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Parelaphostrongylus (Brainworm) Infection in Deer and Elk


Murray Woodbury DVM, MSc.

Specialized Livestock Research and Development Program
Department of Large Animal Clinical Sciences
Western College of Veterinary Medicine
University of Saskatchewn
Saskatoon,Saskatchewan    S7N 5B4

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  Contents
Introduction
Cause
Geographic distribution
Prevalence
Transmission
Other species affected
Clinical signs
Pathology
Diagnosis
Differential diagnosis
Treatment
Control
Significance
Future research
References



Introduction
The parasite Parelaphostrongylus tenuis (P. tenuis) is also known as brain worm, meningeal worm, Pneumostrongylus tenuis, Odocoileostrongylus tenuis, Elaphostrongylus tenuis, or Neurofilaria cornellensis. Infection frequently results in clinical disease called moose sickness, moose disease, moose neurological disease, cerebrospinal parelaphostrongylosis, or cerebrospinal nematodiasis. The existence of this parasite in eastern, but not western, North America and the implications of it's movement west has severely affected live animal trade in the farmed cervid industry of Canada.
 
 

Etiology
Parelaphostrongylosis is caused by the roundworm, Parelaphostrongylus tenuis. The major host for this parasite is the white-tailed deer where it is carried without causing clinical signs of disease.
 

Geographic distribution
P. tenuis is present in eastern and central Canada including Nova Scotia, New Brunswick, southern Quebec, Ontario, Manitoba, and eastern Saskatchewan (5). It is also present in twenty eight of the eastern and central United States (1). It is generally absent from coastal plains of the southeastern United States and St. Croix of the Virgin Islands (14).

The parasite continues to spread extensively as white-tailed deer expand their range in response to environmental changes such as deforestation, agriculture and burning (5). Currently, the meningeal worm is not present in western North America, however it is present in deer of the aspen parkland, and there is no apparent barrier to its continued spread west toward the foothills of the Rockies through such a corridor (5). Biologically, the meningeal worm requires several criteria to be met for survival including the presence of adequate numbers and overlapping populations of definitive (white-tail deer) and intermediate hosts (terrestrial snails and slugs) in sufficient densities to allow for establishment. It also needs a suitable climate for survival of free-living stages of the parasites and suitable numbers of the hosts involved (1). Ecologically, the prairie habitat and its dry conditions may affect the survival of the first stage larvae and this may have some impact on controlling the range of the nematode (9). In addition, the parasite is believed to be associated with certain major soil types in combination with other environmental attributes. However, what constitutes the barrier to generalized distribution is unknown (4).
 

Prevalence
Prevalence of the meningeal worm ranges from less than 1% to greater than 85% throughout North America (1). Within Canada, the prevalence for adult worms in the cranial cavities of deer are as follows: Manitoba 10%, Ontario 41- 61%, Quebec 30%, New Brunswick 60%, and Nova Scotia 51% (1). The prevalence of meningeal worms in aberrant hosts is generally unknown, however surveys have been undertaken to determine the prevalence in such hosts (1).
 

Transmission
The life cycle of the meningeal worm is indirect with a typical prepatent period of 82 to 91 days. However, the length may be inversely related to the number of larvae ingested, and may be considerably longer in individual deer (10). P. tenuis is a true lungworm in that it requires both a definitive host, the white-tailed deer, and an intermediate host, a snail or slug. Deer become infected by accidentally ingesting gastropods (snails) containing infective third-stage larvae (L3) which are found on vegetation (4). Larvae are freed from the gastropod tissue by digestion, and during the following ten days they penetrate the abomasal wall, and migrate across the peritoneal cavity to gain access to the central nervous system, likely through lumbar nerves (4). Once they invade neural tissue, larval development occurs primarily in the dorsal horns of the spinal cord. Fourth stage larvae (L4) emerge about 25 days after initial ingestion (4). The L4 larvae leave the neural tissue and migrate to the subdural space by day 40, after which they molt to the immature adult stage (4). Once mature, some nematodes migrate to the venous sinuses of the cranium (4). Some worms may deposit eggs on the meninges, but most deposit eggs directly into the venous circulation where they are transported to the heart and lungs as emboli (4). Eggs lodge in the lungs where they are incorporated into fibrous nodules. These eggs embryonate into first-stage larvae (L1), move into the alveoli, and up the bronchial escalator where they are coughed up and swallowed to be excreted out in the mucous coat on the feces (4). The excreted L1 penetrate the foot of a terrestrial gastropod, where they grow and molt twice to become the infective L3.

