Encephalitic nematodiasis in a Douglas squirrel and a rock dove ascribed to Baylisascaris procyonis John W. Coates, Judith Siegert, Victoria A. Bowes, Deirdre G. Steer

This report briefly describes the history, clinical signs, treatment, and necropsy findings in a Douglas squir- rel (Tamiasciurus douglasii) and 2 rock doves (Columba livia), in which lesions observed within brain tissue were caused by migrating ascarid larvae suspected of being Baylisascaris procyonis, the raccoon roundworm. Cross-species transmissibility of the migrating larvae of the raccoon roundworm is briefly discussed. One of 2 immature rock doves that had been under the care of the Wildlife Rescue Association of British Columbia in Burnaby for 6 wk suddenly developed central nervous system (CNS) signs of head tremor, incoordination, loss of balance, and torticollis. Three weeks previously, the bird had received a routine, sin- gle administration of 0.03 mg ivermectin (Ivomec, MSD Agvet, Kirkland, Quebec), PO, as prophylaxis against helminths. We suspected head trauma upon onset of the CNS signs, so we administered 0.5 mg of sodium dexamethasone phosphate (Dexamethasone 2, Austin Laboratories, Juliet, Quebec), IM. Twelve hours later, the bird's condition began to deteriorate rapidly, and it was euthanized. Necropsy failed to explain the CNS signs observed |i_f .' F: . X clinically. Histopathological changes in tissues, includ- Figure 1. Photomicrograph of cerebral cortex from a Douglas ing serial brain sections, were not observed, though squirrel. Longitudinal and cross sectional views (arrows) of an portions of brain removed for viral culture had reduced ascarid larva(e) consistent with Baylisascaris procyonis are seen in conjunction with a moderate granulomatous inflammatory the quantity available for microscopic examination. response. Periodic acid-Schiff. Bar = 100 Tissue cultures for avian viruses, including avian gm. paramyxovirus (PMV-I), using separate cell cultures of chick embryo fibroblasts and chick kidney cells were adjacent to a pen containing a 6-month-old, female, also negative, as was toxicological analysis for lead. Douglas squirrel. Bacterial cultures were negative. A week after the death of the rock dove, the Douglas Prior to the bird becoming ill, about 40 rock doves had squirrel in the adjacent pen became ill. It developed been kept intermittently in the same outdoor pen. Over acute, progressively severe, CNS signs, characterized by the previous 4 to 5 y, groups of immature, orphaned rac- initial incoordination, followed by recumbency and coons (Procyon lotor) had been housed in this pen for paddling of the limbs immediately prior to death. about 3 mo at a time. Within 24 h of admission, the The squirrel was hospitalized and initially treated young raccoons were dewormed, using pyrantel pamoate for suspected head injury with dexamethasone sodium oral suspension (Strongid-T, rogar/STB Inc, London, phosphate (Dexamethasone 5, Austin Laboratories), Ontario), PO, at 50 mg/ 7.5 kg body weight (BW), with 0.3 mg, IM, q24h. By the next day, the squirrel's con- a 2nd worming 6 to 8 wk later. The floor of the pen was dition had worsened. At this time, we recalled the CNS composed of roughened cement, which had been washed signs shown by the rock dove from the adjacent pen only with a standard bleach solution (5.25% sodium hypochlo- I wk earlier, and that immature raccoons had been kept rite) and cleaned with pressurized steam following in that enclosure until very recently. For these reasons, release of the young raccoons. Walls in all the pens we then suspected that migrating larvae of the raccoon consisted of an open wooden framework overlaid with roundworm, B. procyonis, were causing the CNS signs heavy-gauge wire mesh. This enclosure was immediately in the squirrel. Ivermectin (Ivomec, MSD Agvet), 0.03 mg, PO, was administered, followed by furosemide (Lasix, Hoechst- Roussel, Sommerville, New Jersey), 0.05 mg, PO, q I 2h Can Vet J 1995; 36: 566-569 for 3 d. Despite treatment, the squirrel's condition pro- It was euthanized 6 d fol- Animal Health Centre, Ministry of Agriculture, Fisheries and gressively deteriorated. finally Food, 1874 Gladwin Road, PO Box 100, Abbotsford, British lowing onset of clinical signs. Columbia V2S 4N8 (Coates, Bowes); 3240 Phillips Avenue, Necropsy of the squirrel failed to demonstrate any Burnaby, British Columbia V5A 2W7 (Siegert); Wildlife gross visible lesions. Tissues from all major organs Rescue Association of British Columbia, 5216 Glencarin and the brain were fixed in 10% neutral buffered for- Drive, Burnaby, British