Parelaphostrongylus Tenuis  (Meningeal Worm) 
Infection in Llamas and Alpacas
Prevention, Diagnosis & Treatment

David E Anderson, DVM, MS, Associate Professor
Department of Veterinary Clinical Sciences,
College of Veterinary Medicine,
The Ohio State University,
Columbus, Ohio 43210.

The meningeal worm (Parelaphostrongylus tenuis), also known as the deer worm or meningeal deer worm, frequently infects llamas and alpacas. Aberrant migration of the meningeal worm in susceptible hosts such as llamas and alpacas causes damage to the central nervous system and may result in death.

Identification and Life Cycle

The meningeal worm is a nematode parasite belonging to the family Protostrongylidae. The definitive host is the white-tailed deer (Odocoileus virginianus) prevalent throughout much of eastern North America.1 Adult meningeal worms reside in the meninges of white-tailed deer and rarely cause clinical signs of disease.1,2

Adult worms lay eggs in the meninges of white-tailed deer. The eggs then pass into the venous circulation and travel to the lungs where they hatch into first-stage larvae (L1). The L1 are coughed up, swallowed, and passed in the feces of infected deer. Larvae then invade or are ingested by snails or slugs (terrestrial gastropods). Snails and slugs serve as intermediate hosts in which the first stage larvae develop into infective third stage larvae (L3) over a period of 3-4 weeks.1-3

Infected snails or slugs are then ingested by susceptible aberrant hosts such as llamas, alpacas, goats, sheep, moose, wapiti, caribou, black-tailed deer, and red deer1, and the L3 are released in the digestive tract. Infective third stage larvae migrate to the spinal cord and continue to migrate aimlessly within the central nervous system causing neurologic disease.1-3

In the definitive host, the white-tailed deer, the infected snails or slugs are ingested and the L3 are released in the abomasum. The L3 then migrate to the spinal cord via the spinal nerves over the next 10 days. The larvae mature in the dorsal horns of the gray matter of the spinal cord for 20-30 days. Adult meningeal worms migrate to the subdural space, then to the brain through the dura mater and cranial venous sinuses.2 The prepatent period in deer is 82-92 days.2,4

Many snails and slugs prefer a moist or wet environment for survival. Consequently, low-lying and wet, poorly drained fields provide an increased risk of exposure to snails and slugs.3 However, exposure risk is not limited to wet climates since dry-land snails and slugs may serve as intermediate hosts. Snails and slugs feed on organic matter, leaf litter, and vegetation. Survival of L3 outside the intermediate host is believed to be short-lived unless water is available. Repeated freezing or desiccation has been shown to decrease survival of the infective L3.2 Therefore, the risk of exposure to llamas and alpacas is lowest when there are prolonged periods of dry-heat or deep freezes.

Clinical Disease

Once the aberrant host is infected, clinical disease begins 45-53 days later as demonstrated by experimental inoculation. 4 Clinical neurologic disease is the result of tissue destruction and inflammation caused by randomly migrating larvae. Thus, the clinical signs observed depend upon the location of the migrating larvae.3

Most commonly, clinical signs reflect asymmetrical, focal spinal cord lesions.4 These include hypermetria,2,5 ataxia,1,2,5,6 stiffness,1,2 muscular weakness,2,5,6 posterior paresis,2,6 paralysis,1,2 head tilt,2 arching neck,2 circling,1,2 blindness,1,2 gradual weight loss,2 apparent depression, seizures, and death.2 Clinical signs generally begin in the hind limbs and progress to the front limbs.2,4 The course of disease may be acute to chronic, ranging from death within days to ataxia which lasts months to years.2 In our experience, clinical sings of meningeal worm infection are exacerbated during summer months because heat stress develops with prolonged periods of recumbency.

