Baylisascaris procyonis encephalitis in Patagonian conures (Cyanoliseus patagonus), crested screamers (Chauna torquata), and a western Canadian porcupine (Erethizon dorsatum epixanthus) in a Manitoba zoo

Abstract

Neurological disease occurred in 4 Patagonian conures (Cyanoliseus patagonus), 2 crested screamer chicks (Chauna torquata), and 1 western Canadian porcupine (Erethizon dorsatum epixanthus) at a Manitoba zoo. Baylisascaris procyonis, the common raccoon roundworm, not previously identified in Manitoba, is considered the likely cause of neural larval migrans in these cases.

In 2006, a 14-year-old, male, Patagonian conure (Cyanoliseus patagonus) was euthanized at the Assiniboine Park Zoo in Winnipeg, Manitoba, after becoming progressively ataxic over a period of 3 wk. At gross necropsy, no significant abnormalities were found. Histological examination of the brain revealed a cross-section of a single nematode larva embedded in the neuropil. A similar case occurred at the zoo approximately 1 mo later in a clutch of 3-week-old crested screamer chicks (Chauna torquata). The 1st female chick, showing signs of ataxia, died following treatment and care, while the 2nd chick, also female, was euthanized after presenting similar signs. No significant findings were present upon gross postmortem examination. Parasitic larvae found in the brain sections of the conure and both chicks were morphologically compatible with a Baylisascaris sp.

The following year, a 4-year-old, male, porcupine (Erethizon dorsatum epixanthus) that was hand-raised at the zoo from the age of 7 wk was euthanized after failing to show clinical improvement of neurological signs that were affecting mobility. These signs had persisted for several months. Gross postmortem examination revealed only white segmented cestodes (Monoecocestus sp.) in the lumen of the small intestine. Histologically, a longitudinal section of a larval nematode (Baylisascaris sp.) was observed in the brain.

Baylisascaris procyonis is considered the cause of the fatal neurological disease in all cases, based on the histological appearance of the larvae, the exposure of the animals to raccoons on zoo grounds, and the presence of the parasite in raccoons live-trapped on the property.

CASE DESCRIPTIONS

A Patagonian conure, along with 4 others, arrived at the zoo in 2001. Upon arrival, this individual had a subluxated left elbow that was later reduced. Otherwise, the group did very well until late 2005. At this time, 4 of the 5 birds became progressively ataxic over a 3-week period. Three of the birds died, but 1 bird did improve over approximately 4 wk to the extent that it could climb and glide well, but not fly. Over the following 4 wk, its condition deteriorated to the point that it was unable to get off the ground. This bird was euthanized by intracardiac barbiturate injection and submitted to the Veterinary Services Branch for necropsy examination.

The carcass weighed 249.6 g and appeared mildly dehydrated. The skin was difficult to remove, the muscles were tacky, and there were urates visible in the kidney. No other significant lesions were observed grossly.

Histopathological evaluation of the brain revealed spongiosis of the cerebellar arbor vitae, with occasional apoptotic cells and spheroids, as well as astrocytosis. A cross section of a nematode larva was observed within the neuropil, proximal to the medulla in the mesencephalon. The embedded nematode was approximately 60 μm in diameter and had platymyarian musculature, a ridged external cuticle with prominent lateral alae, and prominent excretory columns. These excretory columns were smaller than the large digestive tract composed of a few nucleated cells. Its morphology was consistent with that of a Baylisascaris sp. (1,2). There was associated spongiosis, malacia, astrocytosis, numerous spheroids, and occasional neuronal degeneration. No other significant abnormalities were found within the remaining organs.

Tissue samples examined, using modifications of standard DNA amplification tests, were negative for Newcastle disease virus (NDV), influenza A matrix, and West Nile virus (WNV) (3–5). No significant bacteriological isolates or internal parasites were cultured.

A crested screamer chick was removed from its clutch at 3 wk of age showing signs of ataxia. Treatment was initiated with trimethoprim-sulfa (Trivetrin; Schering-Plough, Pointe Claire, Quebec), IM, q12h, and supportive care, but the bird later died. Another chick from the same clutch, with a similar clinical appearance, was removed from the clutch immediately and euthanized. Both chicks were submitted for postmortem examination.

The 1st chick weighed 280.8 g upon arrival for necropsy; it had poorly developed pectoral muscles and little internal fat. The proventriculus contained green plant material, while the gizzard contained fine grit and sand. The lower intestine contained copious amounts of firm, dark-brown contents. The kidneys appeared pale. No significant findings were observed in the remaining organs. The 2nd chick weighed 458.1 g and had moderately developed pectoral muscles and little internal fat. The proventriculus and gizzard contained material similar to that found in the 1st chick, and the large intestine contained the same firm, dark-brown contents at intervals. The trachea, lungs, heart, liver, esophagus, proventriculus, ventriculus, intestine, pancreas, and tibial sections of both chicks were visibly congested, but, otherwise, there were no significant gross findings.

