Parelaphostrongylus tenuis

Parelaphostrongylus tenuis (also known as meningeal worm or brainworm) is a neurotropic nematode parasite common to white-tailed deer, Odocoileus virginianus, which causes damage to the central nervous system.[1][2][3] Moose (Alces alces), elk (Cervus canadensis), caribou (Rangifer tarandus), mule deer (Odocoileus hemionus), and others are also susceptible to the parasite, but are aberrant hosts and are infected in neurological instead of meningeal tissue. The frequency of infection in these species increases dramatically when their ranges overlap high densities of white-tailed deer.[4]

Parelaphostrongylus tenuis
Scientific classification
Kingdom:
Animalia
Phylum:
Nematoda
Class:
Secernentea
Order:
Strongylida
Family:
Protostrongylidae
Genus:
Parelaphostrongylus
Species:
P. tenuis
Binomial name
Parelaphostrongylus tenuis
Dougherty, 1945

The lifecycle begins in infected meningeal tissues in the central nervous system (CNS) where adult brainworms lay eggs. The eggs are dislodged from the CNS and pass into the lungs, where they hatch. The larvae are then coughed up, swallowed, and proceed through the gastrointestinal tract. Snails and slugs then serve as intermediate hosts, which are later eaten by ungulates, allowing the process to continue.[3][5] Changes in climate and habitat beginning in the early 1900s have expanded range overlap between white-tailed deer and moose, increasing the frequency of infection within the moose population.

Lifecycle

The lifecycle of P. tenuis is complex and multistaged.

Adults lay eggs on the dura mater (the outer layer of the meninges) of the brain or directly into the bloodstream of an infected host.[4] The eggs hatch into first-stage larvae, which travel in the bloodstream to the lungs, where they travel up the respiratory tract, are swallowed, and then pass out of the body in the mucus coating of fecal pellets.[4][6]

Gastropods such as snails and slugs feed upon the mucus coating of the fecal pellets and ingest the larvae.[4][6] While in the gastropod, the larvae develop into second- and third-stage larvae, which are capable of infection.[6]

Gastropods carrying second- and third-stage larvae may be accidentally ingested with plants, which results in the larvae being transmitted to a new host. The larvae then move into the new host's stomach wall and make their way to the CNS, as in white-tailed deer, or the brain as in other ungulates. Once in these tissues, they develop into their adult third stage of life and lay eggs to begin the cycle again.[4][6]

Transmission

Adults of P. tenuis can persist for many years in a single host, which allows for many first-stage larvae to be shed in feces.[1][7] It is quite common in many populations of white-tailed deer, which have built up a strong resistance.[4] After gastropod ingestion, moose or other deer may be hosts of the second- and third-stage worms. Moose resistance to P. tenuis is much lower than white-tailed deer, which results in a higher mortality rate.[8]

Infected deer density, temperature, climate conditions, and length of transmission periods all affect transmission levels.

  • Areas with higher deer populations experience dramatic increases in incidental brainworm larvae consumption.[9]
  • The temperature and climate conditions of summers can regulate gastropod abundance, with hot, dry summers reducing populations and cool, dry summers increasing populations.[10]
  • High or low gastropod populations directly affect the transmission rate of larval worms to new hosts. Hot, dry summers also reduce the survival numbers of first-stage larvae on fecal pellets.[8]
  • Variation of transmission periods is based on the time when snow is absent from the ground. Gastropods are dormant during snow periods, thus first-stage worms cannot be transmitted to additional hosts.[8] So, shorter seasons of snow are met with longer transmission periods of increased potential for transmission through the intermediate vector gastropods.

Symptoms/clinical signs

Brainworm affects neurological and behavioral responses. Deer rarely show any external symptoms of P. tenius infection due to their high acquired resistance. Moose, however, have low resistance, and may show a number of symptoms. Though infrequent, cases of moose recovering from brainworm infection have been reported. In both deer and moose, symptom severity does not necessarily vary with severity of infection.

  • Infected individuals may not have any external symptoms.
  • Mild symptoms may include slower movements and response time, frequent stumbling, unusually tilted head, and emaciation.
  • Severe symptoms include extreme weakness, lameness, walking in circles, partial or whole blindness, loss of fear for humans, ataxia, and mortality.

