Surveillance Vol.22 No.1 1995

Elaphostrongylus cervi and its close relatives; a review of protostrongylids (Nematoda, Metastrongyloidea) with spin y-tai led Iarvae

Elaphostrongylus cervi is a par- . The adult worms of the species that came infested, but 12 of the 14 asite of red which, although of no clinical do not infest the lungs are often very calves inoculated with larvae originating significance to farmed deer in New Zealand, difficult to find in the tissues of their from reindeer did become infested. These is important because of its impact on the host. authors believe their results indicate that export of live to some Concurrent infestation with two or several species of Elaphostrongylus infest This nematode belongs to the family Proto- more species may occur in the same palaearctic cervids. They argued that the strongylidae and its first stage larvae have a definitive host. names E. cerviand E. rangiferibe reserved distinctive dorsal spine on the tail. The first stage larvae of many species for worms from red deer and reindeer The protostrongylid family compris- are morphologically very similar. respectively, and that the worms from es 12genera,sevenof which produce first Anthelmintic treatment is seldom may belong to an undescribed stage larvae with a dorsal spine on the 100% effective at killing the parasites species. tail. Protostrongylids with spiny-tailed in the definitive host, but may sup- A new species, E. alces, was described larvae are significant parasites of deer in press larval production for a variable from moose in Sweden by Steen et al. in some parts of the world. Currently, only length of time. 1989(9).These authors present morpho- two protostrongylid species with spiny- Correct diagnosis of the causative or- logical data distinguishing E. alces from tailed larvae, E. cervi and Varestrongylus ganism can be difficult. E. rangiferi and E. cervi. sagittatus, have been recorded in deer in Most protostrongylid species appear Later, Gibbons et al.(1o)revised the ge- New Zealand. Other species could be to have a limited range of definitive host nus Elaphostrongylus. They confirmed the present but unrecognised, although this species in which they can complete their validity of the three species E. cervi, E. is unlikely, or they could be introduced life cycle. Some species, however, are rangiferi and E. alces from Cewus elaphus, in live imported deer. able to infest unsuitable mammalian spe- Rangifer tarandus and Alces alces respec- This review of the protostrongylids cies where they often cause disease, even tively, and redescribed the species using which produce first stage larvae with a though they are unable to complete their light and scanning electron microscopal dorsal spine on their tail is not exhaus- life cycle in the infested mammal. techniques. They believe the literature tive. It concentrates on members of the The seven protostrongylid genera that indicates host specificity. They syno- family that are important to deer and produce spiny-tailed larvae are Elaphos- nymised E. panticola with E. cervi. potentially important to New Zealand. trongylus, Varestrongyli*s,Parelaphostrong- Elaphostrongylus is known in North That is, the two species we have here, and ylus, Muellerius, Cystocaulus, Pneumocau- America only from central Newfound- the species we do not want to accidental- lus and Pneumostrongylus. They will each land, where it was probably introduced ly introduce with live imports. Where be considered in more detail below. with reindeer brought from Norway(Il). possible, reference is made to the most The five protostrongylid genera with The species involved is most probably E. recent review of a topic rather than trying first stage larvae which lack a spine on ~angiferi(~J~),an opinion deferred to by to include all references. the tail are Protostrongylus, Spiculocaulus, Carreno and Lankester when they de- Two valuable sources of information Neostrongylus, Skrjabinocaulus and Orthos- scribe the morphology of E. rangiferi oc- have been Anderson's recently published trongylus. The only species from this curring in woodland caribou (Rangifer book on nematode parasites, and Samu- group to be identified in New Zealand is tarandus caribou) and moose in New- el's bibliography on meningeal worm Protostrongylus rufescens, which was re- foundland.(I2) and its close relative^'^,^'. The nomencla- cently recovered from sheep.