The time required for these two molts to occur is variable and highly dependent on environmental conditions but it may be as short as three to four weeks at summer temperatures. Larvae cease to develop when snails are hibernating but development continues normally once snails become active (10). Laboratory and field studies have shown that larvae are capable of overwintering in the intermediate host (4).

Experimentally, a wide range of terrestrial gastropods may be infected, however only a few species are generally involved in natural transmission. This is likely related to preference of certain gastropods for favorable microenvironments of forested areas with specific moisture content, evaporation, and temperature (13). Commonly, gastropod availability in open meadows is less than forested areas, reducing the likelihood of exposure to particular gastropods for animals that utilize these areas to graze (13). Typically, white-tailed deer spend most of their time in forested areas where gastropods are found whereas elk spend most of their time in meadows and open fields (4). Other equally important factors may include seasonal movement patterns in deer, wapiti or gastropods, food preferences and selectivity for gastropods by the host animal (13).

The early phase of the meningeal worm life cycle in aberrant hosts parallels that in white-tailed deer, however the development of the larvae in the central nervous system tends to produce neurologic signs and even death (4). Meningeal worm larvae tend to be unusually active and damaging in neural tissue of aberrant hosts. Some larvae fail to leave the neural parenchyma which results in damage as the larvae matures and migrates, while other larvae invade the ependymal canal or reinvade the spinal cord or brain after maturation (10). The pathogenesis of the meningeal worm in fallow deer is different from other cervids in that infective larvae penetrate the small intestine rather than the abomasum (4).
 

Other species affected
A wide variety of species are susceptible to infection with P. tenuis, namely, moose, elk, caribou, reindeer, mule deer, black-tailed deer, mule deer/white-tailed deer hybrids, fallow deer, red deer, red deer/elk hybrids, domestic sheep and goats, llamas, guinea pigs, and several bovid and cervid species in zoos (1). It appears that reindeer, caribou, llamas, and domestic goats are very susceptible to meningeal worm infection (1). It is speculated that caribou and reindeer may be more likely to acquire infected gastropods because of their feeding habits (4).
 

Clinical signs
The natural host for this infection is the white-tailed deer, and although the parasite normally migrates to the meninges in this species, the deer typically displays few clinical signs. Lack of apparent disease even with neurological invasion has been attributed to the manner in which the larvae reside in the neuropil of white-tail deer (4). In naturally and experimentally infected white-tail deer, temporary lameness of the forelimb, circling, and rapid oscillation of the eyeballs have been observed (1). Most white-tailed deer survive infection without exhibiting clinical signs, however large larval burdens could precipitate serious signs or even death.

In various cervids, camelids and other wild and domesticated ruminants, very few P. tenuis larvae are required to produce a severe debilitating neurological disease. The disease is expressed by locomotor incoordination, lameness, stiffness, listlessness, progressive hindquarter weakness, circling, abnormal position of the head and neck, blindness, and paralysis (1). Caribou and reindeer also consistently exhibit exophthalmos or a "bug eyed" appearance (4). Naturally infected elk become less wary, leave the herd and remain near roads, fields or woodland clearings (14). Llamas infected with P. tenuis display a sudden onset of weakness or ataxia and at least one of paraparesis (generalized weakness), ataxia, exaggerated patellar reflexes, conscious proprioceptive deficits (can't place feet correctly) or increased extensor tone (rigid muscles) in the rear limbs (6). Cerebrospinal fluid aspirates in infected llamas typically reveal increased protein and eosinophils (6). Fallow deer fawns given high doses of infective larvae die sooner with signs associated with severe peritonitis resulting from perforation of the intestinal wall, compared to fawns given low doses of infective larvae which die later with signs associated with paralysis and inability to rise (8). There is also a continuum of responses to meningeal worm infection in elk: those exposed to large numbers of infective larvae die; those exposed to low numbers survive, often without infection; and those exposed to intermediate numbers often develop patent non-fatal infections (9). Apparently, severity of clinical signs, resolution of clinical signs and death are dose dependent.
 