Columbia V5B 3C I (Steer). malin, embedded in paraffin, and then sectioned and 566 Can Vet J Volume 36, September 1995 which was initially observed as being lethargic and disoriented, stopped eating and developed CNS signs similar to those shown by the 1st bird, including poorly coordinated attempts at flying. The dove was immediately hospitalized and given nursing care. By the 5th d, the dove's condition had worsened, and it was euthanized and submitted for necropsy. Examination of histological sections from the brain of the 2nd dove revealed mutiple, patchy foci of mild granulomatous encephalitis, malacia, edema, and glio- sis, together with mild inflammatory perivascular cuffs within the medulla, brain stem, and cerebellum. A sin- gle ascarid larva observed in longitudinal and cross sectional portions within the bird's cerebellar peduncles was identical in size and morphology to the larvae pre- viously seen in the squirrel's brain. The spinal cord was not examined histologically in either the squirrel or the doves. In retrospect, considering observed clinical signs of weakness, incoordination, and recumbency, lesions due to migrating ascarid larvae might have been present in the spinal cord, as has been reported in other cases (2). - ...t| .... Baylisascaris procyonis is the common roundworm in Figure 2. Photomicrograph of cerebral cortex of a Douglas the small intestine of raccoons. The parasite is similar in squirrel from the same area as in Figure 1. Cross sectional appearance and life cycle to the roundworm of skunks features, such as a single pair of lateral alae (small arrows), (B. columnaris); in morphology, it superficially resem- paired excretory columns (larger arrow) and a prominent bles the canine roundworm Toxocara canis (1). The central digestive canal (arrowhead), are typical of B. procyo- raccoon roundworm is well recognized as a potentially nis. Periodic acid-Schiff. Bar = 50 pm. serious pathogen when its eggs are ingested by other species. Lesions attributed to larval migration of this par- stained with hematoxylin and eosin (H&E) for histo- asite have been described within brain or spinal cord in logical examination. Brain sections were also stained with over 40 mammalian and avian species, including the grey periodic acid-Schiff (PAS). Portions of liver, lung, and fox (1), red squirrels (1), mourning doves (1), chin- intestine were retained for bacterial culture; liver and kid- chillas (5), cottontail rabbits and woodchucks (6), dogs ney were submitted for toxicological analysis for heavy (7), ratites (3,8), and humans (9). Rodents including metals. Portions of fresh brain were kept and frozen for squirrels, as well as birds and rabbits, are considered to subsequent viral studies, if other tests proved to be be the natural intermediate hosts for B. procyonis (1). negative. Bacterial cultures for pathogenic organisms Several other Baylisascaris spp., including B. colum- were negative, as was toxicological analysis on liver and naris of skunks and B. transfuga of bears, as well as those kidney samples for lead and cadmium. of badgers, fishers, and martens, are also capable of Histological examination of sections from the brain causing animal or human disease of a similar nature revealed multifocal, patchy areas of granulomatous (1,2,9). A few species, including cats and larger domes- encephalitis in both the gray and the white matter of the tic livestock, such as sheep and swine, are evidently only cerebral hemispheres (Figure 1). Gliosis with moderate marginally susceptible to B. procyonis (1). numbers of histiocytes, lymphocytes, plasma cells, and The roundworm is a common parasite of raccoons; a few granulocytic cells resembling eosinophils was in 1 report, the prevalence of eggs of B. procyonis present in these malacic areas, as was prominent lym- detected in raccoon scats taken from both rural and phohistiocytic cuffing of vessels. Brain sections stained urban areas varied from 27% to 31% (10). Other animal with H&E and PAS demonstrated multiple larval frag- species, including man, may become infected by ingest- ments in these same foci within the cerebral hemi- ing infective eggs from contaminated soil, water, air, or spheres (Figure 1). fomites (9). Larval crosssections revealed a single pair of lateral We suspect that the ascarid larvae detected within the alae; paired lateral excretory columns, roughly triangular brain tissues of the Douglas squirrel and the 2nd rock in shape; and a prominent central digestive canal dove were those of B. procyonis. The rock doves had (Figure 2). These features are