(6) In this review I am taking the increas- ture used here follows the C I H Keys to the ingly-accepted view that the genus Elap- Nematode Parasites of vertebrate^'^) to the hostrongylus is composed of the follow- generic level. Genus Elaphostrongylus ing species; Characteristic features of the proto- Cameron, 1931 E. cervi Cameron, 1931, found in red strongylid with spiny-tailed deer & maral (Cemuselaphus), roe deer larvae are: Parasites of the skeletal musculature (Capreolus capreolus) and sika deer (C. They have indirect life cycles involv- and CNS of cervids (Cervus, Rangifer and nippon) in Great Britain, Europe and ing a ruminant mammal definitive Alces) in Europe and Asia, and intro- Asia, and introduced into New Zea- host and a molluscan intermediate duced to Newfoundland and New Zea- land. Synonym = E. panticola Liubi- host. land in imported live deer. mov, 1945. They are able to develop from first Elaphostrongylus cervi was last re- E. rangiferi Mitskevich, 1958, found in stage larvae to infective third stage viewed in Surveillance in 1989"). At that reindeer (Rangifer tarandus) in north- larvae in a wide variety of molluscan time most publications followed the view ern Europe, and introduced into New- intermediate host species. of Pryadko and Boe~'~)that Elaphostrong- f oundland . At some stage in their life cycle they ylus was a mono-specific genus of three E. alces Steen, Chabaud & Rehbinder, usually pass through the lungs of their subspecies E. cervi cervi, E. c. panticola and 1989, found in moose (Alces alces) in definitive host. First stage larvae usu- E. c. rangiferi. Publications since then, northern Europe. ally hatch from eggs in the lungs of however, suggest that this is probably There is an indication in the literature their host and these larvae pass up the not the case and that there are at least that the different species are host specific air passages, down the alimentary three valid species of Elaphostrongylus. as far as completing their life cycle is tract and leave their host with the Halvorsen et al. in Norway@)attempt- concerned, but this has yet to be demon- faeces. ed to experimentally infest reindeer calves strated conclu~ively.(~J~) The preferred site for adult worms (Rangifer tarandus tarandus) with third varies with species, but is usually the stage Elaphostrongyliis larvae grown in lungs, central nervous system (CNS), snails from first stage larvae collected Elaphostrongylus cervi or muscles. from reindeer, red deer (Cervus elaphus Elaphostrongylus cemi is widely dis- They live outside the gastrointestinal atlanticus) and moose (Alces alces). None tributed geographically and, although tract of their host, where the environ- of the five reindeer calves inoculated with capable of causing clinical disease, is not ment is not as hostile as that of gas- larvae originating from red deer and none associated with clinical disease in deer trointestinal nematodes and they may of the three reindeer calves inoculated throughout the majority of its range"). It live for several years. with larvae originating from moose be- is able to infest a limited range of deer Surveillance 22(1) 19 Surveillance Vol.22 No.1 1995

species including red deer, maral and etrated the venules of the abomasum and nematode would not complete its life North American wapiti (all C. eluphus), travelled via the liver to the lungs, where cycle in either sheep or goats. sika deer and roe deer. There is one re- the larvae entered pulmonary venules, Lankester et demonstrated that port of it infesting fallow deer (Duma passed into the arterial circulation and fallow deer could be experimentally in- duma) in Hungary(13),which is in contrast reached the CNS and other organs be- fested with a mixed inoculum of infec- to the observations made in New Zea- tween 6 and 10 days post inoculation. tive larvae (25 to 150 larvae) of P. underso- land(14)and other parts of Europe, where Some of the larvae that lodged in tissues ni and E. rungiferi, and not show clinical fallow deer are not regarded as a suitable outside the CNS probably migrated along signs of disease. At necropsy all exposed host. the spinal nerves. Eosinophilia was deer exhibited a mild, to focally intense, There are no records of E. cervi natu- present from day 8 post inoculation. eosinophilic meningitis indicating rally infesting non-cervid species either ' Ina another paper(20)the sameauthors helminthic invasion of the CNS. E. rung- in New Zealand, where there is a close cite a paper submitted for publication by iferi larvae were able to reach the CNS, association between deer and other do- Hemmingsen and others in which it was but it was not possible to determine if mestic animals on farms, in Central concluded that in reindeer E. rungiferi they were able to mature to patency. Asia(15),or in Great Britain.