Pathology
In white-tail deer, lesions associated with developing larvae are relatively minor. Uncoiled larvae are generally located in cell-free tunnels in the dorsal horns of the spinal cord surrounded by compressed neural tissue (4). In white matter, scattered myelin sheath degeneration may be present, with foreign body reactions around pieces of cuticle and hemorrhages associated with larval migration, however, neural parenchyma quickly assumes a normal appearance once larvae have left (4). Lesions associated with the adult meningeal worms in the cranium are unremarkable (4). Lesions in the lungs consist of tiny discolored spots uniformly distributed throughout the parenchyma and under the pleura (10). Nodules may be found within the lungs due to a foreign-body reaction that occurs around the remains of hatched eggshells (4). Congestion, hemorrhages, and eosinophilic and lymphocytic infiltration is common in areas where eggs or larvae have been in the lungs (4). Alveoli may collapse and disappear resulting in subsequent fibrosis of the region which may show as respiratory signs in naturally infected white-tailed deer (4).

Gross pathologic changes in infected aberrant host animals include extensive central nervous system lesions including focal hemorrhages, neuronal degeneration, tracking lesions in the brain and spinal cord, and yellowish accumulations streaked with blood adjacent to the worms (1). Meningeal worms can be found free in the cranial cavity or on the spinal cord or may be embedded in nervous tissue (1).

As identified previously, larval penetration of the small intestine occurs in fallow deer. It is believed that fallow deer are apparently unable to limit the phase of nematode migration through the small intestine, even though they are capable of mounting a substantial immune response against the meningeal worm once it is within the central nervous system (4). This results in colitis and fatal peritonitis, which is different than the pathology seen in all other cervids (4). In fallow deer, the mucosa of the greater curvature of the abomasum is hyperemic with scattered focal hemorrhages, the small intestine is filled with black-red fluid, and the intestinal wall is slightly thickened with rugose congested mucosae (8). Fibrinous adhesions are present throughout the peritoneal cavity.

Microscopic lesions in aberrant hosts include small hemorrhages, masses of parasite eggs, infiltrations of eosinophilic leukocytes, and congestion of very small blood vessels (1). Additional microscopic lesions identified in llamas include multifocal random areas of cavitation, axonal swelling, linear cavities containing a variable number of lipid-laden macrophages and necrosis (6).
 

Diagnosis
Presently, the only definitive method for diagnosing P. tenuis infections is recovery and identification of adult worms from the central nervous system at necropsy (1).

The current diagnostic technique used in live animals is recovery of first-staged larvae in feces or lung tissue using modified Baermann techniques. Unfortunately, other protostrongylid nematodes shed similar cork-screw shaped dorsal spiny-tailed larvae which may make it difficult to definitively identify Parelaphostrongylus tenuis (1). Additionally, the first-stage larvae of P. tenuis are resistant to dessication and freezing (4) and may be readily washed off feces by water or rain (10) making it difficult to recover larvae using this method. Detection of low-levels of infection by this method is complicated by the parasite's long reproductive period which necessitates repeated testing of feces from suspected animals for several months. It is known that the number of larvae shed fluctuates by season with more larvae shed in winter-spring than in summer-autumn and the normal host, the white-tailed deer, tends to shed more larvae than the aberrant hosts such as elk (1). Also, animals infected with only one worm, or worms of the same gender, will not shed larvae (12). It is also possible that immunological factors and age of the host may play a role in the levels of larval shedding (1).

Attempts to diagnose P. tenuis by measuring total protein concentration and enzyme activity within the cerebrospinal fluid of domestic goats and white-tailed deer showed inconclusive results (7). It is clear that parelaphostrongylosis is accompanied by seroconversion, and that both species develop a significant antibody response in cerebrospinal fluid, however the inability to detect antibodies during the prepatent period hinders the application of this technique as a diagnostic aid (7).

A primary objective of a study undertaken in 1996 was to develop simple and reliable blood tests to detect meningeal worm infection in game-farmed animals (3). The blood tests were based on the reaction between unique somatic antigens to P. tenuis located in or on the worm to antibodies from the blood of infected animals (3). A unique 37 kDa antigen of the third-stage larva, which is also present in adult P. tenuis, serves as a serodiagnostic antigen to develop an enzyme-linked immunosorbent assay as a reliable diagnostic test for P. tenuis infection in white-tailed deer (12). However, the use of native 37kDa antigens from either L3 or adults for developing serological tests is impractical because the antigen is in low concentration in the parasite and would be difficult to obtain. (12) Currently the antigen is being cloned and expressed using recombinant DNA technology (12). Serological diagnosis of P. tenuis should offer many advantages over the currently used method of fecal analysis (12), especially with respect to differentiation of P. tenuis from other protostrongylids.
 