characteristic of larvae of been caged in an outdoor aviary pen previously occupied Baylisascaris spp. within the family Ascarididae. The for several months by immature raccoons, and it is greatest larval diameter measured on the sections exam- likely that the floor of this pen, and that of the adjacent ined was 60 to 65 ,um (Figure 2), which is consistent with pen that contained the Douglas squirrel, had become previously reported measurements of B. procyonis (1,2). contaminated with eggs from the raccoon roundworm. Larval diameters measured microscopically vary, depend- In retrospect, the initial administration of an anthelmintic ing upon the point and angle of sectioning, and with the to the young raccoons upon admission would not have stage of development of the larva. prevented the release of ascarid eggs and subsequent A 2nd rock dove, cage-mate of the I st one, became ill contamination of the pen within the first 24 h following 10 d after the onset of illness in the squirrel. The bird, treatment. Can Vet J Volume 36, September 1995 567 Migrating larvae of the raccoon roundworm have a eggs but are impractical for general environmental tropism for nervous tissue in other species (1,4). Larvae use (9). are believed to reach the brain via the arterial blood With adequate moisture and humidity, eggs of B. pro- stream, leaving small arteries where their diameter cyonis may survive for years in soil (1,3). For this rea- approximates that of the blood vessel. Larvae then pen- son, complete removal of contaminated surface soil etrate the brain from the subarachnoid space and within enclosures that previously contained raccoons has choroidal membranes (4). A single ascarid larva wan- been recommended (1). Removal and disposal of feces dering haphazardly through the brain or spinal cord of and bedding from pens previously occupied by raccoons either a natural intermediate host, or an accidental host, is an additional practical step to reduce the likelihood may produce severe and fatal damage. Unlike the larvae of inadvertent mechanical transport and contamina- of Toxocara spp., migrating larvae of the raccoon round- tion of nearby pens (3). Feed storage areas should be worm continue to grow in size upon reaching the brain raccoon-proof. (1,4). Earlier reports link the granulomatous inflam- After postmortem studies on the Douglas squirrel matory response observed within nervous tissue to and the 2nd rock dove confirmed the presence of ascarid mechanical trauma caused by larval movement and larva migrans, the pen that had previously contained actual growth, and to the parasite's release of antigenic raccoons, together with the adjacent pen, were flamed enzymes and metabolic wastes (1-4). with a propane torch to kill roundworm eggs. All wooden In this case, preventing the development of lesions or disposable material remaining in the 2 pens that held attributed to B. procyonis neural larva migrans in both the rock doves and the Douglas squirrel was incinerated. the 2nd rock dove and the squirrel by a single oral pro- Immature raccoons placed in enclosures previously phylactic treatment with ivermectin upon admission to occupied by older raccoons easily become reinfected with the Wildlife Rescue Care Centre was unsuccessful. The eggs, despite an initial program of deworming, as was effectiveness of veterinary treatment of the condition attempted in this case. Baylisascaris procyonis evi- in animals, including the administration of either dently undergoes a prolonged developmental period in anthelmintics, steroids, or both for acute cases of CNS the intestine in 2-month-old raccoons, when eggs will not larva migrans caused by this parasite, is still a quandary be found in feces with the flotation method. Immature (2,9); additional study is needed. raccoons thus pose problems for the control of round- Though steroids are known to exacerbate parasitic worms, since they may have false negative results on infections in host-parasite relationships, some authors fecal examination, only to shed eggs at a later date (1). believe them to be of value in cases of cross-species larva In our view, the knowledge gleaned from this case migrans, since they reduce inflammatory reactions and clearly indicates the importance of housing raccoons eosinophil degranulation, which may be serious and separately and at a distance from other animals in zoos, even life-threatening (9). The CNS certainly has limited game farms, wildlife refuges, rehabilitation centers, or tolerance to either the trauma caused by the migrating similar facilities to prevent contamination by raccoon