(I6) normally develops to maturity within There is a report of posterior ataxia in The presence of E. cervi in red deer in the CNS and then migrates to the skeletal musk oxen (Ovibos moschutus) in north- New Zealand has been responsible for muscles, where it is located in its repro- ern Scandinaviaassociated with CNS le- halting the export of live deer to Canada. ductive phase. sions attributed toimmature Elaphostrong- The Canadian fear is that if E. cetwi infest- E. rungiferi can cause neurologic dis- ylus-like nematodes(2n. ed caribou or other Canadian cervids, it ease in moose and can complete its life may be as pathogenic as E. rungiferi has cycle in moose.(21)TheScandinavian liter- been in Newfoundland. atureonEluphostrongylusinmooseiscom- Elaphostrongylus alces plicated by the recent description and separation of E. ulces. Elaphostrongylus ulces was described Elaphostrongylus rangiferi Norwegian workers reported neuro- by Steen et and redescribed by Gib- logical signs in goats and sheep caused bons et Lesions of the nervous sys- Eluphostrongylus rungiferi, in contrast by adult E. rungiferi migrating through tem have been described from moose to the two other species in the genus, has the CNS.(22,23)These animals had been killed in the field and both lesions and a record of causing disease both in its infested naturally from grazing areas nervous signs have been described from normal reindeer host, and in non-cervid used by reindeer. Subsequently, goats(20,24) experimentally infested moose.(28~29,30) species. and sheep(25)were experimentallyinfest- Stuve and Skorping(m)experimental- The clinical signs and pathological ed with infective larvae of E. rungiferi ly infested a moose calf with360 infestive findings in a reindeer calf that probably originating from reindeer. The goats were larvae. It started to shed first stage larvae died from traumatic lesions in the brain highly susceptible to infestion, the ex- 63 days after inoculation. The highest parenchyma caused by migrating ma- pected lesions were found. Mature fe- faecal count of 1,920 larvae per gram of ture E. rungiferi have been described from male worms containing ova were seen. faeces was 133 days after inoculation. Norway."" 'According to the owner the There was a gradual reduction in intact Clinically signs of intermittent lameness, calf had shown increasing signs of men- worms with increasing time from inocu- mild ataxia and general stiffness were tal confusion [for about a month before it lation indicating a gradual dying out of observed over a 3-month period from died]...... the calf was somnolent and worms in the CNS. No nematodes were day 75 after inoculation. Signs were mild, showed signs of reduced vision and a found associated with the skeletal mus- gradually faded and were not seen dur- lackof naturalshyness. When standings cles. In lambs, the effects were not as ing the last 3 weeks of observation. The lowered head posture was noticed. The severe and the worms died off more calf had a good appetite and body weight right thoracic limb frequently was held quickly. None of the lambs or goats shed increased throughout theexperiment.The off the ground and the hesitated first stage larvae of E. rungiferi in their calf was euthanased 202 days after inoc- putting it down when provoked to move. faeces and the authors concluded that the ulation. Adult nematodes were found in When moving, the animal rushed for-

ward at an increasing speed followed by ~ ~ ~ ~ ~ an abrupt stop. ... The animal occasional- ly collapsed when moving in loosesnow.' Elaphostrongylus cervi' Traumatically caused malacia and sec- ondary axon degenerationwere observed Elaphostrongylus cervi3' in all brain areas. Nematodes were found

in the skeletal muscles, epidural space of Elaphostrongylus rangifeeril' the spinal cord, and in the subdural spac- es and leptomeninges of the cord and brain. Developing nematode ova and re- Pare laphostrongy lus ten~is~~ cently hatched larvae were observed along the migratory tracks in the brain Parelaphostrongylus anders~nr~~ and in other parts of the CNS. The lungs

showed a mild interstitial pneumonia Parelaphostrongylus odocoileus5' associated with nematode ova develop- ing in the alveolar walls. Hatched larvae were seen in the alveoli. The unusual Varestrongylus sagittatus' features of this report are the presence of elaphostrongylid ova in the CNS paren- varestrongylus sagittatus" chyma and the direct association between neurological disturbances in the host and Varestrongytus atpenae" the migration of worms in the CNS pa- I renchyma. Similar information has been ~apitlaris~~ - reported from caribou in Newfound- Muellerius I land.(18) 0 100 200 300 400 500 The migration route of Eluphostrongy- lus in its host has been a matter of conjec- Body length in urn ture. Handeland and Sk~rping(~~)investi- Figure I: Mean and range of body lengths of first stage larvae in micrometres (pmun).Sources of gated this using goats infested with E. measurements show by superscript references. Measurements marked *are unpublished personal rungiferi. They found that the larvae pen- observations. 20 Surveillance 22( 1) Surveillance Vol.22 No.1 1995