Differential Diagnoses

Clinical signs suggestive of meningeal worm infection are non-specific and may affect the spinal cord or brain. Clinical signs of spinal cord lesions include weakness, ataxia, gait abnormalities, lameness, proprioceptive deficits, paresis, and paralysis. Differential diagnoses (Table 1) for camelids with these clinical signs may include vertebral body subluxation or fracture, vertebral body abscessation, trauma, spinal neoplasia, degenerative myelopathy, metabolic diseases such as copper deficiency in neonates, listeriosis, heat stress, and tick paralysis. Clinical signs of intracranial disease include ataxia, abnormal mentation (dementia, stupor, coma), visual abnormalities, circling, falling or rolling, weakness, delayed postural reactions, incoordination, head tilt, altered head and neck position, nystagmus, strabismus, and seizures. Differential diagnoses for camelids with these signs may include neoplasia, trauma, hydrocephalus or other congenital defects, cerebral abscessation, listeriosis, otitis interna, and polioencephalomalacia. Electrolyte imbalances such as hypocalcemia, hypomagnesemia, and hypoglycemia, ketosis, and dietary deficiencies such as copper, vitamin A, vitamin E, selenium, calcium, magnesium, potassium, and phosphorus may each present neurologic signs of disease. In addition, consider toxicoses such as lead poisoning, ingestion of poisonous plants, and salt poisoning. Rabies encephalitis may present with a variety of neurologic signs and should be considered in any neurologic case. These differential diagnoses must be ruled out prior to making a presumptive diagnosis of meningeal worm infection. Although consistent clinical signs and CSF eosinophilia are highly suggestive of meningeal worm infection, antemortem diagnosis of aberrant Parelaphostrongylus tenuis migration is often a diagnosis of exclusion.

Diagnostic Testing

To thoroughly evaluate the patient, collect a database of information which includes the signalment, history including the onset and progression of clinical signs, complete blood count, and serum chemistry profile. Additional diagnostic testing include vertebral radiography, cerebrospinal fluid (CSF) analysis and culture, CSF creatine kinase activity, and plasma fibrinogen concentration. In select cases, advanced diagnostic testing such as myelography, X-ray computed tomography (CT), magnetic resonance imaging (MRI), or electromyography (EMG) may be indicated to rule-out other causes of spinal or intra-cranial disease.

Diagnosis of Meningeal Worm

A presumptive diagnosis is based upon clinical signs consistent with meningeal worm infection, history of exposure to areas inhabited by white-tailed deer, and response to treatment.2,6 No consistent abnormalities in CSF total protein or glucose concentrations, AST or CK activities were identified in llamas experimentally infected with P. tenuis4 (Table 2). The only consistent abnormality was a shift in nucleated cell count from predominantly lymphocytes and monocytes to eosinophils over the course of infection.4,9

The presence of clinical signs and CSF eosinophilia may be used to make a tentative diagnosis of P. tenuis infection in llamas.2,4,6,7 Cerebrospinal fluid analysis may show eosinophilia, but absence of eosinophilia on CSF analysis does not rule out the diagnosis of meningeal worm infection.2,5,6 However, CSF eosinophilia in llamas has been most consistently reported in cases of clinical parelaphostrongylosis.2,6,9 Hematologic samples may show peripheral eosinophilia but frequently show no abnormalities.2,6

One study showed a significant P. tenuis - specific serum antibody response in goats experimentally infected with 50 P. tenuis L3.8 Serum antibody titers were highest 8 weeks after infection. Results of this study suggest that a serum enzyme-linked immunosorbent assay (ELISA) using antigens of adult P. tenuis would be beneficial in the diagnosis of clinical parelaphostrongylosis in goats.2 Modification of this test may show promise in detecting parelaphostrongylosis in llamas.2,9

Definitive diagnosis of meningeal worm infection is made at necropsy. A confirmed diagnosis requires microscopic demonstration of the larvae within the brain or spinal cord.2,9 Microscopic examination of brain and spinal cord tissue may also show linear paths of tissue damage or inflammation suggestive of migrating tracts made by the larvae.6

Therapy

Treatment of meningeal worm infection is most successful when instituted early in the course of disease. A treatment regime (Table 3) which has proven successful at the Ohio State University involves fenbendazole (20 to 50 mg/kg body weight, PO, q24h for 5 days) and flunixin meglumine (1 mg/kg, IV, IM, or SC, q12h for 5 days) or dexamethasone in non-pregnant females and males (0.1 mg/kg, IV, IM, or SC, q24h for 3 days). DMSO (1g/kg given in 500 ml of 5% dextrose solution, IV, q24h) given to effect is useful in some cases but may cause severe appetite suppression. Discontinue DMSO if inappetance or anorexia occurs. Vitamin E, selenium, Vitamins B-complex, and Vitamin A are useful to assist healing of neural tissues.