Differential diagnoses
P. tenuis can be confused with other neurological disorders such as trauma, brain abscesses, tumors, tick paralysis, listeriosis, degenerative myelopathy, rabies and other parasites that cause cerebrospinal nematodiasis. Copper deficiency may cause progressive ataxia, and chronic capture myopathy may have external manifestations similar to some stages of P. tenuis infection (11).
 

Treatment
There are no drugs known to be effective against meningeal worms once they invade the central nervous system (1).

Kocan treated deer with 0.1 mg/kg of ivermectin subcutaneously at 1, 10 and 30 days after exposure to meningeal worm larvae and only prevented infection in deer treated 1 day after exposure (2). Once the larvae emerge from the gastrointestinal tract and enter the central nervous system by six days post-exposure, ivermectin has no effect because it does not readily cross the blood brain barrier except at very high dosages (2). Larvae still penetrating the abomasum, however, are readily killed (2). Treatment of deer with mature worms reduces the number of larvae shed in feces, indicating that ivermectin is effective against first-stage larvae in the lungs and perhaps on egg production or viability, however live adult worms still persist in the central nervous system (2).

According to masters thesis work by Sikarskie at Michigan State University, limited clinical trials of the use of oral albendazole feed at 25 mg/kg in the feed for two weeks, killed adult worms in the meninges of white-tailed deer (11).

Llamas infected with P. tenuis have been treated with anthelmintics including ivermectin and fenbendazole to kill the larval stages of the parasite and anti-inflammatory drugs such as flunixin, phenylbutazone or dexamethasone to decrease the inflammation in the neural tissue associated with migrating or dead larvae (6). In all instances, the animals deteriorated and required euthanasia in spite of treatment.
 

Control
Prevention of pasture contamination by white-tailed deer, and mollusk management are the recommended procedures for controlling P. tenuis in wild populations of white-tailed deer (4, 11). Control of the gastropod intermediates is not feasible nor practical because gastropods are present in a wide variety of environmental locations not readily reached by non-specific molluscicides and would not be desirable because gastropods are very important to the ecosystem (10). Controlling the nematode in the definitive host is also not a viable option because there are no known drugs effective against P. tenuis, and anthelmintic treatment of wild populations is generally not feasible (10). Double fencing and establishment of a sanitary central region, cordon sanitaire, has been used in quarantine stations to prevent access of either white-tailed deer or gastropods (11). The ground of the cordon sanitaire must be regularly harrowed or ploughed to keep it free of vegetation, with periodic application of molluscicides to prevent gastropod migration (11).
 

Significance
The geographical distribution of P. tenuis is very important to wildlife officials and game farm producers because it can cause significant mortality among cervids. It has been suggested that parelaphostrongylosis may be responsible for the decline of moose in some areas of the United States and Canada and is a major factor preventing the establishment of moose, elk, and caribou in areas populated by white-tailed deer (14). Presently, P. tenuis, is considered the greatest threat to game farm animals and provincial wildlife populations if it is accidentally introduced into Saskatchewan populations (1). Concern centers on the potential for translocating and establishing the parasite in nonendemic areas as a result of natural range expansion or translocation of infected hosts (4). Research has illustrated that the meningeal worm can successfully complete its life cycle in elk and that the larvae from such infections are viable and can serve as a source for subsequent infections in white-tailed deer and other elk (9). Current recommendations are that until reliable diagnostic procedures are available, importation of game species from areas where the parasite occurs should not occur (1). One must recognize that should the meningeal worm be introduced into an area free from the disease, it will be extremely difficult, if not impossible, to eradicate (1).

In order to establish quarantine protocols, research would need to be conducted to determine when and how frequently fecal sampling (1) or serological testing would need to be done. Contaminated enclosures used for holding ungulates would need to be kept free of white-tailed deer for a least one to two years and perimeter fences would need to be free of vegetation that could harbor gastropods which could travel into the pens to infect the enclosed animals (10).