the epidural space of the CNS and in worms are intimately associated with the calves examined in March/April 1984 skeletal muscles. Oedema, haemorrhag- lung tissue they are difficult to recover and 1985.(29,31) es, discolouration and extensive inflam- undamaged. It should be possible to pal- Varestrongyluscapricola is a lung para- matoryreactions were observed in the fat pate the nodules in the lungs, but this site of the asiatic ibex (Capra sibirica) in and loose connectivetissue of the epidur- could not be done in the case of the one Asia.'38) al space between the fifth cervical verte- infested red deer examined in New Zea- Varestrongylus alpenae is a parasite of bra and cauda equina. No lesions or nem- land. the small bronchioles of white-tailed deer atodes could be found in the leptomenin- Recent publications from Czechoslo- (Odocoileus virginianus) and possibly also ges or neural parenchyma of the CNS. vakia compare the first stage larvae of V. mule deer (0.kernionus) in eastern and Numerous eggs and larvae associated sagittatus and E. cervi from red deer, and central North Ameri~a.'~,~~,~')Current with moderate pathological changes were compare the pathological changes in the records indicate a disjunctive distribu- observed in the lungs. Similar nervous lungs of red deer infested with V.sagitta- tion, but this may reflect the difficulties system lesions were seen in naturally tus and E. cer~i.(~,~~) associated with identification rather than infested moose.(28,29,31) The first stage larvae of V. sagittatus the real distribution. In experimental The restriction of the nematodes to are shorter than those of E. cervi. Rez% studies all four mule deer and two of the epidural space contrasts with reports a mean length (and range) of 315 three white-tailed deer developed patent Lankester's report of experimental infes- (289-344) pm and 422 (390-459) pm re- infestations after 43-49 days and 54-5.5 tion of a moose calf with E. rangiferi lar- spectively.") Comparable measurements days respectively. Very little lung pa- vae of Newfoundland caribou origin, made from red deer in New Zealand are thology was associated with infestation when worms were found within the lep- 328 (317-350) pm and 428 (383-450) pm in either deer species apart from areas of tomeninges of the brain and spinal cord respectively. In both cases there is no petechial haemorrhage. A few areas of and within the brain ventricles.(21'Thusit overlap in the ranges and so body length focal necrosis (3-5 cm) were found on the seems that E. alces is not capable of pene- can be used diagnostically to differenti- dorsal ridge of the diaphragmatic lobes trating the dura mater of the moose, while ate the two species. Rezir also reports a of one mule deer. Worms were located E. rangiferi can. This may explain why E. difference in maximum body width be- both within and near these necrotic are- alces is only moderately pathogenic, even tween the two species and a slight differ- as. Adult worms are small and cryptic in though the affects may be sufficient to ence in the shape of the final part of the location in the lung parenchyma, and reduce the ability of moose calves to sur- tail, it being relatively straight in E. cervi lesions are few. Adult worms were re- vive the harsh Norwegian winter.'" and S-shaped in V. sagittatusP) Neither covered from only two mule deer of the Attempts to experimentally infest of these characteristicsis as easy to meas- five deer examined. Most worms were sheep and goats with E. alces from moose ure or recognise diagnostically as body found in the diaphragmatic lobes of the in Norway were unsuc~essful.~~~) length. lungs, mainly near the dorsal ridge in one The red deer lungs infested with V. deer but throughout the lung parenchy- sagittatus had a lobular catarrhal bron- ma of the second deer. The first stage Genus Varestrongylus Bhalerao, chopneumonia with dark red or yellow- larvae may be confused with other proto- 1932 ish green nodules containing adult strongylid species such as P. tenuis or P. worms, eggs (46 x 27 pm) and first stage andersoni as their morphology and di- Parasites of the lungs of sheep (Ovis), larvae. Lungs from deer infested with E. mensions are similar.