larvae or the deleterious effects of the inflammatory scats. In this case, it appears that direct contamination reaction that the parasite generates. of the squirrel's and birds' pens with roundworm- Steroids have been used together with anthelmintics contaminated scats from the orphaned raccoons led to in the treatment of toxocaral visceral larva migrans in cross-species infection with B. procyonis. children, including ocular larva migrans (9). Unfortu- Specific pens at the Wildlife Rescue Care Centre are nately, success in treating neural larva migrans due to now designated for holding raccoons, and all fecal and Baylisascaris spp. in animals or humans is much less bedding material from these pens is incinerated after satisfactory. Larvae of B. procyonis can enter the brain removal. Individuals attending the animals wear pro- within the 1st wk of infection, and significant CNS tective and disposable outer clothing and footwear. damage usually occurs prior to the onset of clinical Raccoons are now dewormed immediately during an signs (2,9). initial 24-hour quarantine, followed by additional Embryonated eggs of B. procyonis are extremely dewormings at 10- to 14-d intervals, as has been recom- resistant to environmental conditions and to common mended (9). Fecal examinations are carried out con- disinfectants (1,3), including the combination of bleach currently with dewormings, so that individuals shedding solution and pressurized steam used here following the ascarid eggs can be indentified. release of the young raccoons, but prior to the occurrence Veterinary practitioners caring for wildlife species of the cases. The effectiveness of steam is likely influ- should be aware that larva migrans of B. procyonis is an enced by its pressure and the duration of its application. important differential when determining the origin of ner- Decontamination of pens or enclosures can be achieved vous signs in mammals or birds, especially if the case his- by other forms of heat, including boiling water or the dry tory indicates previous habitation in pens or dirt lots heat of a propane torch (3). Autoclaving of feed bowls, where exposure to raccoon scats may have occurred. etc., should be done where applicable. Public education by veterinarians concerning the Most chemicals are an unsatisfactory means of zoonotic danger of the raccoon roundworm is an ongo- destroying Baylisascaris eggs. The use of bleach solu- ing responsibility. Keeping pet raccoons should be dis- tion to clean pens does not kill the eggs but renders couraged. Handlers of raccoons in zoos, game farms, or them nonadherent, so that they can be rinsed away (9). wildlife rehabilitation centers should be informed of This likely leads to further contamination of the imme- the potential health hazard this parasite poses to them- diate environment. Chemicals, such as 1:1 xylene: selves, to unsuspecting patrons, and to animal species ethanol or 120 ppm aqueous iodine, will kill the under their care. cvJ

568 Can Vet J Volume 36, September 1995 References 1. Kazacos KR. Boyce WM. Bavlisascaris larva migrans. J Am 6. Jacobson HA. Scanlon PF. Nettles VF. Davidson WR. Epizooti- Vet Med Assoc 1989; 195: 894-903. ology of an outbreak of cerebrospinal nematodiasis in cottontail 2. Fox AS, Kazacos KR, Gould NS, Heydemann PT, Chinnamma T. rabbits and woodchucks. J Wild] Dis 1976: 12: 357-360. Boyer KM. Fatal eosinophilic meningo-encephalitis and visceral 7. Thomas JS. Encephalomyelitis in a dog caused by Bavlisascaris larva migrans caused by the raccoon ascarid Baylisascaris pro- procvonis. Vet Pathol 1988: 25: 94-95. c!Yonis. N Engl J Med 1985: 312: 1619-1623. 8. Kwiecien JM. Smith DA. Key DW. Swinton J. Smith-Maxie L. 3. Kazacos KR, Fitzgerald SD. Reed WM. Baylisascaris procvonis Encephalitis attributed to larval migration of Bavlisascaris species as a cause of cerebrospinal nematodiasis in ratites. J Zoo Wildi Med in emus. Can Vet J 1993; 34: 176-178. 1991: 22: 460-465. 9. Kazacos KR. Visceral and ocular larva migrans. Semin Vet Med 4. Sprent JFA. On the invasion of the central nervous system by nema- Surg (Small Anim) 1991: 6: 227-235. todes. 1. Invasion of the nervous system in ascariasis. Parasitology 10. Jacobson JE, Kazacos KR. Montague FH. Prevalence of eggs of 1955: 45: 41-55. Baylisascaris procvonis (Nematoda: Ascaroidea) in raccoon 5. Sanford SE. Cerebral nematodiasis caused by the raccoon ascarid scats from an urban and a rural community. J Wildl Dis 1982: (Bavlisascaris procvonis) in chinchillas. Can Vet J 1989: 30: 902. 18: 461-464.

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