Several other ungulates are susceptible to brainworm infection, including elk, caribou, mule deer, sheep, goats, alpacas, rarely cattle, and rarely horses. Severe neurological damage similar to that of infected moose is shown to occur in these species.

Diagnosis

Presently, a commercial antibody test that can detect P. tenuis antemortem does not exist.[11][12] Diagnosis in deer can be conducted by analyzing fecal pellets for larval P. tenuis, or post mortem necropsy to detect presence of adult P. tenuis in the brain cavity or second- and third-stage worms along the spinal cord.[1][9][10] However, brainworm larvae are difficult to distinguish from other parasitic worm species that can also be found in fecal pellets,[13] so detection of adult worms through necropsy is recommended. Diagnosis in moose is conducted with necropsy to detect worms in the brain or spinal cord.[6][13] Diagnosis in horses can be conducted with postmortem samples used for polymerase chain reaction (PCR) testing.[11][14] Positive PCR results show evidence of P. tenuis infecting equines.[11][14] In veterinary patients, such as goats, an eosinophilic pleocytosis can be suggestive of P. tenuis infection.[15][16]

History

In 1912, an unknown neurological disease affecting moose was first reported in Minnesota.[17] Major declines in the moose population were reported, 1925–27 and 1933–34, following the discovery of this unknown disease. In 1963, a meningeal brainworm, Pneumostrongylus tenuis, was determined as the etiological agent causing neurological disease in moose. Around 1971, taxonomists reclassified it as Parelaphostrongylus tenuis.[18][19][20]

White-tailed deer populations in the eastern United States are now known to be commonly infected with meningeal worm. Infection in the southeastern and western United States is less common. This disease has also been found in the Canadian provinces of Saskatchewan, Manitoba, and Nova Scotia.[21] The grassland biomes of the United States and Canada apparently act as a barrier to the movement of the disease. Evidence from Canada seems to support this, since the western distribution of meningeal worm has changed little since the 1960s.[10][22]

Epidemiology

The geographic ranges of moose and white-tailed deer were historically separate prior to the 20th century.[1][9] Moose are well adapted to winter survival, whereas deer are not. They could not withstand the harsh winters in these regions of the northeastern United States and the southeastern provinces of Canada.[8] Deer populations began to move into the southern portions of moose range in the early 1900s following changes in climate,[10] logging, mining, forest fires, and increasing human development.[1][9] High-quality deer habitat associated with these changes has led to dramatic increases in deer abundance in these regions.[1][9]

White-tailed deer are the normal host of the P. tenuis parasite and are immunologically adapted to its presence. Deer and P. tenuis have coadapted in an evolutionary arms race over time. Deer remain largely unaffected by the presence of P. tenuis because of the immunity they have built as a result of coadaptation.[4][23] The prevalence and infection rate of P. tenuis in deer is density dependent; increased rates of infection by the parasite are the result of higher deer densities.[1][9]

Moose populations on the southern fringes of their range have recently experienced dramatic declines. As deer encroached upon the southern fringes of moose range, they introduced the parasite to a naïve host, the moose.[13] Upon transmission of the pathogen into moose, the worm causes cerebrospinal nematodiasis, a disease of the nervous system that often results in death.[4] P. tenuis may be one factor that has contributed to moose declines in southern portions of their range. This disruption of host-pathogen dynamics due to habitat alterations has promoted the spread of this parasite to a naïve host and has potentially contributed to declines in moose abundance and productivity in regions with high deer densities.[8] Continued increase in deer abundance and density in the southern fringes of moose range are predicted to facilitate sustained transmission of P. tenuis to moose. Continued transmission of deer-related parasites, coupled with low productivity, habitat degradation, and a northward shift in the moose thermonuetral zone, leads to a troubling prognosis for southern moose populations.[13] Murray et al. (2006) predict, if current trends continue, moose populations in these regions will not be viable and population declines will persist.