Dexamethasone should not be administered to pregnant females because this drug may induce abortion. Alternatively, we have used prednisolone sodium succinate (0.5-1.0 mg/kg, IV, IM, or SC, q12h) for no more than three days in pregnant females without subsequent abortion. Prednisolone sodium succinate may have a reduced risk of abortion compared to dexamethasone because it lacks a carbon-16 substitution. Corticosteroids lacking a C-16 substitution may not cross the blood-placental barrier and large doses for prolonged periods of time may be required to terminate pregnancy.10

Ivermectin is most effective against larval stages prior to their entrance into the spinal cord, since it does not readily cross the blood-brain barrier.1,2,11 However, damage to nervous system tissues during larval migration may alter the blood-brain barrier. Although no clinical problem has been identified to date, we have been concerned for the possibility of ivermectin toxicity in these cases. The antiinflammatory drugs are critical to reduce the inflammation associated with the presence of the migrating larvae and the subsequent inflammatory response to the killed larvae. Use of antiinflammatory drugs is important to prevent the clinical signs from becoming more severe after instituting treatment.

In addition to drug therapy, supportive care and physical therapy are essential to aiding recovery. Using slings to support llamas that are unable to stand and performing physical therapy for muscles are beneficial. We also have used hydrofloatation therapy to facilitate recovery after prolonged recumbency (Figure 1). A great deal of perseverance is required to care for severely affected llamas; recovery may take several weeks to months to years.2

Prognosis

Prognosis for survival depends upon how severe the clinical signs become. In our experience, llamas that are unable to stand have a poor prognosis (10-20% recovery); llamas that are able to stand unaided have a fair to good prognosis (75-85% recovery). Llamas that survive clinical disease do not seem to develop patent infections and are unlikely to pose a health risk to other animals.2,3 Many animals suffer permanent neurologic deficits but may remain productive members of the herd for breeding and pets.

Prevention

Prevention of meningeal worm infection may be difficult. Ideally, llamas should not graze the same pasture as white-tailed deer.2,9 However, in many areas of the United States, it is not feasible to separate the two populations. Placing a deer-proof fence may offer some protection, but many fences do not present a sufficient barrier to prevent movement of deer.1,2 Additionally, thick ground cover can be removed to expose the environment to fluctuations in temperature, and vegetation-free buffer zones (i.e. gravel, limestone) can be placed around fencelines to reduce migration of snails and slugs into the pasture.2,9 Molluscicides may be considered to destroy snails and slugs which serve as intermediate hosts, thereby interrupting the life cycle of the meningeal worm and preventing infection in aberrant hosts.1 Drainage should be established in low lying areas and access to swampy areas may be restricted by fencing off these areas. These compounds present a potential environmental risk from contamination of ground water and may be toxic if consumed by camelids or other animals.

Prophylactic treatment against migrating larvae may be achieved administration of ivermectin (0.2 mg/kg) every 30 to 45 days during the high risk periods or throughout the year regions which have mild summers and winters. Anthelmintic resistance is unlikely to become a problem in the meningeal worm because these infections do not become patent.2 However, meningeal worm infection has occurred in some herds that maintain vigilant prophylaxis. These "breaks" in prevention of the larval migration may have been caused by insufficient dosing of anthelmintic, accidental failure to administer the anthelmintic, or some unknown mechanism.

Conclusion

Meningeal worm infection may be severely debilitating and potentially fatal, but infection can be effectively prevented. Routine dewormings every 4-6 weeks, minimized cohabitation with white-tailed deer, and a clean, dry environment unfavorable for the growth of snails and slugs will considerably reduce the herdís risk of infection with the meningeal worm.

References

  1. Fowler, ME: Medicine and Surgery of South American Camelids. Ames, Iowa:Iowa State University Press 161-162; 1989.
  2. Pugh, DG et al: Clinical parelaphostrongylosis in llamas. Compendium on Cont. Ed. for Pract. Vet. 17:600-606;1995.
  3. Smith, MC et al: Goat Medicine. Philadelphia:Lea & Febiger 150; 1994.
  4. Rickard, LG et al: Experimentally induced meningeal worm (Parelaphostrongylus tenuis) infection in the llama (Lama glama): Clinical evaluation and implications for parasite translocation. J Zoo Wildl Med 25:390-402; 1994.
  5. Foreyt, WI et al: Experimental infections of two llamas with the meningeal worm (Parelaphostrongylus tenuis ). J Zoo Wildl Med 23:339-344;1991.
  6. Baumgartner, W et al: Parelaphostrongylosis in llamas. J Am Vet Med Assoc 187:1243-1245;1985.
  7. Welles, EG et al: Composition of cerebrospinal fluid in healthy adult llamas. Am J Vet Res 55:1075-1079;1994.
  8. Dew, TL et al: Parasite-specific immunoglobulin in the serum and cerebrospinal fluid of white-tailed deer (Odocoileus virginianus) and goats (Capra hircus) with experimantally induced parelophostrongylosis. J Zoo Wildl Med 23:281-287;1992.
  9. Rickard, LG. Parasites. Vet Clin North Am Food Anim Pract 10:239-247;1994.
  10. MacDiarmid, SC. Clinical pharmacology of the female reproductive tract: manipulation of parturition, its sequeslae and infections. Clinical Pharmacology and Therapeutics Proceedings 71:21-45;1984.
  11. Kopcha, M et al: Cerebrospinal nematodiasis in a goat herd. J Am Vet Med Assoc 194:1439-1442;1989.