(41) goats (Capra)and deer (Capreolus,Odocoi- cervi had a disseminated interstitial pneu- leus, Alces, Cervus and Dama). Their first monia, with eggs as big as 83 pm (de- stage larvae are morphologically very pending on degree of development) in Genus Parelaphostrongylus similar to the first stage larvae of Elapkos- the capillaries of the interalveolar septa, Boev and Schulz, 1950 trongylus species and Parelaphostrongylus and first stage larvae in the alveoli.(35) species. In many publications the syno- A wide range of terrestrial and even Parasites of the skeletal muscles and nyms Bicaulus or Leptostrongylus may be some aquatic gastropods are potential CNS of cervids in North America. They used. intermediate hosts of V.sagittatus in Eu- have not been reported from New Zea- Unlike the genera Elapkostrongylus and r~pe.'~,~" land. Three species are recognised; Parelapkostrongylus there have been no Parelapkostrongylus odocoilei (Hob- recent reviews of this genus. The follow- maier and Hobmaier, 1934) ing species are considered here, but the Other species of Varestrongylus Parelaphostrongylus tenuis (Dougher- list may be incomplete and may contain ty, 1945) synonyms; V. sagittatus (Mueller, 1890) Varestrongylus pneuinonicus is a para- Parelapkostrongylus andersoni Prest- Dougherty, 1945, V.pneumonicus Bhaler- site of the bronchi and bronchioles of wood, 1972 ao, 1932, V.sckulzi, V. capreoli (Stroh & wild and domestic sheep and goats in Parelaphostrongylus tenuis can cause a Schmid, 1938) Dougherty, 194.5, V.capri- Asia and parts of the Commonwealth of debilitatingneurologic diseasein its hosts. cola (Sarwar, 1944), V.alpenae (Dikmans, Independent States. First stage larvae are Parelapkostrongylus odocoilei and P. ander- 1935) Dougherty, 194.5. similar in morphology to those of Muel- soni inhabit the skeletal muscles of the lerius capillaris and 240-280 pm long.'5' back and limbs. Disturbances in posture Varestrongylus sagitfatus Varestrongylus schulzi is a parasite of and gait, and muscle lesions are seen in the lungs of sheep and goats in Asia. First experimentally infested deer; both spe- Varestrongylus sagittatus (Mueller, stage larvae 240-280 pm long.(38) cies are considered potential pathogens 1890)Dougherty, 1945 is a common lung Varestrongylus capreoli (=V.alces) is a in free-ranging animals. Verminous pneu- parasite of red deer, maral and fallow parasite of the smaller bronchi of roe monia caused by developing eggs and deer in Europe and part of Asia.(5) deer, mouflon (Ovis rnusimon), moose and larvae in the lungs is a significant feature This nematode has been found in red goats in Europe and Asia. First stage of infestation by all three species. Spiny- deer in New Zealand (Mason, PC, in larvae 285-341 pm long.(5) tailed larvae produced by all three spe- preparation).'ll' There is no evidence that The pathological changes associated cies are morphologically indistinguisha- it produces clinical disease but, because with natural infestations of V.capreoli in ble.(12) it produces first stage larvae that are roe deer in Czechoslovakia have been The distribution of elaphostrongyline morphologically very similar to E. cervi, described as inflammatory responses to nematodes in North America was re- more care has to be exercised in the diag- the presence, activity and excretory prod- viewed by Lankester and Fong."') Parela- nosis of infestation with either nema- ucts of the nematode^.'^^' In surveys of pkostrongylus odocoilei occurs most com- tode. moose parasites in Norway Stuve reports monly in mule deer and black-tailed deer The adult worms are found in small that V.alces was found in8%of themoose (0.kernionus), but has also been reported nodules in the lungs of their host and examined in 1983, when 42 animals out from caribou (Rangifer tarandus caribou) occupy a similar niche to Muellerius cap- of 1,852 were infested with both V.alces and mountain goat (Orearnnos arnerica- illaris in sheep and goats. Because the and Elapkostrongylus, and in26%of moose nus),and under experimental conditions Surveillance 22( 1) 21 Surveillance Vol.22 No.1 1995