Treatment

Currently, there is no definitive treatment for P. tenuis in mammals, though research is still being conducted. The use of anthelmintics (ivermectin and fenbendazole) have been attempted in white-tailed deer. The results indicate, however, that ivermectin was ineffective against larvae that had already reached the spinal cord.[24] Fenbendazole and ivermectin, combined with anti-inflammatory therapy have been used to manage infections in goats.[25][26]

Current and past research

The majority of moose brainworm research in North America has been conducted in northern Minnesota, where a historical moose population of 4,000 to 5,000 moose had declined to an estimated 1,200 individuals by 1997.[23] In this region, wildlife managers are challenged to predict and attempt to mitigate moose declines resulting from deer-related pathogens. Because no effective methods to prevent the transmission or infection of brainworm in moose have been found, managers have focused their efforts on decreasing deer densities in these regions.[9] The Minnesota DNR identified that population densities greater than 12 deer/square mile result in increased moose mortality as a result of brainworm. Managers in these areas are responsible for evaluating suitable habitat for moose and deer, as well as setting management priorities and population goals to decrease the transmission of Parelaphostrongylus tenuis in moose.[23] Though the main focus of research has been on white-tailed deer and moose, research has found that the guinea pig can be used as an experimental model of P. tenuis infection.[27]

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References
  1. Duffy MS, Greaves TA, Keppie NJ, Burt MD (April 2002). "Meningeal worm is a long-lived parasitic nematode in white-tailed deer". Journal of Wildlife Diseases. 38 (2): 448–52. doi:10.7589/0090-3558-38.2.448. PMID 12038147.
  2. Smith MC, et al. (1994). Goat Medicine. 150. Lea & Febiger.
  3. ""Brain Worm" (Meningeal Worm) Infestation in Llamas and Alpacas". University of Tennessee. Retrieved 2013-11-14.
  4. "DNR - Brainworm". Michigan DNR. Retrieved 2013-10-24.
  5. Fowler ME (1989). Medicine and Surgery of South American Camelids: Llama, Alpaca, Vicuna, Guanaco (First ed.). Ames, IA: Iowa State University Press. ISBN 978-0813803937. Retrieved January 18, 2017.
  6. "Brain worm". New York State Department of Environmental Conservation. Retrieved 2013-10-24.
  7. Karns PD, Jordan PA (1969). "Pneumostrongylus tenuis in moose on a deer-free island". The Journal of Wildlife Management. 33 (2): 431–433. doi:10.2307/3799850. JSTOR 3799850.
  8. Lankester MW (2010). "Understanding the Impact of Meningeal Worm, Parelaphostrongylus tenuis, on Moose Populations". Alces. 46: 53–70. Retrieved January 18, 2017.
  9. Karns, P.D. (1967). "Pneumostrongylus tenuis in deer in Minnesota and implications for moose". Journal of Wildlife Management. 31 (2): 299–303. doi:10.2307/3798320. JSTOR 3798320.
  10. Wasel SM, Samuel WM, Crichton V (April 2003). "Distribution and ecology of meningeal worm, Parelaphostrongylus tenuis (Nematoda), in northcentral North America". Journal of Wildlife Diseases. 39 (2): 338–46. doi:10.7589/0090-3558-39.2.338. PMID 12910761.
  11. Mittelman NS, Divers TJ, Engiles JB, Gerhold R, Ness S, Scrivani PV, Southard T, Johnson AL (May 2017). "Parelaphostrongylus tenuis Cerebrospinal Nematodiasis in a Horse with Cervical Scoliosis and Meningomyelitis". Journal of Veterinary Internal Medicine. 31 (3): 890–893. doi:10.1111/jvim.14691. PMC 5435076. PMID 28317172.