    More Meningeal Worm Information

    From Dr. Stephen R. Purdy, DVM - Chester, Vermont:
    Meningeal Worm - Diagnosis, Treatment, & Prevention

    From Dr. David Anderson, DVM - Ohio State University
    Meningeal Worm - Infection In Llamas & Alpacas

    From Dr. David Anderson, DVM - Ohio State University
    Prognosis, Diagnosis, & Treament

 


 

Treatment for Meningeal Worm - August, 2003
David E Anderson, DVM, MS, DACVS
Head and Associate Professor of Farm Animal Surgery
Director, International Camelid Initiative
Ohio State University
College of Veterinary Medicine

Our current TREATMENT protocol is:

Fenbendazole (Panacur or Safeguard) at 50 mg/kg body weight orally daily for 5 days
Flunixin (Banamine) 1 mg/kg body weight subQ, twice daily for 3 days, once daily for 3 days
Vitamin E supplement 500 to 1000 units orally daily for 14 days
Omeprazole (Gastrogard) 2 to 4 mg/kg orally daily 7 to 10 days
Physical therapy.  (Hints on how to make a sling to raise the llama)

Note:
Ivermectin or Dectomax are good for PREVENTION, not TREATMENT. Neither of these drugs enters the central nervous system which is where the worms are in CLINICAL cases.

This most recent article was sent out in May, 2001, by Dr. David Anderson from Ohio State University.

"This article is from Dr. Cliff Monahan, our parasitologist researching camelids. He says some thought provoking things! (Cliff Monahan, DVM, PhD; Dept. Veterinary Preventive Medicine; Ohio State University College of Veterinary Medicine)".

"Parelaphostrongylus tenuis is a very real concern in areas of the east where white-tail deer are prevalent. My talk will focus on the biology of the parasite, the epidemiology of the disease seen in camelids within the Ohio River Valley, and control programs that may be more relevant than the monthly treatments presently employed. These monthly treatments as a preventive program have led to drug resistance in the nematodes normally infecting several susceptible species. This highlights the need to have alternatives to the intensive anthelmintic prevention program used today.

Life Cycle: Parelaphostrongylus tenuis utilizes the white-tail deer as its definitive host and has an indirect life cycle, meaning there is an obligatory developmental stage in snails or slugs. The disease CANNOT be passed without the ingestion of an infected snail or slug. First-stage larvae are passed in the feces of P. tenuis infected WTD and these must be ingested by gastropods for development into the infective 3rd stage larvae. Once ingested by snails or slugs, the 1st stage larvae require warmth to develop, thus the rate of development will depend on the ambient temperature. Continued cold weather slows development. Next the snail or slug must be ingested by a susceptible WTD, or in the case of aberrant infections, ingested by a susceptible sympatric ruminant. Without ingestion of the gastropod carrying infective 3rd stage larvae, the infection is not transmitted. Many snails and slugs are consumed inadvertently by grazing or browsing animals, but only during parts of the year conducive to snails and slugs. Gastropods will be less active during cold weather, will hibernate during freezing weather, and will estavate during hot, dry weather.

Clinical cases of meningeal worm affecting camelids have followed a distinct pattern of disease here at the Ohio State University Veterinary Teaching Hospital -- This pattern may not exist in your area!!!! Two major peaks of disease are seen by Dave Anderson here at Ohio State, the major peak being Sept/Oct, the second during Jan/Feb. This implies that there are 2 peak seasons of transmission to correspond with the peaks of disease. During studies conducted at the Wilds in southeastern Ohio, we found that there were no snails or slugs present during freezing temperatures, and the numbers of gastropods increased in the spring as weather warmed, but it remained moist and relatively cool. The heat and dryness of mid summer drove the snails and slugs into estavation, then they reappeared when temperatures cooled again in late summer, early autumn.

Based on the 2 peaks of disease here at Ohio State, the necessity of gastropods for transmission of P. tenuis and the 2 peaks of gastropods on pasture, we speculate that the most important times for meningeal worm prophylaxis are these 2 times when gastropods are most prevalent.