moose (A.alces) and white-tailed deer (0. and caribou in North America. Recent of first stage larvae of C. ocreatus is cited(5) virginianus) are suitable hosts. It has a findings however, challenge this view. to range from 380-480 pm. Not known western North American distribution, Pybus efal.(45)foundP. fenuisin free rang- from New Zealand. being known from California and Wash- ing wapiti in southwestern Manitoba, ington states in the United States and Samuel et found that wapiti would British Columbia and Alberta in Canada. survive light experimental infestations Genus Pneomocaulus Schulz 81 White-tailed deer are the normal host for with P. tenuis, Bogaczyk et al.(4n report Andreeva, 1948 the meningeal worm, Parelaphostrongy- that moose numbers are increasing in an lus tenuis, which is found throughout area of Maine where P. tenuis infested Parasite of bronchi of musk deer (Mo- muchof this host'srange ineasternNorth white-tails are endemic,and Raskevitz et schus) in Not known from New America. It causes severe neurological ,al.,(-) investigating habitat utilisation by Zealand. disease in moose where their range over- sympatric wapiti and white-tailed deer, laps with white-tailed deer and in most suggest that the relationship between P. other North American cervids. Wapiti, tenuis and cervids may be more complex Genus Pneumostrongylus although susceptible to neurological dis- than had been thought. This has stimu- Monnig, 1932 ease, can survive experimentalor natural lated some interesting debate which is infestation and pass larvae, and thus not yet resol~ed.(~~,~*~') Parasites of lungs of African antelope could spread infestation. Details of the Six fallow deer (D.duma) fawns died 6 (Aepyceros, Gazella, Damaliscus, Alcelap- westward limits of distribution of P. ten- to 67 days after receiving 25 to 150 infec- hus and Connochaetus).Not known from uis are poorly known, but it has been tive larvae of P. tenuis. The fawns given New Zealand. reported in white-tailed deer in Canada the higher doses died sooner than those as far west as southwestern Manitoba given thelower doses. Earlierdeaths were and, in the USA, east of a line projected associated with severe acute peritonitis Larval differentiation south from western Minnesota through resulting from perforation of the intesti- The first stage larvae of the species in the middle of Oklahoma and including nal wall while later deaths were associat- each genus are morphologicallyindistin- the extreme eastern portion of Texas. It is ed with paralysis and inability to rise. guishable and are also morphologically absent from the coastal plain region of Numerous adult P. tenuis were found very similar to the first stage larvae of the the southeastern United States, with the within neural tissues of the brain and other genera. This can make identifica- exception of an area in the Florida Ever- spinal cord of the fawns with paralysis(52). tion of the infesting nematode very diffi- glades where white-tails were intro- Earlier records have reported clinical cult, especially since mixed infestations duced. Parelaphostrongylus andersoni, first neurologic disease and death of fallow can occur. The most convenient meas- reported in a few disjunct populations of deer infested with meningeal worm, but urement to make is body length (Figure white-tailed deer in the eastern United some fallow deer apparently survive in- l),as this will allow differentiation Elap- States and Western Canada, also occurs festation and may become resistant to hostrongylus species from Varestrongylus in caribou in northcentral and eastern reinfestati~n.(~~) species and often from Parelaphosfrongy- Canada, including Newfoundland(42). In contrast, Lankester et demon- lus species. No measurements have been This parasite could be much more wide- strated experimentally that fallow deer reported for first stage larvae of E. alces. spread than the literature currently indi- could be experimentally infested with a cates. mixed inoculum of infective larvae (25 to Parelaphostrongylus tenuis was re- 150 larvae) of P. andersoni and E. rangiferi, Concluding remarks viewed by Anderson and Prestwood.(40) not show clinical signs of disease and Under field conditions white-tailed deer pass first stage larvae of P. andersoni. Some Canadians, for example Samuel only rarely display clinical signs of dis- There are no reports of which I am aware et have written papers expressing ease, and there is no evidence to suggest of clinical disease attributable to P. tenuis concern about the risks of translocating that P. tenuis contributes significantly to in red deer imported into Canada from parasites when stock are moved in con- white-tailed deer mortality in the wild. New Zealand, even though many are nection with game farming. Their partic- Livestocksharingpasture withwhite- farmed in parts of North America where ular concern initially was to keep P. ten- tailed deer occasionally acquire infesta- white-tailed deer infested with P. tenuis uis out of the western provinces of Cana- tion by ingesting molluscs containing are endemic. da, but this has now been extended to infective larvae. Naturally occurringneu- Welch et al.