Chapter 34 Baylisascaris Neural Larva Migrans in Zoo Animals
Larva migrans refers to the prolonged migration and persistence of helminth larvae in the organs and tissues of humans and animals, as a normal life cycle occurrence in intermediate hosts; however, it causes extensive tissue damage and inflammation in incidental hosts.3 Disease syndromes caused by the parasite Baylisascaris include visceral larva migrans and ocular larva migrans. The disease process seen most often in zoo species, however, involves neural larva migrans (NLM), or cerebrospinal nematodiasis, and causes fatal or severe neurologic disease. The disease syndrome may vary and is likely dose related and influenced by prior exposure and species differences.3,5
ETIOLOGY AND EPIDEMIOLOGY
Baylisascaris spp. are ascarid nematodes. These species occur primarily in carnivores (B. procyonis in raccoons, B. columnaris in skunks, B. melis in badgers, B. devosi in martens and fishers, B. transfuga in bears, B. schroederi in giant pandas, B. tasmaniensis in Tasmanian devils, quolls, and native “cats”) and in rodents (B. laevis in marmots and ground squirrels).
Transmission of most Baylisascaris spp. involves ingestion of larvae in small mammal intermediate hosts or direct infection by ingestion of eggs. Larva migrans occurs, and the larvae become encapsulated in internal organs and tissues, where they persist for later transmission to the animal, which eats the intermediate host. In addition, ascarid eggs are extremely resistant and long-lived in the environment. Infected raccoons, for example, may shed millions of eggs per day in their feces because one adult female worm produces up to 179,000 eggs per day. Young raccoons become infected by ingesting infective eggs, and older raccoons are infected from third-stage larvae in intermediate hosts (usually rodents). Transmammary and transplacental forms of transmission have not been investigated but are doubtful.3
In human and veterinary literature the primary discussion of NLM focuses on the raccoon roundworm, B. procyonis; however, B. columnaris of skunks and B. melis of badgers also cause this disease. Different species of Baylisascaris vary in their central nervous system (CNS) pathogenicity, based on differences in migration and brain invasion, larval aggressiveness, and the host’s ability to wall off the larvae. Baylisascaris procyonis and B. melis are the most pathogenic, followed by B. columnaris.3
Any areas contaminated with feces that contain the previously listed species of Baylisascaris, from wild animals living and defecating in the zoo, are sources of infection for susceptible zoo animals. It is important to note that it takes 11 to 14 days, with optimal temperature and moisture (22°–25°C [71.6°–77°F] and 100% humidity), for B. procyonis eggs to become infective (second-stage larvae), but under natural conditions it likely takes weeks to months. However, the eggs may remain infective in the environment for years, even surviving harsh winters. Conditions of extreme heat and dryness will kill eggs by desiccation, probably in weeks or months as well.3 Food, bedding, or enclosures contaminated by skunks and raccoons may serve as a source of infection for captive zoo animals. Not only wild (non–zoo collection) animals, but also captive animals purposely housed with susceptible species as a “mixed-species exhibit,” are at risk.
Baylisascaris procyonis is indigenous in raccoons in North America, Europe, and parts of Asia.3 In North America it is more common in the midwestern and northeastern United States and along the West Coast. However, a 2003 report found 22% of raccoons trapped in the metropolitan Atlanta area were positive, discounting prior reports that Baylisascaris was not a concern in the South.2 Local prevalences of B. procyonis may vary, and population density may change over time. Unless active sampling is done, it is impossible to state where this parasite does not reside, and the current focus is on screening raccoons, not other species such as skunks and badgers.7 Wild raccoons have been introduced to Asia and Europe as pets, escaping and taking their B. procyonis with them.
Additionally, intestinal B. procyonis has been recovered from two kinkajous and could be expected to occur in other related procyonids, such as coatimundis and ringtails. It appears that domestic dogs may also serve as adult or intermediate hosts, with infected dogs found in several midwestern states (U.S.) and in Japan.1
Susceptibility to Baylisascaris larva migrans varies among animal groups and species, with a wide-ranging list of more than 90 species; rodents, rabbits, primates, and birds are most often infected. I have also seen numerous cases in Australian marsupials and a case in a fruit bat. Several cases have been seen in carni-vores (Vulpes, Canis, Taxidea, Enhydra, and Mustela). Baylisascaris is also thought to naturally occur in opossums.3 No cases have been seen in zoo hoofstock or livestock. Limited or no migration has been seen in sheep, goats, or swine when experimentally infected. Cats and raptors also appear to be resistant to infection. The susceptibility of poikilothermic vertebrates is unknown, but not expected. Prior exposure, concurrent infections, and hormone fluctuations may influence infection. One newborn lamb was diagnosed and only could have been infected prenatally.3
Although raccoon ascarids are the most likely cause of NLM, skunks and less often badgers infected with Baylisascaris must be considered. Because it is impossible to differentiate the third-stage larvae of these parasites in histologic sections, species determination in cases is impossible, unless an epidemiologic study is done.3 For example, skunks were a much larger problem with greater abundance at the Los Angeles Zoo, and B. columnaris was identified in feces of wild skunks living in the zoo, which was thought to be a greater contributor of disease in that outbreak.9
The severity and progression of CNS disease in NLM depends on the number of eggs ingested, the number of larvae entering the brain, the location and extent of migration damage and inflammation in the brain, and the size of the brain. Although experimentally, larvae enter the somatic tissues, eyes, and brain of some species as early as 3 days after infection, clinical signs are usually not apparent until 2 to 4 weeks or later. If migrating larvae leave the brain or become encapsulated and stop migrating, clinical signs may stabilize.3 I have seen this in numerous cases, only to have signs reappear, probably as a result of reinfection when the animal remains in the same environment. Thus, a “waxing and waning” course may be seen.
Clinical signs are extremely variable and may include depression, lethargy or nervousness, rough hair coat or ruffled feathers, tremors, head and body tilt, circling, jumping, ataxia, leaning, falling, opisthotonos, lateral recumbency, rolling longitudinally, “stargazing,” arching of the head and neck, blindness, nystagmus, motor weakness or posterior paresis, hypertonia or extensor rigidity, paddling movements while recumbent, coma, and death. Arboreal animals may have difficulty with balance and perching, and primates may have difficulty with manual dexterity.3 Intention tremors may be seen and were pronounced in a golden-headed lion tamarin I have seen.5 The problem became so severe in this animal that euthanasia was necessary when it became unable to eat.