This is relevant here in the Ohio River Valley. YOUR area may have some variation on the prevalence of gastropods, thus you MUST adapt these findings to your own area. Further north there may be shorter periods, and further south longer periods.

These recommendations are made in light of the relative risks of P. tenuis transmission and the very likely risk of developing drug resistant llama and alpaca parasites secondary to overuse of ivermectin or other macrocyclic lactones.

Please pay attention to what I am really saying:

1) Overuse of the avermectins (as I see regularly within the camelid industry because of meningeal worm prevention programs) is destined to create more problems than P. tenuis. If these practices create drug resistant camelid parasites by the monthly use of ivermectin, these parasites will be resistant to doramectin and moxidectin as well. The industry will be better served to avoid this eventuality.

2) Due to the seasonality of snails and slugs in our area, I recommend that camelid owners consider using drugs for prophylaxis during the peak risk timepoints, and I recommend that they do not use ivermectin year round for this purpose. This program does not give you 100% protection, but I can tell you all that the creation of drug resistant camelid parasites will be much more a problem.

3) My theoretical position is that camelid owners can use a long-acting macrocyclic lactone, such as doramectin, and this will reduce the number of treatments needed for protection. By reducing the overall number of treatments, you will delay or avoid the development of drug resistance.

IF YOU USE THESE LONG-ACTING DRUGS IN THE SAME FASHION THAT YOU USE IVERMECTIN, YOU DEFEAT THE PURPOSE AND ENHANCE THE DEVELOPMENT OF DRUG RESISTANCE!!!

4) Theoretically, you could inject an animal on May 1st and this would kill any migrating larvae on-board since April 1st. As our preliminary research shows us that there are not many infected snails or slugs present in April, this risk seems reasonable. The long-acting effect of doramectin in cattle kill any infective larvae ingested on pasture for approximately 28 days. I am speculating that the same level of protection will be provided to camelids, thus you do not need to treat again for almost 60 days.

Why 60 days? Theoretically, no ingested larvae will survive while the long-acting drugs are at these levels. After the 28 days of protection have elapsed, you should have ~ 30 day period when any ingested larvae are migrating and susceptible to treatments. I admit this must be verified with experiments in camelids, but this is a rational expectation. So, your injection on May 1st is good until May 29th based on residual activity, then you may add another 30 days before you need to treat again. This means 1 treatment every 60 days instead of every 21 days that I hear regularly."

Another Article From Dr. David Anderson, DVM - Ohio State University:
"Meningeal worm (Parelaphostrongylus tenuis) represents a significantly different problem to llamas. These worm larvae are passed through the feces of deer (natural reservoir), are consumed by snails, and then are consumed by llamas and alpacas. Llamas are not the normal host for these worms and they perform "aberrant migration". During this migration, they may travel into the spinal cord and cause significant harm to the host - even causing lethal consequences. Fencing deer out of the pasture is not enough and chemicals to kill snails cause environmental residues that may be harmful and are of limited efficacy. Therefore, most prevention against meningeal worm larval infection is aimed at killing the larvae during their migration, but prior to entry into the spinal cord. This requires a de-worming frequency of at least every 4 to 6 weeks at least during the high risk periods of the year (April-May through November-December in Ohio). The most efficacious anthelmintics for protection against meningeal worm have been ivermectin (1 cc of 1% ivermectin per 100 pounds body weight, injected under the skin, every 4 to 6 weeks) or fenbendazole (4.5 cc of 10 % fenbendazole per 100 pounds body weight, given orally, once daily for 3 to 5 days)."

From Dr. Stephen R. Purdy, DVM - Chester, Vermont:
Meningeal Worm - Diagnosis, Treatment, & Prevention

From Dr. David Anderson, DVM - Ohio State University
Meningeal Worm - Infection In Llamas & Alpacas
Meningeal Worm - Infection In The Ohio River Valley
Meningeal - Prevention Diagnosis, & Treatment

Treatment for Meningeal Worm - 
From Dr. Norman Evans Field Manual - June 2003

"This manual expresses my current opinions as of June 20, 2003.") 
Treatment for m-worm as Ivomac or Dectomax at 1 cc.25 lb body weight SQ every 24 hours for 3 times along w/ Banamine at 1 cc/100 lb every 24 hours for 3 times. This treatment protocol has shown some promise when used early." 
 "When used early, 90% DMSO at 30 cc/100 lbs body weight diluted in 1000 cc fluids and administered IV for 3 days has shown nice results." 
 


 

 

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