Even if the worm did not cause devastation to common native species it would likely have a tremendous economic impact because of mortality, morbidity, responses to public inquiry, lost natural resources and potential threats to the domestic animal industry (1). Domestic goats appear to be exquisitely sensitive, often dying within a few days of infection, while sheep are considerably less susceptible (10). It is believed that cattle are one of the most resistant of the domestic species, although meningeal worms have been recovered from the central nervous system of healthy individuals and adult worms may reach the CNS before the cattle die (10). Although the role of aberrant hosts in sustaining P. tenuis populations or their role in translocating the parasite is not currently known, introduction of this parasite to domestic farms could have a substantial economic impact.

There is no indication that this parasite poses a risk to humans because it is not infective to humans and meat of infected animals is safe for human consumption (14).
 

Future research
According to W.M. Samuel at the University of Alberta, a variety of questions need to be answered in relation to this parasite (1). These include: Do free-ranging elk in eastern North America shed larvae in their feces? What are the specific boundaries of the meningeal worm distribution and what mechanisms delineate this geographic distribution? How susceptible are various native wild and domestic hosts to the meningeal worm? Hopefully, the answers to these questions will soon become clear and with the development of effective diagnostic tests Parelaphostrongylus tenuis infections will be readily prevented, treated or controlled.
 

References

  1. The review of wildlife disease status in game animals in North America, Saskatchewan Game Farmers Association and The Saskatchewan Game Farming Technical Advisory Committee, 1992.
  2. Kocan AA. The use of ivermectin in the treatment and prevention of infection with Parelaphostrongylus tenuis (Dougherty) (Nematoda: Metastrongyloides) in white-tailed deer (Odocoileus virginianus Zimmerman). Journal of Wildlife Diseases 1985; 21(4): 454-455.
  3. Development of blood tests for Elaphostrongylus cervi and Parelaphostrongylus tenuis in game-farmed animals. Agriculture Development Fund. 1996. Agriculture and Agri-Food Canada.
  4.  Fowler ME, Miller RE. Zoo & Wild Animal Medicine Current Therapy 4. Philadelphia: W. B. Saunders, 1999.
  5.  Bindernagel JA, Anderson RC. Distribution of the meningeal worm in white-tailed deer in Canada. Journal of Wildlife Management 1972; 36(4): 1349 - 1353.
  6. Scarratt WK, Karzenski SS, Wallace MA, et al. Suspected Parelaphostrongylosis in five llamas. Progress in Veterinary Neurology 1996; 7(4): 124 - 129.
  7. Dew TL, Bowman, DD, Grieve RB. Parasite-specific immunoglobulin in the serum and cerebrospinal fluid of white-tailed deer (Odocoileus virginianus) and goats (Capra hircus) with experimentally induce parelaphostrongylosis. Journal of Zoo and Wildlife Medicine 1992; 23:281 - 287.
  8. Pybus MJ, Samuel WM, Welch DA, et al. Mortality of fallow deer (Dama dama) experimentally infected with meningeal worm, Parelaphostrongylus tenuis. Journal of Wildlife Diseases 1992; 28(1): 95 - 101.
  9. Samuel WM, Pybus MJ, Welch DA, Wilke CJ. Elk as a potential host for meningeal worm:implications for translocation. Journal of Wildlife Management 1992; 56(4): 629 - 639.
  10. Davidson WR, Hayes FA, Nettles VF, et al. Lungworms (Anderson RC, Prestwood AK) In Diseases and Parasites of White-tailed Deer. Tallahassee: Tall Timbers Research Station,1981.
  11. Haigh JC, Hudson RJ. Farming Wapiti and Red Deer. St. Louis: Mosby, 1993.
  12. Ogunremi O, Lankester M, Kendall J, Gajadhar A. Serological diagnosis of Parelaphostrongylus tenuis infection in white-tailed deer and identificiation of a potentially unique parasite antigen. Journal of Parasitology; 85(1): 122 - 127.
  13. Raskevitz RF, Kocan AA, Shaw JH. Gastropod availability and habitat utilization by wapiti and white-tailed deer sympatric on range enzootic for meningeal worm. Journal of Wildlife Diseases 1991; 27(1): 92 - 101.
  14. http://www.dnr.state.mi.us/Wildlife/Divi...Publications/Disease_Manual/BRAINWM.html