(53)investigated the relia- keeping E. cervi out of Canada. We in rologic disease has been reported in sheep, bility of the Baermann technique for the New Zealand need to be equally aware of goats, moose, caribou and reindeer, red diagnosis of meningeal worm (P.tenuis) the potential for importing new parasites deer and wapiti, mule and black-tailed infestation in wapiti and concluded that when we import live animals from over- deer, fallow deer, and llamas.'40)Parelap- this technique cannot demonstrate une- seas. We have E. cervi and V.sagittatus. hostrongylus tenuis is now recognised as a quivocally that wapiti are free of menin- We do not have and do not want P. tenuis problem which must be managed when geal worm. and E. rangiferi, because these two seem llama are farmed in endemic area^.(^^,^) to be particularly pathogenic. To prevent Among more exotic animals, neurologic their importation we need to be particu- disease has been reported from a single Genus Muellerius Cameron, 1927 larly careful about the conditions im- eland and from experimentally infested Only one species, M. capillaris (Muel- posed for the importation of cervids from pronghorn antelope.") ler, 1889) Cameron, 1927, which is a cos- Eurasia and North America. It would be There are no reports of neurologic mopolitan parasite of the lungs of sheep, easy to import P. tenuis in live wapiti disease in cattle.") goats and chamois (Rupicapra).This nem- from North America. To prevent this Disturbancesof posture and gait have atode is found in sheep and goats in New happening it is important that parasites been observed in white-tailed deer dosed Zealand. are considered when protocols for live with massive numbers of P. andersoni Transmission by spotted deer (Axis animal imports are being developed. larvae. Usually clinical signs in white- axis) has been reported in India.'") Other tailed deerarerestricted toaneosinophilia reports of infestation in deer have been which is greatest 2-to4 weeks post infes- based on identification of first stage lar- References tation. White-tailed deer become patent vae which may have been incorrect. approximately 60 days after infestation. (I) Mason, PC,1989. Elaphostrongylus cervi - a Larval production is highest 2-to-6 weeks review. SurveiNance 16(1):3-10. (2) Mason, PC, (in press) 1994. Parasites of deer after patency and deer may shed larvae Genus Cystocaulus Schultz, in New Zealand. New Zealand Journal of for over a year from a single infesta- Orloff & Kutass, 1933 zoology. tion.") (3) Anderson, RC, 1992. Nematode Parasites of At one stage, P. tenuis was purported Parasites of the lungs of sheep and Vertebrates. Their Development and Trans- to limit the distribution of moose, wapiti goats in Europe, Africa and Asia. Length mission. CAB International, UK: 578 pp. 22 Surveillance 22( 1) Surveillance Vol.22 No.1 1995

Samuel, WM, 1991. A partially annotated (Elaphostrongylus rangiferi) in goats: 11. Izdatel’stvo Akademia Nauk Kazakhskoi bibliography of meningeal worm, Pathological findings. Journal of Veterinary SSR. (Translated for the National Science Parelaphostrongylus tenuis (Nematoda) and Medicine, Series B 39: 713-722. Foundation and the Department of Agricul- its close relatives. In: Synopsis of the Para- (21) Lankester, MW, 1977. Neurologic disease in ture, Washington, D.C. by the Israel Program sites of Vertebrates. Murray, JK, (editor). moose caused by Elaphostrongylus cervi [or Scientific Translations, Jerusalem, 1962). Animal Health Division, Alberta Agricul- Cameron, 193 1 from caribou. Proceedings of (39) Svarc, R, Pajerskjr, A, 1990. ture, Alberta, Canada. the 13thAnnual North American Moose Con- Pathomorphological changes in roe deer lungs Anderson, RC, 1978. No. 5. 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Elaphostrongylus cervi and its close relatives Continued from page 23

meningesofthe white-taileddeer (Odocoileus virginianus borealis) in Ontario. Canadian Journal of Zoology 41: 115-802. (56) Prestwood, AK, 1972. Parelaphosrrongylus andersoni sp.n. (Metastrongyloidea: Protostrongylidae) from the musculature of the white-taileddeer(Odocoi1eus virginianus). Journal of Parasitology 58: 897-902. (51) Pybus, MJ, Shave, H, 1984. Muellerius capillaris (Mueller, 1889)(Nematoda: Protostrongylidae): an unusual finding in rocky mountain bighorn sheep (Ovis canadensis canadensis Shaw) in South Da- kota. Journal of Wildlife Diseases 20 284- 288. (58) Gerichter, CB, 1951. Studies on the lung nematodes of sheep in the Levant. Parasirol- ogy 41: 166-183. Cited by Anderson, 1992.'

Paul Mason Invermay Animal Health Laboratory

24 Surveillance 22( 1)