  12. Dobey CL, Grunenwald C, Newman SJ, Muller L, Gerhold RW (November 2014). "Retrospective study of central nervous system lesions and association with Parelaphostrongylus species by histology and specific nested polymerase chain reaction in domestic camelids and wild ungulates". Journal of Veterinary Diagnostic Investigation. 26 (6): 748–54. doi:10.1177/1040638714553427. PMID 25274743.
  13. Murray DL, Cox EW, Ballard WB, Whitlaw HA, Lenarz MS, Custer TW, Barnett T, Fuller TK (2006). "Pathogens, nutritional deficiency, and climate influences on a declining moose population". Wildlife Monographs. 166 (1): 1–30. doi:10.2193/0084-0173(2006)166[1:PNDACI]2.0.CO;2.
  14. Tanabe M, Gerhold RW, Beckstead RB, de Lahunta A, Wade SE (July 2010). "Molecular confirmation of Parelaphostrongylus tenuis Infection in a horse with verminous encephalitis". Veterinary Pathology. 47 (4): 759. doi:10.1177/0300985810363488. PMID 20581347.
  15. Breuer, Ryan; Merkatoris, Paul; Tepley, Samantha; Dierks, Caitlyn; Klostermann, Cassandra; Flaherty, Heather; Smith, Joseph (2019-01-01). "Treatment of cerebrospinal nematodiasis in a Boer Buck". Veterinary Record Case Reports. 7 (1): e000706. doi:10.1136/vetreccr-2018-000706. ISSN 2052-6121.
  16. Smith, Joe; Kreuder, Amanda; Breuer, Ryan; Still-Brooks, Kelly (2019-08-12). "Meningeal Worm Infection in Central Iowa Goat Herds II: Individual Cases and Treatment Using a Camelid Therapeutic Protocol". Animal Industry Report. 2019 (1).
  17. Fenstermacher R, Jellison WL (1933). "Diseases affecting moose". University of Minnesota Agriculture Exponent State Bulletin. 6.
  18. Anderson RC (1964). "Neurologic disease in moose infected experimentally with Pneumostrongylus tenuis from white-tailed deer". Pathology. 1 (4): 289–322. doi:10.1177/030098586400100402.
  19. Loken KI, Schlotthauer JC, Kurtz HJ, Karns PD (1965). "Pneumostrongylus tenuis in Minnesota moose (Alces alces)". Bulletin Wildlife Disease Association. 1 (2): 7.
  20. Botzler RG, Brown RW (2014). Foundations of Wildlife Diseases. Univ. of Calif. Press. p. 62.
  21. Benson DA, Dodds GD (1997). The deer of Nova Scotia. Province of Nova Scotia: Department of Lands and Forests. Cited in: Telfer ES (2004). "Continuing environmental change-An example from Nova Scotia". The Canadian Field-Naturalist. 118 (1): 39–44. doi:10.22621/cfn.v118i1.880.
  22. Bindernagel JA, Anderson RC (1972). "Distribution of the meningeal worm in white-tailed deer in Canada". The Journal of Wildlife Management. 36 (4): 1349–1353. doi:10.2307/3799283. JSTOR 3799283.
  23. Peterson B (1997). "Moose Walking in Circles" (online pdf of print issue). The Minnesota Volunteer (September–October): 24–31. Retrieved January 18, 2017.
  24. Kocan AA (October 1985). "The Use of Ivermectin in the Treatment and Prevention of Infection with Parelaphostrongylus tenuis (Dougherty) (Nematoda: Metastrongyloidea) in White-tailed Deer (Odocoileus virginianus Zimmermann)". Journal of Wildlife Diseases. 21 (4): 454–455. doi:10.7589/0090-3558-21.4.454. PMID 3841163.
  25. Smith, Joe; Kreuder, Amanda; Breuer, Ryan; Still-Brooks, Kelly (2019-08-12). "Meningeal Worm Infection in Central Iowa Goat Herds II: Individual Cases and Treatment Using a Camelid Therapeutic Protocol". Animal Industry Report. 2019 (1).
  26. Breuer, Ryan; Merkatoris, Paul; Tepley, Samantha; Dierks, Caitlyn; Klostermann, Cassandra; Flaherty, Heather; Smith, Joseph (2019-01-01). "Treatment of cerebrospinal nematodiasis in a Boer Buck". Veterinary Record Case Reports. 7 (1): e000706. doi:10.1136/vetreccr-2018-000706. ISSN 2052-6121.
  27. Haigh JC, Mackintosh C, Griffin F (2002-08-01). "Viral, parasitic and prion diseases of farmed deer and bison". Revue Scientifique et Technique de l'OIE. 21 (2): 219–248. doi:10.20506/rst.21.2.1331. PMID 11974612.
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