Histologically, the meninges of the cerebrum and the cerebral parenchyma contained nematode larvae measuring approximately 62.5 μm in diameter, with prominent lateral alae; these were tentatively identified as B. procyonis (Figure 1). There were no other associated histological lesions. Kidney sections taken from the 1st chick showed congestion and there were several dilated tubules and basophilic spherical crystals in a few tubules, all consistent with renal gout.

Figure 1.

Cross section of a Baylisascaris procyonis larva in the brain tissue of a crested screamer chick. Note prominent lateral alae (arrows) and triangular excretory columns (E) on both sides of the centrally located, laterally compressed intestines. Hematoxylin and eosin. Bar = 50 μm.

Bacteriologically, no important isolates were found. Results from fecal floatation (modified Sheather’s Solution, specific gravity 1.25–1.27) (6) were negative for parasites in both cases; the chicks also tested negative for influenza A matrix and WNV through polymerase chain reaction (PCR) (3–5).

The western Canadian porcupine began to show neurological signs, including tremors, ataxia, and uncoordinated movement, at 4 y of age. Sensory ability remained intact and appetite remained consistent, but mobility was severely affected. No clinical improvement was observed after 16 mo of supportive care; therefore, it was euthanized.

On gross necropsy, a proliferative dermatopathy, evident as multifocal to coalescing, raised, black nodular skin masses around the nares and oral cavity, was observed. The liver was pale, mottled, and enlarged with round edges, suggestive of hepatic lipidosis. The small intestine contained a few white cestodes. Gross abnormalities were not observed in either the brain or the spinal cord.

Histopathological examination of the brain revealed 2 foci of malacia with accumulations of eosinophils and astrocytes, within the cerebrum, adjacent to the lateral ventricle, at approximately the level of the thalamic nucleus. In 1 of these malacic areas, a section of a nematode larva with a cuticle, prominent lateral alae, lateral cords, and intestine was present; the larva was approximately 75 μm in diameter and was identified as being a Baylisascaris sp. Both distal and proximal to this lesion, malacia and gliosis were present within the neuropil. There was also a focus of malacia, possibly due to infarction, within the arbor vitae of the cerebellum. In the liver, multifocal hepatocytes were expanded by large intracytoplasmic, clear vacuoles, consistent with lipidosis. The nodular skin lesions of the face were characterized by basket weave hyperkeratosis and epidermal hyperplasia with hypergranulosis. Results from immunohistochemical staining were positive for papilloma virus.

Bacteriologic isolates were not significant. A fecal floatation revealed a Monoecocestus sp. eggs, and results from testing for WNV by PCR were negative.

These findings supported a diagnosis of verminous encephalitis due to infection with a Baylisascaris sp., causing neurological disorder, intestinal cestodes (Monocoecestus sp.), squamous papilloma, and hepatic lipidosis.

A retrospective diagnosis in this series of cases was verminous encephalitis (neural larval migrans, NLM) likely caused by B. procyonis. Although histological examination of migrating larvae could not exclude the possibility of B. columnaris, the roundworm of the North American striped skunk, skunks are rare in urban Winnipeg and within the zoo grounds; they are also inefficient climbers, limiting their access to zoo enclosures.

Discussion

Baylisascaris procyonis is a nematode that has been shown to produce NLM in over 100 species of birds and mammals (2). The adult worm is found within the lumen of the small intestine of the raccoon (Procyon lotor), its definitive host (2). The female worm can produce between 115 000 and 179 000 eggs/d in the intestine of the raccoon; these are shed in the feces and can result in heavy environmental contamination (2). Particularly high levels of contamination occur at preferred raccoon defecation sites called latrines (2,7,8). Once shed, the eggs require 2–4 wk in the environment, under optimal conditions, to become infective (2). Infected raccoons appear clinically normal with no superficial signs of infection and have no tissue migratory phase (2).

As with other ascarids, B. procyonis has both a direct and an indirect life cycle. The direct life cycle is considered to be the more common means of raccoon infection. It occurs when young, uninfected raccoons ingest the infective eggs in raccoon feces directly from their environment (2). Alternatively, as part of the indirect life cycle, small rodents and other intermediate hosts can become infected also through the ingestion of eggs, often resulting in neurological disease. Omnivorous raccoons are then capable of preying upon debilitated intermediate hosts, ingesting the larvae, and continuing the parasite’s indirect cycle (2). Clinical signs in intermediate and aberrant hosts may include various combinations of depression, lethargy, nervousness, severe head/body tilts, ataxia, continuous circling, leaning, falling over, opisthotonos, lateral recumbency, rolling, coma, and death (2). Pathologically, the most important lesions are formed in the brain and consist of meningoencephalitis, necrosis, and spongiosis (2). Eosinophils are a major component of the small mammal host’s reactions to the parasite (2,8,9). Severity of clinical signs may vary, depending on the number of infective eggs ingested, and subtle cases with mild signs have been observed (2). Numerous animal species become infected while foraging for seeds and related food items in raccoon feces at latrines (7,8) or by ingesting other contaminated materials, such as hay (2).

