do not reach > 165 μm in length.⁵ Additionally, the parasite in the horse reported here should not be classified as P odocoilei because the geographic range for P odocoilei is restricted to northwestern North America.⁶ The only other elaphostrongyline of consideration in the horse of the present report is Elaphostrongylus rangiferi. However, records indicate that these parasites, which were previously introduced in cervids, remain geographically restricted to Newfoundland.² For typical E rangiferi, total body length would be similar to that of P tenuis but these species would be distinguishable on the basis of structural differences of the spicules and gubernaculum. The parasite in the present report was identified as P tenuis on the basis of structural characteristics of the preserved specimen, compared with the characteristics of parasites in another description,⁴ and in conjunction with the geographic location of the horse (ie, Wisconsin).

A commercially available antemortem diagnostic procedure for P tenuis does not exist for hosts other than cervids. An ELISA can be used to reliably detect serum anti-excretory–secretory antigen antibodies from third-stage larvae in white-tailed deer and elk (Cervus elaphus) within 2 weeks after infection.⁷ However, necropsy and recovery of adult P tenuis remain the only diagnostic tools for identifying infections in noncervid hosts. In the event that parasites are recovered that cannot be identified on the basis of morphological methods, classification should be possible by use of various molecular diagnostic techniques.^8,9

Parelaphostrongylus tenuis (meningeal worm) is considered to be a common (prevalence of up to 86%) neurotropic parasite in white-tailed deer in parts of the United States, including eastern to central North America.^1–3,10 The life cycle of P tenuis has been described elsewhere.^1,2 In white-tailed deer, the adult stage of P tenuis resides in the subarachnoid space and venous sinuses of the brain. Females lay eggs that enter the circulation and are carried to the lungs where they become lodged in alveolar capillaries. The first-stage (dorsal-spined) larvae develop within the eggs, hatch, and penetrate the pulmonary parenchyma to enter the alveoli and migrate along the trachea in an orad direction. The larvae are expectorated from the trachea into the pharynx, swallowed, and excreted in the feces. Then, the first-stage larvae penetrate the foot of a gastropod, which is the obligatory intermediate host. Within the gastropod, the first-stage larva develops into a third-stage larva. Infection with P tenuis results when an infected gastropod is ingested by ungulates during grazing activities. The third-stage larva is released into the abomasum or stomach of the host and migrates through the host tissues to the CNS. In white-tailed deer, the larvae migrate cranially through the gray matter of the spinal cord and into the brain where they mature into adult parasites.

Meningeal worm infection in white-tailed deer generally results in a subclinical condition; however, migration through the CNS in atypical hosts results in a variety of clinical neurologic abnormalities. Infection in atypical hosts, such as bovids and camelids, has been reported.^1,11,12 In hosts other than white-tailed deer, parasites develop (to varying degrees) in extrapulmonary sites, including the CNS, without becoming a patent infection. Nonpatent infections of these hosts cannot be diagnosed by techniques such as fecal flotation or Baermann funnel methods. Nonpatent infections in atypical hosts have been acquired by domestic or free-ranging ungulates that share a common range with white-tailed deer, including game farms or zoos, and where ingestion of gastropod intermediate hosts provides a source of infective larvae for transmission.² The horse of the present report had no history of exposure, and it was not housed in environmental conditions that would typically indicate a readily identifiable route for infection by P tenuis. The horse was pastured only with other horses, and the hay that was fed to the affected horse had been purchased from a farm that raised only cattle and horses. However, because P tenuis–infected white-tailed deer are quite prevalent throughout the range distribution, it is conceivable that infected gastropods may have been in the pasture or perhaps were even trapped in the hay during the baling process. The detection of vitreal changes in the right eye of the horse reported here indicates that this larva likely gained access to the anterior chamber of the eye via migration from the posterior segment.

To our knowledge, only 1 report¹³ of a confirmed infection in an equine host by a protostrongylid nematode (presumed to be P tenuis) exists. A 6-month-old Arabian was examined after an acute onset of clinical neurologic abnormalities (ie, abnormal gait and head tilt). Numerous eggs and nematode larvae were identified microscopically within the cerebellum during histologic examination.¹³ Thus, our report appears to be the first in which there was a confirmed intraocular infection of a horse by P tenuis. Furthermore, our report is the first to provide a description of an affected eye that retained vision after infection.

The first report¹⁴ of a presumed intraocular P tenuis infection was in a 10-month-old female eland (Taurotragus oryx) with progressive, unilateral uveitis of 5 weeks' duration that was nonresponsive to aggressive medical treatment. Unilateral enucleation was performed to alleviate patient discomfort. Histologic examination of that eye revealed marked uveitis and choroiditis, and multiple sections of nematode larvae were detected in the posterior segment near the retina and choroid of the eye. On the basis of morphological characteristics, the nematode was presumably classified as P tenuis; however, this was never definitively confirmed.¹⁴ Clinical manifestation of the intraocular P tenuis infection in that eland is quite dissimilar, compared with that of the horse reported here. We believe that the noninflamed appearance of the horse's eye was attributable to infection by an intact, viable nematode. Furthermore, it may be concluded that if the nematode were to have died in an intraocular location, then a dramatic panuveitis possibly would have ensued.

Although the intraocular infection by the nematode in the horse reported here is unusual, ocular lesions caused by migration of species of neurotropic metastrongyloid nematodes have been reported as a sequela in a number of instances. The most commonly reported are caused by Angiostrongylus cantonensis in humans.¹⁵ Angiostrongylus cantonensis is a parasite of rats that migrates through the brain after ingestion of a gastropod intermediate host and eventually infects the vascular system of the rat's lungs as an adult parasite. In 16% of humans infected with this parasite, ocular lesions, which often include young adult nematodes, have been detected in both the anterior and posterior chambers of the eye.¹⁵ In a report¹⁶ of 3 affected humans from Thailand, 1 live parasite was found in the anterior chamber, vitreous body, or subretinal space of the eye in each person. To our knowledge, A cantonensis infections in dogs from Southeast Asia and Australia have not been associated with ocular sites.^17,18 Angiostrongylus cantonensis is endemic in the rat population of the southern United States.¹⁹ Therefore, similar cases might be reported in this region. In Europe, infections with Angiostrongylus vasorum in the eyes of dogs have been reported²⁰ to consist of developing stages of the parasite. In another report,²¹ a parasite was removed from the anterior chamber of the eye of a cat in Vancouver, BC, Canada, but it could not be classified to a genus. Because of the reported²² efficacy against the neurotropic stages of A cantonensis in rats, some protection from infection might be provided to cats and dogs through monthly topical administration of moxidectin.

Infection with P tenuis appears to be extremely rare in horses. However, P tenuis infection should be considered when an intraocular parasite is identified in a horse, regardless of concurrent clinical signs (or lack thereof) of neurologic disease.