Aberrant hosts, including humans, also become infected by ingesting infective eggs from the environment (2–7,8), primarily as dead end hosts. A small but potentially devastating number of larvae (5%–7%) enter the central nervous system of the aberrant host causing severe neurological disease and, almost invariably, death (1–5). Baylisascaris procyonis is known to cause neurological disease in many wild and domestic animal species (2,10) and has also been associated with ocular disease in animals, including humans (2).

This report documents infection with B. procyonis in 2 avian species; Patagonian conures of the family Psittacidae, members of which are commonly reported to be susceptible, and crested screamers of the family Anhimidae, a family not previously known to be susceptible aberrant hosts.

The prognosis for individuals affected with B. procyonis NLM is typically very poor. While anthelmintics can successfully eliminate B. procyonis worms from the intestines of raccoons, they are much less effective and generally unsuccessful against larvae in the tissues of aberrant hosts (7–9). Therefore, it is important to take the appropriate precautions to prevent infection as Baylisascaris procyonis is indigenous in North American raccoons, with infection rates as high as 70% to 100% in various areas (2). These high infection rates create a potential human health hazard, as raccoons are becoming increasingly familiar inhabitants of suburban and city neighborhoods (2,10).

The racoon is among the fastest growing wildlife populations in the United States, especially in urban environments (8). Raccoons were rare in the early years of the 1900s, causing some to suggest that since then the raccoon has greatly expanded its range throughout the Canadian prairies (11). An early record of raccoons in Manitoba dating from 1800 indicates that raccoons were commonly harvested for both fur and food (12).

Currently, the highest densities of raccoons occur in urban areas where they have access to abundant anthropogenic food sources, such as pet food, gardens, and garbage (11). The expanding urban populations of raccoons increase the probability of human infection with B. procyonis (8,9); also, anthropogenic food sources can increase the intensity and diversity of parasitism in the wild raccoon (13).

The presence of raccoons and B. procyonis not only endangers humans, but numerous animals as well, on farms, in zoo collections, or kept as pets (2). There were numerous cases of central nervous system disease caused by B. procyonis over a 3-year period in the Los Angeles zoo (14), and cases have been reported from other zoos in the United States and Canada. Infection of these animals is often associated with keeping raccoons on the premises, using enclosures or cages that previously held raccoons, using contaminated feed, hay, or straw, or through direct exposure to contaminated feces from wild raccoons (2).

Both the conures and the crested screamers were housed in similar, but separate, enclosures in the same exhibit area (Tropical House) of the zoo. The enclosures measured approximately 4–5 m wide, 4 m deep, and 4 m high. Galvanized chain-link fencing (7-cm mesh) covered the enclosures on 3 sides and the same mesh completely covered the tops of the enclosures. The back wall of the enclosures was formed by the masonry exterior wall of the main exhibit building. The conures were fed from open-topped feeding dishes placed on elevated shelves attached to the enclosure walls. The screamers were fed in open-topped dishes placed on the ground in the enclosure.

Raccoons do not have direct access to the enclosures but, frequently, they do traverse an elevated ledge on the building to which these enclosures are attached and have been observed on the chain-link mesh cage tops.

The porcupine was wild born, but hand-raised from approximately 7 wk of age. It was kept in a protected environment initially and then progressively provided with more outdoor exposure as the summer progressed and the individual matured. The neurological signs observed in the porcupine had a subtle, progressive onset 3 y after it had been placed permanently on display in an enclosure approximately 4 m² and 3 m high; again completely enclosed and roofed with 7-cm chain-link mesh. Wild raccoons do not have direct access to the exhibit area; however, they can access the top of the exhibit by climbing the mesh walls or adjacent trees. The porcupine was fed in the exhibit area, also in an open dish.

Baylisascaris procyonis has not previously been identified in Manitoba, and Winnipeg is near the northern limit of the raccoon distribution in North America (11,15). A series of postmortem examinations on 31 raccoons from a similar latitude in Saskatchewan failed to identify B. procyonis (15). Some isolated populations of raccoons appear to be free of this parasite (16,17).

In the summer of 2007, as part of a proactive surveillance program, infected raccoons were identified on the zoo grounds in Winnipeg. Baylisascaris procyonis eggs were recovered, by flotation (6), from fecal samples collected from wild raccoons live-trapped on the zoo property and from latrine sites of wild raccoons in the surrounding grounds.

In order to better prevent cases of B. procyonis infection in zoo collections, it is important to properly store feed and bedding in areas where raccoons cannot gain access (2). The use of natural materials in exhibits, such as logs, limbs, or rocks collected from surrounding areas, should be avoided without, at least, first cleaning and decontaminating them. Wild raccoons should be controlled on zoo grounds, especially their access to exhibits and enclosures holding susceptible species (2). Bait deworming of stable local raccoon populations has also been advocated, along with cleanup and decontamination of existing latrines. In the face of an outbreak or new case, daily administration of pyrantel salts to exposed animals, prior to the appearance of neurological signs, is known to protect them from new or further infection with B. procyonis (2).